Innate plasticity of a predatory behavior: nonlearned context dependence of avian flush-displays

If a foraging adaptation comprises a signal for sensory exploitationof prey, does the behavior and its use develop through learning,like many foraging behaviors or does it depend on nonlearnedstereotypical motor actions, like many signals for sensory exploitation?We asked whether the visually conspicuous motor pattern of bodypivoting with spread tail and wings used by the painted redstart(Myioborus pictus) to flush insect prey is a nonlearned phenotypictrait. The motion pattern and the increase in these displaysunder branches (context dependence based on physical propertiesof the habitat) help the wild birds in foraging because preythat rest on substrates is visually stimulated, flushed intothe air, and consequently chased in aerial pursuits. In unrewardedconditions in the aviary, both the foraging-experienced adultsand the foraging-naive hand-raised fledglings increased thefrequency of flush-displays at locations with substrates abovebirds, recreating the pattern of foraging observed in adultsin their natural habitats. The results imply that parent–offspringcultural transmission or learning during foraging is not requiredfor the development of both the display motion pattern and theadaptive context-dependent increase in display frequency. Sucha nonlearned context dependence based on physical propertiesof the habitat is remarkable considering that avian foragingcontext-dependent plasticity is often based on learning. Wehypothesize that this innate character of the signals may bea result of evolution to exploit universal properties of visuallytriggered escape behaviors of various insects that are predictablyflushed from their resting sites in the habitat.     

Factors affecting life and death in Serengeti cheetahs: environment, age, and sociality

We examined environmental and social factors affecting reproductivesuccess across a 20-year data set of individually known cheetahson the Serengeti Plains of Tanzania. Because cheetahs are seeninfrequently and are not amenable to mark–recapture techniques,we devised a model to estimate time of death for individualsthat disappeared from our records. We found that males had markedlylower survival than females. Recruitment was negatively affectedby rainfall but positively affected by numbers of Thomson'sgazelles, the cheetahs' chief prey. There was a negative associationbetween recruitment and numbers of lions, demonstrating thatthe high rates of predation observed in previous studies haveimplications for the dynamics of cheetah populations. Recruitmentwas related to mother's age, peaking when she reached 6–7years. Sociality affected survival in two ways. First, adolescentsliving in temporary sibling groups had higher survival thansingletons, particularly males with sisters. Second, adult malesliving in coalitions had higher survival than singletons inperiods when other coalitions were numerous, yet they had lowersurvival when other coalitions were rare. These results corroborateobservations of enhanced prey capture by female adolescentsand antipredator benefits for adolescents in groups, as wellas competitive advantages for adult males in groups. Furthermore,our findings stress the importance of interactions between environmentaland social factors in affecting reproductive success in mammals.     

Cooperatively breeding Arabian babblers call differently when mobbing in different predator-induced situations

Cooperatively breeding Arabian babblers (Turdoides squamiceps) havea repertoire of different calls that they use in predator-induced contexts.We investigated their vocal mobbing behavior in two different predator-inducedsituations. We presented territorial groups of babblers a perched,stuffed owl representing an avian predator and a cat representinga ground predator. Babblers approached in both situations andmobbed the predators with the same two call types. In both predator-inducedsituations their first call was a short, metallic-sounding "tzwick."In response to the cat, babblers continued to primarily usetzwicks. However, in continued response to the owl, the babblersprimarily used long trills. The experiments indicate that differencesin use of two common call types during mobbing provide informationon differences in predator-induced situations, although no calltype per se identified a specific situation. The experiments suggestthat the short tzwicks indicate a higher risk or urgency thantrills and that combinations of both call types may providegraded information about differences in predator-induced situations.The relatively stable groups of these cooperative breeders mighthave favored evolution for using different calls in differentmobbing situations.     

Fathead minnows (Pimephales promelas) learn to recognize chemical stimuli from high-risk habitats by the presence of alarm substance

We exposed fathead minnows (Pimephales promelas) to water fromone of two distinct habitat types (an open water site or a vegetatedcover site in the same stream) that we mixed with either alarmsubstance or a distilled water control. Upon subsequent exposuresto the habitat waters alone, minnows showed a fright responseto the habitat water that they received in conjunction withalarm substance but not to the other habitat water. These resultsindicate that minnows can learn to recognize high-risk habitatsbased on the association of habitat specific chemical cues withalarm substance. The ability to recognize these habitats couldpotentially lower the minnows' risk of predation. These resultsprovide evidence of a long-term benefit to receivers of a chemicalalarm signal.     

Carotenoid status signaling in captive and wild red-collared widowbirds: independent effects of badge size and color

Carotenoid-based plumage ornaments are typically consideredto be sexually selected traits, functioning as honest condition-dependentsignals of phenotypic quality, but few studies have addressedthe function of carotenoid color variation in male contestcompetition. Using two experiments, we investigated the statussignaling function of the variable (ranging from yellow tored) carotenoid throat patch (collar) in the polygynous, sexually dimorphic red-collared widowbird (Euplectes ardens). First,we tested if the red collar functions as a dominance signalby painting spectrometrically controlled collar patches ontothe brown plumage of nonbreeding males and staging dyadic malecontests over food resources. Red-collared males dominatedorange males, which in turn dominated the control brown andnovel blue collars. Red dominance persisted when the collar manipulations were reversed within dyads and also when testedagainst testosterone implanted males. In the second experimentthe collar size and color of breeding males were manipulatedin the field before and after territories were established.All males with enlarged red and most with enlarged orange orreduced red collars obtained territories, whereas most maleswith reduced orange and all with blackened (removed) collarsfailed to establish or retain territories. In addition, amongthe territorial males, those with reduced signals defendedsmaller territories, received more intrusions, and spent moretime in aggressive interactions. Redness and, to a lesser extent,size of the carotenoid ornament both seem to independently indicate male dominance status or fighting ability in male contest competition.     

An enemy of your enemy is your friend: Impact of predators on aggregation behavior of gammarids

Predation pressure may affect many aspects of prey behavior, including forming groups and changes in social interactions. We studied the aggregation behavior of competing gammarids Dikerogammarus villosus and Pontogammarus robustoides (Amphipoda, Crustacea) to check whether they modify their preferences for conspecifics or heterospecifics in response to predator (the racer goby Babka gymnotrachelus) kairomones in the presence or absence of stone shelters (alternative protection source). Both species exhibited preferences toward shelters occupied by conspecifics over empty shelters and conspecifics apart from shelters, suggesting that their aggregation depends not only on habitat heterogeneity, but also on their social interactions. Moreover, gammarids in the presence of shelters (safer conditions) preferred conspecifics over heterospecifics, but predator kairomones made them form aggregations irrespective of species. In the predator presence, P. robustoides increased its aggregation level only in the sheltered conditions, whereas D. villosus exhibited this response only in the absence of shelters, suggesting that this behavior can protect it against predators. Therefore, we tested the antipredator effectiveness of D. villosus aggregations by exposing them to fish predation. Gobies foraged most effectively on immobile single gammarids compared to moving and aggregated individuals. Fish also avoided aggregated prey, confirming the protective character of aggregations. We have demonstrated that the predator presence increases aggregation level of prey gammarids and affects their social behavior by reducing antagonistic interactions and avoidance between competing species. This is likely to affect their distribution and functioning in the wild, where predator pressure is a standard situation.     

The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation

According to current evolutionary theory, advertising traitsthat honestly indicate an organism's genetic quality might becostly to produce or maintain, though the kind of costs involvedin this process are controversial. Recently the immunocompetencehypothesis has proposed that testosterone (T) stimulates theexpression of male sexually selected traits while decreasingimmunocompetence. Even though some recent studies have shownan effect of T on ectoparasite load, the dual effect of thehormone has not been addressed in free-living populations. Herewe report results of an experiment in a free-living populationof the lizard Psammodromus algirus during the mating season.Males implanted with T had larger patches of breeding colorand behaved more aggressively than control males. In T-implantedmales, the increase in number of ticks during the mating seasonwas significantly higher than in control males and this negativelyaffected several hematological parameters. T-males sufferedsignificantly higher mortality than control males during theexperiment The results from the manipulation of T are consistentwith the dual effect of this hormone.     

Predation, sensitivity, and sex: why female black rhinoceroses outlive males

Among sexually dimorphic, polygynous mammals, adult femalestend to outlive males and respond more strongly to predatorsthan males. We asked whether a monomorphic, polygynous speciesvirtually immune to predation due to large size (black rhinoceros,Diceros bicornis) conforms to this pattern. Data on 193 interactionswith lions (Panthera leo) and spotted hyenas (Crocuta crocuta)in two nonhabituated populations in Namibia studied from 1991to 1993 revealed that: (1) females were more vigilant or aggressivethan males to either of the potential predators; and (2) whethersolitary or with calves, females attacked more often than males.Although solitary females tended to be more aggressive to lionsthan to hyenas, neither females with calves or males seemedto discriminate between the two carnivores. We also simulatedthe behavior of human predators (poachers) during 69 encounterswith rhinoceroses. While both sexes abandoned local sites becauseof our presence, females ran farther than males, covering upto 40 km in a day. These findings implicate a behavioral mechanismto explain why secondary sex ratios favor females - males aremore prone to human predation, a prediction consistent withdata from 12 populations throughout Africa. Black rhinocerosesappear to be an unanticipated exception to the well-establishedpattern of male-biased mortality in polygynous mammals; in theabsence of intense human predation (a recent event), male mortalityfails to exceed that of females, suggesting that intrasexualcompetition in a polygynous mammal: may not be the primary causeof unbalanced secondary sex ratios. Our results on the causesof sex differences in mortality and in responsiveness to differentpredators reinforce the relevance of behavioral ecology to conservation;such information is necessary for planning how best to minimizenegative human influences on the few remaining wild Africanrhinos.     

Tail-flagging and other antipredator signals in white-tailed deer: new data and synthesis

We present a series of predictions concerning the costs andbenefits of antipredator behavior in ungulates and then testthem with data on white-tailed deer reacting to a human on foot.Costs of tail-flagging were apparently low and no data supportedthe idea that flagging serves as a warning signal to conspecifics,in either this or in other studies. Flagging deer fled at greaterspeeds than nonflaggers, indicating that flagging could possiblysignal prey's ability to escape. Dropping the tail at the endof the flight may additionally have made deer inconspicuous.Snorting did not appear directed at conspecifics, and comparativedata suggest that it signals that the predator has been detected.In contrast, foot-stamping was effective in alerting other deerto the observer's presence. Deer may have bounded to clear obstaclesalong their flight path. These preliminary data indicate thatseveral aspects of antipredator behavior in white-tailed deermay be pursuit-deterrent signals, and they therefore highlightthe necessity of observing natural predators' reactions to signalsgiven by deer in future studies.     

Deciphering the diet of a wandering spider (Phoneutria boliviensis; Araneae: Ctenidae) by DNA metabarcoding of gut contents

Arachnids are the most abundant land predators. Despite the importance of their functional roles as predators and the necessity to understand their diet for conservation, the trophic ecology of many arachnid species has not been sufficiently studied. In the case of the wandering spider, Phoneutria boliviensis F. O. Pickard‐Cambridge, 1897, only field and laboratory observational studies on their diet exist. By using a DNA metabarcoding approach, we compared the prey found in the gut content of males and females from three distant Colombian populations of P. boliviensis. By DNA metabarcoding of the cytochrome c oxidase subunit I (COI), we detected and identified 234 prey items (individual captured by the spider) belonging to 96 operational taxonomic units (OTUs), as prey for this wandering predator. Our results broaden the known diet of P. boliviensis with at least 75 prey taxa not previously registered in fieldwork or laboratory experimental trials. These results suggest that P. boliviensis feeds predominantly on invertebrates (Diptera, Lepidoptera, Coleoptera, and Orthoptera) and opportunistically on small squamates. Intersex and interpopulation differences were also observed. Assuming that prey preference does not vary between populations, these differences are likely associated with a higher local prey availability. Finally, we suggest that DNA metabarcoding can be used for evaluating subtle differences in the diet of distinct populations of P. boliviensis, particularly when predation records in the field cannot be established or quantified using direct observation.     

Asymmetric larval mobility and the evolutionary transition from siblicide to nonsiblicidal behavior in parasitoid wasps

The widespread evolution of gregarious development in parasitoidwasps presents a theoretical challenge because the conditionsunder which larval tolerance can spread in an intolerant populationare very stringent (the individual fitness of larvae developingtogether must increase with clutch size). Recent empirical workhas suggested that gregarious development can arise throughthe loss of larval mobility rather than through the gain oftolerant behavior. Using analytical genetic models, we exploredwhether decreased mobility presents a less stringent route togregariousness than the gain of tolerance. Reduced mobilitycan spread under a wide range of conditions. The critical conditionfor the spread of immobility is much less stringent than thatfor larval tolerance. In contrast with previous models of tolerance,the criterion for the spread of a rare immobility allele isindependent of any bias in the sex ratio and the likelihoodof single sex broods. Superparasitism increases the stringencyof the criterion for the spread of immobility, whereas doublekilling relaxes the criterion. Tolerance can subsequently replaceimmobility if there is any cost to the retention of fightingability. Our results suggest that asymmetric larval mobilitymay explain many instances of the evolution of gregarious development.     

The kinds of traits involved in male--male competition: a comparison of plumage, behavior, and body size in quail

I compared the role of ornate plumage, behavior, and body sizeduring male—male competition in two species of New Worldquail. Gambel's quail (Callipepla gambelii) is a highly ornateand dichromatic species, whereas scaled quail (C. squamata)is unornamented and monochromatic. During paired contests betweenunfamiliar males, high rates of testosterone-mediated behaviors(tidbitting, calling) and large body size (mass, tarsus, andtail length) corresponded to winners. In the highly ornate Gambel's quail, male head plumes also influenced the outcomeof contests. Plume enhancement made Gambel's quail more likelyto win contests, whereas plume removal made males more likelyto lose. Plume position also reflected male status. Winningmales erected plumes, whereas losers frequently flattened them.Some plumage ornaments, such as belly patches, did not playa primary role during male contests. Unlike static ornaments,head plumes are highly modifiable and likely signal immediateinformation regarding a male's intent, similar to a coverablebadge. Combined, intrasexual selection favored dynamic traits(fast display rates, modifiable ornaments) and static traits(body size) as indicators of male condition or motivation.In scaled quail only, male size was favored both by male—malecompetition and female choice. Accordingly, the degree of sizedimorphism (tarsus length) is greater in scaled than in Gambel'squail. The frequency of overt aggression (chases, pecks, displacement)also differed between species. Gambel's quail were very aggressive,and subordinates often challenged their opponents. In contrast, scaled quail were less aggressive, and subordinates rarely disputedrank. Interspecific comparison indicated differences in themaintenance of male status and possibly in the honesty of signaling.Both appear to be related to differences in social system.     

Experiments and a model examining learning in the area-restricted search behavior of ferrets (Mustela putorius furo)

Area-restricted searches have been described as important componentsof the foraging behavior of many organisms. It is unclear, however,whether individual foragers can use learning to fine-tune theirsearches, or even whether these searches are efficiently performed.I used a simulation model to make qualitative predictions aboutsearch behavior in a laboratory system. The simulation modelindicates that the sinuosity and path length of searches stronglyaffect search efficiency. The model predicts that, for a rate-maximizingforager, path length should increase and search sinuosity shoulddecrease as prey become less clumped. Foraging animals may thereforebe selected to learn the path length and sinuosity of searchesin response to changing degrees of dumping of prey. These predictionswere tested in a laboratory system involving ferrets (Mustelaputorius furo) foraging for oil-drop "prey items." Search pathschanged in a graded manner to experimental manipulations ofthe dumping of prey. As predicted by the model, ferrets learnedto perform longer and less sinuous search paths as prey becameless clumped. This study provides the first evidence that area-restrictedsearch behavior is learned and can be fine-tuned to efficientlyexploit different spatial distributions of food.     

A cure for the plague of parameters: constraining models of complex population dynamics with allometries

A major goal of ecology is to discover how dynamics and structure of multi-trophic ecological communities are related. This is difficult, because whole-community data are limited and typically comprise only a snapshot of a community instead of a time series of dynamics, and mathematical models of complex system dynamics have a large number of unmeasured parameters and therefore have been only tenuously related to real systems. These are related problems, because long time-series, if they were commonly available, would enable inference of parameters. The resulting ‘plague of parameters’ means most studies of multi-species population dynamics have been very theoretical. Dynamical models parametrized using physiological allometries may offer a partial cure for the plague of parameters, and these models are increasingly used in theoretical studies. However, physiological allometries cannot determine all parameters, and the models have also rarely been directly tested against data. We confronted a model of community dynamics with data from a lake community. Many important empirical patterns were reproducible as outcomes of dynamics, and were not reproducible when parameters did not follow physiological allometries. Results validate the usefulness, when parameters follow physiological allometries, of classic differential-equation models for understanding whole-community dynamics and the structure–dynamics relationship.     

Integrating disparate datasets to model the functional response of a marine predator: A case study of harbour porpoises in the southern North Sea

1. Quantifying consumption and prey choice for marine predator species is key to understanding their interaction with prey species, fisheries, and the ecosystem as a whole. However, parameterizing a functional response for large predators can be challenging because of the difficulty in obtaining the required data on predator diet and on the availability of multiple prey species.
2. This study modeled a multi‐species functional response (MSFR) to describe the relationship between consumption by harbour porpoises (Phocoena phocoena) and the availability of multiple prey species in the southern North Sea. Bayesian methodology was employed to estimate MSFR parameters and to incorporate uncertainties in diet and prey availability estimates. Prey consumption was estimated from stomach content data from stranded harbour porpoises. Prey availability to harbour porpoises was estimated based on the spatial overlap between prey distributions, estimated from fish survey data, and porpoise foraging range in the days prior to stranding predicted from telemetry data.
3. Results indicated a preference for sandeels in the study area. Prey switching behavior (change in preference dependent on prey abundance) was confirmed by the favored type III functional response model. Variation in the size of the foraging range (estimated area where harbour porpoises could have foraged prior to stranding) did not alter the overall pattern of the results or conclusions.
4. Integrating datasets on prey consumption from strandings, predator foraging distribution using telemetry, and prey availability from fish surveys into the modeling approach provides a methodological framework that may be appropriate for fitting MSFRs for other predators.

     

Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues

The ability to accurately assess local predation risk is criticalto prey individuals, as it allows them to maximize threat-sensitivetrade-offs between predator avoidance and other fitness relatedactivities. A wide range of taxonomically diverse prey (includingmany freshwater fishes) relies on chemical alarm cues (alarmpheromones) as their primary information source for local riskassessment. However, the value of chemical alarm cues has beenquestioned due to the availability of additional sensory inputs(i.e., visual cues) and the lack of an overt antipredator responseunder conditions of low perceived risk. In this paper, we testthe hypothesis that chemical alarm cues at concentrations belowthe point at which they elicit an overt behavioral responsefunction to increase vigilance towards other sensory modalities(i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammuserythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide(the putative Ostariophysan alarm pheromone) did not exhibitan overt antipredator response in the absence of secondary visualcues (not different than the distilled water control). However,when exposed to the sight of a visually alarmed conspecific,they significantly increased the intensity of their antipredatorresponse (not different from shoals exposed to the suprathresholdalarm cue). This study demonstrates that prey may benefit fromresponding to low concentration alarm cues by increasing vigilancetowards secondary cues during local risk assessment, even inthe absence of an overt behavioral response. By increasing vigilancetowards secondary risk assessment cues in the presence of alow risk chemical cue, individuals are likely able to maximizethe threat-sensitive trade-offs between predator avoidance andother fitness related activities.     

Unexpected Effects of Predators Upon Their Prey: The Case of the American Alligator

Indirect trophic effects play important roles in ecosystem dynamics and can at times oppose and dominate the action of direct feeding linkages. Each predator directly exerts a negative effect upon its prey, but predators may also provide indirect benefits to their prey. In ecosystems, such benefits are effected via indirect trophic pathways that can provide a more than compensating positive influence. The ecosystem of the Big Cypress National Preserve (southwest Florida) appears to contain an unusually high number of such predators—most notably, the American alligator, Alligator mississippiensis. The trophic exchanges of carbon among the 68 principal taxa comprising the cypress wetland ecosystem have been quantified during both wet and dry seasons. The network analysis program IMPACTS identified predators that potentially have a positive influence on some of their prey. A total of 64 of these instances were recorded for the wet season and 44 for the dry. Taxa that, on balance, have positive effects upon their prey include fishes, turtles, snakes, birds, and, most significantly, alligators. The feeding habits of alligators benefit a conspicuous number (11) of their prey (invertebrates, frogs, mice, and rats). Further trophic analysis reveals that the predation by alligators on snakes and turtles accounts for most of the trophic benefits bestowed. The actions of alligators in modifying their physical environment has been cited elsewhere as contributing to the maintenance of biotic diversity. It appears that the trophic influence of this species adds further evidence to the important role it plays in the functional ecology of the cypress wetland. Received 4 March 1998; accepted 21 October 1998     

Sharks shape the geometry of a selfish seal herd: experimental evidence from seal decoys

Many animals respond to predation risk by forming groups. Evolutionary explanations for group formation in previously ungrouped, but loosely associated prey have typically evoked the selfish herd hypothesis. However, despite over 600 studies across a diverse array of taxa, the critical assumptions of this hypothesis have remained collectively untested, owing to several confounding problems in real predator–prey systems. To solve this, we manipulated the domains of danger of Cape fur seal (Arctocephalus pusillus pusillus) decoys to provide evidence that a selfish reduction in a seals'' domain of danger results in a proportional reduction in its predation risk from ambush shark attacks. This behaviour confers a survival advantage to individual seals within a group and explains the evolution of selfish herds in a prey species. These findings empirically elevate Hamilton''s selfish herd hypothesis to more than a ‘theoretical curiosity’.     

Vigilance and its complex synchrony in the red-necked pademelon, Thylogale thetis

Several adaptive functions, including gaining information fromother group members and detecting predators, are generally ascribedto vigilance in groups of animals subject to predation. Moststudies of the effects of neighbors on vigilance have focusedon individual vigilance. We investigated the effects of neighborson vigilance in wild red-necked pademelons Thylogale thetisforaging at night in nonpersistent aggregations in a clearingin rain forest. Neither the total number of pademelons in theclearing nor the numbers at various distances around focal individualsaffected the individual vigilance of focal animals. However,focal animals’ individual vigilance did change with thedistance to their nearest neighbor and also with distance tocover. Pairs of individuals closer than 10 m apart tended tosynchronize their bouts of individual vigilance and foraging.The degree of synchrony within pairs increased with both distanceto cover and the total number of pademelons foraging in thearea and decreased with increasing distance to the pair's nearestneighbor but did not vary with the distance separating the membersof the pair. Thus, despite their individual vigilance beingunaffected by the number of other pademelons in the feedingaggregation, pademelons were nonetheless sensitive to the presenceof conspecifics and adjusted their behavior in relation to theirseparation from neighbors. Thus, some vigilance benefits maybe obtained from the presence of conspecifics even in speciesthat aggregate only temporarily on food patches without formingmore permanent social groups.