Winter in water: differential responses and the maintenance of biodiversity.

The ecological consequences of winter in freshwater systems are an understudied but rapidly emerging research area. Here, we argue that winter periods of reduced temperature and light (and potentially oxygen and resources) could play an underappreciated role in mediating the coexistence of species. This may be especially true for temperate and subarctic lakes, where seasonal changes in the thermal environment might fundamentally structure species interactions. With climate change already shortening ice-covered periods on temperate and polar lakes, consideration of how winter conditions shape biotic interactions is urgently needed. Using freshwater fishes in northern temperate lakes as a case study, we demonstrate how physiological trait differences (e.g. thermal preference, light sensitivity) drive differential behavioural responses to winter among competing species. Specifically, some species have a higher capacity for winter activity than others. Existing and new theory is presented to argue that such differential responses to winter can promote species coexistence. Importantly, if winter is a driver of niche differences that weaken competition between, relative to within species, then shrinking winter periods could threaten coexistence by tipping the scales in favour of certain sets of species over others.

Consumer trophic positions respond variably to seasonally fluctuating environments.

The effects of environmental seasonality on food web structure have been notoriously understudied in empirical ecology. Here, we focus on seasonal changes in one key attribute of a food web, consumer trophic position. We ask whether fishes inhabiting tropical river-floodplain ecosystems behave as seasonal omnivores, by shifting their trophic positions in relation to the annual flood pulse, or whether they feed at the same trophic position all year, as much empirical work implicitly assumes. Using dietary data from the Tonle Sap Lake, Cambodia, and a literature review, we find evidence that some fishes, especially small piscivores, increased consumption of invertebrates and/or plant material during the wet season, as predicted. However, nitrogen stable isotope (δ15 N) data for 26 Tonle Sap fishes, spanning a broader range of functional groups, uncovered high variation in seasonal trophic position responses among species (0 to ±0.52 trophic positions). Based on these findings, species respond to the flood pulse differently. Diverse behavioral responses to seasonality, underpinned by spatiotemporal variation at multiple scales, could be central for rerouting matter and energy flow in these dynamic ecosystems. Seasonally flexible foraging behaviors warrant further study given their potential influence on food web dynamics in a range of fluctuating environments.

Rescaling the trophic structure of marine food webs.

Measures of trophic position (TP) are critical for understanding food web interactions and human-mediated ecosystem disturbance. Nitrogen stable isotopes (δ(15) N) provide a powerful tool to estimate TP but are limited by a pragmatic assumption that isotope discrimination is constant (change in δ(15) N between predator and prey, Δ(15) N = 3.4‰), resulting in an additive framework that omits known Δ(15) N variation. Through meta-analysis, we determine narrowing discrimination from an empirical linear relationship between experimental Δ(15) N and δ(15) N values of prey consumed. The resulting scaled Δ(15) N framework estimated reliable TPs of zooplanktivores to tertiary piscivores congruent with known feeding relationships that radically alters the conventional structure of marine food webs. Apex predator TP estimates were markedly higher than currently assumed by whole-ecosystem models, indicating perceived food webs have been truncated and species-interactions over simplified. The scaled Δ(15) N framework will greatly improve the accuracy of trophic estimates widely used in ecosystem-based management.

Consistent seasonal flexibility of the gut and its regions across wild populations of a winter-quiescent fish.

Seasonality in north-temperate environments imposes drastic temperature and resource variations that shape the seasonal ecophysiology of resident organisms. A better understanding of an organism's capacity to flexibly respond to this drastic seasonal variation may reveal important mechanisms for tolerating or responding to environmental variation introduced by global change. In fishes, the digestive system is both the interface between resource and energy acquisition and one of the most expensive organ systems to maintain. However, little evidence describing the capacity for seasonal flexibility in the digestive tract of wild northern fishes exists. Here, we investigated phenotypic flexibility in the size of the gastrointestinal (GI) tract across three northern populations of a winter-dormant warm-water fish, pumpkinseed sunfish (Lepomis gibbosus). In all populations, pumpkinseed exhibited pronounced structural flexibility in the GI tract, aligned with winter and the timing of reproduction. The dry mass of the GI increased by 1.3- to nearly 2.5-fold in the early spring. The pyloric caeca demonstrated the greatest capacity for flexibility, increasing by up to 3.7-fold prior to reproduction. In all populations, minimum dry GI mass was consistently achieved during winter and mid-summer. This capacity for gut flexibility may represent a novel mechanism for facilitating rapid adaptive responses (e.g. metabolic plasticity) to future environmental change.

Species portfolio effects dominate seasonal zooplankton stabilization within a large temperate lake.

Portfolio effects (PEs) in ecology refer to the suite of phenomenon where the temporal variation of aggregate ecosystem properties (i.e., abundance) is lower than that of their ecosystem components. An example of this is where differential responses of species to environmental variation generate stability at higher levels of ecological organization (e.g., local community, metapopulation, metacommunity). Most of the research examining such PEs has focused on spatial or interannual variation of ecosystems; however, as global change continues to alter seasonality and ecosystem functioning, understanding the underlying food web structures that help maintain stability at multiple spatial and temporal scales is critical to managing ecological systems. Recent advances investigating diversity-stability relationships has led to the development of frameworks that incorporate a metacommunity perspective which allows for the partitioning of PEs across organizational scales (i.e., local community, metapopulation, cross-community, metacommunity) from local population dynamics (total). This partitioning yields insights into the mechanisms that generate observed PEs in nature. Here, we employed one of these recently developed frameworks on a temporally (1986-1999, 2008-2019) and spatially (five sampling stations, local communities) extensive data set of zooplankton abundance (e.g., density) within a large temperate lake to investigate how temporal (seasonal) and spatial (among site) PEs influence stability within the zooplankton metacommunity. We found that seasonal asynchrony of different zooplankton species within local communities and across communities generated the vast majority of stabilization, while spatial (i.e., metapopulation) dynamics were more synchronous and contributed little to overall system stability. Furthermore, significantly positive diversity-asynchrony relationships at the total, local- and cross-community scales were found as asynchrony was positively correlated with local Shannon diversity. Last, a comparison of PEs over the time periods, during which significant local and global changes (i.e., climate warming, invasive species) have occurred suggests that PEs may be eroding, as increasingly synchronous dynamics and declining diversity in recent years have led to a rise in metacommunity variability. We end by arguing for the critical importance of understanding seasonally driven stabilizing mechanisms as local and global changes threaten to fundamentally alter seasonal signals with potentially strong implications for the structures that lend stability to ecosystems.

Applied winter biology: threats, conservation and management of biological resources during winter in cold climate regions.

Winter at high latitudes is characterized by low temperatures, dampened light levels and short photoperiods which shape ecological and evolutionary outcomes from cells to populations to ecosystems. Advances in our understanding of winter biological processes (spanning physiology, behaviour and ecology) highlight that biodiversity threats (e.g. climate change driven shifts in reproductive windows) may interact with winter conditions, leading to greater ecological impacts. As such, conservation and management strategies that consider winter processes and their consequences on biological mechanisms may lead to greater resilience of high altitude and latitude ecosystems. Here, we use well-established threat and action taxonomies produced by the International Union of Conservation of Nature-Conservation Measures Partnership (IUCN-CMP) to synthesize current threats to biota that emerge during, or as the result of, winter processes then discuss targeted management approaches for winter-based conservation. We demonstrate the importance of considering winter when identifying threats to biodiversity and deciding on appropriate management strategies across species and ecosystems. We confirm our expectation that threats are prevalent during the winter and are especially important considering the physiologically challenging conditions that winter presents. Moreover, our findings emphasize that climate change and winter-related constraints on organisms will intersect with other stressors to potentially magnify threats and further complicate management. Though conservation and management practices are less commonly considered during the winter season, we identified several potential or already realized applications relevant to winter that could be beneficial. Many of the examples are quite recent, suggesting a potential turning point for applied winter biology. This growing body of literature is promising but we submit that more research is needed to identify and address threats to wintering biota for targeted and proactive conservation. We suggest that management decisions consider the importance of winter and incorporate winter specific strategies for holistic and mechanistic conservation and resource management.

Trophic transfer of contaminants in a changing arctic marine food web: Cumberland Sound, Nunavut, Canada.

Contaminant dynamics in arctic marine food webs may be impacted by current climate-induced food web changes including increases in transient/subarctic species. We quantified food web organochlorine transfer in the Cumberland Sound (Nunavut, Canada) arctic marine food web in the presence of transient species using species-specific biomagnification factors (BMFs), trophic magnification factors (TMFs), and a multifactor model that included δ(15)N-derived trophic position and species habitat range (transient versus resident), and also considered δ(13)C-derived carbon source, thermoregulatory group, and season. Transient/subarctic species relative to residents had higher prey-to-predator BMFs of biomagnifying contaminants (1.4 to 62 for harp seal, Greenland shark, and narwhal versus 1.1 to 20 for ringed seal, arctic skate, and beluga whale, respectively). For contaminants that biomagnified in a transient-and-resident food web and a resident-only food web scenario, TMFs were higher in the former (2.3 to 10.1) versus the latter (1.7 to 4.0). Transient/subarctic species have higher tissue contaminant levels and greater BMFs likely due to higher energetic requirements associated with long-distance movements or consumption of more contaminated prey in regions outside of Cumberland Sound. These results demonstrate that, in addition to climate change-related long-range transport/deposition/revolatilization changes, increasing numbers of transient/subarctic animals may alter food web contaminant dynamics.

Subsidy accessibility drives asymmetric food web responses.

Global change is fundamentally altering flows of natural and anthropogenic subsidies across space and time. After a pointed call for research on subsidies in the 1990s, an industry of empirical work has documented the ubiquitous role subsidies play in ecosystem structure, stability, and function. Here, we argue that physical constraints (e.g., water temperature) and species traits can govern a species' accessibility to resource subsidies, which has been largely overlooked in the subsidy literature. We examined the input of a high-quality, point-source anthropogenic subsidy (aquaculture feed) into a recipient freshwater lake food web. Using a combined bio-tracer approach, we detect a gradient in accessibility of the anthropogenic subsidy within the surrounding food web driven by the thermal preferences of three constituent species, effectively rewiring the recipient lake food web. Because aquaculture is predicted to increase significantly in coming decades to support growing human populations, and global change is altering temperature regimes, then this form of food web alteration may be expected to occur frequently. We argue that subsidy accessibility is a key characteristic of recipient food web interactions that must be considered when trying to understand the impacts of subsidies on ecosystem stability and function under continued global change.

Seasonal variation of behavior and brain size in a freshwater fish.

Teleost fishes occupy a range of ecosystem, and habitat types subject to large seasonal fluctuations. Temperate fishes, in particular, survive large seasonal shifts in temperature, light availability, and access to certain habitats. Mobile species such as lake trout (Salvelinus namaycush) can behaviorally respond to seasonal variation by shifting their habitat deeper and further offshore in response to warmer surface water temperatures during the summer. During cooler seasons, the use of more structurally complex nearshore zones by lake trout could increase cognitive demands and potentially result in a larger relative brain size during those periods. Yet, there is limited understanding of how such behavioral responses to a seasonally shifting environment might shape, or be shaped by, the nervous system.Here, we quantified variation in relative brain size and the size of five externally visible brain regions in lake trout, across six consecutive seasons in two different lakes. Acoustic telemetry data from one of our study lakes were collected during the study period from a different subset of individuals and used to infer relationships between brain size and seasonal behaviors (habitat use and movement rate).Our results indicated that lake trout relative brain size was larger in the fall and winter compared with the spring and summer in both lakes. Larger brains coincided with increased use of nearshore habitats and increased horizontal movement rates in the fall and winter based on acoustic telemetry. The telencephalon followed the same pattern as whole brain size, while the other brain regions (cerebellum, optic tectum, olfactory bulbs, and hypothalamus) were only smaller in the spring.These findings provide evidence that flexibility in brain size could underpin shifts in behavior, which could potentially subserve functions associated with differential habitat use during cold and warm seasons and allow fish to succeed in seasonally variable environments.

Comparative Brain Morphology of the Greenland and Pacific Sleeper Sharks and its Functional Implications.

In cartilaginous fishes, variability in the size of the brain and its major regions is often associated with primary habitat and/or specific behavior patterns, which may allow for predictions on the relative importance of different sensory modalities. The Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic and are among the longest living vertebrates ever described. Despite a presumed visual impairment caused by the regular presence of parasitic ocular lesions, coupled with the fact that locomotory muscle power is often depressed at cold temperatures, these sharks remain capable of capturing active prey, including pinnipeds. Using magnetic resonance imaging (MRI), brain organization of S. microcephalus and S. pacificus was assessed in the context of up to 117 other cartilaginous fish species, using phylogenetic comparative techniques. Notably, the region of the brain responsible for motor control (cerebellum) is small and lacking foliation, a characteristic not yet described for any other large-bodied (>3 m) shark. Further, the development of the optic tectum is relatively reduced, while olfactory brain regions are among the largest of any shark species described to date, suggestive of an olfactory-mediated rather than a visually-mediated lifestyle.

Food web rewiring in a changing world.

Climate change is asymmetrically altering environmental conditions in space, from local to global scales, creating novel heterogeneity. Here, we argue that this novel heterogeneity will drive mobile generalist consumer species to rapidly respond through their behaviour in ways that broadly and predictably reorganize - or rewire - food webs. We use existing theory and data from diverse ecosystems to show that the rapid behavioural responses of generalists to climate change rewire food webs in two distinct and critical ways. First, mobile generalist species are redistributing into systems where they were previously absent and foraging on new prey, resulting in topological rewiring - a change in the patterning of food webs due to the addition or loss of connections. Second, mobile generalist species, which navigate between habitats and ecosystems to forage, will shift their relative use of differentially altered habitats and ecosystems, causing interaction strength rewiring - changes that reroute energy and carbon flows through existing food web connections and alter the food web's interaction strengths. We then show that many species with shared traits can exhibit unified aggregate behavioural responses to climate change, which may allow us to understand the rewiring of whole food webs. We end by arguing that generalists' responses present a powerful and underutilized approach to understanding and predicting the consequences of climate change and may serve as much-needed early warning signals for monitoring the looming impacts of global climate change on entire ecosystems.

Evidence of indiscriminate fishing effects in one of the world's largest inland fisheries.

While human impacts like fishing have altered marine food web composition and body size, the status of the world's important tropical inland fisheries remains largely unknown. Here, we look for signatures of human impacts on the indiscriminately fished Tonle Sap fish community that supports one of the world's largest freshwater fisheries. By analyzing a 15-year time-series (2000-2015) of fish catches for 116 species obtained from an industrial-scale 'Dai' fishery, we find: (i) 78% of the species exhibited decreasing catches through time; (ii) downward trends in catches occurred primarily in medium to large-bodied species that tend to occupy high trophic levels; (iii) a relatively stable or increasing trend in catches of small-sized species, and; (iv) a decrease in the individual fish weights and lengths for several common species. Because total biomass of the catch has remained remarkably resilient over the last 15 years, the increase in catch of smaller species has compensated for declines in larger species. Our finding of sustained production but altered community composition is consistent with predictions from recent indiscriminate theory, and gives a warning signal to fisheries managers and conservationists that the species-rich Tonle Sap is being affected by heavy indiscriminate fishing pressure.

Essential and non-essential element concentrations in two sleeper shark species collected in arctic waters.

A number of elements/metals have increased in arctic biota and are of concern due to their potential toxicity. Most studies on elements in the Arctic have focused on marine mammals and seabirds, but concentrations in the Greenland shark (Somniosus microcephalus) and Pacific sleeper shark (Somniosus pacificus), the only two shark species known to regularly inhabit arctic waters, have never been reported. To address this data gap, concentrations and patterns of 25 elements were analyzed in liver of Greenland sharks collected about Cumberland Sound (n=24) and Pacific sleeper sharks collected about Prince William Sound (n=14). Several non-essential elements differed between species/locations, which could suggest geographical exposure differences or ecological (e.g., diet) differences between the species. Certain essential elements also differed between the two sleeper sharks, which may indicate different physiological requirements between these closely related shark species, although information on such relationships are lacking for sharks and fish.

Origins of the Greenland shark (Somniosus microcephalus): Impacts of ice-olation and introgression.

Herein, we use genetic data from 277 sleeper sharks to perform coalescent-based modeling to test the hypothesis of early Quaternary emergence of the Greenland shark (Somniosus microcephalus) from ancestral sleeper sharks in the Canadian Arctic-Subarctic region. Our results show that morphologically cryptic somniosids S. microcephalus and Somniosus pacificus can be genetically distinguished using combined mitochondrial and nuclear DNA markers. Our data confirm the presence of genetically admixed individuals in the Canadian Arctic and sub-Arctic, and temperate Eastern Atlantic regions, suggesting introgressive hybridization upon secondary contact following the initial species divergence. Conservative substitution rates fitted to an Isolation with Migration (IM) model indicate a likely species divergence time of 2.34 Ma, using the mitochondrial sequence DNA, which in conjunction with the geographic distribution of admixtures and Pacific signatures likely indicates speciation associated with processes other than the closing of the Isthmus of Panama. This time span coincides with further planetary cooling in the early Quaternary period followed by the onset of oscillating glacial-interglacial cycles. We propose that the initial S. microcephalus-S. pacificus split, and subsequent hybridization events, were likely associated with the onset of Pleistocene glacial oscillations, whereby fluctuating sea levels constrained connectivity among Arctic oceanic basins, Arctic marginal seas, and the North Atlantic Ocean. Our data demonstrates support for the evolutionary consequences of oscillatory vicariance via transient oceanic isolation with subsequent secondary contact associated with fluctuating sea levels throughout the Quaternary period-which may serve as a model for the origins of Arctic marine fauna on a broad taxonomic scale.

Current-use pesticides in seawater and their bioaccumulation in polar bear-ringed seal food chains of the Canadian Arctic.

The distribution of current-use pesticides (CUPs) in seawater and their trophodynamics were investigated in 3 Canadian Arctic marine food chains. The greatest ranges of dissolved-phase concentrations in seawater for each CUP were endosulfan sulfate (less than method detection limit (MDL) to 19 pg L(-1) ) > dacthal (0.76-15 pg L(-1) ) > chlorpyrifos (less than MDL to 8.1 pg L(-1) ) > pentachloronitrobenzene (less than MDL to 2.6 pg L(-1) ) > α-endosulfan (0.20-2.3 pg L(-1) ). Bioaccumulation factors (BAFs, water-respiring organisms) were greatest in plankton, including chlorothalonil (log BAF = 7.4 ± 7.1 L kg(-1) , mean ± standard error), chlorpyrifos (log BAF = 6.9 ± 6.7 L kg(-1) ), and α-endosulfan (log BAF = 6.5 ± 6.0 L kg(-1) ). The largest biomagnification factors (BMFs) were found for dacthal in the capelin:plankton trophic relationship (BMF = 13 ± 5.0) at Cumberland Sound (Nunvavut), and for ß-endosulfan (BMF = 16 ± 4.9) and α-endosulfan (BMF = 9.3 ± 2.8) in the polar bear-ringed seal relationship at Barrow and Rae Strait (NU), respectively. Concentrations of endosulfan sulfate exhibited trophic magnification (increasing concentrations with increasing trophic level) in the poikilothermic portion of the food web (trophic magnification factor = 1.4), but all of the CUPs underwent trophic dilution in the marine mammal food web, despite some trophic level-specific biomagnification. Together, these observations are most likely indicative of metabolism of these CUPs in mammals. Environ Toxicol Chem 2016;35:1695-1707. © 2016 SETAC.

Impacts of food web structure and feeding behavior on mercury exposure in Greenland Sharks (Somniosus microcephalus).

Benthic and pelagic food web components in Cumberland Sound, Canada were explored as sources of total mercury (THg) to Greenland Sharks (Somniosus microcephalus) via both bottom-up food web transfer and top-down shark feeding behavior. Log10THg increased significantly with δ(15)N and trophic position from invertebrates (0.01 ± 0.01 µg · g(-1) [113 ± 1 ng · g(-1)] dw in copepods) to Greenland Sharks (3.54 ± 1.02 µg · g(-1)). The slope of the log10THg vs. δ(15)N linear regression was higher for pelagic compared to benthic food web components (excluding Greenland Sharks, which could not be assigned to either food web), which resulted from THg concentrations being higher at the base of the benthic food web (i.e., in benthic than pelagic primary consumers). However, feeding habitat is unlikely to consistently influence shark THg exposure in Cumberland Sound because THg concentrations did not consistently differ between benthic and pelagic shark prey. Further, size, gender and feeding behavior (inferred from stable isotopes and fatty acids) were unable to significantly explain THg variability among individual Greenland Sharks. Possible reasons for this result include: 1) individual sharks feeding as generalists, 2) high overlap in THg among shark prey, and 3) differences in turnover time between ecological tracers and THg. This first assessment of Greenland Shark THg within an Arctic food web revealed high concentrations consistent with biomagnification, but low ability to explain intra-specific THg variability. Our findings of high THg levels and consumption of multiple prey types, however, suggest that Greenland Sharks acquire THg through a variety of trophic pathways and are a significant contributor to the total biotic THg pool in northern seas.

Food Web Structure in Temporally-Forced Ecosystems.

Temporal variation characterizes many of Earth's ecosystems. Despite this, little is known about how food webs respond to regular variation in time, such as occurs broadly with season. We argue that season, and likely any periodicity, structures food webs along a temporal axis in an analogous way to that previously recognized in space; predators shift their diet as different resource compartments and trophic levels become available through time. These characteristics are likely (i) central to ecosystem function and stability based on theory, and (ii) widespread across ecosystem types based on empirical observations. The temporal food web perspective outlined here could provide new insight into the ecosystem-level consequences of altered abiotic and biotic processes that might accompany globally changing environments.

Comparative organochlorine accumulation in two ecologically similar shark species (Carcharodon carcharias and Carcharhinus obscurus) with divergent uptake based on different life history.

Trophic position and body mass are traits commonly used to predict organochlorine burdens. Sharks, however, have a variety of feeding and life history strategies and metabolize lipid uniquely. Because of this diversity, and the lipid-association of organochlorines, the dynamics of organochlorine accumulation in sharks may be predicted ineffectively by stable isotope-derived trophic position and body mass, as is typical for other taxa. The present study compared ontogenetic organochlorine profiles in the dusky shark (Carcharhinus obscurus) and white shark (Carcharodon carcharias), which differ in metabolic thermoregulation and trophic position throughout their ontogeny. Although greater organochlorine concentrations were observed in the larger bodied and higher trophic position white shark (e.g., p,p'-dichlorodiphenyldichloroethylene: 20.2 ± 2.7 ng/g vs 9.3 ± 2.2 ng/g in the dusky shark), slopes of growth-dilution corrected concentrations with age were equal to those of the dusky shark. Similar ontogenetic trophic position increases in both species, less frequent white shark seal predation than previously assumed, or inaccurate species-specific growth parameters are possible explanations. Inshore habitat use (indicated by δ(13)C values) and mass were important predictors in white and dusky sharks, respectively, of both overall compound profiles and select organochlorine concentrations. The present study clarified understanding of trophic position and body mass as reliable predictors of interspecific organochlorine accumulation in sharks, whereas regional endothermy and diet shifting were shown to have less impact on overall rates of accumulation.