Nocturnal activity positively correlated with auditory sensitivity in noctuoid moths

We investigated the relationship between predator detection threshold and antipredator behaviour in noctuoid moths. Moths with ears sensitive to the echolocation calls of insectivorous bats use avoidance manoeuvres in flight to evade these predators. Earless moths generally fly less than eared species as a primary defence against predation by bats. For eared moths, however, there is interspecific variation in auditory sensitivity. At the species level, and when controlling for shared evolutionary history, nocturnal flight time and auditory sensitivity were positively correlated in moths, a relationship that most likely reflects selection pressure from aerial-hawking bats. We suggest that species-specific differences in the detection of predator cues are important but often overlooked factors in the evolution and maintenance of antipredator behaviour.     

Light might suppress both types of sound‐evoked antipredator flight in moths

Urbanization exposes wild animals to increased levels of light, affecting particularly nocturnal animals. Artificial light at night might shift the balance of predator–prey interactions, for example, of nocturnal echolocating bats and eared moths. Moths exposed to light show less last‐ditch maneuvers in response to attacking close‐by bats. In contrast, the extent to which negative phonotaxis, moths’ first line of defense against distant bats, is affected by light is unclear. Here, we aimed to quantify the overall effect of light on both types of sound‐evoked antipredator flight, last‐ditch maneuvers and negative phonotaxis. We caught moths at two light traps, which were alternately equipped with loudspeakers that presented ultrasonic playbacks to simulate hunting bats. The light field was omnidirectional to attract moths equally from all directions. In contrast, the sound field was directional and thus, depending on the moth''s approach direction, elicited either only negative phonotaxis, or negative phonotaxis and last‐ditch maneuvers. We did not observe an effect of sound playback on the number of caught moths, suggesting that light might suppress both types of antipredator flight, as either type would have caused a decline in the number of caught moths. As control, we confirmed that our playback was able to elicit evasive flight in moths in a dark flight room. Showing no effect of a treatment, however, is difficult. We discuss potential alternative explanations for our results, and call for further studies to investigate how light interferes with animal behavior.     

Trait independence primes convergent trait loss

The repeated, independent evolution of traits (convergent evolution) is often attributed to shared environmental selection pressures. However, developmental dependencies among traits can limit the phenotypic variation available to selection and bias evolutionary outcomes. Here, we determine how changes in developmentally correlated traits may impact convergent loss of the tympanic middle ear, a highly labile trait within toads that currently lack adaptive explanation. The middle ear's lability could reflect evolutionary trade‐offs with other skull features under selection, or the middle ear may evolve independently of the rest of the skull, allowing it to be modified by active or passive processes without pleiotropic trade‐offs with other skull features. We compare the skulls of 55 species (39 eared, 16 earless) within the family Bufonidae, spanning six hypothesized independent middle ear transitions. We test whether shared or lineage‐specific changes in skull shape distinguish earless species from eared species and whether earless skulls lack other late‐forming skull bones. We find no evidence for pleiotropic trade‐offs between the middle ear and other skull structures. Instead, middle ear loss in anurans may provide a rare example of developmental independence contributing to evolutionary lability of a sensory system.     

Flight and thermoregulation in moths were shaped by predation from bats

Most larger nocturnal moths ("macrolepidoptera") are equipped with ultrasonic tympanic organs (ears), which give them a considerable survival advantage in encounters with echolocating bats. However, 4.2% of the Scandinavian species lack such organs, and are presumably deaf. Our results show that the earless species are larger and have higher wing loadings than the tympanate forms. They also fly with higher body temperatures. They are thus adapted for fast and erratic flight, and may represent an alternative evolutionary pathway to efficient bat defence, but one that is energetically more demanding. We suggest that the tympanic organs in nocturnal moths were key innovations that "released" their bearers from the energetic constraints imposed by a high flight body temperature, necessary to avoid bats, and probably set the stage for subsequent adaptive radiation of slow flying forms.     

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator–prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats'' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths'' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.     

Differential Senescence of Maize Hybrids following Ear Removal : II. Selected Leaf

In conjunction with a study of the effects of ear removal on the senescence of whole maize (Zea mays L.) plants, visual symptoms and associated changes in constituent contents and activities of a selected leaf (first leaf above the ear) were determined. Leaves were sampled from field-grown eared and earless Pioneer brand 3382, B73 × Mo17, and Farm Services brand 854 maize hybrids at nine times during the grainfilling period.

Visual symptoms indicated the following sequence and rate of senescence: earless B73 × Mo17 > earless P3382 » eared B73 × Mo17 » eared P3382 ≤ earless FS854 > eared FS854. All earless hybrids showed increases in leaf dry weight and sugar content; however, the increases were transitory for P3382 and B73 × Mo17, but continuous throughout the grain-filling period for FS854, indicative of continued photosynthetic activity of the latter. All earless hybrids exhibited similar and transitory starch accumulation patterns. Thus, FS854 was an exception to the concept that carbohydrate accumulation accelerates leaf senescence. Ear removal resulted in accelerated losses of reduced N, phosphoenolpyruvate and ribulose bisphosphate carboxylases, phosphorus, chlorophyll, nitrate reductase activity, and moisture for P3382 and B73 × Mo17 plants. In contrast, the loss of all components (except phosphorus) was similar for the selected leaf of earless and eared FS854.

Although the loss of nitrate reductase activity, reduced N, and carboxylating enzymes accurately reflected the development of senescence of the selected leaf, the rate of net loss of reduced N and carboxylating enzymes appeared to be regulated. We deduced that the rate of flux of N into the leaf was a factor in regulating the differing rates of senescence observed for the six treatments; however, we cannot rule out the possibility of concurrent influence of growth regulators or other metabolites.

     

Is food resource partitioning responsible for deviation of echolocation call frequencies from allometry in <Emphasis Type="Italic">Rhinolophus macrotis</Emphasis>?

There is an apparent allometric relationship between peak frequency of echolocation and body size in rhinophilids. However, some rhinolophids deviate from this rule. To date this variation has been explained as a result of partitioning of communication channels. An alternative hypothesis that food resource partitioning results in this divergence in expected frequencies was tested by comparing prey selection between Rhinolophus macrotis Blyth, 1844 and Rhinolophus lepidus Blyth, 1844 in Yunnan Province, China. These two sympatric species are morphologically similar but acoustically divergent: R. macrotis has an echolocation frequency significantly lower than that predicted by the allometric relationship, whereas that of R. lepidus agreed with expectations. Prey selection experiments, conducted in a flight tent, indicated that the dominant prey taxa of R. macrotis were Lasiocampidae, Arctiidae and Noctuidae, whilst that of R. lepidus were Arctiidae, Noctuidae and Ichneumonidae. R. macrotis ate more earless moths and fewer eared moths than R. lepidus, and R. macrotis fed on larger prey in general and captured a wider size range than that captured by R. lepidus. These results confirmed the existence of finely tuned trophic niche differentiation and suggested that food resource partitioning is one of the factors leading to lower peak frequency of calls in R. macrotis.     

Predator detection and evasion by flying insects

Echolocating bats detect prey using ultrasonic pulses, and many nocturnally flying insects effectively detect and evade these predators through sensitive ultrasonic hearing. Many eared insects can use the intensity of the predator-generated ultrasound and the stereotyped progression of bat echolocation pulse rate to assess risk level. Effective responses can vary from gentle turns away from the threat (low risk) to sudden random flight and dives (highest risk). Recent research with eared moths shows that males will balance immediate bat predation risk against reproductive opportunity as judged by the strength and quality of conspecific pheromones present. Ultrasound exposure may, in fact, bias such decisions for up to 24 hours through plasticity in the CNS olfactory system. However, brain processing of ultrasonic stimuli to yield adaptive prey behaviors remains largely unstudied, so possible mechanisms are not known.     

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°–100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat’s pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.     

Auditory changes in noctuid moths endemic to a bat-free habitat

If the ears of moths exist primarily to detect the echolocation calls of hunting bats, endemic moths in bat-free areas (i.e., species that have evolved in the absence of the selection pressure maintaining ears) should exhibit signs of deafness. Noctuid moths from the Pacific islands of French Polynesia, a site that has never possessed bats, were sampled and electrophysiologically analysed to test this hypothesis. The auditory sensitivities of seven endemic and twelve immigrant species, captured from the islands of Tahiti, Moorea, and Hiva Oa, were compared. Both classes possess neurally responsive ears, but endemics are significantly deafer than immigrants at frequencies above 35 kHz. This form of deafness is similar to other moths presumably released from the selection pressure of bat predation. I conclude that endemic moths at this site exhibit preliminary stages of deafness and that, considering their small cellular investment, ears in moths will be lost at a slower rate than more complex sensory organs.     

Whispers from vestigial nubbins: Arrested development provokes trait loss in toads

Despite the use of acoustic communication, many species of toads (family Bufonidae) have lost parts of the tympanic middle ear, representing at least 12 independent evolutionary occurrences of trait loss. The comparative development of the tympanic middle ear in toads is poorly understood. Here, we compared middle ear development among two pairs of closely related toad species in the genera Atelopus and Rhinella that have (eared) or lack (earless) middle ear structures. We bred toads in Peru and Ecuador, preserved developmental series from tadpoles to juveniles, and examined ontogenetic timing and volume of the otic capsule, oval window, operculum, opercularis muscle, columella (stapes), and extracolumella in three‐dimensional histological reconstructions. All species had similar ontogenesis of the otic capsule, oval window, operculum, and opercularis muscle. Moreover, cell clusters of primordial columella in the oval window appeared just before metamorphosis in both eared and earless lineages. However, in earless lineages, the cell clusters either remained as small nubbins or cell buds in the location of the columella footplate within the oval window or disappeared by juvenile and adult stages. Thus, columella growth began around metamorphosis in all species but was truncated and/or degenerated after metamorphosis in earless species, leaving earless adults with morphology typical of metamorphic anurans. Shifts in the timing or expression of biochemical pathways that regulate the extension or differentiation of the columella after metamorphosis may be the developmental mechanism underlying convergent trait loss among toad lineages.     

Moth hearing on the Faeroe Islands, an area without bats

ABSTRACT. The ultrasound-sensitive ears found in several families of moths are believed to be part of a predator (bat) specific defence strategy; the moth's evasive responses, elicited by the calls of bats, reduce its chances of being caught. Bats have never been found on the Faeroe Islands, whereas moths migrated there before the last Ice Age, and have since been isolated from areas with bats. For this reason, the hearing characteristics of moths from the Faeroes are investigated in this study. All noctuid moths caught there have functional ears sensitive to ultrasound. Audiograms are determined for thirty-two individuals of four noctuid species: Cerapteryx gramminis L., Apamea crenata Hūfn., Apamea maillardi Gey. and Diarsia mendica F. The auditory characteristics of the moths from the Faeroes resemble those of moths from other temperate zones where bats are abundant. The audiograms revealed best frequencies between 20 and 45 kHz, relatively broad turnings (Q_10dB around 1), and thresholds of 35–50 dB SPL at the best frequency. The fact that the moths on the Faeroes possess such sensitive ears is explained by the large time spans which might be required for reduction of a character which is not directly opposed by a selection pressure.     

The effects of ear removal on senescence and metabolism of maize

Ears were removed from field grown maize (Zea mays L.) to determine the effects on senescence and metabolism and to clarify conflicting literature reports pertaining to these effects. Ears were removed at three days after anthesis and comparisons were made of changes in metabolism between eared and earless plants until grain of the eared plants matured as judged by black layer formation.     

Predation risk and mating behavior: the responses of moths to bat-like ultrasound

In the presence of predators, animals may reduce or alter theirmating activities. There has been little experimental studyof whether mating behavior varies with the level of predationrisk. Two species of moths, Pseudaletia unipuncta (Noctuidae)and Ostrinia nubilalis (Pyralidae), significantly reduced theirmate-seeking behavior under high levels of simulated predationrisk. Male moths aborted upwind flight in a pheromone plume,and females stopped releasing pheromone in response to soundssimulating the echolocation calls of bats. For O. nubilalis,but not for P. unipuncta, the response varied significantlywith the level of predation risk. Interspecific differencesin behavioral responses likely reflect differences in physiologicalauditory sensitivity and/or behavioral thresholds. Female behavioralresponses to sounds simulating the calls of bats that gleantheir prey from surfaces were significantly weaker than theirresponses to sounds resembling the calls of aerially hawkingbats; these results support the neurophysiological data thatthe calls of gleaning bats are relatively inaudible to moths.This study indicates that some animals can modify their reproductiveactivities in response to auditory cues from predators.     

Bidirectional Echolocation in the Bat Barbastella barbastellus: Different Signals of Low Source Level Are Emitted Upward through the Nose and Downward through the Mouth

The Barbastelle bat (Barbastella barbastellus) preys almost exclusively on tympanate moths. While foraging, this species alternates between two different signal types. We investigated whether these signals differ in emission direction or source level (SL) as assumed from earlier single microphone recordings. We used two different settings of a 16-microphone array to determine SL and sonar beam direction at various locations in the field. Both types of search signals had low SLs (81 and 82 dB SPL rms re 1 m) as compared to other aerial-hawking bats. These two signal types were emitted in different directions; type 1 signals were directed downward and type 2 signals upward. The angle between beam directions was approximately 70°. Barbastelle bats are able to emit signals through both the mouth and the nostrils. As mouth and nostrils are roughly perpendicular to each other, we conclude that type 1 signals are emitted through the mouth while type 2 signals and approach signals are emitted through the nose. We hypothesize that the “stealth” echolocation system of B. barbastellus is bifunctional. The more upward directed nose signals may be mainly used for search and localization of prey. Their low SL prevents an early detection by eared moths but comes at the expense of a strongly reduced detection range for the environment below the bat. The more downward directed mouth signals may have evolved to compensate for this disadvantage and may be mainly used for spatial orientation. We suggest that the possibly bifunctional echolocation system of B. barbastellus has been adapted to the selective foraging of eared moths and is an excellent example of a sophisticated sensory arms race between predator and prey.     

Animal locomotion: a new spin on bat flight

Biologists and engineers have long struggled to understand the hovering flight of insects, birds, and bats. The enormous diversity of these groups would suggest they fly using a variety of mechanisms, but a new study shows that hovering bats use the same aerodynamic mechanisms as do moths and other insects.     

Biomechanical and neurophysiological studies on audition in eared and earless harlequin frogs (Atelopus)

Tissue displacement of various body surfaces and the auditory midbrain sensitivities to sound were measured in Atelopus species with or without a tympanic middle ear (“eared” and “earless”, respectively). Tissue displacement (vibration) of body regions was measured by laser Doppler vibrometer . The body wall directly overlying the lung is most dramatically displaced by sound pressure in all species tested. The otic (lateral head) region showed low displacement in earless species, but significant displacement to high-frequency sound in eared species. Peak tissue displacement of the body wall occurred within the frequency range of each species' advertisement vocalization. Peak tissue displacement of the otic region of the eared species also occurred within these frequencies. Multi-unit neurophysiological recordings of the auditory midbrain (torus semicircularis) also were obtained. Auditory sensitivity curves showed three distinct regions of sensitivity at low, middle, and high frequencies, the latter located within the frequency range of each species' advertisement vocalization. The correlation between auditory midbrain sensitivity and tissue displacement of the body wall region at advertisement vocalization frequencies, suggests that the body wall/lungs serve as the route of sound transfer to the inner ear in earless species and possibly in the eared species as well. Accepted: 4 April 1998     

Bats and moths: what is there left to learn?

Abstract.  Over 14 families of moths have ears that are adapted to detect the ultrasonic echolocation calls of bats. On hearing a bat, these moths respond with an escape response that reduces their chances of being caught. As an evolutionary response, bats may then have evolved behavioural strategies or changes in call design to overcome the moth's hearing. The nature of this interaction is reviewed. In particular, the role of the echolocation calls of bats in the shaping of the structure, neurophysiology and behavioural responses of moths is discussed. Unresolved issues, such as the structural complexity of the moth's auditory system, the nature of temporal integration and the role of the non-auditory B cell, are described. Issues in which the interactions between bats and moths may be of more general interest to biologists, such as noise filtering within the central nervous system, protean behaviours and coevolution between predator and prey, are also discussed. The interaction between bats and moths has much to interest general biologists, and may provide a useful model in understanding the neurophysiological basis of behaviour, including protean escape behaviours. The validity of the term coevolution as applied to this system is discussed, as there is no doubt that the auditory system of moths is a response to the echolocation calls of bats, although the evolutionary response of bats to moths is more ambiguous.     

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.     

Effect of foliar applications of urea on accelerated senescence of maize induced by ear removal

Field grown maize (Zea mays L. cv B73 × Mo17) plants, with and without ears, were sprayed with urea solutions to determine whether foliar application of N could prevent or delay the accelerated loss of reduced N from the leaf and leaf senescence induced by ear removal. Urea sprays were applied at 7, 14, and 21 days after anthesis in three separate and equal applications that provided a total of 67 kilograms N per hectare or 1 gram N per plant. Treatments were arranged in a 2 × 2 factorial in a randomized complete block with five replicates. Appropriate plant and leaf samplings and assays were made.

In response to spray treatments, net increases of reduced N were detected in the whole shoot and plant parts, especially the stalk of the earless plants and grain of the eared plants. There was no effect of urea spray treatment on the normal loss of N from the leaves or rate of senescence of the eared plants or on the accelerated loss of N from the leaves or rate of senescence induced by ear removal. Grain and stover yields were unaffected by the spray treatment.

Apparently the plants were unable to utilize the urea N applied to the vegetation (primarily leaves) after anthesis to enhance or extend the accumulation of dry weight by either eared or earless plants.