Assess Predation Risk Research Articles

When good animals love restored habitat in bad neighborhoods: ecological traps for eastern cottontails in agricultural landscapes

Large-scale restoration programs have been implemented worldwide to counteract habitat loss and fragmentation from expansion and intensification of agriculture. These agri-environment programs create habitat patches imbedded in an agricultural matrix. The assumption is these patches benefit wildlife and that individuals either avoid agricultural fields or use them to increase their fitness. We selected eastern cottontails (Sylvilagus floridanus) as a focal species on restored grasslands in Illinois, USA to assess survival and to determine if maladaptive habitat selection for agricultural fields could create an ecological trap. We also investigated whether a mismatch between real and perceived predation risk could explain their habitat selection. We radiotracked 95 cottontails and estimated habitat-specific survival using known-fate models, and measured habitat selection using Manly’s standardized selection ratios. We also assessed perceived predation risk with giving-up density experiments. Survival of cottontails was higher in restored grasslands relative to agricultural and developed areas. Habitat selection did not reflect this spatial variation in mortality risk, however, when crops were present on the landscape. Agricultural lands created an equal-preference trap. Cottontails did not accurately assess predation risk; they did not recognize that agricultural fields were risky. This mismatch could be due to cottontails’ emphasis on protecting themselves from avian predators rather than from coyotes (Canis latrans), which currently are their main predator. Our novel study demonstrates how dynamic landscape context can create ecological traps. Such unexpected outcomes can reduce the conservation benefits of restoration programs.

Antipredator behaviour of invasive geckos in response to chemical cues from snakes

AbstractAntipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacépède]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat‐sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat‐sensitive to some Australian predacious snakes.

Predation risk assessment based on uncertain information: interacting effects of known and unknown cues.

Predation risk assessment based on uncertain information: interacting effects of known and unknown cues.

What does a butterfly hear? Physiological characterization of auditory afferents in Morpho peleides (Nymphalidae).

Many Nymphalidae butterflies possess ears, but little is known about their hearing. The tympanal membrane of butterflies typically comprises distinct inner and outer regions innervated by auditory nerve branches NII and NIII and their respective sensory organs. Using the Blue Morpho butterfly (Morpho peleides) as a model, we characterized threshold and suprathreshold responses of NII and NIII. Both are broadly tuned to 1-20kHz with best frequencies at 1-3kHz, but NIII is significantly more sensitive than NII. The compound action potentials (CAPs) of both branches increase their first peak amplitudes and areas in response to higher sound levels. NII and NIII differed in their suprathreshold CAP responses to sound frequencies, with stronger responses to 1-3 and 4-6kHz, for NIII and NII respectively; results that are consistent with tympanal membrane mechanics. These results indicate that butterflies are capable of amplitude and frequency discrimination. Both auditory branches responded to playbacks of the flight and calls of predatory birds. We propose that the ears of butterflies, like those of many vertebrate prey such as some rabbits and lizards, function primarily in predator risk assessment.

Predator (Carcinus maenas) nonconsumptive limitation of prey (Nucella lapillus) feeding depends on prey density and predator cue type

Predators often have nonconsumptive effects (NCEs) on prey. For example, upon detection of predator cues, prey can reduce feeding activities to hamper being detected by predators. Previous research showed that waterborne chemical cues from green crabs (Carcinus maenas, predator) limit the dogwhelk (Nucella lapillus, prey) consumption of barnacles regardless of dogwhelk density, even though individual predation risk for dogwhelks decreases with conspecific density. Such NCEs might disappear with dogwhelk density if dogwhelks feed on mussels, as mussel stands constitute better antipredator refuges than barnacle stands. Through a laboratory experiment, we effectively found that crab chemical cues limit the per-capita consumption of mussels by dogwhelks at low dogwhelk density but not at high density. The combination of tactile and chemical cues from crabs, however, limited the dogwhelk consumption of mussels at both dogwhelk densities. The occurrence of such NCEs at both dogwhelk densities could have resulted from tactile cues indicating a stronger predation risk than chemical cues alone. Overall, the present study reinforces the notions that prey evaluate conspecific density when assessing predation risk and that predator cue type affects their perception of risk.

The Scent of Danger: the Impact of Predator Chemical Cues on Emergence from Refuge and Willingness to Autotomize Limbs in the House Cricket (Acheta domesticus)

Prey can accurately assess predation risk via the detection of chemical cues and take appropriate measures to survive encounters with predators. Research on the chemical ecology of terrestrial invertebrate predator-prey interactions has repeatedly found that direct chemical cues can alter prey organisms’ antipredator behavior. However, much of this research has focused on the chemical mediation of avoidance and immobility by cues from lycosid spiders neglecting other prominent invertebrate predators and behavior such as autotomy. In our study, house crickets (Acheta domesticus) were exposed to cues from cricket-fed orange-footed centipedes (Cormocephalus aurantiipes), red-back spiders (Latrodectus hasselti), an odorous (cologne) control, and a non-odorous control to determine whether direct chemical cues had any influence on two types of anti-predatory behavior: the willingness (latency) to emerge from a refuge and to autotomize limbs. Exposure to C. aurantiipes cues resulted in a significantly slower emergence from a refuge, but exposure to L. hasselti cues did not. Direct chemical cues had no influence on initial autotomy, but exposure to L. hasselti cues did significantly decrease the latency to autotomize a second limb. That cues from L. hasselti had an influence on a second autotomy, but not initial autotomy may be because crickets that undergo autotomy for a second time may perceive themselves to be already at a higher risk of predation as they were already missing a limb. Variation in responses to cues from different predators demonstrates a need to examine the influence of chemical cues from a wider variety of invertebrate predators on anti-predator behavior.

Sex-based differences in anti-predator response of crickets to chemical cues of a mammalian predator.

Anti-predator behaviors like vigilance or hiding come at the expense of other fitness increasing behaviors such as foraging. To compensate for this trade-off, prey assess predation risk and modify the frequency of anti-predator behaviors according to the likelihood of the threat. In this study, we tested the ability of house crickets (Acheta domesticus) to indirectly assess predation risk via odors from a mammalian predator, Elliot’s short-tailed shrew (Blarina hylophaga). As natural differences in encounter rates and predation risk differs between sexes, we tested if male and female crickets perceive similar rates of predation risk from the presence of shrew odor measured via anti-predator behavioral response. Crickets were placed in enclosed, cardboard-lined chambers either treated with shrew odor or control, along with a food source. Time until foraging was measured for each individual and compared across treatment and sex. We found that in the presence of shrew odor, female crickets delayed foraging while males showed no response. These results suggest adult crickets can use chemical cues to detect mammalian predators. Furthermore, we demonstrate that female crickets associate greater predation risk from shrew predators than do male crickets, which are more stationary yet acoustically conspicuous. As predation risk potentially differs drastically for each sex, changes to the operational sex ratios of wild cricket populations could be influenced by the identity of the predator community.

Impacts of sea star predation on mussel bed restoration

Predation by sea stars has the potential to cause elevated levels of mortality in reestablished populations of bivalves relative to levels of recruitment. Recent efforts to restore beds of the nearly extirpated green‐lipped mussel within the Hauraki Gulf, New Zealand, resulted in high abundances of sea stars occupying those beds and it is unknown whether predation poses a potential limitation to the success of restoration in this bivalve species. The contribution of predation by sea stars to the mortality of mussels across four experimental mussel beds over a 2‐year period was estimated using data from regular assessments of sea star abundance and an experimentally determined consumption rate of sea stars upon mussels. In addition, the potential size selection of mussels by sea stars was assessed to determine if large sea stars selected for recent settlers. Sea stars' abundance within the mussel beds grew to an average of 0.57 sea stars/m2 within 9 months, remaining at similar levels throughout the study. These predominantly large sea stars were estimated to have consumed 30.1% of the mussels over a 25‐month period, representing a contribution of 40.4% of the mussel mortality. Sea stars predominantly selected for larger mussels, and their predation likely contributes little to any lack in mussel recruitment. Sea star predation is clearly a limiting factor on the survival of transplanted adult mussels and the present study highlights the need to continually assess predation risk to determine if remediation is necessary for the persistence of the restored beds.

Antipredator response of pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch

To escape from predators, herbivorous prey could leave their current patch and relocate to an alternative patch. However, when other predators are present on the new patch, prey are again exposed to predation risk. Thus, patch leaving might be affected by the other predators. We studied patch leaving of pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in response to ladybird larvae Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on broad bean Vicia faba L. shoots that were offered as patches for aphids. We tested whether shoot leaving was affected by the presence of predators on alternative shoots under laboratory conditions. Odors from alternative shoots were evaluated as possible cues used by aphids to assess predation risk on the shoots. We exposed aphids to odors from alternative shoots with conspecifics plus either adult or larval ladybirds or larval green lacewings Mallada desjardinsi Navas (Neuroptera: Chrysopidae). Shoot leaving was reduced only when adult ladybirds were present on the alternative shoots compared with controls (i.e., no predators on the alternative shoots). Odors of both adult ladybirds and of conspecifics being attacked by ladybird larvae were required for reduced leaving. Hence, predation risks on current and alternative patches might affect the antipredator responses of aphids.

Comparing the antipredator behaviour of two sympatric, but not syntopic, Liolaemus lizards

The microhabitat preferences of prey animals can modulate how they perceive predation risk, and therefore, their antipredator behaviour. We tested under standardized conditions how microhabitat preferences of two Liolaemus lizards affected their responses when confronted with two types of ambush predators (raptor vs. snake), under two levels of predation risk (low vs. high). These lizard species are sympatric, but not syntopic; L. chiliensis basks on bushes, a complex microhabitat that may provide protection against visual predators, while L. nitidus prefers open microhabitats, basking on the top of large bare rocks, highly exposed to visual predators. If microhabitat complexity modulates the antipredator response, L. chiliensis may perceive lower predation risk, exhibiting lower intensity of antipredator responses than L. nitidus. Both species reduced their activity after being exposed to both predators, but lizards differed in the assessment of predation risk; L. nitidus reduced its activity independently of the predation risk experienced, while L. chiliensis only reduced its activity in the high-risk condition. The microhabitat preferences shaped during the evolution of these species seem to modulate their perception of predation risk, which may cause interspecific differences in the associated costs of their antipredator responses.

A Shift in Escape Strategy by Grasshopper Prey in Response to Repeated Pursuit

We used grasshoppers as a model organism to examine the response of prey to repeated approach from a persistent predator (human observer). We randomly assigned adult Chortophaga australior (Southern Greenstriped Grasshopper) to either low- or highrisk treatments. For both groups, we approached each grasshopper during 15 consecutive encounters and recorded the distance fled (DF) and overall flight path. We approached grasshoppers assigned to the low-risk treatment after a 30-second delay upon landing between each escape flight. Those in the high-risk treatment were approached immediately upon landing and given no opportunity to recover. Grasshoppers assigned to the low-risk treatment exhibited an erratic, or protean flight path to evade detection and traveled shorter distances across consecutive encounters. Those in the high-risk treatment exhibited longer escape flights that were more commonly oriented directly away from the approach of the observer. The results of our study provide additional evidence that prey may shift escape strategies in response to real-time assessment of predation risk.

Social security: are socially connected individuals less vigilant?

Group size effects, whereby animals allocate less time to antipredator vigilance as a function of increasing numbers of animals foraging together, are reported in many taxa, but group size is but one of many social attributes that could increase an individual's perception of predation risk or what might be referred to as a ‘sense of security’. Indeed, meta-analyses suggest that group size only explains a small amount of variation in vigilance, and studies have shown that other social attributes, such as dominance status, also influence perceived risk and time allocated to vigilance. Social network analysis is an emerging technique to quantify a variety of specific social attributes, some of which have been suggested to influence ‘security’. Using the proportion of time looking as an indicator of vigilance and predation risk assessment, we tested the prediction that more socially connected yellow-bellied marmots, Marmota flaviventer, look less while foraging compared to their less socially connected counterparts. For females and males separately, we used observational data to create intrasexual, weighted social networks. We used principal component analysis to reduce correlated measures to unrelated and independent descriptions of connectedness. Using linear mixed effect models to account for potentially confounding variables, we found that no social network measure explained variation in vigilance. Social group size explained variation in female vigilance after accounting for variation due to vegetation height and date. Foraging group size and vegetation height explained variation in male vigilance. While social network measures themselves were not significant, our results mirror the fact that yellow-bellied marmots live in female-dominated societies and suggest that overall social group size is relatively more important for females than for males. Systematically studying whether and how social factors and intrasexual social relationships influence antipredator behaviour in other animals will create a better understanding of the benefits of sociality.

Social security: social relationship strength and connectedness influence how marmots respond to alarm calls

Individuals vary in the number and types of social relationships they maintain. If beneficial, social relationships may reduce predation risk and thus increase an individual’s sense of security. We tested this hypothesis by studying the responses of female yellow-bellied marmots (Marmota flaviventer) to broadcast alarm calls from unfamiliar individuals. First, we quantified affiliative interactions of animals in the field to calculate a set of social network measures. Because attributes of sociality are often correlated, we used principal component analysis to reduce our social network metrics to two unrelated factors and used the social network measure that accounted for the most variance for each principal component in further analyses. We then quantified the change in time allocated to vigilance and foraging following alarm call playback from baseline levels to the first 30 s and the second 30 s period (i.e., 31–60 s) following playback. We expected that if marmots with strong affiliative relationships felt more secure, they would forage more and allocate less time to vigilance after their immediate vigilance response to the broadcast alarm calls. Using mixed effects models that controlled for variation explained by a number of biologically important covariates and permutation tests to test the significance of social network variables, we found that marmots with a higher incloseness allocated significantly more time to vigilance in both the first and second 30 s after hearing a novel alarm call. Additionally, and while not significant (the observed parameter estimate fell between the 90 and 95% CI), marmots with a higher outstrength increased foraging in the second 30 s after hearing a novel alarm call. If we assume that time allocated to foraging is a measure of security, then marmots with strong affiliative relationships reacted more to an alarm call from a novel individual and seemingly felt more secure than their counterparts. Our results, therefore, suggest that strong social relationships increase perceptions of security and illustrate an effect of social relationships on predation risk assessment. In many species, including humans, there are benefits from maintaining good social relationships. These benefits include better health and greater longevity. We studied yellow-bellied marmots, a ground-dwelling squirrel that is notable because it has variable social relationships. Capitalizing on this social variation, we found that marmots that maintain strong affiliative relationships with other marmots may indeed forage more after hearing an artificially broadcast alarm call than marmots with weaker affiliative relationships. This result suggests that marmots that are more socially connected with others in their group may feel relatively more secure, possibly because they have others that can help them assess risk, and that a benefit of maintaining strong friendly social ties is that it permits animals to forage more. Thus, we suggest a new way that social relationships can be beneficial: they increase perceptions of security and this ultimately may facilitate foraging.

Stress responses to conspecific visual cues of predation risk in zebrafish.

Chemical communication relating to predation risk is a trait common among fish species. Prey fish under threat of predation can signal risk to conspecific fish, which then exhibit defensive responses. Fish also assess predation risk by visual cues and change their behavior accordingly. Here, we explored whether these behavioral changes act as visual alarm signals to conspecific fish that are not initially under risk. We show that shoals of zebrafish (Danio rerio) visually exposed to a predator display antipredator behaviors. In addition, these defensive maneuvers trigger antipredator reactions in conspecifics and, concomitantly, stimulate the hypothalamus-pituitary-interrenal axis, leading to cortisol increase. Thus, we conclude that zebrafish defensive behaviors act as visual alarm cues that induce antipredator and stress response in conspecific fish.

Rural-Urban Differences in Escape Behavior of European Birds across a Latitudinal Gradient

Behavioral adjustment is a key factor that facilitates species’ coexistence with humans in a rapidly urbanizing world. Because urban animals often experience reduced predation risk compared to their rural counterparts, and because escape behaviour is energetically costly, we expect that urban environments will select for increased tolerance to humans. Many studies have supported this expectation by demonstrating that urban birds have reduced flight initiation distance (FID = predator-prey distance when escape by the prey begins) than rural birds. Here we advanced this approach and, for the first time, assessed how 32 species of birds, found in 92 paired urban-rural populations, along a 3,900 km latitudinal gradient across Europe, changed their predation risk assessment and escape strategy as a function of living in urban areas. We found that urban birds took longer than rural birds to be alerted to human approaches, and urban birds tolerated closer human approach than rural birds. While both rural and urban populations take longer to be aware of an approaching human as latitude increased, this behavioral change with latitude is more intense in urban birds (for a given unit of latitude, urban birds increased their distance more than rural birds). We also found that as mean alert distance was shorter, urban birds escaped more quickly from approaching humans, but there was no such a relationship in rural populations. Although both rural and urban populations tended to escape more quickly as latitude increased, urban birds delayed their escape more at low latitudes when compared with rural birds. These results suggest that urban birds in Europe live under lower predation risk than their rural counterparts. Furthermore, the patterns found in our study indicate that birds prioritize the reduction of on-going monitoring costs when predation risk is low. We conclude that splitting escape variables into constituent components may provide additional and complementary information on the underlying causes of escape. This new approach is essential for understanding, predicting, and managing wildlife in a rapidly urbanizing world.

Predator Cues Reduce American Beaver Use of Foraging Trails

Herbivores must balance energy needs with avoiding risks, using various cues to assess predation risk. The American beaver (Castor canadensis) is a semi-aquatic herbivore vulnerable to predation on land by wolves (Canis lupis). We tested the use of wolf urine as a potential tool to reduce human-beaver confl icts. We used infrared cameras to monitor use of terrestrial foraging trails by beavers during food cache construction in Seney National Wildlife Refuge, Michigan, from September to November 2008. Two foraging trails at 15 colonies (30 total trails) were monitored for 1 week to establish baseline use. One trail from each colony was then treated with wolf urine, and all trails were monitored an additional week to estimate changes in trail use. Mean number of beavers detected decreased 95% on urine- treated trails and was unchanged on untreated trails. Beavers also spent 95% less time on urine-treated trails as estimated by photograph time stamps, but did not change time spent on untreated trails. Sixteen other taxa of wildlife were detected; however, avoidance of urine-treated trails was not observed in these taxa. Species richness increased with urine treatment, mostly due to increased visitation by carnivores. Beavers appear to use olfaction to assess predation risk on land. Wolf urine may be a suitable deterrent for beaver herbivory.

Does Cohistory Constrain Information Use? Evidence for Generalized Risk Assessment in Nonnative Prey.

Though prey use a variety of information sources to assess predation risk, evolutionary cohistory with a predator could constrain information use, and nonnative prey might fail to recognize risk from a novel predator. Nonnative prey might instead use generalized risk assessment, relying on general alarm signals from injured conspecifics rather than cues from predators. I tested the influence of shared predator-prey history on information use, comparing responses among three native and four nonnative prey species to chemical cues from a native predator and cues from injured conspecific prey. Nonnative prey demonstrated information generalism: (1) responding stronger to alarm cues released by injured conspecific prey than to cues from predators and (2) responding similarly to alarm cues as to cues from predators consuming injured conspecific prey. By contrast, for native prey, multiple information sources were required to elicit the greatest defense. The influence of other sources of chemical information was not predicted by cohistory with the predator: only one nonnative snail responded to the predator; digestion was important for only two native species; the identity of injured prey was important for all prey; and predator and prey cues contributed additively to prey response. Information generalism, hypothesized to be costly in coevolved interactions, could facilitate invasions as a driver of or response to introduction to novel habitats.

The correlated evolution of antipredator defences and brain size in mammals.

Mammals that possess elaborate antipredator defences such as body armour, spines and quills are usually well protected, intermediate in size, primarily insectivorous and live in simple open environments. The benefits of such defences seem clear and may relax selection on maintaining cognitive abilities that aid in vigilance and predator recognition, and their bearers may accrue extensive production and maintenance costs. Here, in this comparative phylogenetic analysis of measurements of encephalization quotient and morphological defence scores of 647 mammal species representing nearly every order, we found that as lineages evolve stronger defences, they suffer a correlated reduction in encephalization. The only exceptions were those that live in trees-a complex three-dimensional world probably requiring greater cognitive abilities. At the proximate level, because brain tissue is extremely energetically expensive to build, mammals may be trading off spending more on elaborate defences and saving by building less powerful brains. At the ultimate level, having greater defences may also reduce the need for advanced cognitive abilities for constant assessment of environmental predation risk, especially in simple open environments.

The Use of Chemical Cues by Granite Night Lizards (Xantusia henshawi) to Evaluate Potential Predation Risk

Squamate reptiles have highly developed chemosensory systems used to detect both predators and prey. Although the general ability of squamates to assess predation risk using chemical cues is well known, the detail to which squamates can make discriminations concerning risk is largely unexamined. Granite Night Lizards (Xantusia henshawi) are habitat specialists that live in exfoliations of granite boulders in dense populations. We measured the responses of Granite Night Lizards to the scent of a sympatric predator, the Lyre Snake (Trimorphodon lyrophanes), maintained on two different diets (lizard-fed and mouse-fed), as well as a non-predatory snake (the Shovelnose Snake, Chionactis occipitalis) and a blank control. We also evaluated the potential use of conspecific chemical cues to assess predation risk by quantifying the response of lizards to the scent of both calm and stressed conspecifics. We collected scents for both experiments on paper pads, which we then placed at the entrance of a shelter within a testing arena containing a focal lizard. We then used video cameras to record the behavior of focal lizards over a 60-minute period. We found that, compared to the blank control, Night Lizards in the presence of chemical cues from snakes took longer to enter the shelter, spent longer investigating chemical cues, and traveled further before entering the shelter. Lizards also spent longer investigating chemical cues from Lyre Snakes than Shovelnose Snakes. However, there were no significant differences between responses to lizard-fed and mouse-fed Lyre Snake chemical cues. We also found no evidence that lizards use conspecific chemical cues to evaluate predation risk. This study demonstrates that Granite Night Lizards can use chemical cues from their predators to assess predation risk, but further research is needed to assess whether these responses differ based on the diet of the predator.

Risk assessment and predator learning in a changing world: understanding the impacts of coral reef degradation.

Habitat degradation is among the top drivers of the loss of global biodiversity. This problem is particularly acute in coral reef system. Here we investigated whether coral degradation influences predator risk assessment and learning for damselfish. When in a live coral environment, Ambon damselfish were able to learn the identity of an unknown predator upon exposure to damselfish alarm cues combined with predator odour and were able to socially transmit this learned recognition to naïve conspecifics. However, in the presence of dead coral water, damselfish failed to learn to recognize the predator through alarm cue conditioning and hence could not transmit the information socially. Unlike alarm cues of Ambon damselfish that appear to be rendered unusable in degraded coral habitats, alarm cues of Nagasaki damselfish remain viable in this same environment. Nagasaki damselfish were able to learn predators through conditioning with alarm cues in degraded habitats and subsequently transmit the information socially to Ambon damselfish. Predator-prey dynamics may be profoundly affected as habitat degradation proceeds; the success of one species that appears to have compromised predation assessment and learning, may find itself reliant on other species that are seemingly unaffected by the same degree of habitat degradation.