Competition between birds and mammals: A comparison of giving-up densities between crested larks and gerbils

We combined the concept of mechanisms of co-existence with the approach of giving-up densities to study inter-taxon competition between seed-eating birds and mammals. We measured feeding behaviour in food patches to define and study the guild of seed-eating vertebrates occupying sandy habitats at Bir Asluj, Negev Desert, Israel. Despite a large number of putatively granivorous rodents and birds at the site, two gerbil species (Allenbys gerbil, Gerbillus allenbyi, and the greater Egyptian gerbil, G. pyramidum) dominated nocturnal foraging, and a single bird species (crested lark, Galerida cristata) contributed all of the daytime foraging. We used giving-up densities to quantify foraging behaviour and foraging efficiencies. A low giving-up density demonstrates the ability of a forager to profitably harvest food at low abundances and to profitably utilize the foraging opportunities left behind by the less efficient forager. Gerbils had lower giving-up densities in the bush than open microhabitat, and lower giving-up densities in the semi-stabilized than stabilized sand habitats. Crested larks showed the opposite: lower giving-up densities in the open than bush, and on the stabilized than semi-stabilized sand habitats. Despite these patterns, gerbils had substantially lower giving-up densities than crested larks in both microhabitats, all sand habitats, and during each month. Several mechanisms may permit the crested lark to co-exist with the gerbils. Larks may be cream skimmers on the high spatial and temporal variability in seed abundances. Larks may rely on insects, fruit or smaller seeds. Or, larks may rely on adjacent rocky habitats.     

Taxonomic status of the Forest Buzzard Buteo oreophilus trizonatus

The foraging efficiencies of four sympatric southern African seed-eating birds, namely Bronze Mannikin Spermestes cucullatus, Cape Sparrow Passer melanurus, Southern Red Bishop Euplectes orix and Thick-billed Weaver Amblyospiza albifrons, and a domesticated species, the Bengalese Finch Lonchura domestica, were measured and compared using giving-up densities (the amount of food remaining following patch exploitation) in experimental food patches. Foraging efficiency was quantified using giving-up densities by offering individual birds equal foraging opportunities. A low giving-up density displays the ability of a forager to profitably harvest food at low resource densities and to gainfully exploit the foraging opportunities overlooked by a less efficient forager. Ten individuals of each of the five species were allowed to forage on six different seed types. Thick-billed Weavers had significantly lower giving-up densities for all seed types except the smallest, namely red manna. Bronze Mannikins showed the converse trend, foraging most efficiently on the smallest seeds. The results of the present study revealed that Thick-billed Weavers were the most efficient foragers (i.e. had the lowest giving-up densities on seeds in feeding trays).     

Food choice and food competition among the three major primate species of French Guiana

The three most important primates of French Guiana are frugivorous species, but to different degrees. Ateles paniscus is almost exclusively frugivorous, Alouatta seniculus frugivorous-folivorous, and Cehus apellu partially insectivorous; thus, the overall specific diet spectra arc well separated. During the season when fruit production is minimal, fruit intake by all species is also minimal which results in the greatest diversities in diet and the lowest diet overlaps. Real competition for the common main food category, i.e. fruits, only occurs during the most favourable period. Nevertheless, some fruit characteristics (e.g. size…) separate the monkey species from each other in fruit choice and make the interspecific competition of little importance.     

Densities of Two Frugivorous Primates with Respect to Forest and Fragment Tree Species Composition and Fruit Availability

Conservation of wildlife populations requires extensive knowledge of their habitat requirements, efficient methods to evaluate habitat quality, and an understanding of the value of fragments and edges. Kibale National Park, Uganda has areas that differ in the densities of 2 species of frugivorous monkeys—Cercopithecus mitis and Lophocebus albigena—including one on an edge and forest fragments outside the park that lack both species. We compared the basal area densities of important food trees with primate densities. The density of Cercopithecus mitis correlates most strongly with the basal area density of all types of food trees combined. The density of Lophocebus albigena does not correlate with the basal area densities of any category of food trees or with fruit availability. An index of their density—number of groups seen per km walked—correlates to fruit availability but with marginal significance. Lack of a relationship between the basal area densities of food trees and density of Lophocebus albigena may be the result of a mismatch in scale between the forest area measured and their large home ranges. We compared the unused area of forest to the other areas of the forest and the fragments and found it had higher basal area densities in all food tree categories for both species than the fragments and lower basal area densities of most categories than the other parts of the forest, indicating that the fragments are poor quality and would probably be unused even if dispersal were likely.     

Does landscape structure affect resource tracking by avian frugivores in a fragmented Afrotropical forest?

Frugivorous species heavily depend on patchy food resources and are believed to track these in space and time, thereby providing an important seed dispersal function that might be critical toward the regeneration of fruiting plants. However, isolation of suitable food patches due to habitat fragmentation or changes in landscape connectivity may hamper food tracking behaviour and adversely affect populations of both frugivores (through starvation) and food plants (through interruption of seed dispersal). We here test whether density fluctuations in four frugivorous Afrotropical bird species were larger and/or matched fluctuations in ripe fruit densities better in study plots embedded in large tracts of indigenous forest than in equally-sized plots embedded in cultivated lands. We compared these results with those of four non-frugivorous species (out-group) which were not expected to track fruit resources. Whereas densities of both frugivores and fruit crops strongly fluctuated in space and time, these fluctuations were not synchronised, nor did the level of synchrony differ in relation to matrix type. For some but not all bird species, lower densities and smaller temporal fluctuations in forest plots surrounded by cultivation may reflect decreased mobility. The observed fluctuations in bird densities most likely reflect exchange with the surrounding landscape matrix, suggesting that small pockets of fruiting trees in farmland may comprise critical food resources for frugivores inhabiting highly fragmented landscapes, apart from increasing connectivity for both bird and seed dispersal.     

Linking foraging decisions to residential yard bird composition

Urban bird communities have higher densities but lower diversity compared with wildlands. However, recent studies show that residential urban yards with native plantings have higher native bird diversity compared with yards with exotic vegetation. Here we tested whether landscape designs also affect bird foraging behavior. We estimated foraging decisions by measuring the giving-up densities (GUD; amount of food resources remaining when the final forager quits foraging on an artificial food patch, i.e seed trays) in residential yards in Phoenix, AZ, USA. We assessed how two yard designs (mesic: lush, exotic vegetation; xeric: drought-tolerant and native vegetation) differed in foraging costs. Further, we developed a statistical model to calculate GUDs for every species visiting the seed tray. Birds foraging in mesic yards depleted seed trays to a lower level (i.e. had lower GUDs) compared to birds foraging in xeric yards. After accounting for bird densities, the lower GUDs in mesic yards appeared largely driven by invasive and synanthropic species. Furthermore, behavioral responses of individual species were affected by yard design. Species visiting trays in both yard designs had lower GUDs in mesic yards. Differences in resource abundance (i.e., alternative resources more abundant and of higher quality in xeric yards) contributed to our results, while predation costs associated with foraging did not. By enhancing the GUD, a common method for assessing the costs associated with foraging, our statistical model provided insights into how individual species and bird densities influenced the GUD. These differences we found in foraging behavior were indicative of differences in habitat quality, and thus our study lends additional support for native landscapes to help reverse the loss of urban bird diversity.     

Hardness as a basis of fruit choice in two sympatric primates

Fruit color and size are significant determinants of food choice in mammals and birds, but hardness, an important physical property of fruit and seeds, has generally been overlooked as a determinant of food choice in studies of mammalian foraging behavior. Two methods were used to determine fruit hardness during a field study of two sympatric primates, the black spider monkey (Ateles paniscus) and the bearded saki monkey (Chiropotes satanas) in Surinam. We measured both puncture resistance of fruit pericarp and crushing resistance of seeds. Puncture resistance of the pericarp of some fruit opened by Chiropotes was as much as 15 times greater than that of all fruit successfully opened by Ateles. In contrast, crushing resistance of species of seeds masticated by Chiropotes was significantly lower than that of seeds swallowed by Ateles. These data demonstrate that hardness of both fruit pericarp and seed may play a significant role in food choice among sympatric vertebrates. Measurements of both puncture resistance of the pericarp and crushing resistance of the seed are necessary for understanding the significance of fruit hardness in these primates.     

Effects of habitat disturbance and food supply on population densities of three primate species in the Kakamega Forest, Kenya

While habitat disturbance and food availability are major factors thought to determine the abundance of primates, evidence for their importance is uneven. We assessed the effects of these factors on three monkey species, guerezas ( Colobus guereza ) , blue monkeys ( Cercopithecus mitis ) and redtails ( Cercopithecus ascanius ), in four areas of the Kakamega Forest, Kenya. Group densities of guerezas and blue monkeys were higher in areas where disturbance levels were also higher. Food availability measured as basal area density of food trees did not correlate significantly with the group densities of any of the three monkeys. The diversity of food trees, another potential measure of food abundance did, however, correlate with group densities of guerezas and blue monkeys suggesting that food availability may positively influence monkey density, and may sometimes increase with disturbance. Group densities of redtails did not correlate with any habitat variable examined, suggesting that factors other than those we considered may have influenced the abundance of this species particularly.     

Seasonal dietary niche contraction in coexisting Neotropical frugivorous bats (Stenodermatinae)

Tropical dry forests are characterized by punctuated seasonal precipitation patterns that drive primary production and the availability of fruits, seeds, flowers, and insects throughout the year. In environments in which the quantity and quality of food resources varies seasonally, consumers should adjust their foraging behavior to maximize energy intake while minimizing overlap with competitors during periods of low food availability. Here, we investigated how the diets of frugivorous bats in tropical dry forests of NW Mexico varied in response to seasonal availability and how this affected dietary overlap of morphologically similar species. We performed stable isotope analyses to understand temporal and interspecific patterns of overall isotopic niche breadth, trophic position, and niche overlap in the diet of six frugivorous species of closely related New World leaf-nosed bats (family Phyllostomidae, subfamily Stenodermatinae). We estimated seasonal changes in resource abundance in two complementary ways: (a) vegetative phenology based on long-term remote sensing data and (b) observational data on food availability from previously published insect and plant fruiting surveys. In all species, there was a consistent pattern of reduced isotopic niche breadth during periods of low food availability. However, patterns of niche overlap varied between morphologically similar species. Overall, results from our study and others suggest that seasonal food availability likely determines overall dietary niche breadth in Phyllostomidae and that despite morphological specialization, it is likely that other mechanisms, such as opportunistic foraging and spatiotemporal niche segregation, may play a role in maintaining coexistence rather than simply dietary displacement.     

Long-Term Habitat Use by Mountain Gorillas (Gorilla gorilla beringei). 2. Reuse of Foraging Areas in Relation to Resource Abundance, Quality, and Depletion

Resource depression caused by current feeding and the rate of resource renewal should influence foragers' decisions about when to revisit foraging areas. Adjustment of foraging paths and revisit rates should be particularly important when resources renew slowly. Foragers can also benefit by returning more often to highly profitable than to less profitable foraging areas. Many highly frugivorous primates seem to time revisits to fruit sources so as to harvest fruit efficiently and, also, use efficient search paths. Fewer data on non-frugivores exist. Mountain gorillas are folivores that eat mostly perennially available, continuously growing herbs and vines. Vegetation regenerates slowly from the effects of gorilla trampling, though trampling can also facilitate food species productivity, at least in the short term. Adjustment of intervals between visits to foraging areas to the extent of previous use and to resource renewal rates should increase gorilla foraging efficiency. Long-term data on habitat use by 6 mountain gorilla social units show that revisit intervals vary in association with variation in the extent of previous use and in plant productivity. However, they also revisit areas more often, the higher the biomass and nutritional quality of food there. These data are generally consistent with the hypothesis that the gorillas crop resources on a sustained-yield basis, though more precise data on areal revisits and complementary long-term data on vegetation composition would be needed to test the hypothesis.     

Are Primates Ecosystem Engineers?

Animals can play important roles in structuring the plant communities in which they live. Some species are particularly influential in that they modify the physical environment by changing, maintaining, and/or creating new habitats; the term ecosystem engineer has been used to describe such species. We here assess the two major foraging strategies of primates, frugivory and folivory, in terms of the potential for primates to function as ecosystem engineers. We argue that whereas the role of primates as seed dispersers has received a great deal of attention, the potential role that folivorous primates play in structuring their environment through herbivory has received much less attention. Further, while quantifying if frugivorous primates are ecosystem engineers through their seed dispersal has proved very difficult, it is not as difficult to ascertain whether folivorous primates are ecosystem engineers. We document situations in which folivorous primates act as ecosystem engineers by 1) eating the leaves and/or bark of trees to the extent that they kill trees, 2) feeding on trees to the degree that they slow their growth relative to nonpreferred tree species, 3) eating the flowers of species to the extent that it does not set fruit, or 4) feeding on plants in such a way as to increase their productivity and abundance. Because evidence from the literature is very limited, where possible we present new evidence of these processes from the colobus monkeys at our long-term field site in Kibale National Park, Uganda. We conclude by discussing promising research programs that could be established to refine our understanding of the role primates play in shaping the structure of plant communities, especially tropical forests.     

Intratree Variation in Fruit Production and Implications for Primate Foraging

We tested the hypothesis that fruit quantity and quality vary vertically within trees. We quantified intratree fruit production before exploitation by frugivores at different heights in 89 trees from 17 species fed on by primates in Kibale National Park, Uganda. We also conducted a pilot study to determine if the nutritional value of fruit varied within tree crowns. Depending on the species and crown size, we divided tree canopies into 2 or 3 vertical layers. In 2-layered trees, upper crowns produced fruits that were 9.6–30.1% bigger and 0.52–140 times the densities of those from lower crowns, with one exception. Among 2-layered trees, upper crowns produced a mean of 46.9 fruits/m³ (median 12.1), while lower crowns produced a mean of 14.1 fruits/m³ (median 2.5). Among 3-layered trees, upper crowns produced a mean density of 49.9 fruits/m³ (median 12.5), middle crowns a mean of 16.8 fruits/m³ (median 6.6), and lower crowns a mean of 12.8 fruits/m³ (median 1.8). Dry pulp and moisture were systematically greater per fruit in the highest compared to the lowest canopy layers (22.4% and 16.4% respectively in 2-layered trees, 49.7% and 21.8% respectively in 3-layered trees). In 1 tree of Diospyros abyssinica, a pilot nutritional study showed that upper crown ripe fruit contained 41.9% more sugar, 8.4% more crude proteins, and 1.8 times less of the potentially toxic saponin than lower crown ripe fruit, but the result needs to be verified with more individuals and species of trees. We discuss the consequences of intratree variations in fruit production with respect to competition among frugivorous primates.     

Massive Destruction of Symphonia globulifera (Clusiaceae) Flowers by Central American Spider Monkeys (Ateles geoffroyi)1

Although more than 39 primate species have been described as nectar feeders, no studies have documented the negative affect this behavior may have on the reproductive success of the plants they consume. Here we report, for the first time, massive flower destruction of the tropical tree Symphonia globulifera by the frugivorous spider monkey, Ateles geoffroyi, and document the detrimental effect this behavior has on fruit set. Foraging behavior was collected from one troop of A. geoffroyi during 460 contact hours from June 1999 to May 2000 in the tropical humid forest at the Refugio de Vida Silvestre Punta Rio Claro (8°39′N, 83°44′E) in the Osa Peninsula in Southwestern Costa Rica. Detailed phenological data were collected from ten S. globulifera trees that the monkeys fed upon and ten trees that were outside of their home range, but in the Refugio. From July to September 1999 S. globulifera was the most important species consumed, representing from 86 to 100 percent of the total feeding time each month. Monkey foraging on S. globulifera flowers was destructive, detaching the flowers completely from the branches in 80 percent of the foraging bouts, and leaving flowers without petals and with damaged reproductive parts in 20 percent of the bouts. None of the ten trees where the monkeys were foraging set fruit, but seven of ten trees outside of their home range set fruit in November and December 1999. These results suggest that some primates may play an important role in floral herbivory in tropical forests and the subsequent reduction in reproductive success. Future studies should focus on evaluating the long‐term effect this foraging behavior may have on the population structure of this species and evaluate the effect of primate floral herbivory on the reproductive success of other plant species.     

Measuring fruit patch size for three sympatric indonesian primate species

Food availability is one of the basic factors affecting primate density and socioecology, but food availability is difficult to assess. Two different ways to obtain accurate estimates of food availability have been proposed: using phenology data or using the behaviour of animals. Phenology data can be refined by only including trees that are large enough to be used; including (potential) tree species in which by the concerned primate species forage; or including (fruiting) trees of these species that actually produce fruit. Alternatively, the sizes of the actually visited trees (foraging trees) give an estimate of fruit availability. These measures are compared for three sympatric primate species at the Ketambe Research Station, Sumatra, Indonesia: the Thomas langur, the long-tailed macaque and the orangutan. The sizes of fruiting trees and the foraging trees are larger than the potential trees. The sizes of the potential trees and of the fruiting trees are similar for the three primate species. This, however, is not reflected in the use of trees: the langurs forage on average in trees of similar size to those producing fruit, whereas the macaques and orangutans forage in trees larger than those producing fruit. The use of trees does not necessitate a different cut off point of included dbhs for the three compared primate species. The use of trees of different sizes, however, may be regulated by food competition. This indicates that sympatric primates make different foraging decisions and that behavioural measures of food availability will be less reliable.     

Direct and indirect cues of predatory risk and patch use by fox squirrels and thirteen-lined ground squirrels

We used giving-up densities in food patches to measure the effectsof several direct (left by the predator) and indirect (environmentalcorrelates of risk) cues of predatory risk on the foraging behaviorof free-living fox squirrels (Sciurus niger) and thirteen-linedground squirrels (Spermophihis tridtctmlineatus). Increasesin giving-up density in response to stimuli allow quantitativecomparisons of the effects of different types of cues. We usedolfactory (urine of red fox) and visual (plastic models of owls)direct cues. As indirect cues, we used mkrohabitat (near orfar from a refuge), background coloration (white, green, andbrown tarpaulins), and escape substrate (canvas tarpaulins versusnatural surrounding substrates). Both squirrel species respondedmost strongly to microhabitat Fox squirrels increased theirgiving-up density by 97% when feeding 4–6 m from a treecompared to feeding at the tree base. Thirteen-lined groundsquirrels increased giving-up densities 84% when feeding 2 mfrom their burrows compared to feeding at the burrow entry.In response to an unfavorable escape substrate (canvas versusgrass), fox squirrel giving-up densities increased 61%. Foxsquirrels and ground squirrels increased giving-up densities26% and 35%, respectively, in response to a plastic owL Backgroundcoloration had no demonstrable effect on the giving-up densitiesof fox squirrels. In contrast to other work on nocturnal mammalianherbivores and granivores, the diurnal fox squirrels did notrespond to olfactory cues.     

Resource tracking and its conservation implications for an obligate frugivore (Procnias tricarunculatus,the three‐wattled bellbird)

In Monteverde, Costa Rica, the vulnerable Three‐wattled Bellbird (Procnias tricarunculatus) feeds primarily upon the fruit of Lauraceae species during its reproductive and post‐reproductive seasons. To understand and advance appropriate conservation measures, this study identified the bellbird's foraging challenges in its search for a temporally and spatially fluctuating resource. Although there are at least 96 species of Lauraceae found in the five life zones of Monteverde, the distinct distributions of tree species both among and within life zones require the bellbirds to track seasonal fruiting across the various zones. In this 6‐year study, we monitored the fruiting of tree species and bellbird abundance in 24 study plots within its post‐reproductive life zone, the Premontane Wet forest, to identify preferred bellbird food resources and how the fruiting of these species drives the spatial distribution of the bellbird. Our research revealed phenological patterns of annual, biennial, and triennial fruiting with high levels of fruiting synchrony within several identified key fruit species. Of critical conservation importance is that no single species of Lauraceae produced a consistent food supply for bellbirds each year. Therefore, even within life zones, the bellbird's survival depends on its mobility to search for and obtain fruit, as well as the availability of fruits of multiple tree species. The conservation implications include focused attention on multiple core areas within given life zones, protection of existing forest and remnant trees, and forest restoration with plantings of multiple tree species. We suspect that other tropical frugivorous species face similar conservation challenges.     

The Impact of Forest Disturbance on the Seasonal Foraging Ecology of a Critically Endangered African Primate

Forest loss and fragmentation threaten many primates globally, and often leads to a reduction in food resources. During a 22 ‐ mo period, the foraging ecology of the critically endangered kipunji Rungwecebus kipunji was studied in the heterogeneous Rungwe–Livingstone forests, southwest Tanzania, to identify periods of possible ecological stress, fallback foods used by the species, and the impact of forest disturbance on feeding resources. The studied group had a wide diet and was predominantly frugivorous. Fruit consumption was driven by fruit availability which peaked during the wet season, and dipped during the driest months. During this period, two fallback foods: mature leaves and pith were widely consumed, with Macaranga capensis an essential fallback species. α diversity and evenness of diet was remarkably similar across months, but there was high β diversity in diets at the cusp of wet and dry seasons, and during periods of low fruit availability. This suggests considerable dietary adaptability to fluctuating resources, which may act to buffer against further forest disturbance. Tree species associated with relatively undisturbed forest were significantly more important in the diet, especially in the dry season, than those of disturbed forests. Regeneration of key trees (determined through counting of seedlings and saplings in plots) appeared healthy except in two important Ficus species. Conservation management, while focusing on promoting old growth forest, should also consider populations of some important pioneer tree species such as Macaranga capensis both inside the forest and in any reforestation schemes outside the species’ current area of occupancy.     

Foraging efficiency of <Emphasis Type="Italic">Akodon azarae</Emphasis> under different plant cover and resource levels

The goal of this work was to determine how the foraging behaviour of Akodon azarae changes with predation risk and food availability in cropfield borders of Buenos Aires, Argentina. Our hypotheses were that A. azarae has a greater foraging efficiency in safe areas than in risky ones and that the foraging behaviour of A. azarae also depends on the level of resources. We measured giving-up densities (GUDs) and food consumption twice a year in artificial foraging patches (bottles with known amounts of millet seed) in covered and open areas and with two different levels of seed abundance. In both periods, GUDs were lower in the covered areas than in the open ones independently of food level. Consumption increased with food level in covered areas but not in open areas. Based on these results, we conclude that A. azarae appears to maximize its consumption depending on predation risk.     

Scale-free foraging by primates emerges from their interaction with a complex environment

Scale-free foraging patterns are widespread among animals. These may be the outcome of an optimal searching strategy to find scarce, randomly distributed resources, but a less explored alternative is that this behaviour may result from the interaction of foraging animals with a particular distribution of resources. We introduce a simple foraging model where individual primates follow mental maps and choose their displacements according to a maximum efficiency criterion, in a spatially disordered environment containing many trees with a heterogeneous size distribution. We show that a particular tree-size frequency distribution induces non-Gaussian movement patterns with multiple spatial scales (Lévy walks). These results are consistent with field observations of tree-size variation and spider monkey (Ateles geoffroyi) foraging patterns. We discuss the consequences that our results may have for the patterns of seed dispersal by foraging primates.     

Foraging behaviour of a frugivorous bat helps bridge landscape connectivity and ecological processes in a fragmented rainforest

1. Landscape connectivity may greatly influence the distribution of animals when it alters their movements and their ability to reach food patches. Depending on their foraging behaviour, organisms may or may not adapt to anthropogenic changes in landscape connectivity and may eventually undergo local extinctions. 2. Recent studies underlined the need to use indicators of functional landscape connectivity based on the behaviour and movement abilities of studied animals to better link landscape structure to ecological processes in disturbed and fragmented areas. 3. The objectives of this study were: to elaborate an index of functional connectivity for Rhinophylla pumilio, a Neotropical understorey frugivorous bat; to use this index to investigate the possible mechanisms controlling its distribution and sustainability in a fragmented landscape; and to test whether this index could be applied to other species of the same guild. 4. We pursued a 10-year bat mist-net survey, coupled to local estimates of food availability, in a mature forest of French Guiana that was recently fragmented by the completion of a reservoir lake. The 18 sampling sites range from undisturbed continuous forest sites to small remote forest fragments. A connectivity value, based on radio-tracking surveys, was attributed to each site. Connectivity measures mean forest cover within neighbouring landscape units, weighted by the probability that bats would use them, as estimated by frequency distribution of flight distance data. 5. The abundance of R. pumilio was positively correlated with landscape connectivity and not correlated with local food availability. Its foraging strategy has evolved in response to the highly scattered distribution of its fruit resource. In spite of its high mobility, R. pumilio apparently failed to exploit a food resource that is distributed patchily over a low-connective habitat because its foraging movements are not well adapted to habitat disruptions. 6. The connectivity index contributed to explain general tendencies of abundance variations in other understorey frugivorous bats, although the spatial scale we examined was probably too small for these species. We make recommendations to adapt a functional connectivity index to species whose large-scale movements are difficult to survey.