Vision complements echolocation in an aerial-hawking bat

The northern bat Eptesicus nilssonii normally hunts flying insects in the air using frequency-modulated echolocation calls. It is also known to detect and catch visually conspicuous prey (white moths) hovering low among grass stalks. To overcome the problem with acoustic clutter from the grass, which interferes with target echo detection, the bats make use of visual cues in addition to those of echolocation. We therefore investigated the minimum size of prey that the bats could distinguish by using vision, by presenting the bats with different sized dead and spread moths. We found that vision increased the chance of detection only when the moths had a wingspan of at least 5 cm. Smaller targets were detected using echolocation alone. The mean detection range was 3.5 m, suggesting that the bats need a visual acuity of 49 of arc to detect the prey. This is consistent with results of optomotor response tests and counts of retinal ganglion cells in closely related species. Our results suggest that the visual acuity of Eptesicus bats may not be adequate for prey detection under normal conditions, but that the bats can use vision when the prey is unusually large and conspicuous. The northern bats display a flexibility in prey detection techniques not previously recognised among aerial-hawking bats and they are able to use their full visual capacity in the field.     

Echolocation calls of Poey’s flower bat (<Emphasis Type="Italic">Phyllonycteris poeyi</Emphasis>) unlike those of other phyllostomids

Unlike any other foraging phyllostomid bat studied to date, Poey’s flower bats (Phyllonycteris poeyi-Phyllostomidae) emit relatively long (up to 7.2 ms), intense, single-harmonic echolocation calls. These calls are readily detectable at distances of at least 15 m. Furthermore, the echolocation calls contain only the first harmonic, which is usually filtered out in the vocal tract of phyllostomids. The foraging echolocation calls of P. poeyi are more like search-phase echolocation calls of sympatric aerial-feeding bats (Molossidae, Vespertilionidae, Mormoopidae). Intense, long, narrowband, single-harmonic echolocation calls focus acoustic energy maximizing range and favoring detection, which may be particularly important for cruising bats, like P. poeyi, when flying in the open. Flying in enclosed spaces, P. poeyi emit short, low-intensity, frequency-modulated, multiharmonic echolocation calls typical of other phyllostomids. This is the first report of a phyllostomid species emitting long, intense, single-harmonic echolocation calls with most energy in the first harmonic.     

Ignoring the irrelevant: auditory tolerance of audible but innocuous sounds in the bat-detecting ears of moths

Noctuid moths listen for the echolocation calls of hunting bats and respond to these predator cues with evasive flight. The African bollworm moth, Helicoverpa armigera, feeds at flowers near intensely singing cicadas, Platypleura capensis, yet does not avoid them. We determined that the moth can hear the cicada by observing that both of its auditory receptors (A1 and A2 cells) respond to the cicada's song. The firing response of the A1 cell rapidly adapts to the song and develops spike periods in less than a second that are in excess of those reported to elicit avoidance flight to bats in earlier studies. The possibility also exists that for at least part of the day, sensory input in the form of olfaction or vision overrides the moth's auditory responses. While auditory tolerance appears to allow H. armigera to exploit a food resource in close proximity to acoustic interference, it may render their hearing defence ineffective and make them vulnerable to predation by bats during the evening when cicadas continue to sing. Our study describes the first field observation of an eared insect ignoring audible but innocuous sounds.     

Acoustic mirror effect increases prey detection distance in trawling bats

Many different and phylogenetically distant species of bats forage for insects above water bodies and take insects from and close to the surface; the so-called trawling behaviour. Detection of surface-based prey by echolocation is facilitated by acoustically smooth backgrounds such as water surfaces that reflect sound impinging at an acute angle away from the bat and thereby render a prey object acoustically conspicuous. Previous measurements had shown that the echo amplitude of a target on a smooth surface is higher than that of the same target in mid-air, due to an acoustic mirror effect. In behavioural experiments with three pond bats (Myotis dasycneme), we tested the hypothesis that the maximum distances at which bats can detect prey are larger for prey on smooth surfaces than for the same prey in an airborne situation. We determined the moment of prey detection from a change in echolocation behaviour and measured the detection distance in 3D space from IR-video recordings using stereo-photogrammetry. The bats showed the predicted increase in detection distance for prey on smooth surfaces. The acoustic mirror effect therefore increases search efficiency and contributes to the acoustic advantages encountered by echolocating bats when foraging at low heights above smooth water surfaces. These acoustic advantages may have favoured the repeated evolution of trawling behaviour.     

Sound strategy: acoustic aposematism in the bat–tiger moth arms race

The night sky is the venue for an ancient arms race. Insectivorous bats with their ultrasonic sonar exert an enormous selective pressure on nocturnal insects. In response insects have evolved the ability to hear bat cries, to evade their hunting maneuvers, and some, the tiger moths (Arctiidae), to utter an ultrasonic reply. We here determine what it is that tiger moths say to bats. We chose four species of arctiid moths, Cycnia tenera, Euchaetes egle, Utetheisa ornatrix, and Apantesis nais, that naturally differ in their levels of unpalatability and their ability to produce sound. Moths were tethered and offered to free-flying naïve big brown bats, Eptesicus fuscus. The ability of the bats to capture each species was compared to their ability to capture noctuid, geometrid, and wax moth controls over a learning period of 7 days. We repeated the experiment using the single arctiid species E. egle that through diet manipulation and simple surgery could be rendered palatable or unpalatable and sound producing or mute. We again compared the capture rates of these categories of E. egle to control moths. Using both novel learning approaches we have found that the bats only respond to the sounds of arctiids when they are paired with defensive chemistry. The sounds are in essence a warning to the bats that the moth is unpalatable—an aposematic signal.Electronic Supplementary Material  Supplementary material is available for this article at     

Cryptic mammalian species: a new species of whiskered bat (Myotis alcathoe n. sp.) in Europe

The analysis of morphological, behavioural and genetic characters of whiskered bats revealed a new European bat species within the family Vespertilionidae. We describe the morphology, karyology, genetic similarity, ecology and distribution of Myotis alcathoe n. sp. It closely resembles Myotis mystacinus, Myotis brandtii and Myotis ikonnikovi in morphology, but all four species show clear genetic differences in two mitochondrial genes (ND1 and 12S rRNA). Myotis alcathoe n. sp. is the smallest species among the European whiskered bats and uses the highest-frequency echolocation calls of all the European Myotis species. It prefers to hunt in small valleys with deciduous trees and flowing water, which is an endangered habitat. Records from Greece and Hungary indicate a distribution range in south-eastern Europe.     

David and Goliath: potent venom of an ant-eating spider (Araneae) enables capture of a giant prey

It is rare to find a true predator that repeatedly and routinely kills prey larger than itself. A solitary specialised ant-eating spider of the genus Zodarion can capture a relatively giant prey. We studied the trophic niche of this spider species and investigated its adaptations (behavioural and venomic) that are used to capture ants. We found that the spider captures mainly polymorphic Messor arenarius ants. Adult female spiders captured large morphs while tiny juveniles captured smaller morphs, yet in both cases ants were giant in comparison with spider size. All specimens used an effective prey capture strategy that protected them from ant retaliation. Juvenile and adult spiders were able to paralyse their prey using a single bite. The venom glands of adults were more than 50 times larger than those of juvenile spiders, but the paralysis latency of juveniles was 1.5 times longer. This suggests that this spider species possesses very potent venom already at the juvenile stage. Comparison of the venom composition between juvenile and adult spiders did not reveal significant differences. We discovered here that specialised capture combined with very effective venom enables the capture of giant prey.     

Prey detection without successful capture affects spider’s orb-web building behaviour

Animals obtain information from past foraging experience to adjust their foraging activity according to their environment. The ability of spiders to obtain information from unsuccessful predation experiences was investigated by examining the effects on web building, a significant foraging investment, of prey detection without successful capture in the orb-web spider Cyclosa octotuberculata. Four treatments were employed: (1) successful capture and feeding: one syrphid fly was allowed to be captured and consumed by the spider on the web; (2) single prey-item detection: a syrphid fly was placed on the web to lure the spider, but was removed before capture; (3) five prey-item detection: above prey-item detection stimulus was given five times; and, (4) control: neither prey nor feeding on the web. While control spiders decreased the total thread length and capture area of their webs, prey-item detection spiders in both conditions increased them, indicating that the spider obtained information from unsuccessful predation experience to adjust their foraging investment. The fed spiders exhibited a significantly greater increase than the prey-detection-only spiders, suggesting that prey detection alone and prey detection with consumption had different informational effects. Total thread length did not differ between single and five prey-item detection spiders, but distance between two adjacent sticky spirals increased only in the former spiders, possibly because five times unsuccessful predations prevented spiders to reduce web stickiness. It suggests that the spider changed web morphology according to the number of prey detection.     

When attempts at robbing prey turn fatal

Because group-hunting arboreal ants spread-eagle insect prey for a long time before retrieving them, these prey can be coveted by predatory flying insects. Yet, attempting to rob these prey is risky if the ant species is also an effective predator. Here, we show that trying to rob prey from Azteca andreae workers is a fatal error as 268 out of 276 potential cleptobionts (97.1?%) were captured in turn. The ant workers hunt in a group and use the “Velcro?” principle to cling firmly to the leaves of their host tree, permitting them to capture very large prey. Exceptions were one social wasp, plus some Trigona spp. workers and flies that landed directly on the prey and were able to take off immediately when attacked. We conclude that in this situation, previously captured prey attract potential cleptobionts that are captured in turn in most of the cases.     

The functionality of female reciprocal calls in the Iberian midwife toad (<Emphasis Type="Italic">Alytes cisternasii</Emphasis>): female-female acoustic competition?

Female midwife toads (genus Alytes) emit highly variable reciprocal calls of unclear function prior to and during courtship. In some species, female-female competition, expressed as physical fighting, has been reported. Males of Majorcan midwife toads (Alytes muletensis) show phonotactic response to female calls, and females of Iberian midwife toads (Alytes cisternasii) respond differently according to the male call characteristics. In this study, I test the hypothesis of female-female acoustic competition as an additional function of female reciprocal calls. Playback tests indicate that female calls are not clearly involved in female acoustic competition in the Iberian midwife toad, therefore female calls could be directed at males rather than towards competitive females.     

The hunter becomes the hunted: when cleptobiotic insects are captured by their target ants

Here we show that trying to rob prey (cleptobiosis) from a highly specialized predatory ant species is risky. To capture prey, Allomerus decemarticulatus workers build gallery-shaped traps on the stems of their associated myrmecophyte, Hirtella physophora. We wondered whether the frequent presence of immobilized prey on the trap attracted flying cleptoparasites. Nine social wasp species nest in the H. physophora foliage; of the six species studied, only Angiopolybia pallens rob prey from Allomerus colonies. For those H. physophora not sheltering wasps, we noted cleptobiosis by stingless bees (Trigona), social wasps (A. pallens and five Agelaia species), assassin bugs (Reduviidae), and flies. A relationship between the size of the robbers and their rate of capture by ambushing Allomerus workers was established for social wasps; small wasps were easily captured, while the largest never were. Reduviids, which are slow to extract their rostrum from prey, were always captured, while Trigona and flies often escaped. The balance sheet for the ants was positive vis-à-vis the reduviids and four out of the six social wasp species. For the latter, wasps began by cutting up parts of the prey’s abdomen and were captured (or abandoned the prey) before the entire abdomen was retrieved so that the total weight of the captured wasps exceeded that of the prey abdomens. For A. pallens, we show that the number of individuals captured during attempts at cleptobiosis increases with the size of the Allomerus’ prey.     

Armoured spiderman: morphological and behavioural adaptations of a specialised araneophagous predator (Araneae: Palpimanidae)

In a predator–prey system where both intervenients come from the same taxon, one can expect a strong selection on behavioural and morphological traits involved in prey capture. For example, in specialised snake-eating snakes, the predator is unaffetced by the venom of the prey. We predicted that similar adaptations should have evolved in spider-eating (araneophagous) spiders. We investigated potential and actual prey of two Palpimanus spiders (P. gibbulus, P. orientalis) to support the prediction that these are araneophagous predators. Specific behavioural adaptations were investigated using a high-speed camera during staged encounters with prey, while morphological adaptations were investigated using electron microscopy. Both Palpimanus species captured a wide assortment of spider species from various guilds but also a few insect species. Analysis of the potential prey suggested that Palpimanus is a retreat-invading predator that actively searches for spiders that hide in a retreat. Behavioural capture adaptations include a slow, stealthy approach to the prey followed by a very fast attack. Morphological capture adaptations include scopulae on forelegs used in grabbing prey body parts, stout forelegs to hold the prey firmly, and an extremely thick cuticle all over the body preventing injury from a counter bite of the prey. Palpimanus overwhelmed prey that was more than 200% larger than itself. In trials with another araneophagous spider, Cyrba algerina (Salticidae), Palpimanus captured C. algerina in more than 90% of cases independent of the size ratio between the spiders. Evidence indicates that both Palpimanus species possesses remarkable adaptations that increase its efficiency in capturing spider prey.     

Stereotypical rapid source level regulation in the harbour porpoise biosonar

Some odontocetes and bats vary both click intensity and receiver sensitivity during echolocation, depending on target range. It is not known how this so-called automatic gain control is regulated by the animal. The source level of consecutive echolocation clicks from a harbour porpoise was measured with a hydrophone array while the animal detected an aluminium cylinder at 2, 4 or 8?m distance in a go/no-go paradigm. On-axis clicks had source levels of 145–174?dB re 1?μPa peak-to-peak. During target-present trials the click trains reached comparable source levels independent of the range to the target after three clicks. After an additional click, the source level was reduced for the 2 and 4?m trials until it equalled the one-way transmission loss. During target-absent trials, the source level remained high throughout the entire click train. Given typical values of harbour porpoise inter-click intervals, the source level reduction commenced within a few 100?ms from the first click in the click train. This may indicate a sub-cortically regulated source level regulation in the harbour porpoise.     

Reverse positional orientation in a neotropical orb-web spider, <Emphasis Type="Italic">Verrucosa arenata</Emphasis>

Most orb-web spiders face downwards in the web. A downward orientation has been proposed to be the optimal strategy because spiders run faster downwards and thus can catch prey quicker. Consequently, orb-web spiders also extend their web in the lower part, leading to top-down web asymmetry. Since the majority of orb-web spiders face downwards, it has been difficult to test the effect of orientation on prey capture and web asymmetry. In this study, we explored the influence of reverse orientation on foraging efficiency and web asymmetry in Verrucosa arenata, a neotropical orb-web spider that faces upwards in the web. We show that reverse orientation does not imply reverse web asymmetry in this species. V. arenata spiders captured more prey in the lower part of the web but more prey per area on the upper part. The average running speeds of spiders did not differ between upward and downward running, but heavier spiders took longer to capture prey while running upwards. We discuss these findings in the context of foraging efficiency and web asymmetry.     

Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey

Prey-specialised predators have evolved specific cognitive adaptations that increase their prey searching efficiency. In particular, when the prey is social, selection probably favours the use of prey intraspecific chemical signals by predatory arthropods. Using a specialised ant-eating zodariid spider, Zodarion rubidum, which is known to prey on several ant species and possesses capture and venom adaptations more effective on Formicinae ants, we tested its ability to recognise chemical cues produced by several ant species. Using an olfactometer, we tested the response of Z. rubidum towards air with chemical cues from six different ant species: Camponotus ligniperda, Lasius platythorax and Formica rufibarbis (all Formicinae); and Messor structor, Myrmica scabrinodis and Tetramorium caespitum (all Myrmicinae). Z. rubidum was attracted to air carrying chemical cues only from F. rufibarbis and L. platythorax. Then, we identified that the spiders were attracted to airborne cues coming from the F. rufibarbis gaster and Dufour's gland, in particular. Finally, we found that among several synthetic blends, the decyl acetate and undecane mixture produced significant attraction of spiders. These chemicals are produced only by three Formicine genera. Furthermore, we investigated the role of these chemical cues in the communication of F. rufibarbis and found that this blend reduces their movement. This study demonstrates the chemical cognitive capacity of Z. rubidum to locate its ant prey using chemical signals produced by the ants. The innate capacity of Z. rubidum to olfactory detect different ant species is narrow, as it includes only two ant genera, confirming trophic specialisation at lower than subfamily level. The olfactory cue detected by Zodarion spiders is probably a component of the recruitment or trail pheromone.     

Tympanal mechanics and neural responses in the ears of a noctuid moth

Ears evolved in many groups of moths to detect the echolocation calls of predatory bats. Although the neurophysiology of bat detection has been intensively studied in moths for decades, the relationship between sound-induced movement of the noctuid tympanic membrane and action potentials in the auditory sensory cells (A1 and A2) has received little attention. Using laser Doppler vibrometry, we measured the velocity and displacement of the tympanum in response to pure tone pulses for moths that were intact or prepared for neural recording. When recording from the auditory nerve, the displacement of the tympanum at the neural threshold remained constant across frequencies, whereas velocity varied with frequency. This suggests that the key biophysical parameter for triggering action potentials in the sensory cells of noctuid moths is tympanum displacement, not velocity. The validity of studies on the neurophysiology of moth hearing rests on the assumption that the dissection and recording procedures do not affect the biomechanics of the ear. There were no consistent differences in tympanal velocity or displacement when moths were intact or prepared for neural recordings for sound levels close to neural threshold, indicating that this and other neurophysiological studies provide good estimates of what intact moths hear at threshold.     

First evidence of poisonous shrews with an envenomation apparatus

Herein, we report evidence of an envenomation apparatus (EA) in two different species of extinct “giant” shrews, Beremendia and an indeterminate soricine (Mammalia, Eulipotyphla, Soricidae), documented by very well preserved fossil specimens recovered from two Early Pleistocene cave deposits of the Sierra de Atapuerca in Burgos, Spain. The two soricine taxa from Atapuerca have evolved specialized teeth as EAs, which differ from those of recently reported mammals of the Paleocene age, being more similar to the ones described in the modern Solenodon. This discovery reveals the first instance of shrews possessing what appears to be an EA, an evolutionary adaptation that, in these species, was probably related to an increase in body mass and hunting of a larger-sized prey. The Atapuerca specimens would have a highly specialized EA, one of the very few reported for an extinct or living mammal of any time. In addition to the presence of a gutter-like groove along the medial side of the crown of the lower incisors, these two species also present stout jaws and a modified mandibular symphysis with a conspicuous cavity, which in life would likely contain large amounts of connective tissue. The strong mandible architecture of these large shrews would be, in this way, reinforced by a more immovable symphysis, increasing the bite force exerted over a potential prey. This adaptation, together with the grooved incisors, would ensure a rapid and efficient transmission of the poisonous saliva to paralyze relatively large-sized prey.     

Reduced light avoidance in spiders from populations in light-polluted urban environments

Increased urbanisation is leading to a rise in light pollution. Light pollution can disrupt the behaviour and physiology of animals resulting in increased mortality. However, animals may also benefit from artificial light sources, as these may aggregate prey or signal suitable environments. For example, spiders are commonly seen congregating around artificial light sources. Changes in selective pressures engendered by urban environments are driving changes in urban organisms, driving better adaptation to these environments. Here, we ask whether urban populations of the synanthropic spider Steatoda triangulosa show different responses to light compared to rural populations. Egg-sacs from urban and rural populations were collected and incubated in a common garden setting, and the emerging spiderlings tested for light preference. While rural spiderlings avoided light (37% built webs in the light), urban spiderlings were indifferent to it (49% built webs in the light). Reduced light avoidance may benefit spiders through increased prey capture, increased movement into suitable habitats, or due to a release from selection pressure from visually hunting predators which do not enter buildings.     

Female reciprocal calling in the Iberian midwife toad (Alytes cisternasii) varies with male call rate and dominant frequency: implications for sexual selection

Male midwife toads (Alytes cisternasii) responded differently depending on the call frequency and call rate of other males. I tested female Iberian midwife toads with the same set of stimuli used earlier with males. Females responded faster to high call rates, and female vocal activity was greater in response to low-frequency male calls. Thus, in both sexes, the vocal response differs in the same direction according to signal frequency variation, but the magnitude of the response is greater in males than in females. In the light of these results, I discuss the implications for sexual selection of this reciprocal calling.     

Vertebrate diet decreases winter torpor use in a desert marsupial

One of the energetic benefits of daily torpor over prolonged hibernation is that it enables animals to regularly forage and, therefore, replenish food reserves between bouts of torpor. However, little is known about the diet of predators undergoing torpor or whether differences in prey composition among individuals influence torpor characteristics. Here, we test the hypothesis that prey composition affects winter torpor use and patterns of a population of carnivorous marsupial, the brush-tailed mulgara (Dasycercus blythi), in the Great Sandy Desert, Australia. Mulgaras in the study population captured a wide range of prey including vertebrates (mammals, reptiles, birds), seven insect orders, spiders and centipedes. The proportion of vertebrates in the diet was negatively correlated with both frequency of torpor use and maximum bout duration. This variation in torpor use with diet can be explained by the higher energetic content of vertebrates as well as their larger size. Even assuming uniform intake of prey biomass among individuals, those that subsisted on an invertebrate-dominated diet during winter apparently suffered energetic shortages as a result of the scarcity of invertebrate taxa with high energy content (such as insect larvae). Our study is the first to demonstrate a link between diet composition and daily torpor use in a free-ranging mammal.