Inequalities in intraspecific plant–lemur interactions drive seed dispersal patterns

In this paper, I describe how ecological variables (diet, food availability, patch characteristics) and variables unrelated to food availability such as reproduction and territoriality, affect daily and long-term ranging patterns in two primate species in southeastern Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Daily path lengths (DPL), home range size, and the distance traveled between patches were compared and contrasted between lemur species. Rufous lemurs ranged further on a daily and long-term basis than red-bellied lemurs. Group ranges overlapped extensively and rufous lemurs did not defend home range borders. In contrast, red-bellied lemurs maintained exclusive use of their home range and actively defended boundaries. Additionally, rufous lemurs used more scattered patches and traveled further between these patches than red-bellied lemurs Ranging patterns in both lemur species were not correlated with food availability but were influenced by three seasonal variations in diet: the number of food patches visited, dietary diversity, and the number of feeding bouts. Rufous lemurs traveled furthest when each of these variables was highest and coincided to the same time period when females were lactating. A similar seasonal peak in red-bellied lemurs ranging patterns was not observed although they traveled further when daily diet was more diverse. It is suggested that the presence of several reproductively active females in rufous lemur groups may influence food choice and consequently, ranging patterns. In contrast, red-bellied lemur’s territoriality may limit group movements and constrain daily and seasonal ranging.

Networks of mutualistic interactions between animals and plants are considered a pivotal part of ecological communities. However, mutualistic networks are rarely studied from the perspective of species-specific roles, and it remains to be established whether those animal species more relevant for network structure also contribute more to the ecological functions derived from interactions. Here, we relate the contribution to seed dispersal of vertebrate species with their topological role in frugivore-plant interaction networks. For one year in two localities with remnant patches of Colombian tropical dry forest, we sampled abundance, morphology, behaviour and fruit consumption from fleshy-fruited plants of various frugivore species. We assessed the network topological role of each frugivore species by integrating their degree of generalization in interactions with plants with their contributions to network nestedness and modularity. We estimated the potential contribution of each frugivore species to community-wide seed dispersal, on the basis of a set of frugivore ecological, morphological and behavioural characteristics important for seed dispersal, together with frugivore abundance and frugivory degree. The various frugivore species showed strong differences in their network structural roles, with generalist species contributing the most to network modularity and nestedness. Frugivores also showed strong variability in terms of potential contribution to seed dispersal, depending on the specific combinations of frugivore abundance, frugivory degree and the different traits and behaviours. For both localities, the seed dispersal potential of a frugivore species responded positively to its contribution to network structure, evidencing that the most important frugivore species in the network topology were also those making the strongest contribution as seed dispersers. Contribution to network structure was correlated with frugivore abundance, diet and behavioural characteristics. This suggests that the species-level link between structure and function is due to the fact that the occurrence of frugivore-plant interactions depends largely on the characteristics of the frugivore involved, which also condition its ultimate role in seed dispersal.

Bird foraging behaviour is a major factor involved in mutualistic interactions of fleshy-fruited plants. Despite much research, we still lack quantified demonstrations of how fruit display traits affect fruit removal behaviour. Although the fruit crop size hypothesis proposes a general mechanism for fruit trait selection, it overlooks the fact that distinctive bird behaviours in a bird assemblage would have different effects on fruit crop size. Here, we show that the relevance of fruit crop size for bird fruit consumption is driven by two basic components of fruit foraging behaviour: fruit handling and residence time. We assessed bird fruit-eating behaviour (fruit consumption, fruit handling and residence time) and its relationship with fruit crop size, taking into account body size and spatial focal context (conspecific neighbour density and distance to the forest edge from individual plants) in a population of Vassobia breviflora (Solanaceae) in Tucumán, Argentina. At the assemblage level, fruit consumption was positively related to fruit crop size and residence time, and the interaction between fruit crop size and residence time depended on fruit-handling behaviour. At the functional group level, both gulpers and pulp consumers showed a positive relationship between fruit consumption and residence time. However, gulpers showed a negative interaction between fruit crop size and residence time, while pulp consumers showed no interaction. At the species level, fruit consumption by Turdus rufiventris (gulper) was positively related to fruit crop size, whereas fruit consumption by Thraupis sayaca and Zonotrichia capensis (pulp consumers) depended positively on residence time. Essentially, gulpers spent short residence times in plants with larger fruit crops, whereas pulp consumers spent long residence times in plants regardless of fruit crop size. The segregation between fruit-eating behaviours and their relationship with fruit crop size suggests that bird functional groups (i.e. gulpers and pulp consumers) would shape fruit display traits with different intensities.

Range overlap and spatiotemporal relationships of frugivorous lemurs at Kianjavato, Madagascar

Primate species face growing risks of extinction throughout the world. To better protect their populations, effective monitoring techniques are needed. The goal of this study was to evaluate the use of arboreal camera traps and occupancy modeling as conservation tools for threatened lemur species. This project aimed to (1) estimate the occupancy and detection probabilities of lemur species, (2) investigate factors potentially affecting lemur habitat use, and (3) determine whether ground or arboreal cameras are better for surveying lemur assemblages. We conducted camera trapping research in five forest fragments (total trap nights = 1770; 900 arboreal trap nights (134 photo events); 870 ground trap nights (2 photo events)) and reforestation areas (total trap nights = 608; 1 photo event) in Kianjavato, Madagascar from May to September 2019. We used arboreal trap data from fragments to estimate occupancy for five species: the red-fronted brown lemur (Eulemur rufifrons; ψ = 0.54 ± SD 0.03), Jolly's mouse lemur (Microcebus jollyae; ψ = 0.14 ± 0.17), the greater dwarf lemur (Cheirogaleus major; ψ = 0.42 ± 0.30), the red-bellied lemur (Eulemur rubriventer; ψ = 0.24 ± 0.03), and the black-and-white ruffed lemur (Varecia variegata; ψ = 0.24 ± 0.08). Tree diameter, elevation, distance to village, and canopy connectivity were important predictors of occupancy, while camera height, canopy connectivity, fragment ID, and fragment size predicted detection. Arboreal cameras recorded significantly higher species richness compared with ground cameras. We suggest expanded application of arboreal camera traps in future research, but we recommend longer trapping periods to better sample rarer species. Overall, arboreal camera trapping combined with occupancy modeling can be a highly efficient and useful approach for monitoring and predicting the occurrence of elusive lemur species and has the potential to be effective for other arboreal primates and canopy taxa across the globe.

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity.

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.

BackgroundSpecies recognition, i.e., the ability to distinguish conspecifics from heterospecifics, plays an essential role in reproduction. The role of facial cues for species recognition has been investigated in several non-human primate species except for lemurs. We therefore investigated the role of facial cues for species recognition in wild red-fronted lemurs (Eulemur rufifrons) at Kirindy Forest. We presented adult red-fronted lemurs pictures of male faces from five species including red-fronted lemurs, three closely related species, white-fronted lemurs (E. albifrons), brown lemurs (E. fulvus), rufous brown lemurs (E. rufus), and genetically more distant red-bellied lemurs (E. rubriventer), occurring in allopatry with the study population. We predicted that red-fronted lemurs respond stronger to conspecific than to heterospecific pictures and that females show stronger responses than males. In addition, if genetic drift has played a role in the evolution of facial color patterns in the members of this genus, we predicted that responses of red-fronted lemurs correlate negatively with the genetic distance to the different species stimuli.ResultsRed-fronted lemurs looked significantly longer at pictures of their own species than at those of heterospecifics. Females spent less time looking at pictures of white-fronted, brown and red-bellied lemurs than males did, but not to pictures of red-bellied lemurs and a control stimulus. Individuals also exhibited sniffing behavior while looking at visual stimuli, and the time spent sniffing was significantly longer for pictures of conspecifics compared to those of heterospecifics. Moreover, the time spent looking and sniffing towards the pictures correlated negatively with the genetic distance between their own species and the species presented as stimulus.ConclusionsWe conclude that red-fronted lemurs have the ability for species recognition using visual facial cues, which may allow them to avoid costly interbreeding. If so, sexual selection might have influenced the evolution of facial patterns in eulemurs. Since responses also correlated with genetic distance, our findings suggest a potential role of genetic drift as well as sexual selection in influencing the evolution of facial variation in eulemurs. Because study subjects looked and sniffed towards the presented pictures, red-fronted lemurs might have the ability for multi-modal species recognition.

The reproductive cycle of several lemur species is synchronized by photoperiodic changes and it is attuned to the seasonal fluctuations in food supply. Nevertheless, irregular periods of food shortage occur in Madagascar, which can result in a negative energy balance and reduced fitness, especially in frugivorous species. Here, we tested whether ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur rufifrons × collaris) use fat stores to maintain their energy balance in a gallery forest of Madagascar (Berenty Reserve). We assessed the energy intake from weight-based estimates of food intake (mouthful count) and macronutrient contents in the diet during dry and wet months. The metabolizable energy ingested by these frugivorous/folivorous species was high during the late wet season, but it was insufficient to meet their energy requirements during the dry season. These preliminary data suggest that these lemurs must store sufficient amount of fat mass during the period of food abundance to meet their maintenance requirements and to cope with the energetic burden of the mating season. Estimates based on models assuming no fiber digestibility during the dry season are consistent with the prediction that brown lemurs should supplement their daytime diet with nighttime feeding in addition to the use of body fat stores.

Various factors may mediate the visitation of frugivores to fruiting plants, which can dictate the quantum of seeds removed (dispersed) away from the parent plant. Past studies have laid emphasis on species‐specific factors and environmental contexts that frugivores may use as cues to make foraging decisions and differentially visit various plant species. However, differences in plant traits (intrinsic factors) and local environmental contexts (extrinsic factors) can influence the diversity and abundance of frugivores that visit individual plants of the same species, resulting in intraspecific variation in seed dispersal. We observed individuals of two co‐fruiting plant species with morphologically similar fruits—Naringi crenulata and Ziziphus oenopolia—for 134 h and examined the influence of fruit crop size, plant height, and fruiting neighborhood on the diversity of visiting avian frugivores and quantum of fruit removal for individual plants. We found that despite their similarity in fruits and sharing of a similar set of frugivore species, the two plant species differed in how they attracted frugivores, with consequences for fruit removal rates. Fruit crop size was an important determinant of fruit removal for N. crenulata¸ while plant height led to greater visitation and fruit removal for Z. oenopolia. We discuss potential reasons for the difference in frugivore visitation and fruit removal for the two plant species. Our results support a growing body of evidence that intraspecific variation in seed dispersal is pervasive and highly context‐dependent, and describe frugivore interactions of two plant species from an understudied tropical savanna.

The major histocompatibility complex (MHC) is a highly polymorphic and polygenic genomic region that plays a crucial role in immune-related diseases. Given the need for comparative studies on the variability of immunologically important genes among wild populations and species, we investigated the allelic variation of MHC class II DRB among three congeneric true lemur species: the red-fronted lemur (Eulemur rufifrons), red-bellied lemur (Eulemur rubriventer), and black lemur (Eulemur macaco). We noninvasively collected hair and faecal samples from these species across different regions in Madagascar. We assessed DRB exon 2 polymorphism with a newly developed primer set, amplifying nearly all non-synonymous codons of the antigen-binding sites. We defined 26 DRB alleles from 45 individuals (17 alleles from E. rufifrons (N = 18); 5 from E. rubriventer (N = 7); and 4 from E. macaco (N = 20). All detected alleles are novel and show high levels of nucleotide (26.8%) and non-synonymous codon polymorphism (39.4%). In these lemur species, we found neither evidence of a duplication of DRB genes nor a sharing of alleles among sympatric groups or allopatric populations of the same species. The non-sharing of alleles may be the result of a geographical separation over a long time span and/or different pathogen selection pressures. We found dN/dS rates > 1 in the functionally important antigen recognition sites, providing evidence for balancing selection. Especially for small and isolated populations, quantifying and monitoring DRB variation are recommended to establish successful conservation plans that mitigate the possible loss of immunogenetic diversity in lemurs.

In this paper, I describe the differential patterns of flower feeding observed in rufous lemurs (Eulemur fulvus rufus) and red-bellied lemurs (E. rubriventer) in the Ranomafana National Park, Madagascar. Red-bellied lemurs licked nectar from flowers while rufous lemurs ate all flower parts from the same flower species. Several hypotheses are examined to explain the significance of flower feeding in these two species. In many primate species, flower feeding functions as a keystone resource and/or primates act as pollinators while feeding on flowers. Although peak flower feeding occurred during a decline in food availability, fruit was always (the preferred food item so that flowers did not function as a keystone resource. Second, red-bellied lemurs appear to be potentially better pollinators compared to the rufous lemurs because 1) they left flower reproductive parts intact while feeding, 2) they visited more than one tree or liana of the same plant species in the same day, 3) pollen was observed on the faces of individuals as they traveled from plant to plant, and 4) they have a feathered, brush-like tip on their tongue which rufous lemurs lack. Finally, the difference in flower feeding styles between the lemur species also affected three aspects of diet: 1) feeding bout duration, 2) the size of feeding subgroups, and 3) return visits to flowering sources. These subtle differences in diet within food categories can allow these two otherwise similar lemur species to coexist. © 1992 Wiley-Liss, Inc.

The alarming rate of deforestation in Madagascar is driving some endemic primates to extinction. Surprisingly, anthropogenic habitat disturbance is not always deleterious. The effect of disturbance on lemur abundance may be related to diet, with frugivorous species more prone to population declines than folivores or insectivores. To test the effects of disturbance on lemur abundance and group size, we surveyed 2 sites within contiguous forest at Ranomafana National Park, 1 lightly disturbed primary forest (Vato) and 1 heavily logged forest (Tala). We quantified forest structure variables along 6 survey routes and conducted 68 diurnal and 42 nocturnal lemur surveys. Canopy closure, canopy height, and understory visibility were greater in Vato than in Tala. We encountered 2 frugivorous lemurs (Eulemur rufifrons, Varecia variegata) and 1 folivore (Avahi peyrierasi) significantly more frequently in Vato than in Tala, whereas the opposite was true for the insectivorous Microcebus rufus. Rates did not differ statistically for 1 frugivore (Eulemur rubriventer) and 2 folivores (Propithecus edwardsi, Hapalemur griseus). Comparisons across the 6 survey routes suggest that the abundance was heterogeneous within as well as between sites. Neither group size nor composition differed between sites. Encounter rates for Varecia variegata were positively related to canopy closure, and encounter rates for Avahi peyrierasi were positively related to canopy height. Encounter rates for Microcebus rufus were negatively related to canopy closure, height, and understory visibility. Similar to other studies, the results suggest that some lemurs, including folivores, may cope with anthropogenic disturbance better than others, including some frugivores. Lemur abundance is heterogeneous, though, even on small spatial scales.

Dietary data are used to categorize species diets, but these categorizations do not take into account the mutability of food resources in time or space, the level of interspecific competition in various communities as these resources change, nor the dietary flexibility of species. In this study, we assess the diets of three sympatric species, Eulemur rufifrons, Propithecus edwardsi, and Varecia variegata, in the Vatoharanana site in Ranomafana National Park, Madagascar. We determine dietary diversity, overlap, and interannual variation with data collected from 2001 to 2003. We then compare results on food preference and time feeding with data collected on each species in the late 1980s and early 1990s to determine whether these findings are consistent over the long term. We found little interannual variation in the proportion of time spent eating particular plant parts for each of the lemur species during the three study years (2001–2003), and between the earlier and current study. Food items were not always consumed based solely on availability. Dietary diversity was lower in the two frugivorous species (V. variegata and E. rufifrons) compared with the folivorous species (P. edwardsi), and V. variegata and E. rufifrons were more likely to focus their feeding time on one particular genus and plant part in each year. The study species used different strategies to deal with food, particularly fruit, shortages such as a plastic social structure (V. variegata), habitat shifting (E. rufifrons), and dietary switching (P. edwardsi). Although there was low dietary overlap between the study species, they depended on a small number of shared fruits in each of the study years (Chrysophyllum, Syzygium, Ocotea, Plagioscyphus), which may indicate some potential for interspecific competition. Because these lemur species, like all primates, lead relatively long lives (avg. >30 years) and have slow rates of aging, longitudinal studies are needed to test hypotheses reliant on basic dietary information.

How social and ecological factors are associated with variation in dominance style across species of animals has been studied frequently, but the underlying processes are often not addressed. Theoretical research indicates that stronger spatial cohesion among individuals in a group causes a higher frequency of fighting and, thus, through the self-reinforcing effects of winning and losing fights, a stronger differentiation of the dominance hierarchy and dominance of females over more males. Our aim in the present paper is to study whether the same interrelationship among processes may underlie differences in dominance style among three species of lemur that differ in their degree of despotism: Lemur catta, Propithecus verreauxi and Eulemur rufifrons. We investigated their agonistic interactions and spatial cohesion based on 2752 h of observational data of 20 wild groups of these three species. We determined dominance style using the proportion of counter-aggression, with a lower proportion indicating a more despotic dominance style. We found that stronger spatial cohesion among individuals is associated with a higher rate of aggression, stronger despotism and dominance of females over more males. The results of our study emphasise the general importance of spatial cohesion in determining dominance style.Significance statementTheoretical studies have shown that the spatial configuration of individuals in a group influences the dominance style. In an agent-based model, DomWorld, individuals are guided by simple rules of grouping and fighting and emergent patterns of behaviour switch between resembling those of despotic or egalitarian primates depending on the degree of cohesion in groups. Yet this link has seldom been studied empirically. We, therefore, examine the relevance of spatial cohesion on patterns of behaviour of individuals in groups of three species of lemur. We confirm the predictions from the model and show that stronger spatial cohesion results in more frequent aggression, a more despotic dominance style and stronger female dominance over males. In light of this, we urge future research of animal dominance to include measures of cohesion.