183. Godwin, SC; Krkosek, M; Reynolds, JD; Bateman, AW. (2021) Bias in self-reported parasite data from the salmon farming industry.Ecol. Appl. 31 Bias in self-reported parasite data from the salmon farming industry
Caligus clemensi; environmental compliance; environmental management; environmental policy; industry data; Lepeophtheirus salmonis; Pacific salmon; policy implementation; salmon farms; salmon lice; sea lice; self‐ reported data
Many industries are required to monitor themselves in meeting regulatory policies intended to protect the environment. Self-reporting of environmental performance can place the cost of monitoring on companies rather than taxpayers, but there are obvious risks of bias, often addressed through external audits or inspections. Surprisingly, there have been relatively few empirical analyses of bias in industry self-reported data. Here, we test for bias in reporting of environmental compliance data using a unique data set from Canadian salmon farms, where companies monitor the number of parasitic sea lice on fish in open sea pens, in order to minimize impacts on wild fish in surrounding waters. We fit a hierarchical population-dynamics model to these sea-louse count data using a Bayesian approach. We found that the industry's monthly counts of two sea-louse species, Caligus clemensi and Lepeophtheirus salmonis, increased by a factor of 1.95 (95% credible interval: 1.57, 2.42) and 1.18 (1.06, 1.31), respectively, in months when counts were audited by the federal fisheries department. Consequently, industry sea-louse counts are less likely to trigger costly but mandated delousing treatments intended to avoid sea-louse epidemics in wild juvenile salmon. These results highlight the potential for combining external audits of industry self-reported data with analyses of their reporting to maintain compliance with regulations, achieve intended conservation goals, and build public confidence in the process. DOI PubMed
182. Godwin, SC; Krkosek, M; Reynolds, JD; Bateman, AW. (2021) Sea-louse abundance on salmon farms in relation to parasite-control policy and climate change.ICES J. Mar. Sci. 78: 377-387 Sea-louse abundance on salmon farms in relation to parasite-control policy and climate change
aquaculture; Caligus clemensi; climate change; environmental policy; herring; Lepeophtheirus salmonis; Pacific salmon; sea lice; temperature; wild salmon
The ectoparasitic copepods, sea lice (Lepeophtheirus salmonis and Caligus spp.), are major pests to salmon aquaculture and can also affect the health and survival of wild salmon. Policies exist to protect wild salmon by delousing farmed fish when louse abundance exceeds a threshold, but their effectiveness under future climate change is uncertain. We fitted a Bayesian model for sea-louse population dynamics and management to timeseries data of sea lice on farmed salmon in Pacific Canada and analysed the model under scenarios of warmer climates. We found that in high-temperature years, current parasite control policy becomes ineffective as sea-louse abundance is expected to increase. We simulated two alternative management scenarios and observed that both would decrease average louse counts on farms in high-temperature years relative to the current system but relied on more delousing treatments than are currently performed. We also found evidence that non-salmonids can play a role in louse transmission to farms, as increased farm colonization of Caligus clemensi occurs in April, coincident with wild herring (Clupea pallasii) spawner abundance. Our results highlight the need for careful management of sea lice on salmon farms in warmer years and the importance of policies designed to account for future environmental change. DOI
181. Kieran, CN; Obrist, DS; Munoz, NJ; Hanly, PJ; Reynolds, JD. (2021) Links between fluctuations in sockeye salmon abundance and riparian forest productivity identified by remote sensing.Ecosphere 12 Links between fluctuations in sockeye salmon abundance and riparian forest productivity identified by remote sensing
ecosystem; fertilization effect; marine-derived nutrients; migratory species; NDVI; nitrogen; Oncorhynchus; Pacific Northwest; productivity; remote sensing; riparian vegetation; spatial subsidy
Pacific salmon (Oncorhynchus spp.) carcasses can fertilize riparian forests with marine-derived nutrients when populations make their annual return to natal streams to spawn; however, the strength of this cross-system linkage likely varies substantially among years due to the interannual fluctuations in abundance that characterize most salmon populations. Here, we used a 36-yr time series (1984-2019) of satellite imagery and salmon abundance estimates to assess spatiotemporal associations between forest greenness (a measure of plant productivity) and adult sockeye salmon (Oncorhynchus nerka) abundance in the lower Adams River, British Columbia, Canada. The Adams River sockeye population displays a quadrennial pattern of abundance, with a dominant cohort that spawns every four years in numbers that are typically two to three orders of magnitude larger than non-dominant cohorts. We found that variation in forest greenness was consistently explained best by models including dominant cohort year, whereas models lacking an index of salmon abundance were the lowest-ranked. Greenness of riparian vegetation increased by an average of 0.015 NDVI units (approximately 1%) in the summer after a dominant cohort return, and this effect on greenness persisted into the subsequent fall (11-13 months after spawning). The positive association between quadrennial pulses of salmon and riparian greenness occurred in plots both within 30 m of the stream and 95-125 m away from the stream, indicating that the spatial extent of fertilization may occur well beyond areas directly adjacent to the riverbank. These results suggest that forests respond to cyclical variation in salmon abundance and that overwinter storage of marine-derived nutrients within catchments allows plants to capitalize on these nutrients in the following growing season. Continued advances in remote sensing technology will enhance our understanding of cross-system resource linkages and can inform the ecosystem-based management of Pacific salmon. DOI
180. Munoz, NJ; Reid, B; Correa, C; Neff, BD; Reynolds, JD. (2021) Non-native Chinook salmon add nutrient subsidies and functional novelty to Patagonian streams.Freshw. Biol. 66: 495-508 Non-native Chinook salmon add nutrient subsidies and functional novelty to Patagonian streams
eutrophication; invasive species; Oncorhynchus; periphyton; stable isotopes
The impacts of non-native species are hypothesised to be proportional to the functional distinctiveness of invaders in their invaded ecosystems. Throughout the Patagonia region of southern South America, Chinook salmon (Oncorhynchus tshawytscha) have recently established non-native populations, and their anadromous, semelparous life cycle could be functionally unique such that marine-derived nutrients are delivered to streams which have historically lacked such a resource linkage with the ocean. We tested the hypothesis that salmon subsidise biofilm-associated algae in streams throughout the Aysen province of southern Chile. Using spatial and temporal variation in the presence of salmon among multiple streams and across two spawning seasons, we found strong evidence of salmon-subsidised algae in three out of four streams examined that have spawning salmon populations. The biofilm of subsidised streams had enriched stable isotopic ratios of nitrogen and carbon, indicating that marine-derived nutrients were incorporated by biofilms. This nutrient uptake translated into increased algal biomass and percent of total biofilm biomass composed of algae, indicating that the incorporation of marine-derived nutrients stimulated autotrophic production of biomass. In one stream, the incorporation of marine-derived nutrients by biofilm occurred in only one of the two studied spawning seasons. Incorporation occurred in a year with low flows of water throughout salmon spawning (4.59 m(3)/s) and did not occur in a year with much higher flows (41.6 m(3)/s), suggesting that inter-annual variation in discharge can mediate the subsidising effect of salmon. These results indicate that Chinook salmon have bridged the historical gap between productive marine ecosystems and nutrient-poor stream ecosystems in Patagonia. Anadromous salmon can be a significant source of nutrients in nutrient-limited catchments, and their ongoing expansion in southern South America is likely to entail ecological impacts in stream and riparian food webs. DOI
179. Price, MHH; Moore, JW; Connors, BM; Wilson, KL; Reynolds, JD. (2021) Portfolio simplification arising from a century of change in salmon population diversity and artificial production.J. Appl. Ecol. 58: 1477-1486 Portfolio simplification arising from a century of change in salmon population diversity and artificial production
artificial production; biodiversity loss; conservation genetics; fisheries; historical ecology; population diversity; portfolio effects; salmon abundance
Population and life-history diversity can buffer species from environmental variability and contribute to long-term stability through differing responses to varying conditions akin to the stabilizing effect of asset diversity on financial portfolios. While it is well known that many salmon populations have declined in abundance over the last century, we understand less about how different dimensions of diversity may have shifted. Specifically, how has diminished wild abundance and increased artificial production (i.e. enhancement) changed portfolios of salmon populations, and how might such change influence fisheries and ecosystems? We apply modern genetic tools to century-old sockeye salmon Oncorhynchus nerka scales from Canada's Skeena River watershed to (a) reconstruct historical abundance and age-trait data for 1913-1947 to compare with recent information, (b) quantify changes in population and life-history diversity and the role of enhancement in population dynamics, and (c) quantify the risk to fisheries and local ecosystems resulting from observed changes in diversity and enhancement. The total number of wild sockeye returning to the Skeena River during the modern era is 69% lower than during the historical era; all wild populations have declined, several by more than 90%. However, enhancement of a single population has offset declines in wild populations such that aggregate abundances now are similar to historical levels. Population diversity has declined by 70%, and life-history diversity has shifted: populations are migrating from freshwater at an earlier age, and spending more time in the ocean. There also has been a contraction in abundance throughout the watershed, which likely has decreased the spatial extent of salmon provisions to Indigenous fisheries and local ecosystems. Despite the erosion of portfolio strength that this salmon complex hosted a century ago, total returns now are no more variable than they were historically perhaps in part due to the stabilizing effect of artificial production. Policy implications. Our study provides a rare example of the extent of erosion of within-species biodiversity over the last century of human influence. Rebuilding a diversity of abundant wild populations-that is, maintaining functioning portfolios-may help ensure that watershed complexes like the Skeena are robust to global change. DOI
178. Rammell, NF; Dennert, AM; Ernst, CM; Reynolds, JD. (2021) Effects of spawning Pacific salmon on terrestrial invertebrates: Insects near spawning habitat are isotopically enriched with nitrogen-15 but display no differences in body size.Ecol. Evol. 11: 12728-12738 Effects of spawning Pacific salmon on terrestrial invertebrates: Insects near spawning habitat are isotopically enriched with nitrogen-15 but display no differences in body size
body condition; body size; Carabidae; Curculionidae; insects; isotope; marine-derived nutrients; nitrogen; Pacific salmon
When Pacific salmon (Oncorhynchus spp.) spawn and die, they deliver marine-derived nutrient subsidies to freshwater and riparian ecosystems. These subsidies can alter the behavior, productivity, and abundance of recipient species and their habitats. Isotopes, such as nitrogen-15 (N-15), are often used to trace the destination of marine-derived nutrients in riparian habitats. However, few studies have tested for correlations between stable isotopes and physiological responses of riparian organisms. We examined whether increases in delta N-15 in terrestrial insect bodies adjacent to salmon spawning habitat translate to changes in percent nitrogen content and body size. This involved comparisons between distance from a salmon-bearing river, marine-derived nutrients in soils and insects, soil moisture content, and body size and nitrogen content in two common beetle families (Coleoptera: Curculionidae, Carabidae). As predicted, delta N-15 in riparian soils attenuated with distance from the river but was unaffected by soil moisture. This gradient was mirrored by delta N-15 in the herbivorous curculionid beetles, whereas carabid beetles, which feed at a higher trophic level and are more mobile, did not show discernable patterns in their delta N-15 content. Additionally, neither distance from the river nor body delta N-15 content was related to beetle body size. We also found that nitrogen-15 was not correlated with total percent nitrogen in insect bodies, meaning that the presence of spawning salmon did not increase the percent nitrogen content of these insects. We conclude that while salmon-derived nutrients had entered terrestrial food webs, the presence of delta N-15 alone did not indicate meaningful physiological changes in these insects in terms of percent nitrogen nor body size. While stable isotopes may be useful tracers of marine-derived nutrients, they cannot necessarily be used as a proxy for physiologically important response variables. DOI PubMed
177. Walters, KE; Reynolds, JD; Ydenberg, RC. (2021) Ideal free eagles: Bald Eagle (Haliaeetus leucocephalus) distribution in relation to Pacific salmon (Oncorhynchus spp.) availability on four spawning rivers.Can. J. Zool. 99: 792-800 Ideal free eagles: Bald Eagle (Haliaeetus leucocephalus) distribution in relation to Pacific salmon (Oncorhynchus spp.) availability on four spawning rivers
Bald Eagles; Haliaeetus leucocephalus; Pacific salmonids; Oncorhynchus spp.; Ideal Free Distribution; resource patches; behavioural ecology; spatial distribution; scavengers; temporal distribution
The movement of individuals according to the availability of resources has a fundamental effect on animal distributions. In the Pacific Northwest, Bald Eagles (Haliaeetus leucocephalus (Linnaeus, 1766)) rely heavily on scavenging opportunities during the non-breeding period, and their distribution and movements are thought to be strongly influenced by the availability of post-spawning Pacific salmon (genus Oncorhynchus Suckley, 1861) carcasses. We surveyed the abundance of eagles and salmon on four adjacent rivers on Vancouver Island, British Columbia, Canada, during the 2017 fall spawning season. Salmon began to arrive in late September, peaked in abundance in mid-November, and were absent after early December. The seasonal progression of Bald Eagle abundance matched that of salmon carcass availability. The slope of proportional eagle-salmon relationship was significantly positive, though lower than the 1:1 match predicted by Ideal Free Distribution theory. The numerical response of Bald Eagles to salmon abundance was elevated on one of the rivers, potentially due to physical features such as sandbars and mudflats that increased the availability of carcasses and provided access points for eagles. DOI
176. Wilcox, KA; Wagner, MA; Reynolds, JD. (2021) Salmon subsidies predict territory size and habitat selection of an avian insectivore.PLoS One 16 Salmon subsidies predict territory size and habitat selection of an avian insectivore
The annual migration and spawning event of Pacific salmon (Oncorhynchus spp.) can lead to cross-boundary delivery of marine-derived nutrients from their carcasses into adjacent terrestrial ecosystems. The densities of some passerine species, including Pacific wrens (Troglodytes pacificus), have been shown to be positively correlated with salmon abundance along streams in Alaska and British Columbia, but mechanisms maintaining these densities remain poorly understood. Riparian areas near salmon streams could provide higher quality habitat for birds through greater food availability and more suitable vegetation structure for foraging and breeding, resulting in wrens maintaining smaller territories. We examined relationships between salmon biomass and Pacific wren territory size, competition, and habitat selection along 11 streams on the coast of British Columbia, Canada. We show that male wren densities increase and territory sizes decrease as salmon-spawning biomass increases. Higher densities result in higher rates of competition as male wrens countersing more frequently to defend their territories along streams with more salmon. Wrens were also more selective of the habitats they defended along streams with higher salmon biomass; they were 68% less likely to select low-quality habitat on streams with salmon compared with 46% less likely at streams without salmon. This suggests a potential trade-off between available high-quality habitat and the cost of competition that structures habitat selection. Thus, the marine-nutrient subsidies provided by salmon carcasses to forests lead to higher densities of wrens while shifting the economics of territorial defence toward smaller territories being defended more vigorously in higher quality habitats. DOI PubMed
175. Brown, CJ; Parker, B; Hocking, MD; Reynolds, JD. (2020) Salmon abundance and patterns of forest greenness as measured by satellite imagery.Sci. Total Environ. 725 Salmon abundance and patterns of forest greenness as measured by satellite imagery
Nutrient flows; Ecosystem-based management; NDVI; Diadromous fish
Linkages across ecosystems can shape productivity. Salmon carcasses are exemplary of cross-system linkages, because they can fertilize riparian vegetation and shape patterns of terrestrial biodiversity. Detection of salmon fertilization effects has been confined to field-based studies that are limited in scale. Here we use satellite images to quantify the effects of salmon on greenness of riparian vegetation. We measure tree greenness across spatial and temporal gradients of salmon fertilization effects in two regions. In the first case study, we find that deciduous trees are greener in years following large salmon spawning events, and that the magnitude of this effect was related to the specific abundance of spawning salmon. In the second case study we compare greenness of mixed evergreen and deciduous forests across different watersheds that have different salmon spawning densities. We found greenness was related positively to salmon spawning density near streams with high evergreen cover and flat stream banks. These findings suggest that the effect of salmon carcasses on riparian vegetation may be detectable from space. Further work on this approach, especially with high spatial, temporal and spectral data, may allow estimation of the spatial extent of nutrient enrichment from salmon carcasses and aid ecosystem-based management to protect important ecosystem linkages. (C) 2020 Elsevier B.V. All rights reserved. DOI PubMed
174. Castaneda, RA; Burliuk, CMM; Casselman, JM; Cooke, SJ; Dunmall, KM; Forbes, LS; Hasler, CT; Howland, KL; Hutchings, JA; Klein, GM; Nguyen, VM; Price, MHH; Reid, AJ; Reist, JD; Reynolds, JD; Van Nynatten, A; Mandrak, NE. (2020) A Brief History of Fisheries in Canada.Fisheries 45: 303-318 A Brief History of Fisheries in Canada
173. Obrist, DS; Hanly, PJ; Kennedy, JC; Fitzpatrick, OT; Wickham, SB; Ernst, CM; Nijland, W; Reshitnyk, LY; Darimont, CT; Starzomski, BM; Reynolds, JD. (2020) Marine subsidies mediate patterns in avian island biogeography.Proc. R. Soc. B-Biol. Sci. 287 Marine subsidies mediate patterns in avian island biogeography
island biogeography; spatial subsidies; marine-derived nutrients; avian ecology
The classical theory of island biogeography, which predicts species richness using island area and isolation, has been expanded to include contributions from marine subsidies, i.e. subsidized island biogeography (SIB) theory. We tested the effects of marine subsidies on species diversity and population density on productive temperate islands, evaluating SIB predictions previously untested at comparable scales and subsidy levels. We found that the diversity of terrestrial breeding bird communities on 91 small islands (approx. 0.0001-3 km(2)) along the Central Coast of British Columbia, Canada were correlated most strongly with island area, but also with marine subsidies. Species richness increased and population density decreased with island area, but isolation had no measurable influence. Species richness was negatively correlated with marine subsidy, measured as forest-edge soil delta N-15. Density, however, was higher on islands with higher marine subsidy, and a negative interaction between area and subsidy indicates that this effect is stronger on smaller islands, offering some support for SIB. Our study emphasizes how subsidies from the sea can shape diversity patterns on islands and can even exceed the importance of isolation in determining species richness and densities of terrestrial biota. DOI
171. Siemens, LD; Dennert, AM; Obrist, DS; Reynolds, JD. (2020) Spawning salmon density influences fruit production of salmonberry (Rubus spectabilis).Ecosphere 11 Spawning salmon density influences fruit production of salmonberry (Rubus spectabilis)
British Columbia; chum salmon; fruit production; marine‐ derived nutrients; Pacific salmon; pink salmon; plant traits; riparian vegetation; Rubus spectabilis; salmonberry; spawning salmon density; subsidy
Annual spawning migrations by Pacific salmon can provide substantial subsidies to nutrient-limited freshwater and riparian ecosystems, which can affect the abundance, diversity, and physical characteristics of plant and animal species in these habitats. Here, we provide the first investigation of how salmon subsidies affect reproductive output in plants, focusing on a common riparian shrub, salmonberry (Rubus spectabilis). We studied 14 streams with a range of spawning salmon densities on the central coast of British Columbia, Canada. We determined the effects of chum (Oncorhynchus keta), pink (O. gorbuscha), and total salmon spawning density on the number of fruits per shrub, number of seeds per fruit, fruit weight, and estimated sugar content (degrees Brix) of salmonberry fruits. We found that the number of fruits per salmonberry shrub increased with increasing salmon density. However, we found no effect of salmon density on the number of seeds per fruit, fruit weight, or sugar content. The effect of salmon density was species-dependent; the number of fruits per shrub increased with chum salmon density but was not affected by pink salmon density. This could be because chum salmon occur at higher densities and are transferred from water to land at higher rates than pink salmon in our study area. Higher salmonberry fruit production could lead to a larger input of salmonberry fruits to coastal food webs. These results demonstrate how salmon can cross ecological boundaries and influence reproductive output of terrestrial species. DOI
170. Walsh, JC; Connors, K; Hertz, E; Kehoe, L; Martin, TG; Connors, B; Bradford, MJ; Freshwater, C; Frid, A; Halverson, J; Moore, JW; Price, MHH; Reynolds, JD. (2020) Prioritizing conservation actions for Pacific salmon in Canada.J. Appl. Ecol.Prioritizing conservation actions for Pacific salmon in Canada
conservation planning; decision-support tool; Indigenous knowledge; Pacific salmon; Priority Threat Management; recovery planning; stream restoration; Wild Salmon Policy
Current investment in conservation is insufficient to adequately protect and recover all ecosystems and species. The challenge of allocating limited funds is acute for Pacific salmon Oncorhynchus spp. in Canada, which lack a strategic approach to ensure that resources are spent on actions most likely to cost-effectively recover diminished populations. We applied the Priority Threat Management framework to prioritize strategies most likely to maximize the number of thriving Pacific salmon populations on the Central Coast of British Columbia, Canada. These included 79 genetically, ecologically and spatially distinct population groups called conservation units (CUs) for five salmon species. This region has high salmon biodiversity and spans the territories of four First Nations: the Heiltsuk, Nuxalk, Kitasoo/Xai'xais and Wuikinuxv. Using structured expert elicitation of Indigenous and other experts, we quantified the estimated benefits, costs and feasibility of implementing 10 strategies. Under a business-as-usual scenario (i.e. no additional investments in salmon conservation or management), experts predicted that only one in four CUs would have >50% chance of achieving a thriving status within 20 years. Limiting future industrial development in salmon habitats, which was predicted to safeguard CUs from future declines, was identified as the most cost-effective strategy. Investment in three strategies: (a) removal of artificial barriers to fish migration, (b) watershed protection and (c) stream restoration-at 11.3M CAD per year-was predicted to result in nearly half (34 of 79) of the CUs having a >60% chance of meeting the conservation objective. If all conservation strategies were implemented, experts estimated a >50% probability of achieving a thriving status for 78 of 79 CUs, at an annual cost of 17.3M CAD. However, even with the implementation of all strategies, most sockeye salmon CUs were unlikely to achieve higher probability targets of reaching the objective. Policy implications. We illustrate how Priority Threat Management can incorporate the perspectives and expertise of Indigenous peoples and other experts to prioritize conservation strategies based on their cost, benefit and feasibility. Implementation of this framework can help safeguard and recover Pacific salmon in Canada, and could also be used to prioritize actions for other conservation issues globally. DOI
169. Walsh, JC; Pendray, JE; Godwin, SC; Artelle, KA; Kindsvater, HK; Field, RD; Harding, JN; Swain, NR; Reynolds, JD. (2020) Relationships between Pacific salmon and aquatic and terrestrial ecosystems: implications for ecosystem-based management.EcologyRelationships between Pacific salmon and aquatic and terrestrial ecosystems: implications for ecosystem-based management
anadromous; ecological benchmark; ecological indicator; ecological threshold; ecosystem engineering; ecosystem-based management; fisheries; marine-derived nutrient; nutrient cycling; nutrient subsidy; Pacific salmon; salmonid
Pacific salmon influence temperate terrestrial and freshwater ecosystems through the dispersal of marine-derived nutrients and ecosystem engineering of stream beds when spawning. They also support large fisheries, particularly along the west coast of North America. We provide a comprehensive synthesis of relationships between the densities of Pacific salmon and terrestrial and aquatic ecosystems, summarize the direction, shape, and magnitude of these relationships, and identify possible ecosystem-based management indicators and benchmarks. We found 31 studies that provided 172 relationships between salmon density (or salmon abundance) and species abundance, species diversity, food provisioning, individual growth, concentration of marine-derived isotopes, nutrient enhancement, phenology, and several other ecological responses. The most common published relationship was between salmon density and marine-derived isotopes (40%), whereas very few relationships quantified ecosystem-level responses (5%). Only 13% of all relationships tended to reach an asymptote (i.e., a saturating response) as salmon densities increased. The number of salmon killed by bears and the change in biomass of different stream invertebrate taxa between spawning and nonspawning seasons were relationships that usually reached saturation. Approximately 46% of all relationships were best described with linear or curved nonasymptotic models, indicating a lack of saturation. In contrast, 41% of data sets showed no relationship with salmon density or abundance, including many of the relationships with stream invertebrate and biofilm biomass density, marine-derived isotope concentrations, or vegetation density. Bears required the highest densities of salmon to reach their maximum observed food consumption (i.e., 9.2 kg/m(2)to reach the 90% threshold of the relationship's asymptote), followed by freshwater fish abundance (90% threshold = 7.3 kg/m(2)of salmon). Although the effects of salmon density on ecosystems are highly varied, it appears that several of these relationships, such as bear food consumption, could be used to develop indicators and benchmarks for ecosystem-based fisheries management. DOI PubMed
168. Wickham, SB; Shackelford, N; Darimont, CT; Nijland, W; Reshitnyk, LY; Reynolds, JD; Starzomski, BM. (2020) Sea wrack delivery and accumulation on islands: factors that mediate marine nutrient permeability.Mar. Ecol.-Prog. Ser. 635: 37-54 Sea wrack delivery and accumulation on islands: factors that mediate marine nutrient permeability
Sea wrack; Marine-terrestrial subsidy; Spatial subsidy; Ecosystem connectivity; Wrack deposition; Wrack accumulation; Macrophyte; British Columbia; Remote sensing
Sea wrack provides an important vector of marine-derived nutrients to many terrestrial environments. However, little is known about the processes that facilitate wrack transport, deposition, and accumulation on islands. Three broad factors can affect the stock of wrack along shorelines: the amount of potential donor habitat nearby, climatic events that dislodge seaweeds and transfer them ashore, and physical characteristics of shorelines that retain wrack at a site. To determine when, where, and how wrack accumulates on island shorelines, we surveyed 455 sites across 101 islands in coastal British Columbia, Canada. At each site, we recorded wrack biomass, species composition, and shoreline biogeographical characteristics. Additionally, over a period of 9 mo, we visited a smaller selection of sites (n = 3) every 2 mo to document temporal changes in wrack biomass and species composition. Dominant wrack species were Zostera marina, Fucus distichus, Macrocystis pyrifera, Nereocystis luetkeana, Pterygophora californica, and Phyllospadix spp. The amount of donor habitat positively affected the presence of accumulated biomass of sea wrack, whereas rocky substrates and shoreline slope negatively affected the presence of sea wrack biomass. Biomass was higher during winter months, and species diversity was higher during summer months. These results suggest that shorelines with specific characteristics have the capacity to accumulate wrack, thereby facilitating the transfer of marine-derived nutrients to the terrestrial environment. DOI
167. Harding, JMS; Harding, JN; Field, RD; Pendray, JE; Swain, NR; Wagner, MA; Reynolds, JD. (2019) Landscape Structure and Species Interactions Drive the Distribution of Salmon Carcasses in Coastal Watersheds.Front. Ecol. Evol. 7 Landscape Structure and Species Interactions Drive the Distribution of Salmon Carcasses in Coastal Watersheds
cross-ecosystem; fisheries; landscape ecology; nutrient subsidies; pacific salmon
The disproportionate effects of some species can drive ecosystem processes and shape communities. This study investigates how distributions of spawning Pacific salmon within streams, salmon consumers, and the surrounding landscape mediate the distribution of salmon carcasses to riparian forests and estuaries. This work demonstrates how carcass transfer can vary spatially, within and among watersheds, through differences in pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon distributions within 16 streams on the central coast of British Columbia over a five-year period. Spawning pink salmon concentrated in the lower reaches of all streams, whereas chum salmon shifted from lower to upper stream reaches as the area of spawning habitat increased. Salmon carcasses transferred to riparian areas by gray wolves (Canis lupus) were concentrated in estuaries and lower stream reaches, particularly shallow reaches of larger streams surrounded by large meadow expanses. Black and grizzly bears (Ursus americanus and U. arctos) transferred higher numbers and proportions of salmon carcasses to riparian areas compared to wolves, transferred more carcasses in areas of higher spawning density, and tended to focus more on chum salmon. Riparian subsides were increasingly driven by bear-chum salmon associations in upper stream reaches. In addition, lower proportions of salmon carcasses were exported into estuaries when densities of spawning salmon were lower and spawning reaches of streams were longer. This study demonstrates how salmon subsidies vary between and within watersheds as a result of species associations and landscape traits, and provides a nuanced species-specific and spatially explicit understanding of salmon-subsidy dynamics. DOI
164. Price, MHH; Connors, BM; Candy, JR; McIntosh, B; Beacham, TD; Moore, JW; Reynolds, JD. (2019) Genetics of century-old fish scales reveal population patterns of decline.Conserv. Lett.Genetics of century-old fish scales reveal population patterns of decline
conservation genetics; ecosystems; fisheries; historical ecology; population depletion; recovery; salmon; extinction risk; Skeena River
Conservation scientists rarely have the information required to understand changes in abundance over more than a few decades, even for important species like Pacific salmon. Such lack of historical information can underestimate the magnitude of decline for depressed populations. We applied genetic tools to a unique collection of 100-year-old salmon scales to reveal declines of 56%-99% in wild sockeye populations across Canada's second largest salmon watershed, the Skeena River. These analyses reveal century-long declines that are much greater than those based on modern era abundance data, which suggested that only 7 of 13 populations declined over the last five decades. Populations of larger-bodied fish have declined the most in abundance, likely because of size-selective commercial fisheries. Our findings illustrate how a deep historical perspective can expand our understanding of past abundances to a time before species incurred significant losses from fishing, and help inform conservation for diminished populations. DOI
163. Wagner, MA; Reynolds, JD. (2019) Salmon increase forest bird abundance and diversity.PLoS One 14 Salmon increase forest bird abundance and diversity
Resource subsidies across ecosystems can have strong and unforeseen ecological impacts. Marine-derived nutrients from Pacific salmon (Onchorhycus spp.) can be transferred to streams and riparian forests through diverse food web pathways, fertilizing forests and increasing invertebrate abundance, which may in turn affect breeding birds. We quantified the influence of salmon on the abundance and composition of songbird communities across a wide range of salmon-spawning biomass on 14 streams along a remote coastal region of British Columbia, Canada. Point-count data spanning two years were combined with salmon biomass and 13 environmental covariates in riparian forests to test for correlates with bird abundance, foraging guilds, individual species, and avian diversity. We show that bird abundance and diversity increase with salmon biomass and that watershed size and forest composition are less important predictors. This work provides new evidence for the importance of salmon to terrestrial ecosystems and information that can inform ecosystem-based management. DOI PubMed
162. Wickham, SB; Darimont, CT; Reynolds, JD; Starzomski, BM. (2019) Species-specific wet-dry mass calibrations for dominant Northeastern Pacific Ocean macroalgae and seagrass.Aquat. Bot. 152 Species-specific wet-dry mass calibrations for dominant Northeastern Pacific Ocean macroalgae and seagrass
Biomass; Mass calibration; Wet weight; Dry weight; Ratio; Macroalgae; Macrophyte; Sea wrack; Seagrass; Kelp; Northeast pacific ocean
Macroalgae and seagrasses form the base of productive ecosystems in the Northeastern Pacific Ocean. Often, ecological research on macroalgae, seagrasses, and sea wrack requires the conversion of biomass from wet to dry to create consistency across investigations. This process, however, can be destructive, impractical, time consuming, and labour intensive. We collected samples of twelve common Northeastern Pacific Ocean seaweed species (Alaria marginata, Codium fragile, Egregia menziesii, Fucus distichus, Macrocystis pyrifera, Mazzaella spp., Nereocystis luetkeana, Pterygophora californica, Pyropia spp., Ulva spp., and the seagrasses Zostera marina and Phyllospadix spp.) in two states: wet and fresh, or aged and partially desiccated. We weighed, dried, and compared samples, finding that many species displayed a strong (R-2 > 0.8) and predictable linear relationship between wet and dried conditions. In contrast, half the aged samples did not have a significant relationship between partially desiccated and dried conditions. Our results provide practical wet weight to dry weight ratios for many species, and with further research, a reliable set of species-specific wet to dry weight ratios for all species could be established. Wet to dry weight ratios are useful for macroalgae, seagrass, and sea wrack research or commercial applications and would reduce the need to conduct extensive wet-dry calibrations in each study. DOI
161. Andersson, LC; Reynolds, JD. (2018) Habitat features mediate selective consumption of salmon by bears.Can. J. Fish. Aquat. Sci. 75 Habitat features mediate selective consumption of salmon by bears
Salmon provide a key source of marine-derived nutrients to aquatic and surrounding terrestrial habitats in coastal areas of the North Pacific. Bears are a major predator of salmon and provide an important pathway for carcass transfer to riparian zones. We studied selective consumption of salmon (Oncorhynchus keta and Oncorhynchus gorbuscha) by bears (Ursus arctos and Ursus americanus) on 12 streams on the central coast of British Columbia, Canada. We predicted that bears would select more energy-rich parts, and eat less of each fish (i.e., selective consumption), in streams with more prey and simpler habitat (i.e., streams that facilitate salmon capture). Bears were 12% more likely to consume fish selectively in narrow, shallow streams with less pool volume, where salmon are easier to catch, than in deep, wide streams. However, bears were also 21% more likely to selectively consume fish in streams with more wood obstacles and undercut banks, where hunting was predicted to be more difficult. This suggests that stream characteristics can have significant indirect effects on riparian nutrient subsidies to ecosystems through selective feeding by bears. DOI
160. Artelle, KA; Reynolds, JD; Treves, A; Walsh, JC; Paquet, PC; Darimont, CT. (2018) Working constructively toward an improved North American approach to wildlife management.Sci. Adv. 4 Working constructively toward an improved North American approach to wildlife management
Mawdsley et al. (2018) respond disapprovingly to our 2018 review of 667 wildlife management systems across Canada and the United States, which found that many of these systems lacked the scientific hallmarks of clear objectives, evidence, transparency, and independent review. Although we strongly agree with several of Mawdsley et al.'s points about the role of science in management, their response suggests confusion about three elements of our approach that we clarify herein: (i) the selection of hallmarks, (ii) the role of science in wildlife management, and (iii) our engagement with wildlife agencies. We contend that both critics and defenders of the current approach to wildlife management in Canada and the United States similarly desire rigorous management that achieves social and ecological benefits. Our original study-which used a clear approach to define hallmarks of science-based management, employed a reasonable set of indicator criteria to test for them, and was based on data available to the general public on whose behalf management is conducted-found evidence that the current approach falls short. However, it also provided a framework for addressing shortcomings moving forward. We suggest that advancing discussion on the operational role of science in management, including clarifying what "science-based management" actually means, could curtail practitioners and critics of the status quo talking over each other's heads and encourage all parties to work constructively to improve the governance of wildlife at a continental scale. DOI PubMed
159. Artelle, KA; Reynolds, JD; Treves, A; Walsh, JC; Paquet, PC; Darimont, CT. (2018) Hallmarks of science missing from North American wildlife management.Sci. Adv. 4 Hallmarks of science missing from North American wildlife management
Resource management agencies commonly defend controversial policy by claiming adherence to science-based approaches. For example, proponents and practitioners of the "North American Model of Wildlife Conservation, "which guides hunting policy across much of the United States and Canada, assert that science plays a central role in shaping policy. However, what that means is rarely defined. We propose a framework that identifies four fundamental hallmarks of science relevant to natural resource management (measurable objectives, evidence, transparency, and independent review) and test for their presence in hunt management plans created by 62 U.S. state and Canadian provincial and territorial agencies across 667 management systems (species-jurisdictions). We found that most (60%) systems contained fewer than half of the indicator criteria assessed, with more criteria detected in systems that were peer-reviewed, that pertained to "big game," and in jurisdictions at increasing latitudes. These results raise doubt about the purported scientific basis of hunt management across the United States and Canada. Our framework provides guidance for adopting a science-based approach to safeguard not only wildlife but also agencies from potential social, legal, and political conflict. DOI PubMed
158. Atkinson, EM; Bateman, AW; Dill, LM; Krkosek, M; Reynolds, JD; Godwin, SC. (2018) Oust the louse: leaping behaviour removes sea lice from wild juvenile sockeye salmon Oncorhynchus nerka.J. Fish Biol. 93 Oust the louse: leaping behaviour removes sea lice from wild juvenile sockeye salmon Oncorhynchus nerka
aquaculture; host-parasite; leaping; louse; sub-lethal effects; trade-offs
We conducted a manipulative field experiment to determine whether the leaping behaviour of wild juvenile sockeye salmon Oncorhynchus nerka dislodges ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis by comparing sea-lice abundances between O. nerka juveniles prevented from leaping and juveniles allowed to leap at a natural frequency. Juvenile O. nerka allowed to leap had consistently fewer sea lice after the experiment than fish that were prevented from leaping. Combined with past research, these results imply potential costs due to parasitism and indicate that the leaping behaviour of juvenile O. nerka does, in fact, dislodge sea lice. DOI PubMed
157. Bailey, CJ; Braun, DC; McCubbing, D; Reynolds, JD; Ward, B; Davies, TD; Moore, JW. (2018) The roles of extrinsic and intrinsic factors in the freshwater life-history dynamics of a migratory salmonid.Ecosphere 9 The roles of extrinsic and intrinsic factors in the freshwater life-history dynamics of a migratory salmonid
anadromy; artificial nutrient addition; fisheries; life-history diversity; long-term study; marine-derived nutrients; steelhead
Key life-cycle transitions, such as metamorphosis or migration, can be altered by a variety of external factors, such as climate variation, strong species interactions, and management intervention, or modulated by density dependence. Given that these life-history transitions can influence population dynamics, understanding the simultaneous effects of intrinsic and extrinsic controls on life-history expression is particularly relevant for species of management or conservation importance. Here, we examined how life histories of steelhead (Oncorhynchus mykiss) are affected by weather, pink salmon abundance (Oncorhynchus gorbuscha), experimental nutrient addition, and density-dependent processes. We tested for impacts on the size of steelhead smolts (juveniles migrating to the sea), as well as their age and abundance across four decades in the Keogh River, British Columbia, Canada. Larger steelhead smolts were associated with warmer years and artificial nutrient addition. In addition, higher pink salmon abundance and artificial nutrient addition correlated with juvenile steelhead migrating at younger ages. While density dependence appeared to be the primary factor regulating the abundance of steelhead smolts, nutrient addition and temperature were positively and negatively associated with smolt production, respectively, prior to 1991, and pink salmon spawning abundance was positively associated with smolt production after 1990. Thus, this study provides evidence that the temporal dynamics of one species of salmon is linked to the juvenile life history of co-occurring steelhead. A complex interplay of species interactions, nutrient subsidies, density dependence, and climatic variation can control the life-history expression of species with complex life cycles. DOI
156. Godwin, SC; Krkosek, M; Reynolds, JD; Rogers, LA; Dill, LM. (2018) Heavy sea louse infection is associated with decreased stomach fullness in wild juvenile sockeye salmon.Can. J. Fish. Aquat. Sci. 75 Heavy sea louse infection is associated with decreased stomach fullness in wild juvenile sockeye salmon
Foraging success can be mediated by parasites, but this is poorly understood for marine fish whose aggregations and patchy prey fields create conditions for intense intraspecific competition. We evaluated whether sea louse infection is associated with decreased stomach fullness of wild juvenile sockeye salmon (Oncorhynchus nerka) in Johnstone Strait, British Columbia, during their marine migration from the Fraser River. Catigus clemensi comprised 98.6% of the pre-adult and adult lice and 86.5% of the copepodites (freshly attached juvenile lice); the rest were Lepeophtheinis salmonis. We found that infection status was an important predictor of relative stomach fullness for juvenile sockeye (wet stomach content mass divided by body mass), as indicated by mixed-effects model selection, and that highly infected fish had 17% +/- 8% lower relative stomach fullness than did lightly infected fish. This louse-associated reduction in relative stomach fullness occurs as the juvenile sockeye migrate through a food-limited environment and, presumably, elevated competition. Given that early marine growth for juvenile salmon is often a predictor of survival, our results highlight the importance of understanding sublethal effects of parasites on salmonids and possibly other fish species. DOI
155. Pardo, SA; Cooper, AB; Reynolds, JD; Dulvy, NK. (2018) Quantifying the known unknowns: estimating maximum intrinsic rate of population increase in the face of uncertainty.ICES J. Mar. Sci. 75 Quantifying the known unknowns: estimating maximum intrinsic rate of population increase in the face of uncertainty
bycatch; Carcharhinus; Chondrichthyes; demography; Elasmobranchii; reference points; risk assessment
Sensitivity to overfishing is often estimated using simple models that depend upon life history parameters, especially for species lacking detailed biological information. Yet, there has been little exploration of how uncertainty in life history parameters can influence demographic parameter estimates and therefore fisheries management options. We estimate the maximum intrinsic rate of population increase (rmax) for ten coastal carcharhiniform shark populations using an unstructured life history model that explicitly accounts for uncertainty in life history parameters. We evaluate how the two directly estimated parameters, age at maturity amat and annual reproductive output b, most influenced rmax estimates. Uncertainty in age at maturity values was low, but resulted in moderate uncertainty in rmax estimates. The model was sensitive to uncertainty in annual reproductive output for the least fecund species with fewer than 5 female offspring per year, which is not unusual for large elasmobranchs, marine mammals, and seabirds. Managers and policy makers should be careful to restrict mortality on species with very low annual reproductive output< 2 females per year. We recommend elasmobranch biologists to measure frequency distributions of litter sizes (rather than just a range) as well as improving estimates of natural mortality of data-poor elasmobranchs. DOI
154. van den Top, GG; Reynolds, JD; Prins, HHT; Mattsson, J; Green, DJ; Ydenberg, RC. (2018) From salmon to salmonberry: The effects of salmon-derived nutrients on the stomatal density of leaves of the nitriphilic shrub Rubus spectabilis.Funct. Ecol. 32 From salmon to salmonberry: The effects of salmon-derived nutrients on the stomatal density of leaves of the nitriphilic shrub Rubus spectabilis
Great Bear Rainforest; nutrient subsidy; Rubus spectabilis; salmonberry; salmon-derived nutrients; stomata; stomatal density
Nutrients derived from the carcasses of Pacific salmon have been shown to have wide-ranging effects on riparian systems. These include changes in community species composition and an increase in leaf nitrogen concentration, with the latter effect pronounced in the nitriphilic shrub Rubus spectabilis (salmonberry). Experimental work with other species has shown that leaf stomatal density increases in response to nitrogen fertilization. We predicted that the stomatal density of salmonberry leaves would vary directly with the density of spawning salmon in salmonberry leaves collected from 16 streams in the vicinity of Bella Bella, on British Columbia's central coast. We estimated the stomatal density along each stream, and quantified stream characteristics, including the number of spawning salmon (Oncorhynchus spp.), canopy cover, stem density and soil moisture. We found that salmon have both direct and indirect effects on stomatal density, the latter mediated by canopy cover and stem density. Salmonberry stomatal density increased by 1.12 stomata per mm(2) (similar to 0.5%) for every kg of salmon per metre of stream. Over the range of salmon densities observed (1.8-49.0 kg per metre of stream), stomatal density increased by almost 45 mm(-2), or more than 20%. These data confirm that the stomatal density in salmonberry responds positively to the opportunity for greater productivity provided by salmon carcasses. The data provide insight into the physiological and morphological processes supporting nitrogen uptake, which in turn influences plant community composition. A is available for this article. DOI
152. Godwin, SC; Dill, LM; Krkosek, M; Price, MHH; Reynolds, JD. (2017) Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice.J. Fish Biol. 91: 41-57 Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice
aquaculture; Fraser River; host-parasite; indirect effects; otolith; Pacific salmon
Daily growth rings were examined in the otoliths of wild juvenile sockeye salmon Oncorhynchus nerka to determine whether infection by ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis was associated with reduced host body growth, an important determinant of survival. Over 98% of the sea lice proved to be C. clemensi and the fish that were highly infected grew more slowly than uninfected individuals. Larger fish also grew faster than smaller fish. Finally, there was evidence of an interaction between body size and infection status, indicating the potential for parasite-mediated growth divergence. DOI
151. Jeffrey, KM; Côté, IM; Irvine, JR; Reynolds, JD. (2017) Changes in body size of Canadian Pacific salmon over six decades.Canadian Journal of Fisheries and Aquatic Sciences 74: 191-201 Changes in body size of Canadian Pacific salmon over six decades
Body size can sometimes change rapidly as an evolutionary response to selection or as a phenotypic response to changes in environmental conditions. Here, we revisit a classic case of rapid change in body size of five species of Pacific salmon (Oncorhynchus spp.) caught in Canadian waters, with a six-decade analysis (1951-2012). Declines in size at maturity of up to 3 kg in Chinook (Oncorhynchus tshawytscha) and 1 kg in coho salmon (Oncorhynchus kisutch) during the 1950s and 1960s were later reversed to match or exceed earlier sizes. In contrast, there has been little change in sockeye salmon (Oncorhynchus nerka) sizes and initial declines in pink (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) sizes have halted. Biomass of competing salmon species contributed to changes in size of all five species, and ocean conditions, as reflected by the North Pacific Gyre Oscillation and the Multivariate ENSO (El Nino -Southern Oscillation) indices, explained variation in four of the species. While we have identified a role of climate and density dependence in driving salmon body size, any additional influence of fisheries remains unclear. DOI
150. Kindsvater, HK; Reynolds, JD; de Mitcheson, YS; Mangel, M. (2017) Selectivity matters: Rules of thumb for management of plate-sized, sex-changing fish in the live reef food fish trade.Fish. Fish. 18: 821-836 Selectivity matters: Rules of thumb for management of plate-sized, sex-changing fish in the live reef food fish trade
capture-based aquaculture; egg limitation; fishery selectivity; live reef food fish; protogynous hermaphrodite; spawning potential ratio
Effective management of fisheries depends on the selectivity of different fishing methods, control of fishing effort and the life history and mating system of the target species. For sex-changing species, it is unclear how the truncation of age-structure or selection of specific size or age classes (by fishing for specific markets) affects population dynamics. We specifically address the consequences of plate-sized selectivity, whereby submature, plate-sized fish are preferred in the live reef food fish trade. We use an age-structured model to investigate the decline and recovery of populations fished with three different selectivity scenarios (asymptotic, dome-shaped and plate-sized) applied to two sexual systems (female-first hermaphroditism and gonochorism). We parameterized our model with life-history data from Brown-marbled grouper (Epinephelus fuscoguttatus) and Napoleon fish (Cheilinus undulatus). Plate-sized selectivity had the greatest negative effect on population trajectories, assuming accumulated fishing effort across ages was equal, while the relative effect of fishing on biomass was greatest with low natural mortality. Fishing such sex-changing species before maturation decreased egg production (and the spawning potential ratio) in two ways: average individual size decreased and, assuming plasticity, females became males at a smaller size. Somatic growth rate affected biomass if selectivity was based on size at age because in slow growers, a smaller proportion of total biomass was vulnerable to fishing. We recommend fisheries avoid taking individuals near their maturation age, regardless of mating system, unless catch is tightly controlled. We also discuss the implications of fishing post-settlement individuals on population dynamics and offer practical management recommendations. DOI
149. Nijland, W; Reshitnyk, LY; Starzomski, BM; Reynolds, JD; Darimont, CT; Nelson, TA. (2017) Deriving Rich Coastal Morphology and Shore Zone Classification from LIDAR Terrain Models.J. Coast. Res. 33: 949-958 Deriving Rich Coastal Morphology and Shore Zone Classification from LIDAR Terrain Models
British Columbia; coast; digital elevation model; substrate
Comprehensive mapping of shore-zone morphology supports evaluation of shore habitat, monitoring of environmental hazards, and characterization of the transfer of nutrients between marine and terrestrial environments. This article shows how rich shore-zone morphological metrics can be derived from LIDAR terrain models and evaluates the application of LIDAR to classify shore-zone substrates. The utility of LIDAR methods was tested in comparison with the current best-practice method of photo interpretation (i.e. the BC ShoreZone system) on Calvert Island, British Columbia, Canada. Wider applications are considered. Indicators of shore-zone morphology (i.e. slope, width, roughness, backshore elevation) were calculated from LIDAR terrain models for regularly spaced transects perpendicular to the coastline. A combination of boosted regression-tree modeling and direct-rule application was used to classify the shore-zone morphology according to the British Columbia (BC) ShoreZone system. Classification accuracy was assessed against existing ShoreZone classification data. Shore-zone substrate was classified from LIDAR-derived morphometric indicators with 90% accuracy (five classes). A full classification, which combined substrate with shore width and slope, results in lower correspondence (40%; 25 classes) when compared with ShoreZone classes. Differences can likely be attributed, in part, to variation in spatial resolution of elevation-based methods and photo interpretation. It is concluded that LIDAR data can be used to support characterization of shore-zone morphology. Differences in processing and interpretation cause a low direct correspondence with the current image-based classification system, but LIDAR has the advantage of higher resolution, rich terrain information, speed, and an objective and repeatable method for monitoring future change in coastal environments. DOI
148. Price, MHH; English, KK; Rosenberger, AG; MacDuffee, M; Reynolds, JD. (2017) Canada's Wild Salmon Policy: an assessment of conservation progress in British Columbia.Canadian Journal of Fisheries and Aquatic Sciences 74: 1507-1518 Canada's Wild Salmon Policy: an assessment of conservation progress in British Columbia
Canada's Policy for Conservation of Wild Pacific Salmon has been heralded as a transformative approach to the management of wild salmon whereby conservation is the highest priority. Given that changes to the Policy are under consideration, it is timely that we understand whether our state of knowledge and the status of wild salmon in Canada have indeed improved after its adoption in 2005. To answer these questions, we used two indices of improvement: (i) monitoring effort and (ii) abundance of spawning adults. Our results, based on data for all species from British Columbia's north and central coasts, show that monitoring effort has continued to erode, abundance of spawning adults has significantly declined for several species, the status of many salmon Conservation Units are in zones of concern, and 42% of the Conservation Units that we assessed as Red (threatened) would have improved in status had the Canadian fishery been reduced. We conclude with recommendations to help improve our knowledge of the status of salmon and enable a robust and successfully implemented Wild Salmon Policy for the future. DOI
146. Artelle, KA; Anderson, SC; Reynolds, JD; Cooper, AB; Paquet, PC; Darimont, CT. (2016) Ecology of conflict: marine food supply affects human-wildlife interactions on land.Scientific Reports 6 Ecology of conflict: marine food supply affects human-wildlife interactions on land
Human-wildlife conflicts impose considerable costs to people and wildlife worldwide. Most research focuses on proximate causes, offering limited generalizable understanding of ultimate drivers. We tested three competing hypotheses (problem individuals, regional population saturation, limited food supply) that relate to underlying processes of human-grizzly bear (Ursus arctos horribilis) conflict, using data from British Columbia, Canada, between 1960-2014. We found most support for the limited food supply hypothesis: in bear populations that feed on spawning salmon (Oncorhynchus spp.), the annual number of bears/km(2) killed due to conflicts with humans increased by an average of 20% (6-32% [ 95% CI]) for each 50% decrease in annual salmon biomass. Furthermore, we found that across all bear populations (with or without access to salmon), 81% of attacks on humans and 82% of conflict kills occurred after the approximate onset of hyperphagia (July 1st), a period of intense caloric demand. Contrary to practices by many management agencies, conflict frequency was not reduced by hunting or removal of problem individuals. Our finding that a marine resource affects terrestrial conflict suggests that evidence-based policy for reducing harm to wildlife and humans requires not only insight into ultimate drivers of conflict, but also management that spans ecosystem and jurisdictional boundaries. DOI
145. Hurteau, LA; Mooers, AO; Reynolds, JD; Hocking, MD. (2016) Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages.Ecology 97: 450-460 Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages
angiosperms; community assembly; flowering plants; marine nutrient subsidy; mean nearest taxon distance; Oncorhynchus; phylogenetic community structure; salmon
A signature of nonrandom phylogenetic community structure has been interpreted as indicating community assembly processes. Significant clustering within the phylogenetic structure of a community can be caused by habitat filtering due to low nutrient availability. Nutrient limitation in temperate Pacific coastal rainforests can be alleviated to some extent by marine nutrient subsidies introduced by migrating salmon, which leave a quantitative signature on the makeup of plant communities near spawning streams. Thus, nutrient-mediated habitat filtering could be reduced by salmon nutrients. Here, we ask how salmon abundance affects the phylogenetic structure of riparian flowering plant assemblages across 50 watersheds in the Great Bear Rainforest of British Columbia, Canada. Based on a regional pool of 60 plant species, we found that assemblages become more phylogenetically dispersed and species poor adjacent to streams with higher salmon spawning density. In contrast, increased phylogenetic clumping and species richness was seen in sites with low salmon density, with steeper slopes, further from the stream edge, and within smaller watersheds. These observations are all consistent with abiotic habitat filtering and biotic competitive exclusion acting together across local and landscape-scale gradients in nutrient availability to structure assembly of riparian flowering plants. In this case, rich salmon nutrients appear to release riparian flowering-plant assemblages from the confines of a low-nutrient habitat filter that drives phylogenetic clustering. DOI
144. Kindsvater, HK; Braun, DC; Otto, SP; Reynolds, JD. (2016) Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon.Ecology Letters 19: 687-696 Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon
Costs of reproduction; demography; iteroparity; life history theory; offspring size; salmon; semelparity
Species' life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage-structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co-variation in salmonids, we generate new hypotheses for the evolution of trade-offs among life history traits. DOI
143. Kindsvater, HK; Mangel, M; Reynolds, JD; Dulvy, NK. (2016) Ten principles from evolutionary ecology essential for effective marine conservation.Ecology and Evolution 6: 2125-2138 Ten principles from evolutionary ecology essential for effective marine conservation
Conservation; demography; extinction risk; fish; life-history theory; management; reference points; sustainability
Sustainably managing marine species is crucial for the future health of the human population. Yet there are diverse perspectives concerning which species can be exploited sustainably, and how best to do so. Motivated by recent debates in the published literature over marine conservation challenges, we review ten principles connecting life-history traits, population growth rate, and density-dependent population regulation. We introduce a framework for categorizing life histories, POSE (Precocial-Opportunistic-Survivor-Episodic), which illustrates how a species' life-history traits determine a population's compensatory capacity. We show why considering the evolutionary context that has shaped life histories is crucial to sustainable management. We then review recent work that connects our framework to specific opportunities where the life-history traits of marine species can be used to improve current conservation practices. DOI
142. Pardo, SA; Kindsvater, HK; Reynolds, JD; Dulvy, NK. (2016) Maximum intrinsic rate of population increase in sharks, rays, and chimaeras: the importance of survival to maturity.Canadian Journal of Fisheries and Aquatic Sciences 73: 1159-1163 Maximum intrinsic rate of population increase in sharks, rays, and chimaeras: the importance of survival to maturity
The maximum intrinsic rate of population increase (r(max)) is a commonly estimated demographic parameter used in assessments of extinction risk. In teleosts, r(max) can be calculated using an estimate of spawners per spawner, but for chondrichthyans, most studies have used annual reproductive output (b) instead. This is problematic as it effectively assumes all juveniles survive to maturity. Here, we propose an updated r(max) equation that uses a simple mortality estimator that also accounts for survival to maturity: the reciprocal of average life-span. For 94 chondrichthyans, we now estimate that r(max) values are on average 10% lower than previously published. Our updated r(max) estimates are lower than previously published for species that mature later relative to maximum age and those with high annual fecundity. The most extreme discrepancies in r(max) values occur in species with low age at maturity and low annual reproductive output. Our results indicate that chondrichthyans that mature relatively later in life, and to a lesser extent those that are highly fecund, are less resilient to fishing than previously thought. DOI
141. Weir, LK; Kindsvater, HK; Young, KA; Reynolds, JD. (2016) Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon.American Naturalist 188: 264-271 Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon
alternative mating strategies; competition; latitudinal clines; salmonids; sexual selection
Large male body size is typically favored by directional sexual selection through competition for mates. However, alternative male life-history phenotypes, such as "sneakers," should decrease the strength of sexual selection acting on body size of large "fighter" males. We tested this prediction with salmon species; in southern populations, where sneakers are common, fighter males should be smaller than in northern populations, where sneakers are rare, leading to geographical clines in sexual size dimorphism (SSD). Consistent with our prediction, fighter male body size and SSD (fighter male: female size) increase with latitude in species with sneaker males (Atlantic salmon Salmo salar and masu salmon Oncorhynchus masou) but not in species without sneakers (chum salmon Oncorhynchus keta and pink salmon Oncorhynchus gorbuscha). This is the first evidence that sneaker males affect SSD across populations and species, and it suggests that alternative male mating strategies may shape the evolution of body size. DOI
140. Braun, DC; Reynolds, JD; Patterson, DA. (2015) Using watershed characteristics to inform cost-effective stream temperature monitoring.Aquatic Ecology 49: 373-388 Using watershed characteristics to inform cost-effective stream temperature monitoring
Monitoring; Cost effective; Fish; Habitat; Temperature; Watershed; Spawning; Oncorhynchus
Water temperature is a key driver of aquatic processes. Monitoring stream water temperature is key to understanding current species distributions and future climate change impacts on freshwater ecosystems. However, a very small fraction of streams are continuously monitored for water temperature throughout North America, due to prohibitive logistical costs. We develop a framework that aids in developing cost-effective stream temperature monitoring by using stream habitat features to inform strategic site selection of temperature monitoring sites. We test this framework using sockeye salmon spawning streams as a model, which included 19 streams in the northern-most watershed of the Fraser River Basin, British Columbia, Canada. The objective of this framework is to evaluate the trade-off between cost (i.e., the number of streams monitored) and the effectiveness of monitoring scenarios at meeting different monitoring objectives. We compared monitoring scenarios that were informed by well-established relationships between variables and that are commonly collected or available as part of other monitoring activities (stream length, magnitude, order, gradient, wetted width, and spot temperatures) and water temperature metrics (maximum, mean, and variance during August) derived from continuously monitored streams to monitoring scenarios where streams were randomly selected. Informed scenarios included streams that were selected in order of watershed level and stream habitat characteristics (e.g., longest to shortest); ordering was based on the relationship between each habitat variable and temperature metrics. Informed monitoring scenarios were then compared to random selection of monitoring sites with regard to how well monitoring scenarios met two management objectives during the critical salmon spawning period: (1) identifying streams that exceed a temperature threshold and (2) identifying streams that represent the temperature regime of a complex of streams (e.g., mean and variance of streams within an aggregate of streams). Management objectives were met by monitoring fewer streams using the informed monitoring scenarios rather than the average of the random scenarios. This highlights how common inexpensive watershed level variables that relate to stream temperature can inform the strategic selection of sites and lead to more cost-effective stream temperature monitoring. DOI
139. Godwin, SC; Dill, LM; Reynolds, JD; Krkosek, M. (2015) Sea lice, sockeye salmon, and foraging competition: lousy fish are lousy competitors.Canadian Journal of Fisheries and Aquatic Sciences 72: 1113-1120 Sea lice, sockeye salmon, and foraging competition: lousy fish are lousy competitors
Pathogens threaten wildlife globally, but these impacts are not restricted to direct mortality from disease. For fish, which experience periods of extremely high mortality during their early life history, infections may primarily influence population dynamics and conservation through indirect effects on ecological processes such as competition and predation. We conducted a competitive foraging experiment using outmigrating juvenile Fraser River sockeye salmon (Oncorhynchus nerka) to determine whether fish with high abundances of parasitic sea lice (Caligus clemensi and Lepeophtheirus salmonis) have reduced competitive abilities when foraging. Highly infected sockeye were 20% less successful at consuming food, on average, than lightly infected fish. Competitive ability also increased with fish body size. Our results provide the first evidence that parasite exposure may have negative indirect effects on the fitness of juvenile sockeye salmon and suggest that indirect effects of pathogens may be of key importance for the conservation of marine fish. DOI
138. Harding, JMS; Segal, MR; Reynolds, JD. (2015) Location Is Everything: Evaluating the Effects of Terrestrial and Marine Resource Subsidies on an Estuarine Bivalve.PLoS One 10 Location Is Everything: Evaluating the Effects of Terrestrial and Marine Resource Subsidies on an Estuarine Bivalve
Estuaries are amongst the world's most productive ecosystems, lying at the intersection between terrestrial and marine environments. They receive substantial inputs from adjacent landscapes but the importance of resource subsidies is not well understood. Here, we test hypotheses for the effects of both terrestrial- and salmon-derived resource subsidies on the diet (inferred from stable isotopes of muscle tissue), size and percent nitrogen of the soft-shell clam (Mya arenaria), a sedentary estuarine consumer. We examine how these relationships shift across natural gradients among 14 estuaries that vary in upstream watershed size and salmon density on the central coast of British Columbia, Canada. We also test how assimilation and response to subsidies vary at smaller spatial scales within estuaries. The depletion and enrichment of stable isotope ratios in soft-shell clam muscle tissue correlated with increasing upstream watershed size and salmon density, respectively. The effects of terrestrial- and salmon-derived subsidies were also strongest at locations near stream outlets. When we controlled for age of individual clams, there were larger individuals with higher percent nitrogen content in estuaries below larger watersheds, though this effect was limited to the depositional zones below river mouths. Pink salmon exhibited a stronger effect on isotope ratios of clams than chum salmon, which could reflect increased habitat overlap as spawning pink salmon concentrate in lower stream reaches, closer to intertidal clam beds. However, there were smaller clams in estuaries that had higher upstream pink salmon densities, possibly due to differences in habitat requirements. Our study highlights the importance of upstream resource subsidies to this bivalve species, but that individual responses to subsidies can vary at smaller scales within estuaries. DOI
137. Nelson, MC; Hocking, MD; Harding, JN; Harding, JMS; Reynolds, JD. (2015) Quantifying the effects of stream habitat on populations of breeding Pacific salmon.Canadian Journal of Fisheries and Aquatic Sciences 72: 1469-1476 Quantifying the effects of stream habitat on populations of breeding Pacific salmon
Recognizing the mechanisms by which environmental conditions drive population dynamics can greatly benefit conservation and management. For example, reductions in densities of spawning Pacific salmon (Oncorhynchus spp.) have received considerable attention, but the role of habitat characteristics on population sizes of breeding salmon is not fully understood. We studied relationships between habitat characteristics and stream population densities of spawning chum (Oncorhynchus keta) and pink (Oncorhynchus gorbuscha) salmon in 44 streams in the Great Bear Rainforest of coastal British Columbia, Canada, with individual streams as the unit of comparison. Our results indicate that a small number of habitat characteristics are important in predicting population density of spawning chum and pink salmon in streams, namely pH for chum salmon and riparian slope and large wood volume for pink salmon. This is the largest multivariable comparison to examine habitat-population relationships in adult spawning salmon and may provide useful quantitative emphasis in guiding management. DOI
136. Nelson, MC; Reynolds, JD. (2015) Effects of subsidies from spawning chum and pink salmon on juvenile coho salmon body size and migration timing.Ecosphere 6 Effects of subsidies from spawning chum and pink salmon on juvenile coho salmon body size and migration timing
ecosystem-based management; fisheries; migration timing; nutrient subsidy; salmon
Organisms transporting nutrients from highly productive ecosystems can subsidize food webs and alter ecosystem processes. For example, the carcasses and eggs of migratory Pacific salmon (Oncorhynchus spp.) provide a high-quality food source that could potentially benefit other species of salmon rearing in fresh water. We investigated relationships between spawning chum (O. keta) and pink (O. gorbuscha) salmon density, and the body size and age of juvenile coho salmon (O. kisutch) in 17 streams on the central coast of British Columbia, Canada. Chum salmon density was the most consistently important and positive correlate of coho body size, in comparison with pink salmon density, juvenile coho salmon density, and numerous characteristics of habitats. This was shown by comparisons both among and within streams, and between sites above and below natural barriers to spawning chum and pink salmon. In addition, streams that had higher chum and pink salmon spawning densities had a higher proportion of age 0 coho (less age 1), suggesting earlier juvenile coho salmon migration to the ocean with increased spawning salmon nutrient availability. Most of the coho salmon sampled had little or no direct contact with spawning chum and pink salmon, which suggests an indirect, time-delayed influence on coho salmon body size. DOI
135. Swain, NR; Reynolds, JD. (2015) Effects of Salmon-Derived Nutrients and Habitat Characteristics on Population Densities of Stream-Resident Sculpins.PLoS One 10 Effects of Salmon-Derived Nutrients and Habitat Characteristics on Population Densities of Stream-Resident Sculpins
Movement of nutrients across ecosystem boundaries can have important effects on food webs and population dynamics. An example from the North Pacific Rim is the connection between productive marine ecosystems and freshwaters driven by annual spawning migrations of Pacific salmon (Oncorhynchus spp). While a growing body of research has highlighted the importance of both pulsed nutrient subsidies and disturbance by spawning salmon, their effects on population densities of vertebrate consumers have rarely been tested, especially across streams spanning a wide range of natural variation in salmon densities and habitat characteristics. We studied resident freshwater prickly (Cottus asper), and coastrange sculpins (C. aleuticus) in coastal salmon spawning streams to test whether their population densities are affected by spawning densities of pink and chum salmon (O. gorbuscha and O. keta), as well as habitat characteristics. Coastrange sculpins occurred in the highest densities in streams with high densities of spawning pink and chum salmon. They also were more dense in streams with high pH, large watersheds, less area covered by pools, and lower gradients. In contrast, prickly sculpin densities were higher in streams with more large wood and pools, and less canopy cover, but their densities were not correlated with salmon. These results for coastrange sculpins provide evidence of a numerical population response by freshwater fish to increased availability of salmon subsidies in streams. These results demonstrate complex and context-dependent relationships between spawning Pacific salmon and coastal ecosystems and can inform an ecosystem-based approach to their management and conservation. DOI
133. Braun, DC; Reynolds, JD. (2014) Life history and environmental influences on population dynamics in sockeye salmon.Canadian Journal of Fisheries and Aquatic Sciences 71: 1198-1208 Life history and environmental influences on population dynamics in sockeye salmon
Understanding linkages among life history traits, the environment, and population dynamics is a central goal in ecology. We compared 15 populations of sockeye salmon (Oncorhynchus nerka) to test general hypotheses for the relative importance of life history traits and environmental conditions in explaining variation in population dynamics. We used life history traits and habitat variables as covariates in mixed-effect Ricker models to evaluate the support for correlates of maximum population growth rates, density dependence, and variability in dynamics among populations. We found dramatic differences in the dynamics of populations that spawn in a small geographical area. These differences among populations were related to variation in habitats but not life history traits. Populations that spawned in deep water had higher and less variable population growth rates, and populations inhabiting streams with larger gravels experienced stronger negative density dependence. These results demonstrate, in these populations, the relative importance of environmental conditions and life histories in explaining population dynamics, which is rarely possible for multiple populations of the same species. Furthermore, they suggest that local habitat variables are important for the assessment of population status, especially when multiple populations with different dynamics are managed as aggregates. DOI
132. Ciannelli, L; Hunsicker, M; Beaudreau, A; Bailey, K; Crowder, LB; Finley, C; Webb, C., Reynolds, J.D. , Sagmiller,K., Andries, J.M., Hawthorne, D., Parrish, J., Heppell, S., Conway, F., Chigbu, P. Reynolds, J; Sagmiller, K; Anderies, JM; Hawthorne, D; Parrish, J; Heppell, S; Conway, F; Chigbu, (2014) Transdisciplinary graduate education in marine resource science and management.ICES Journal of Marine Science 71: 1047-1051 Transdisciplinary graduate education in marine resource science and management
experiential learning; graduate education; professional skills; transdisciplinary
In this article we consider the current educational needs for science and policy in marine resource management, and we propose a way to address them. The existing literature on cross-disciplinary education in response to pressing environmental problems is vast, particularly in conservation biology. However, actual changes in doctoral-level marine science programs lag behind this literature considerably. This is in part because of concerns about the time investment in cross-disciplinary education and about the job prospects offered by such programs. There is also a more fundamental divide between educational programs that focus on knowledge generation and those that focus on professional development, which can reinforce the gap in communication between scientists and marine resource managers. Ultimately, transdisciplinary graduate education programs need not only to bridge the divide between disciplines, but also between types of knowledge. Our proposed curriculum aligns well with these needs because it does not sacrifice depth for breadth, and it emphasizes collaboration and communication among diverse groups of students, in addition to development of their individual knowledge and skills. DOI
131. Favaro, C; Moore, JW; Reynolds, JD; Beakes, MP. (2014) Potential loss and rehabilitation of stream longitudinal connectivity: fish populations in urban streams with culverts.Can. J. Fish. Aquat. Sci. 71: 1805-1816 Potential loss and rehabilitation of stream longitudinal connectivity: fish populations in urban streams with culverts
Riverine connectivity is important to the persistence of fish communities, but culverts may impede fish movements to varying degrees and in both directions. Baffles can be installed in culverts to mitigate upstream connectivity loss; however, evaluation of their effectiveness is limited. To examine the potential impacts of culverts and their potential rehabilitation with baffles, we sampled fish populations in 26 streams that contained either (i) nonbaffled culverts or (ii) baffled culverts or (iii) lacked culverts (reference streams) in Metro Vancouver, British Columbia, Canada. Using mixed effects models, we compared fish responses across these three stream types to infer effects at the whole-stream scale (i.e., over both upstream and downstream positions equally), the within-stream scale (i.e., upstream versus downstream of culverts), and the interaction of scales. Densities (n.m(-2)) of coastrange sculpin (Cottus aleuticus) and prickly sculpin (Cottus asper) were significantly lower in nonbaffled and baffled stream types than in reference stream types, while densities of cutthroat trout (Oncorhynchus clarkii) and rainbow trout (Oncorhynchus mykiss) were significantly lower in reference stream types, indicating whole-stream differences. Using multivariate statistics, we similarly found that fish community compositions were significantly different across stream types. For our various fish responses, we found no interaction between stream type and upstream or downstream position. Further, we found reaches directly downstream of baffled culverts had greater fish biomass and that overall species richness increased with age of baffles. These data suggest that culverts may drive changes in fish populations at whole-stream scales, and restoration of these effects with baffles may take decades. DOI
130. Harding, JMS; Reynolds, JD. (2014) From earth and ocean: investigating the importance of cross-ecosystem resource linkages to a mobile estuarine consumer.Ecosphere 5 From earth and ocean: investigating the importance of cross-ecosystem resource linkages to a mobile estuarine consumer
connectivity; conservation; cross-ecosystem processes; ecosystem-based management; fisheries; flux; Great Bear Rainforest; landscape structure; Pacific Northwest; particulate organic matter; salmon; subsidy
Externally derived resources often contribute to the structuring of ecological communities. Estuaries are one of the most productive ecosystems in the world and provide an ideal system to test how communities may be shaped by resource subsidies because they occur at the intersection of marine, freshwater and terrestrial habitats. Here we tested the effects of both terrestrial- and salmon-derived subsidies, in addition to other factors such as habitat area, on the diet (inferred from stable isotopes), abundance and size of a mobile estuarine consumer, the Dungeness crab (Metacarcinus magister). Crab trap surveys encompassed 19 watersheds over two seasons in the central coast of British Columbia, Canada, which spanned natural gradients in estuary size, watershed size, riparian tree composition, and Pacific salmon spawning density. Stable isotope ratios of crab tissue confirmed the predictions that estuarine nutrient regimes can be strongly affected by upstream watershed size, salmon density, and the dominance of nitrogen-fixing red alder (Alnus rubra). There were more crabs in larger estuaries and the largest crabs were found in estuaries below the largest watersheds. The proportional contributions of terrestrial- and salmon-derived subsidies to the diet of Dungeness crabs increased with watershed size and salmon density, respectively. These results confirmed that resource subsidies can constitute large proportions of the Dungeness crab's diet, that crab abundance is determined by habitat size, but that crab size is affected by the magnitude of terrestrial resource influx. DOI
129. Harding, JN; Harding, JMS; Reynolds, JD. (2014) Movers and shakers: nutrient subsidies and benthic disturbance predict biofilm biomass and stable isotope signatures in coastal streams.Freshwater Biology 59: 1361-1377 Movers and shakers: nutrient subsidies and benthic disturbance predict biofilm biomass and stable isotope signatures in coastal streams
aufwuchs; ecosystem-based management; fisheries; nutrient pulse; periphyton
Nutrient subsidies and physical disturbance from migrating species can have strong impacts on primary producers. In the north Pacific, adult salmon (Oncorhynchus spp.) transport marine-derived nutrients back to freshwater streams and can also significantly disrupt the substratum during spawning events. We tested for effects of spawning pink (O.gorbuscha) and chum (O.keta) salmon on stream biofilm. Biofilm is a mix of algae, fungi and bacteria that provides food and habitat and forms the base of these aquatic food webs. We collected rock biofilm samples to compare stable isotopes and biomass prior to and following peak salmon spawning in 16 catchments on the central coast of British Columbia, Canada. We conducted two separate analyses. The first was a within-stream comparison, which focused on 5 catchments that had a barrier to pink and chum salmon migration. The second was an among-stream analysis that included all 16 catchments and explicitly considered biotic and abiotic factors, in addition to salmon density, known to influence biofilm growth and isotope ratios. Salmon density proved to be the best predictor of biofilm 15N. Biofilm 13C was best predicted by salmon density and catchment size. While spring chlorophyll a increased with mean salmon density, it was on average lower during spawning in the autumn, probably due to physical disturbance from spawning salmon. These results show that of the several variables considered to affect biofilm isotopes and biomass, salmon density and catchment size are among the most influential in coastal streams where salmon spawn. DOI
128. Harding, JN; Reynolds, JD. (2014) Opposing forces: Evaluating multiple ecological roles of Pacific salmon in coastal stream ecosystems.Ecosphere 5 Opposing forces: Evaluating multiple ecological roles of Pacific salmon in coastal stream ecosystems
ecosystem-based management; fisheries; freshwater; Great Bear Rainforest; insects; resource subsidy; river
Resource flows and disturbance from species migrations can alter the productivity, structure and function of an ecosystem. Annual mass migrations of Pacific salmon (Oncorhynchus spp.) to coastal watersheds import vast quantities of potentially limiting nutrients that have been shown to increase primary and secondary productivity in streams and lakes. Substrate disturbance during spawning can also export nutrients and reduce primary and secondary production. Here we study the impacts of these dual roles of salmon on stream invertebrates. We collected benthic macroinvertebrates in 15 streams prior to and following peak salmon spawning on British Columbia's central coast. Along with other habitat measurements including stream water chemistry, temperature, and watershed size, we investigated the effects of salmon on invertebrate delta N-15, delta C-13 and biomass density (mg/m(2)) among 15 streams and within 5 streams, upstream and downstream of barriers to spawning salmon. We found that stream invertebrates assimilate salmon-derived nutrients in proportion to availability but invertebrate biomass density declines in both seasons with increasing salmon density. Benthic disturbance appears to be the cause of this decline in the fall, but the decline in the spring may be due to the slow recovery of invertebrates from substrate disturbance the previous fall or salmon nutrients may be indirectly driving declines in spring invertebrate biomass by subsidizing other trophic levels and eliciting a trophic cascade. DOI
127. Lapointe, NWR; Cooke, SJ; Imhof, JG; Boisclair, D; Casselman, JM; Curry, RA; Langer, OE; McLaughlin, RL; Minns, CK; Post, JR; Power, M; Rasmussen, JB; Reynolds, JD; Richardson, JS; Tonn, WM. (2014) Principles for ensuring healthy and productive freshwater ecosystems that support sustainable fisheries.Environmental Reviews 22: 110-134 Principles for ensuring healthy and productive freshwater ecosystems that support sustainable fisheries
biodiversity; connectivity; cumulative effects; global processes; habitat; watershed
Freshwater ecosystems and the fisheries they support are increasingly threatened by human activities. To aid in their management and protection, we outline nine key principles for supporting healthy and productive ecosystems based on the best available science, including laws of physics and chemistry apply to ecology; population dynamics are regulated by reproduction, mortality, and growth; habitat quantity and quality are prerequisites of fish productivity; connectivity among habitats is essential for movements of fishes and their resources; freshwater species and their habitats are tightly linked to surrounding watersheds; biodiversity can enhance ecosystem resiliency and productivity; global processes affect local populations; anthropogenic stressors have cumulative effects; and evolutionary processes can be important. Based on these principles, we provide general recommendations for managing and protecting freshwater ecosystems and the fisheries they support, with examples of successful implementation for each strategy. Key management strategies include engage and consult with stakeholders; ensure that agencies have sufficient capacity, legislation, and authority to implement policies and management plans; define metrics by which fisheries resources and management success or failure will be measured; identify and account for threats to ecosystem productivity; adopt the precautionary approach to management; embrace adaptive management; implement ecosystem-based management; account for all ecosystem services provided by aquatic ecosystems; protect and restore habitat as the foundation for fisheries; and protect biodiversity. Ecosystems are complex with many intertwined components and ignoring linkages and processes significantly reduces the probability of management success. These principles must be considered when identifying management options and developing policies aiming to protect productive freshwater ecosystems and sustainable fisheries.Website DOI
126. Nelson, MC; Reynolds, JD. (2014) Time-Delayed Subsidies: Interspecies Population Effects in Salmon.PLOS One 9 Time-Delayed Subsidies: Interspecies Population Effects in Salmon
Cross-boundary nutrient inputs can enhance and sustain populations of organisms in nutrient-poor recipient ecosystems. For example, Pacific salmon (Oncorhynchus spp.) can deliver large amounts of marine-derived nutrients to freshwater ecosystems through their eggs, excretion, or carcasses. This has led to the question of whether nutrients from one generation of salmon can benefit juvenile salmon from subsequent generations. In a study of 12 streams on the central coast of British Columbia, we found that the abundance of juvenile coho salmon was most closely correlated with the abundance of adult pink salmon from previous years. There was a secondary role for adult chum salmon and watershed size, followed by other physical characteristics of streams. Most of the coho sampled emerged in the spring, and had little to no direct contact with spawning salmon nutrients at the time of sampling in the summer and fall. A combination of techniques suggest that subsidies from spawning salmon can have a strong, positive, time-delayed influence on the productivity of salmon-bearing streams through indirect effects from previous spawning events. This is the first study on the impacts of nutrients from naturally-occurring spawning salmon on juvenile population abundance of other salmon species.Website DOI PubMed
125. Swain, NR; Hocking, MD; Harding, JN; Reynolds, JD. (2014) Effects of salmon on the diet and condition of stream-resident sculpins.Canadian Journal of Fisheries and Aquatic Sciences 71: 521-532 Effects of salmon on the diet and condition of stream-resident sculpins
Pacific salmon (Oncorhynchus spp.) can subsidize freshwater food webs with marine-derived nutrients from their eggs, juveniles, and carcasses. However, trophic interactions between spawning salmon and freshwater fish across natural gradients in salmon subsidies remain unclear. We tested how salmon affected the diets and condition of two dominant freshwater consumers - prickly and coastrange sculpins (Cottus asper and Cottus aleuticus, respectively) - across a wide gradient of pink salmon (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) biomass from 33 streams in the Great Bear Rainforest of British Columbia, Canada. Sculpin diets shifted from invertebrates and juvenile salmonids to salmon eggs when salmon arrived in autumn, with salmon-derived nutrient contributions to diets and sculpin condition increasing with increasing biomass of spawning salmon among streams. Season, habitat, and individual sculpin body size and species also mediated the effects of salmon on sculpin diet as inferred from their carbon and nitrogen stable isotope signatures. This study shows the timing and pathways by which spawning salmon influence the diets and condition of freshwater consumers, and some of the individual and environmental factors that can regulate uptake of salmon nutrients in streams, thus informing ecosystem-based management. DOI
124. Artelle, KA; Anderson, SC; Cooper, AB; Paquet, PC; Reynolds, JD; Darimont, CT. (2013) Confronting Uncertainty in Wildlife Management: Performance of Grizzly Bear Management.PLOS One 8 Confronting Uncertainty in Wildlife Management: Performance of Grizzly Bear Management
DECISION-MAKING; CONSERVATION; FISHERIES; POPULATION; MORTALITY
Scientific management of wildlife requires confronting the complexities of natural and social systems. Uncertainty poses a central problem. Whereas the importance of considering uncertainty has been widely discussed, studies of the effects of unaddressed uncertainty on real management systems have been rare. We examined the effects of outcome uncertainty and components of biological uncertainty on hunt management performance, illustrated with grizzly bears (Ursus arctos horribilis) in British Columbia, Canada. We found that both forms of uncertainty can have serious impacts on management performance. Outcome uncertainty alone - discrepancy between expected and realized mortality levels - led to excess mortality in 19% of cases (population-years) examined. Accounting for uncertainty around estimated biological parameters (i.e., biological uncertainty) revealed that excess mortality might have occurred in up to 70% of cases. We offer a general method for identifying targets for exploited species that incorporates uncertainty and maintains the probability of exceeding mortality limits below specified thresholds. Setting targets in our focal system using this method at thresholds of 25% and 5% probability of overmortality would require average target mortality reductions of 47% and 81%, respectively. Application of our transparent and generalizable framework to this or other systems could improve management performance in the presence of uncertainty. DOI
123. Braun, DC; Patterson, DA; Reynolds, JD. (2013) Maternal and environmental influences on egg size and juvenile life-history traits in Pacific salmon.Ecology and Evolution 3: 1727-1740 Maternal and environmental influences on egg size and juvenile life-history traits in Pacific salmon
SOCKEYE-SALMON; ONCORHYNCHUS-NERKA; OFFSPRING PERFORMANCE; BRITISH-COLUMBIA; ATLANTIC SALMON; FRASER-RIVER; CLUTCH SIZE; FEMALE SIZE; EVOLUTION; MIGRATION
Life-history traits such as fecundity and offspring size are shaped by investment trade-offs faced by mothers and mediated by environmental conditions. We use a 21-year time series for three populations of wild sockeye salmon (Oncorhynchus nerka) to test predictions for such trade-offs and responses to conditions faced by females during migration, and offspring during incubation. In years when their 1100km upstream migration was challenged by high water discharges, females that reached spawning streams had invested less in gonads by producing smaller but not fewer eggs. These smaller eggs produced lighter juveniles, and this effect was further amplified in years when the incubation water was warm. This latter result suggests that there should be selection for larger eggs to compensate in populations that consistently experience warm incubation temperatures. A comparison among 16 populations, with matching migration and rearing environments but different incubation environments (i.e., separate spawning streams), confirmed this prediction; smaller females produced larger eggs for their size in warmer creeks. Taken together, these results reveal how maternal phenotype and environmental conditions can shape patterns of reproductive investment and consequently juvenile fitness-related traits within and among populations. DOI
122. Field, RD; Reynolds, JD. (2013) Ecological links between salmon, large carnivore predation, and scavenging birds.Journal of Avian Biology 44: 9-16 Ecological links between salmon, large carnivore predation, and scavenging birds
COASTAL BRITISH-COLUMBIA; PACIFIC SALMON; FOOD WEBS; ECOSYSTEMS; LANDSCAPE; SIZE; ONCORHYNCHUS; COMMUNITIES; ENRICHMENT; DIVERSITY
We compared scavenging bird abundance and diversity across 17 estuaries on the Central Coast of British Columbia, Canada in relation to landscape characteristics and biomass of spawning salmon and senescent and depredated salmon carcasses. We discovered that all metrics for spawning salmon and carcass biomasses were strong predictors of scavenger abundance and diversity. Specifically, Shannons diversity, which emphasizes rare species richness, and total abundances of scavengers, corvids (Corvus spp.), and small and large gulls (Larus spp.) were most strongly predicted by total biomass of carcasses. In contrast, the abundance of bald eagles Haliaeetus leucocephalus was most strongly predicted by biomass of carcasses that had been killed or scavenged by other predators (mostly bears and wolves). Simpsons diversity, which emphasizes evenness of common species, was best predicted by total spawning salmon biomass. Estuary area also featured prominently among top predictors of most scavenger metrics. Our results suggest a link between terrestrial salmon predators and bald eagles, and that available salmon biomass is important for maintaining the abundance and diversity of scavenging birds that congregate at estuaries throughout the spawning season. DOI
121. Hocking, MD; Dulvy, NK; Reynolds, JD; Ring, RA; Reimchen, TE. (2013) Salmon subsidize an escape from a size spectrum.Proceedings of the Royal Society B-Biological Sciences 280 Salmon subsidize an escape from a size spectrum
SPECIES ABUNDANCE DISTRIBUTIONS; BODY MASS RELATIONSHIPS; STRUCTURED FOOD WEBS; PACIFIC SALMON; POPULATION-DENSITY; ENERGY USE; COMMUNITIES; ECOSYSTEMS; PREDATION; NUTRIENTS
A general rule in ecology is that the abundance of species or individuals in communities sharing a common energy source decreases with increasing body size. However, external energy inputs in the form of resource subsidies can modify this size spectrum relationship. Here, we provide the first test of how a marine resource subsidy can affect size spectra of terrestrial communities, based on energy derived from Pacific salmon carcasses affecting a forest soil community beside streams in western Canada. Using both species-based and individual approaches, we found size structuring in this forest soil community, and transient community-wide doubling of standing biomass in response to energy pulses from Pacific salmon carcasses. One group of species were clear outliers in the middle of the size spectrum relationship: larval calliphorid and dryomyzid flies, which specialize on salmon carcasses, and which showed a tenfold increase in biomass in their size class when salmon were available. Thus, salmon subsidize their escape from the size spectrum. These results suggest that using a size-based perspective of resource subsidies can provide new insights into the structure and functioning of food webs. DOI
120. Price, MHH; Glickman, BW; Reynolds, JD. (2013) Prey Selectivity of Fraser River Sockeye Salmon during Early Marine Migration in British Columbia.Transactions of the American Fisheries Society 142: 1126-1133 Prey Selectivity of Fraser River Sockeye Salmon during Early Marine Migration in British Columbia
JUVENILE PACIFIC SALMON; ONCORHYNCHUS-NERKA; CHINOOK SALMON; CLIMATE-CHANGE; NORTH-AMERICA; COHO SALMON; SEA LICE; STRAIT; GEORGIA; SURVIVAL
Mortality of salmon during early marine life has long been thought to be a critical factor in limiting overall abundance. One of the key hypotheses proposed to explain the long-term productivity decline of Canada's iconic Fraser River Sockeye Salmon Oncorhynchus nerka, is deficient habitat conditions experienced during early marine life. Our study is a first step towards testing this hypothesis, with an aim of understanding food availability and prey choice of juvenile salmon early in their coastal migration. We investigated zooplankton density, diet composition, and foraging selectivity of juvenile Fraser Sockeye Salmon during the 2009 and 2010 migrations and determined whether the timing of their migration was related to feeding success. Sockeye Salmon diets showed high prey diversity and a preference for euphausiid, amphipod, decapod, terrestrial insect, fish, egg, and cumacean prey. Calanoid copepods, the most abundant available prey, were not strongly selected in either year. Zooplankton densities were highest in the tidally mixed Discovery Passage-Johnstone Strait area. The fish appeared to have an adequate prey resource pool during their early marine migration, and in the 2years of our study we observed similar feeding success throughout the migration period. Importantly, we found no evidence of food limitations that might indicate that juveniles suffered food deprivation. Further research is needed to test the generality of these findings, including the potential impacts of warming ocean temperatures on the timing and availability of prey during migration. Received October 29, 2012; accepted April 18, 2013 DOI
119. Braun, DC; Reynolds, JD. (2012) Cost-effective variable selection in habitat surveys.Methods in Ecology and Evolution 3: 388-396 Cost-effective variable selection in habitat surveys
conservation; cost-effectiveness; diminishing returns; efficiency; monitoring; multicollinearity; survey design
1. Researchers usually expect to understand the ecological systems better when they examine more variables. However, we cannot measure everything because time and money are limited, so we need to make difficult choices. Decisions are complicated by the fact that variables are often either uninformative or highly correlated, leading to diminishing returns on information with new variables. Correlated variables and diminishing returns on information per variable can be explicitly incorporated with costs of data collection to design cost-effective survey programmes. 2. We develop a step-by-step quantitative protocol to evaluate the cost-effectiveness of survey designs under different cost scenarios to help scientists and managers design cost-effective surveys. We illustrate this protocol using a case study that relates physical stream habitat variables to variation in sockeye salmon spawning populations. 3. We present our protocol by comparing linear regression models containing different combinations of variables representing different survey designs. The steps of the protocol are to (i) eliminate redundant variables, (ii) calculate costs scenarios, (iii) calculate survey performance metrics and (iv) identify and compare a subset of survey designs that maximize effectiveness at a given cost. Survey designs are compared by their ranked performance using R 2, AICc, average cost-effectiveness ratio and incremental cost-effectiveness ratio. 4. Our case study shows diminishing returns on the information provided by the addition of more variables as survey costs increase. The protocol supports the design of cost-effective monitoring programmes and leads to a general discussion relating changing environmental conditions to survey costs, including the need for clear and measurable objectives, which allow scientific information to be translated into management options. DOI
118. Connors, B.M., Braun, D.C., Peterman, R.M., Cooper, A.B., Reynolds, J.D., Dill, L.M., Ruggerone, G.T. & Krkosek, M. (2012) Migration links ocean-scale competition and local ocean conditions with exposure to farmed salmon to shape wild salmon dynamics.Conservation Letters 2012, 1-9 Migration links ocean-scale competition and local ocean conditions with exposure to farmed salmon to shape wild salmon dynamics.
Climate, competition, and disease are well-recognized drivers of population
dynamics. These stressors can be intertwined by animal migrations, leading to
uncertainty about the roles of natural and anthropogenic factors in conservation
and resource management. We quantitatively assessed the four leading
hypotheses for an enigmatic long-term decline in productivity of Canada’s
iconic Fraser River sockeye salmon: (1) delayed density-dependence, (2) local
oceanographic conditions, (3) pathogen transmission from farmed salmon, and
(4) ocean-basin scale competition with pink salmon. Our findings suggest that
the long-term decline is primarily explained by competition with pink salmon,
which can be amplified by exposure to farmed salmon early in sockeye marine
life, and by a compensatory interaction between coastal ocean temperature
and farmed-salmon exposure. These correlative relationships suggest oceanicscale
processes, which are beyond the reach of current regulatory agencies,
may exacerbate local ecological processes that challenge the coexistence of
fisheries and aquaculture-based economies in coastal seas.Website DOI
115. Hocking, MD; Reynolds, JD. (2012) Nitrogen uptake by plants subsidized by Pacific salmon carcasses: a hierarchical experiment.Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 42: 908-917 Nitrogen uptake by plants subsidized by Pacific salmon carcasses: a hierarchical experiment
Bears (Ursus spp.) and other predators can capture and transport large numbers of Pacific salmon (Oncorhynchus spp.) to riparian areas beside small coastal streams, a process that may affect site productivity and local plant communities. We used a novel experimental manipulation of salmon carcasses to analyze understory plant uptake of salmon-derived N. A hierarchical before-after, control-impact design was used with the addition of chum salmon (Oncorhynchus keta (Walbaum in Artedi, 1792)) carcasses to forest sites along 11 streams on the central coast of British Columbia, Canada. Eight months after carcass placement, the foliar %N and delta N-15 in three herbaceous and one moss species had increased by an average of 14%-60% (%N) and 0.5-3.3% (delta N-15) at treatment carcass sites versus control sites. Treatment effects for %N were typically greater than for delta N-15. Nitrogen isotope signatures at carcass sites were highly variable (delta N-15 range = 30.1%) and were mediated by plant species, stream salmon density, carcass mass, and individual plant foliar %N. These results show that understory plants use N from salmon during an important period of plant growth many months after carcasses were deposited in riparian areas. However, they also indicate that habitat variation across spatial scales from individual plants to streams needs to be considered when estimating the contribution of salmon to plant nutrition. DOI
112.Reynolds, J.D., Favaro, B. & Côté. (2012) Canada: A bleak day for the environment.Nature 487, 171 Canada: A bleak day for the environment
It was a dark day for environmental science and policy in Canada on 29 June.
The country's Conservative Party has been steadily dismantling environmental protection since winning a majority government last year (see, for example, Nature http://doi.org/h2v; 2012). Further alarming changes to environmental laws were concealed in a 'budget bill' that was ratified by the Senate on 29 June.
For example, the Canadian Environmental Assessment Act has been replaced by a weaker law that reduces government oversight of the environmental impact of a proposed pipeline from the Alberta oil sands to tankers off British Columbia. Canada's Fisheries Act now allows for more pollution and no longer protects fish habitats, except for fisheries. The National Round Table on the Environment and the Economy, which provides independent scientific advice on sustainable development, will be dissolved in March 2013. A finance committee that had no scientific or public input has decided that this massive legislative overhaul could proceed as written.
Globally significant research facilities have already been axed, including the renowned Experimental Lakes Area and the Polar Environment Atmospheric Research Laboratory in the high Arctic. Scientific agencies such as Fisheries and Oceans Canada (DFO), Environment Canada and Parks Canada have had to sack most of the personnel responsible for habitat management and monitoring, including those in the DFO's marine-pollution programme.
The new legislative framework marginalizes science in environmental management, and could do irreparable harm to the environment and the economy it supports. Such tactics match Canada's intransigence on climate change: the same bill made it the first country to pull out of the Kyoto agreement.Website DOI
111. Braun, DC; Reynolds, JD. (2011) Relationships between habitat characteristics and breeding population densities in sockeye salmon (Oncorhynchus nerka).Canadian Journal of Fisheries and Aquatic Sciences 68: 758-767 Relationships between habitat characteristics and breeding population densities in sockeye salmon (Oncorhynchus nerka)
We examine the importance of stream habitat characteristics in governing variation in spawning densities of sockeye salmon (Oncorhynchus nerka) across 32 streams in the Fraser River Basin, British Columbia, Canada. We used mixed-effects models to examine four competing hypotheses for the influence of abiotic stream characteristics acting on either adult salmon or embryo mortality. All models that received support using Akaike's information criterion included stream characteristics that are associated with cover. These included the percent area of pools, percentage of the banks that were undercut, and large woody debris (in that order). These results suggest the importance of stream characteristics, which reduce risk of predation on adults, in determining spawning sockeye salmon densities. Thus, identification of a small number of physical characteristics of streams provides insight into ecological processes that determine population densities. This information can be used to quantify habitat quality, which can guide habitat prioritization for conservation. DOI
110. Field, RD; Reynolds, JD. (2011) Sea to sky: impacts of residual salmon-derived nutrients on estuarine breeding bird communities.Proceedings of the Royal Society B-Biological Sciences 278: 3081-3088 Sea to sky: impacts of residual salmon-derived nutrients on estuarine breeding bird communities
coastal watersheds; ecosystem-based management; biodiversity; wetlands; fisheries; Great Bear Rainforest
Pacific salmon (Oncorhynchus spp.) returning to streams around the North Pacific Rim provide a nutrient subsidy to these ecosystems. While many species of animals feed directly on salmon carcasses each autumn, salmon-derived nutrients can also be stored in coastal habitats throughout the year. The effects of this storage legacy on vertebrates in other seasons are not well understood, especially in estuaries, which can receive a large portion of post-spawning salmon nutrients. We examine the effects of residual salmon-derived nutrients, forest habitats and landscape features on summer breeding birds in estuary forests. We compared models containing environmental variables and combined chum (Oncorhynchus keta) and pink (Oncorhynchus gorbuscha) salmon biomass to test predictions concerning bird density and diversity. We discovered that total bird, insectivore, golden-crowned kinglet and Pacific wren densities and Shannon's diversity in the summer were strongly predicted by salmon biomass in the autumn. For most metrics, this relationship approaches an asymptote beyond 40 000 kg of salmon biomass. Foliage height diversity, watershed catchment area and estuary area were also important predictors of avian communities. Our study suggests that the legacy of salmon nutrients influences breeding bird density and diversity in estuaries that vary across a wide gradient of spawning salmon biomass. DOI
109. Hocking, MD; Reynolds, JD. (2011) Impacts of Salmon on Riparian Plant Diversity.Science 331 Impacts of Salmon on Riparian Plant Diversity
The study of natural gradients in nutrient subsidies between ecosystems allows for predictions of how changes in one system can affect biodiversity in another. We performed a large-scale empirical test of the role of Pacific salmon (Oncorhynchus spp.) in structuring riparian plant communities. A comparison of 50 watersheds in the remote Great Bear Rainforest of British Columbia's central coast in Canada shows that salmon influence nutrient loading to plants, shifting plant communities toward nutrient-rich species, which in turn decreases plant diversity. These effects are mediated by interactions between salmon density and the physical characteristics of watersheds. Predicting how salmon affect terrestrial ecosystems is central to conservation plans that aim to better integrate ecosystem values into resource management. DOI
108. Molloy, PP; Paddack, MJ; Reynolds, JD; Gage, MJG; Côté, IM. (2011) Relative size-at-sex-change in parrotfishes across the Caribbean: is there variance in a supposed life-history invariant?Evolutionary Ecology 25: 429-446 Relative size-at-sex-change in parrotfishes across the Caribbean: is there variance in a supposed life-history invariant?
Hermaphroditism; Invariant life-history analysis; Protandry; Protogyny; Sex allocation theory; Sex change
Invariant life-history theory has been used to identify parallels in life histories across diverse taxa. One important invariant life-history model predicts that, given simple assumptions and conditions, size-at-sex-change relative to maximum attainable body size (relative size-at-sex-change, RSSC) will be invariant across populations and species in sequential hermaphrodites. Even if there are broad species-wide limits to RSSC, populations could fine-tune RSSC to local conditions and, consequently, exhibit subtle but important differences in timing of sex change. Previous analyses of the invariant sex-change model have not explicitly considered the potential for meaningful differences in RSSC within the confines of a broader 'invariance'. Furthermore, these tests differ in their geographical and taxonomic scope, which could account for their conflicting conclusions. We test the model using several populations of three female-first sex-changing Caribbean parrotfish species. We first test for species-wide invariance using traditional log-log regressions and randomisation analyses of population-specific point estimates of RSSC. We then consider error around these point estimates, which is rarely incorporated into invariant analyses, to test for differences among populations in RSSC. Log-log regressions could not unequivocally diagnose invariance in RSSC across populations; randomisation tests identified an invariant RSSC in redband parrotfish only. Analyses that incorporated within-population variability in RSSC revealed differences among populations in timing of sex change, which were independent of geography for all species. While RSSC may be evolutionarily constrained (as in redband parrotfish), within these bounds the timing of sex change may vary among populations. This variability is overlooked by traditional invariant analyses and not predicted by the existing invariant model. DOI
107. Price, MHH; Proboszcz, SL; Routledge, RD; Gottesfeld, AS; Orr, C; Reynolds, JD. (2011) Sea Louse Infection of Juvenile Sockeye Salmon in Relation to Marine Salmon Farms on Canada's West Coast.PLoS One 6 Sea Louse Infection of Juvenile Sockeye Salmon in Relation to Marine Salmon Farms on Canada's West Coast
Background: Pathogens are growing threats to wildlife. The rapid growth of marine salmon farms over the past two decades has increased host abundance for pathogenic sea lice in coastal waters, and wild juvenile salmon swimming past farms are frequently infected with lice. Here we report the first investigation of the potential role of salmon farms in transmitting sea lice to juvenile sockeye salmon (Oncorhynchus nerka). Methodology/Principal Findings: We used genetic analyses to determine the origin of sockeye from Canada's two most important salmon rivers, the Fraser and Skeena; Fraser sockeye migrate through a region with salmon farms, and Skeena sockeye do not. We compared lice levels between Fraser and Skeena juvenile sockeye, and within the salmon farm region we compared lice levels on wild fish either before or after migration past farms. We matched the latter data on wild juveniles with sea lice data concurrently gathered on farms. Fraser River sockeye migrating through a region with salmon farms hosted an order of magnitude more sea lice than Skeena River populations, where there are no farms. Lice abundances on juvenile sockeye in the salmon farm region were substantially higher downstream of farms than upstream of farms for the two common species of lice: Caligus clemensi and Lepeophtheirus salmonis, and changes in their proportions between two years matched changes on the fish farms. Mixed-effects models show that position relative to salmon farms best explained C. clemensi abundance on sockeye, while migration year combined with position relative to salmon farms and temperature was one of two top models to explain L. salmonis abundance. Conclusions/Significance: This is the first study to demonstrate a potential role of salmon farms in sea lice transmission to juvenile sockeye salmon during their critical early marine migration. Moreover, it demonstrates a major migration corridor past farms for sockeye that originated in the Fraser River, a complex of populations that are the subject of conservation concern. DOI PubMed
106. Brooks, SE; Allison, EH; Gill, JA; Reynolds, JD. (2010) Snake prices and crocodile appetites: Aquatic wildlife supply and demand on Tonle Sap Lake, Cambodia.Biological Conservation 143: 2127-2135 Snake prices and crocodile appetites: Aquatic wildlife supply and demand on Tonle Sap Lake, Cambodia
Wildlife trade; Conservation; Trade regulation; Exploitation; Crocodile farming; Consumer preferences; Substitutability; Price elasticity
Commercial trade is a major driver of over-exploitation of wild species, but the pattern of demand and how it responds to changes in supply is poorly understood. Here we explore the markets for snakes from Tonle Sap Lake in Cambodia to evaluate future exploitation scenarios, identify entry points for conservation and, more generally, to illustrate the value of multi-scale analysis of markets to traded wildlife conservation. In Cambodia, the largest driver of snake exploitation is the domestic trade in snakes as crocodile food. We estimate that farmed crocodiles consume between 2.7 and 12.2 million snakes per year. The market price for crocodiles has been in decline since 2003, which, combined with rising prices for their food, has led to a reduced frequency of feeding and closure of small farms. The large farms that generate a disproportionate amount of the demand for snakes continue to operate in anticipation of future market opportunities, and preferences for snakes could help maintain demand if market prices for crocodiles rise to pre 2003 levels. In the absence of a sustained demand from crocodile farms, it is also possible that alternative markets will develop, such as one for human snack food. The demand for snakes, however, also depends on the availability of substitute resources, principally fish. The substitutability and low price elasticity of demand offers a relatively sustainable form of consumerism. Given the nature of these market drivers, addressing consumer preferences and limiting the protection of snakes to their breeding season are likely to be the most effective tools for conservation. This study highlights the importance of understanding the structure of markets and the behaviour of consumer demand prior to implementing regulations on wildlife hunting and trade. (C) 2010 Elsevier Ltd. All rights reserved. DOI
105. Brooks, SE; Kebede, B; Allison, EH; Reynolds, JD. (2010) The Balance of Power in Rural Marketing Networks: A Case Study of Snake Trading in Cambodia.Journal of Development Studies 46: 1003-1025 The Balance of Power in Rural Marketing Networks: A Case Study of Snake Trading in Cambodia
Producers in small-scale rural markets often receive unfavourable prices for their goods as a result of more powerful market participants. This study uses a combination of price analysis and interview data to assess the position of snake hunters in the aquatic snake market from Tonle Sap Lake in Cambodia. Despite the hunters' dependence on intermediary traders for market access and credit, the evidence implies that they are not powerless participants. Intermediary traders operate under high competition as a result of the increasing scarcity of snakes and therefore, despite interlocked credit and snake markets, offer relatively high prices to hunters. DOI
104. Darimont, CT; Bryan, HM; Carlson, SM; Hocking, MD; MacDuffee, M; Paquet, PC; Price, MHH; Reimchen, TE; Reynolds, JD; Wilmers, CC. (2010) Salmon for terrestrial protected areas.Conservation Letters 3: 379-389 Salmon for terrestrial protected areas
Ecosystem-based fisheries management; freshwater; marine subsidies; protected areas; salmon; Oncorhynchus; terrestrial
Although managers safeguard protected areas for migratory species, little consideration has been given to how migratory species might benefit parks. Additionally, whereas land-sea connections are considered in management of protected areas, most effort has focused on reducing negative "downstream" processes. Here, we offer a proposal to promote positive "upstream" processes by safeguarding the seasonal pulse of marine nutrients imported into freshwater and riparian ecosystems by spawning migrations of Pacific salmon. Currently, high rates of fishing limit this important contribution to species and processes that terrestrial parks were designed to protect. Accordingly, we propose limiting exploitation in areas and periods through which salmon runs bound for terrestrial protected areas can migrate. Best suited for less commercially valuable but relatively abundant and widespread pink and chum salmon (O. gorbuscha and keta), our proposal thus considers ecosystem and societal needs for salmon. We conclude by outlining strategies to overcome socio-economic barriers to implementation. DOI
103. Losos, CJC; Reynolds, JD; Dill, LM. (2010) Sex-selective Predation by Threespine Sticklebacks on Sea Lice: A Novel Cleaning Behaviour.Ethology 116: 981-989 Sex-selective Predation by Threespine Sticklebacks on Sea Lice: A Novel Cleaning Behaviour
Cleaning interactions have been described in a wide range of fish species and other taxa. We observed a novel cleaning behaviour during a study of the transmission dynamics of sea lice (Lepeophtheirus salmonis) between juvenile pink salmon (Oncorhynchus gorbuscha) and threespine sticklebacks (Gasterosteus aculeatus) in the Broughton Archipelago, British Columbia, Canada. Experiments showed that sticklebacks significantly reduced the number of sea lice on individual juvenile salmon. Adult female lice were preferentially consumed by sticklebacks, and gravid female lice also experienced egg string cropping. Overall, 76% of gravid female lice experienced either consumption, egg string cropping, or both by sticklebacks. This preference by sticklebacks for female parasites may stem from female lice being larger than males and the added nutritional value of egg strings on gravid females. Cleaning by sticklebacks can potentially have an impact on sea louse populations on wild juvenile salmon. DOI
102. Price, MHH; Morton, A; Reynolds, JD. (2010) Evidence of farm-induced parasite infestations on wild juvenile salmon in multiple regions of coastal British Columbia, Canada.Canadian Journal of Fisheries and Aquatic Sciences 67:1925-1932 Evidence of farm-induced parasite infestations on wild juvenile salmon in multiple regions of coastal British Columbia, Canada
Salmon farms are spatially concentrated reservoirs of fish host populations that can disrupt natural salmonid host-parasite dynamics. Sea lice frequently infect farm salmon and parasitize sympatric wild juvenile salmonids, with negative impacts on survival in Europe and Pacific Canada. We examined louse parasitism of wild juvenile chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha) from three salmon farming regions in British Columbia (Finlayson, Broughton Archipelago, and Georgia Strait). We compared sites of low and high exposure to farms and included an area without farms (Bella Bella) to assess baseline infection levels. Louse prevalence and abundance were lowest and most similar to natural baseline levels at low-exposure sites and highest at high-exposure sites in all farm regions. A significantly greater proportion of the lice were Lepeophtheirus salmonis at high-exposure sites. Exposure to salmon farms was the only consistently significant factor to explain the variation in prevalence data, with a secondary role played by salinity. Our results support the hypothesis that salmon farms are a major source of sea lice on juvenile wild salmon in salmon farming regions and underscore the importance of using management techniques that mitigate threats to wild stocks.
101. Verspoor, JJ; Braun, DC; Reynolds, JD. (2010) Quantitative Links Between Pacific Salmon and Stream Periphyton.Ecosystems 13: 1020-1034 Quantitative Links Between Pacific Salmon and Stream Periphyton
aquatic conservation; food web; ecosystem-based management; ecosystem engineer; resource subsidy; marine-derived nutrients; nutrient pulse
Species' impacts on primary production can have strong ecological consequences. In freshwater ecosystems, Pacific salmon (Oncorhynchus spp.) may influence stream periphyton through substrate disturbance during spawning and nutrient subsidies from senescent adults. The shape of relationships between the abundance of spawning salmon and stream periphyton, as well as interactions with environmental variables, are incompletely understood and may differ across the geographic range of salmon. We examined these relationships across 24 sockeye salmon (Oncorhynchus nerka) spawning streams in north-central British Columbia, Canada. The influence of salmon abundance and environmental variables (temperature, light, dissolved nutrients, water velocity, watershed size, and invertebrate grazer abundance) on post-spawning periphyton abundance and nitrogen stable isotope signatures, which can indicate the uptake of salmon nitrogen, was evaluated using linear regression models and Akaike Information Criterion. Periphyton nitrogen stable isotope signatures were best described by a positive log-linear relationship with an upstream salmon abundance metric that includes salmon from earlier years. This suggests the presence of a nutrient legacy. In contrast, periphyton abundance was negatively related to the spawning-year salmon density, which likely results from substrate disturbance during spawning, and positively related to dissolved soluble reactive phosphorus prior to spawning, which may indicate phosphorus limitation in the streams. These results suggest that enrichment from salmon nutrients does not always translate into elevated periphyton abundance. This underscores the need to directly assess the outcome of salmon impacts on streams rather than extrapolating from stable isotope evidence for the incorporation of salmon nutrients into food webs. DOI
100. Allison, EH; Perry, AL; Badjeck, MC; Adger, WN; Brown, K; Conway, D; Halls, AS; Pilling, GM; Reynolds, JD; Andrew, NL; Dulvy, NK. (2009) Vulnerability of national economies to the impacts of climate change on fisheries.Fish and Fisheries 10: 173-196 Vulnerability of national economies to the impacts of climate change on fisheries
COD GADUS-MORHUA; NINO SOUTHERN-OSCILLATION; GLOBAL FOOD SECURITY; SEA-LEVEL RISE; ADAPTIVE CAPACITY; NORTH-SEA; EL-NINO; ECOLOGICAL RESILIENCE; POPULATION-DYNAMICS; OCEAN ACIDIFICATION
Anthropogenic global warming has significantly influenced physical and biological processes at global and regional scales. The observed and anticipated changes in global climate present significant opportunities and challenges for societies and economies. We compare the vulnerability of 132 national economies to potential climate change impacts on their capture fisheries using an indicator-based approach. Countries in Central and Western Africa (e.g. Malawi, Guinea, Senegal, and Uganda), Peru and Colombia in north-western South America, and four tropical Asian countries (Bangladesh, Cambodia, Pakistan, and Yemen) were identified as most vulnerable. This vulnerability was due to the combined effect of predicted warming, the relative importance of fisheries to national economies and diets, and limited societal capacity to adapt to potential impacts and opportunities. Many vulnerable countries were also among the world's least developed countries whose inhabitants are among the world's poorest and twice as reliant on fish, which provides 27% of dietary protein compared to 13% in less vulnerable countries. These countries also produce 20% of the world's fish exports and are in greatest need of adaptation planning to maintain or enhance the contribution that fisheries can make to poverty reduction. Although the precise impacts and direction of climate-driven change for particular fish stocks and fisheries are uncertain, our analysis suggests they are likely to lead to either increased economic hardship or missed opportunities for development in countries that depend upon fisheries but lack the capacity to adapt.Website DOI
99. Brooks, SE; Allison, EH; Gill, JA; Reynolds, JD. (2009) Reproductive and Trophic Ecology of an Assemblage of Aquatic and Semi-Aquatic Snakes in Tonle Sap, Cambodia.Copeia : 7-20 Reproductive and Trophic Ecology of an Assemblage of Aquatic and Semi-Aquatic Snakes in Tonle Sap, Cambodia
SEXUAL SIZE DIMORPHISM; WATER SNAKES; FEEDING ECOLOGY; COLUBRIDAE; LAKE; LATICAUDINAE; HOMALOPSINAE; CONSTRAINTS; MORPHOLOGY; PATTERNS
We studied the reproductive and trophic ecology of a group of aquatic and semi-aquatic snakes that face severe hunting pressure in Cambodia. Over a two-year period we sampled hunters' catches, measuring and dissecting a total of 8982 specimens of seven snake species, five of which belong to the family Homalopsidae. The seven species-Enhydris enhydris, Enhydris longicauda, Homalopsis buccata, Enhydris bocourti, Erpeton tentaculatus, Xenochrophis piscator, and Cylindrophis ruffus-all Inhabit Tonle Sap Lake, the largest lake In South-East Asia. All species are sexually dimorphic In either body size or tall length. The larger species, E. bocourti and H. buccata, have a larger size at maturity, and the non-homalopsids, X. piscator and C. ruffus, have the highest and lowest fecundities, respectively. Clutch size increases significantly with female body size In all species, and with body condition In E. enhydris. Our data also suggest that relative Investment in reproduction Increases with size In E. enhydris, which has the largest sample size. All species except one are synchronized In their timing of reproduction with the seasonally receding flood waters of the lake. There was variation In both the frequency of feeding and the prey size and type among species, with the homalopsids more similar to one another than to the other non-homalopsid species. The prey to predator mass ratio ranged from 0.04 to 0.1 In the homalopsids, compared to 0.15 to 0.17 In the non-homalopsids. There was also variation in the feeding frequency between the sexes that differed between species and six species continued to feed while gravid. These detailed life history analyses can help provide a basis for assessing conservation options for these heavily exploited species. DOI
98. Dulvy NK, Pinnegar JK and Reynolds JD. (2009) Holocene extinctions in the sea.In Holocene Extinctions in the Sea. (Ed S.T. Turvey), Pp. 129-150. Oxford University Press, Oxford.Holocene extinctions in the sea.
96. Garcia-Pena, GE; Thomas, GH; Reynolds, JD; Szekely, T. (2009) Breeding systems, climate, and the evolution of migration in shorebirds.Behavioral Ecology 20: 1026-1033 Breeding systems, climate, and the evolution of migration in shorebirds
LONG-DISTANCE MIGRATION; SEXUAL SELECTION; PARENTAL CARE; CORRELATED EVOLUTION; DISCRETE CHARACTERS; EXTRAPAIR PATERNITY; LATITUDINAL CLINES; AVIAN MIGRATION; BIRD MIGRATION; ARRIVAL TIMES
Migratory behavior incurs energetic costs that may influence the time and energy available for reproduction including territory establishment, courtship, pair formation, incubation, and brood care. Conversely pair formation and parental care may leave less time and energy available for migration and other nonbreeding behaviors. Therefore, natural selection favoring migratory behavior may influence breeding system evolution and vice versa. We used phylogenetic comparative methods to investigate relationships between migration distance and the wide diversity of breeding systems in shorebirds (sandpipers, plovers and allies). Consistent with previous studies, we show that long-distance migration is associated with reduced male care across shorebird species. We then use directional phylogenetic analyses to test whether migration distances have tended to increase or decrease over time and whether such evolutionary changes have preceded or followed changes in parental care. We show that evolutionary transitions from short-distance migration to long-distance migration have coevolved with changes from full biparental care to reduced male care. Furthermore, our directional analyses suggest that increments in migration distance are more likely to have preceded reductions in male care than vice versa. We also show that male polygamy is associated with northern breeding latitudes when the nonbreeding latitude is controlled statistically. Although this suggests that mating systems, parental care, and migration have more complex relationships than previously thought, our results are consistent with the hypothesis that migration influences breeding system evolution. DOI
95. Hunter, E; Cotton, RJ; Metcalfe, JD; Reynolds, JD. (2009) Large-scale variation in seasonal swimming patterns of plaice in the North Sea.Marine Ecology-Progress Series 392: 167-178 Large-scale variation in seasonal swimming patterns of plaice in the North Sea
PLEURONECTES-PLATESSA L; TIDAL STREAM TRANSPORT; ATLANTIC BLUEFIN TUNA; DIEL VARIATION; MANAGEMENT STRATEGIES; POPULATION-STRUCTURE; MIGRATORY BEHAVIOR; FISH; CATCHABILITY; MOVEMENTS
We examined the mid-water swimming activity of 139 mature female plaice Pleuronectes platessa L. These were tagged with electronic data storage tags (DST1s and DST3s) to test whether swimming at different times of the year differed among areas of the North Sea with average tidal current velocities ranging from fast (West), to intermediate (East), to slow (North). Longer swimming duration and more tidal activity were predicted for the western group, where fast-flowing tidal currents allow efficient selective tidal stream transport. Individual depth data were converted into binary records representing either swimming or resting; repeated patterns of swimming were analysed according to cycle-length frequencies. Most swimming occurred during expected times of migration and spawning (October to March). Plaice infrequently spent >5 h in mid-water, and rarely left the sea-bed during summer. DST1 tagged plaice (West only) spent the longest times swimming (p > 0.001), but there was no significant effect of Area for DST3s (all areas), suggesting that swimming plays an important behavioural role in migration in addition to transport between feeding and spawning areas. Tidal patterns of activity occurred in all 3 sub-stocks, predominantly during the migratory period (albeit at a significantly lower frequency in the North). These data provide one of few examples where the annual behaviour patterns of a fish stock have been recorded across a large part of its geographical range. The results have important implications for understanding the energetics of fish migration and the availability of demersal stocks to capture by commercial and survey vessels. DOI
94. Molloy, PP; Reynolds, JD; Gage, MJG; Côté, IM. (2009) Effects of an artisanal fishery on non-spawning grouper populations.Marine Ecology-Progress Series 392: 253-262 Effects of an artisanal fishery on non-spawning grouper populations
IDEAL FREE DISTRIBUTION; US-VIRGIN-ISLANDS; SOUTHEASTERN UNITED-STATES; SEX-CHANGING FISH; GULF-OF-MEXICO; EPINEPHELUS-GUTTATUS; RED HIND; FLORIDA-KEYS; CORAL-REEF; SIZE DISTRIBUTION
Many populations of groupers (Teleostei: Serranidae) are overfished, partly because most species form spawning aggregations that are temporally and spatially predictable and therefore easily targeted by fisheries. However, most grouper fisheries operate year-round, thus there can also be high mortality during non-spawning periods. We investigated the impact of fishing around Anguilla, British West Indies, on a commercially important grouper, the red hind Epinephelus guttatus, during the non-breeding season. We combined information on the spatial intensity of the fishery with underwater surveys of groupers to test for associations between fishing intensity and fish size and density across 19 sites. Red hind density was unrelated to fishing intensity but red hinds were larger in areas that were targeted more intensively by fishers. While these results might be taken to suggest that fishing has no negative impacts on red hind demographics, we present evidence from fish markets that fishing intensity on this species during the non-spawning season is high. A variety of mechanisms may mask site-specific negative impacts on density and size of red hinds. In particular, fishers can easily move among sites to track grouper abundance and body size, thereby making it difficult to detect impacts on red hinds during the non-spawning season. DOI
93. Paddack, MJ; Reynolds, JD; Aguilar, C; Appeldoorn, RS; Beets, J; Burkett, EW; Chittaro, PM; Clarke, K; Esteves, R; Fonseca, AC; Forrester, GE; Friedlander, AM; Garcia-Sais, J; Gonzalez-Sanson, G; Jordan, LKB; McClellan, DB; Miller, MW; Molloy, PP; Mumby, PJ; Nagelkerken, I; Nemeth, M; Navas-Camacho, R; Pitt, J; Polunin, NVC; Reyes-Nivia, MC; Robertson, DR; Rodriguez-Ramirez, A; Salas, E; Smith, SR; Spieler, RE; Steele, MA; Williams, ID; Wormald, CL; Watkinson, AR; Côté, IM. (2009) Recent Region-wide Declines in Caribbean Reef Fish Abundance.Current Biology 19: 590-595 Recent Region-wide Declines in Caribbean Reef Fish Abundance
GREAT-BARRIER-REEF; MASS MORTALITY; CORAL-REEFS; DIADEMA-ANTILLARUM; TROPHIC CASCADES; MARINE RESERVES; PROTECTED AREAS; COMMUNITIES; POPULATIONS; ECOSYSTEMS
Profound ecological changes are occurring on coral reefs throughout the tropics [1-3], with marked coral cover losses and concomitant algal increases, particularly in the Caribbean region . Historical declines in the abundance of large Caribbean reef fishes likely reflect centuries of overexploitation [5-7]. However, effects of drastic recent degradation of reef habitats on reef fish assemblages have yet to be established. By using meta.-analysis, we analyzed time series of reef fish density obtained from 48 studies that include 318 reefs across the Caribbean and span the time period 1955-2007. Our analyses show that overall reef fish density has been declining significantly for more than a decade, at rates that are consistent across all subregions of the Caribbean basin (2.7% to 6.0% loss per year) and in three of six trophic groups. Changes in fish density over the past half-century are modest relative to concurrent changes in benthic cover on Caribbean reefs. However, the recent significant decline in overall fish abunclance and its consistency across several trophic groups. and among both fished and nonfished species indicate that Caribbean fishes have begun to respond negatively to habitat degradation. DOI
92. Brooks, S; Reynolds, JD; Allison, E. (2008) Sustained by Snakes? Seasonal Livelihood Strategies and Resource Conservation by Tonle Sap Fishers in Cambodia.Human Ecology 36: 835-851 Sustained by Snakes? Seasonal Livelihood Strategies and Resource Conservation by Tonle Sap Fishers in Cambodia
SMALL-SCALE FISHERIES; BIODIVERSITY CONSERVATION; POVERTY ALLEVIATION; MANAGEMENT; BUSHMEAT; LAKE; SUSTAINABILITY; VULNERABILITY; RESILIENCE; HARVEST
This paper situates concerns for conservation of aquatic snakes and livelihood sustainability in Cambodia within a social-ecological systems context and thereby presents a challenge to conventional species-based conservation programmes. Fishing for low-value water snakes has become a widespread activity within the floating communities of Tonle Sap Lake in the last 20 years in response to new market opportunities, provided primarily by a crocodile farming industry. The scale and intensity of this new form of exploitation and reports of declines in catch per fisher have highlighted this activity as a conservation concern, yet its role within local livelihood strategies was previously unknown. We show that it is of increasing importance to the less well-off, and is linked to higher incomes within this group, where it potentially reduces their vulnerability to fluctuations and declines in fish catches. It is particularly important as a means to smooth seasonality of incomes in this flood pulse-driven social-ecological system. We argue that shifts between snake-hunting and fishing, as a market-driven adaptive livelihood strategy by the poor, may be more compatible with wider ecosystem conservation and development goals than alternatives such as increased fishing effort or converting floodplain habitats for seasonal agriculture. DOI
91. Einum, S; Nislow, KH; Reynolds, JD; Sutherland, WJ. (2008) Predicting population responses to restoration of breeding habitat in Atlantic salmon.Journal of Applied Ecology 45: 930-938 Predicting population responses to restoration of breeding habitat in Atlantic salmon
carrying capacity; exploitation; habitat restoration; individual based modelling; intercohort competition; local density dependence; population regulation; spatial modelling
1. Habitat degradation is seriously threatening stream biodiversity and productivity world-wide. For salmonid fish, restoration projects in disturbed systems commonly aim at increasing the availability of suitable breeding habitats, but expectations of effects on population abundance based on explicit models are lacking. 2. We used a spatial population model to predict how breeder dispersion may influence population dynamics of salmonids. Simulations involved changing the relative abundance of habitat suitable for two juvenile size classes (small fry and larger parr), the type of density-dependent regulation (effects on survival only vs. effects on survival and growth) and intercohort competitive mechanisms. 3. Increased breeding dispersion could alter patterns of density-dependent mortality and increase equilibrium adult abundance and maximum sustainable yield (MSY). However, there was a strong interaction between stage-specific habitat abundance and breeding dispersion. The most pronounced effects of breeding dispersion were observed under intermediate levels of fry habitat abundance. 4. When fry habitat was abundant, density-dependent mortality was most intense during the parr stage, and increased breeding dispersion did not increase adult abundance or MSY. In fact, when populations were regulated in the parr stage, increased breeding dispersion could cause decreased adult abundance because of the effects of intercohort competition. This negative effect only occurred, however, when competition among juveniles was symmetric (no age or size advantage). 5. Synthesis and applications. The population effects of restoring breeding habitat can differ among environments, and we have demonstrated how these differences can be understood in the light of stage-specific density dependence. Increasing spatial dispersion of breeders may often be an efficient measure for conserving threatened populations and increasing yields in fished populations. However, if direct evidence or habitat considerations suggest that fish populations experience density-dependent mortality during the parr stage, attempts to increase abundance through increased breeding distribution or artificial stocking should be avoided, as these are likely to be ineffective or even detrimental. The difference between fishing rates providing maximum sustainable yield and extinction is particularly small for such populations, suggesting that fish managers should adopt a conservative and flexible regulation regime. DOI
90. Hard, JJ; Gross, MR; Heino, M; Hilborn, R; Kope, RG; Law, R; Reynolds, JD. (2008) Evolutionary consequences of fishing and their implications for salmon.Evolutionary Applications 1: 388-408 Evolutionary consequences of fishing and their implications for salmon
SIZE-SELECTIVE MORTALITY; FISHERIES-INDUCED EVOLUTION; WHITEFISH COREGONUS-CLUPEAFORMIS; BACTERIAL KIDNEY-DISEASE; 3 DIFFERENT TEMPERATURES; LIFE-HISTORY EVOLUTION; RIVER SOCKEYE-SALMON; JUVENILE COHO SALMON; ATLANTIC SALMON; CHINOOK SALMON
We review the evidence for fisheries-induced evolution in anadromous salmonids. Salmon are exposed to a variety of fishing gears and intensities as immature or maturing individuals. We evaluate the evidence that fishing is causing evolutionary changes to traits including body size, migration timing and age of maturation, and we discuss the implications for fisheries and conservation. Few studies have fully evaluated the ingredients of fisheries-induced evolution: selection intensity, genetic variability, correlation among traits under selection, and response to selection. Most studies are limited in their ability to separate genetic responses from phenotypic plasticity, and environmental change complicates interpretation. However, strong evidence for selection intensity and for genetic variability in salmon fitness traits indicates that fishing can cause detectable evolution within ten or fewer generations. Evolutionary issues are therefore meaningful considerations in salmon fishery management. Evolutionary biologists have rarely been involved in the development of salmon fishing policy, yet evolutionary biology is relevant to the long-term success of fisheries. Future management might consider fishing policy to (i) allow experimental testing of evolutionary responses to exploitation and (ii) improve the long-term sustainability of the fishery by mitigating unfavorable evolutionary responses to fishing. We provide suggestions for how this might be done. DOI
89. Lengkeek, W; Didderen, K; Côté, IM; van der Zee, EM; Snoek, RC; Reynolds, JD. (2008) Plasticity in sexual size dimorphism and Rensch's rule in Mediterranean blennies (Blenniidae).Canadian Journal of Zoology-Revue Canadienne de Zoologie 86: 1173-1178 Plasticity in sexual size dimorphism and Rensch's rule in Mediterranean blennies (Blenniidae)
Comparative analyses of sexual size dimorphism (SSD) across species have led to the discovery of Rensch's rule. This rule states that SSD increases with body size when males are the largest sex, but decreases with increasing size when females are larger. Within-species comparisons of SSD in fish are rare, yet these may be a valuable tool to investigate evolutionary patterns on a fine scale. This study compares SSD among closely related populations of three species of Mediterranean blennies (Blenniidae): Microlipophrys canevae (Vinciguerra, 1880), Parablennius incognitus (Bath 1968), and Aidablennius sphynx (Valenciennes, 1836). SSD varied more among populations than among species and Rensch's rule was confirmed within two species. It is not likely that the variation among populations in SSD mirrors genetic variation, as many of the populations were in close proximity of one another, with a high potential for genetic exchange. This study complements larger scale analyses of other taxa and demonstrates the fine scale on which evolutionary processes responsible for Rensch's rule may be operating. DOI
88. Molloy, PP; Reynolds, JD; Gage, MJG; Mosqueirac, L; Côté, IM. (2008) Links between sex change and fish densities in marine protected areas.Biological Conservation 141: 187-197 Links between sex change and fish densities in marine protected areas
body size; exploitation; fishing; grouper; hermaphroditism; meta-analysis; parrotfish
Sex change is widespread among marine fishes, including many species that are fished heavily, and is thought to be of conservation concern under some circumstances. As such, an important question in conservation is whether the implementation of marine protected areas (MPAs), which is a commonly used marine conservation tool, works as effectively for sex-changers as for non-sex-changers. To address this issue, we used meta-analyses of the ratio of fish abundances inside vs. outside MPAs to determine whether sex change affects the extent to which fish densities respond to protection. When all data were considered, there were similar responses to protection irrespective of reproductive mode. However, when analyses were restricted to older reserves (at least 10 years' protection), female-first sex-changers consistently benefited from protection, Non-sex-changers and male-first sex-changers showed more variable responses to protection and, as a result, there were no significant differences between fish with different reproductive modes in their overall response to protection. The same results were observed when the effects of fisheries status (targeted vs. not targeted) were controlled. Our results support the use of MPAs as important components of conservation and demonstrate that old reserves are most consistently beneficial to female-first sex-changing species. Finally, our results highlight the fact that some effects of protection are only detectable after several generations. (c) 2007 Elsevier Ltd. All rights reserved. DOI
87. Walters, C.J., Lichatowich, J.A., Peterman, R.J. & Reynolds, J.D. (2008) Report of the Skeena Independent Science Review Panel.A Report to the Canadian Department of Fisheries and Oceans and the British Columbia Ministry of the Environment. May 15, 2008. 140 P. Report of the Skeena Independent Science Review Panel.
86. Brooks, S.E., Reynolds, J.D. & Allison, E.H. (2007) The exploitation of water snakes from Tonle Sap Lake, Cambodia.In: Homalopsine Snakes; Evolutionary Experiments in Terrestrial-Aquatic Transitions (Ed. J.C. Murphy). Krieger Publishing, Melbourne, Fl, Usa.The exploitation of water snakes from Tonle Sap Lake, Cambodia.
85. Brooks, SE; Allison, EH; Reynolds, JD. (2007) Vulnerability of Cambodian water snakes: Initial assessment of the impact of hunting at Tonle Sap Lake.Biological Conservation 139: 401-414 Vulnerability of Cambodian water snakes: Initial assessment of the impact of hunting at Tonle Sap Lake
fisheries; homalopsidae; enhydris; reptile; Cambodia; Sustainability; conservation
This paper documents the emergent snake 'fishery' occurring on Tonle Sap Lake where an estimated 6.9 million snakes (mostly homalopsids) are removed annually, representing the world's largest exploitation of a single snake assemblage. Based on inter-views with hunters, we found that snake catches declined by 74-84% between 2000 and 2005, raising strong concerns about the sustainability of this hunting operation. A combination of experimental trials to estimate population sizes and extensive catch and trade monitoring programs - indicated that population density varies both spatially and temporally, largely due to the seasonally fluctuating environment of Tonle Sap Lake. The quantity of snakes captured mirrors the lake's seasonal fluctuations, due to temporal changes in both catch per unit effort and the number of people hunting. Through inter-views with hunters we scored the seven exploited species for perceived changes in catch size. All species were reported as declining and their scores match their predicted vulnerability based on a combination of timing of exploitation relative to breeding, proportion of catch consisting of mature females and large fecund females, fecundity, body size, size at maturity, and vulnerability to capture by gill nets. This information can inform conservation decisions for the longterm preservation of this snake assemblage. We propose emphasis should be placed on the snake skin trade that is targeting the largest, highly fecund females, and that any efforts to reduce hunting should focus on the peak in trade that occurs during the main breeding season. (C) 2007 Elsevier Ltd. All rights reserved. DOI
84. Jennings, S. & Reynolds, J.D. (2007) Body size, exploitation and conservation of marine organisms.In: Body Size: the Structure and Function of Aquatic Ecosystems (Eds. A.G. Hildrew, D. Rafaelli & R. Edmonds-Brown), Pp. 266-285. Cambridge University Press, CambridgeBody size, exploitation and conservation of marine organisms.
83. Molloy, PP; Goodwin, NB; Côté, IM; Gage, MJG; Reynolds, JD. (2007) Predicting the effects of exploitation on male-first sex-changing fish.Animal Conservation 10: 30-38 Predicting the effects of exploitation on male-first sex-changing fish
barramundi; fisheries model; fishing; hermaphroditism; protandry; protogyny; shrimp
Sex change is widespread among tropical marine fishes, many of which are targeted by fisheries. Conservation concerns have been raised that sex-changing species may be particularly prone to overexploitation by size-selective fishing. In the case of male-first sex-changers, populations may become egg limited if large females are disproportionately killed. However, if males reduce the size at which they change sex in response to higher female mortality, the population may still be sufficiently productive. We develop an age-based model to explore the effects of fishing on two types of male-first sex-changing fish: one with flexibility in size-at-sex-change and one without. These effects were compared with those of non-sex-changing populations with similar life-history and population characteristics. The model predicts that if male-first sex-changers cannot respond to elevated female mortality by adjusting their size-at-sex-change, the population will be more prone to recruitment limitation and extinction than non-sex-changers. These effects will be amplified as smaller individuals become susceptible to fishing mortality. However, if size-at-sex-change is flexible, sex-changers may be as resilient to fishing as non-sex-changers. Knowledge of a species' size-at-sex-change, and the mechanisms controlling it, should be fundamental to the selection of fisheries conservation strategies.PDF DOI
82. Molloy, PP; Goodwin, NB; Côté, IM; Reynolds, JD; Gage, MJG. (2007) Sperm competition and sex change: A comparative analysis across fishes.Evolution 61: 640-652 Sperm competition and sex change: A comparative analysis across fishes
hermaphrodite; mating system; protogyny; reproductive model; sex allocation theory; size-advantage model; Teleostei
Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change. DOI
80. Whiteman, EA; Côté, IM; Reynolds, JD. (2007) Ecological differences between hamlet (Hypoplectrus : Serranidae) colour morphs: between-morph variation in diet.Journal of Fish Biology 71: 235-244 Ecological differences between hamlet (Hypoplectrus : Serranidae) colour morphs: between-morph variation in diet
ecological specialization; morpho-species; niche partitioning; speciation; sympatry
Dietary differences between hamlet Hypoplectrus spp. colour morphs were examined in fishes from Puerto Rico, U.S. Virgin Islands, Curacao, Honduras and Belize. Hamlet diet across all countries was characterized by large overlap between most colour morphs in both the proportion and numbers of dietary items consumed, although some differences between morphs were apparent. Indigo hamlets Hypoplectrus indigo were the only morph to consume fishes (blue chromis Chromis cyanea and sunshinefish Chromis insolata) almost exclusively. The sympatric occurrence of other ecologically indistinguishable colour morphs, however, suggests that divergent ecological selection alone cannot explain population divergence in hamlets. Geographical variation in diet was also observed within black Hypoplectrus nigricans and yellowtail Hypoplectrus chlorurus hamlets which may reflect geographical differences in prey availability or differences in prey choice. (c) 2007 The Authors Journal compilation. (c) 2007 The Fisheries Society of the British Isles.PDF DOI
73. Bolle, LJ; Hunter, E; Rijnsdorp, AD; Pastoors, MA; Metcalfe, JD; Reynolds, JD. (2005) Do tagging experiments tell the truth? Using electronic tags to evaluate conventional tagging data.ICES Journal of Marine Science 62: 236-246 Do tagging experiments tell the truth? Using electronic tags to evaluate conventional tagging data
data storage tags; mark-recapture experiments; North Sea; plaice; Pleuronectes platessa
For more than a century, scientists have used mark-recapture techniques to describe the spatial dynamics of marine demersal fish species in the North Sea. Although such experiments have provided extensive data sets, the information is limited to the date and position at release and at recapture. Furthermore, these data may be biased due to the distribution of fishing effort. Recently, electronic (archival) data storage tags (DSTs) have successfully been used to reconstruct the movements of free-ranging demersal fish between release and recapture. Data from DST experiments allow the calculation of fisheries independent migration parameters, and thereby provide a means of evaluating conventional tagging data. We compared the migration patterns of North Sea plaice (Pleuronectes platessa L.) as inferred from a database of twentieth century conventional tagging experiments (CT), with data from 132 plaice tagged with DST. In general, the CT experiments allowed a reliable interpretation of migration patterns, although for certain release areas the migration distances were biased due to the heterogeneous distribution of fishing effort. (C) 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
72. Dulvy, NK; Jennings, S; Goodwin, NB; Grant, A; Reynolds, JD. (2005) Comparison of threat and exploitation status in North-East Atlantic marine populations.Journal of Applied Ecology 42: 883-891 Comparison of threat and exploitation status in North-East Atlantic marine populations
CITES; extinction risk; marine fisheries; minimum viable population; Red List
1. Threat listing of exploited marine species has been controversial because of the scientific uncertainty of extinction risk as well as the social, economic and political costs of management procedures that may be triggered by designation of species as threatened. 2. We applied three sets of threat criteria to 76 stocks (populations) of 21 exploited marine fish and invertebrate species. Two criteria sets were based on decline rates: World Conservation Union (IUCN A1) and the American Fisheries Society (AFS). The third set of criteria, based on population viability (IUCN E), was assessed using non-parametric simulation and two diffusion approximation methods. 3. We compared extinction risk outcomes (threatened or not) against the exploitation status of each stock as reported in fish stock assessments (inside or outside safe biological limits). For each combination of threat and exploitation we assessed the rate of hits, misses and false alarms. 4. Our analyses suggest that decline rate criteria provide risk categorizations consistent with population viability analyses when applied to exploited marine stocks. Nearly a quarter of the fish and invertebrate populations (n = 18) considered met one or more of the threat criteria. 5. None of the threat metrics produced false alarms, where sustainably exploited stocks were categorized as threatened. The quantitative IUCN E metrics produced higher hit rates than the decline rate metrics (IUCN A1 and AFS) and all of the metrics produced similar miss rates. However, the IUCN E methods could be applied to fewer stocks (12-14) compared with IUCN A1 decline rate and AFS criteria, both of which could be applied all 76 stocks. 6. Synthesis and applications. Threat criteria provide warnings of population collapse that are consistent with those provided in fisheries stock assessments. Our results suggest that scientists with different backgrounds and objectives should usually be able to agree on the stocks for which the most urgent management action is needed. Moreover, IUCN A1 decline rate metrics may provide useful indicators of population status when the information needed for full fisheries stock assessment is not available. DOI
71. Goodwin, NB; Dulvy, NK; Reynolds, JD. (2005) Macroecology of live-bearing in fishes: latitudinal and depth range comparisons with egg-laying relatives.Oikos 110: 209-218 Macroecology of live-bearing in fishes: latitudinal and depth range comparisons with egg-laying relatives
We examine how fishes with contrasting reproductive modes (egg-laying versus live-bearing) differ in geographic range size and distribution. One hypothesis based on dispersal suggests that egg-laying taxa should occupy a wider range of latitudes than live-bearing, whereas the opposite prediction has been derived from the idea that enhanced maternal input and a 'safe harbor' during development will enable live-bearers to occupy a wider range of latitudes and depths than egg-layers. Cross-species analysis supports the first hypothesis for teleosts, with egg-layers living in a wider range of latitudes than live-bearers but at lower latitudes, across a narrower depth range and at shallow depth. However, elasmobranchs show the opposite pattern, live-bearers having wider latitudinal ranges. Phylogenetic paired comparisons of sister egg-laying and live-bearing taxa confirm these contrasting patterns between teleosts and elasmobranchs. However, depth range, maximum latitude and depth do not differ with reproductive mode. Latitudinal range size increases with body size among all taxa. However, only teleosts have a positive relationship between body size and maximum latitude, depth and depth range, but this does not differ between reproductive modes. Egg-laying elasmobranchs have low dispersal, but live-bearers have not extended their maximum latitude or depth, despite the benefits of sheltered offspring. The differences in range size between egg-layers and live-bearers and the distinction between teleosts and elasmobranchs is consequence of contrasting mechanisms of dispersal and benefits of maternally buffered transport of developing offspring.
70. Green, RE; Balmford, A; Crane, PR; Mace, GM; Reynolds, JD; Turner, RK. (2005) A framework for improved monitoring of biodiversity: Responses to the World Summit on Sustainable Development.Conservation Biology 19: 56-65 A framework for improved monitoring of biodiversity: Responses to the World Summit on Sustainable Development
assessment; biodiversity measurement; biodiversity monitoring; evaluation; World Summit on Sustainable Development
The Convention on Biological Diversity (CBD) and the World Summit on Sustainable Development (WSSD) endorsed the Hague Ministerial Declaration that calls for a significant reduction of the current rate of biodiversity loss at the global, regional, and national levels by 2010. We argue that there is a shortage of standardized, regularly repeated measurements of the state of biomes and their biota that could be used to monitor progress toward this goal. In particular, there are few data that directly or indirectly measure the delivery of ecosystem services that depend on biodiversity. Given the link made in the declaration between biodiversity and poverty alleviation, this deficiency is of special concern. We suggest that greater attention should be given to defining the questions about changes in biodiversity that are relevant to CBD and WSSD goals and propose a framework through which the links between these questions and programs of monitoring and research could be made stronger and more explicit. The framework consists of three stages. First is a scoping stage in which reviews of existing knowledge and interactions with stakeholders help to define the subject of the evaluation and lead to a preliminary model of the system of interest. Second is a design stage in which the types of measurement and sampling strategies are selected by evaluating their fitness for purpose and the resources available to conduct the work. The final stage is implementation and reporting, which considers data collection and storage and the evaluation and dissemination of results. This framework can be applied across a broad range of biodiversity attributes and scales and, if combined with a systematic review of the most important and relevant questions about changes in biodiversity, would improve the coverage, fitness for purpose, and value for money of biodiversity monitoring. Slowing the rate of loss of biodiversity requires conservation action, but to know where this is most needed and whether it is working requires better and more comprehensive monitoring.
69. Mills, SC; Taylor, MI; Reynolds, JD. (2005) Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium hypothesis.Animal Behaviour 70: 31-37 Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium hypothesis
Two major hypotheses of host-parasite interactions have been proposed to explain cases where hosts do not defend themselves against parasites. The evolutionary lag hypothesis suggests that there has been insufficient time for a host response to evolve, whereas the evolutionary equilibrium hypothesis proposes that host defence does not evolve because it carries costs that outweigh the benefits. We tested potential benefits and costs of host defence in an unusual interaction, between a freshwater fish, the European bitterling, Rhodeus sericeus, and live unionid mussels that are used as hosts for the fish's eggs. We found a significant reduction in ventilation rate of mussels that were incubating bitterling embryos, which became more severe with an increasing number of embryos. We tested the hypothesis that the risk of ejecting a mussel's own larvae while ejecting bitterling embryos has constrained the evolution of a host response. This predicts that brooding female mussels would retain more bitterling larvae than males or nonbrooding females. This prediction was not supported: brooding female mussels contained as many larvae per accessible gill as, and fewer in total than, males or nonbrooding females. In summary, based on the costs and benefits of ejection that we measured, we found no evidence in support of the evolutionary equilibrium hypothesis. However, other differences between mussel species, such as gill structure as measured in this study, ventilation rates and differences in the distance eggs are lodged into the gills, may contribute to differences in egg ejection rates. (c) 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
68. Perry, AL; Low, PJ; Ellis, JR; Reynolds, JD. (2005) Climate change and distribution shifts in marine fishes.Science 308: 1912-1915 Climate change and distribution shifts in marine fishes
We show that the distributions of both exploited and nonexploited North Sea fishes have responded markedly to recent increases in sea temperature, with nearly two-thirds of species shifting in mean latitude or depth or both over 25 years. For species with northerly or southerly range margins in the North Sea, half have shown boundary shifts with warming, and all but one shifted northward. Species with shifting distributions have faster life cycles and smaller body sizes than nonshifting species. Further temperature rises are likely to have profound impacts on commercial fisheries through continued shifts in distribution and alterations in community interactions.
67.Reynolds, JD; Dulvy, NK; Goodwin, NB; Hutchings, JA. (2005) Biology of extinction risk in marine fishes.P Roy Soc B-Biol Sci 272: 2337-2344 Biology of extinction risk in marine fishes
fisheries; conservation; life histories; IUCN; CITES
We review interactions between extrinsic threats to marine fishes and intrinsic aspects of their biology that determine how populations and species respond to those threats. Information is available on the status of less than 5% of the world's approximately 15 500 marine fish species, most of which are of commercial importance. By 2001, based on data from 98 North Atlantic and northeast Pacific populations, marine fishes had declined by a median 65% in breeding biomass from known historic levels; 28 populations had declined by more than 80%. Most of these declines would be sufficient to warrant a status of threatened with extinction under international threat criteria. However, this interpretation is highly controversial, in part because of a perception that marine fishes have a suite of life history characteristics, including high fecundity and large geographical ranges, which might confer greater resilience than that shown by terrestrial vertebrates. We review 15 comparative analyses that have tested for these and other life history correlates of vulnerability in marine fishes. The empirical evidence suggests that large body size and late maturity are the best predictors of vulnerability to fishing, regardless of whether differences among taxa in fishing mortality are controlled; there is no evidence that high fecundity confers increased resilience. The evidence reviewed here is of direct relevance to the diverse criteria used at global and national levels by various bodies to assess threat status of fishes. Simple life history traits can be incorporated directly into quantitative assessment criteria, or used to modify the conclusions of quantitative assessments, or used as preliminary screening criteria for assessment of the similar to 95% of marine fish species whose status has yet to be evaluated either by conservationists or fisheries scientists.
65.Reynolds, JD; Webb, TJ; Hawkins, LA. (2005) Life history and ecological correlates of extinction risk in European freshwater fishes.Canadian Journal of Fisheries and Aquatic Sciences 62: 854-862 Life history and ecological correlates of extinction risk in European freshwater fishes
We used phylogenetically based comparative analyses to test for associations between extinction risk in European freshwater fishes and a variety of life history, ecological, and biogeographical traits. Based on the World Conservation Union classification scheme, a total of 47% of Europe's 287 native species are classified as threatened with extinction. Threatened species are significantly smaller than less-threatened species in the same genera when analyses are restricted to fully freshwater species. This trend is reversed when anadromous genera are included. These comprise many large-bodied species in which fishing has often played a greater role in declines than in other taxa. Threatened species did not differ significantly in their habitats, although they tended to occupy a narrower variety of habitats biased toward streams and rivers. Threatened species occupy much narrower latitudinal ranges than close relatives that are less threatened, and they also have more southerly distributions where pressures on habitats are intense. This study suggests that links between life histories and threat status of freshwater fishes are not as clearcut as for marine species. For fish restricted entirely to freshwater, small-bodied species are most at risk owing to their naturally small ranges, which may put them in a more precarious position when their habitats are impacted by humans.
64. Dulvy, NK; Ellis, JR; Goodwin, NB; Grant, A; Reynolds, JD; Jennings, S. (2004) Methods of assessing extinction risk in marine fishes.Fish and Fisheries 5: 255-276 Methods of assessing extinction risk in marine fishes
CITES; fish; IUCN; Red List; life history; refence points; threat
The decline and disappearance of species from large parts of their former geographical ran-e has become an important issue in fisheries ecology. There is a need to identify which species are at risk of extinction. The available approaches have been subject to considerable debate - particularly when applied to commercially exploited species. Here we have compiled methods that have been used or may be used for assessing threat status of marine organisms. We organize the methods according to the availability of data on the natural history, ecology and population biology of species. There are three general approaches to inferring or assessing extinction risk: (i) correlative approaches based on knowledge of life histories and ecology: (ii) time-series approaches that examine changes in abundance: and (iii) demographic approaches based on age- or stage-based schedules of vital rates and fisheries reference points. Many methods are well suited to species that are highly catchable and/or have relatively low productivity, but theory is less well developed for assessing extinction risk in species exhibiting narrow geographical distributions or ecological specialization. There is considerable variation in both definitions of extinction risk and the precision and defensibility of the available risk assessment methods, so we suggest a two-tiered approach for defining and assessing extinction risk. First. simple methods requiring a few easily estimated parameters are used to triage or rapidly assess large numbers of populations and species to identify potentially vulnerable populations or species. Second. the populations and species identified as vulnerable by this process can then be subject to more detailed and rigorous population analysis explicitly considering sources of error and uncertainty.
63. Hunter, E; Metcalfe, JD; Arnold, GP; Reynolds, JD. (2004) Impacts of migratory behaviour on population structure in North Sea plaice.Journal of Animal Ecology 73: 377-385 Impacts of migratory behaviour on population structure in North Sea plaice
bird migration; data storage tags; fisheries; fish behaviour; flatfish; spatial dynamics; thermal stratification
1. Migration is widespread among marine fishes, yet little is known about variation in the migration of individuals within localities, and the consequences for spatial population structure. We tested the hypothesis that variation in the migratory behaviour among plaice (Pleuronectes platessa L.) in the North Sea could be explained by large-scale differences in the speed and directions of the tidal streams, which the fish use as a transport mechanism. 2. We released 752 mature female plaice tagged with electronic data storage tags at eight locations with contrasting tidal flow properties between December 1993 and September 1999. 3. The experiment yielded 20 403 days of data from 145 plaice. Individual tags recorded depth and temperature for up to 512 days. The position of each fish was determined at intervals throughout the liberty period using the tidal location method. 4. The results show that the fish were segregated into three discrete feeding aggregations during the summer non-breeding season. Two clusters were in warm, thermally mixed water in the eastern and western North Sea, respectively, and one was in deeper, cold, thermally stratified water to the north. 5. In the winter spawning period, fish from all three aggregations mixed together in the southern North Sea, and fish from the eastern and northern subunits spawned in the south-eastern North Sea. The only fish that left the North Sea were western subunit plaice that visited spawning grounds in the eastern English Channel. 6. Our results re-affirmed the major role of the tidal streams in the southern North Sea in structuring plaice dispersion, both by providing transport and guidance and by delimiting the extent of distribution due to thermal stratification during the summer. However, plaice from the northern North Sea did not use tidal stream transport. 7. These results confirm the prediction that large-scale variation in migration behaviour can be explained in part by the tidal guidance and transport mechanisms available. They have also revealed features of spatial dynamics not observed previously from a century of conventional tagging experiments and illustrate how the study of individual fish can successfully define the migratory characteristics of populations.
62. Hunter, E; Metcalfe, JD; O'Brien, CM; Arnold, GP; Reynolds, JD. (2004) Vertical activity patterns of free-swimming adult plaice in the southern North Sea.Marine Ecology-Progress Series 279: 261-273 Vertical activity patterns of free-swimming adult plaice in the southern North Sea
plaice; migration; data storage tags; vertical activity; stock assessment; accessibility; fisheries
Analysis of continuous behaviour records of adult female plaice Pleuronectes platessa tagged with electronic data storage tags, and released in the southern North Sea, has yielded new insights into spatial and temporal variation in vertical activity (swimming). Here we describe migration-linked changes in vertical activity patterns observed from 31 plaice released between December 1993 and February 1997. Fish migrations of up to 220 d were reconstructed using the tidal location method. Analysis of the periodicity of activity revealed high levels of vertical activity during the southward spawning migration into Southern Bight and the eastern English Channel following release in December and January. We observed spatially varying, migration-linked changes in vertical activity, with a tidal pattern of vertical activity during the pre- and post-spawning migrations and a circadian period of rhythmicity in the spawning grounds. Circadian periodicity was dominant in 23 of 31 individuals (74%), 13 of which also demonstrated significant 12 h periodicity. The other 8 fish exhibited a dominant 25 h periodicity. A significant 336 h (14 d) rhythm was observed in the averaged population data, in phase with the spring-neap cycle, with periods of reduced activity associated with times of expected high tides. Our results provide important information about systematic changes in migration-linked behaviour in plaice, and also illustrate how the accessibility of plaice to capture by trawling may vary in space and in time.
61. Hutchings, JA; Reynolds, JD. (2004) Marine fish population collapses: Consequences for recovery and extinction risk.Bioscience 54: 297-309 Marine fish population collapses: Consequences for recovery and extinction risk
conservation biology; biodiversity; Atlantic cod; endangered species; population ecology
Rapid declines threaten the persistence of many marine fish. Data from more than 230 populations reveal a median reduction of 83% in breeding population size from known historic levels. Few populations recover rapidly; most exhibit little or no change in abundance up to 15 years after a collapse. Reductions in fishing pressure, although clearly necessary for population recovery, are often insufficient. Persistence and recovery are also influenced by life history, habitat alteration, changes to species assemblages, genetic responses to exploitation, and reductions in population growth attributable to the Allee effect, also known as depensation. Heightened extinction risks were highlighted recently when a Canadian population of Atlantic cod (Gadus morhua) was listed as endangered, on the basis of declines as high as 99.9% over 30 years. Unprecedented reductions in abundance and surprisingly low rates of recovery draw attention to scientists' limited understanding of how fish behavior, habitat, ecology, and evolution affect population growth at low abundance. Failure to prevent population collapses, and to take the conservation biology of marine fishes seriously, will ensure that many severely depleted species remain ecological and numerical shadows in the ecosystems that they once dominated.
60. Mills, SC; Reynolds, JD. (2004) The importance of species interactions in conservation: the endangered European bitterling Rhodeus sericeus and its freshwater mussel hosts.Animal Conservation 7: 257-263 The importance of species interactions in conservation: the endangered European bitterling Rhodeus sericeus and its freshwater mussel hosts
Species conservation may be complicated in symbiotic interactions. Sub-lethal impacts of human activities on one species may be lethal to other species on which they depend. We investigated the impact of two aspects of eutrophication - changes in phytoplankton and oxygen levels - on the interaction between a freshwater fish that is endangered in several countries, the European bitterling, Rhodeus sericeus, and the unionid mussel hosts that they require for spawning. Reduced concentrations of algae and oxygen each led to a greater proportion of bitterling embryos being ejected prematurely from the mussel hosts. Reduced algal concentrations also led to reductions in mussel ventilation rates and to mussels spending less time with their valves open. Bitterling mortality may have been due to three causes: direct effects of environmental conditions on embryonic survival, active expulsion by mussels when stressed and through responses by mussels that created internal conditions that bitterling embryos could not survive. Our study shows that the sub-lethal effects of pollution on one species can have lethal effects on another species with which it interacts. Such interactions need to be considered in conservation programmes.
59. Szekely, T; Freckleton, RP; Reynolds, JD. (2004) Sexual selection explains Rensch's rule of size dimorphism in shorebirds.Proceedings of the National Academy of Sciences of the United States of America 101: 12224-12227 Sexual selection explains Rensch's rule of size dimorphism in shorebirds
Sexual size dimorphism shows a remarkably widespread relationship to body size in the animal kingdom: within lineages, it decreases with size when females are the larger sex, but it increases with size when males are the larger sex. Here we demonstrate that this pattern, termed Rensch's rule, exists in shorebirds and allies (Charadriides), and it is determined by two components of sexual selection: the intensity of sexual selection acting on males and the agility of the males'display. These effects are interactive so that the effect of sexual selection on size dimorphism depends on male agility. As a control, we also examine dimorphism in bill length, which is a functionally selected trait. As such, dimorphism in bill length neither exhibits Rensch's rule nor is associated with sexual selection and display. Our results show that variation among taxa in the direction and magnitude of sexual size dimorphism, as manifested as Rensch's rule, can be explained by the interaction between the form and strength of sexual selection acting on each sex in relation to body size.
58. Debuse, VJ; Addison, JT; Reynolds, JD. (2003) Effects of breeding site density on competition and sexual selection in the European lobster.Behavioral Ecology 14: 396-402 Effects of breeding site density on competition and sexual selection in the European lobster
Crustacea; mate choice; mating system; reproduction; resource defense
The availability of breeding sites has been predicted to affect the intensity of sexual selection, including mate competition, mate choice and ultimately, variation in mating success. We tested the hypothesis that reduced density of shelters would cause an increase in the intensity of sexual selection in European lobsters, Homarus gammarus. However, we found little support for our predictions. For example, within-sex competition by males and by females was not more intense when shelters were scarce. Indeed, females attempted to evict one another from shelters significantly more often when shelters were common. When shelters were abundant, shelter-holding males had greater mating success than males without shelters, yet females did not show more interest towards these males during courtship encounters. Mate attraction was more strongly related to large male body size when shelters were scarce. Overall, the results suggest that reduced shelter density does not lead to more overt within-sex aggression in this species. Instead, we suggest that impacts of breeding resource availability on sexual selection may depend on the range over which resources are measured, with extreme scarcity of shelters rendering overt competition uneconomical. Furthermore, females may become more selective of male traits such as large size, which enhance male control of breeding sites and hence protection of females.
57. Dulvy, NK; Sadovy, Y; Reynolds, JD. (2003) Extinction vulnerability in marine populations.Fish and Fisheries 4: 25-64 Extinction vulnerability in marine populations
biodiversity; conservation; detection; fisheries; recovery; Red List; risk
Human impacts on the world's oceans have been substantial, leading to concerns about the extinction of marine taxa. We have compiled 133 local, regional and global extinctions of marine populations. There is typically a 53-year lag between the last sighting of an organism and the reported date of the extinction at whatever scale this has occurred. Most disappearances (80%) were detected using indirect historical comparative methods, which suggests that marine extinctions may have been underestimated because of low-detection power. Exploitation caused most marine losses at various scales (55%), followed closely by habitat loss (37%), while the remainder were linked to invasive species, climate change, pollution and disease. Several perceptions concerning the vulnerability of marine organisms appear to be too general and insufficiently conservative. Marine species cannot be considered less vulnerable on the basis of biological attributes such as high fecundity or large-scale dispersal characteristics. For commercially exploited species, it is often argued that economic extinction of exploited populations will occur before biological extinction, but this is not the case for non-target species caught in multispecies fisheries or species with high commercial value, especially if this value increases as species become rare. The perceived high potential for recovery, high variability and low extinction vulnerability of fish populations have been invoked to avoid listing commercial species of fishes under international threat criteria. However, we need to learn more about recovery, which may be hampered by negative population growth at small population sizes (Allee effect or depensation) or ecosystem shifts, as well as about spatial dynamics and connectivity of subpopulations before we can truly understand the nature of responses to severe depletions. The evidence suggests that fish populations do not fluctuate more than those of mammals, birds and butterflies, and that fishes may exhibit vulnerability similar to mammals, birds and butterflies. There is an urgent need for improved methods of detecting marine extinctions at various spatial scales, and for predicting the vulnerability of species.
56. Einum, S; Fleming, IA; Côté, IM; Reynolds, JD. (2003) Population stability in salmon species: effects of population size and female reproductive allocation.Journal of Animal Ecology 72: 811-821 Population stability in salmon species: effects of population size and female reproductive allocation
density fluctuations; egg size; fecundity; phylogenetic comparisons; population dynamics
1. Population stability (i.e. level of temporal variation in population abundance) is linked commonly to levels of environmental disturbances. However, populations may also differ in their propensity to dampen or amplify the effects of exogenous forces. Here time-series of population estimates were used to test for such differences among 104 populations of six salmon species. 2. At the species level, Atlantic (Salmo salar L.), chinook (Oncorhynchus tshawytscha Walbaum) and coho salmon (O. kisutch W) were less variable than sockeye (O. nerka W) and pink salmon (O. gorbuscha W). Chum salmon (O. keta W) was more similar to sockeye and pink salmon. These differences may be related in part to differences in body size, and hence susceptibility to adverse environmental conditions, at the time when they migrate to the sea or lakes. 3. At the population level no effect of fecundity on variability was found, in contrast to findings for marine fishes, nor of egg size. Whereas substantial differences in the temporal stability of environmental factors among geographically close populations may override any effects of fecundity or egg size in fresh water, this is less likely in the marine environment where spatial autocorrelations of environmental variability are more pronounced. 4. Variation in population sizes was related positively to the duration of time-series when using standard deviations of In-transformed population estimates, and also when using linearly detrended population variation, suggesting non-linear long-term abundance trends in salmon populations that extend beyond the 7-year period of the shortest time-series. 5. When controlling for differences among species, stability increased with increasing population size, and it is hypothesized that this is due to large populations having a more complex spatial and genetic structure than small populations due to wider spatial distribution. The effects of population size on stability, as well as differences in stability among species, suggest that population- and organism-specific characteristics may interact with exogenous forces to shape salmon population dynamics.
55. Hunter, E; Metcalfe, JD; Reynolds, JD. (2003) Migration route and spawning area fidelity by North Sea plaice.Proceedings of the Royal Society of London Series B-Biological Sciences 270: 2097-2103 Migration route and spawning area fidelity by North Sea plaice
Pleuronectes platessa; electronic data storage tag; behaviour; homing; philopatry; metapopulation
Data from plaice, Pleuronectes platessa L., tagged with electronic data storage tags, were used to test whether these fishes exhibited migration route and spawning area fidelity in successive spawning seasons. Depth and temperature data were recorded for each fish over 365-512 days in the central North Sea and this information was used to reconstruct movements based on tidal locations. We discovered highly directed seasonal migrations from the winter spawning area south of a major topographical feature, Dogger Bank Tail End, to summer feeding grounds 250 km to the north in deep, cold, thermally stratified water. Our results show synchronous timing of migration, repeated pre- and post-spawning migration routes and 100% spawning area fidelity, including two individuals that returned to within 20 km of their previous season's spawning location. This is the first study to provide a complete reconstruction of annual migrations by individual fishes, showing strong homing behaviour along consistent migration routes.
54. Lindenfors, P; Szekely, T; Reynolds, JD. (2003) Directional changes in sexual size dimorphism in shorebirds, gulls and alcids.Journal of Evolutionary Biology 16: 930-938 Directional changes in sexual size dimorphism in shorebirds, gulls and alcids
Charadrii; sexual selection; size dimorphism; waders
The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.
53. Mills, SC; Reynolds, JD. (2003) The bitterling-mussel interaction as a test case for co-evolution.Journal of Fish Biology 63: 84-104 The bitterling-mussel interaction as a test case for co-evolution
acheilognathinae; Anodonta; cuckoo; parasitism; symbiosis; Unio
The European bitterling Rhodeus sericeus (Cyprinidae) spawns in the gills of freshwater mussels (Unionidae) and shows some obvious adaptations to this type of spawning, such as the development of an ovipositor. Furthermore, recent studies have shown that the fish avoid species of mussels that have a high likelihood of ejecting their eggs prematurely. This leads to the question of whether the interaction between bitterling and mussels could represent a case of co-evolution, involving evolutionary responses by both species to selection imposed by the other. The evidence for and against co-evolution is reviewed, incorporating new results front two sets of experiments designed to test for adaptive choices by bitterling according to the mussels' sex and reproductive state, as well as a preliminary study of potential benefits for mussels from exposure to bitterling. Host preferences by bitterling, both among and within Mussel species, may indeed have evolved in response to differences in benefits for offspring survival. There is no evidence yet for any benefits to mussels from receiving eggs, whereas there are costs due to reduced ventilation rates when the gills contain bitterling eggs. While there are differences among mussel species and individuals in their tendency to reject bitterling embryos, these differences do not provide strong evidence for co-evolution. For example, they may reflect differences in host physiology such as ventilation rate and generalized response, to expelling objects from their gills. Therefore, while bitterling are well adapted for their obligate spawning relationship with mussels, it has been much more difficult to find evidence for adaptations by mussels for dealing with bitterling. This suggests that any co-evolutionary dynamics between bitterling and mussels may be asymmetric, with stronger responses to selection by the fish than by mussels. (C) 2003 The Fisheries Society of the British Isles.
52. Mills, SC; Reynolds, JD. (2003) Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus.Behavioral Ecology and Sociobiology 54: 98-104 Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus
sexual selection; density dependence; alternative reproductive behaviour; cyprinidae
We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.
51.Reynolds, JD; Bruford, MW; Gittleman, JL; Wayne, RK. (2003) The first five years.Animal Conservation 6: 1-2 The first five years
49. Candolin, U; Reynolds, JD. (2002) Adjustments of ejaculation rates in response to risk of sperm competition in a fish, the bitterling (Rhodeus sericeus).Proceedings of the Royal Society of London Series B-Biological Sciences 269: 1549-1553 Adjustments of ejaculation rates in response to risk of sperm competition in a fish, the bitterling (Rhodeus sericeus)
alternative reproductive behaviours; mate guarding; sexual selection; trade-offs; Cyprinidae; Unionidae
Game theory models of sperm competition predict that within species, males should increase their sperm expenditure when they have one competitor, but decrease expenditure with increasing numbers of competitors. So far, there have been few tests or support for this prediction. Here, we show that males of a freshwater fish, the European bitterling, Rhodeus sericeus, do indeed adjust their ejaculation rate to the number of male competitors by first increasing and then decreasing their ejaculation rates as the number of competitors increases. However, this occurred only under restricted conditions. Specifically, the prediction was upheld as long as no female had deposited eggs in the live mussels that are used as spawning sites. After one or more females had spawned, males did not decrease their ejaculation rates with the number of competitors, but instead they became more aggressive, This indicates that decreased ejaculation rate and increased aggression are alternative responses to increased risk of sperm competition.
48. Candolin, U; Reynolds, JD. (2002) Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus.Behavioral Ecology and Sociobiology 51: 146-152 Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus
alternative mating behavior; sperm competition; mate choice; reproductive trade-offs; sexual selection
In most species, males attack other males that attempt to gain fertilizations through sneak copulations. Here we report on a system where dominant males show a low level of aggression against sneakers at the initial stages of territory establishment. Females of the Europe,in bitterling, Rhodeus sericeus, lay their eggs in living mussels and males fertilize the eggs by releasing sperm over the mussels both before and after egg laying. When we allowed males to court females to a mussel containing no eggs at different male densities - one, two, four, or six males - the dominant male showed a low level of aggression against other males that released sperm. The dominant male became aggressive toward the other males only after eggs had been laid. This unusual pattern could be due to either some benefit of accepting sneakers or a high cost of aggression. We found support for both possibilities. The presence of several males decreased the time until a female spawned, whereas increased aggression by the dominant male against other males during a second female presentation, when the male was more territorial, interrupted courtship and increased the time until spawning. Females appeared to be attracted by both the presence of several males around a mussel and increased courtship under male competition. The bitterling mating system possibly differs from that of other species due to lack of investment in nest building and parental care, and high costs of defending the spawning site against sneakers.
46. Denney, NH; Jennings, S; Reynolds, JD. (2002) Life-history correlates of maximum population growth rates in marine fishes.Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2229-2237 Life-history correlates of maximum population growth rates in marine fishes
conservation; comparative study; Ricker; stock-recruitment; population growth rate; fisheries
Theory predicts that populations of animals with late maturity, low fecundity, large body size and low body growth rates will have low potential rates of population increase at low abundance. If this is true, then these traits may be used to predict the intrinsic rate of increase for species or populations, as well as extinction risks. We used life-history and population data for 63 stocks of commercially exploited fish species from the northeast Atlantic to test relationships between life-history parameters and the rate of population increase at low abundance. We used cross-taxonomic analyses among stocks and among species, and analyses that accounted for phylogenetic relationships. These analyses confirmed that large-bodied, slow-growing stocks and species had significantly lower rates of recruitment and adult production per spawning adult at low abundance. Furthermore, high ages at maturity were significantly correlated with low maximum recruit production. Contrary to expectation, fecundity was significantly negatively related to recruit production, due to its positive relationship with maximum body size. Our results support theoretical predictions, and suggest that a simply measured life-history parameter can provide a useful tool for predicting rates of recovery from low population abundance.
45. Dulvy, NK; Reynolds, JD. (2002) Predicting extinction vulnerability in skates.Conservation Biology 16: 440-450 Predicting extinction vulnerability in skates
Relatively few marine fishes have been assessed tender World Conservation Union criteria, yet it is believed that marine fish extinction rates have been underestimated by one order of magnitude McKinney 1999). Given the paucity of data required for traditional assessment methods, we explored the use of potential correlates of extinction vulnerability to prioritize species for conservation assessment. We focused oil the world's 230 species of skates and rays (Rajidae) because they have been identified (is one of the most vulnerable groups of marine fishes, We searched for all documented cases of local extinction tend compiled it database of body size and latitudinal and depth ranges for all species for which data were available. We found that species that have disappeared from substantial parts of Their ranges ("locally extinct") have large body sizes compared with all other skates, bill that latitudinal and depth ranges were similar to those of other species. The body size correlate may be due to higher mortality rates and correlations with life-history parameters such as late age at maturity. We used the locally extinct species that held the smallest size or ranges as benchmarks to generate lists of other species that may be vulnerable. Body size generated the smallest species list (7), excluding the known local extinctions, compared with lists generated b), size of latitudinal (150) or depth range (63). Body size was the only trait that correctly identified the known local extinctions, suggesting that it is more useful them range sizes for identifying potentially vulnerable fishes, This provides a simple, objective method of prioritizing species for further assessment, which complements direct methods that are more data-intensive and time-consuming.
44. Goodwin, NB; Dulvy, NK; Reynolds, JD. (2002) Life-history correlates of the evolution of live bearing in fishes.Philosophical Transactions of the Royal Society B-Biological Sciences 357: 259-267 Life-history correlates of the evolution of live bearing in fishes
comparative method; reproduction; viviparity; phylogeny; shark; coelacanth
Selection for live bearing is thought to occur when the benefits of increasing offspring survival exceed the costs of reduced fecundity, mobility and the increased metabolic demands of carrying offspring throughout development. We present evidence that live bearing has evolved from egg laying 12 times in teleost (bony) fishes, bringing the total number of transitions to 21 to 22 times in all fishes, including elasmobranchs (sharks and rays). Live bearers produce larger offspring than egg layers in all of 13 independent comparisons for which data were available. However, contrary to our expectation there has not been a consistent reduction in fecundity; live bearers have fewer offspring in seven out of the 11 available comparisons. It was predicted that live bearers would have a larger body size, as this facilitates accommodation of developing offspring. This prediction was upheld in 14 out of 20 comparisons. However, this trend was driven by elasmobranchs, with large live bearers in seven out of eight comparisons. Thus, while the evolution of live bearing in elasmobranchs is correlated with predicted increases in offspring size and adult size, teleost live bearers do not have such a consistent suite of life-history correlates. This suggests that constraints or selection pressures on associated life histories may differ in live-bearing elasmobranchs and teleost fishes. DOI
43. Mills, SC; Reynolds, JD. (2002) Host species preferences by bitterling, Rhodeus sericeus, spawning in freshwater mussels and consequences for offspring survival.Animal Behaviour 63: 1029-1036 Host species preferences by bitterling, Rhodeus sericeus, spawning in freshwater mussels and consequences for offspring survival
Two hypotheses have been advanced to explain the evolution of host responses to parasites: the arms race-evolutionary lag and equilibrium hypotheses. We investigated predictions from these hypotheses based on interspecies host preferences and adaptations in an obligate spawning relationship between a freshwater fish, the European bitterling (Cyprinidae) and four species of freshwater mussels (Unionidae), which the fish use as hosts for their eggs. We found a significant trend in preference by the fish for mussels in the following order: Unio pictorum, U. tumidus, Anodonta anatina and A. cygnea. Male and female bitterling both showed this ranking and the clutch sizes deposited into each species also followed this trend. These host preferences proved to be adaptive in terms of egg ejection, which was lowest in the most preferred species (U. pictorum). Furthermore, these hierarchical host preferences were flexible, as females switched species when individuals of the preferred species ejected a greater number of eggs. The similarity in mussel defences between the U.K. population and. a European population of ancient sympatry suggests that the absence of a defence in some mussel species may not be due to evolutionary lag. Mussel ejection behaviour may have reached an evolutionary equilibrium in each host species, or alternatively the fish may have evolved adaptive preferences that coincide with generalized mussel responses to foreign objects in their gills. (C) 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.
42. Mills, SC; Reynolds, JD. (2002) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus.Oecologia 131: 473-478 Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus
Anodonta; coevolution; host-parasite interaction; Unio; Unionidae
A range of cues may be used by parasites in selecting hosts, yet few studies have examined multiple cues simultaneously. We investigated the proximate cues involved in spawning decisions of the European bitterling, Rhodeus sericeus, a species of fish which lays its eggs in four species of freshwater mussel. When offered a choice of both live and artificial mussels within a single species, females preferred mussels that have high flow speeds and that pump a large volume of water per unit time. Furthermore, the time taken to spawn for a second time in a mussel was accurately predicted from a mussel's ventilation rate. These bitterling preferences based on mussel ventilation rates may benefit the embryos through enhanced oxygenation. We found no preferences for mussel species based on visual or olfactory cues, though the latter cannot be ruled out entirely. Ventilation rates should indicate the quality of host species for offspring survival.
39.Reynolds, JD; Goodwin, NB; Freckleton, RP. (2002) Evolutionary transitions in parental care and live bearing in vertebrates.Philosophical Transactions of the Royal Society B-Biological Sciences 357: 269-281 Evolutionary transitions in parental care and live bearing in vertebrates
comparative study; Charadriiformes; amphibian; reptile; mammal; invertebrate
We provide the first review of phylogenetic transitions in parental care and live bearing for a wide variety of vertebrates. This includes new analyses of both numbers of transitions and transition probabilities. These reveal numerous transitions by shorebirds and anurans toward uniparental care by either sex. Whereas most or all of the shorebird transitions were from biparental care, nearly all of the anuran transitions have been from no care, reflecting the prevalence of each form of care in basal lineages in each group. Teleost (bony) fishes are similar to anurans in displaying numerous transitions toward uniparental contributions by each sex. Whereas cichlid fishes have often evolved from biparental care to female care, other teleosts have usually switched from no care to male care. Taxa that have evolved exclusive male care without courtship-role reversal are characterized by male territoriality and low costs of care per brood. Males may therefore benefit from care through female preference of parental ability in these species. Primates show a high frequency of transitions from female care to biparental care, reflecting the prevalence of female care in basal lineages. In the numerous taxa that display live bearing by females, including teleosts, elasmobranchs, squamate reptiles and invertebrates, we find that live bearing has always evolved from a lack of care. Although the transition counts and probabilities will undoubtedly be refined as phylogenetic information and methodologies improve, the overall biases in these taxa should help to place adaptive hypotheses for the evolution of care into a stronger setting for understanding directions of change.
38. Whiteman, EA; Côté, IM; Reynolds, JD. (2002) Do cleaning stations affect the distribution of territorial reef fishes?Coral Reefs 21: 245-251 Do cleaning stations affect the distribution of territorial reef fishes?
damselfish; habitat selection; cleaning symbioses; territoriality; cleaning gobies
We investigated the role of cleaning stations in determining the distribution of territorial reef species. Cleaner fish reduce their clients' ectoparasite loads and, therefore, proximity to cleaning stations should be advantageous for territorial fish. We focused on five damselfish species which hold permanent territories and cleaning stations occupied by cleaning gobies (Elacatinus spp.) on a Caribbean reef. Contrary to our predictions of higher densities near cleaning stations, we found that bicolor damselfish were less abundant near cleaning stations than at ecologically similar points without cleaning gobies whereas no effects were seen for longfin, dusky, yellowtail, and threespot damselfish. In addition, although damselfish densities were higher in the immediate vicinity of cleaning stations than 1.5-3 in away for most species, this was also the case at points without cleaners. Because cleaning stations are usually located on prominent coral heads or sponges, the overall significant attraction of damselfish to such structures, whether occupied by cleaning gobies or not, could reflect attraction to past or potential cleaning stations. However, it is more likely that interspecific competition and/or the low benefits of being cleaned at our study site prevent aggregation around cleaners. Cleaning stations may play only a minor rote in determining the distribution of territorial reef fishes.
37. Candolin, U; Reynolds, JD. (2001) Sexual signaling in the European bitterling: females learn the truth by direct inspection of the resource.Behavioral Ecology 12: 407-411 Sexual signaling in the European bitterling: females learn the truth by direct inspection of the resource
bitterlings; mate choice; multiple ornaments; reliable signaling; resource quality; Rhodeus sericeus; sexual selection
In many taxa females appear to base their mate choice on multiple traits. But the relative importance of different traits in mate choice has rarely been determined. Here we show that females of a freshwater fish. the European bitterling, Rhodeus sericeus, base their mate choice on multiple traits that differ in their reliability as indicators of expected reproductive success and are used at different stages of the decision process, The initial decision to inspect a male is based on male behavior and red coloration, whereas the final spawning decision is based on the quality of the live unionid mussel, Anodonta anatina, that the male is defending as an oviposition site. Male traits may indicate which males are worth inspecting by reflecting male quality, such as reproductive condition and genetic constitution. Male traits do not, however, reflect mussel quality as bright males also court females vigorously toward mussels that yield a low probability of survival of the offspring. Females, on the other hand. are choosier than males in their choice of spawning site and seem to gain reliable information about the survival probability of the eggs by inspecting the mussel directly.
36. Côté, IM; Mosqueira, I; Reynolds, JD. (2001) Effects of marine reserve characteristics on the protection of fish populations: a meta-analysis.Journal of Fish Biology 59: 178-189 Effects of marine reserve characteristics on the protection of fish populations: a meta-analysis
fisheries; marine conservation; marine protected area; reefs; tropics
Meta-analyses of published data for 19 marine reserves reveal that marine protected areas enhance species richness consistently, but their effect on fish abundance is more variable. Overall, there was a slight (11%) but significant increase in fish species number inside marine reserves, with all reserves sharing a common effect. There was a substantial but non-significant increase in overall fish abundance inside marine reserves compared to adjacent, non-reserve areas. When only species that are the target of fisheries were considered, fish abundance was significantly higher (by 28%) within reserve boundaries. Marine reserves vary significantly in the extent and direction of their response. This variability in relative abundance was not attributable to differences in survey methodology among studies, nor correlated with reserve characteristics such as reserve area, years since protection, latitude nor species diversity. The effectiveness of marine reserves in enhancing fish abundance may be largely related to the intensity of exploitation outside reserve boundaries and to the composition of the fish community within boundaries. It is recommended that studies of marine reserve effectiveness, should routinely report fishing intensity, effectiveness of enforcement and habitat characteristics. (C) 2001 The Fisheries Society of the British Isles.
35. Debuse, VJ; Addison, JT; Reynolds, JD. (2001) Morphometric variability in UK populations of the European lobster.Journal of the Marine Biological Association of the United Kingdom 81: 469-474 Morphometric variability in UK populations of the European lobster
European lobsters (Homarus gammarus) were sampled from nine sites around the UK coast to determine whether populations Could be differentiated oil the basis of morphometric variability, and to relate this to depth and indices of population size at each site. Discriminant analysis indicated that exoskeleton damage was the only characteristic that could distinguished males between sites. In contrast, females were distinguished between sites on the basis of variation in exoskeleton damage, claw spines and rostrum teeth, which tended to be positively correlated to indices of population density. This study suggests that female morphology may respond more strongly than male morphology to local selection pressures, albeit ill a limited capacity.
33. Liker, A; Reynolds, JD; Szekely, T. (2001) The evolution of egg size in socially polyandrous shorebirds.Oikos 95: 3-14 The evolution of egg size in socially polyandrous shorebirds
In classical and multi-clutch polyandry, females lay multiple clutches during a breeding season for more than one mate. The production of multiple clutches may be energetically demanding. We used comparative analyses to investigate three possible ways of reducing such egg-laying costs in polyandrous shorebirds: (1) reduction in egg size, (2) reduction in clutch size, and (3) evolutionary increase in female size. Paired comparisons of polyandrous and non-polyandrous taxa showed that females of polyandrous shorebirds lay smaller eggs than females of closely related monogamous and polygynous species. Directional analyses corroborated this result by indicating a significant decrease in egg size after phylogenetically independent origins of polyandry. The comparative analyses uniformly rejected the two alternatives, i.e. neither clutch size nor female size is related to social mating pattern. We also tested and rejected three alternative explanations for reduced egg size in polyandrous taxa, First, we found no evidence that polyandrous females have evolved smaller egg sizes in response to selection to match smaller size of males, which provide the parental care in these species. Second, reduction in egg size was not related to longer breeding seasons (and hence more opportunity for re-nesting). Third, reduced egg sizes were also not related to rates of clutch predation (another potential correlate of multiple clutch production). Our results are thus consistent with the hypothesis that selection for reducing laying costs explains small egg size in socially polyandrous shorebirds.
31. Dulvy, NK; Metcalfe, JD; Glanville, J; Pawson, MG; Reynolds, JD. (2000) Fishery stability, local extinctions, and shifts in community structure in skates.Conservation Biology 14: 283-293 Fishery stability, local extinctions, and shifts in community structure in skates
Skates are arguably the most vulnerable of exploited marine fishes. Their vulnerability is often assessed by examining fisheries catch trends, but these data are not generally recorded on a species basis except in France. Aggregated skate catch statistics tend to exhibit more stable trends than those of other elasmobranch fisheries. We tested whether such apparent stability in aggregated catch trends could mask population declines of individual species. We examined two time series of species-specific surveys of a relatively stable skate fishery in the norhteast Atlantic. These surveys revealed the disappearance of two skate species, long-nose skate (Dipturus oxyrhinchus) and white skate (Rostroraja alba) and confirmed a previously documented decline of the common skate (D. batis). Of the remaining five skate species, the three larger ones have declined, whereas two smaller species have increased in abundance. The increase in abundance and biomass of the smaller species has resulted in the stability of the aggregated catch trends. Because there is significant dietary overlap among species, we suggest the increase in abundance of the smaller species may be due to competitive release as the larger species declined. A consequence of this kind of stability is that declining species cannot be detected without species-specific data, especially in taxa exhibiting competitive interactions. This may explain why previously documented disappearances of two species of skates went unnoticed for so long. The conservation of skates and other elasmobranchs requires species-specific monitoring and special attention to larger species.
30. Mosqueira, I; Côté, IM; Jennings, S; Reynolds, JD. (2000) Conservation benefits of marine reserves for fish populations.Animal Conservation 3: 321-332 Conservation benefits of marine reserves for fish populations
We synthesize the results of empirical studies of marine reserves to assess the potential benefits of protection for fish populations. Our meta-analyses demonstrate that the overall abundance of fishes inside reserves is, on average, 3.7 times higher than outside reserve boundaries. This enhancement is mainly a result of a significant increase in abundance of species that are the target of fisheries. Non-target species are equally abundant inside and outside reserves. Large-bodied species also respond more to protection, irrespective of their fishery status. Species within genera show great heterogeneity in their response to protection despite similarities in their life histories. Our study confirms that marine reserves benefit fish populations and highlights the need for monitoring prior to reserve establishment to provide more accurate, habitat-controlled studies of the effects of marine reserves on fish populations.
29. Perdices, A; Doadrio, I; Côté, IM; Machordom, A; Economidis, P; Reynolds, JD. (2000) Genetic divergence and origin of Mediterranean populations of the River Blenny Salaria fluviatilis (Teleostei : Blenniidae).Copeia : 723-731 Genetic divergence and origin of Mediterranean populations of the River Blenny Salaria fluviatilis (Teleostei : Blenniidae)
The current distribution of the River Blenny Salaria (= Blennius) fluviatilis, one of the two freshwater representatives of a large, cosmopolitan marine fish family, poses an interesting biogeographical problem because this species inhabits widely separate circum-Mediterranean watersheds. Potential scenarios of its dispersal were examined using allozyme analysis of several populations from the Iberian and Greek peninsulas. Based on Nei genetic distances, the most divergent populations were the populations inhabiting lakes, Lake Trichonis in Greece, and Ruidera Lakes in Spain. Their high divergence suggests their early isolation from the main ingroup populations. In contrast, low genetic distances were found among river populations regardless of geographic location. There was a correlation between genetic distance and geographic distance among Iberian river populations, suggesting that dispersal following the colonization of fresh water occurred via the sea to nearby, unconnected river basins. The ancestor of S. fluviatilis may have been a euryhaline species, allowing incursions into fresh water and subsequent dispersal via the sea. This dispersal scenario could theoretically be combined with multiple colonization episodes. The two old lake populations shared a unique allele at the Pgdh-A locus in high frequency with its closest relative S. pave, which was absent from other populations. This may indicate two initial incursions into fresh water by a wide-ranging marine ancestor that possessed this allele. Differential selection on this allele in lake habitats or convergence are less likely possibilities. Thus, the present distribution of S. fluviatilis appears to stem from a combination of "raceme" origins (i.e., more than one colonization episode) and subsequent dispersal and divergence in new watersheds.
28. Pope, JG; MacDonald, DS; Daan, N; Reynolds, JD; Jennings, S. (2000) Gauging the impact of fishing mortality on non-target species.ICES Journal of Marine Science 57: 689-696 Gauging the impact of fishing mortality on non-target species
conservation; ecosystem effects; fisheries; mortality; non-target species; stock assessment
The most obvious effect of fishing on non-target species is direct mortality. To quantify this effect on the vulnerability of species requires measurement of the current fishing mortality rate and of the tolerance of the species to fishing mortality. These are difficult to estimate for the little-studied non-target species. We describe two potential methods for estimating current fishing mortality rate when data are limited. Their application is illustrated for dab (Limanda limanda) and grey gurnard (Eutrigula gurnardus), two common non-target species in the North Sea. We also develop approaches to define tolerance levels for fishing mortality for little-studied and rare species, based on the phi potential jeopardy level: the fishing mortality that causes a phi reduction in spawning stock biomass per recruit relative to the unexploited situation. We propose that for non-target species, models founded on basic knowledge of life history parameters, and on generally established relationships between these parameters, may offer the only practical approach. (C) 2000 International Council for the Exploration of the Sea.
27. Rickman, SJ; Dulvy, NK; Jennings, S; Reynolds, JD. (2000) Recruitment variation related to fecundity in marine fishes.Canadian Journal of Fisheries and Aquatic Sciences 57: 116-124 Recruitment variation related to fecundity in marine fishes
An understanding of the processes that control recruitment variation is central to explaining the population dynamics of fishes and predicting their responses to exploitation. Theory predicts that interannual variation in recruitment should be positively correlated with the fecundity of fish species, but empirical studies have not supported this hypothesis. Here, we adopt a phylogenetic comparative approach, which accounts for evolutionary relatedness among stocks and species, to investigate this relationship. We calculated the mean fecundity of fishes from 52 stocks at the mean length of maturity and related this to interannual recruitment variation. We found that in 13 of 14 comparisons between stocks or closely related species, the stocks with higher fecundity have higher recruitment variation. This was true whether or not we controlled for spawning stock size. However, when the analyses were repeated using a traditional cross-species approach, which did not account for the evolutionary relatedness of stocks, the relationships were not significant. This is the first empirical study to link fecundity with recruitment variation and suggests that fecundity is an important component of fish stock dynamics.
26. Smith, C; Reynolds, JD; Sutherland, WJ. (2000) Population consequences of reproductive decisions.Proceedings of the Royal Society of London Series B-Biological Sciences 267: 1327-1334 Population consequences of reproductive decisions
individual behaviour; population dynamics; bitterling; Rhodeus sericeus
Behaviour can be a key component of animal population ecology yet the population consequences of behavioural decisions are poorly understood. We conducted a behavioural and demographic study of the bitterling Rhodeus sericeus, a freshwater fish that spawns in live unionid mussels. We used a population model incorporating game theory decisions and measurements of demographic parameters in order to provide predictions of population size among 13 populations of this fish. Our model predicted that the observed behavioural spawning decisions, while maximizing individual fitness, cause a significant 6% reduction in population size compared with randomly distributed spawnings. We discuss our findings in the context of the population consequences of adaptive behaviour.
25. Smith, C; Reynolds, JD; Sutherland, WJ; Jurajda, P. (2000) Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus).Behavioral Ecology and Sociobiology 48: 29-35 Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus)
oviposition; density dependence; freshwater mussel; ideal free distribution model
Choice of a site for oviposition can have fitness consequences. We investigated the consequences of female oviposition decisions for offspring survival using the bitterling, Rhodeus sericeus, a freshwater fish that spawns inside living unionid mussels. A field survey of nine bitterling populations in the Czech Republic revealed a significantly lower rate of release of juvenile bitterling from Anodonta cygnea compared to three other mussel species. A field experiment demonstrated that female bitterling show highly significant preferences for spawning in A. anatina, Unio pictorum, and U. tumidus. Within a species, female bitterling avoided mussels containing high numbers of bitterling embryos. Mortality rates of bitterling embryos in mussels were strongly density dependent and the strength of density dependence varied significantly among mussel species, Female preferences for mussels matched survival rates of embryos within mussels and females distributed their eggs among mussels such that embryo mortalities conformed to the predictions of an ideal free distribution model. Thus, female oviposition choice is adaptive and minimizes individual embryo mortality.
24. Szekely, T; Reynolds, JD; Figuerola, J. (2000) Sexual size dimorphism in shorebirds, gulls, and alcids: The influence of sexual and natural selection.Evolution 54: 1404-1413 Sexual size dimorphism in shorebirds, gulls, and alcids: The influence of sexual and natural selection
Charadrii; display behavior; niche division; sexual selection; size dimorphism; waders
Charadrii (shorebirds, gulls, and alcids) have an unusual diversity in their sexual size dimorphism, ranging from monomorphism to either male-biased or female-biased dimorphism. We use comparative analyses to investigate whether this variation relates to sexual selection through competition for mates or natural selection through different use of resources by males and females. As predicted by sexual selection theory, we found that in taxa with socially polygynous mating systems, males were relatively larger than females compared with less polygynous species. Furthermore, evolution toward socially polyandrous mating systems was correlated with decreases in relative male size. These patterns depend on the kinds of courtship displays performed by males. In taxa with acrobatic flight displays, males are relatively smaller than in taxa in which courtship involves simple flights or displays from the ground. This result remains significant when the relationship with mating system is controlled statistically, thereby explaining the enigma of why males are often smaller than females in socially monogamous species. We did not find evidence that evolutionary changes in sexual dimorphism relate to niche division on the breeding grounds. In particular, biparental species did nor have greater dimorphism in bill lengths than uniparental species, contrary to the hypothesis that selection for ecological divergence on the breeding grounds has been important as a general explanation for patterns of bill dimorphism. Taken together, these results strongly suggest that sexual selection has had a major influence on sexual size dimorphism in Charadrii, whereas divergence in the use of feeding resources while breeding was not supported by our analyses.
23. Côté, IM; Vinyoles, D; Reynolds, JD; Doadrio, I; Perdices, A. (1999) Potential impacts of gravel extraction on Spanish populations of river blennies Salaria fluviatilis (Pisces, Blenniidae).Biological Conservation 87: 359-367 Potential impacts of gravel extraction on Spanish populations of river blennies Salaria fluviatilis (Pisces, Blenniidae)
Lipophrys fluviatilis; Blennius fluviatilis; environmental disturbance; conservation; Mediterranean freshwater
River blennies Salaria fluviatilis have a wide circum-Mediterranea distribution, but they are mostly confined to small, very localised populations. In the Iberian Peninsula, they are endangered due to a variety of causes, including gravel extraction. This study identified the breeding requirements of river blennies at a site where gravel extraction takes place and at three other sites in different drainage basins in Spain. Breeding males chose nest stones that were significantly larger than other stones available in the immediate vicinity. Although clutch area was significantly related to stone size in two of three populations, male size was not. Stone size appeared to be the main correlate of clutch size, and stone sizes were significantly smaller at sites where gravel had been extracted. The potential effects of stone and gravel removal on nesting density and egg productivity were simulated, and it was found that a 75% reduction in stone size, as observed in this study, could result in a 47% decrease in nesting density. Because of the relationship between clutch size and nest stone size, egg production would be reduced even further, to 25% of its initial level. Removal of stones and gravel from the river bed also causes structural alterations which may render the habitat unsuitable for breeding blennies despite the presence of apparently suitable nest stones. Our results may be applicable to the conservation of other substrate-spawning fish. (C) 1998 Elsevier Science Ltd. All rights reserved.
22. Debuse, VJ; Addison, JT; Reynolds, JD. (1999) The effects of sex ratio on sexual competition in the European lobster.Animal Behaviour 58: 973-981 The effects of sex ratio on sexual competition in the European lobster
During the breeding season an individual's access to mates may be affected by operational sex ratios, causing strong variation in mating success. We manipulated adult sex ratios of the European lobster, Homarus gammarus, to test the predictions of models that relate sexual competition to (1) the sex ratio, (2) the time that an individual is not available to mate and (3) 'collateral investment', whereby two males contribute to a single clutch. The model predictions proved to be relatively insensitive to collateral investment Male-male competition predominated in the male-biased but not in the female-biased sex ratio. This matches the predictions of one model that incorporates an extended period of female receptivity because the time that a male was unavailable to mate was small compared to the time spent by females in cohabitation and parental care. Although females increased their competitiveness when males were in the minority, male competition remained high. The insensitivity of male-male competition to sex ratios may be due to an upper limit to the costs that males can afford when there is a serious risk of injury, preventing males from increasing their aggression when females are in short supply. (C) 1999 The Association for the Study of Animal Behaviour.
21. Jennings, S; Greenstreet, SPR; Reynolds, JD. (1999) Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories.Journal of Animal Ecology 68: 617-627 Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories
community structure; fisheries exploitation; life history; North Sea; phylogeny
1, An understanding of the links between life histories and responses to exploitation could provide the basis for predicting shifts in community structure by identifying susceptible species and linking life-history tactics with population dynamics. 2, We examined long-term trends in the abundance of species in the North Sea bottom-dwelling (demersal) fish community. Between 1925 and 1996 changes in species composition led to an increase in mean growth rate, while mean maximum size, age at maturity and size at maturity decreased. The demersal fish community was increasingly heavily fished during this period. 3, Trends in mean life-history characteristics of the community were linked to trends in abundance of component species. An approach based on phylogenetic comparisons was used to examine the differential effects of fishing on individual species with contrasting life histories. 4, Those species that decreased in abundance relative to their nearest relative, matured later at a greater size, grew more slowly towards a greater maximum size and had lower rates of potential population increase. The phylogenetically based analyses demonstrated that trends in community structure could be predicted from the differential responses of related species to fishing, 5, This is the first study to link exploitation responses of an entire community to the life histories of individual species, The results demonstrate that fishing has greater effects on slower growing, larger species with later maturity and lower rates of potential population increase. The comparative approach provides a basis for predicting structural change in other exploited communities.
20. Jennings, S; Reynolds, JD; Polunin, NVC. (1999) Predicting the vulnerability of tropical reef fishes to exploitation with phylogenies and life histories.Conservation Biology 13: 1466-1475 Predicting the vulnerability of tropical reef fishes to exploitation with phylogenies and life histories
Fishing has led to local extirpations of reef fishes. For conservation and management purpose, it is important to identify all those species that are vulnerable to fishing, but this cannot be done using a priori assessments or by describing trends in abundance because the necessary scientific resources are not available. Thus the predictions of vulnerability that provide the basis for conservation action will have to be made with existing data or data that can be acquired rapidly before further extirpations occur. The life histories of species may determine their responses to exploitation, and we describe how an easily measured parameter, maximum observed size, is related to population trends of exploited fishes on coral reefs. Using a phylogenetic comparative approach, we demonstrated that species of grouper (Epinephelinae), snapper (Lujanidae), and parrotfish (Scaridae) that decreased in abundance more than their nearest phylogenetic relative had greater maximum size. Our results suggest that one can predict the vulnerability of reef fishes to exploitation based on responses of their relatives. The quality of the prediction was good for the intensively fished groupers and snappers but poor for the lightly fished parrotfishes. Our approach may help proactive conservationists and fishery managers identify and conserve vulnerable species in new, developing, or lightly exploited fisheries, thereby reducing their reliance on reactive management methods.
19. Jones, JC; Reynolds, JD. (1999) Oxygen and the trade-off between egg ventilation and brood protection in the common goby.Behaviour 136: 819-832 Oxygen and the trade-off between egg ventilation and brood protection in the common goby
1. We examined compromises between defence of nests against predation and ventilation of eggs in the common goby (Pomatoschistus microps). Females are known to prefer nests with small entrances, which are less vulnerable to predatory shore crabs, Carcinus maenus. However, small nest entrances may hamper egg ventilation by males. This may be especially detrimental under conditions of low dissolved oxygen. 2. Males did not make smaller entrances to their nests when in the presence of predatory crabs, but they had larger entrances under low oxygen than in normal oxygen levels. 3. Males diverted time from ventilating nests to attacking crabs. 4. Thus, males exchanged direct care of the eggs for protection against predators by reducing their fanning activity, but not according to needs of their eggs for oxygenation. This trade-off may therefore impose a greater cost to egg survival for males in low oxygen.
18. Jones, JC; Reynolds, JD. (1999) Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen.Animal Behaviour 57: 181-188 Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen
This study examines the effects of harsh environmental conditions on life history trade-offs in parental care in a marine fish, the common goby, Pomatoschistus microps. We compared male parental care and hatching success over two sequential brood cycles in fish breeding in conditions of either low dissolved oxygen or normal levels of oxygen. Males compensated for a low oxygen environment by increasing the time they spent fanning water over their eggs, as well as their fanning tempo. They also increased the frequency of egg-directed activities and decreased nest-building activities. Males in the low oxygen treatment lost more weight than control fish during the first spawning, and were more likely to abandon care during the second spawning. Males that completed care under low oxygen conditions did not differ from control males in the hatching success of their offspring or the size of young at hatching, but hatching started on average 1 day later. Thus, greater parental allocations to offspring while breeding in a harsh environment led to reduced future allocations. (C) 1999 The Association for the Study of Animal Behaviour.
17. Jones, JC; Reynolds, JD. (1999) The influence of oxygen stress on female choice for male nest structure in the common goby.Animal Behaviour 57: 189-196 The influence of oxygen stress on female choice for male nest structure in the common goby
This study examines the role of dissolved oxygen in modifying female mate choice in the common goby, Pomatoschistus microps. Experimental manipulations of nests showed that under normal (saturated) oxygen conditions, females preferred to spawn in nests with the most elaborate construction, that is, those with the most sand on top and the smallest entrance. Such manipulated nests proved less vulnerable to detection by an egg predator, the shore crab, Carcinus maenas, but these small entrances may reduce oxygenation of eggs. indeed, in a low oxygen environment females with a choice between nests of high build and nests of low build did not significantly prefer either. This may have been due tb weakened preference or perhaps detection of a mismatch between the male's parental quality and the increased ventilation needs of eggs when nest entrance sizes are small and ambient oxygen levels are low. When nests were not manipulated, those males that built small entrances fanned their eggs more often, such that hatching success in the absence of a predator was not related to the initial size of the nest entrance area. Thus, under normal oxygen conditions males may initially build nests with the smallest entrance they are capable of ventilating successfully, and females choosing such males gain from nest camouflage. Under low oxygen, the risk that manipulated males may be unable to compensate fully may outweigh such benefits, and females may use other criteria that signal willingness to provide parental care. (C) 1999 The Association for the Study of Animal Behaviour.
16. Kokko, H; Mackenzie, A; Reynolds, JD; Lindstrom, J; Sutherland, WJ. (1999) Measures of inequality are not equal.American Naturalist 154: 358-382 Measures of inequality are not equal
variance in fitness; reproductive skew; resource acquisition; sampling error; statistical power; leks
Inequalities in reproductive success or resource acquisition are fundamental to evolution and population ecology. There is, however, no unique way to measure inequality. We review 21 measures used to quantify it and clarify the conceptual difference between inequality and skewness. In two very different families of distributions, all indices except three give higher values for more unequal distributions of resources, although some of them are poor at distinguishing between similar inequality values. When applied correctly by testing against a null hypothesis of no inequality among individuals, most indices can therefore be used to detect deviations from randomness, but with varying ease as most lack statistical tables and rely on resampling techniques instead. As an example to test the performance of the 21 indices, we used each index to analyze 71 data sets of unequal mating success in leks. In pairwise comparisons, 24% of the indices fail to show a positive intercorrelation. This reflects differences in how indices incorporate variation in the number of competitors and mean acquisition of the resource. All indices are sensitive to these aspects if inequality is measured in data arising from different distributions. These results illustrate the general conclusion that a unique "best" solution is not available; each measure presents its own definition of inequality. The choice of an inequality index requires specifying the null expectations and interpreting deviating values in relation to the biological question being addressed. This means, for example, considering individual male mating success in the context of lekking or relating the mass distribution of individual plants to alternative hypotheses about competition in plant population ecology. When sample sizes vary, testing robustness by using several measures is advisable.
15.Reynolds, JD; Jones, JC. (1999) Female preference for preferred males is reversed under low oxygen conditions in the common goby (Pomatoschistus microps).Behavioral Ecology 10: 149-154 Female preference for preferred males is reversed under low oxygen conditions in the common goby (Pomatoschistus microps)
common gobies; female choice; fish spawning; mate copying; oxygenation; Pomatoschistus microps
Female preference for males that already have eggs in their nest has been reported in many fish species. The presence of eggs may provide a cue for copying the choice of previous females and may indicate that high-quality care will be available. Consistent with a review of 13 studies, we found that female common gobies (Pomatoschistus microps) preferred to spawn with males that had already been chosen by females and whose nests therefore already contained eggs. However, this preference was reversed under conditions of low dissolved oxygen. We would not expect this reversal if the second female were using eggs as a signal of male genetic attractiveness to other females unless the benefits were outweighed by direct selection. The reversal also could not be explained by differences in active courtship by males, as courtship rates did not differ under low oxygen between males with or without eggs. Low oxygen conditions corresponded with a nearly threefold increase in male ventilation of eggs and a reduction in time spent near a selecting female. The reversal is therefore most likely due to females avoiding males that would be unable to meet the demands of care of a second clutch under low oxygen conditions. Thus, an abiotic feature of the environment reveals plasticity of female choice, consistent with hypothesized changes in benefits of mating with preferred males.
13. Rogers, SI; Clarke, KR; Reynolds, JD. (1999) The taxonomic distinctness of coastal bottom-dwelling fish communities of the North-east Atlantic.Journal of Animal Ecology 68: 769-782 The taxonomic distinctness of coastal bottom-dwelling fish communities of the North-east Atlantic
taxonomic diversity; groundfish; community structure; fishing impact; NW Europe
41. New techniques for identifying the average taxonomic range of species assemblages were applied to an extensive dataset of bottom-dwelling fish in the coastal waters of NW Europe. These taxonomic distinctness indices provided much greater resolution than traditional diversity indices as they incorporated information on taxonomic relationships into an index which measures species dominance. Unlike standard measures of species richness and diversity, the mean value of these statistics is independent of sampling effort, and this allows objective comparisons to be made between samples from studies where sampling effort is not standardized. 2. A reduction in the average taxonomic range between the fauna of western waters of the UK and that of the southern North Sea was consistent with the general decline in species richness observed between these regions, and suggests that these two factors may be spatially positively correlated. Indices calculated for individual samples of fish on a local scale, however, did not all fit this trend. 3. Much of the variability in taxonomic diversity within the coastal waters of NW Europe was caused by the variable geographical distribution of the elasmobranchs. Of all the families which comprise the fish communities, this group has life-history characteristics which make it most susceptible to impact by commercial trawl fisheries. 4. The use of taxonomic distinctness measures provided additional insights, of relevance to biodiversity assessment, suggesting that they might usefully be applied to other aquatic and terrestrial fauna.
12. Côté, IM; Arnal, C; Reynolds, JD. (1998) Variation in posing behaviour among fish species visiting cleaning stations.Journal of Fish Biology 53: 256-266 Variation in posing behaviour among fish species visiting cleaning stations
cleaning symbiosis; Gobiosoma; coral reefs
The adaptive significance of posing behaviour by fish visiting cleaning stations on a Barbadian fringing reef was investigated. The probability of a visitor being cleaned by cleaning gobies (Elacatinus spp.) was significantly higher after posing than after failing to pose upon arrival at a cleaning station. Despite this, not all visitors posed, and there was much variation among species in tendency to pose. This interspecific variation was not related to the probability of being cleaned, either after posing or after failing to pose, nor was it related to trophic level or fish total length. The latter was true both for cross-species analyses and phylogenetically independent contrasts. A cost-benefit model is proposed to understand interspecific variation in posing behaviour, which considers both decisions by clients and by cleaners. As well as explaining the results, this may reconcile differences among anecdotal and experimental observations from previous studies. (C) 1998 The Fisheries Society of the British Isles.
10. Goodwin, NB; Balshine-Earn, S; Reynolds, JD. (1998) Evolutionary transitions in parental care in cichlid fish.Proceedings of the Royal Society of London Series B-Biological Sciences 265: 2265-2272 Evolutionary transitions in parental care in cichlid fish
Cichlidae; evolution; phylogeny; reproduction; sexual selection; teleost
Cichlid fishes (Cichlidae) are well suited for testing theories of the evolution of vertebrate parental care. These freshwater teleost fish provide parental care for their offspring, display many different forms of care and have interspecific variation in which sex slays with the young. Here, we assemble the first family-wide composite phylogeny based on morphological and molecular studies, and trace two sets of character evolution: form of care (substrate guarding and mouthbrooding), and sex of care-giver (biparental, female-only, and male-only). Mouthbrooding has evolved from ancestral substrate guarding with 10-14 transitions and 0-3 reversals. The data support hypothesized transitions in the sex of caregiver, with uniparental female care having arisen from biparental care 21-30 times with 0-10 reversals. There is also evidence that male-only care evolved once from biparental care. These transitions in parental care characters are the most numerous reported for any family of vertebrates and, to our knowledge, provide the first quantitative support for models of parental care evolution in fish.
9. Jennings, S; Reynolds, JD; Mills, SC. (1998) Life history correlates of responses to fisheries exploitation.Proceedings of the Royal Society of London Series B-Biological Sciences 265: 333-339 Life history correlates of responses to fisheries exploitation
conservation; exploitation; fishes; fisheries; life history; phylogeny
We use an approach based on phylogenetic comparisons to identify life history correlates of abundance trends in 18 intensively exploited fish stocks from the north-east Atlantic. After accounting for differences in fishing mortality, we show that those fishes that have decreased in abundance compared with their nearest relatives mature later, attain a larger maximum size, and exhibit significantly lower potential rates of population increase. Such trends were not evident in a more traditional cross-species analysis. This is the first phylogenetically independent evidence to link life histories with abundance trends, and provides a quantitative basis for assessing vulnerability of fish populations to exploitation. Our approach can be applied to the conservation and management of other exploited taxa.
8. Kokko, H; Sutherland, WJ; Lindstrom, J; Reynolds, JD; Mackenzie, A. (1998) Individual mating success, lek stability, and the neglected limitations of statistical power.Animal Behaviour 56: 755-762 Individual mating success, lek stability, and the neglected limitations of statistical power
The evolution of leks (aggregations of males displaying to females) cannot be explained solely by an increasing average gain in matings for each male as group size increases. This is because the mating skew, that is, the inequality among males in mating success, is often high and may vary with lek size. Here, we show that the common observation that matings become more evenly divided as lek size increases is also insufficient to explain by itself the benefits of aggregating. The benefits to individual males are highly sensitive to the exact relationship between mating skew and lek size, and very similar relationships can lead to opposite predictions concerning individual benefits. With data on published mating success for 18 species (71 leks), we show that different species have very similar skew versus lek size relationships. With current sample sizes, however,there is insufficient statistical power to distinguish between completely different alternatives concerning individual optima of males. (C) 1998 The Association for the Study of Animal Behaviour.
7.Reynolds, JD; Guillaume, HP. (1998) Effects of phosphate on the reproductive symbiosis between bitterling and freshwater mussels: implications for conservation.Journal of Applied Ecology 35: 575-581 Effects of phosphate on the reproductive symbiosis between bitterling and freshwater mussels: implications for conservation
Anodonta anatina; fish; phosphorus; pollution; Rhodeus sericeus
1. We examined the effects of phosphorus. an important pollutant in fresh waters, on mussels Anodonta anatina and embryos of European bitterling Rhodeus sericeus amarus. These species are involved in an unusual symbiosis, with the fish depositing eggs inside the mussels' gills, where the embryos develop for 3-6 weeks until the larvae leave the mussel, 2. High concentrations of phosphate (500 mu g L-1 and higher) caused a significant increase in the rate of premature expulsion and emergence of bitterling embryos from the mussels, with a concomitant increase in fish mortality. 3. At concentrations of 750 mu g L-1 and higher, mussels reduced their frequency of ventilation and movements through the substratum. 4. These results have implications for understanding the nature of the symbiosis between the fish and their mussel hosts, showing that mussels have control over bitterling developing in their gills. The premature expulsion of bitterling embryos at high phosphate levels is detrimental to the fish that they harbour. 5. Recommendations for the conservation of bitterling and species of mussels, which are threatened or endangered over parts of their ranges, include reductions in levels of phosphorus in natural habitats and the need for low levels in reintroduction sites for the fish and their mussel hosts.
6. Dulvy, NK; Reynolds, JD. (1997) Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays.Proceedings of the Royal Society of London Series B-Biological Sciences 264: 1309-1315 Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays
Sharks and rays are thought to have a large number of independent origins of live-bearing. We examined evolutionary transitions to live-bearing and maternal input to embryos in this subclass by optimizing reproductive characters onto a composite phylogeny. Egg-laying (40% of all species) is the likely ancestral reproductive mode for this clade, and there is evidence that live-bearing has evolved independently 9-10 times and maternal input 4-5 times. Most transitions (12-15) have been toward live-bearing with provisioning limited to yolk. These have occurred from egg-laying ancestors or live-bearing taxa that provide maternal input to embryos. Only 2-3 transitions have occurred in the other direction, i.e. away from yolk-only live-bearing. Egg-laying has evolved from live-bearing ancestors in skates, Rajidae (25% of all species) and possibly in the zebra shark, Stegostoma fasciata. Thus, although there has been an overall trend toward the evolution of live-bearing in elasmobranchs, the evolution of additional maternal input has been extremely labile.
5. Jones, JC; Reynolds, JD. (1997) Effects of pollution on reproductive behaviour of fishes.Reviews in Fish Biology and Fisheries 7: 463-491 Effects of pollution on reproductive behaviour of fishes
This review attempts to integrate pollution research with behavioural ecology by focusing on reproductive behaviour of fishes. A search of Aquatic Sciences and Fisheries Abstracts and other sources showed that only 0.1% of 19,199 studies of aquatic pollution and fishes during the past 20 years have made this link. Effects on parental care and courtship have been investigated using a variety of pollutants (e.g. acidification, herbicide, thermal effluent) in several fish families (e.g. Cichlidae, Poeciliidae, Gasterosteidae, Cyprinidae). Eleven of the 19 studies found a change in behaviour from the norm. Effects on courtship included decreases or increases in frequency of displays, increased courtship duration, or performance of male-like behaviour by masculinized females. Studies of parental care have found decreased nest-building activity, decreased offspring defence, or changes in division of parental care between the sexes. Few studies have measured reproductive success or extrapolated their results to effects on populations. We develop a framework for exploring links between pollution and behavioural ecology which suggests potential impacts on life history trade-offs in reproduction, genetic changes in populations, and population sizes. Many reproductive behaviours of fish species are readily quantifiable and behaviours such as courtship by male guppies and other members of the Poeciliidae show some promise for pollution monitoring and behavioural toxicity tests. Choice of such assays would have to compete with the sensitivity and practicality of more traditional methods but may serve as useful complements. There is considerable scope for further research into conservation. A synthesis between behavioural ecology and toxicology should thus provide useful insights for both fields.
4.Reynolds, JD; Debuse, VJ; Aldridge, DC. (1997) Host specialisation in an unusual symbiosis: European bitterlings spawning in freshwater mussels.Oikos 78: 539-545 Host specialisation in an unusual symbiosis: European bitterlings spawning in freshwater mussels
This study investigated host specialisation in an unusual symbiosis between a species of fish, the European bitterling (Rhodeus sericeus: family Cyprinidae, subfamily Acheilognathinae), and four species of freshwater mussels (family Unionidae) which bitterlings use for spawning. A field study from a single site in England examined four aspects of host use. First, comparisons among mussel species showed significant differences in production of bitterling young: Unio pictorum released the most young fish, followed in order by Anodonta anatina, Unio tumidus, and Anodonta cygnea. These findings pertained to mussels which had received eggs naturally, and were repeated in an experiment in the wild which controlled for mussel density and prior occupancy by bitterling embryos. Second, there were no significant differences within species in host productivity according to mussel size for individuals >60 mm in length. Third, field manipulations indicated microhabitat differences in host use which depended on the mussel species: U. pictorum individuals were used most heavily when closest to the river bank, whereas the opposite trend occurred for U. tumidus and A. anatina. Finally, the total productivity of mussels which had been clustered in groups of three was three times higher than single individuals. This latter effect suggests a benefit to males from choosing to defend groups of mussels. Benefits from specialisation among mussel species are not clear, but host use may reflect the broader context of overlaps between the fish and mussels in habitats. The ranges of all four mussel species overlap widely with those of bitterlings, but the least-used mussel species, A. cygnea, has the least habitat overlap with bitterlings, suggesting the potential for weaker selection on the fish for host recognition or adaptation to this species.
3.Reynolds, JD; Szekely, T. (1997) The evolution of parental care in shorebirds: Life histories, ecology, and sexual selection.Behavioral Ecology 8: 126-134 The evolution of parental care in shorebirds: Life histories, ecology, and sexual selection
aves; body size; Charadrii; desertion; life history; migration; parental care; sexual selection; shorebirds
Parental care is expected to evolve according to a tradeoff between the benefits of increased survival of offspring and costs of reduced survival and future reproduction of adults. Here we investigate the components of this life-history trade-off in shorebirds (Charadriides, excluding Laroidea), an avian infraorder displaying all unusual diversity in extent of care by each sex. We show that evolutionary increases in the duration of care in one sex are associated with decreased care by the other. We found no evidence that various hypothesised benefits of care provide a general explanation for the duration of care by either or both sexes, although parental feeding of the voting was too conservative for comparisons. Sexual dimorphism in body size had a similar relationship re:, parental care in both sexes: reductions in duration of care by either sex were matched by increases in the size of that sex relative to the other. Whereas this pattern could he explained by sexual selection in males, it was retained within socially monogamous females. Reduced care in males (but not in females) appears to have facilitated the evolution of greater migration distances. These results suggest that parental care has had different causes and consequences in each sex. Benefits of desertion due to sexual selection are more clearly demonstrable for males, whereas correlates of care are less clear for females.
2. Johnstone, RA; Reynolds, JD; Deutsch, JC. (1996) Mutual mate choice and sex differences in choosiness.Evolution 50: 1382-1391 Mutual mate choice and sex differences in choosiness
mate choice; parental care; parental investment; sex role reversal; sexual selection
Sexual competition is associated closely with parental care because the sex providing less care has a higher potential rate of reproduction, and hence more to gain from competing for multiple mates. Sex differences in choosiness are not easily explained, however. The lower-caring sex (often males) has both higher costs of choice, because it is more difficult to find replacement mates, and higher direct benefits, because the sex providing more care (usually females) is likely to exhibit more variation in the quality of contributions to the young. Because both the costs and direct benefits of mate choice increase with increasing parental care by the opposite sex, general predictions about sex difference in choosiness are difficult. Furthermore, the level of choosiness of one sex will be influenced by the choosiness of the other. Here, we present an ESS model of mutual mate choice, which explicitly incorporates differences between males and females in life history traits that determine the costs and benefits of choice, and we illustrate our results with data from species with contrasting forms of parental care. The model demonstrates that sex differences in costs of choice are likely to have a much stronger effect on choosiness than are differences in quality variation, so that the less competitive sex will commonly be more choosy. However, when levels of male and female care are similar, differences in quality variation may lead to higher levels of both choice and competition in the same sex.
1.Reynolds, JD. (1996) Animal breeding systems.Trends in Ecology & Evolution 11: A68-A72 Animal breeding systems
The study of breeding systems explores relationships between mating behaviour and parental care. Recent findings have shown that in many birds, fishes, anurans, and insects, females play a more active role than previously thought, by engaging in mate choice, mating with more than one male, and selecting genetic partners separately from social partners, Theoretical advances have improved our understanding of the effect of parental care on sex differences in mating behaviour, though less attention has been devoted to feedback in the opposite direction, The original emphasis on the role of ecology in determining breeding systems has been overshadowed by studies of individual interactions, but modern comparative techniques may provide a new fusion between ecology, life histories, and reproductive behaviour.