Female Calls Research Articles

Copulation calls in wild Mueller’s gibbons (Hylobates muelleri)

AbstractMating activity of a wild Mueller’s gibbon group (Hylobates muelleri) was observed in the Danum Valley Conservation Area, Sabah, Malaysia. The purpose of this study was to investigate the function of copulation calls in gibbons. The female emitted copulation calls at the time of intromission and pelvic thrusting. Copulation calls were composed of two notes and one of them was sung only while mating. Approximately half of copulation calls were sung near the range boundary. Mating with copulation calls sometimes occurred while singing. According to the model that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition, copulation calls should be rare in species with little female promiscuity. As gibbons usually live in pair-living social organization and have a monogamous mating system, no vocal signals by female gibbons are considered to be needed. However, clear copulation calls were emitted by the female. It suggests that the relationship between paired gibbons is unstable. Copulation calls by the female Mueller’s gibbon may function to increase mate guarding and strengthen the pair bond.

Long‐term rearing affects pheromone‐mediated flight behaviour of the Indian meal moth, Plodia interpunctella

AbstractThe pest Plodia interpunctella (Hübner) is reared in many research laboratories. In a culture established in 1996, attraction of males to the female‐produced sex pheromone in flight tunnel assays gradually decreased after ≈15 years of rearing. A new culture was established to enable comparison with the old culture regarding traits associated with mate finding. Female calling activity, pheromone titre and male antennal response to pheromone components did not differ between cultures. In contrast, very few males from the old culture reached the pheromone source in flight tunnel assays compared with 61%–81% of males from the other culture. Our results highlight the importance of maintaining viable insect cultures for research purposes and suggest frequent evaluation of traits involved in chemical communication in such cultures to ensure reliable results in experiments.

Female calling behaviour in the Asian longhorned beetle (Coleoptera: Cerambycidae)

AbstractFemale Asian longhorned beetles, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae), were observed rhythmically extruding their genitalia, resembling the calling behaviour observed in other species of Cerambycidae. We demonstrate that only female A. glabripennis adults perform this behaviour, which lasts up to nearly six minutes and typically includes two types: (1) extrusion of only the tip of genitalia and (2) genitalia fully extruded and deflexed. The frequency and duration of this behaviour are affected by temperature and posteclosion feeding experience, but do not vary with the female age. Anoplophora glabripennis adult males were observed flexing their abdomen downward while extruding their genitalia but only when exposed to the odour of live females with host twigs. In Y-tube olfactometer assays, the volatiles from live females or female genital extracts both attracted more males than the volatiles from live males, male genital extracts, or solvent controls, all in the presence of host-plant volatiles. These findings indicate that A. glabripennis females may produce volatile sexual attractants in association with genital extrusion.

Spacing and Mate Attraction: Sex-Specific Function of Advertisement Calls in the Northern Giant Mouse Lemur (Mirza zaza)

It has been proposed that primates use advertisement calls exclusively to negotiate spacing, but the function of female calls has rarely been studied. Here, we investigated the function of male and female advertisement calls in the northern giant mouse lemur (Mirza zaza),a non-gregarious nocturnal primate from north-western Madagascar. We recorded advertisement calls and associated behaviours of 35 M. zaza individuals at the Duke University Lemur Center. We found that females of M. zazaexclusively use their advertisement calls to advertise oestrus. In contrast, male advertisement calls appeared to be used in a spacing context. These findings show that primates can use their advertisement calls for both spacing and mate attraction, and that the sexes may differ in how they use these calls. The novel find of females of M. zazaattracting mates with loud advertisement calls contrasts with many non-primate taxa, where acoustic mate attraction is usually a function of male advertisement calls, and with other primates, where females use visual and olfactory cues to attract males. The loud female advertisement calls of M. zaza likely ensure mating success during the short receptive phase in this non-gregariously foraging, nocturnal primate.

The reproductive behavior and evaluation of sex pheromone gland extracts of Ectropis grisescens (Lepidoptera: Geometridae)

The geometrid, Ectropis grisescens Warren, is one of the most serious defoliators of the green tea, Camellia sinensis. In the present study, adult emergence, calling behavior, mating activities, and oviposition patterns were observed and the effect of female sex pheromone was evaluated under laboratory conditions (25 ± 1 °C, 14:10 light/dark and 70–75% RH). Adult emergence and calling behavior occurred only at the scotophase. The peak emergence occurred 2 h into the scotophase for males and 3 h for females. Female calling behavior occurred during 1–4 days after eclosion, with most callings among the 1-day-old and the calling gradually decreasing by the age. Mating behavior was first observed at the 2 h into the scotophase. While the mating peak time was similar, 6–8 h into the scotophase for single-pair and multiple-pair groups, the peak of oviposition was 3 days after mating. The pheromone gland extracts from the abdominal tips of 1–2 days virgin female moths were more attractive than the virgin females or the control in the wind tunnel tests. Our findings provide scientific basis to ecological control of E. grisescens.

Diel patterns of emergence and reproductive behaviour in the invasive swede midge (Diptera: Cecidomyiidae)

AbstractSwede midge (Contarinia nasturtii (Kieffer); Diptera: Cecidomyiidae) is a serious invasive pest of Brassica Linnaeus (Brassicaceae) oilseed and vegetable crops in Canada and the United States of America. Pheromone mating disruption is a promising new tactic for managing this difficult pest, but research is needed to determine how pheromone delivery can be optimised. With an understanding of swede midge diel mating patterns, pest managers could limit pheromone release to periods when midges are sexually active. We conducted a series of 24-hour trials to test whether swede midge exhibit diel periodicity of emergence, female calling, and male capture in pheromone traps. We found that females began releasing pheromones almost immediately following emergence within the first five hours after dawn. In the field, we found that males were most active from dawn until late morning, indicating that midges mate primarily during the first five hours of photophase. Low levels of reproductive activity during midday and nighttime hours present opportunities to turn off dispensers and reduce the cost of pheromone inputs in a swede midge mating disruption system.

Common cuckoo females may escape male sexual harassment by color polymorphism

Sexual conflict over mating rate is widely regarded as a selective force on the evolution of female-limited color polymorphism in invertebrates, such as damselflies and butterflies. However, evidence confirming its use in higher vertebrates remains limited. The common cuckoo, Cuculus canorus, is an avian brood parasite that does not provide parental care and represents a rare example of female-limited polymorphism in higher vertebrates. Specifically, males exhibit a monomorphic gray morph, while females are either gray or rufous colored, like juveniles. To test a prediction from the hypothesis that the rufous plumage of female cuckoos may help avoid excessive sexual harassment by males (the harassment avoidance hypothesis), we investigate color morph preference in male cuckoos. Mate choice experiments using playbacks of female calls with decoys mimicking both color morphs indicated that the attracted males immediately copulated with decoys without courtship displays, recognizing both color morphs as a sexual partner. However, the males attempted to copulate more frequently and excessively with the gray morph, which is consistent with the prediction from the harassment avoidance hypothesis. We propose that the absence of parental care augments sexual conflict over mating in cuckoos, resulting in the unusual evolution of female-limited polymorphism in this higher vertebrate.

Sex-specific responses to simulated territorial intrusions in the common cuckoo: a dual function of female acoustic signaling

The two-note call of the male common cuckoo (Cuculus canorus), the so-called “cu-coo”, is well known to people as a natural and cultural signal. However, the so-called “bubbling” call of the female cuckoo is almost unknown to most, and its function in the social organization of cuckoos remains understudied. We carried out a study of a possible intraspecific communication function of female bubbling calls, using playbacks to female cuckoos in their natural environment. Regarding vocal responses, both female and male cuckoos paid attention to the bubbling calls as they consistently responded acoustically by calling but did not so during control playbacks of collared dove (Streptopelia decaocto) calls. Accordingly, in about 63% of trials, females approached the loudspeaker closely and 81% uttered bubbling calls themselves during the experiment. These results are consistent with a function that the bubbling call plays a role in territorial signaling and defense among females. Male cuckoos also showed strong responses to playbacks of bubbling calls, as they approached the speaker and themselves called in 94% of playbacks; this is consistent with a scenario that they are interested in unfamiliar, new females in the area. Specifically, males approached the speaker repeatedly by flight, often flew around it and then perched on a tree, and uttered different call types beside the general “cu-coo” (e.g., quick “cu-cu-coo”, “gowk” call, and “guo” call). Our results represent an illustrative example that a simple female call may have multiple functions, as the cuckoo bubbling call advertises territory need for female cuckoos and attracts males.Significance statement Avian brood parasites lay their eggs in nests of other bird species, causing hosts to incubate, feed, and rear the parasitic offspring. Parasitic adult common cuckoos maintain a complex acoustic communication system, but female cuckoo calls are only beginning to be studied. The basic intraspecific functions of females’ sparrowhawk-like “bubbling calls” have not yet been characterized, whereas interspecifically, they use it for reducing antiparasitic attacks by their hosts. Our playback experiments with bubbling calls revealed that both female and male cuckoos responded acoustically to unfamiliar bubbling calls and more males than females approached the speaker, relative to control playbacks. We conclude that bubbling call has dual basic intraspecific functions: mate attraction, and territorial spacing.

Daily rhythmicity in the sexual behaviour of Monema flavescens (Lepidoptera: Limacodidae)

Daily rhythmicity in the sexual behaviour of Monema flavescens Walker (Lepidoptera: Limacodidae) was studied under laboratory conditions. There was a distinct diel periodicity in female calling, male responsiveness and mating behaviour of M. flavescens. As females aged there was an advance in the onset and more time spent calling. One day old females started calling 4 h after the onset of the scotophase, and 5 to 6 day old females called during the first hour of the scotophase. About 34.5% of females called on the night they emerged (1 day old) and the peak in calling of 97.8% was recorded for 2 day old females, after which the incidence of calling decreased rapidly with advancing age. Wind tunnel and copulation tests showed that males were sexually mature on the third night and female moths on the second night. The highest value for the percentage mating was recorded for 3 day old virgin females 4 to 6 h after the onset of the scotophase. In field tests, traps baited with 2 day and 3 day old virgin females captured more males than any other trap and most males were captured 4 to 6 h (1 to 2 day old), 3 to 5 h (3 to 4 day old) and 2 to 4 h (5 to 6 day old) after the onset of the scotophase. These results indicate that there is a daily rhythm in the reproductive behaviour of M. flavescens and provides a better understanding of its sexual behaviour.

Study on adult emergence, female calling and mating behaviour in Maruca vitrata F. (Lepidoptera: Crambidae) in Kerala, India

Behavioural studies on the legume spotted pod borer, Maruca vitrata was done at 27±2oC, 65-70% RH and photoperiod of 12L: 12D. Adult emergence occurred throughout the day. Emergence of moths during scotophase (6 pm - 5 am) was 70%, which constitutes 63% of males and 76% of females. During photophase, (6 am - 5 pm) emergence was 30%, which constitutes 36% for males, and 24% for females. Highest emergence peak for male was observed at 4 pm (photophase) and for females, at 10 pm (scotophase). Calling behaviour of M.vitrata females observed from one to eight days. Female started calling from 2nd hour of scotophase (7 pm) and terminated at 3 am (scotophase). The mean percentage of calling was maximum at 6th hour of scotophase in 3-day old moth with 44%. None of the females called during first hours of scotophase. Mating of M. vitrata observed throughout scotophase up to 8 days and highest mating occurred in 3-day-old moths with 26%.

Mantid sex pheromones: female calling behaviour and male responses in the Australian false garden mantid, Pseudomantis albofimbriata (Dictyoptera: Mantidae)

ABSTRACTPheromones are important components of insect reproductive biology. They play a broader role in praying mantid behaviour by aggregating individuals and facilitating sexual recognition. Female calling behaviour in praying mantids is a specific posture associated with the emission of pheromones. We describe the calling behaviour of female Australian false garden mantids, Pseudomantis albofimbriata (Stal), and identify the age at which they first start calling based on observations conducted both in the laboratory and in large field enclosures. We found that unmated females displayed a characteristic calling posture that exposed coloured abdominal intersegment membranes, whilst exhibiting a rhythmic pumping movement of the abdomen. Unlike other mantid species, P. albofimbriata females did not lift their wings during this display. Both observations showed that the female calling posture is typically adopted throughout the night; however, it predominantly occurs at 2300 hrs. The average female age at first calling is 14 days after adult emergence. We also found that males did not respond to mated females but responded only to the signals emitted by calling unmated females under natural and semi-natural conditions. Males responded towards calling females within a short period (10–15 minutes) and were attracted from long distances. Importantly, female calling behaviour and male response behaviour occurred in a synchronous manner during the entire nocturnal period. This study provides evidence that female calling behaviour and pheromone emission are intimately linked in praying mantids.

Baboon vocal repertoires and the evolution of primate vocal diversity

A remarkable and derived trait of humans is the faculty for language, and considerable research effort has been devoted to understanding the evolution of speech. In contrast to spoken language, which constitutes a (learned) symbolic communication system, the acoustic structure of nonhuman primate vocalizations is largely genetically fixed. Yet, appreciable differences between different genera and species may exist. Environmental conditions, sexual selection, and characteristics of the social system have been invoked to explain these differences. Here, we studied the acoustic variation of call types and vocal repertoires in the genus Papio. Because the genus comprises both stable groups as well as multi-level societies, and reveals striking variation in the degree of aggressiveness from south to north, it constitutes a promising model to assess the link between social system characteristics and vocal communication. We found that, the vocal repertoires of the different species were composed of the same general call types. A quantitative analysis of the acoustic features of the grunts and loud calls of chacma (Papio ursinus), olive (P. anubis), and Guinea (P. papio) baboons showed subtle acoustic differences within call types, however. Social system characteristics did not map onto acoustic variation. We found no correlation between the structure of grunts and geographic distance; the same was true for female loud calls. Only for male loud calls from three populations, call structure varied with geographic distance. Our findings corroborate the view that the structure of nonhuman primate vocalizations is highly conserved, despite the differences in social systems. Apparently, variation in rate and intensity of occurrence of signals, probably due to different behavioral dispositions in species, are sufficient to allow for plasticity at the level of the social relationships, mating patterns, and social organization.

Components of variation in female common cuckoo calls

Investigations on bird vocalizations have largely focused on males. Female vocalizations are widespread in birds but few studies have investigated female vocal characteristics, particularly in non-Passeriformes. In this study, we use new field recordings from China, and calls available from an online sound library to examine temporal patterns, call consistency and geographical variation in vocalizations of female common cuckoos Cuculus canorous. The peak in vocal activity (both male and female) was in the morning, which contrasts to what would be predicted if the sole function of the female call was to distract the attention of hosts after parasitizing a host’s nest in the afternoon. Both male and female common cuckoos were more vocally active in sunny weather, than rainy weather. We also found larger intra-individual variation in female rather than in male calls, which may benefit female cuckoos by increasing stimulation to host species. Peak frequency of female calls decreased with increased latitude, while differences in female call features were not associated with geographic distance. In summary, our findings that female calls are used in the morning, rather than at peak egg laying, yet are highly variable and show little geographic patterns suggest that the function of these female calls may be more variable and intricate than previously thought. However, because research on female vocalizations is underrepresented, future studies are still needed.

FemaleDiaphania glauculalis(Guenée) Calling Behavior Diel Rhythm and Temporal Change in Pheromone Production

Diaphania glauculalis (Guenee) is a defoliating pest of the Laran tree, Anthocephalus chinensis (Lamk.) Rich. ex Walp., which is an important tree species for reforestation efforts in tropical and subtropical regions. Currently, little information is available about the calling behavior and pheromone production of D. glauculalis females, but such information is important in developing pheromone-based monitoring systems for the pest. Thus, female calling behavior and its correlation with pheromone production was studied using electroantennogram (EAG) technology, qualitative analysis of gas chromatography-mass spectrometry (GC-MS), and Y-tube olfactometer assays. Calling females release a sex pheromone from a gland located on the dorsal membrane between the eighth and ninth abdominal segments, as observed with a stereomicroscope. Peak calling behavior occurred with females 3 d after emergence and 6 h into the scotophase. Pheromone release typically increased with the female age and scotophase and then decreased gradually. GC-MS analysis showed that the amount of pheromone in extracts from the pheromone glands were greatest at the onset of the calling behavior and decreased thereafter. Y-tube olfactometer assays confirmed that pheromone gland extracts at 6 h into the scotophase elicited stronger attractiveness in comparison to 5, 7, and 8 h after emergence.

Do sexual calls in female black capuchin monkeys (Sapajus nigritus) vary with fertility? An acoustic analysis.

Females across a range of animal taxa produce vocalizations and signals uniquely associated with periods of mating. While such signals may ultimately function to increase female attractivity to males, conflicting findings challenge the extent to which these signals co-vary in accordance with the probability of conception. Female black capuchin monkeys (Sapajus nigritus) display an elaborate repertoire of both vocal and visual components as part of their socio-sexual behavior, and previous analyses have shown that the rates of production of visual, but not vocal, components provide graded information on female ovulation. It remains possible, however, that the acoustic parameters of these sexual calls, rather than their rate of productions, co-vary with female fertility. To test this, we analyzed structural and temporal call parameters from estrous calls and post-copulatory calls recorded over five consecutive mating seasons in 12 sexually mature females at Iguazú National Park, Argentina. Calls given during the fertile phase of the female ovarian cycle were compared with those given during the non-fertile phase, as determined by profiles of female reproductive hormones. Similarly, within the fertile phase, we tested whether temporal or spectral acoustic parameters of calls gradually change with the approach of ovulation. We did not find any significant relationship between call parameters and the two measures of female fertility in either female estrous calls or post-copulatory calls. However, some differences between pre- and post-copulatory calls were apparent. Overall, our results indicate that sexual calls in black capuchin females do not provide precise information about the timing of ovulation, but may allow listeners to make probabilistic inferences about whether copulations have taken place. This, combined with previous findings, suggests that females in our study may use signals in different modalities to convey information about their fertility and sexual behavior with varying degrees of precision.

Number of syllables in cuckoo Cuculus canorus calls: A test using a citizen science project

Recent studies revealed that the call of the common cuckoo Cuculus canorus has more inter-individual than intra-individual variation and that the number of syllables depends on environmental conditions, but also the presence of male and female conspecifics. However, still very little is known about how song varies at a global scale, especially considering the wide distribution of this species across most of Europe and Asia. Xeno-canto.org is a vocalization repository for birdsong. We used xeno-canto.org as a data source for investigating the variables that affect the number of syllables in cuckoo calls at a large spatial scale. At a very broad geographical scale, the number of syllables in cuckoo calls predicted bird species richness. Additionally, female calls were associated with shorter males calls, and there was a positive correlation between the interaction between female calls and the number of host races parasitized by the cuckoo. These findings confirm that intraspecific and interspecific interactions significantly affect the number of syllables in cuckoo calls, and both environmental variables and biotic interactions should be considered in future studies of vocalizations in cuckoos. Last but not least, we demonstrated that a citizen science project is a useful source for ecological studies at large spatial scales.

Postnatal Growth and Vocalization Development in the Long-fingered Bat, Myotis capaccinii (Chiroptera, Vespertilionidae).

Robab Mehdizadeh, Hojjat Eghbali, and Mozafar Sharifi (2018) We simultaneously monitored postnatal growth and vocalization development in a free living population of the long-fingered bat, Myotis capaccinii, in a maternity colony in the Mahidasht cave, western Iran. Length of forearm and body mass of 1-day-old neonates averaged 19.59 ± 1.23 mm and 3.59 ± 0.23 g and followed linear pattern of growth at mean growth rates of 0.74 mm/day and 0.15 g/day until 28 days of age, after which is increased slowly. A similar nonlinear growth pattern was found for ten wing characteristics (wingspan, wing area, handwing length, handwing area, armwing length, armwing area, aspect ratio, wing loading, tip length ratio, and tip area ratio). However, postnatal growth followed a two phase linear pattern of increase-decrease for the epiphyseal-phalangeal gap and decrease- increase for wing loading. At birth, infant bats produced low, short frequency sonar and oral calls in isolation before they could open their eyes. Isolation calls obtained at age 1-4 days old from M. capaccinii pups were frequency modulated shallow calls with longer duration (7.54 ± 1.83 ms) and lower peak frequency (20.07 ± 0.89 kHz) compared to adult female calls (2.35 ± 0.75 ms and 54.02 ± 4.34 kHz). During days 12-16, calls began to resemble adult echolocation calls. Duration of calls increased slightly before 7 days old and then gradually decreased. The peak, start and end frequencies of spontaneous calls increased with age. When the juvenile bats started foraging outside the cave, they only omitted nasal FM calls with 1-2 harmonics. Comparing postnatal changes in body and wing characteristics with those of vocalization, we found that the most positive correlation was between body (forearm length and body mass) and wing features (wing area, wingspan, handwing area, armwing area and aspect ratio) and call parameters (peak, start and end frequency), while wing loading had a significant negative correlation with the call parameters.

Understanding sources of variance and correlation among features of Bornean gibbon (Hylobates muelleri) female calls

Acoustic signals serve important functions in mate choice, resource defense, and species recognition. Quantifying patterns and sources of variation in acoustic signals can advance understanding of the evolutionary processes that shape behavioral diversity more broadly. Animal vocalization datasets are inherently multivariate and hierarchical, wherein multiple features are estimated from calls of many individuals across different recording locations. Patterns of variation within different hierarchical levels-notwithstanding the challenges they present for modeling and inference-can provide insight into processes shaping vocal variation. The current work presents a multivariate, variance components model to investigate three levels of variance (within-female, between-female, and between-site) in Bornean gibbon calls. For six of the eight features estimated from call spectrograms, between-female variance was the most important contributor to total variance. For one feature, trill rate, there were site-level differences, which may be related to geographic isolation of certain gibbon populations. There was also a negative relationship between trill rate and duration of the introduction, suggesting trade-offs in the production of gibbon calls. Given substantial inter-individual variation in gibbon calls, it seems likely that there has been selection to confer information regarding caller identity, but mechanisms leading to site-level variation in trill rate remain to be determined.

Lobesia botrana males mainly fly at dusk: video camera-assisted pheromone traps and implications for mating disruption

Pheromone-mediated mating disruption (MD) is currently considered an effective strategy to control the European grapevine moth (EGVM), Lobesia botrana, with a successful interference on natural female calling during the male searching flight. However, little is known on the impact of the hour of the day on EGVM male flight. While various models forecasting the day of maximum presence of males per flight have been developed, field research on the male flight activity over 24 hours is scarce. Hence, we used video camera-assisted pheromone traps to allow a continuous monitoring of EGVM flights over daylight and night hours, quantifying captures of males. Experiments were carried out in three vineyards located in northern Spain over two years (2016 and 2017). Results showed that EGVM flight mainly occurred between 21:00 and 23:00 h (GMT+1, daylight saving time). Furthermore, male catches significantly differed over the study year, annual flight period and vineyard. Most of the dispensers used worldwide for EGVM MD continuously release the main sex pheromone component [(7E,9Z)-7,9-dodecadien-1-yl acetate], except for some automatic devices releasing puffs of sex pheromones at selected time intervals. The findings presented here can be useful to optimize the MD technique, identifying selected time intervals when the release of EGVM synthetic pheromones can be concentrated, boosting MD efficacy against this important pest, minimizing the release of synthetic sex pheromone molecules in the environment and reducing application costs.

Calling and Mating Behavior of Diaphania angustalis (Lepidoptera: Crambidae).

Diaphania angustalis Snellen (Lepidoptera: Crambidae) has emerged as a very important pest of blackboard tree, Alstonia scholaris (L.) R. Br. (Apocynaceae), in China during the last two decades. Understanding its biology and behavior is crucial for designing effective and environmentally friendly pest management strategies. Under laboratory conditions [25-28°C, 12:12 (L:D) h, 75-80% RH], adults emerged during both light and dark hours with peak emergence occurring between the first and fifth hours of scotophase, and unmated males and females lived for a mean (±SE) 5.4 ± 0.4 and 5.3 ± 0.7 d, respectively. Female calling behavior was observed only during scotophase (peaking in the fifth hour) by 1- to 5-d-old females, and mating activities occurred 2-5 d after emergence, peaking on day 3. These behavioral characteristics could inform control programs targeting adults.