The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

Pleistocene origin and colonization history of Lobelia columnaris Hook. f. (Campanulaceae: Lobelioideae) across sky islands of West Central Africa

We aimed to infer ancestral area and historical colonization of Lobelia columnaris in the sky islands of Bioko and Cameroon through dated phylogeny using chloroplast genomes. Specifically, we aim to answer the following questions: (1) What are the phylogenetic relationships among Bioko Island and Cameroon populations? (2) Are the older populations found in the older sky islands? We assembled novel plastomes from 20 individuals of L. columnaris from 5 mountain systems. The plastome data were explored with phylogenetic analyses using Maximum Likelihood and Bayesian Inference. The populations of L. columnaris have a monophyletic origin, subdivided into three plastomes‐geographic clades. The plastid phylogenomic results and age of the sky islands indicate that L. columnaris colonized first along with the Cameroon Volcanic Line''s young sky islands of Bioko. The crown group (1.54 Ma) split the population in Bioko and mainland Cameroon. It is possible that Bioko was the ancestral area and likely isolated during cold and dry conditions in forest refugia. Presumably, the colonization history occurred during the middle‐late Pleistocene from South Bioko''s young sky island to North Bioko and the northern old sky islands in Cameroon. Furthermore, the central depression with lowland forest between North and South Bioko is a current geographic barrier that keeps separating the populations of Bioko from each other. Also, the shallow sea channel keeps isolated the populations of Bioko and the mainland populations. The Pleistocene climatic oscillations led to the divergence of the Cameroon and Bioko populations into three clades. L. columnaris colonized the older sky islands in mainland Cameroon after establishment in Bioko''s younger sky islands. Contrary to expectations, the biogeography history was an inverse progression with respect to the age of the Afromontane sky islands.     

Evidence for Dialects in Three Captive Populations of Common Marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.     

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2-12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with 'their' females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.     

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). I. Vocal repertoire and call emission

Vocal communication in wild long-tailed macaques (Macaca fascicularis) is described in terms of (1) a preliminary vocal repertoire and the situations in which calls occur in the natural habitat of this species and (2) quantitative measurement of the natural occurrence of calls in the field. Although a number of calls are relatively discrete (e.g., a male loud call), gradation is pronounced for both wide-spectrum (“harsh”) and narrow-spectrum (“clear”) vocal signals. Thirteen general types of harsh calls are identified provisionally as elements of the vocal repertoire. The exact number of discrete clear calls contributing to the vocal repertoire could not be ascertained precisely, but these calls were classified operationally into six broadly acoustically different classes in order to measure natural vocal behavior. Vocalizations tended to occur in temporal “clusters” during sample, periods. Narrow-band clear or “coo” calls were more frequently performed by macaques than wide-band harsh calls. The possible functional implications of the correlated occurrence of multiple vocal signals are discussed.     

Freshwater snails of São Tomé, with special reference to Bulinus forskalii (Ehrenberg), host of Schistosoma intercalatum

São Tomé Island has 3 known taxa of freshwater gastropod, here identified to species for the first time; Neritina afra Sowerby, Ferrissia eburnensis Binder and a distinctive form of Bulinus forskalii (Ehrenberg). The Bulinus acts as intermediate host for the parasite Schistosoma intercalatum Fisher, the cause of human schistosomiasis in foci of infection detected in recent years on São Tomé. A morphological characterization of this snail is presented, in respect of the shell, radula and copulatory organ. It is compared with B. forskalii populations sampled on the African mainland (Nigeria, Cameroon, Gabon and Angola) and with related taxa. Despite differences in the shell from the commonly found form of B. forskalii it seems appropriate to identify the São Tomé population as an extreme conchological variant of this taxon.     

No need to shout: Effect of signal loudness on sibling communication in barn owls Tyto alba

In animal communication, signal loudness is often ignored and seldom measured. We used a playback experiment to examine the role of vocal loudness (i.e., sound pressure level) in sibling to sibling communication of nestling barn owls Tyto alba. In this species, siblings vocally negotiate among each other for priority access to parental food resources. Call rate and call duration play key roles in this vocal communication system, with the most vocal nestlings deterring their siblings from competing for access to the food item next delivered by parents. Here, we broadcast calls at different loudness levels and call rate to live nestlings. The loudness of playback calls did not affect owlets' investment in call rate, call duration or call loudness. The rate at which playback calls were broadcast affected owlets' call rate but did not influence their response in terms of loudness. This suggests that selection for producing loud signals may be weak in this species, as loud calls may attract predators. Moreover, given that owlets do not overlap their calls and that they communicate to nearby siblings in the silence of the night, loud signals may not be necessary to convey reliable information about food need.     

Loud calls of male Nilgiri langurs (Presbytis johnii): Age-, individual-, and population-specific differences

Adult male Nilgiri langurs (Presbytis johnii) utter loud call bouts consisting of one or more phrases. Phrases are made up of several units showing similar or different structural features. The units involved differ with respect to not only their physical structure but also their overall utilization: three vocal patterns are uttered exclusively by mature males living in bisexual groups or all-male bands and, in addition to being part of loud call bouts, are given during encounters with terrestrial predators; two vocal patterns are uttered by males and females, again not just as constituents of loud calls; and one vocal pattern is given exclusively by mature males living in bisexual groups. Within a given bout, phrases differ not only with respect to their composition but also in their temporal organization. In addition to the acoustic components, loud calls are regularly accompanied by stereotyped motoric displays. The motoric and acoustic components of loud call displays appear independently of each other and at different times during ontogeny. The development of the display is characterized by combination of units with different structural features and synchronization of vocal and motoric components. Although more evidence is needed, our observations suggest that the development of loud call displays coincides with the aquisitation of social maturation and competence and requires not only social experience but also a certain amount of motoric training. In spite of the high degree of ritualization, loud call displays are not completely fixed in form, but instead are open to individual- and population-specific variation.     

Acoustic and Temporal Variation in Gelada (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>) Loud Calls Advertise Male Quality

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.     

The blackflies (Diptera: Simuliidae) of Bioko (Republic of Equatorial Guinea) and the Gulf of Guinea with a description of the larvae of the 'Pomeroy' form of Simulium cervicornutum

Abstract.  Like many other organisms, Simuliidae often show a high degree of endemism on oceanic islands, and the Gulf of Guinea, including its islands, is a region of general biogeographical interest in view of the uniqueness of its flora and fauna. This paper presents a comprehensive review of the Simuliidae in the region, and is the first faunistic record of blackflies from Bioko. Simuliidae (larvae, pupae and neonate adults) were collected from Bioko and from around Mount Cameroon and compared with previous findings from Mount Cameroon, Príncipe and São Tomé. Twenty-seven species are known from the region. Twenty-five species have been recorded around Mount Cameroon, eight species on Bioko, three species on São Tomé and one species on Príncipe. Two taxonomic 'forms' (one on Bioko alone, and one on both Bioko and around Mount Cameroon) and one species (found only on São Tomé) are endemic to the region. A study of the variation in the morphology of Simulium cervicornutum revealed two morphotypes, one from Bioko and around Mount Cameroon and the other from the rest of Africa. The speciation and biogeography of the Simuliidae in the Gulf of Guinea are discussed.     

On the altitudinal limits of birds on BasilC Peak (Bioko Island; Equatorial Guinea)

Pérez del Val, J. 2000. On the altitudinal limits of birds on Basile Peak (Bioko Island; Equatorial Guinea). Ostrich 71(1 & 2): 342.

The lower altitudinal limit of the montane avifauna in Africa has generally been set at 1 500- 800 m, corresponding to vegetation belts of the main mountain ranges of East Africa. However, much lower limits have been reported from the East Usambaras (Tanzania), Mount Cameroon, and Bioko Island. Basilé Peak is a volcano of 3 011 m which constitutes the northern half of Bioko Island. Below 400–900 m the forest has been logged and largely replaced by cocoa plantations, but the vegetation is relatively undisturbed at higher altitudes. Annual rainfall ranges between 2 000 mm and 3 500 mm. From January 1990 to July 1992 mist-nets were set at 13 standardised stations on Basilé Peak; 1 427 birds of 71 species were captured. Previous data from non-standardised mist-netting at 6 other localities, together with sight and sound records, published data, and 1 047 skins in the collections of Museo Naçional de Ciençias Naturales (Madrid), Estacion Biologica de Donaiia (Sevilla) and the Natural History Museum (Tring) were also used to compile distribution lists. From published botanical surveys, I recognised four vegetation zones: Lowland Rain Forest up to 800 m; Mountain Rain Forest at 80CL1 800 m; Araliaceus Forest 1 800–2 500 m; and Ericaceus Stands above 2 500 m. An analysis of similarity (using the index of Czechanowski) grouped 68 bird species into altitudinal classes at 200 m intervals. This suggests a division between lowland and montane birds at 800–1 000 m, broadly coinciding with the change between Lowland and Mountain Rain Forest. There does not seem to be a discrete bird community restricted to either of the upper zones (Araliaceus Forest or Ericaeus Stands), with only the Yellow Bishop Euplectes capensis restricted to the upper 500 m of the mountain. Most species which reach the summit are found in all vegetation zones, notably the endemic subspecies of the African Goshawk Accipiter tachiro lopezi. It is suggested that low temperatures, high rainfall, and in particular the seasonal distribution of rainfall, may explain the lower altitudinal limits of the montane avifauna on Bioko and on Mount Cameroon.     

Molecular evidence for deep phylogenetic divergence in Mandrillus sphinx

Mandrills (Mandrillus sphinx) are forest primates indigenous to western central Africa. Phylogenetic analysis of 267 base pairs (bp) of the cytochrome b gene from 53 mandrills of known and 17 of unknown provenance revealed two phylogeographical groups, with haplotypes differentiated by 2.6% comprising seven synonymous transitions. The distribution of the haplotypes suggests that the Ogooué River, Gabon, which bisects their range, separates mandrill populations in Cameroon and northern Gabon from those in southern Gabon. The haplotype distribution is also concordant with that of two known mandrill simian immunodeficiency viruses, suggesting that these two mandrill phylogroups have followed different evolutionary trajectories since separation.     

Geographical Variation in Duet Songs of Sulawesi Tarsiers: Evidence for New Cryptic Species in South and Southeast Sulawesi

Geographic populations of Sulawesi tarsiers differ conspicuously in the acoustic structure of the loud duet calls produced by mated pairs. There is evidence that the differences in call features relate to species differentiation. Duet calls can thus be used as a tool to identify cryptic species and for their monitoring in the field. We recorded duets from various geographically isolated populations of Tarsius tarsier in south and southeast Sulawesi to survey the species identity of the tarsiers in these regions. We compared their calls with the duet calls of the Manado tarsier (= Tarsius spectrum), Tarsius dianae, and the Togian Island tarsier. In addition, we recorded and analyzed the duet call of the tarsier from Peleng Island, Tarsius pelengensis. Qualitative characteristics of duet songs of both sexes, analysis of frequency and temporal parameters, and multivariate statistics show 4 distinct vocal forms that predict the existence of 4 new species. These are found on Selayar Island, on the south mainland (Bantimurung), on the southeast mainland (Puwato), and on the Islands of Kabaena and Buton. Our analysis of the call of the Peleng tarsier revealed striking similarities with the call of Tarsius dianae. Further morphological analyses are needed to support the proposed new species in south and southeast Sulawesi and to clarify the taxonomic affinity between the central Sulawesi tarsier species Tarsius pelengensis and T. dianae.     

Comparative avian phylogeography of Cameroon and equatorial Guinea mountains: implications for conservation

We illustrate the use of Faith's 'Phylogenetic Diversity' measure to compare the phylogeographic structure of two bird species with patterns of avian endemism across six mountains in Cameroon and Equatorial Guinea. The Mountain Greenbul and Cameroon Blue-headed Sunbird showed phylogeographic patterns that together defined three biogeographic regions: Bioko, Mt. Cameroon, and the northern mountains of Cameroon. In contrast, the distributions of endemic species were largely a function of geographical distance, with close mountains sharing more endemic species than distant mountains. Moreover, for both species, populations on Mt. Cameroon were distinctive with respect to the ecologically relevant character bill size. Our results, while preliminary, illustrate the utility of a comparative approach for identifying geographical regions that harbour evolutionarily distinct populations and caution against using only the distributional patterns of endemics to prioritize regions for conservation. Results show that patterns of endemism may not be concordant with patterns of phylogenetic diversity nor morphological variation in a character important in fitness. While incorporation of additional species from unrelated taxa will be necessary to draw definitive conclusions about evolutionarily distinct regions, our preliminary results suggest a conservation approach for the Afromontane region of the Gulf of Guinea that would: (i) emphasize protection of both Bioko and Mt. Cameroon, thereby maximizing preservation of within-species phylogenetic and morphologic diversity; (ii) emphasize protection within the northern mountains to further conserve intraspecific phylogenetic diversity and maximize protection of endemic species.     

Family- and sex-specific vocal traditions in a cooperatively breeding songbird

Although songbirds provide well-known examples of cultural transmission of vocalizations, little is known about this process in species that live in stable social groups. Here I describe complex vocal traditions in a cooperatively breeding songbird, the stripe-backed wren (Campylorhynchus nuchalis). Repertoires of stereotyped calls were recorded from individually marked males and females in cooperative family groups. Males in the same patriline, whether in the same group or in different groups, had call repertoires that were nearly identical. Females in the same matriline also had identical call repertoires; however, female calls never matched the calls of males in the same group or in any nearby groups. Unrelated birds almost never shared calls. Call repertoires are apparently learned preferentially from same-sex relatives within family groups, so that call traditions separately follow patrilines and matrilines. This unique pattern of transmission results in vocal cues that reflect both sex and kinship.     

Microgeographic Variation and Sharing of the Gargle Vocalization and Its Component Syllables in Black-Capped Chickadee (Aves, Paridae, Poecile atricapillus) Populations

Throughout the year during agonistic encounters, black‐capped chickadees (Poecile atricapillus) emit a vocal signal known as the gargle call. Each bird has a repertoire of structurally differing gargle calls; some are shared with others in the local area. As a basis for understanding the cultural evolution of this social signal, we initiated a study of gargle call repertoires of birds living in a narrow belt of continuous riparian habitat occupied throughout by a resident population of chickadees. During two consecutive winter seasons, we sampled repertoires at three locations over a distance of 8.4 km to quantify micro‐geographical variation. Analyses of vocal sharing and population differentiation were carried out on whole gargle calls and on the individual acoustic units (syllables) from which the whole calls are constructed. We analysed 28 380 calls of 46 subjects in the two seasons of study. Birds averaged 7.6 different calls in their gargle repertoires. Calls were composed of about 10 syllables on average. Fifty‐six different syllables were used to construct the calls of all birds. Each study site had some gargle calls unique to the local birds and some that were shared with one or both of the other two sites. There was significantly greater sharing of both calls and syllables among birds within sample sites than between sample sites. The frequencies of the different kinds of gargles and syllables were significantly correlated across the 2 yr of the study, but the correlation was stronger (r² = 0.93) for syllables than for whole gargle calls (r² = 0.61).     

Genetic isolation within the malaria mosquito Anopheles melas

Anopheles melas is a brackish water–breeding member of the Anopheles gambiae complex that is distributed along the coast of West Africa and is a major malaria vector within its range. Because little is known about the population structure of this species, we analysed 15 microsatellite markers and 1161 bp of mtDNA in 11 A. melas populations collected throughout its range. Compared with its sibling species A. gambiae, A. melas populations have a high level of genetic differentiation between them, representing its patchy distribution due to its fragmented larval habitat that is associated with mangroves and salt marsh grass. Populations clustered into three distinct groups representing Western Africa, Southern Africa and Bioko Island populations that appear to be mostly isolated. Fixed differences in the mtDNA are present between all three clusters, and a Bayesian clustering analysis of the microsatellite data found no evidence for migration from mainland to Bioko Island populations, and little migration was evident between the Southern to the Western cluster. Surprisingly, mtDNA divergence between the three A. melas clusters is on par with levels of divergence between other species of the A. gambiae complex, and no support for monophyly was observed in a maximum‐likelihood phylogenetic analysis. Finally, an approximate Bayesian analysis of microsatellite data indicates that Bioko Island A. melas populations were connected to the mainland populations in the past, but became isolated, presumably when sea levels rose after the last glaciation period (≥10 000–11 000 bp ). This study has exposed species‐level genetic divergence within A. melas and also has implications for control of this malaria vector.     

The use of Vocalizations of the Sambirano Mouse Lemur (<Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>) in an Acoustic Survey of Habitat Preference

Primate vocalizations convey a variety of information to conspecifics. The acoustic traits of these vocalizations are an effective vocal fingerprint to discriminate between sibling species for taxonomic diagnosis. However, the vocal behavior of nocturnal primates has been poorly studied and there are few studies of their vocal repertoires. We compiled a vocal repertoire for the Endangered Sambirano mouse lemur, Microcebus sambiranensis, an unstudied nocturnal primate of northwestern Madagascar, and compared the acoustic properties of one of their call types to those of M. murinus and M. rufus. We recorded vocalizations from radio-collared individuals using handheld recorders over 3 months. We also conducted an acoustic survey to measure the vocal activity of M. sambiranensis in four forest habitat types at the study site. We identified and classified five vocalization types in M. sambiranensis. The vocal repertoires of the three Microcebus species contain very similar call types but have different acoustic properties, with one loud call type, the whistle, having significantly different acoustic properties between species. Our acoustic survey detected more calls of M. sambiranensis in secondary forest, riparian forest, and forest edge habitats, suggesting that individuals may prefer these habitat types over primary forest. Our results suggest interspecific differences in the vocal repertoire of mouse lemurs, and that these differences can be used to investigate habitat preference via acoustic surveys.     

THE SOUND SIGNALS OF THE ADULT AVOCET RECURVIROSTRA A VOSETTA DURING THE PERINATAL PHASE

Recordings of Avocet vocalizations were collected from three pairs, using a microphone placed close to nests at the end of incubation in a colony on the French Atlantic coast, in Vendée. From sonagraphic analyses, ten vocal structures were identified and described. Particular attention is given to the internal components of each call in an attempt to demonstrate structural relationships. In terms of general melodic features, three vocal groups are identified: chuckle calls, ascending chirping calls and sustained calls with whistled components. The existence of numerous gradation forms is emphasized. Verification of gestural behaviour at the time of the recordings additionally allows the context of emission to be clarified. It is distinguished thus: parental calls, calls concerned in the maintenance of individual distance and calls produced in the presence of predators. Finally, the Avocet sound signals are compared with those of other species, mainly waders.