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Energetic and health effects of protein overconsumption constrain dietary adaptation in an apex predator

Studies of predator feeding ecology commonly focus on energy intake. However, captive predators have been documented to selectively feed to optimize macronutrient intake. As many apex predators experience environmental changes that affect prey availability, limitations on selective feeding can affect energetics and health. We estimated the protein:fat ratio of diets consumed by wild polar bears using a novel isotope-based approach, measured protein:fat ratios selected by zoo polar bears offered dietary choice and examined potential energetic and health consequences of overconsuming protein. Dietary protein levels selected by wild and zoo polar bears were low and similar to selection observed in omnivorous brown bears, which reduced energy intake requirements by 70% compared with lean meat diets. Higher-protein diets fed to zoo polar bears during normal care were concurrent with high rates of mortality from kidney disease and liver cancer. Our results suggest that polar bears have low protein requirements and that limitations on selective consumption of marine mammal blubber consequent to climate change could meaningfully increase their energetic costs. Although bear protein requirements appear lower than those of other carnivores, the energetic and health consequences of protein overconsumption identified in this study have the potential to affect a wide range of taxa.

Scientific Reports

Estimating and forecasting spatial population dynamics of apex predators using transnational genetic monitoring

The ongoing recovery of terrestrial large carnivores in North America and Europe is accompanied by intense controversy. On the one hand, reestablishment of large carnivores entails a recovery of their most important ecological role, predation. On the other hand, societies are struggling to relearn how to live with apex predators that kill livestock, compete for game species, and occasionally injure or kill people. Those responsible for managing these species and mitigating conflict often lack fundamental information due to a long-standing challenge in ecology: How do we draw robust population-level inferences for elusive animals spread over immense areas? Here we showcase the application of an effective tool for spatially explicit tracking and forecasting of wildlife population dynamics at scales that are relevant to management and conservation. We analyzed the world’s largest dataset on carnivores comprising more than 35,000 noninvasively obtained DNA samples from over 6,000 individual brown bears ( Ursus arctos ), gray wolves ( Canis lupus ), and wolverines ( Gulo gulo ). Our analyses took into account that not all individuals are detected and, even if detected, their fates are not always known. We show unequivocal quantitative evidence of large carnivore recovery in northern Europe, juxtaposed with the finding that humans are the single-most important factor driving the dynamics of these apex predators. We present maps and forecasts of the spatiotemporal dynamics of large carnivore populations, transcending national boundaries and management regimes.

Proceedings of the National Academy of Sciences of

Feeding ecology of native and nonnative salmonids during the expansion of a nonnative apex predator in Yellowstone Lake, Yellowstone National Park

The illegal introduction of Lake Trout Salvelinus namaycush into Yellowstone Lake, Yellowstone National Park, preceded the collapse of the native population of Yellowstone Cutthroat Trout Oncorhynchus clarkii bouvieri , producing a four-level trophic cascade. The Yellowstone Cutthroat Trout population’s collapse and the coinciding increase in Lake Trout abundance provided a rare opportunity to evaluate the feeding ecology of a native prey species and a nonnative piscivore species after the restructuring of a large lentic ecosystem. We assessed diets, stable isotope signatures, and depth-related CPUE patterns for Yellowstone Cutthroat Trout and Lake Trout during 2011–2013 to evaluate trophic overlap. To evaluate diet shifts related to density, we also compared 2011–2013 diets to those from studies conducted during previous periods with contrasting Yellowstone Cutthroat Trout and Lake Trout CPUEs. We illustrate the complex interactions between predator and prey in a simple assemblage and demonstrate how a nonnative apex predator can alter competitive interactions. The diets of Yellowstone Cutthroat Trout were dominated by zooplankton during a period when the Yellowstone Cutthroat Trout CPUE was high and were dominated by amphipods when the CPUE was reduced. Lake Trout shifted from a diet that was dominated by Yellowstone Cutthroat Trout during the early stages of the invasion to a diet that was dominated by amphipods after Lake Trout abundance had increased and after Yellowstone Cutthroat Trout prey had declined. The shifts in Yellowstone Cutthroat Trout and Lake Trout diets resulted in increased trophic similarity of these species through time due to their shared reliance on benthic amphipods. Yellowstone Cutthroat Trout not only face the threat posed by Lake Trout predation but also face the potential threat of competition with Lake Trout if amphipods are limiting. Our results demonstrate the importance of studying the long-term feeding ecology of fishes in invaded ecosystems.

Wyoming

American white pelican predation on Cui-ui in Pyramid Lake, Nevada

Anthropogenic changes to the Pyramid Lake–Truckee River ecosystem in Nevada are suspected to have altered the predator–prey balance between American white pelican Pelecanus erythrorhynchos and Cui-ui Chasmistes cujus . We estimated the loss of the adult Cui-ui population to pelican predation over a 13-year period by netting and tagging Cui-uis as they aggregated at the mouth of the Truckee River prior to their spawning migration into the Truckee River. Cui-ui access to the Truckee River typically required traversing a shallow delta (a foraging advantage for these American white pelicans). Dams and greater frequency of low stream flows also contributed to American white pelican foraging success. We used tag recoveries from Pyramid Lake's nesting colony of American white pelicans along with an experiment to estimate the chance of tag recovery within the colony to calculate the number of tagged fish taken by American white pelicans. We also used numbered tags to test whether there was a size preference for Cui-uis taken. Our results showed that the primary source of adult Cui-ui mortality was from American white pelican predation in the Truckee River. Within a 13-year period American white pelicans had taken 90% of the tags deployed during the first 7 years of the interval. There was no preference for the size of Cui-uis taken. A better understanding of the effects of heavy cropping by American white pelicans on Cui-ui population dynamics is still needed.

Nevada

Biogeographic and ecological regulation of disease: Prevalence of Sin Nombre virus in island mice is related to island area, precipitation, and predator richness

The relative roles of top-down and bottom-up forces in affecting disease prevalence in wild hosts is important for understanding disease dynamics and human disease risk. We found that the prevalence of Sin Nombre virus (SNV), the agent of a severe disease in humans (hantavirus pulmonary syndrome), in island deer mice from the eight California Channel Islands was greater with increased precipitation (a measure of productivity), greater island area, and fewer species of rodent predators. In finding a strong signal of the ecological forces affecting SNV prevalence, our work highlights the need for future work to understand the relative importance of average rodent density, population fluctuations, behavior, and specialist predators as they affect SNV prevalence. In addition to illustrating the importance of both bottom-up and top-down limitation of disease prevalence, our results suggest that predator richness may have important bearing on the risk of exposure to animal-borne diseases that affect humans.

California

Brown bear–sea otter interactions along the Katmai coast: Terrestrial and nearshore communities linked by predation

Sea otters were extirpated throughout much of their range by the maritime fur trade in the 18th and 19th centuries, including the coast of Katmai National Park and Preserve in southcentral Alaska. Brown bears are an important component of the Katmai ecosystem where they are the focus of a thriving ecotourism bear-viewing industry as they forage in sedge meadows and dig clams in the extensive tidal flats that exist there. Sea otters began reoccupying Katmai in the 1970s where their use of intertidal clam resources overlapped that of brown bears. By 2008, the Katmai sea otter population had grown to an estimated 7,000 animals and was likely near carrying capacity; however, in 2006–2015, the age-at-death distribution (AADD) of sea otter carcasses collected at Katmai included a higher-than-expected proportion of prime-age animals compared to most other sea otter populations in Alaska. The unusual AADD warranted scientific investigation, particularly because the Katmai population is part of the Threatened southwest sea otter stock. Brown bears in Katmai are known to prey on marine mammals and sea otters, but depredation rates are unknown; thus, we investigated carnivore predation, especially by brown bears, as a potential explanation for abnormally high prime-age otter mortality. We installed camera traps at two island-based marine mammal haulout sites within Katmai to gather direct evidence that brown bears prey on seals and sea otters. Over a period of two summers, we gathered photo evidence of brown bears making 22 attempts to prey on sea otters of which nine (41%) were successful and 12 attempts to prey on harbor seals of which one (8%) was successful. We also developed a population model based on the AADD to determine if the living population is declining, as suggested by the high proportion of prime-age animals in the AADD. We found that the population trend predicted by the modeled AADDs was contradictory to aerial population surveys that indicated the population was not in steep decline but was consistent with otter predation. Future work should focus on the direct and indirect effects these top-level predators have on each other and the coastal community that connects them.

Alaska

Compensatory mortality explains rodent resilience to an invasive predator

Invasive Burmese pythons ( Python bivittatus ) in the Everglades of Florida, United States, have drastically reduced populations of mammals, yet populations of some rodents appear unaffected by the invasion. To understand this pattern, we radio-tagged cotton rats ( Sigmodon hispidus ) in areas of high and low python occurrence densities (hereafter occurrence) and quantified the effects of python occurrence, seasonality, and sex on their survival and cause-specific mortality. Cotton rat survival was not influenced by difference in python occurrence (hazard ratio = 1.32, 95% CI = 0.77–2.26, P = 0.30). However, cotton rats were at greater risk from mortalities caused by mammals in areas of low python occurrence. In areas with elevated python occurrence, we attributed most cotton rat mortalities to birds of prey (48.6%) and reptiles (non-python = 24.3%, python = 16.2%). Where python occurrence was relatively low, we attributed cotton rat mortalities to native reptilian (28.6%), avian (35.7%), and mammalian predators (35.7%) with no python-related deaths. In total, pythons were responsible for 11.8% of all cotton rat mortalities. Finding no difference in the survival of cotton rats, despite differences in the causative agents of mortality, suggests that predation pressure from an invasive predator was compensatory for cotton rat population dynamics. This type of compensatory mortality is common for small mammals and helps explain why mammal communities in python-invaded portions of the Greater Everglades Ecosystem are increasingly dominated by cotton rats and other rodents.

Journal of Mammalogy

Spatial variation in landlocked Atlantic Salmon smolt survival associated with dam passage, avian predation, and stocking location

Objective We evaluated survival differences between upstream and downstream stocking for landlocked Atlantic Salmon Salmo salar smolts in a tributary to Lake Champlain. Methods We radio-tagged smolts and stocked them concurrently with 22,000 smolts at two release sites in 2 years. The downstream location (DS, river kilometer 16, no dam passage) was a historically used site in a dam tailrace, whereas the upstream site (US, river kilometer 27, two dams to pass) was in a side channel and stocked for the first time. We estimated survival, counted birds during stocking, and searched nesting colonies for transmitters. Results Within stocking reaches, survival per kilometer for the DS release group was markedly lower than that for the US group (US 2021 and 2022 = 0.98, 0.98, respectively; DS 2021 and 2022 = 0.82, 0.69, respectively). At the DS site, we documented a tenfold increase in avian predators following stocking, whereas no increase was detected at the US site. Passage was >96% at both dams, but postpassage survival (per kilometer) was much lower at the second dam (2021 = 0.78, 2022 = 0.82) compared to the first dam (2021 = 0.96, 2022 = 0.97). Surprisingly, cumulative survival to Lake Champlain was higher for fish that were released upstream in 2022 (US = 43%; DS = 32%) despite dam passage and additional migratory distance. At least 20% (2021) and 7% (2022) of successful migrants were later consumed by birds in the river delta or in Lake Champlain. Conclusions Upstream stocking did not consistently result in lower cumulative survival, likely due to predators habituated to annually reoccurring stocking in a dam tailrace that increased stocking-related mortality at the DS release site. We highlight the importance of evaluating historically used stocking sites, as substantial loss of smolts could be avoided by simple changes to stocking practices. Avian predation was a major source of mortality, necessitating further studies to understand and address survival issues within Lake Champlain.

Vermont

Grizzly bear predation links the loss of native trout to the demography of migratory elk in Yellowstone

The loss of aquatic subsidies such as spawning salmonids is known to threaten a number of terrestrial predators, but the effects on alternative prey species are poorly understood. At the heart of the Greater Yellowstone ecosystem, an invasion of lake trout has driven a dramatic decline of native cutthroat trout that migrate up the shallow tributaries of Yellowstone Lake to spawn each spring. We explore whether this decline has amplified the effect of a generalist consumer, the grizzly bear, on populations of migratory elk that summer inside Yellowstone National Park (YNP). Recent studies of bear diets and elk populations indicate that the decline in cutthroat trout has contributed to increased predation by grizzly bears on the calves of migratory elk. Additionally, a demographic model that incorporates the increase in predation suggests that the magnitude of this diet shift has been sufficient to reduce elk calf recruitment (4–16%) and population growth (2–11%). The disruption of this aquatic–terrestrial linkage could permanently alter native species interactions in YNP. Although many recent ecological changes in YNP have been attributed to the recovery of large carnivores—particularly wolves—our work highlights a growing role of human impacts on the foraging behaviour of grizzly bears.

Yellowstone National Park

El Niño/Southern Oscillation-driven rainfall pulse amplifies predation by owls on seabirds via apparent competition with mice

Most approaches for assessing species vulnerability to climate change have focused on direct impacts via abiotic changes rather than indirect impacts mediated by changes in species interactions. Changes in rainfall regimes may influence species interactions from the bottom-up by increasing primary productivity in arid environments, but subsequently lead to less predictable top-down effects. Our study demonstrates how the effects of an EL Niño/Southern Oscillation (ENSO)-driven rainfall pulse ricochets along a chain of interactions between marine and terrestrial food webs, leading to enhanced predation of a vulnerable marine predator on its island breeding grounds. On Santa Barbara Island, barn owls ( Tyto alba ) are the main predator of a nocturnal seabird, the Scripps's murrelet ( Synthliboramphus scrippsi ), as well as an endemic deer mouse. We followed the links between rainfall, normalized difference vegetation index and subsequent peaks in mouse and owl abundance. After the mouse population declined steeply, there was approximately 15-fold increase in the number of murrelets killed by owls. We also simulated these dynamics with a mathematical model and demonstrate that bottom-up resource pulses can lead to subsequent declines in alternative prey. Our study highlights the need for understanding how species interactions will change with shifting rainfall patterns through the effects of ENSO under global change.

California

Predictive modelling of habitat use by marine predators with respect to the abundance and depth distribution of pelagic prey

Understanding the ecological processes that underpin species distribution patterns is a fundamental goal in spatial ecology. However, developing predictive models of habitat use is challenging for species that forage in marine environments, as both predators and prey are often highly mobile and difficult to monitor. Consequently, few studies have developed resource selection functions for marine predators based directly on the abundance and distribution of their prey. We analysed contemporaneous data on the diving locations of two seabird species, the shallow-diving Peruvian Booby ( Sula variegata ) and deeper diving Guanay Cormorant ( Phalacrocorax bougainvilliorum ), and the abundance and depth distribution of their main prey, Peruvian anchoveta ( Engraulis ringens ). Based on this unique data set, we developed resource selection functions to test the hypothesis that the probability of seabird diving behaviour at a given location is a function of the relative abundance of prey in the upper water column. For both species, we show that the probability of diving behaviour is mostly explained by the distribution of prey at shallow depths. While the probability of diving behaviour increases sharply with prey abundance at relatively low levels of abundance, support for including abundance in addition to the depth distribution of prey is weak, suggesting that prey abundance was not a major factor determining the location of diving behaviour during the study period. The study thus highlights the importance of the depth distribution of prey for two species of seabird with different diving capabilities. The results complement previous research that points towards the importance of oceanographic processes that enhance the accessibility of prey to seabirds. The implications are that locations where prey is predictably found at accessible depths may be more important for surface foragers, such as seabirds, than locations where prey is predictably abundant. Analysis of the relative importance of abundance and accessibility is essential for the design and evaluation of effective management responses to reduced prey availability for seabirds and other top predators in marine systems.

Gulf of Guinea

Broad‐scale occurrence of a subsidized avian predator: reducing impacts of ravens on sage‐grouse and other sensitive prey

Expanding human enterprise across remote environments impacts numerous wildlife species. Anthropogenic resources provide subsidies for generalist predators that can lead to cascading effects on prey species at lower trophic levels. A fundamental challenge for applied ecologists is to disentangle natural and anthropogenic influences on species occurrence, and subsequently develop spatially explicit models to help inform management and conservation decisions. Using Bayesian hierarchical occupancy models, we mapped the broad‐scale occurrence of common ravens Corvus corax as a function of natural and anthropogenic landscape covariates using >15,000 point count surveys performed during 2007–2016 within the Great Basin region, USA. Raven abundance and distribution is substantially increasing across the American west due to unintended anthropogenic resource subsidies. Importantly, ravens prey on eggs and chicks of numerous species including greater sage‐grouse Centrocercus urophasianus , an indicator species whose decline is at the centre of national conservation strategies and land use policies.Anthropogenic factors that contributed to greater raven occurrence were: increased road density, presence of transmission lines, agricultural activity, and presence of roadside rest areas. Natural landscape characteristics included lower elevations with greener vegetation (NDVI), greater stream and habitat edge densities, and lower percentages of big sagebrush A. tridentata spp . Interactions between anthropogenic sources of nesting substrate and food subsidies suggested that raven occurrence increased multiplicatively when these resource subsidies co‐occurred. Overall, the average probability of raven occurrence estimated within sagebrush ecosystems of the study area was ~0.83. Synthesis and applications . We demonstrate how anthropogenic factors can be disentangled from natural effects when making spatially‐explicit predictions of subsidized predators occurring across expansive landscapes. This approach can guide management decisions where subsidized predators overlap sensitive prey habitats. For example, we identify areas where elevated raven occurrence coincides with breeding sage‐grouse concentration areas and appears to be largely driven by anthropogenic factors. Management applications could focus on reducing raven access to anthropogenic subsidies in these areas, while prioritizing habitat improvements for sage‐grouse elsewhere. Our approach is applicable to other species where widespread survey data are available.

Journal of Applied Ecology

Consequences of migratory coupling of predators and prey when mediated by human actions

Aim Animal migrations influence ecosystem structure, dynamics and persistence of predator and prey populations. The theory of migratory coupling postulates that aggregations of migrant prey can induce large-scale synchronized movements in predators, and this coupling is consequential for the dynamics of ecological communities. The degree to which humans influence these interactions remains largely unknown. We tested whether creation of large resource pulses by humans such as seasonal herding of reindeer Rangifer tarandus and hunting of moose, Alces alces , can induce migratory coupling with Golden Eagles, Aquila chrysaetos, and whether these lead to demographic consequences for the eagles. Location Fennoscandia. Methods We used movement data from 32 tracked Golden Eagles spanning 125 annual migratory cycles over 8 years. We obtained reindeer distribution data through collaboration with reindeer herders based on satellite tracking of reindeer, and moose harvest data from the national hunting statistics for Sweden. We assessed demographic consequences for eagles from ingesting lead from ammunition fragments in moose carcasses through survival estimates and their links with lead concentrations in eagles' blood. Results In spring, eagles migrated hundreds of kilometres to be spatially and temporally coupled with calving reindeer, whereas in autumn, eagles matched their distribution with the location and timing of moose hunt. Juveniles were more likely to couple with reindeer calving, whereas adults were particularly drawn to areas of higher moose harvest. Due to this coupling, eagles ingested lead from spent ammunition in moose offal and carcasses and the resulting lead toxicity increased the risk of mortality by 3.4 times. Main conclusions We show how migratory coupling connects landscape processes and that human actions can influence migratory coupling over large spatial scales and increase demographic risks for predators. We provide vital knowledge towards resolving human–wildlife conflicts and the conservation of protected species over a large spatial and temporal scale.

Diversity and Distributions

Population-level effects of egg predation on a native planktivore in a large freshwater lake

Using a 37-year recruitment time series, we uncovered a field pattern revealing a strong, inverse relationship between bloater Coregonus hoyi recruitment success and slimy sculpin Cottus cognatus biomass in Lake Michigan (United States), one of the largest freshwater lakes of the world. Given that slimy sculpins (and deepwater sculpin Myoxocephalus thompsonii) are known egg predators that spatiotemporally overlap with incubating bloater eggs, we used recently published data on sculpin diets and daily ration to model annual bloater egg consumption by sculpins for the 1973&ndash;2010 year-classes. Although several strong year-classes were produced in the late 1980s when the proportion of eggs consumed by slimy sculpins was extremely low (i.e., <0.001) and several weak year-classes were produced when the proportion of bloater eggs consumed was at its highest (i.e., >0.10&ndash;1.0), egg predation failed to explain why recruitment was weak for the 1995&ndash;2005 year-classes when the proportion consumed was also low (i.e., <0.02). We concluded that egg predation by slimy and deepwater sculpins could have limited bloater recruitment in some years, but that some undetermined factor was more important in many other years. Given that slimy sculpin densities are influenced by piscivorous lake trout Salvelinus namaycush, the restoration of which in Lake Michigan has lagged behind those in lakes Superior and Huron, our study highlights the importance of an ecosystem perspective when considering population dynamics of fishes.

Lake Michigan

Linking anti-predator behaviour to prey demography reveals limited risk effects of an actively hunting large carnivore

Ecological theory predicts that the diffuse risk cues generated by wide-ranging, active predators should induce prey behavioural responses but not major, population- or community-level consequences. We evaluated the non-consumptive effects (NCEs) of an active predator, the grey wolf (Canis lupus), by simultaneously tracking wolves and the behaviour, body fat, and pregnancy of elk (Cervus elaphus), their primary prey in the Greater Yellowstone Ecosystem. When wolves approached within 1 km, elk increased their rates of movement, displacement and vigilance. Even in high-risk areas, however, these encounters occurred only once every 9 days. Ultimately, despite 20-fold variation in the frequency of encounters between wolves and individual elk, the risk of predation was not associated with elk body fat or pregnancy. Our findings suggest that the ecological consequences of actively hunting large carnivores, such as the wolf, are more likely transmitted by consumptive effects on prey survival than NCEs on prey behaviour.

Montana;Wyoming;Idaho

Predators of Dusky Canada Goose goslings and the effect of transmitters on gosling survival

The population of Dusky Canada Geese (Branta canadensis occidentalis) has been in long-term decline, likely due to reduced breeding productivity. To identify causes of mortality, we monitored goslings marked with radio transmitters on the western Copper River Delta, Alaska, from 1997 to 1999. Almost all gosling mortality (96%; 81 of 84) was due to predation, with mink (Mustela vison) and Bald Eagles (Haliaeetus leucocephalus) the most important predators. Bald Eagles are also major nest predators and, thus, appear to play a key role in limiting the breeding productivity of Dusky Canada Geese. Daily survival rate for goslings to 28 d of age was lower (0.011; 95% CI 0.002-0.024) for those with transmitters than for those without, but did not differ for older goslings (29-45 d). Although finer resolution in the timing of the transmitter effect within the first 28 d was not possible, we found that, by limiting our sample to goslings that survived until after 2-3 d posthatching, support for a transmitter effect was much reduced. Younger, smaller birds are inherently more vulnerable than older birds to transmitter effects. In addition, the process of radio-marking may have delayed the departure of goslings from nests and increased their risk of mortality shortly after hatching. Although radio transmitters may often be the only practical means for determining causes of mortality for young waterfowl, we suggest caution in using transmitters because of their potential negative effects, particularly during the first few days after hatching. ?? 2008 Association of Field Ornithologists.

Journal of Field Ornithology

Patterns of foraging and distribution of bluegill sunfish in a Mississippi River backwater: Influence of macrophytes and predation

We studied the trophic interactions and spatial distributions of bluegills Lepomis macrochirus and largemouth bass Micropterus salmoides in a macrophyte bed in Lake Onalaska, a backwater lake in the upper Mississippi River. The diets of adult and age-0 bluegills were similar and changed seasonally probably in response to changes in life stages of macroinvertebrates (i. e. emergence of winged adults). Diets and diel patterns of abundance of bluegill suggest that age-O and adults were feeding in the vegetated, littoral zone. Predation by age-O largemouth bass appears to influence use of vegetated habitat by age-0 bluegills. In summer, when most age-O bluegills were vulnerable to predation by age-O largemouth bass, bluegill abundance was strongly correlated with vegetation biomass. In October and November, piscivory by age-O largemouth bass was limited by gape. Consequently, the relationship between the abundance of age-O bluegills and vegetation biomass was weakened because predation risk by age-O largemouth bass was reduced.

Wisconsin

The effect of predation on stunted and nonstunted white perch

Predation is widely regarded as a means to prevent or minimise the establishment of a stunted (high density of slow growing individuals) population. We investigated the effect of predation on two different white perch Morone americana populations (stunted and nonstunted) by examining the stomach contents of piscivorous fishes. White perch and gizzard shad dominated piscivore diets in Branched Oak Lake, whereas white perch dominated piscivore diets in Pawnee Lake. White perch consumed in the stunted population (Branched Oak Lake) were larger and older than white perch consumed in the nonstunted population (Pawnee Lake). Many of the consumed white perch in the stunted population were sexually mature and had the opportunity to spawn at least once. In contrast, all of the consumed white perch in the nonstunted population were sexually immature. Predation may have reinforced the stunting of white perch in Branched Oak Lake through removal of the largest, oldest individuals. ?? 2010 John Wiley & Sons A/S.

Ecology of Freshwater Fish