Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests

Two sympatric species of galago,Galago zanzibaricus andG. garnettii, differed significantly in diet (judged mainly by fecal analysis) and substrate use at each of two coastal forest sites in Kenya. The larger-bodiedG. garnettii tended to use branches of a bigger diameter and to be found higher in the canopy than the smallerG. zanzibaricus. The latter species spent most of its time in the thick undergrowth. The larger species ate more fruit than the smaller. There were differences between the species in the type of invertebrate prey remains found in the feces. It is suggested that the differences in habitat use were influenced by the different body sizes of the two galagos, which so enabled these closely related species to coexist. Order of authorship is alphabetical.     

Social organization of Galagos in Kenyan coastal forests: II. Galago garnettii

The social organization of Galago garnettii was studied for the first time and the study included data from two different sites in the coastal forests of Kenya. A combination of mark-recapture and radio-tracking techniques was used to investigate patterns of inter- and intrasexual home range overlap. Patterns of range use were established by radio tracking focal individuals. Adult females of different ages shared highly overlapping ranges, while like-aged females showed little range overlap. Females matured and had their first infants in their natal ranges. Adult males' ranges were larger than those of females and overlapped them extensively. Resident adult males showed little range overlap with each other, unless they were of different ages. Turnover of males was frequent in both populations. Males probably dispersed from their natal ranges. Adults rarely slept together. The social organization of G. garnettii is relatively similar to that of the closely related G. crassicaudatus of southern Africa but contrasts with that of its sympatric congener, G. zanzibaricus. The differences and similarities between these three species are discussed in relation to diet and body size.     

Social organization of Galagos in Kenyan coastal forests: I. Galago zanzibaricus

The social organization of Galago zanzibaricus was studied for the first time and the study included data from two different sites in the coastal forests of Kenya. A combination of mark-recapture and radio-tracking techniques was used to investigate patterns of inter- and intrasexual home range overlap. Associations in sleeping groups indicated social ties between individuals. Patterns of range use were established by radio-tracking focal individuals. Adult males generally had nonoverlapping ranges, shared with one or two females and their offspring with which the male regularly slept. Young females remained longer in their natal ranges than males and reproduced within their natal ranges. Range size and distance traveled per night were similar between the sexes; both sexes probably defended territories. None of the other galago (bushbaby) species studied to date show the degree of close male-female association found in G. zanzibaricus. This study thus extends the variety of social organization documented in nocturnal prosimians.     

Distribution of erythrocytic allozymes in two sibling species of greater galago [Galago crassicaudatus E. Geoffroy 1812 and G. garnettii (Ogilby 1838)]

This study investigated the use of erythrocyte enzymes as indicators of the presence or absence of gene flow between the sibling species G. crassicaudatus and G. garnettii. Fifty-five animals deriving from 14 different source populations were included in the analyses. In addition to hemoglobin, eight enzyme systems were examined: acid phosphatase, adenylate kinase, carbonic anhydrase II, esterase D, glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, peptidase A, and peptidase B. of these, adenylate kinase, glucose-6-phosphate dehydrogenase, hemoglobin, peptidase A, and peptidase B showed no interspecific or intraspecific variation. Esterase D was polymorphic in certain populations of G. crassicaudatus but not in others or in G. garnettii. Acid phosphatase and 6-phosphogluconate dehydrogenase were polymorphic in G. garnettii but monomorphic in all G. crassicaudatus populations. The taxa showed fixation for different alleles at the carbonic anhydrase II locus, indicating a lack of gene exchange between the taxa. We suggest that acid phosphatase, 6-phosphogluconate dehydrogenase, and carbonic anhydrase II may be used as genetic markers in the identification of these two taxa.     

Isolation of females prior to parturition reduces neonatal mortality in Galago

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effects of isolation of pregnant females on neonatal mortality rates. Isolation significantly decreased neonatal mortality rates in all three species over neonatal mortality rates in infants born to unisolated females. The frequency of cannibalism of infants did not differ between isolated and unisolated females. Secondary sex ratio differed significantly from 1:1 for all three species, but higher mortality in males in the first 10 days of life resulted in sex ratios that did not differ from 1:1 in G. garnettii and G. crassicaudatus.     

Loud calls ofGalago crassicaudatus andG. garnettii and their relation to habitat structure

Long distance vocalizations have been shown to be good indicators of genetic species in primates. Here the loud calls of two recently identified greater galago taxa —Galago crassicaudatus andG. garnettii — are compared and analyzed statistically. Observed differences in call structures are investigated further as potential indicators of differences in the structures of habitats frequented by the two species. Although the calls share a repetitive structure, and show similar dominant frequency bands (1,000 – 1,500 Hz), they differ significantly in the number of units per call, unit duration, inter-unit interval, highest frequency, lowest frequency, dominant frequency band, first harmonic, and call duration. The duration of theG. crassicaudatus call is more than twice that ofG. garnettii. Strong intraspecific consistency is seen in the most energetic frequency bands (dominant frequency band and first harmonic), and durations of the individual units and inter-unit intervals. Information important to species recognition is thus most likely to be contained in these features. Individual recognition may be encoded in the relative emphasis of higher level harmonics. The frequency structures of the calls will reflect requirements for acoustical transmission in a forest environment, as well as structural constraints imposed by body size. Higher frequencies detected in theG. garnettii call (up to 8,500 Hz) may have a functional significance related to distance estimation, or may simply be a reflection of smaller body size. The greater modulation of theG. garnettii call suggests that its habitat constitutes a denser or more turbulent medium for sound transmission than does the habitat ofG. crassicaudatus.     

The use of hair morphology in the classification of galagos (Primates, subfamily galagoninae)

The outer epidermal hair structure of bushbabies or galagos varies considerably between genera and species. Comparative morphology can therefore be useful in taxonomic studies, particularly when assessing the true status of newly nominated or misclassified species. Quantitative measurements of outer epidermal hair scales (scale frequency and scale complexity) were made for populations representing 13 taxa within the subfamily Galagoninae. Intraspecific variations in both measures of hair morphology were relatively minor. By contrast, significant interspecific differences were observed, even between closely related, well-established species (e.g. in the greater galagosOtolemur crassicaudatus andO. garnettii and lesser galagosGalago senegalensis andGalago moholi). Assessment of scale frequency resulted in the recognition of all species of the greater and needle-clawed galago genera and added support for nomination to species status of two former subspecies (O. argentatus andE. pallidus). Similar divisions were made in the lesser and dwarf galagos with respect to scale complexity. Possible explanations for the differences in outer epidermal hair scales are discussed. Characteristics of outer epidermal hair scales provide a useful guide to species identity in the subfamily Galagoninae, and the same may prove to be true for other groups of nocturnal mammals.     

Reproductive and dietary parameters in wild greater galago populations

Information concerning habitat, body size, reproductive status, and diet was recorded from 348 greater galagos, captured at six different localities in Tanzania and southern Africa between 1953 and 1955. The localities extended from Pemba Island in the north to Chikwawa, Malawi, in the south and varied broadly in the same order in degree of climatic aridity— from well-watered clove and coconut plantations to seasonally very dry woodland. Animals from the three northern localities fell within the geographic range of Galago garnettii,while the rest were assumed to be G. crassicaudatus.Statistical analysis of body size parameters confirmed this allocation. Data on fetal occurrence, vaginal and labial condition, and lactation indicate a restricted breeding season for both species, with peak proportions in estrus in August in G. garnettiiand in May-July in G. crassicaudatus.Gut content data indicate a variety of foods, with a preponderance in the northern localities of soft fruit such as mango, pawpaw, and coconut pulp; gum was a major carbohydrate source in the southernmost localities. Contrary to expectations, tooth damage, in the form of both loss and breakage, was much more prevalent in G. garnettiithan in G. crassicaudatus.The teeth most commonly lost were the upper incisors— perhaps because of the high acid and sugar content of a frugivorous diet. The high incidence of breakage of the lower incisors and upper canines indicates the inclusion of hard-shelled food sources in the diet of G. garnettii.     

Metabolism during starvation/dehydration stress in two species of galagos

Two species of galagos (G. senegalensis moholi andG. garnettii) were subjected to dehydration and starvation stress in order to determine whether, as is common in other animals, these hypometabolic prosimians would lower their metabolic rate even further. Dehydration was confirmed by losses in body mass, a decrease in fecal water content and a rise in urine osmolality. At the height of dehydration, 20 to 25% reduction in body mass, 30 to 40% reduction in fecal water content and urine osmolality ranging from 1.8 to 3.5 Osmol kg⁻¹ H₂O, were recorded in some of the animals. Basal metabolic rate of 0.536 ml O₂ (g·h)⁻¹ inG. s. moholi and 0.302 ml O₂ (g·h)⁻¹ inG. garnettii were recorded, representing 50 to 42% reduction in metabolic rate, respectively, compared with mass specific values. In none of the tested animals did we observe significant reduction in basal metabolism during dehydration/starvation stress compared with the rates observed during the control period. Basal metabolism in the bushbabies seems to have reached the lowest level and no further adjustment is apparently possible as a strategy for energy saving during starvation and/or dehydration stress.     

The use of hand morphology in the taxonomy of galagos

Measurements of volar (hand) pad area were made for 244 specimens, representing 12 species and 4 genera of galagos (sub-family Galaginae). When corrected for body weight, statistically significant differences were identified, at both the genus and species levels in the areas of the volar pads. Most informative, in terms of taxonomic differences, were measurements of two of the five pads; interdigjtal pad number 4 and thenar pad number 5. Closely related species were distinguishable on the basis of these measurements. The thick-tailed galago (Otolemur crassicaudatus) was separate from Garnett's galago (O. garnettii) and the specific status of the silver greater galago (O. argentatus) was supported. Likewise, the two needle-clawed galagos (Euoticus elegantulus andE. pallidus), recently separated on mitochodrial DNA grounds, were found to differ significantly in their volar pad morphology. These studies show that comparative studies of volar hand pad morphology provide a novel approach to the re-assessment of galago taxonomy, and may be applicable also in taxonomic studies of other prosimian groups.     

Mother-infant cannibalism in thick-tailed bushbabies (Galago crassicaudatus umbrosus)

Mother-infant cannibalism in species of galagos as in several other species of non-human primates is a common phenomenon. In non-human primates kept in laboratory conditions many of the observed cases of cannibalism were not associated with starvation and with infanticide. Cannibalism in galagos was observed in at least five different species. In several laboratories, like the Duke University Primate Center, the frequencies of cannibalism in galagos species in captivity have been reduced by the isolation of pregnant female before the parturition from her companions, especially adult males. At the Primate Behaviour Research Group (University of Witwatersrand, Johannesburg, South Africa) three cases of cannibalism were observed in twoGalago crassicaudatus umbrosus' mothers before the end of the third day after birth. To understand the reasons why the mothers cannibalize their own infants, it was decided to analyze the mother-infant interaction which preceded the death of the infants. InGalago crassicaudatus twin and triplet births are very common. In one of our two observed mothers who cannibalized their infants, there was one triplet birth. In this study the two pregnant females were isolated in two separated cages ten days before giving birth. One of the two observed mothers gave birth to triplets, the other had a single birth. At the end all four infants were cannibalized. In all cases the cannibalization started after the infant's death. The infants' deaths were caused by lack of maternal care which caused them to starve. The results show that the triplet's mother differed in some of her behaviour towards her infants. In one of the cannibalized infants behaviours such asNipple andMother Passive Prevent were never seen before death. In our cases it seems that cannibalism was probably due to the laboratory condition that for generation to generation caused stress to the mothers and changed their maternal behaviours, which lead to the death of the offspring which after death became a consumable resource.     

Space-time diversification of Androcymbium Willd. (Colchicaceae) in western South Africa

 We examined patterns of cpDNA RFLP variability using 21 restriction endonucleases in 21 populations of Androcymbium that represent 12 endemic species distributed in the winter rainfall areas of South Africa to explore the diversification of the genus in its area of maximum species diversity. Our results are supportive of a diversification landscape characterized by continued opportunistic short-range invasion, naturalization, and rapid speciation, in which the selective action of the different environments where Androcymbium species occur determined their colonization success and subsequent short-range geographic expansion. The historical presence of fire, the constraint imposed by the low concentration of nutrients throughout southwestern South Africa and the different reproductive capabilities of Androcymbium species have also likely stimulated species' diversification. Our divergence time estimates bolster the view that speciation of South African Androcymbium initiated in the late Eocene, intensified in the Oligocene and proceeded more sporadically during the Miocene. These chronological estimates also substantiate the previous hypothesis that most lineages of Androcymbium in South Africa are much more ancient than their North African relatives, whose diversification began in the late Miocene-early Pliocene. Received July 25, 2001 Accepted December 6, 2001     

Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships

A comparative bioacustic analysis of vocalizations of the prosimian subfamily Galaginae revealed that morphologically similar sibling taxa within the main groups of the lesser galagos and the greater galagos can be reliably identified phenotypically on the basis of the acoustic structure of their loud call or advertisement call. Results confirm the separation of two distinct species of greater galagos, Galago crassicaudatus and Galago garnettii, and strongly suggest the discrimination of three distinct species from the senegalensis lesser bushbaby group, Galago senegalensis, Galago moholi and Galao zanzibaricus. An investigation of the ontogenetic development of the loud call indicated that it is derived from the infant's isolation call, displaying in all studied bushbaby taxa a fairly similar acoustic pattern. Shared acoustic characters of the loud call among the different taxa as well as the infant's isolation call were used to propose a hypothesis about the phylogenetic affinities in bushbabies. The results seem to be supported by recent fossil records.     

Annual cycles are the most common reproductive strategy in African tropical tree communities

We present the first cross‐continental comparison of the flowering and fruiting phenology of tropical forests across Africa. Flowering events of 5446 trees from 196 species across 12 sites and fruiting events of 4595 trees from 191 species across 11 sites were monitored over periods of 6 to 29 years and analyzed to describe phenology at the continental level. To study phenology, we used Fourier analysis to identify the dominant cycles of flowering and fruiting for each individual tree and we identified the time of year African trees bloom and bear fruit and their relationship to local seasonality. Reproductive strategies were diverse, and no single regular cycle was found in >50% of individuals across all 12 sites. Additionally, we found annual flowering and fruiting cycles to be the most common. Sub‐annual cycles were the next most common for flowering, whereas supra‐annual patterns were the next most common for fruiting. We also identify variation in different subsets of species, with species exhibiting mainly annual cycles most common in West and West Central African tropical forests, while more species at sites in East Central and East African forests showed cycles ranging from sub‐annual to supra‐annual. Despite many trees showing strong seasonality, at most sites some flowering and fruiting occurred all year round. Environmental factors with annual cycles are likely to be important drivers of seasonal periodicity in trees across Africa, but proximate triggers are unlikely to be constant across the continent.     

Galago locomotion in Kibale National Park, Uganda

Very few locomotor studies have been conducted on galagos. This is surprising given their interesting anatomy and ecology, as well as their increasing species diversity. In this study we investigated locomotion and postures in two sympatric galagos species (Galagoides thomasi and Galago matschiei) living in Kibale National Park, Uganda. G. thomasi uses arboreal quadrupedalism and leaping, while G. matschiei is more leaping-oriented. Both species utilize small oblique branches in the mid-canopy. These similarities in substrate use are most likely due to the similar body sizes and anatomies of the two species, as well as to the structure and availability of trees in Kibale National Park. Lastly, we compare the locomotor patterns of G. thomasi and G. matschiei with those observed in the few other quantitative locomotor studies available for galagos.     

The taxonomic status and distribution of Bushbabies in Malawi with emphasis on the significance of vocalizations

The debated identity of a small forest bushbaby in Malawi is resolved by a short-term field study of the animals’ behavior. Locomotor styles, calling patterns, and the structure of advertising calls confirm that the species is Galago zanzibaricusrather than G. demidoffor G. thomasi.A detailed comparison of acoustic structure between the Malawi animals and G. zanzibaricusin Kenya demonstrates a degree of between-population variation, although the calls remain conservative in those parameters expected to aid recognition of conspecifics. Distribution records extend the known geographical range of G. zanzibaricusover most of the northern half of Malawi. Further studies are required to link the animals from this region with either of the previously recognized subspecies: G. z. zanzibaricusfrom East Africa or G. z. grantifrom southern Malawi, Mozambique, and Zimbabwe.     

Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair

Carbon and nitrogen stable isotope ratios were measured in hair samples from two species of Galago from Gedi Ruins National Monument in eastern Kenya and from Lepilemur leucopus from Beza Mahafaly Special Reserve in southern Madagascar. Forest structure was generally similar in the two areas but average rainfall was lower in Madagascar. Species average ¹³C values varied with feeding height in the forest canopy and with average rainfall level as expected from reported variation in plant ¹³C values. G. garnettii, which feeds higher in the forest canopy, had less negative ¹³C values than G. zanzibaricus, which spends more time below 5 m. L. leucopus, from a drought-afflicted forest, had less negative hair ¹³C values than the two galago species. The values within the Lepilemur sample showed a positive linear relation with percent dependence on a CAM tree species and with xeric conditions within the species reserve. Nitrogen stable isotope ratios varied with trophic level of feeding and with time spent feeding on leguminous plants. The insectivorous galagos had significantly more positive ¹⁵N values than the folivorous L. leucopus. Within the Lepilemur sample, ¹⁵N values varied inversely with the percent of feeding time spent on leguminous plants. The range of ¹⁵N and ¹³C values in each of the prosimian species is larger than reported for animals fed monotonous diets and for New World monkey species. The monkey species feed as groups of individuals whereas the prosimians have solitary feeding habits. The ranges in the prosimian species apparently reflect the greater variation in diet among individual prosimians compared to individual monkeys. The isotope data reported here are equivalent, on average, to those reported for other arboreal species from similar forest habitats and with similar dietary habits. This supports the use of such data for paleoecological reconstruction of forest and woodland systems and diet reconstruction of extinct primate populations and species. Received: 18 April 1997 / Accepted: 11 August 1997     

Lactation length in three species of Galago

Milk expression was used to determine lactation length in three species of Galago at the Duke University Primate Center. Lactation length in G. senegalensis moholi was significantly shorter than the lactation length of either G. garnettii or G. crassicaudatus, but lactation length did not differ between G. garnettii or G. crassicaudatus. Litter size had no significant effect on lactation length. The lactation lengths determined in this study are substantially longer than those reported by investigators who used observational techniques. These discrepancies may be partially explained by failure to observe nursing during the diurnal inactive period.     

Convergence and contingency in production–precipitation relationships in North American and South African C4 grasslands

Mesic grasslands in North America and South Africa share many structural attributes, but less is known of their functional similarities. We assessed the control of a key ecosystem process, aboveground net primary production (ANPP), by interannual variation in precipitation amount and pattern via analysis of data sets (15- and 24-year periods) from long-term research programs on each continent. Both sites were dominated by C₄ grasses and had similar growing season climates; thus, we expected convergence in precipitation–ANPP relationships. Lack of convergence, however, would support an alternative hypothesis—that differences in evolutionary history and purportedly greater climatic variability in South Africa fundamentally alter the functioning of southern versus northern hemisphere grasslands. Neither mean annual precipitation nor mean ANPP differed between the South African and North American sites (838 vs. 857 mm/year, 423.5 vs. 461.4 g/m² respectively) and growing season precipitation–ANPP relationships were similar. Despite overall convergence, there were differences between sites in how the seasonal timing of precipitation affected ANPP. In particular, interannual variability in precipitation that fell during the first half of the growing season strongly affected annual ANPP in South Africa (P < 0.01), but was not related to ANPP in North America (P = 0.098). Both sites were affected similarly by late season precipitation. Divergence in the seasonal course of available soil moisture (chronically low in the winter and early spring in the South African site vs. high in the North American site) is proposed as a key contingent factor explaining differential sensitivity in ANPP to early season precipitation in these two grasslands. These long-term data sets provided no support for greater rainfall, temperature or ANPP variability in the South African versus the North American site. However, greater sensitivity of ANPP to early season precipitation in the South African grassland suggests that future patterns of productivity may be more responsive to seasonal changes in climate compared with the North American site.     

Speciation in the greater galagos (Prosimii: Galaginae): review and synthesis*

A marked morphological and genetical discontinuity among the greater galagos points to the existence of two genetical species within the taxon, Galago crassicaudatus E. Geofl'roy 1812. This contribution investigates the conditions surrounding this speciation event, and places it within a phylogenetic context. Information pertaining to body size, litter size, sexual dimorphism, locomotor mode and karyotypic structure is assessed. It is hypothesized that G. crassicaudatus diverged from its more gracile sibling, G. garnettii, approximately 2 million years ago, in respotise lo the increasing aridification of Africa that accompanied the Northern Hemisphere Pleistocene glaciations.