Ecology and genetics of hybrid zones in the southern African Pycnonotus bulbul species complex

Lloyd, P., Craig, A.J.F.K., Hulley, P.E., Essop, M.F., Bloomer, P. & Crowe, T.M. 1997. Ecology and genetics of hybrid zones in the southern African Pycnonotus bulbul species complex. Ostrich 68 (2–4): 90–96.

The closely related Blackeyed Bulbul Pycnonotus barbatus, Cape Bulbul P. capensis and Redeyed Bulbul P. nigricans have parapatric to locally sympatric distributions within southern Africa. Extensive hybridization along narrow transition zones between each of the three species pairs is described in a region of the Eastern Cape province, South Africa. The transition zones coincide with ecotones between different vegetation types, which in turn follow escarpments or mountain ranges. The lack of population density depressions within the hybrid zones, together with the variability of the hybrids, suggests the hybrids are viable. Sharp step clines in various phenotypic characters are described across the P. barbatus/P. nigricans hybrid zone. A mtDNA analysis found evidence of possible introgression between P. barbatus and P. capensis. All eight P. barbatus x P. nigricans hybrids analysed possessed P. barbatus mtDNA, suggesting the existence of either positive assortative mating or strong directional selection, but our data are unable to distinguish which. Our results do not support the dynamic-equilibrium model, but are compatible with the bounded-hybrid-superiority model. We conclude that the maintenance of the parapatric distributions of the different taxa is due mainly to differences in environmentally-associated fitness between parental phenotypes or among parental and hybrid phenotypes along an ecotone, with the narrowness of the hybrid zones maintained by the steepness of the environmental gradients crossing them.     

THE ROLE OF COURTSHIP SONGS IN REPRODUCTIVE ISOLATION AMONG POPULATIONS OF GREEN LACEWINGS OF THE GENUS CHRYSOPERLA (NEUROPTERA: CHRYSOPIDAE)

Male and female lacewings tremulate during courtship, establishing duets that always precede copulation. Three distinct courtship songs are found in populations of the green lacewing Chrysoperla plorabunda (P1, P2 and P3 song morphs). Analysis of five features of the songs for individuals collected from Connecticut, Idaho, Oregon and California showed few differences within song morphs, but sympatric song morphs differed significantly in temporal features of the songs and their mode of presentation. Playback experiments using recorded songs were performed on females with all possible sympatric and allopatric combinations of females and recorded songs. The results showed that females strongly prefer to duet with recordings of males of their own song type and usually showed no responses to songs of other types. Thus, song differences are effective barriers to reproduction between the sympatric morphs. Our results support the hypothesis that the three song morphs are true biological species.     

Acoustic Monitoring Reveals Congruent Patterns of Territorial Singing Behaviour in Male and Female Tropical Wrens

Many animals defend territories against conspecific individuals using acoustic signals. In birds, male vocalizations are known to play a critical role in territory defence. Territorial acoustic signals in females have been poorly studied, perhaps because female song is uncommon in north‐temperate ecosystems. In this study, we compare male vs. female territorial singing behaviour in Neotropical rufous‐and‐white wrens Thryothorus rufalbus, a species where both sexes produce solo songs and often coordinate their songs in vocal duets. We recorded free‐living birds in Costa Rica using an eight‐microphone Acoustic Location System capable of passively triangulating the position of animals based on their vocalizations. We recorded 17 pairs of birds for 2–4 consecutive mornings and calculated the territory of each individual as a 95% fixed kernel estimate around their song posts. We compared territories calculated around male vs. female song posts, including separate analyses of solo vs. duet song posts. These spatial analyses of singing behaviour reveal that males and females use similarly sized territories with more than 60% overlap between breeding partners. Territories calculated based on solo vs. duet song posts were of similar size and similar degrees of overlap. Solos and duets were performed at similar distances from the nest for both sexes. Overall, male and female rufous‐and‐white wrens exhibit very similar spatial territorial singing behaviour, demonstrating congruent patterns of male and female territoriality.     

Effects of fragmentation and hybridization on geographical patterns of song variation in the endangered Yellow Cardinal Gubernatrix cristata

The song learning process may lead to small‐scale geographical variation in vocalizations of oscine birds. This variation can be further enhanced by the effects of habitat fragmentation or hybridization. Populations of the endangered Yellow Cardinal Gubernatrix cristata are now patchily distributed in the southern South American thorny shrubland forests and are small as a consequence of the pressure exerted by increased habitat transformation and illegal trade. We study the Yellow Cardinal's vocalizations throughout its distribution and assess how habitat characteristics and fragmentation, as well as hybridization with the Common Diuca Diuca diuca, have affected song patterns of different populations. We expected to find song differences among populations and songs to be more similar to those of the Common Diuca in areas where hybridization occurs. Multivariate analyses revealed significant differences in song between the four populations studied and confirmed that songs are more similar to those of Common Diuca where hybridization takes place. These results, in conjunction with genetic studies, can help to establish management units that preserve genetic and cultural variation in this endangered species.     

Diel and seasonal variation of Striped Cuckoo (Tapera naevia) vocalizations revealed using automated signal recognition

Studying seasonal changes in the vocal activity of birds may shed light on the function of avian vocalizations and the phenology of life history events. Our current knowledge regarding the seasonality of the vocal behaviour of tropical birds in general, and avian brood parasites in particular, is very limited. Here, we employed passive acoustic monitoring with automated signal recognition to monitor the vocal behaviour of the Striped Cuckoo Tapera naevia over a complete annual cycle in the Brazilian Pantanal. We evaluated whether the pattern of vocal activity differed between the two main vocalizations of the species (sem-fim and wee-series songs) and whether vocal activity varied with time of day and season. The diel pattern of vocal activity for both vocalization types showed a bimodal pattern, with the first peak of vocal activity in the few hours after sunrise and the second peak before sunset, in agreement with prior studies in other cuckoos. The sem-fim song was also produced during the night, while the wee-series song was produced only during the day. Both vocalization types showed clear seasonality and were produced between mid-June and mid-February. Seasonal changes in vocal activity suggest that the Striped Cuckoo breeds during the dry season and leaves the study area during the flooding period. The seasonal pattern of the wee-series song showed strong seasonality, with 90% of these calls detected in September and October, whereas the sem-fim song showed weaker seasonality, with 80% of the calls detected during the July–October period. Our study indicates that automated signal recognition might be a reliable tool for monitoring cuckoos. Further research could evaluate whether the different seasonal patterns of the sem-fim and wee-series songs of the Striped Cuckoo are related to different functions.     

Vocal mimicry of the paraside whydahs (Vidua) and response of female whydahs to the songs of their hosts (Pytilia) and their mimics

Parasitic paradise whydahs (Vidua paradisaea) mimic the vocalizations of their hosts, Pytilia melba. Photostimulated female whydahs isolated in large aviaries responded to broadcasts of recorded song. Approach occurred significantly more often to songs of the host species P. melba than to the similar P. phoenicoptera. Females approached with equal frequency the songs recorded from their hosts and the mimetic songs of the male whydahs. No significant differences were found between the responses of females to songs of sympatric and allopatric forms of their host. It is suggested that mimetic songs of males and the responses of females are behavioural isolating mechanisms among species of whydahs.     

SONGS OF BLUE TITS PARUS CAERULEUS PALMENSIS FROM LA PALMA (CANARY ISLANDS)—A TEST OF HYPOTHESES

ABSTRACT

Parus major and Parus caeruleus palmensis have some song types in common. They consist of whistled element-types in different frequency ranges. Both species show territorial reactions to playback of the song-types belonging to the other species. P.c. palmensis does not share any songtypes with Central European Parus caeruleus. This is confirmed by playback experiments with the different song types, which do not elicit any territorial behaviour. The songs of P.c. palmensis also differ from those of blue tits from any other Canary Island. They may be derived from contact calls of the Lanzarote population. They have been developed by young birds that had not yet learnt their songs when they colonized La Palma from Lanzarote without reaching any of the other Canary Islands. It is suggested that the uniform song repertoire was developed by adapting the already learned contact calls to each other. The similarities to song types of P. major are due to convergence rather than character displacement. All other Canary Island tit populations share the main features of their songs, which are characterized by quick frequency changes. It seems most likely that these islands have been colonized by birds which had already learnt their songs. Differences in song repertoires are mainly caused by drift events which happen to occur because of population bottlenecks during the colonization process.     

CONVERGENT EVOLUTION OF COURTSHIP SONGS AMONG CRYPTIC SPECIES OF THE CARNEA GROUP OF GREEN LACEWINGS (NEUROPTERA: CHRYSOPIDAE: CHRYSOPERLA)

Although traits of related species are likely to be similar due to common ancestry, mating signals are an exception. In singing insects, for example, song similarity has been documented only for allopatric or allochronic species pairs, and even then, not often. Where song similarity does occur, it has been logically attributed to the inheritance of ancestral traits rather than convergence. It is quite common for related, sympatric insect species to differ dramatically in calling song, which is predicted by evolutionary theory to maximize intraspecific mating success. Given that there are a limited number of ways to make sounds on anatomically similar organs and given that there would be no selective pressure for songs to differ in widely separated geographic areas, convergence in songs among related species living on different continents might be expected. Here we present the first well-documented case of such convergence, in a group of sibling, cryptic species characterized by substrate-borne vibrational mating songs. In this example from green lacewings of the carnea group of the genus Chrysoperla, a variety of statistical tests shows that one species in North America and another in Asia possess songs that are strikingly similar to each other. DNA data demonstrate that the species involved belong to divergent speciose lineages, and behavioral data demonstrate that the convergent songs are readily accepted by members of both species.     

Song modification in the Orthoptera I. Proclamation songs of Platycleis spp. (Tettigoniidae)

Orthopteran song terminology is briefly reviewed taking into account new proposals concerning the term ‘chirp’ by Broughton (1976). The song of Platycleis intermedia is analysed in detail. Synchronous or unison singing between conspecifics of this species is maintained, despite ambient temperature differences, by the individual at the lower temperature instantaneously extending its echeme interval. The normal songs of P.afinis, P.falx, P.sabulosa and P.albopunctata are described and compared with each other and with the song of P.intermedia. The songs of all five species are similar at the syllable level but different at the echeme level. It appears to be these similarities and differences that are responsible for song modification on the part of P.intermedia when it hears the song of one of the other four species.     

Responsiveness of a male Mueller's gibbon to his own species-song,that of a lar gibbon,and a synthetic song of similar frequency

The study compared the responsiveness of a captive male Mueller's gibbon to audio recordings of dawn songs of wild-living male Mueller's gibbons and lar gibbons, and to a synthetic song constructed from screech owl vocalizations. Though wild-caught, the subject had not been exposed to songs of his own species for at least 10 years, and in fact, only rarely performed the dawn song himself. Initially, the subject responded vigorously to all three recordings, with no preference being shown for the recording of his own species. However, a very strong preference for Mueller's vocalizations did develop following a period of concentrated and exclusive exposure to Mueller's songs.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Does Interspecific Eavesdropping Promote Aerial Aggregations in European Pipistrelle Bats During Autumn?

Eavesdropping is a widespread strategy to optimize decision‐making. Bats are interesting models for investigating acoustic information transfer, as they possess a broad vocalization repertoire of echolocation and social calls. Yet, the knowledge of the extent to which eavesdropping plays a role in bat communication is scarce. Here, we examined the vocal and spatial activity patterns of three congeneric bat species (Pipistrellus pipistrellus, P. pygmaeus, P. nathusii, hereafter called pipistrelles) during autumn – their migration and mating season. We hypothesized that pipistrelles utilize information of conspecifics and congenerics to localize stopover sites for mating or other information purposes during migration. We found that bats formed small multispecies aggregations on the wing, suggesting interspecific eavesdropping on feeding buzzes and/or courtship calls could occur among these species. Pipistrelles produced similar proportions of feeding buzzes and social calls at aggregation sites. To test whether pipistrelles respond to the courtship vocalizations of conspecifics and congenerics, we conducted a playback experiment with P. pipistrellus where we presented courtship vocalizations of the three pipistrelle species and as a control, a motif of the noctule bat's song (Nyctalus noctula). Pipistrellus pipistrellus decreased the rate of social calls in response to the broadcast of songs of P. nathusii, yet they tended to increase the rate in response to the playback of their own species. We conclude that interspecific eavesdropping occurs at least between P. pipistrellus and P. nathusii and might thus favour the formation of multispecies aggregations. Our findings provide novel insights into the social behaviour and interspecific communication of a bat community during the season of migration and mating.     

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution. Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between‐site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic‐acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species‐specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song.     

MICRODIALECT AND GROUP SIGNATURE IN THE SONG OF THE SKYLARK ALAUDA ARVENSIS

ABSTRACT

The Skylark Alauda arvensis is a territorial species of open landscape in which pairs settle in stable and adjacent territories during the breeding season. Due to the heterogeneity of the habitat, territories are gathered in patches spaced by a few kilometres, in which each male produces very long and complex flight songs as a part of the territorial behaviour. We showed that, in a given patch, all the males (neighbours) share some particular sequences of syllables in their songs, whereas males settled in different patches (strangers) have almost no sequences in common. Such a phenomenon is known as microdialect. To test the hypothesis that these shared sequences support a group signature, we made playback experiments with “chimeric” signals: songs of strangers where the sequences shared by neighbours were artificially inserted. Behavioural responses to playbacks indicated a neighbour-stranger discrimination consistent with the dear enemy phenomenon, i.e. a reduced aggression toward neighbours compared to strangers. Furthermore, the same level of responses, observed when a “chimeric” song and a neighbour song were broadcast, indicated that shared sequences are recognised and identified as markers of the neighbourhood identity.     

Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird

Song complexity in many songbirds is a trait subject to sexual selection. It is often associated with male territorial defence. Empirical studies testing differential male responses to rival song in vocally complex songbirds have, however, been scarce. We conducted playback experiments of the endemic New Zealand Tui Prosthemadera novaeseelandiae to test the aggressive response of territorial male Tui to rival songs with differing complexity levels. Overall, complex songs evoked significantly stronger responses from territorial males than did simple songs. Following playback of complex songs, focal males approached the playback more closely and rapidly, and responded with songs of higher complexity than they did to playback of simple songs. This suggests males could both distinguish between different levels of complexity within the Tui repertoire, and perceive a more complex song as a greater territorial threat. Our study is one of the first to demonstrate strong aggressive responses to increased levels of song complexity in a songbird species with highly complex vocalizations.     

Vibrational communication and mating behaviour of Dichelops melacanthus (Hemiptera: Pentatomidae) recorded from loudspeaker membranes and plants

Vibrational communication is important for successful mating in various stink bugs species. The vibrational signals from males and females of Dichelops melacanthus Dallas (Hemiptera: Pentatomidae) are recorded from a nonresonant substrate (i.e. a loudspeaker membrane) to characterize the temporal and spectral properties of these vibrational signals, as well as on a resonant substrate (i.e. bean plants) to obtain information about how these signals are altered when they are transmitted through the plants. On the loudspeaker membrane, D. melacanthus males and females emit only one male or one female song, respectively. However, when the insects are placed on bean leaves, a more complex repertoire is recorded, with three different songs for each sex. The first female and male songs appear to have calling functions and the third male and female songs are emitted during courtship. The second female and male songs are emitted after the first song, although their functions in mating behaviour are not clear. The identified repertoire is similar to those of other Neotropical stink bugs, starting with songs 1 and 2 and developing into song 3. Frequency modulation is observed in the female songs recorded from the loudspeaker membrane and the plants. The signals recorded from plants present higher harmonic peaks compared with the signals recorded from the loudspeaker membrane. The presence of species and sex‐specific songs during mating confirms the important role of vibrational communication in mate location and recognition. The temporal and spectral characteristic signals are influenced by the substrate used to record the songs emitted by D. melacanthus.     

Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences

We conducted a tutoring experiment to determine whether female brown-headed cowbirds (Molothrus ater) would attend to vocalizations of other females and use those cues to influence their own preferences for male courtship songs. We collected recordings of male songs that were unfamiliar to the subject females and paired half of the songs with female chatter vocalizations—vocalizations that females give in response to songs sung by males that are courting the females effectively. Thus, chatter immediately following a song provided a cue indicating that the song was sung by a male who was of high-enough quality to court a female successfully. Using a cross-over design, we tutored two groups of females with song–chatter pairings prior to the breeding season. In the breeding season, we placed the tutored females into sound-attenuating chambers and played them the same songs without the chatter. Females produced significantly more copulation solicitation displays in response to the songs that they had heard paired with chatter than to songs that had not been paired with chatter. This experiment is the first demonstration that females can modify their song preferences by attending to the vocal behaviour of other females.     

Nucleotide and repeat length variation at the nonA gene of the Drosophila virilis group species and its effects on male courtship song

Genes found to affect male courtship song characters in Drosophila melanogaster are good candidates when tracing genes responsible for species-specific songs in other Drosophila species. It has previously been shown that Thr–Gly repeat length variation at the period gene affects song traits in D. melanogaster, which gives the repetitive regions a special interest. In this work, we have characterised the patterns of nucleotide variation for gene regions containing two Gly and one Gln–Ala repeat in another D. melanogaster song gene, no-on-transient A, in D. virilis group species. The levels of nucleotide variability in D. virilis nonA were similar to those found for other genes of the species, and the gene sequences showed no signs of deviation from neutrality. The Gly 2 repeat preceding the central domain of the gene exhibited length variation, which did not, however, correlate with song variation either within D. virilis or between the species of D. virilis group. The Gly 3 repeat located on the other side of the central domain showed amino acid divergence parallel to the consensus phylogeny of the D. virilis group species. The species of the virilis subgroup having Asn after the first three glycines in this repeat have simple songs with no species-specificity, while the species of the montana subgroup having two Gly or Asn–Ser in this site have unique courtship songs. Amino acid differences between the species in this repeat may, however, reflect species phylogeny rather than have an effect on song divergence per se.     

He hears,she hears: Are there sex differences in auditory processing?

Songbirds learn individually unique songs through vocal imitation and use them in courtship and territorial displays. Previous work has identified a forebrain auditory area, the caudomedial nidopallium (NCM), that appears specialized for discriminating and remembering conspecific vocalizations. In zebra finches (ZFs), only males produce learned vocalizations, but both sexes process these and other signals. This study assessed sex differences in auditory processing by recording extracellular multiunit activity at multiple sites within NCM. Juvenile female ZFs (n = 46) were reared in individual isolation and artificially tutored with song. In adulthood, songs were played back to assess auditory responses, stimulus‐specific adaptation, neural bias for conspecific song, and memory for the tutor's song, as well as recently heard songs. In a subset of females (n = 36), estradiol (E2) levels were manipulated to test the contribution of E2, known to be synthesized in the brain, to auditory responses. Untreated females (n = 10) showed significant differences in response magnitude and stimulus‐specific adaptation compared to males reared in the same paradigm (n = 9). In hormone‐manipulated females, E2 augmentation facilitated the memory for recently heard songs in adulthood, but neither E2 augmentation (n = 15) nor E2 synthesis blockade (n = 9) affected tutor song memory or the neural bias for conspecific song. The results demonstrate subtle sex differences in processing communication signals, and show that E2 levels in female songbirds can affect the memory for songs of potential suitors, thus contributing to the process of mate selection. The results also have potential relevance to clinical interventions that manipulate E2 in human patients. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 75: 302–314, 2015     

Understanding the function of nocturnal song in ovenbirds: males do not countersing at night

Many diurnal bird species vocalize at night, however the function of nocturnal song is, generally, still poorly understood. Previous research has suggested that nocturnal song may serve a social function and is influenced by environmental factors. To test whether males attend to the nocturnal song of conspecifics, we experimentally exposed ovenbirds Seiurus aurocapilla to nocturnal flight songs, and recorded their response both during the night and during the following dawn chorus. We compared latency to song and vocal output before and after playback exposure to determine if males altered their vocalizations in response to exposure to flight songs from an unknown male. We found no evidence of counter singing or change in nocturnal song output, nor a change in vocal output during the dawn chorus following playback exposure. Our results suggest that, in ovenbirds, nocturnal song does not serve as an intraspecific social function. Nocturnal song, through rare, may be significant in the mating systems of some diurnal bird species, and requires additional study.