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Phosphorylated cyclic AMP response element binding protein expression induced in the periaqueductal gray by predator stress: its relationship to the stress experience, behavior and limbic neural plasticity.

Electrophysiological studies in cats and recently in rats implicate neuroplasticity in the periaqueductal gray (PAG) and its afferents in stressor-induced increases in fearful behavior and anxiety-like behavior (ALB). Such increases may model aspects of affective changes following traumatic stress in humans. The present study explored the role of neuroplasticity in PAG and its connection with the central nucleus of the amygdala (ACE) in male rodent anxiety-like response to predator stress. In the first of two studies, the effects of predator stress on the induction of phosphorylated cyclic AMP response element binding protein (pCREB) were investigated. pCREB expression in the PAG and ventromedial hypothalamus (VMH) was examined immunohistochemically. Predator stress increased the degree of pCREB expression in PAG cells (measured densitometrically) but did not increase the number of cells expressing pCREB (measured stereologically). Moreover, predator stress-specific increase in pCREB-like immunoreactivity (lir) was restricted to the right lateral column of the PAG. In addition, pCREB lir in the right lateral column likely reflects aspects of the stress experience because the stressor (cat behavior) and the response to the stressor (rat defensive behavior) are highly predictive of degree of pCREB expression. There was no effect of predator stress on pCREB lir in the VMH. Because pCREB expression has been associated with long-lasting potentiation (LLP) of neural transmission, we examined the effects of predator stress on transmission in the ACE-PAG pathway in a second study. Predator stress elevated evoked potential measures of ACE-PAG transmission in the right hemisphere but not in the left hemisphere 11-12 days after predator stress. This finding is consistent with the longer-lived effects of pharmacological stress on amygdalo-PAG transmission in the right hemisphere but not in the left hemisphere in cats. Of interest is the fact that the same aspects of the stressor experience and reaction to it, which are predictive of the degree of pCREB expression, are also highly predictive of the degree of potentiation of measures of ACE-PAG transmission. Behavioral analyses revealed that the most consistent effects of predator stress are on behavior in the plus maze (open arm exploration and risk assessment) and on startle. In addition, covariance analysis suggests that ACE-PAG potentiation mediates some but not all of the changes in ALB produced by predator stress. Because pCREB expression may be a precursor to neuroplastic changes in certain forms of memory and LLP, the present findings complement studies in the cat, showing that neuroplastic changes in the PAG underlie changes in affect following stress. Furthermore, these findings suggest that neuroplastic changes in PAG may be important mediators of predator stress-induced changes in affective behavior in rodents. Finally, consistent with cat and human studies, the right hemisphere appears particularly important in long-term response to stress.

Animals↗

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.

Animals↗

Interactions in an acarine predator guild: impact on Typhlodromalus aripo abundance and biological control of cassava green mite in Benin, West Africa.

To determine the impact of an acarine predator guild on the abundance of a shared herbivorous prey and its principal exotic predator, a series of surveys were conducted in ca. 200 cassava fields in swamp and non-swamp areas in southwestern Benin, West Africa. For each field, the surveys provided data on the density of a pest arthropod, the cassava green mite Mononychellus tanajoa (Bondar), of an introduced and successfully established natural enemy, the apex-inhabiting predatory mite Typhlodromalus aripo DeLeon, and on occurrence of other predator species that inhabit the leaves and share the same prey. These other predators included one exotic species, Typhlodromalus manihoti Moraes, that is successfully established mainly in swamp areas, and two indigenous species, Euseius fustis (Pritchard and Baker) and Typhlodromalus saltus (Denmark and Matthysse), that are commonly found on cassava in Africa. Our aim was to assess the association between the density of M. tanajoa and that of T. aripo, the most successful predator in terms of establishment and abundance, and subsequently determine how this association was affected by the presence or absence of the other predator species. No obvious density-dependent relationship was found by inspecting the scattergrams of T. aripo versus M. tanajoa densities, but high T. aripo densities did not occur when M. tanajoa densities were low and--during the dry season in February--the densities of M. tanajoa steeply increased when T. aripo numbers were low. Given the establishment of T. aripo in all fields, the presence of other species of predatory mites (T. manihoti, both in swamp and non-swamp areas; T. saltus in absence--as well as presence--of T. manihoti in swamp areas; E. fustis in absence of T. manihoti in non-swamp areas) reduced the density of M. tanajoa by a factor 2-3. Thus in all these cases, the presence of an exotic or indigenous species of predatory mite in addition to T. aripo was associated with lower M. tanajoa density. The density of T. aripo was usually positively affected by the presence of other predator species except for T. saltus in presence of T. manihoti that negatively affected the density of T. aripo in swamp areas, an effect likely mediated by either intraguild predation or competition for food. Path analysis showed that indigenous phytoseiid species were more important in suppression of M. tanajoa populations in cassava fields than previously thought. We suggest that the lack of negative effects of the predator species complex is likely due to differential niche use by the various species which reduces interference among the predators. Manipulative experiments are, however, needed to provide details on the relative importance in M. tanajoa suppression by each species within this acarine predator guild.

Animals↗

High reproductive rates result in high predation risks: a mechanism promoting the coexistence of competing prey in spatially structured populations.

I tested the hypothesis that spatial structure provides a trade-off between reproduction and predation risk and thereby facilitates predator-mediated coexistence of competing prey species. I compared a cellular automata model to a mean-field model of two prey species and their common predator. In the mean-field model, the prey species with the higher reproductive rate (the superior competitor) always outcompeted the other species (the inferior competitor), both in the presence of and the absence of the predator. In the cellular automata model, both prey species, which differed only in their reproductive rates, coexisted for a long time in the presence of their common predator at intermediate levels of predation. At low predation rates, the superior competitor dominated, while high predation rates favored the inferior competitor. This discrepancy in the results of the different models was due to a trade-off that spontaneously emerged in spatially structured populations; that is, the more clustered distribution of the superior competitor made it more susceptible to predation. In addition, coexistence of competing prey species declined with increasing dispersal ranges of either prey or predator, which suggests that the trade-off that results from spatial structure becomes less important as either prey or predator disperse over a broader range.

Animals↗

Predator diet breadth influences the relative importance of bottom-up and top-down control of prey biomass and diversity.

We investigated the effects of predator diet breadth on the relative importance of bottom-up and top-down control of prey assemblages, using microbial food webs containing bacteria, bacterivorous protists and rotifers, and two different top predators. The experiment used a factorial design that independently manipulated productivity and the presence or absence of two top predators with different diet breadths. Predators included a "specialist" predatory ciliate Euplotes aediculatus, which was restricted to feeding on small prey, and a "generalist" predatory ciliate Stentor coeruleus, which could feed on the entire range of prey sizes. Both total prey biomass and prey diversity increased with productivity in the predator-free control and specialist predator treatments, a pattern consistent with bottom-up control, but both remained unchanged by productivity in the generalist predator treatment, a pattern consistent with top-down control. Linear food chain models adequately described responses in the generalist predator treatment, whereas food web models incorporating edible and inedible prey (which can coexist in the absence of predators) adequately described responses in the specialist predator treatment. These results suggest that predator diet breadth can play an important role in modulating the relative strength of bottom-up and top-down forces in ecological communities.

Animals↗

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey.

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.

Animals↗

Hatching responses of subsocial spitting spiders to predation risk.

The carrying of eggs often renders parents vulnerable to predators due to increased conspicuousness or decreased mobility. Nonetheless, egg-carrying parents can escape from the predators to which they are vulnerable. Previous studies have demonstrated heavy predation by spider-eating jumping spiders (Portia labiata) on egg-carrying spitting spider (Scytodes pallida) females, but little predation on eggless females. If the timing of hatching is phenotypically plastic, then both S. pallida females and their eggs could reduce the risk of predation by hatching early. Hence, this study examines the hatching responses of S. pallida to chemical cues from P. labiata, both in the laboratory and in the field, and addresses the following questions. (i) Do cues from predatory P. labiata influence the hatching traits of S. pallida? (ii) Are the olfactory cues from predators sufficient for predator detection by S. pallida ? (iii) Are hatching responses to predatory P. labiata controlled by egg-carrying S. pallida females, or directly by their embryos? The study provides evidence of hatching as a life-history switch point, which shows an adaptive plasticity in response to predation risk in egg-carrying S. pallida. Egg-carrying S. pallida females, but not unattended eggs, adjust egg-hatching time (the interval between oviposition and hatching) in response to the threat of predation on both the female and her eggs by P. labiata. In the presence of P. labiata, eggs that are carried by females hatch sooner; the hatchlings of these eggs are therefore smaller than hatchlings born in the absence of P. labiata. Chemical cues that are released from the draglines of P. labiata are sufficient to elicit changes in the egg-hatching traits of S. pallida. Hatching early in response to this predator may benefit both females and their offspring. To my knowledge, this is the first direct experimental study to demonstrate predator-induced hatching plasticity in spiders and, in particular, in animals with parental care.

Adaptation, Physiological↗

Predator-driven phenotypic diversification in Gambusia affinis.

Predation is heterogeneously distributed across space and time, and is presumed to represent a major source of evolutionary diversification. In fishes, fast-starts--sudden, high-energy swimming bursts--are often important in avoiding capture during a predator strike. Thus, in the presence of predators, we might expect evolution of morphological features that facilitate increased fast-start speed. We tested this hypothesis using populations of western mosquitofish (Gambusia affinis) that differed in level of predation by piscivorous fish. Body morphology of G. affinis males, females, and juveniles diverged in a consistent manner between predatory environments. Fish collected from predator populations exhibited a larger caudal region, smaller head, more elongate body, and a posterior, ventral position of the eye relative to fish from predator-free populations. Divergence in body shape largely matched a priori predictions based on biomechanical principles, and was evident across space (multiple populations) and time (multiple years). We measured maximum burst-swimming speed for male mosquitofish and found that individuals from predator populations produced faster bursts than fish from predator-free populations (about 20% faster). Biomechanical models of fish swimming and intrapopulation morphology-speed correlations suggested that body shape differences were largely responsible for enhanced locomotor performance in fish from predator populations. Morphological differences also persisted in offspring raised in a common laboratory environment, suggesting a heritable component to the observed morphological divergence. Taken together, these results strongly support the hypothesis that divergent selection between predator regimes has produced the observed phenotypic differences among populations of G. affinis. Based on biomechanical principles and recent findings in other species, it appears that the general ecomorphological model described in this paper will apply for many aquatic taxa, and provide insight into the role of predators in shaping the body form of prey organisms.

Analysis of Variance↗

Effects of predation and dispersal on Mastomys natalensis population dynamics in Tanzanian maize fields.

1. We investigate the effects of different levels of predation pressure and rodent dispersal on the population dynamics of the African pest rodent Mastomys natalensis in maize fields in Tanzania. 2. Three levels of predation risk were used in an experimental set-up: natural level (control), excluding predators by nets and attracting avian predators by nest boxes and perch poles. Because dispersal of the rodents could mask the predation pressure treatment effects, control and predator exclusion treatments were repeated with enclosed rodent populations. 3. Population growth during the annual population rise period was faster in the absence of predators and peak population size was higher, but otherwise dynamics patterns were similar for populations where predators had access or were attracted, indicating that compensatory mechanisms operate when rodents are exposed to high levels of predation risk. Reducing dispersal of rodents removed the effect of predation on population growth and peak size, suggesting that local predators may play a role in driving rodent dispersal, but have otherwise little direct effect on population dynamics.

Animals↗

Predator-induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.

Animals↗

Estimation of predation by the larvae of Toxorhynchites splendens on the aquatic stages of Aedes aegypti.

Predation by instars of Toxorhynchites splendens on aquatic stages of Aedes aegypti was studied by estimating functional response parameters such as attack rate (a') and handling time (Th) in the laboratory. The predator displayed typical type-II functional response, similar to that of most insect predators when presented with increasing densities of any given size class of prey. Second instar predator attacked prey significantly at higher rate than the other instars. Small prey were attacked at higher rate than the predation on larger prey. Except second instar predator, other instars showed significant reduction in a' with increase in Th. Foraging surface area did not influence the predation rate. Predation was high at high water temperature and this was more prominent in the second instar predator. However, prey handling time was independent of the water temperature. Modeling of the predation of mixed age populations of prey and the predator through this short-term functional response experiment is discussed.

Aedes↗

Outer membrane changes enable evolutionary escape from bacterial predation.

Antimicrobial resistance (AMR) is a threat to modern medicine. To combat AMR pathogens, natural predators like bacteriophages and predatory bacteria have gained interest recently. Predatory bacterium Bdellovibrio bacteriovorus is ubiquitous and has a broad prey range. It is particularly potent at killing many AMR Gram-negative bacterial pathogens featured on the WHO priority list. However, it is currently unclear whether prey bacteria can evolve genetically-determined resistance against predation by B. bacteriovorus. Here, we show that the model bacterium Escherichia coli K-12 consistently evolves resistance against B. bacteriovorus during experimental evolution. Selection for resistance scaled positively with predation pressure and was widespread after two cycles of predator exposure. Similar to antibiotics, predation resistance was costly, manifesting in a trade-off between predation resistance and fitness in the absence of predators. Genetic analysis combined with proteomics identified mutations that lead to the down-regulation of the outer membrane porin OmpF as a common resistance mechanism. In addition, a rarer mutation in cell envelope lipopolysaccharide-modifying enzyme WaaF also conferred predation resistance, likely by a pleiotropic effect, which included OmpF down regulation. While our study uncovers evolutionary and mechanistic aspects of prey escape from predation, it also highlights that the high cost of resistance reflects a handicap for the pathogen and can thus be exploited to increase treatment sustainability. Altogether, our work generates essential knowledge in ecologically important predator-prey interactions and can advance predatory bacteria as "living antibiotics" to combat AMR.

Bdellovibrio bacteriovorus↗

Leopard predation and primate evolution.

Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai; forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.

Adaptation, Physiological↗

What happens when predators do not completely consume their prey?

A mathematical model is presented for the dynamics of predator-prey interactions when predators do not consume prey (or clumps of prey) in their entirety. Using a combination of analytical and numerical methods, I demonstrate that predator-mediated changes in the distribution of intact and partially consumed prey can affect the outcome of competition between predators in unexpected ways. In come cases, two predators can coexist on a single prey species owing to tradeoffs between the ability to consume prey completely and other competitive abilities. In other cases, predators exhibit frequency-dependent dynamics in which the first predator to occupy the habitat can prevent the other from invading. Conditions for stable coexistence usually expand if the larger predator scatters uneaten prey parts, if prey renewal includes both small and large items, or if the predator with the smaller retrieval capacity is poor at catching intact prey relative to the other predator.

Animals↗

The effects of habitat fragmentation on persistence of source-sink metapopulations in systems with predators and prey or apparent competitors.

We consider systems with one predator and one prey, or a common predator and two prey species (apparent competitors) in source and sink habitats. In both models, the predator species is vulnerable to extinction, if productivity in the source is insufficient to rescue demographically deficient sink populations. Conversely, in the model with two prey species, if the source is too rich, one of the prey species may be driven extinct by apparent competition, since the predator can maintain a large population because of the alternative prey. Increasing the rate of predator movement from the source population has opposite effects on prey and predator persistence. High emigration rate exposes the predator population to danger of extinction, reducing the number of individuals that breed and produce offspring in the source habitat. This may promote coexistence of prey by relaxing predation pressure and apparent competition between the two prey species. The number of sinks and spatial arrangement of patches, or connectivity between patches, also influence persistence of the species. More sinks favor the prey and fewer sinks are advantageous to the predator. A linear pattern with the source at one end is profitable for the predator, and a centrifugal pattern in which the source is surrounded by sinks is advantageous to the prey. When the dispersal rate is low, effects of the spatial structure may exceed those of the number of sinks. In brief, productivity in patches and patterns of connectivity between patches differentially influence persistence of populations in different trophic levels.

Animals↗

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore.

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.

Adaptation, Physiological↗

On the density-dependence of seed predation in Dipteryx micrantha, a bat-dispersed rain forest tree.

We studied the effect of seed density on seed predation by following the fate of bat-dispersed Dipteryx micrantha (Leguminosae) seeds deposited under bat feeding roosts. The study was conducted in Cocha Cashu biological station, Amazonian Peru, during the fruiting period of Dipteryx. Predation of Dipteryx seeds in the area is mainly by large to medium-sized rodents. Seed deposits beneath bat feeding roosts were monitored for a 13-week period in an 18-ha study area. A total of 210 seed deposits were found, and on average, seed predators encountered 22% of them during any one week. About one-third of the seed deposits escaped predation, and those deposits that had relatively few seeds were more likely to go unnoticed by rodents than were deposits with many seeds. The mean seed destruction rate was 8% per week; deposits with many seeds tended to lose a smaller proportion of their seeds to seed predators than did deposits with few seeds. Regression tests for the weekly data showed that, at the beginning of the observation period, seed predation was not density-dependent. Later, when the total seed crop beneath roosts was high, the number of seeds predated per deposit was positively density-dependent, while the proportion of seeds predated was negatively density-dependent, indicating predator satiation. Seed deposits that had been visited by seed predators once had a higher probability of being revisited the week after, especially if they contained many seeds when first encountered. This indicates that the foraging behavior of rodents may be affected by their remembering the location of seed-rich patches.

Animals↗

Multiple predator effects result in risk reduction for prey across multiple prey densities.

Investigating how prey density influences a prey's combined predation risk from multiple predator species is critical for understanding the widespread importance of multiple predator effects. We conducted experiments that crossed six treatments consisting of zero, one, or two predator species (hellgrammites, greenside darters, and creek chubs) with three treatments in which we varied the density of mayfly prey. None of the multiple predator effects in our system were independent, and instead, the presence of multiple predator species resulted in risk reduction for the prey across both multiple predator combinations and all three levels of prey density. Risk reduction is likely to have population-level consequences for the prey, resulting in larger prey populations than would be predicted if the effects of multiple predator species were independent. For one of the two multiple predator combinations, the magnitude of risk reduction marginally increased with prey density. As a result, models predicting the combined risk from multiple predator species in this system will sometimes need to account for prey density as a factor influencing per-capita prey death rates.

Analysis of Variance↗