Chris Harrod

Implications of climate change for the fishes of the British Isles

Recent climatic change has been recorded across the globe. Although environmental change is a characteristic feature of life on Earth and has played a major role in the evolution and global distribution of biodiversity, predicted future rates of climatic change, especially in temperature, are such that they will exceed any that has occurred over recent geological time. Climate change is considered as a key threat to biodiversity and to the structure and function of ecosystems that may already be subject to significant anthropogenic stress. The current understanding of climate change and its likely consequences for the fishes of Britain and Ireland and the surrounding seas are reviewed through a series of case studies detailing the likely response of several marine, diadromous and freshwater fishes to climate change. Changes in climate, and in particular, temperature have and will continue to affect fish at all levels of biological organization: cellular, individual, population, species, community and ecosystem, influencing physiological and ecological processes in a number of direct, indirect and complex ways. The response of fishes and of other aquatic taxa will vary according to their tolerances and life stage and are complex and difficult to predict. Fishes may respond directly to climate-change-related shifts in environmental processes or indirectly to other influences, such as community-level interactions with other taxa. However, the ability to adapt to the predicted changes in climate will vary between species and between habitats and there will be winners and losers. In marine habitats, recent changes in fish community structure will continue as fishes shift their distributions relative to their temperature preferences. This may lead to the loss of some economically important cold-adapted species such as Gadus morhua and Clupea harengus from some areas around Britain and Ireland, and the establishment of some new, warm-adapted species. Increased temperatures are likely to favour cool-adapted (e.g. Perca fluviatilis) and warm-adapted freshwater fishes (e.g. roach Rutilus rutilus and other cyprinids) whose distribution and reproductive success may currently be constrained by temperature rather than by cold-adapted species (e.g. salmonids). Species that occur in Britain and Ireland that are at the edge of their distribution will be most affected, both negatively and positively. Populations of conservation importance (e.g.Salvelinus alpinus and Coregonus spp.) may decline irreversibly. However, changes in food-web dynamics and physiological adaptation, for example because of climate change, may obscure or alter predicted responses. The residual inertia in climate systems is such that even a complete cessation in emissions would still leave fishes exposed to continued climate change for at least half a century. Hence, regardless of the success or failure of programmes aimed at curbing climate change, major changes in fish communities can be expected over the next 50 years with a concomitant need to adapt management strategies accordingly.

Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes

Ecological speciation has been the subject of intense research in evolutionary biology but the genetic basis of the actual mechanism driving reproductive isolation has rarely been identified. The extreme polymorphism of the major histocompatibility complex (MHC), probably maintained by parasite-mediated selection, has been proposed as a potential driver of population divergence. We performed an integrative field and experimental study using three-spined stickleback river and lake ecotypes. We characterized their parasite load and variation at MHC class II loci. Fish from lakes and rivers harbor contrasting parasite communities and populations possess different MHC allele pools that could be the result of a combined action of genetic drift and parasite-mediated selection. We show that individual MHC class II diversity varies among populations and is lower in river ecotypes. Our results suggest the action of homogenizing selection within habitat type and diverging selection between habitat types. Finally, reproductive isolation was suggested by experimental evidence: in a flow channel design females preferred assortatively the odor of their sympatric male. This demonstrates the role of olfactory cues in maintaining reproductive isolation between diverging fish ecotypes.

Phenotype‐environment correlations in a putative whitefish adaptive radiation

1. The adaptive radiation of fishes into benthic (littoral) and pelagic (lentic) morphs in post-glacial lakes has become an important model system for speciation. Although these systems are well studied, there is little evidence of the existence of morphs that have diverged to utilize resources in the remaining principal lake habitat, the profundal zone. 2. Here, we tested phenotype-environment correlations of three whitefish (Coregonus lavaretus) morphs that have radiated into littoral, pelagic and profundal niches in northern Scandinavian lakes. We hypothesized that morphs in such trimorphic systems would have a morphology adapted to one of the principal lake habitats (littoral, pelagic or profundal niches). Most whitefish populations in the study area are formed by a single (monomorphic) whitefish morph, and we further hypothesized that these populations should display intermediate morphotypes and niche utilization. We used a combination of traditional (stomach content, habitat use, gill raker counts) and more recently developed (stable isotopes, geometric morphometrics) techniques to evaluate phenotype-environment correlations in two lakes with trimorphic and two lakes with monomorphic whitefish. 3. Distinct phenotype-environment correlations were evident for each principal niche in whitefish morphs inhabiting trimorphic lakes. Monomorphic whitefish exploited multiple habitats, had intermediate morphology, displayed increased variance in gillraker-counts, and relied significantly on zooplankton, most likely due to relaxed resource competition. 4. We suggest that the ecological processes acting in the trimorphic lakes are similar to each other, and are driving the adaptive evolution of whitefish morphs, possibly leading to the formation of new species.

Ecological impacts of an invasive predator explained and predicted by comparative functional responses

Forecasting the ecological impacts of invasive species is a major challenge that has seen little progress, yet the development of robust predictive approaches is essential as new invasion threats continue to emerge. A common feature of ecologically damaging invaders is their ability to rapidly exploit and deplete resources. We thus hypothesized that the ‘functional response’ (the relationship between resource density and consumption rate) of such invasive species might be of consistently greater magnitude than those of taxonomically and/or trophically similar native species. Here, we derived functional responses of the predatory Ponto-Caspian freshwater ‘bloody red’ shrimp, Hemimysis anomala, a recent and ecologically damaging invader in Europe and N. America, in comparison to the local native analogues Mysis salemaai and Mysis diluviana in Ireland and Canada, respectively. This was conducted in a novel set of experiments involving multiple prey species in each geographic location and a prey species that occurs in both regions. The predatory functional responses of the invader were generally higher than those of the comparator native species and this difference was consistent across invaded regions. Moreover, those prey species characterized by the strongest and potentially de-stabilizing Type II functional responses in our laboratory experiments were the same prey species found to be most impacted by H. anomala in the field. The impact potential of H. anomala was further indicated when it exhibited similar or higher attack rates, consistently lower prey handling times and higher maximum feeding rates compared to those of the two Mysis species, formerly known as ‘Mysis relicta’, which itself has an extensive history of foodweb disruption in lakes to which it has been introduced. Comparative functional responses thus merit further exploration as a methodology for predicting severe community-level impacts of current and future invasive species and could be entered into risk assessment protocols.

Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes

Freshwater populations of three-spined sticklebacks (Gasterosteus aculeatus) in northern Germany are found as distinct lake and river ecotypes. Adaptation to habitat-specific parasites might influence immune capabilities of stickleback ecotypes. Here, naive laboratory-bred sticklebacks from lake and river populations were exposed reciprocally to parasite environments in a lake and a river habitat. Sticklebacks exposed to lake conditions were infected with higher numbers of parasite species when compared with the river. River sticklebacks in the lake had higher parasite loads than lake sticklebacks in the same habitat. Respiratory burst, granulocyte counts and lymphocyte proliferation of head kidney leucocytes were increased in river sticklebacks exposed to lake when compared with river conditions. Although river sticklebacks exposed to lake conditions showed elevated activation of their immune system, parasites could not be diminished as effectively as by lake sticklebacks in their native habitat. River sticklebacks seem to have reduced their immune-competence potential due to lower parasite diversity in rivers.

Tracing early stages of species differentiation: Ecological, morphological and genetic divergence of Galápagos sea lion populations

BackgroundOceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation.ResultsWe find significant ecological, morphological and genetic divergence between the western colonies and colonies from the central region of the archipelago that are exposed to different ecological conditions. Stable isotope analyses indicate that western animals use different food sources than those from the central area. This is likely due to niche partitioning with the second Galápagos eared seal species, the Galápagos fur seal (Arctocephalus galapagoensis) that exclusively dwells in the west. Stable isotope patterns correlate with significant differences in foraging-related skull morphology. Analyses of mitochondrial sequences as well as microsatellites reveal signs of initial genetic differentiation.ConclusionOur results suggest a key role of intra- as well as inter-specific niche segregation in the evolution of genetic structure among populations of a highly mobile species under conditions of free movement. Given the monophyletic arrival of the sea lions on the archipelago, our study challenges the view that geographical barriers are strictly needed for the build-up of genetic divergence. The study further raises the interesting prospect that in social, colonially breeding mammals additional forces, such as social structure or feeding traditions, might bear on the genetic partitioning of populations.

Parallel and nonparallel ecological, morphological and genetic divergence in lake-stream stickleback from a single catchment

Parallel phenotypic evolution in similar environments has been well studied in evolutionary biology; however, comparatively little is known about the influence of determinism and historical contingency on the nature, extent and generality of this divergence. Taking advantage of a novel system containing multiple lake–stream stickleback populations, we examined the extent of ecological, morphological and genetic divergence between three‐spined stickleback present in parapatric environments. Consistent with other lake–stream studies, we found a shift towards a deeper body and shorter gill rakers in stream fish. Morphological shifts were concurrent with changes in diet, indicated by both stable isotope and stomach contents analysis. Performing a multivariate test for shared and unique components of evolutionary response to the distance gradient from the lake, we found a strong signature of parallel adaptation. Nonparallel divergence was also present, attributable mainly to differences between river locations. We additionally found evidence of genetic substructuring across five lake–stream transitions, indicating that some level of reproductive isolation occurs between populations in these habitats. Strong correlations between pairwise measures of morphological, ecological and genetic distance between lake and stream populations supports the hypothesis that divergent natural selection between habitats drives adaptive divergence and reproductive isolation. Lake–stream stickleback divergence in Lough Neagh provides evidence for the deterministic role of selection and supports the hypothesis that parallel selection in similar environments may initiate parallel speciation.

Human effects on ecological connectivity in aquatic ecosystems: Integrating scientific approaches to support management and mitigation

Understanding the drivers and implications of anthropogenic disturbance of ecological connectivity is a key concern for the conservation of biodiversity and ecosystem processes. Here, we review human activities that affect the movements and dispersal of aquatic organisms, including damming of rivers, river regulation, habitat loss and alteration, human-assisted dispersal of organisms and climate change. Using a series of case studies, we show that the insight needed to understand the nature and implications of connectivity, and to underpin conservation and management, is best achieved via data synthesis from multiple analytical approaches. We identify four key knowledge requirements for progressing our understanding of the effects of anthropogenic impacts on ecological connectivity: autecology; population structure; movement characteristics; and environmental tolerance/phenotypic plasticity. Structuring empirical research around these four broad data requirements, and using this information to parameterise appropriate models and develop management approaches, will allow for mitigation of the effects of anthropogenic disturbance on ecological connectivity in aquatic ecosystems.

Isotopic variation complicates analysis of trophic relations within the fish community of Plußsee:a small, deep, stratifying lake

Analysis of carbon and nitrogen stable isotopes has allowed freshwater ecologists to examine lake food webs in increasing detail. Many such studies have highlighted the existence of separate within-lake pelagic and benthic-littoral food webs but are typically conducted on large (> 10 km2) lakes, whereas the majority of lakes are actually relatively small. We used stable isotope analysis (δ13C & δ15N) to examine trophic interactions between fish and their prey in Plussee, as an example of a small, stratifying lake, and to determine whether separate pelagic/benthic-littoral food webs could be distinguished in such systems. Our results indicate that the Plussee food web was complicated, and due to extensive intra-annual isotopic variation in zooplankton (e.g.cladoceran δ13C annual range = 25.6‰), it may be impossible to definitively assign consumers from small, eutrophic stratified lakes to pelagic or benthic-littoral food webs. We present evidence that some components of the Plussee food web (large bream) may be subsidised by carbon of methanogenic origin.

Accounting for the effects of lipids in stable isotope (δ13C and δ15N values) analysis of skin and blubber of balaenopterid whales

RATIONALE Stable isotope values (δ(13)C and δ(15)N) of darted skin and blubber biopsies can shed light on habitat use and diet of cetaceans, which are otherwise difficult to study. Non-dietary factors affect isotopic variability, chiefly the depletion of (13)C due to the presence of (12)C-rich lipids. The efficacy of post hoc lipid-correction models (normalization) must be tested. METHODS For tissues with high natural lipid content (e.g., whale skin and blubber), chemical lipid extraction or normalization is necessary. C:N ratios, δ(13)C values and δ(15)N values were determined for duplicate control and lipid-extracted skin and blubber of fin (Balaenoptera physalus), humpback (Megaptera novaeangliae) and minke whales (B. acutorostrata) by continuous-flow elemental analysis isotope ratio mass spectrometry (CF-EA-IRMS). Six different normalization models were tested to correct δ(13)C values for the presence of lipids. RESULTS Following lipid extraction, significant increases in δ(13)C values were observed for both tissues in the three species. Significant increases were also found for δ(15)N values in minke whale skin and fin whale blubber. In fin whale skin, the δ(15)N values decreased, with no change observed in humpback whale skin. Non-linear models generally out-performed linear models and the suitability of models varied by species and tissue, indicating the need for high model specificity, even among these closely related taxa. CONCLUSIONS Given the poor predictive power of the models to estimate lipid-free δ(13)C values, and the unpredictable changes in δ(15)N values due to lipid-extraction, we recommend against arithmetical normalization in accounting for lipid effects on δ(13)C values for balaenopterid skin or blubber samples. Rather, we recommend that duplicate analysis of lipid-extracted (δ(13)C values) and non-treated tissues (δ(15)N values) be used.