Behavioural Response of Bats to Perceived Predation Risk While Foraging

The ability to detect and respond to predation risk while foraging may have important fitness consequences for prey organisms. Anti‐predator behaviours may reduce the probability of mortality because of predation, but they may also be associated with reduced foraging efficiency. Several behaviours of bats have been suggested to serve as anti‐predator responses, and there is evidence that predation, particularly by avian predators such as owls, may be an important cause of bat mortality. Previous studies have attempted to determine whether predator presence affects bat behaviour when emerging from roost sites, but few have examined effects of predator presence on bat behaviour while foraging. In this study, we investigated whether foraging bats respond to predator cues by presenting bats with an acoustic cue simulating the presence of an owl. Within matched trials, which were conducted at different locations each of 18 nights, significantly fewer bat detections were recorded at owl playback stations than at control stations (no auditory cue), suggesting an avoidance response by bats. An acoustic control (i.e. station playing woodpecker calls), however, did not have significantly more detections than the stations playing the owl calls, suggesting that bats may simply be avoiding noise and more detailed investigation is warranted. Although evidence for owl predation on bats is minimal in North America, results of this study may indicate that the perceived presence of owls may represent a factor influencing the behaviour of bats while foraging.     

Predation by squirrel monkeys and double-toothed kites on tent-making bats

Central American squirrel monkeys (Saimiri oerstedi) appear to recognize the modified leaves that phyllostomid bats utilize for diurnal roost sites. The monkeys visually and manually search these bat tents for both bats and insects. Adult males are the most successful at capturing bats. Nonvolant juvenile bats are more vulnerable to monkey predation than are adults. Bats that escape monkey predation frequently are captured by doubletoothed kites (Harpagus bidentatus) that tend foraging troops of monkeys. Predation by squirrel monkeys, coupled with that of double-toothed kites, may be a significant source of mortality for tent-making bats.     

Airport noise disturbs foraging behavior of Japanese pipistrelle bats

The expansion of anthropogenic noise poses an emerging threat to the survival and reproductive success of various organisms. Previous investigations have focused on the detrimental effects of anthropogenic noise on the foraging behavior in some terrestrial and aquatic animals. Nevertheless, the role of airport noise in impairing foraging activities of most wild animals has been neglected. Here, we aimed to assess whether foraging behavior in free‐living Japanese pipistrelle bats (Pipistrellus abramus) can be disturbed by airport noise. We used audio recording to monitor foraging activities of bats at 11 sites around the runway of a municipal airport. We quantified noise level and spectra, aircraft activity, habitat type, nightly temperature, wind speed, and moon phase for each site. The analysis revealed that noise level and aircraft activity were significant negative predictors for the number of bat passes and feeding buzzes around the runway, even after controlling for the effects of other environmental factors. There was no marked spectral overlap between bat echolocation pulses and airport noise in the presence and absence of low‐flying aircraft. The spectro‐temporal parameters of echolocation vocalizations emitted by bats were dependent on noise level, aircraft activity, and habitat type. These results provide correlative evidence that airport noise can reduce foraging activities of wild pipistrelle bats. Our findings add to the current knowledge of adverse impacts of airport noise on foraging bats in artificial ecosystems and provide a basis for further research on the mechanisms behind noise pollution near airports.     

Lunar Philia in a Nocturnal Primate

The influence of moonlight on behavior has been well documented for many nocturnal mammals, including rodents, lagomorphs, badgers and bats. These studies have consistently shown that nocturnal mammals respond to bright moonlight by reducing their foraging activity, restricting their movement, and reducing their vocalizations. Lunar phobia among nocturnal mammals is generally believed to be a form of predator avoidance: numerous studies indicate that predation increases during moonlit nights. A study I conducted at Tangkoko Nature Reserve in Sulawesi, Indonesia, demonstrates that spectral tarsiers, (Tarsius spectrum), are not lunar phobic, but are lunar philic; they become more active during full moons. During full moons, spectral tarsiers increased foraging, decreased resting, increased travel (distance traveled per unit time, nightly path length, and home range size), increased the frequency of group travel and decreased the frequency of olfactory communication. I explore several potential hypotheses to account for the lack of lunar phobia and potential increased risk of predation resulting from this unusual behavior. Two hypotheses that may account for the behavior are that: 1) foraging efficiency increases during full moons and outweighs the increased risk of predation, and 2) predation risk is not greater during full moons. Instead, predation risk increases during new moons.     

Predation by a snake of a flower-visiting bat at parkia nitida (Leguminosae: Mimosoideae)

An observation of a snake catching a bat visiting a capitulum of the chiropterophilous treeParkia nitida is described. The implications of predator avoidance on the behavior of pollinators and hence on cross-pollination are discussed. Fear of predation may be the reason why some bats make only brief visits toParkia capitula.     

Numerical and Functional Responses of Forest Bats to a Major Insect Pest in Pine Plantations

Global change is expected to modify the frequency and magnitude of defoliating insect outbreaks in forest ecosystems. Bats are increasingly acknowledged as effective biocontrol agents for pest insect populations. However, a better understanding is required of whether and how bat communities contribute to the resilience of forests to man- and climate-driven biotic disturbances. We studied the responses of forest insectivorous bats to a major pine defoliator, the pine processionary moth pityocampa, which is currently expanding its range in response to global warming. We used pheromone traps and ultrasound bat recorders to estimate the abundance and activity of moths and predatory bats along the edge of infested pine stands. We used synthetic pheromone to evaluate the effects of experimentally increased moth availability on bat foraging activity. We also evaluated the top-down regulation of moth population by estimating T. pityocampa larval colonies abundance on the same edges the following winter. We observed a close spatio-temporal matching between emergent moths and foraging bats, with bat activity significantly increasing with moth abundance. The foraging activity of some bat species was significantly higher near pheromone lures, i.e. in areas of expected increased prey availability. Furthermore moth reproductive success significantly decreased with increasing bat activity during the flight period of adult moths. These findings suggest that bats, at least in condition of low prey density, exhibit numerical and functional responses to a specific and abundant prey, which may ultimately result in an effective top-down regulation of the population of the prey. These observations are consistent with bats being useful agents for the biocontrol of insect pest populations in plantation forests.     

Trophic structure of frugivorous bats in the Neotropics: emergent patterns in evolutionary history

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Lunar phobia in bats and its ecological correlates: A meta-analysis

Animals show several behavioral strategies to reduce predation risks. Presumably, moonlight avoidance is a strategy used by some nocturnal species to reduce the risk of predation. In bats, some research indicates that foraging activity is negatively correlated with moonlight intensity, a phenomenon better known as lunar phobia. However, the currently available evidence is contradictory because some bat species reduce their activity during nights with more moonlight while the opposite occurs in other species. We quantitatively evaluated the strength and direction of the relationship between moonlight intensity and bat activity using a meta-analysis. We also looked at some ecological correlates of lunar phobia in bats. Specifically, we examined foraging habitat and latitude as potential moderators of the size of the lunar phobia effect. Our results show that, regardless of the method used to evaluate bat activity, the overall relationship between moonlight intensity and bat activity is significant and negative (r = ?0.22). Species foraging on the surface of the water (piscivores and insectivores; r = ?0.83) and forest canopy species (i.e., big frugivores; r = ?0.30) are more affected by moonlight than those with different foraging habitats (understory, subcanopy, open air). Latitude was positively correlated with lunar phobia (r = 0.023). The stronger lunar phobia for bats foraging on the water surface and in the forest canopy may suggest that the risk of predation is greater where moonlight penetrates more easily. The significant effect of latitude as a moderator of lunar phobia suggests that there is a weak geographic pattern, with this phobia slightly more common in tropical bats than in temperate species.     

Phylogeographical, ecological and biological patterns shown by nuclear (ssrRNA and gGAPDH) and mitochondrial (Cyt b) genes of trypanosomes of the subgenus Schizotrypanum parasitic in Brazilian bats

The genetic diversity and phylogeographical patterns of Trypanosoma species that infect Brazilian bats were evaluated by examining 1043 bats from 63 species of seven families captured in Amazonia, the Pantanal, Cerrado and the Atlantic Forest biomes of Brazil. The prevalence of trypanosome-infected bats, as estimated by haemoculture, was 12.9%, resulting in 77 cultures of isolates, most morphologically identified as Trypanosoma cf. cruzi, classified by barcoding using partial sequences from ssrRNA gene into the subgenus Schizotrypanum and identified as T. cruzi (15), T. cruzi marinkellei (37) or T. cf. dionisii (25). Phylogenetic analyses using nuclear ssrRNA, glycosomal glyceraldehyde 3-phosphate dehydrogenase (gGAPDH) and mitochondrial cytochrome b (Cyt b) gene sequences generated three clades, which clustered together forming the subgenus Schizotrypanum. In addition to vector association, bat trypanosomes were related by the evolutionary history, ecology and phylogeography of the bats. Trypanosoma cf. dionisii trypanosomes (32.4%) infected 12 species from four bat families captured in all biomes, from North to South Brazil, and clustered with T. dionisii from Europe despite being separated by some genetic distance. Trypanosoma cruzi marinkellei (49.3%) was restricted to phyllostomid bats from Amazonia to the Pantanal (North to Central). Trypanosoma cruzi (18.2%) was found mainly in vespertilionid and phyllostomid bats from the Pantanal/Cerrado and the Atlantic Forest (Central to Southeast), with a few isolates from Amazonia.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

Effects of stoat's presence and auditory cues indicating its presence on tree seedling predation by meadow voles

Predators may control the impact of herbivores on their plant resources by 1) decreasing herbivore numbers, 2) imposing predation risk affecting foraging behavior. The goal of the present study was to examine the effects of a predator and auditory cues indicating its presence on the rate of tree seedling (Acer rubrum, Betula lenta) consumption by meadow voles (Microtus pennsylvanicus). The first of our experiments involved introduction of a stoat (Mustela erminea) into an enclosed vole population and the second a playback of recordings of vole distress calls, movements of a stoat and its vocalizations. In both experiments we manipulated vegetation cover and the availability of food next to the experimental seedlings to assess the effects of microhabitat under the different risk situations. The results of the first unreplicated experiment suggested an increased rate of seedling predation in the presence of the stoat. Consistent with these results, the playback of predator sounds in the second replicated experiment caused an increased rate of seedling predation compared to control plots with no recordings. A mowed circle around a seedling station, representing increased risk of predation on the voles, decreased seedling consumption. This effect was modest in the playback treatment. We suggest the results to be due to displacement behavior by the voles exposed to prolonged risk and conflicting demands of foraging and avoiding predators. Alternatively, as suggested by the model of Lima and Bednekoff, prolonged risk of predation forced the voles to decrease their levels of vigilance during low‐risk playback breaks. The modest inhibitory effect of cover removal on seedling predation in the playback treatment is consistent with this interpretation. The results confirm recent evidence for trophic cascades mediated by behavioral interactions between predator and prey. They are novel in suggesting that the presence of predation risk can increase the inhibitory effects of consumers on their resources.     

Activity Pattern of the Trawling Phyllostomid Bat,Macrophyllum macrophyllum,in Panamá1

We studied activity patterns of long‐legged bats, Macrophyllum macrophyllum (Phyllostomidae), in the Barro Colorado Nature Monument, Panamá, using radio‐telemetry. Activity of four males and five females equipped with radio‐transmitters were monitored for 4–7 entire nights each between April and July 2002. Bats exhibited maximum activity around dusk and high activity during the night. Males and females foraged for equal amounts of time in continuous flight (mean: 7 min, maximum 1 h) with interspersed resting phases (mean: 15 min, maximum 3 h). Activity of M. macrophyllum was sensitive to several factors. Time of emergence and return to day roost were correlated with time of sunset and sunrise, respectively. Maximum bat activity coincided with high abundance of aerial insects. Finally, heavy rain caused bats to reduce or cease flight activity. Direct observations and field video recordings support the assumption that M. macrophyllum employs two distinct foraging modes: trawling of insects from and capture of aerial insects at low heights above water. Combination of foraging modes gives M. macrophyllum high flexibility and efficiency in prey search. Activity, foraging mode, and morphology, which are similar to trawling bats from other families, distinguish M. macrophyllum from all other phyllostomid species and grant it access to open habitat above water, a habitat no other phyllostomid bat has conquered.     

Infection reduces anti‐predator behaviors in house finches

Infectious diseases can cause host mortality through direct or indirect mechanisms, including altered behavior. Diminished anti‐predator behavior is among the most‐studied causes of indirect mortality during infection, particularly for systems in which a parasite's life‐cycle requires transmission from prey to predator. Significantly less work has examined whether directly‐transmitted parasites and pathogens also reduce anti‐predator behaviors. Here we test whether the directly‐transmitted bacterial pathogen, Mycoplasma gallisepticum (MG), reduces responses to predation‐related stimuli in house finches Haemorhous mexicanus. MG causes conjunctivitis and reduces survival among free‐living finches, but rarely causes mortality in captivity, suggesting a role for indirect mechanisms. Wild‐caught finches were individually housed in captivity and exposed to the following treatments: 1) visual presence of a stuffed, mounted predator (a Cooper's hawk Accipiter cooperii) or control object (a vase or a stuffed, mounted mallard duck Anas platyrhynchos), 2) vocalizations of the same predator and non‐predator, 3) approach of a researcher to enclosures, and 4) simulated predator attack (capture by hand). MG infection reduced anti‐predator responses during visual exposure to a mounted predator and simulated predator attack, even for birds without detectable visual obstruction from conjunctivitis. However, MG infection did not significantly alter responses during human approach or audio playback. These results are consistent with the hypothesis that predation plays a role in MG‐induced mortality in the wild, with reduced locomotion, a common form of sickness behavior for many taxa, as a likely mechanism. Our results therefore suggest that additional research on the role of sickness behaviors in predation could prove illuminating.     

Seasonal Trophic Niche Shift and Cascading Effect of a Generalist Predator Fish

Few studies have examined how foraging niche shift of a predator over time cascade down to local prey communities. Here we examine patterns of temporal foraging niche shifts of a generalist predator (yellow catfish, Pelteobagrus fulvidraco) and the abundance of prey communities in a subtropical lake. We predicted that the nature of these interactions would have implications for patterns in diet shifts and growth of the predator. Our results show significant decreases in planktivory and benthivory from late spring to summer and autumn, whereas piscivory increased significantly from mid-summer until late autumn and also increased steadily with predator body length. The temporal dynamics in predator/prey ratios indicate that the predation pressure on zooplankton and zoobenthos decreased when the predation pressure on the prey fish and shrimps was high. Yellow catfish adjusted their foraging strategies to temporal changes in food availability, which is in agreement with optimal foraging theory. Meanwhile the decrease in planktivory and benthivory of yellow catfish enabled primary consumers, such as zooplankton and benthic invertebrates, to develop under low grazing pressure via trophic cascading effects in the local food web. Thus, yellow catfish shifts its foraging niche to intermediate consumers in the food web to benefit the energetic demand on growth and reproduction during summer, which in turn indirectly facilitate the primary consumers. In complex food webs, trophic interactions are usually expected to reduce the strength and penetrance of trophic cascades. However, our study demonstrates strong associations between foraging niche of piscivorous fish and abundance of prey. This relationship appeared to be an important factor in producing top-down effects on both benthic and planktonic food webs.     

Behaviors of Western Spruce Budworm Moths (Choristoneura occidentalis) as Defences Against Bat Predation

We investigated potential defense behaviors of adult western spruce budworm (Choristoneura occidentalis), a non-auditive lepidopteran, against bat predation. Although western spruce budworm moths started to fly before sunset, earlier than many species of moths, temporal isolation of flying moths from foraging bats was incomplete as moths were most active after sunset once bats were foraging. Flying C. occidentalis were most active close to their host trees, and thus were isolated from some bat activity because vegetation limits foraging by some bats. Moths mostly flew near the tops of trees, an area that may have a high predation pressure from bats. Resting western spruce budworm spent little time fluttering their wings or crawling, behaviors that are used as cues by gleaning bats. The outbreak nature of this species, in which large numbers of moths are active at one time, may allow dilution effects to reduce predation risk.     

Effects of Predation Risk on Vertical Habitat Use and Foraging of Pardosa milvina

Animals face the risk of predation while engaging in regular activities, such as foraging, mate‐seeking, and reproducing. In order to avoid predation, prey can modify behavior to prevent capture. Pardosa milvina may climb in response to chemotactile cues of Hogna helluo, a larger cooccurring wolf spider, to avoid predation. The purpose of this study was to test the effects of the location of predator cues on the climbing response of P. milvina and to test how this antipredator behavior affected foraging success. In experimental arenas, when cues were on the bottom of the containers, P. milvina moved upward, and when cues were on the walls, individuals moved downward. These results suggest that P. milvina respond to H. helluo cues with general avoidance and do not automatically climb in response to the cues. As H. helluo spend most of their time on the ground, P. milvina may avoid predation by spending more time climbing in areas with H. helluo cues. The presence of predator cues significantly decreased foraging by P. milvina. But within the predator cue treatments, climbing ability had no effect on foraging, possibly due to the short height of the feeding arenas. Future studies are needed to determine if climbing by P. milvina in response to cues of H. helluo has direct and indirect negative effects on herbivores in the field.     

Bats as prey of diurnal birds: a global perspective

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Sensory cues of a top‐predator indirectly control a reef fish mesopredator

Behavioural trophic cascades highlight the importance of indirect/risk effects in the maintenance of healthy trophic‐level links in complex ecosystems. However, there is limited understanding on how the loss of indirect top–down control can cascade through the food‐web to modify lower level predator–prey interactions. Using a reef fish food‐web, our study examines behavioural interactions among predators to assess how fear elicited by top‐predator cues (visual and chemical stimuli) can alter mesopredator behaviour and modify their interaction with resource prey. Under experimental conditions, the presence of any cue (visual, chemical, or both) from the top‐predator (coral trout Plectropomus leopardus) strongly restricted the distance swum, area explored and foraging activity of the mesopredator (dottyback Pseudochromis fuscus), while indirectly triggering a behavioural release of the resource prey (recruits of the damselfish Pomacentrus chrysurus). Interestingly, the presence of a large non‐predator species (thicklip wrasse Hemigymnus melapterus) also mediated the impact of the mesopredator on prey, as it provoked mesopredators to engage in an ‘inspection’ behaviour, while significantly reducing their feeding activity. Our study describes for the first time a three‐level behavioural cascade of coral reef fish and stresses the importance of indirect interactions in marine food‐webs.     

Distress Calls of a Fast-Flying Bat (Molossus molossus) Provoke Inspection Flights but Not Cooperative Mobbing

Many birds and mammals produce distress calls when captured. Bats often approach speakers playing conspecific distress calls, which has led to the hypothesis that bat distress calls promote cooperative mobbing. An alternative explanation is that approaching bats are selfishly assessing predation risk. Previous playback studies on bat distress calls involved species with highly maneuverable flight, capable of making close passes and tight circles around speakers, which can look like mobbing. We broadcast distress calls recorded from the velvety free-tailed bat, Molossus molossus, a fast-flying aerial-hawker with relatively poor maneuverability. Based on their flight behavior, we predicted that, in response to distress call playbacks, M. molossus would make individual passing inspection flights but would not approach in groups or approach within a meter of the distress call source. By recording responses via ultrasonic recording and infrared video, we found that M. molossus, and to a lesser extent Saccopteryx bilineata, made more flight passes during distress call playbacks compared to noise. However, only the more maneuverable S. bilineata made close approaches to the speaker, and we found no evidence of mobbing in groups. Instead, our findings are consistent with the hypothesis that single bats approached distress calls simply to investigate the situation. These results suggest that approaches by bats to distress calls should not suffice as clear evidence for mobbing.     

Brevity is prevalent in bat short-range communication

Animal communication follows many coding schemes. Less is known about the coding strategy for signal length and rates of use in animal vocal communication. A generalized brevity (negative relation between signal length and frequency of use) is innovatively explored but remains controversial in animal vocal communication. We tested brevity for short-range social and distress sounds from four echolocating bats: adult black-bearded tomb bat Taphozous melanopogon, Mexican free-tailed bat Tadarida brasiliensis, adult greater horseshoe bat Rhinolophus ferrumequinum, and adult least horseshoe bat Rhinolophus pusillus. There was a negative association between duration and number of social but not distress calls emitted. The most frequently emitted social calls were brief, while most distress calls were long. Brevity or lengthiness was consistently selected in vocal communications for each species. Echolocating bats seem to have convergent coding strategy for communication calls. The results provide the evidence of efficient coding in bat social vocalizations, and lay the basis of future researches on the convergence for neural control on bats’ communication calls.