The subspecies concept in primatology: The case of mountain gorillas

The criteria for the application of subspecific units in living primate populations have received little attention relative to other vertebrate taxa, even though they have important implications for conservation strategies for many nonhuman primate populations. One of the most critically endangered primates is the mountain gorilla,Gorilla gorilla beringei, of which 600 animals exist in east-central Africa. FollowingSarmiento et al. (1996), taxonomists have proposed splitting these populations into two subspecies as part of a revised taxonomy of the genusGorilla. In this paper I review the application of the subspecies concept in primatology, using the gorillas of Bwindi Impenetrable National Park and the Virungas as case studies. An examination of genetic, morphological, biogeographic, ecological, and behavioral evidence indicates that reclassifying Bwindi gorillas as taxonomically distinct from those in the Virungas is not well supported and needs further study. Because taxonomy provides the basis of conservation management policies, a cautious and conservative approach to the subspecies question is warranted in the case of endangered primate populations.     

The evolution of intraspecific variation in social organization

Many species show intraspecific variation in their social organization (IVSO), which means the composition of their social groups can change between solitary living, pair living, or living in groups. Understanding IVSO is important because it demonstrates species resilience to environmental change and can help us to study ultimate and proximate reasons for group living by comparing solitary and group‐living individuals in a single species. It has long been realized that the environment plays a key role in explaining the occurrence of IVSO. IVSO is expected to have evolved in variable environments and can thus be a key adaptation to environmental change. It has previously been suggested that four different mechanisms relying on the environment exist that can lead to IVSO: environmental disrupters, genetic differentiation, developmental plasticity, and social flexibility. All four mechanisms depend on the environment such that focusing only on environmental factors alone cannot explain IVSO. Importantly, only three represent evolved mechanisms, while environmental disrupters leading to the death of important group members induce nonadaptive IVSO. Environmental disrupters can be expected to cause IVSO even in species where IVSO is also an adaptive response. Here, we focus on the questions of why IVSO occurs and why it evolved. To understand IVSO at the species level, it is important to conduct continuous long‐term studies to differentiate between nonadaptive and adaptive IVSO. We predict that IVSO evolves in environments that vary in important ecological variables, such as rainfall, food availability, and population density. IVSO might also depend on life history factors, especially longevity. IVSO is predicted to be more common in species with a short life span and that breed only for one breeding season, being selected to respond optimally to the prevailing environmental situation. Finally, we emphasize the importance of accounting for IVSO when studying social evolution, especially in comparative studies, as not every species can be assigned to one single form of social organization. For such comparative studies, it is important to use data based on the primary literature.     

Impact of ecological and social factors on ranging in western gorillas

We examined the influence of ecological (diet, swamp use, and rainfall) and social (intergroup interaction rate) factors on ranging behavior in one group of western gorillas (Gorilla gorilla gorilla) during a 16-month study. Relative to mountain gorillas, western gorillas live in habitats with reduced herb densities, more readily available fruit (from seasonal and rare fruit trees), and, at some sites, localized large open clearings (swamps and "bais"). Ranging behavior reflects these ecological differences. The daily path length (DPL) of western gorillas was longer (mean=2,014 m) than that of mountain gorillas, and was largely related to fruit acquisition. Swamp use occurred frequently (27% of days) and incurred a 50% increase in DPL, and 77% of the variation in monthly frequency of swamp use was explained by ripe fruit availability within the swamp, and not by the absence of resources outside the swamp. The annual home-range size was 15.4 km2. The western gorilla group foraged in larger areas each month, and reused them more frequently and consistently through time compared to mountain gorillas. In contrast to mountain gorillas, intergroup encounters occurred at least four times more frequently, were usually calm rather than aggressive, and had no consistent effect on DPL or monthly range size for one group of western gorillas. High genetic relatedness among at least some neighboring males [Bradley et al., Current Biology, in press] may help to explain these results, and raises intriguing questions about western gorilla social relationships.     

Functional variation among frugivorous birds: implications for rainforest seed dispersal in a fragmented subtropical landscape

Seed dispersal plays a critical role in rainforest regeneration patterns, hence loss of avian seed dispersers in fragmented landscapes may disrupt forest regeneration dynamics. To predict whether or not a plant will be dispersed in fragmented forests, it is necessary to have information about frugivorous bird distribution and dietary composition. However, specific dietary information for frugivorous birds is often limited. In such cases, information on the seed-crushing behaviour, gape width and relative dietary dominance by fruit may be used to describe functional groups of bird species with respect to their potential to disperse similar seeds. We used this information to assess differences in the seed dispersal potential of frugivorous bird assemblages in a fragmented rainforest landscape of southeast Queensland, Australia. The relative abundance of frugivorous birds was surveyed in extensive, remnant and regrowth rainforest sites (16 replicates of each). Large-gaped birds with mixed diets and medium-gaped birds with fruit-dominated diets were usually less abundant in remnants and regrowth than in continuous forest. Small-gaped birds with mixed diets and birds with fruit as a minor dietary component were most abundant in regrowth. We recorded a similar number of seed-crushing birds and large-gaped birds with fruit-dominated diets across site types. Bird species that may have the greatest potential to disperse a large volume and wide variety of plants, including large-seeded plants, tended to be less abundant outside of extensive forests, although one species, the figbird Sphecotheres viridis, was much more abundant in these areas. The results suggest that the dispersal of certain plant taxa would be limited in this fragmented landscape, although the potential for the dispersal of large-seeded plants may remain, despite the loss of several large-gaped disperser species.     

Seasonal change in the composition of the diet of eastern lowland gorillas

Details are presented of the composition of the diet of eastern lowland gorillas, derived mainly from a study of their fresh trails and fecal analysis, during the course of an entire year in the tropical lowland forests of the Itebero region, Zaire. Gorillas ate 194 plant foods from 121 species and 45 families. They consumed 48 species of fruits; and 89% of fecal samples contained fruit seeds, but fruits were a relatively small part (25%) of the total number of food items. The composition of their diet changed seasonally. When consumption of fruit decreased in the long rainy and the long dry seasons, the gorillas ate, in addition to Zingiberaceae and Marantaceae, many kinds of leaf and bark, which may be an important buffer against the shortage of fruits. Gorillas also fed regularly on ants (Ponerinae), and the frequency of consumption showed small seasonal variations. From a comparison of diet composition, eastern lowland gorillas appeared to be intermediate between the other two subspecies. The choice of food showed differences in preference of fruits and insects between subspecies and may reflect high similarities within subspecies in lowland and montane forests.     

Domestic pigs alter their social strategy in response to social group size

In a series of studies, we investigated the concept that domesticated pigs may adopt cost efficient social strategies, in which individuals become less aggressive due to a higher number of potential competitors, in large social groups. Six blocks, each comprising four pens of 18 pigs (small group, SG) and two pens of 108 pigs (large group, LG) were used. Pigs were 11 weeks old at the initial group formation. Weeks 1, 6 and 12 following SG and LG formation, two randomly selected pigs with SG or LG social experience were incorporated into another SG or LG for a period of 2 h and the aggressive behaviour of pigs was observed. Four test combinations were used (SG to SG (SS), SG to LG (SL), LG to SG (LS) and LG to LG (LL)). There was less aggression in the LL compared to SS, SL and LS combinations (1.6% versus 2.5, 2.3, and 2.5% of time, respectively, P = 0.009). Furthermore, 8 weeks following SG and LG formation, a total of 200 pigs were regrouped for 2 h in groups of four in a neutral test arena to assess the effect of prior social experience (SG vs. LG) on aggressive behaviour. Pigs were regrouped with their own group members (familiar), or with unfamiliar non-group members either from SG or LG. Five test combinations were used (four pigs from the same SG (S), four pigs from the same LG (L), two pigs from a SG and two pigs from a LG (SL), two pigs each from two different LG (LL) and two pigs each from two different SG (SS)). Pigs derived from SG fought aggressively (duration, s) with unfamiliar pigs, compared to those derived from LG (4.9, 6.7, 16.1, 12.1 and 9.5 s for S, L, SS, SL and LL test combinations respectively, P < 0.001). In addition, the latency to initiate first aggressive interaction was shorter (duration, s) in SS than LL treatment combination (23.3, 22.5, 10.8, 11.8 and 19.2 s for S, L, SS, SL and LL test combinations respectively, P = 0.008). Taken together, our results suggest that pigs become less aggressive and may shift to a low-aggressive social strategy in large social groups. This may provide potential benefits for welfare of pigs under commercial production situations.     

Playing together,laughing together: rapid facial mimicry and social sensitivity in lowland gorillas

In nonhuman animals, the phenomenon of rapid facial mimicry (RFM)—the automatic, involuntary, and rapid (<1 s) replication of others’ facial expressions—has been mainly investigated in the playful domain. In immature lowland gorillas Gorilla gorilla gorilla both play face (PF) and full PF (FPF) are rapidly mimicked between the players. This makes the species suitable to test hypotheses on the factors influencing RFM during play. The observations on 3 captive groups of lowland gorillas (N = 27) revealed that contrary to expectations, the closeness of social bond negatively influenced the occurrence of RFM but it did not affect either RFM latency or its overlapping index (OVERLAP). RFM was affected by the degree of symmetry of play fighting: the more balanced the session, the higher the occurrence of RFM. Players of the same sex class responded faster than players of different sex. These findings suggest that RFM may help synchronizing behaviors of playmates matching in size (same-sex) and promote symmetric playful interactions. “Laughing together” (measured by the RFM OVERLAP) lasted longer when the responder perfectly mirrored the partner expression (PF→PF; FPF→FPF). If PF and FPF convey information on the different play roughness degree, through “laughing together” the players could coordinate their actions and share positive moods and playful intensity. If the perfect congruency in the motor resonance, also known as social sensitivity, can foster a possible emotional dialogue between gorillas remains to be investigated.     

Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic

The objectives of this 27 month study were to document the positional behaviors used by lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic and to compare the effects of body size dimorphism on the use of arboreal substrates. During this study, despite their great size, all gorillas used trees regularly. Predictions concerning the relationship of body size to arboreal behavior were generally upheld. Small branch and suspensory activities were rare for silverbacks. Females used smaller and multiple substrates and suspensory postures more frequently than males. Although females foraged in the periphery of trees, males stayed close to the cores and rarely used terminal branches. In addition to body size, this study found that party size, social rank, and tree structure all influence an animal's substrate choice and subsequent positional activities. Lone males typically remained in the cores of trees where substrates are large. Group males may have been forced to use all parts of trees because others were present. Lone males used small crown trees which provided easy access to terminal branch foods. Males and females foraging together used larger trees (containing more feeding sites) than single sex groups. Female positional behavior may have been affected by the presence of males. When apart from males, females used the cores of trees and larger substrates more than when foraging with males. As habitat and social context both influence substrate use, they should be considered essential components of body-sized based interpretations of the behavior of fossil or extant species. © 1995 Wiley-Liss, Inc.     

Fission-fusion and the evolution of hominin social systems

The course of hominin evolution has involved successive migrations towards higher absolute latitudes over the past three million years. Poorer habitat quality further from the equator has led to the necessity for groups occupying higher latitudes to live at lower population densities. Coupled with a trend towards increasing group size over this time period, this tendency towards expansion has led to exponential increases in the area requirements of hominin groups, and a concomitant need to adjust foraging patterns. The current analyses suggest that the development of increasingly complex, multi-level fission-fusion social systems could have freed hominins of the foraging constraints imposed by large group sizes and low population densities. Analyses of the fossil record suggest latitudinally-driven differences in area requirements of the australopithecines from East and South Africa, and African and Asian Homo erectus. In contrast, chronologically-driven differences appear between H. erectus as a whole and Homo heidelbergensis, and between H. heidelbergensis and the Neanderthals. These results are discussed in relation to studies of the foraging patterns of primates and hunter-gatherers.     

Population structure and group composition of western lowland gorillas in North‐Western Republic of Congos

Population studies are an essential part of conservation actions. Under exceptional observation conditions we studied a western lowland gorilla population visiting the Maya salt‐clearing (north of the Parc national d'Odzala, P.N.O., Congo) over an 8 month period; 36 groups and 18 solitary individuals (a total of 420 individuals) have been identified visiting the clearing, which suggests a high gorilla density in the region. Ninety‐six percent of the gorillas entered the clearing in groups. One‐male groups had a mean size of 11.2. Ninety percent of solitary individuals were silver‐back males. Compared with other populations of both lowland gorillas and mountain gorillas, the Maya population had the highest immature rate and the highest number of infants per female. Ecological correlates that could explain the attractiveness of the Maya clearing are discussed. The present status and the renewal rate of the Maya population indicate the need for further studies and confirm the importance of developing eco‐tourism in this region as part of the sustainable park management activities developed by the ECOFAC programme (European Union). The results also provide arguments to support the proposal for extending the P.N.O. to include this region, which is rich in salt‐clearings and attracts many other key‐species of mammal such as forest elephants. Am. J. Primatol. 48:1–14, 1999. © 1999 Wiley‐Liss, Inc.     

Interspecific variation in egg testosterone levels: implications for the evolution of bird song

Although interspecific variation in maternal effects via testosterone levels can be mediated by natural selection, little is known about the evolutionary consequences of egg testosterone for sexual selection. However, two nonexclusive evolutionary hypotheses predict an interspecific relationship between egg testosterone levels and the elaboration of sexual traits. First, maternal investment may be particularly enhanced in sexually selected species, which should generate a positive relationship. Secondly, high prenatal testosterone levels may constrain the development of sexual characters, which should result in a negative relationship. Here we investigated these hypotheses by exploring the relationship between yolk testosterone levels and features of song in a phylogenetic study of 36 passerine species. We found that song duration and syllable repertoire size were significantly negatively related to testosterone levels in the egg, even if potentially confounding factors were held constant. These relationships imply that high testosterone levels during early development of songs may be detrimental, thus supporting the developmental constraints hypothesis. By contrast, we found significant evidence that song-post exposure relative to the height of the vegetation is positively related to egg testosterone levels. These results support the hypothesis that high levels of maternal testosterone have evolved in species with intense sexual selection acting on the location of song-posts. We found nonsignificant effects for intersong interval and song type repertoire size, which may suggest that none of the above hypothesis apply to these traits, or they act simultaneously and have opposing effects.     

Intrapopulation differences in ant eating in the mountain gorillas of Bwindi Impenetrable National Park, Uganda

Variability in ant eating has been observed in several populations of eastern and western gorillas. We investigated the occurrence of ant (Dorylus sp.) eating in two groups of mountain gorillas (Gorilla beringei beringei) with overlapping home ranges within Bwindi Impenetrable National Park, Uganda from September 2001 to August 2002. We calculated the frequency of ant eating by an indirect method of analyzing fecal samples from silverbacks, adult females, and juveniles. One group consumed ants significantly more often than the other (3.3 vs 17.6% of days sampled). Furthermore, the group that consumed ants more often also consumed them on a seasonal basis (September–February monthly range: 0–8%; March–August monthly range: 30–42.9%). Finally, females and juveniles of this group consumed ants significantly more often than did the silverback (total samples containing ants: silverback, 2.1%; adult female, 13.2%; juvenile, 11.2%). Differences in ant eating between groups are likely due to variability in use of habitats where ants occur (particularly secondary forests). Surveys of ant densities in differing habitats, nutritional analysis of ants, and quantification of the amount of ants in their diets are necessary to understand if ant consumption is due to availability, nutritional value, group traditions, or taste preference.     

Inter-group encounters and female transfer in mountain gorillas: Influence of group composition on male behavior

This paper examines the behaviors used by male gorillas (G. gorilla beringei) to influence female choice during inter-group encounters. Encounters are related to the acquisition of females rather than to the defense of a group's range. Data on 58 independent encounters confirms that encounters are generally aggressive, but that contact aggression is less frequent than previously reported. A high number of potential migrants in one of the groups involved, rather than the newness of either group, predicts the likelihood of contact aggression between males. Encounters with a newly formed unit last longer than encounters involving established groups. Male herding serves to prevent female transfer. Females without dependent offspring are more likely than others to be herded. Proceptive females are the target of herding more often than non-proceptive cycling females. Groups where herding has been observed are more likely to be newly formed, and they include significantly more males. This last result confirms that there are advantages to male cooperation in gorillas. It also raises the question of why such cooperation does not occur more often. © 1993 Wiley-Liss, Inc.     

Play behaviour in lowland gorillas: Age differences,sex differences,and possible functions

A study on lowland gorilla (Gorilla gorilla gorilla) play behaviour was conducted on four exhibits at three different zoological parks so that 19 gorillas were observed. Juvenile gorillas played the most, but play continued at fairly high frequencies through adolescence. Most social play occurred between dyads. Triadic groups usually chased each other. No sex differences in type of play were observed, but gender differences in partner preferences were observed. Males played with both other males and females, while females seldom played together. These data support the social skills hypothesis (Baldwin & Baldwin, 1974) of play. Data were gathered while the author was a graduate student at Tulane University and a visiting lecturer at the University of California, Riverside.     

Baby-transfer and other interactions between its mother and grandmother in a captive social group of lowland gorillas

This report describes the responses of an experienced gorilla mother to inappropriate maternal behavior displayed by her young adult daughter toward a newborn baby and repeated acts of baby-transfer between these two females in a captive social group of lowland gorillas (Gorilla g. gorilla). The quality of infant care by the young adult daughter clearly improved during the first 4 days after birth, and this improvement was at least partly based on her mothers encouragement. Thus, the mothers activities can be considered scaffolding for her daughter with regard to maternal infant care.     

Correlates of sexual and maternal competence in captive gorillas

The captive gorilla population may not be self-sustaining, in part because the overall birth rate is low and because many potential founders have failed to reproduce. We used questionnaires to collect standardized biographies of every gorilla held in North America. These biographies were searched for factors associated with reproductive success or failure. Captive-born gorillas are reproducing at least as well as wild-borns, when reproductive success is expressed as number of infants per year of reproductive opportunity. Mother-reared females are reproductively more successful than hand-reared females, but there is no difference in the reproductive success of mother-reared and hand-reared males. Social access to conspecifics in the 1st year is associated with higher reproductive success, at least for females. Reproductively successful and unsuccessful gorillas of both sexes have had equal access to potential mates, but unsuccessful animals are less likely than successful ones to exhibit normal sexual behavior. We conclude that many cases of reproductive failure are due to deficits in sexual behavior, which in turn may result from lack of early social experience with conspecifics. Some reproductive failure involves medical problems; interventive diagnostic techniques continue to be useful, if only to identify healthy individuals that can be managed intensively. The probability that a female will be a competent mother is not affected by her being wild-born or captive-born, or mother-reared or hand-reared.