Density‐dependent mortality in Pacific salmon: the ghost of impacts past?

Conservation biologists often ignore density dependence because at‐risk populations are typically small relative to historical levels. However, if populations are reduced as a result of impacts that lower carrying capacity, then density‐dependent mortality may exist at low population abundances. Here, we explore this issue in threatened populations of juvenile chinook salmon (Oncorhynchus tshawytscha). We followed the fate of more than 50 000 juvenile chinook in the Snake River Basin, USA to test the hypothesis that their survival was inversely associated with juvenile density. We also tested the hypotheses that non‐indigenous brook trout and habitat quality affect the presence or strength of density dependence. Our results indicate that juvenile chinook suffer density‐dependent mortality and the strength of density dependence was greater in streams in which brook trout were absent. We were unable to detect an effect of habitat quality on the strength of density dependence. Historical impacts of humans have greatly reduced population sizes of salmon, and the density dependence we report may stem from a shortage of nutrients normally derived from decomposing salmon carcasses. Cohorts of juvenile salmon may experience density‐dependent mortality at population sizes far below historical levels and recovery of imperiled populations may be much slower than currently expected.     

Diverse foraging opportunities drive the functional response of local and landscape-scale bear predation on Pacific salmon

The relationship between prey abundance and predation is often examined in single habitat units or populations, but predators may occupy landscapes with diverse habitats and foraging opportunities. The vulnerability of prey within populations may depend on habitat features that hinder predation, and increased density of conspecifics in both the immediate vicinity and the broader landscape. We evaluated the relative effects of physical habitat, local, and neighborhood prey density on predation by brown bears on sockeye salmon in a suite of 27 streams using hierarchical Bayesian functional response models. Stream depth and width were inversely related to the maximum proportion of salmon killed, but not the asymptotic limit on total number killed. Interannual variation in predation was density dependent; the number of salmon killed increased with fish density in each stream towards an asymptote. Seven streams in two geographical groups with ≥23 years of data in common were then analyzed for neighborhood density effects. In most (12 of 18) cases predation in a stream was reduced by increasing salmon abundance in neighboring streams. The uncertainty in the estimates for these neighborhood effects may have resulted from interactions between salmon abundance and habitat that influenced foraging by bears, and from bear behavior (e.g., competitive exclusion) and abundance. Taken together, the results indicated that predator–prey interactions depend on density at multiple spatial scales, and on habitat features of the surrounding landscape. Explicit consideration of this context dependency should lead to improved understanding of the ecological impacts of predation across ecosystems and taxa.     

Density-dependent prey behaviours and mutable predator foraging modes induce Allee effects and over-prediction of prey mortality rates

1. Predator–prey models are often used to represent consumptive interactions between species but, typically, are derived using simple experimental systems with little plasticity in prey or predator behaviours. However, many prey and predators exhibit a broad suite of behaviours. Here, we experimentally tested the effect of density-dependent prey and predator behaviours on per capita relative mortality rates using Florida bass (Micropterus floridanus) consuming juvenile Bluegill (Lepomis macrochirus).
2. Experimental ponds were stocked with a factorial design of low, medium, and high prey and predator densities. Prey mortality, prey–predator behaviours, and predator stomach contents were recorded over or after 7 days. We assumed the mortality dynamics followed foraging arena theory. This pathologically flexible predator–prey model separates prey into invulnerable and vulnerable pools where predators can consume prey in the latter. As this approach can represent classic Lotka–Volterra and ratio-dependent dynamics, we fit a foraging arena predator–prey model to the number of surviving prey.
3. We found that prey exhibited density-dependent prey behaviours, hiding at low densities, shoaling at medium densities, and using a provided refuge at high densities. Predators exhibited ratio-dependent behaviours, using an ambush foraging mode when one predator was present, hiding in the shadows at low prey–high predator densities, and shoaling at medium and high prey–high predator densities. The foraging arena model predicted the mortality rates well until the high prey–high predator treatment where group vigilance prey behaviours occurred and predators probably interfered with one another resulting in the model predicting higher mortality than observed.
4. This is concerning given the ubiquity of predator–prey models in ecology and natural resource management. Furthermore, as Allee effects engender instability in population regulation, it could lead to inaccurate predictions of conservation status, population rebuilding or harvest rates.

     

Competition for safe real estate,not food,drives density‐dependent juvenile survival in a large herbivore

Density‐dependent competition for food reduces vital rates, with juvenile survival often the first to decline. A clear prediction of food‐based, density‐dependent competition for large herbivores is decreasing juvenile survival with increasing density. However, competition for enemy‐free space could also be a significant mechanism for density dependence in territorial species. How juvenile survival is predicted to change across density depends critically on the nature of predator–prey dynamics and spatial overlap among predator and prey, especially in multiple‐predator systems. Here, we used a management experiment that reduced densities of a generalist predator, coyotes, and specialist predator, mountain lions, over a 5‐year period to test for spatial density dependence mediated by predation on juvenile mule deer in Idaho, USA. We tested the spatial density‐dependence hypothesis by tracking the fate of 251 juvenile mule deer, estimating cause‐specific mortality, and testing responses to changes in deer density and predator abundance. Overall juvenile mortality did not increase with deer density, but generalist coyote‐caused mortality did, but not when coyote density was reduced experimentally. Mountain lion‐caused mortality did not change with deer density in the reference area in contradiction of the food‐based competition hypothesis, but declined in the treatment area, opposite to the pattern of coyotes. These observations clearly reject the food‐based density‐dependence hypothesis for juvenile mule deer. Instead, our results provide support for the spatial density‐dependence hypothesis that competition for enemy‐free space increases predation by generalist predators on juvenile large herbivores.     

Foraging responses of Coccinella septempunctata,Hippodamia variegata and Chrysoperla carnea to changing in density of two aphid species

The successful use of predators in classical biocontrol programmes needs several background laboratory investigations, one of which is the evaluation of predator behavioural responses to changes in the density of their prey. The impact effect of the density of two prey species [Myzus persicae Sulzer and Aphis craccivora Koch (Hemiptera: Aphididae)] on the predation rates of third-instar Chrysoperla carnea Stephens (Chrysopidae: Neuroptera) and fourth-instar Coccinella septempunctata L. and Hippodamia variegata Goeze (Coccinellidae: Coleoptera) larvae was studied. Although prey species, predator species, prey density, and their interactions all had significant effects on the numbers of aphids consumed, the type of functional response did not vary, remaining a type II response in all treatments. However, the type II parameters differed among predator species on the same prey species, and for each predator species on the two prey species. Chrysoperla. carnea on M. persicae and H. variegata on A. craccivora were more voracious than other predators. In the context of functional response and biological control, the release of these predators, that show inverse density-dependent mortality, has to be started in early season to build up their population on low aphid densities and attack later high aphid populations.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Effects of density-dependent migrations on stability of a two-patch predator-prey model

We consider a predator-prey model in a two-patch environment and assume that migration between patches is faster than prey growth, predator mortality and predator-prey interactions. Prey (resp. predator) migration rates are considered to be predator (resp. prey) density-dependent. Prey leave a patch at a migration rate proportional to the local predator density. Predators leave a patch at a migration rate inversely proportional to local prey population density. Taking advantage of the two different time scales, we use aggregation methods to obtain a reduced (aggregated) model governing the total prey and predator densities. First, we show that for a large class of density-dependent migration rules for predators and prey there exists a unique and stable equilibrium for migration. Second, a numerical bifurcation analysis is presented. We show that bifurcation diagrams obtained from the complete and aggregated models are consistent with each other for reasonable values of the ratio between the two time scales, fast for migration and slow for local demography. Our results show that, under some particular conditions, the density dependence of migrations can generate a limit cycle. Also a co-dim two Bautin bifurcation point is observed in some range of migration parameters and this implies that bistability of an equilibrium and limit cycle is possible.     

Spatially correlated recruitment of a marine predator and its prey shapes the large-scale pattern of density-dependent prey mortality

Patterns of predator dispersal can be critical to the dynamics of prey metapopulations. In marine systems, oceanic currents may shape the dispersal of planktonic larvae of both predators and prey, producing spatial correlations in the recruitment of both species and distinctive geographic patterns of prey mortality. I examined the potential for this phenomenon in two fishes, a wrasse and its grouper predator, at a Caribbean island where the near-shore oceanographic regime produces a temporally consistent spatial pattern of fish recruitment. I found that recruitment and adult abundance of groupers were spatially correlated with recruitment of wrasse prey. Furthermore, the local abundance of predators strongly affected the nature of density-dependent prey mortality. At sites with few predators, wrasse mortality was inversely density-dependent, while mortality was positively density-dependent at sites with higher predator densities. This phenomenon could be important to the dynamics of any metacommunity in which physical forces produce correlated dispersal.     

Density-dependence in the survival and reproduction of Bald Eagles: Linkages to Chum Salmon

During the late 20th Century, due to decreases in both contamination and persecution, bald eagle (Haliaeetus leucocephalus) populations increased dramatically. Currently, mechanisms regulating eagle populations are not well understood. To examine potential regulating processes in the Pacific Northwest, where eagles are no longer primarily regulated by contaminants or direct persecution, we examined bald eagle reproductive success, breeding populations, winter populations, mortality, and salmon stream use. Wintering and breeding eagle populations in south-coastal British Columbia (BC) quadrupled between the early 1980s and the late 1990s, and have since stabilized. Density-dependent declines in reproduction occurred during 1986–2009, but not through changes in site quality. Mid-winter survival was crucial as most mortality occurred then, and models showed that density-dependent reductions in population growth rates were partially due to reduced survival. Wintering eagles in British Columbia fed heavily on chum salmon (Oncorhynchus keta) runs, and then switched to birds in late winter, when mortality was highest. Eagles tended to arrive after the peak in salmon availability at streams in BC as part of a migration associated with salmon streams from Alaska to northern Washington. Eagles were most abundant in southern BC during cold Alaskan winters and in years of high chum salmon availability. We suggest that eagle populations in the Pacific Northwest are currently partially limited by density on the breeding grounds and partially by adult mortality in late winter, likely due to reduced late winter salmon stocks forcing eagles to exploit more marginal prey supplies. Larger eagle populations have affected some local prey populations. © 2011 The Wildlife Society.     

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.     

The impact of mortality on predator population size and stability in systems with stage-structured prey

The relationships between a predator population's mortality rate and its population size and stability are investigated for several simple predator-prey models with stage-structured prey populations. Several alternative models are considered; these differ in their assumptions about the nature of density dependence in the prey's population growth; the nature of stage-transitions; and the stage-selectivity of the predator. Instability occurs at high, rather than low predator mortality rates in most models with highly stage-selective predation; this is the opposite of the effect of mortality on stability in models with homogeneous prey populations. Stage-selective predation also increases the range of parameters that lead to a stable equilibrium. The results suggest that it may be common for a stable predator population to increase in abundance as its own mortality rate increases in stable systems, provided that the predator has a saturating functional response. Sufficiently strong density dependence in the prey generally reverses this outcome, and results in a decrease in predator population size with increasing predator mortality rate. Stability is decreased when the juvenile stage has a fixed duration, but population increases with increasing mortality are still observed in large areas of stable parameter space. This raises two coupled questions which are as yet unanswered; (1) do such increases in population size with higher mortality actually occur in nature; and (2) if not, what prevents them from occurring? Stage-structured prey and stage-related predation can also reverse the 'paradox of enrichment', leading to stability rather than instability when prey growth is increased.     

No evidence of nonlinear effects of predator density,refuge availability,or body size of prey on prey mortality rates

Predator density, refuge availability, and body size of prey can all affect the mortality rate of prey. We assume that more predators will lead to an increase in prey mortality rate, but behavioral interactions between predators and prey, and availability of refuge, may lead to nonlinear effects of increased number of predators on prey mortality rates. We tested for nonlinear effects in prey mortality rates in a mesocosm experiment with different size classes of western mosquitofish (Gambusia affinis) as the prey, different numbers of green sunfish (Lepomis cyanellus) as the predators, and different levels of refuge. Predator number and size class of prey, but not refuge availability, had significant effects on the mortality rate of prey. Change in mortality rate of prey was linear and equal across the range of predator numbers. Each new predator increased the mortality rate by about 10% overall, and mortality rates were higher for smaller size classes. Predator–prey interactions at the individual level may not scale up to create nonlinearity in prey mortality rates with increasing predator density at the population level.     

Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments

Summary Predator-prey studies in semi-arid eastern Australia demonstrated that populations of rabbits (Oryctolagus cuniculus) could be regulated by predators. The functional, numerical and total responses of foxes (Vulpes vulpes) to rabbits and the numerical response of feral cats (Felis catus) to rabbits, are described. Measurement of the rabbit component of foxes' stomach contents indicates a Type III functional response. The size of the fox population in summer was dependent on the availability of rabbits over the immediately preceding rabbit breeding season but there appeared to be no density-dependent aggregation of young foxes in areas of surplus food. The total response of foxes, estimated using the short-term numerical response of dispersing foxes, was directly density-dependent for low rabbit densities and inversely density-dependent for high rabbit densities. Two states are possible with this form of total response: a state with low rabbit densities regulated by predators and a state with high rabbit densities which occurs when rabbits escape predator regulation. The boundary between regulation and non-regulation by predators was demonstrated by a predator-removal experiment. In the treated areas, predators were initially culled and rabbits increased to higher densities than in an untreated area where predators were always present. When predators were allowed back into the treated areas, rabbit populations continued to increase and did not decline to the density in the untreated area. This is the critical evidence for a two-state system. When predators were present, rabbits could be maintained at low densities which were in the density-dependent part of the total response curve for foxes. Exceptionally high rabbit recruitment, or artificially reduced predation, could result in rabbits escaping predator-regulation. Under these circumstances, rabbits could move into the inversely density-dependent region of the total response curve for foxes.     

Seasonal variation in the functional response of a coral-reef piscivore alters the inverse density-dependent mortality of its prey

Density-dependent processes are critical for regulating species’ populations, and piscivory of coral-reef fishes is frequently density dependent. However, the mechanism driving this density-dependent mortality is poorly understood, but may be caused by changes in a predator’s feeding rate at different prey densities (its functional response). An aquarium experiment replicated in winter and summer examined the functional response after 22 and 47 h of Cephalopholis cruentata feeding on Halichoeres pictus. With the exception of summer data after 47 h (density-independent mortality), mortality was inversely density dependent across all prey densities and increased with higher summer temperatures. The absence of an asymptotic pattern of inverse density-dependent mortality was caused by type II (summer) or dome-shaped type IV (winter) functional responses, with the benefits of schooling likely to cause the low mortality rates at higher prey densities. Predators’ functional responses may underlie the inverse density-dependent mortality reported in field studies of aggregating fishes.     

The structure of sculpin populations along a stream size gradient

Synopsis Data on spatial variation of sculpin density, growth and fecundity support the hypothesis that populations of stream fish are structured by changes in risk of predation and prey availability along a gradient in stream size. Cottus bairdi in warm streams and C. cognatus in cold streams exhibit similar patterns. Sculpins in large streams have faster individual growth rates and higher fecundities than those in small streams, but occur at lower density. The patterns appear to be persistent and suggest that predation reduces sculpin density in larger streams. Competitive release, variations in prey productivity, and local factors probably contribute to the variation in sculpin growth.     

Variation in foraging success among predators and its implications for population dynamics

The effects of the expected predation rate on population dynamics have been studied intensively, but little is known about the effects of predation rate variability (i.e., predator individuals having variable foraging success) on population dynamics. In this study, variation in foraging success among predators was quantified by observing the predation of the wolf spider Pardosa pseudoannulata on the cricket Gryllus bimaculatus in the laboratory. A population model was then developed, and the effect of foraging variability on predator–prey dynamics was examined by incorporating levels of variation comparable to those quantified in the experiment. The variability in the foraging success among spiders was greater than would be expected by chance (i.e., the random allocation of prey to predators). The foraging variation was density‐dependent; it became higher as the predator density increased. A population model that incorporates foraging variation shows that the variation influences population dynamics by affecting the numerical response of predators. In particular, the variation induces negative density‐dependent effects among predators and stabilizes predator–prey dynamics.     

Density dependence,prey accessibility and prey depletion by fisheries drive Peruvian seabird population dynamics

In marine ecosystems top predator populations are shaped by environmental factors affecting their prey abundance. Coupling top predators’ population studies with independent records of prey abundance suggests that prey fluctuations affect fecundity parameters and abundance of their predators. However, prey may be abundant but inaccessible to their predators and a major challenge is to determine the relative importance of prey accessibility in shaping seabird populations. In addition, disentangling the effects of prey abundance and accessibility from the effects of prey removal by fisheries, while accounting for density dependence, remains challenging for marine top predators. Here, we investigate how climate, population density, and the accessibility and removal of prey (the Peruvian anchovy Engraulis ringens) by fisheries influence the population dynamics of the largest sedentary seabird community (≈ 4 million individuals belonging to guanay cormorant Phalacrocorax bougainvillii, Peruvian booby Sula variegata and Peruvian pelican Pelecanus thagus) of the northern Humboldt Current System over the past half‐century. Using Gompertz state–space models we found strong evidence for density dependence in abundance for the three seabird species. After accounting for density dependence, sea surface temperature, prey accessibility (defined by the depth of the upper limit of the subsurface oxygen minimum zone) and prey removal by fisheries were retained as the best predictors of annual population size across species. These factors affected seabird abundance the current year and with year lags, suggesting effects on several demographic parameters including breeding propensity and adult survival. These findings highlight the effects of prey accessibility and fishery removals on seabird populations in marine ecosystems. This will help refine management objectives of marine ecosystems in order to ensure sufficient biomass of forage fish to avoid constraining seabird population dynamics, while taking into account of the effects of environmental variability.     

Is there safety‐in‐numbers for prey?

The abundance of prey affects the rate of predation, but little consensus exists on whether this enhances or reduces per capita mortality. Studies of aggregating prey in marine habitats generally emphasise that the probability of predation of any individual is the reciprocal of the number of prey within a school. A field experiment tested the alternative hypotheses that predation by predatory fish on schooling prey (1) increased with an increase in the number of prey per school and that this caused (2) survival to be lower in schools with more individuals. The number of prey (juvenile Acanthochromis polyacanthus ) per school was manipulated in replicate treatments with natural densities of large predatory fish (open plots) and treatments without large predatory fish (exclusion cages). Large predatory fish preyed on juveniles in a density-dependent manner and this was the key source of density-dependent mortality in plots open to all predators. There was some suggestion that small predatory fish also prey on juveniles in a density-dependent manner, but this was weak and did not translate into density-dependent mortality of juveniles. It would appear that aggregation of prey may be a successful strategy against predation from some predators, but not always every predator, or all predators in combination.     

The Effects of Relaxed and Reversed Selection by Predators on the Antipredator Behavior of the Threespine Stickleback, Gasterosteus aculeatus

Isolation from predators can lead to the reduction or loss of ancestral behavioral defenses in prey, but does not always do so. Predators introduced to populations that have experienced relaxed selection from some ancestral predators can favor the evolution of antipredator behavior that has been lost. We examined these possibilities by eliciting antipredator behavior in three populations of threespine stickleback fish, Gasterosteus aculeatus : an oceanic population thought to resemble the ancestral form, and two populations historically (up to 20 000 yr) devoid of piscine predators (relaxed selection), one of which has been stocked with salmonids for nearly 25 yr (reversed selection). We used three kinds of predator models: a sculpin (ambush predator), a rainbow trout (chasing predator), and an overhead silhouette of an arctic tern. Stickleback reacted differently to the three models, indicating that they distinguished among them. Individuals from all populations responded similarly to the tern model. The ancestral population showed the weakest response to the sculpin model despite being the only population that encounters these predators naturally. Stickleback from the trout-free population displayed slightly reduced responses to the trout model, and recovery times like those in the ancestral population providing only weak evidence for loss of the ancestral antipredator repertoire. Fish from the reverse-selected population exhibited fascinating, elevated responses to both the trout and sculpin models relative to the other two populations. These findings offer initial evidence of (1) a partial alteration of the ancestral behavioral repertoire during a long period of relaxed selection from piscine predators, and (2) rapid acquisition of extreme responses to piscine predators under reverse selection.     

Predictable changes in predation mortality as a consequence of changes in food availability and predation risk

Theory predicts that animals will have lower activity levels when either the risk of predation is high or the availability of resources in the environment is high. If encounter rates with predators are proportional to activity level, then we might expect predation mortality to be affected by resource availability and predator density independent of the number of effective predators. In a factorial experiment, we tested whether predation mortality of larval wood frogs, Rana sylvatica, caused by a single larval dragonfly, Anax junius, was affected by the presence of additional caged predators and elevated resource levels. Observations were consistent with predictions. The survival rate of the tadpoles increased when additional caged predators were present and when additional resources were provided. There was no significant interaction term between predator density and food concentration. Lower predation rates at higher predator density is a form of interference competition. Reduced activity of prey at higher predator density is a potential general mechanism for this widespread phenomenon. Higher predation rates at low food levels provides an indirect mechanism for density-dependent predation. When resources are depressed by elevated consumer densities, then the higher activity levels associated with low resource levels can lead to a positive association between consumer density and consumer mortality due to predation. These linkages between variation in behaviour and density-dependent processes argue that variation in behaviour may contribute to the dynamics of the populations. Because the capture rate of predators depends on the resources available to prey, the results also argue that models of food-web dynamics will have to incorporate adaptive variation in behaviour to make accurate predictions.