Balancing food and predator pressure induces chronic stress in songbirds

The never-ending tension between finding food and avoiding predators may be the most universal natural stressor wild animals experience. The 'chronic stress' hypothesis predicts: (i) an animal's stress profile will be a simultaneous function of food and predator pressures given the aforesaid tension; and (ii) these inseparable effects on physiology will produce inseparable effects on demography because of the resulting adverse health effects. This hypothesis was originally proposed to explain synergistic (inseparable) food and predator effects on demography in snowshoe hares (Lepus americanus). We conducted a 2 x 2, manipulative food addition plus natural predator reduction experiment on song sparrows (Melospiza melodia) that was, to our knowledge, the first to demonstrate comparable synergistic effects in a bird: added food and lower predator pressure in combination produced an increase in annual reproductive success almost double that expected from an additive model. Here we report the predicted simultaneous food and predator effects on measures of chronic stress in the context of the same experiment: birds at unfed, high predator pressure (HPP) sites had the highest stress levels; those at either unfed or HPP sites showed intermediate levels; and fed birds at low predator pressure sites had the lowest stress levels.     

Scale Dependence of Female Ungulate Reproductive Success in Relation to Nutritional Condition,Resource Selection and Multi-Predator Avoidance

Female ungulate reproductive success is dependent on the survival of their young, and affected by maternal resource selection, predator avoidance, and nutritional condition. However, potential hierarchical effects of these factors on reproductive success are largely unknown, especially in multi-predator landscapes. We expanded on previous research of neonatal white-tailed deer (Odocoileus virginianus) daily survival within home ranges to assess if resource use, integrated risk of 4 mammalian predators, maternal nutrition, winter severity, hiding cover, or interactions among these variables best explained landscape scale variation in daily or seasonal survival during the post-partum period. We hypothesized that reproductive success would be limited greater by predation risk at coarser spatiotemporal scales, but habitat use at finer scales. An additive model of daily non-ideal resource use and maternal nutrition explained the most (69%) variation in survival; though 65% of this variation was related to maternal nutrition. Strong support of maternal nutrition across spatiotemporal scales did not fully support our hypothesis, but suggested reproductive success was related to dam behaviors directed at increasing nutritional condition. These behaviors were especially important following severe winters, when dams produced smaller fawns with less probability of survival. To increase nutritional condition and decrease wolf (Canis lupus) predation risk, dams appeared to place fawns in isolated deciduous forest patches near roads. However, this resource selection represented non-ideal resources for fawns, which had greater predation risk that led to additive mortalities beyond those related to resources alone. Although the reproductive strategy of dams resulted in greater predation of fawns from alternative predators, it likely improved the life-long reproductive success of dams, as many were late-aged (>10 years old) and could have produced multiple litters of fawns. Our study emphasizes understanding the scale-dependent hierarchy of factors limiting reproductive success is essential to providing reliable knowledge for ungulate management.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Interactions of multiple predators with different foraging modes in an aquatic food web

Top predators can have different foraging modes that may alter their interactions and effects on food webs. Interactions between predators may be non-additive resulting from facilitation or interference, whereas their combined effects on a shared prey may result in emergent effects that are risk enhanced or risk reduced. To test the importance of multiple predators with different foraging modes, we examined the interaction between a cruising predator (largemouth bass, Micropterus salmoides) and an ambush predator (muskellunge, Esox masquinongy) foraging on a shared prey (bluegill sunfish, Lepomis macrochirus) with strong anti-predator defense behaviors. Additive and substitution designs were used to compare individual to combined predator treatments in experimental ponds. The multiple predator interaction facilitated growth of the cruising predator in the combined predator treatments, whereas predator species had substitutable effects on the growth of the ambush predator. The combined predator treatments created an emergent effect on the prey; however, the direction was dependent on the experimental design. The additive design found a risk-reducing effect, whereas the substitution design found a risk-enhancing effect for prey fish. Indirect effects from the predators weakly extended to lower trophic levels (i.e., zooplankton community). Our results highlight the need to consider differences in foraging mode of top predators, interactions between predators, and emergent effects on prey to understand food webs.     

Reproductive success of individuals with different fruit production patterns. What does it mean for the predator satiation hypothesis?

The predator satiation hypothesis states that synchronous periodic production of seeds is an adaptive strategy evolved to reduce the pressure of seed predators. The seed production pattern is crucial to the predator satiation hypothesis, but there are few studies documenting the success of individuals that are in synchrony and out of synchrony with the whole population. This study is based on long-term data on seed production of Sorbus aucuparia and specialised pre-dispersal seed predation by Argyresthia conjugella, in a subalpine spruce forest in the Western Carpathians (Poland). At the population level, we tested whether functional and numerical responses of predators to the variation of fruit production operate. At the individual level, we tested whether individuals with higher interannual variability in their own seed crops and higher synchrony with the population have higher percentages of uninfested fruits. The intensity of pre-dispersal seed predation was high (average 70 %; range 19–100 %). There were both functional and numerical responses of predators to the variation of fruit production at the population level. We found that individuals that were expected to be preferred under seed predator pressure had higher reproductive success. With increasing synchrony of fruit production between individual trees and the population, the percentage of infested fruits decreased. There was also a negative relationship between the interannual variation in individual fruit production and the percentage of infested fruits. These results confirm selection for individuals with a masting strategy. However, the population does not seem well adapted to strong seed predation pressure and we suggest that this may be a result of prolonged diapause of A. conjugella.     

Predation on mutualists can reduce the strength of trophic cascades

Ecologists have put forth several mechanisms to predict the strength of predator effects on producers (a trophic cascade). We suggest a novel mechanism – in systems in which mutualists of plants are present and important, predators can have indirect negative effects on producers through their consumption of mutualists. The strength of predator effects on producers will depend on their relative consumption of mutualists and antagonists, and on the relative importance of each to producer population dynamics. In a meta-analysis of experiments that examine the effects of predator reduction on the pollination and reproductive success of plants, we found that the indirect negative effects of predators on plants are quite strong. Most predator removal experiments measure the strength of predator effects on producers through the antagonist pathway; we suggest that a more complete understanding of the role of predators will be achieved by simultaneously considering the effects of predators on plant mutualists.     

Contrasting mortality in young freshwater leeches and triclads

A guild of leeches and triclads coexist and are the most numerous invertebrate predators on the stony shores of productive British lakes. Populations of all species are food-limited. Mortality of recruited young is considerably higher in leech than in triclad populations, and this paper investigates reasons for this. In particular, the feeding success of young leeches and triclads in relation to prey species, prey size, prey condition (alive or crushed), spatial heterogeneity (with or without the presence of stones or gravel), and the presence or absence of other young or adults predators (leeches or triclads) of the same or different species are investigated in the laboratory. Feeding success by young leeches and triclads on crushed prey without the presence of stones was high, but declined dramatically in leeches but not triclads when stones were present. Young leeches and triclads were inept at capturing live prey, of a small or large size, with the exception of soft-bodied prey such as oligochaetes. Feeding success by young predators on live prey was not increased by the presence of other young predators of the same or different species. With only a few exceptions, the presence of adult leeches, and to a much lesser extent adult triclads, increased the feeding success, growth and survival of young leeches and triclads. It is concluded that the high mortality of young leeches, compared to triclads, in field populations is due to their inability to locate damaged food in an environment with spatial heterogeneity due to a poorly developed chemosensory system. High and low levels of juvenile morality are accompanied by high and low reproductive rates in leech and triclad populations, respectively. It is unusual for a food limited population to have a high level of recruitment, but it is speculated that the characteristically high reproductive output in parasitic leeches, from which predaceous leeches are derived or have affinities, has been retained to counterbalance high juvenile mortality rates.     

Food use is affected by the experience of nest predation: implications for indirect predator effects on clutch size

Indirect predator effects on prey demography include any effect not attributable to direct killing and can be mediated by perceived predation risk. Though perceived predation risk clearly affects foraging, few studies have yet demonstrated that it can chronically alter food intake to an extent that affects demography. Recent studies have used stable isotopes to gauge such chronic effects. We previously reported an indirect predator effect on the size of subsequent clutches laid by song sparrows (Melospiza melodia). Females that experienced frequent experimental nest predation laid smaller clutches and were in poorer physiological condition compared to females not subject to nest predation. Every female was provided with unlimited supplemental food that had a distinctive ¹³C signature. Here, we report that frequent nest predation females had lower blood δ¹³C values, suggesting that the experience of nest predation caused them to eat less supplemental food. Females that ate less food gained less fat and were in poorer physiological condition, consistent with the effect on food use contributing to the indirect predator effect on clutch size. Tissue δ¹⁵N values corroborated that clutch size was not likely constrained by endogenous resources. Finally, we report that the process of egg production evidently affects egg δ¹³C values, and this may mask the source of nutrients to eggs. Our results indicate that perceived predation risk may impose food limitation on prey even where food is unlimited and such predator-induced food limitation ought to be added to direct killing when considering the total effect of predators on prey numbers.     

Linking the green and brown worlds through nonconsumptive predator effects

Predators can indirectly affect lower trophic levels by either consuming their prey (consumptive effect, CE) or by changing the physiology or behavior of their prey (nonconsumptive effect, NCE). Cascading effects of predators on primary producers are common, and can be propagated by CEs, NCEs, or a combination of both mechanisms. Predator impacts in detrital food webs (the ‘brown world’) have received considerably less attention than their effects on systems with primary producers at the base (the ‘green world’), and only recently have we begun to appreciate the importance of above‐ground predators indirectly impacting below‐ground processes. Numerous studies reveal the total impact (CEs and NCEs) of predators in brown food webs, but our understanding of the role of isolated NCEs is limited. Many habitats and major taxa have not been studied, and patterns are difficult to distinguish due to frequent reporting of mixed effects. Predators play an important role as connectors between brown and green worlds when they feed from both food webs (multichannel feeding). We are only beginning to understand how NCEs influence detrital food webs, and it is unknown whether multichannel fear is an essential component of predator–prey ecology that regulates ecosystem function. Synthesis Predators have been shown to impact ecosystems through both consumptive and nonconsumptive effects on their prey Historically, herbivory‐based ‘green’ systems have been the venue for documenting these predator effects, while detritus‐based ‘brown’ systems received considerably less attention. However, similar mechanisms exist in green and brown worlds, suggesting strong parallels. We review and synthesize predator effects in detrital systems, highlighting important shortcomings in current understanding. Furthermore, we build upon the idea of multichannel feeding (i.e. consumption of prey from both green and brown food webs) to propose the existence of ‘multichannel fear’. We provide a framework for documenting multichannel fear to facilitate continued exploration of how predators link seemingly disparate systems.     

Can redistribution of breeding colonies on a landscape mitigate changing predation danger?

The reproductive success of colonially breeding species depends in part upon a trade‐off between the benefit of a dilution effect against nestling predation within larger colonies and colony conspicuousness. However, there may be no net survivorship benefit of dilution if smaller colonies are sufficiently inconspicuous. This raises the question about how the size distribution of breeding colonies on a landscape might change as the predation danger for nestlings changes. In southwest British Columbia, Canada, bald eagle Haliaeetus leucocephalus populations have increased exponentially at ～5% per year in recent decades and prey upon nestlings of colonial breeding great blue herons Ardea herodias faninni. Motivated by field data on reproductive success in relation to colony size, modeling is used to ask under which circumstances trading off a dilution benefit against colony conspicuousness can improve population reproductive success. That is, which colonial nesting distribution, dispersed and cryptic versus clumped and conspicuous, best mitigates predation danger on nestlings? When predators are territorial, the modeling predicts a dispersed nesting strategy as attack rate increases, but not as predator numbers increase. When predators are non‐territorial, the modeling predicts a dispersed nesting strategy as predator numbers and/or attack rates increase. When predators are both territorial and non‐territorial, colonial nesting within a predator's territory improves reproductive success when attack rates are low. This suggests nesting in association with territorial predators may offer decreased levels of predation when compared with nesting amongst non‐territorial predators. Thus a change in the colony size distribution of colonially breeding species might be anticipated on a landscape experiencing a change in predation danger.     

Individual base model of predator-prey system shows predator dominant dynamics

Individual base model of predator-prey system is constructed. Both predator and prey species have age structure and cohorts of early reproductive age have competitive advantage. The model has linear functional response in predation behavior and includes the effect of interference among predators and delay of population growth from resource intake, not by functional response but by calculation procedure. Each foraging action is calculated successively and surplus or scarce of acquired resources is interpreted into population size through individual birth and death. This model shows that biomass of prey killed by predator is dependent on demand of predator and that heterogeneity in predator population is essential in persistency and stability of predator-prey system. Heterogeneity of predator makes predator individuals of less competing ability die rapidly. Rapid death of weak individuals causes rapid decrease of total demand of predator and that makes enough room for survived predators. Therefore, the biomass of killed prey is dependent on predator's demand. As young or infant population of predator are the more vulnerable to shortage of prey, and when many of them cannot survive to reproductive age, they can stabilize the system by wasting excessive prey with only temporal numerical increase of predator population.     

Do phytoseiid mites select the best prey species in terms of reproductive success?

Optimal foraging theory predicts that predators prefer those prey species that are most rewarding in terms of reproductive success, which is dependent on prey quality and prey availability. To investigate which selection pressures may have moulded prey preference in an acarine system consisting of two prey species and three predator species, we tested whether prey preference of the predators is matched by the associated reproductive success.The predators involved areAmblyseius finlandicus (Oudemans),Am. potentillae (Garman) andTyphlodromus pyri Scheuten. The prey species are the apple rust mite (Aculus schlechtendali (Nalepa)) and the fruit-tree red spider mite (Panonychus ulmi (Koch)).Reproductive success was assessed in terms of intrinsic rate of increase and for one predator also in terms of diapause induction. All three predator species reached highest reproductive success on the same prey species: apple rust mite. This was most pronounced for the predatorAm. finlandicus, because its larval stage suffered severe mortality when feeding onP. ulmi.An independent study on prey preference of the three predator species (Dicke et al., 1988) revealed thatAm. finlandicus prefersAc. schlechtendali toP. ulmi, whereas the other two predator species have the reverse preference.Thus, on the basis of current data, prey preference ofAm. finlandicus can be understood in terms of reproductive success. However, this is not so for prey preference ofT. pyri andAm. potentillae. Investigations needed for a better understanding of prey preference of the last-named two predator species are discussed.     

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.     

Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem

Long-term changes in the physical environment in the Antarctic Peninsula region have significant potential for affecting populations of Antarctic krill (Euphausia superba), a keystone food web species. In order to investigate this, we analysed data on krill-eating predators at South Georgia from 1980 to 2000. Indices of population size and reproductive performance showed declines in all species and an increase in the frequency of years of low reproductive output. Changes in the population structure of krill and its relationship with reproductive performance suggested that the biomass of krill within the largest size class was sufficient to support predator demand in the 1980s but not in the 1990s. We suggest that the effects of underlying changes in the system on the krill population structure have been amplified by predator-induced mortality, resulting in breeding predators now regularly operating close to the limit of krill availability. Understanding how krill demography is affected by changes in physical environmental factors and by predator consumption and how, in turn, this influences predator performance and survival, is one of the keys to predicting future change in Antarctic marine ecosystems.     

Plant production and alternate prey channels impact the abundance of top predators

While numerous studies have examined the effects of increased primary production on higher trophic levels, most studies have focused primarily on the grazing food web and have not considered the importance of alternate prey channels. This has happened despite the fact that fertilization not only increases grazing herbivore abundance, but other types of consumers such as detritivores that serve as alternate prey for generalist predators. Alternate prey channels can sustain generalist predators at times when prey abundance in the grazing food web is low, thus increasing predator densities and the potential for trophic cascades. Using arthropod data from a fertilization experiment, we constructed a hierarchical Bayesian model to examine the direct and indirect effects of plant production and alternate prey channels on predators in a salt marsh. We found that increased plant production positively affected the density of top predators via effects on lower trophic level herbivores and mesopredators. Additionally, while the abundance of algivores and detritivores positively affected mesopredators and top predators, respectively, the effects of alternate prey were relatively weak. Because previous studies in the same system have found that mesopredators and top predators rely on alternate prey such as algivores and detritivores, future studies should examine whether fertilization shifts patterns of prey use by predators from alternate channels to the grazing channel. Finally, the hierarchical Bayesian model used in this study provided a useful method for exploring trophic relationships in the salt marsh food web, especially where causal relationships among trophic groups were unknown.     

Optimal foraging when predation risk increases with patch resources: an analysis of pollinators and ambush predators

Pollinators and their predators share innate and learned preferences for high quality flowers. Consequently, pollinators are more likely to encounter predators when visiting the most rewarding flowers. I present a model of how different pollinator species can maximize lifetime resource gains depending on the density and distribution of predators, as well as their vulnerability to capture by predators. For pollinator species that are difficult for predators to capture, the optimal strategy is to visit the most rewarding flowers as long as predator density is low. At higher predator densities and for pollinators that are more vulnerable to predator capture, the lifetime resource gain from the most rewarding flowers declines and the optimal strategy depends on the predator distribution. In some cases, a wide range of floral rewards provides near‐maximum lifetime resource gains, which may favor generalization if searching for flowers is costly. In other cases, a low flower reward level provides the maximum lifetime resource gain and so pollinators should specialize on less rewarding flowers. Thus, the model suggests that predators can have qualitatively different top‐down effects on plant reproductive success depending on the pollinator species, the density of predators, and the distribution of predators across flower reward levels.     

Variation in a sparrow's reproductive success with rainfall: food and predator-mediated processes

From 1997 to 1999, we monitored the reproductive success of individual rufous-crowned sparrows (Aimophila ruficeps) in coastal sage scrub habitat of southern California, USA. Annual reproductive output of this ground-nesting species varied strongly with annual variation in rainfall, attributed to the El Niño-Southern Oscillation. Birds fledged 3.0 young per breeding pair in 1997, when rainfall was near the long-term mean, 5.1 offspring per pair in 1998, a wet El Niño year, and 0.8 fledglings per pair in 1999, a dry La Niña year. Variation in many components of reproductive output was consistent with the hypothesis that food availability was positively correlated with rainfall. However, the factor most responsible for the high reproductive output in 1998 was low early season nest predation which, combined with favorable nesting conditions, enabled more pairs to multiple-brood. Cool, rainy El Niño conditions may have altered the activity of snakes, the main predator of these nests, in the early season of 1998. Overall, more of the annual variation in fecundity was attributable to variation in within-season components of reproductive output (mean number of nests fledged per pair) than to within-nest components (mean brood size). Annual variation in rufous-crowned sparrow fecundity appears to be driven primarily by food resource-mediated processes in La Niña years and by predator-mediated processes in El Niño years.     

Within‐season increase in parental investment in a long‐lived bird species: investment shifts to maximize successful reproduction?

In nest‐building species predation of nest contents is a main cause of reproductive failure and parents have to trade off reproductive investment against antipredatory behaviours. While this trade‐off is modified by lifespan (short‐lived species prioritize current reproduction; long‐lived species prioritize future reproduction), it may vary within a breeding season, but this idea has only been tested in short‐lived species. Yet, life history theory does not make any prediction how long‐lived species should trade off current against future reproductive investment within a season. Here, we investigated this trade‐off through predator‐exposure experiments in a long‐lived bird species, the brown thornbill. We exposed breeding pairs that had no prior within‐season reproductive success to the models of a nest predator and a predator of adults during their first or second breeding attempt. Overall, parents reduced their feeding rate in the presence of a predator, but parents feeding second broods were more risk sensitive and almost ceased feeding when exposed to both types of predators. However, during second breeding attempts, parents had larger clutches and a higher feeding rate in the absence of predators than during first breeding attempts and approached both types of predators closer when mobbing. Our results suggest that the trade‐off between reproductive investment and risk‐taking can change in a long‐lived species within a breeding season depending on both prior nest predation and renesting opportunities. These patterns correspond to those in short‐lived species, raising the question of whether a within‐season shift in reproductive investment trade‐offs is independent of lifespan.     

Multi-predator effects across life-history stages: non-additivity of egg- and larval-stage predation in an African treefrog

The effects of multiple predators on their prey are frequently non‐additive because of interactions among predators. When prey shift habitats through ontogeny, many of their predators cannot interact directly. However, predators that occur in different habitats or feed on different prey stages may still interact through indirect effects mediated by prey traits and density. We conducted an experiment to evaluate the combined effects of arboreal egg‐stage and aquatic larval‐stage predators of the African treefrog, Hyperolius spinigularis. Egg and larval predator effects were non‐additive – more Hyperolius survived both predators than predicted from their independent effects. Egg‐stage predator effects on aquatic larval density and size and age at hatching reduced the effectiveness of larval‐stage predators by 70%. Our results indicate that density‐ and trait‐mediated indirect interactions can act across life‐stages and habitats, resulting in non‐additive multi‐predator effects.     

Effect of scavenging on predation in a food web

Scavenging can have important consequences for food web dynamics, for example, it may support additional consumer species and affect predation on live prey. Still, few food web models include scavenging. We develop a dynamic model that includes two facultative scavenger species, which we refer to as the predator or scavenger species according to their natural scavenging propensity, as well as live prey, and a carrion pool to show ramifications of scavenging for predation in simple food webs. Our modeling suggests that the presence of scavengers can both increase and decrease predator kill rates and overall predation in model food webs and the impact varies (in magnitude and direction) with context. In particular, we explore the impact of the amount of dynamics (exploitative competition) allowed in the predator, scavenger, and prey populations as well as the direction and magnitude of interference competition between predators and scavengers. One fundamental prediction is that scavengers most likely increase predator kill rates, especially if there are exploitative feedback effects on the prey or carrion resources like is normally observed in natural systems. Scavengers only have minimal effects on predator kill rate when predator, scavenger, and prey abundances are kept constant by management. In such controlled systems, interference competition can greatly affect the interactions in contrast to more natural systems, with an increase in interference competition leading to a decrease in predator kill rate. Our study adds to studies that show that the presence of predators affects scavenger behavior, vital rates, and food web structure, by showing that scavengers impact predator kill rates through multiple mechanisms, and therefore indicating that scavenging and predation patterns are tightly intertwined. We provide a road map to the different theoretical outcomes and their support from different empirical studies on vertebrate guilds to provide guidance in wildlife management.