Resource Use in a Landscape Matrix by an Arboreal Primate: Evidence of Supplementation in Black howlers (Alouatta pigra)

Across the tropics, landscapes of continuous rain forest are being replaced by forest fragments embedded in a matrix of pastures and farmlands. This conversion has endangered many species, including arboreal primates. Species vary, however, in how they are able to supplement their diets from the matrix, although this is rarely studied in primates. We studied two groups of black howlers (Alouatta pigra) for a total of 1156 h, one inhabiting a smaller fragment (0.4 ha) and the other a larger fragment (20 ha). monkeys inhabiting the smaller fragment spent more time in the matrix than in the habitat fragment, spending 50 % of their time (335 of 667 h) in an abandoned mango (Mangifera indica) plantation, 8.8 % in scattered trees, and 0.2 % in pastures. In contrast, monkeys in the larger fragment spent 75 % of their time (368 of 489 h) in the forest fragment and only 25 % of their time in the matrix. Feeding in the matrix accounted for 53 % and 12 % of the foraging time for groups in the smaller and larger fragments respectively. We suggest that Alouatta pigra can use resources in the matrix to supplement their diet by means of crop raiding or taking other resources in many fragmented landscapes and that this may be true also for many fragment-dwelling primates. It is important to include a consideration of the matrix in conservation planning, considering both the total resources available to primates and the consequences of crop raiding for farmers.     

Arboreal spiders in eastern hemlock

Eastern hemlock [Tsuga canadensis (L.) Carrière] is a foundation species in forests of eastern North America that plays a key role in ecosystem function. It is highly susceptible to the exotic invasive hemlock woolly adelgid (Adelges tsugae Annand), which is causing widespread hemlock mortality. We surveyed the spider communities of eastern hemlock and deciduous canopies over 2 yr, collecting over 4,000 spiders from 21 families. We found that eastern hemlock canopies harbored a more abundant, rich, and diverse spider community than did deciduous canopies. Five spider families were present in our hemlock collections that were absent from the deciduous collections, including Mysmenidae, Theridiosomatidae, Mimetidae, Lycosidae, and Agelenidae. In hemlock canopies there were 4× the number of web builders, consisting primarily of the Tetragnathidae and Araneidae, than active hunters, consisting primarily of the Anyphaenidae and the Salticidae. Ours is the first in depth study of the spider community in eastern hemlock. Spider abundance in hemlock canopies suggest that they may play a role regulating herbivore populations, and could possibly affect the invasive hemlock woolly adelgid, either through direct consumption of the adelgids themselves or through interactions with classical biological control agents.     

Arboreal locomotion in small new-world monkeys

The postural and locomotor activity and its relation to substrates was observed in 3 Saguinus oedipus, and 3 Saimiri sciureus for comparison, during a period of 10 h for each individual. The animals moved freely in cages of 3.40 m x 3.40 m x 2.40 m (height) on rather diverse substrates. Observations were made according to the focal-animal-method, with combined instantaneous and continuous sampling. They were protocoled in schematic form and video-recorded. In addition, 3 further Saguinus oedipus were subjected to an X-ray cinematographic study on a modified treadmill to unveil metric parameters of the locomotor pattern preferred on slender and compliant ("arboreal") substrates, the walk. Independent from the substrates, the postures of the two species differed in details, as do the preferred substrates. Horizontal, comfortable substrates are favored most. Walking ranked top in frequency, followed by jumping and galloping (in a strict sense). All other locomotor modes described for primates played a minor role or lacked entirely, like the trot. Average distance of leaps was only 0.60 m, landings were mainly on the same level as take-offs. In Saguinus, the movements of both limbs, including the shoulder blade, followed the pattern common to small mammals in general: At the end of the stance phase, humerus and tibia are nearly parallel to the substrate, while just before touchdown ulna and femur are in this position. The walk in both species was surprisingly fast (1 m/s), reaching the speed of much larger cursorial animals, like humans.     

Vigilance in a Cooperatively Breeding Primate

Collective vigilance is considered a major advantage of group living in animals. We investigated vigilance behavior in wild mustached tamarins (Saguinus mystax), small, arboreal, cooperatively breeding New World primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We aimed 1) to investigate whether vigilance patterns change according to individual activity and 2) to examine whether there is a social component of vigilance in their cooperative and nonaggressive society. We studied 11 factors that may influence vigilance and used this data to interpret the possible functions of vigilance. We observed 44 individuals in 3 mixed-species and 2 single-species groups of 2 populations that differed in population density and home range sizes. Vigilance changed greatly when individuals were engaged in different activities and individual vigilance was affected by different sets of factors depending on the activity. As vigilance decreased in proximity of conspecifics and heterospecifics when feeding, and in larger mixed-species groups when resting, we conclude that the predominant function of vigilance in mustached tamarins is predator related. However, the absence of the group size effect in very large single-species groups suggests that it may also function to maintain group cohesion. In the population with higher density and smaller home ranges individuals also increased their vigilance in home range overlap areas. We found no evidence that mustached tamarins monitor group mates to avoid food stealing or aggression. The effect of heterospecifics on individual vigilance suggests that collective vigilance might have been an important incentive in the evolution of tamarin mixed-species groups.     

Spatial Distribution of Dominant Arboreal Ants in a Malagasy Coastal Rainforest: Gaps and Presence of an Invasive Species

We conducted a survey along three belt transects located at increasing distances from the coast to determine whether a non-random arboreal ant assemblage, such as an ant mosaic, exists in the rainforest on the Masoala Peninsula, Madagascar. In most tropical rainforests, very populous colonies of territorially dominant arboreal ant species defend absolute territories distributed in a mosaic pattern. Among the 29 ant species recorded, only nine had colonies large enough to be considered potentially territorially dominant; the remaining species had smaller colonies and were considered non-dominant. Nevertheless, the null-model analyses used to examine the spatial structure of their assemblages did not reveal the existence of an ant mosaic. Inland, up to 44% of the trees were devoid of dominant arboreal ants, something not reported in other studies. While two Crematogaster species were not associated with one another, Brachymyrmex cordemoyi was positively associated with Technomyrmex albipes, which is considered an invasive species—a non-indigenous species that has an adverse ecological effect on the habitats it invades. The latter two species and Crematogaster ranavalonae were mutually exclusive. On the other hand, all of the trees in the coastal transect and at least 4 km of coast were occupied by T. albipes, and were interconnected by columns of workers. Technomyrmex albipes workers collected from different trees did not attack each other during confrontation tests, indicating that this species has formed a supercolony along the coast. Yet interspecific aggressiveness did occur between T. albipes and Crematogaster ranavalonae, a native species which is likely territorially dominant based on our intraspecific confrontation tests. These results suggest that the Masoala rainforest is threatened by a potential invasion by T. albipes, and that the penetration of this species further inland might be facilitated by the low density of native, territorially dominant arboreal ants normally able to limit its progression.     

Lunar Philia in a Nocturnal Primate

The influence of moonlight on behavior has been well documented for many nocturnal mammals, including rodents, lagomorphs, badgers and bats. These studies have consistently shown that nocturnal mammals respond to bright moonlight by reducing their foraging activity, restricting their movement, and reducing their vocalizations. Lunar phobia among nocturnal mammals is generally believed to be a form of predator avoidance: numerous studies indicate that predation increases during moonlit nights. A study I conducted at Tangkoko Nature Reserve in Sulawesi, Indonesia, demonstrates that spectral tarsiers, (Tarsius spectrum), are not lunar phobic, but are lunar philic; they become more active during full moons. During full moons, spectral tarsiers increased foraging, decreased resting, increased travel (distance traveled per unit time, nightly path length, and home range size), increased the frequency of group travel and decreased the frequency of olfactory communication. I explore several potential hypotheses to account for the lack of lunar phobia and potential increased risk of predation resulting from this unusual behavior. Two hypotheses that may account for the behavior are that: 1) foraging efficiency increases during full moons and outweighs the increased risk of predation, and 2) predation risk is not greater during full moons. Instead, predation risk increases during new moons.     

Primate molecular phylogenetics in a genomic era

A primary objective of molecular phylogenetics is to use molecular data to elucidate the evolutionary history of living organisms. Dr. Morris Goodman founded the journal Molecular Phylogenetics and Evolution as a forum where scientists could further our knowledge about the tree of life, and he recognized that the inference of species trees is a first and fundamental step to addressing many important evolutionary questions. In particular, Dr. Goodman was interested in obtaining a complete picture of the primate species tree in order to provide an evolutionary context for the study of human adaptations. A number of recent studies use multi-locus datasets to infer well-resolved and well-supported primate phylogenetic trees using consensus approaches (e.g., supermatrices). It is therefore tempting to assume that we have a complete picture of the primate tree, especially above the species level. However, recent theoretical and empirical work in the field of molecular phylogenetics demonstrates that consensus methods might provide a false sense of support at certain nodes. In this brief review we discuss the current state of primate molecular phylogenetics and highlight the importance of exploring the use of coalescent-based analyses that have the potential to better utilize information contained in multi-locus data.     

Foraging Behavior in the Arboreal Boid Corallus grenadensis

Corallus grenadensis is an arboreal boa endemic to the Grenada Bank. Thirty-five encounters with boas resulted in 17.65 hours of observations, including 6.3 hours of video-tape (which included two acts of predation). Boas under 100 cm are largely active foragers that move slowly through bushes and trees and tongue-flick leaf and branch surfaces apparently seeking chemosensory evidence of nocturnally quiescent lizard (Anolis) prey. Significantly more search time was directed to branches below the snake rather than to either the branches supporting the snake or to those above the snake, and tongue-flick rates were significantly higher for moving snakes than for those that were stationary. Smaller snakes prey on nocturnally quiescent lizards and they spent more time moving than did large snakes that feed on nocturnally active rodents and often employ an ambush foraging strategy. Once visual and, presumably, thermal information was received from a sleeping anole, C. grenadensis adopted a lengthy stalking process devoid of tongue-flicks. Snakes approached inactive lizards from adjacent branches with great stealth, moving at a rate of about 1 cm/min. The strike was made from close range (within 3 cm), and the prey was never released once contact was made. We conclude that, if chemosensory cues successfully lead a treeboa to a visual encounter with a sleeping lizard, subsequent behavior ensures a high rate of predation success.     

Association of Terrestrial Mangabeys (Cercocebus atys) with Arboreal Monkeys: Experimental Evidence for the Effects of Reduced Ground Predator Pressure on Habitat Use

We examined the behavior of two arboreal monkeys—Piliocolobus badius (western red colobus) and Cercopithecus diana (Diana monkey)—in the presence and absence of a third, predominately terrestrial monkey, Cercocebus atys (sooty mangabey) in the Ivory Coast's Taï Forest. Via experimental data, we show that sooty mangabeys are effective sentinels for ground predators. Then we compared strata use of red colobus and Diana monkeys in the presence and absence of mangabeys. Our data indicate that red colobus and Diana monkeys descend to low forest levels and to the forest floor significantly more often when mangabeys are spatially intermingled with them, i.e. in polyspecific associations. The niche extension may provide some foraging advantage, especially for red colobus. We identified the specific causal agent—relaxed ground predator pressure—of a temporary shift in habitat use. In this instance, the presence of one species (Cercocebus atys) leads to the temporary expansion of a niche normally avoided by others Piliocolobus badius and Cercopithecus diana.     

Habitat Use and Activity Patterns as an Indication of Fragment Quality in a Strepsirrhine Primate

Considerable intraspecific variation exists in responses to habitat fragmentation owing to regional differences in fragment quality. Habitat use and activity patterns of resident populations are related to the abundance and predictability of resources in time and space, and thus space use is one of the most important considerations for evaluating habitat quality. Here I examine inter- and intrasite differences in the ranging behavior; use of the matrix, i.e., surrounding nonhabitat; and activity budgets of ring-tailed lemurs (Lemur catta) inhabiting two forest fragments—Anja Special Reserve and Tsaranoro Valley Sacred Forest—in Madagascar’s central highlands to test the prediction that intraspecific variation in habitat use and activity patterns is indicative of fragment quality. At Anja, Lemur catta has access to abundant year-round anthropogenic resources (introduced fruit trees, agricultural crops, water), whereas the population at Tsaranoro relies on seasonally variable and patchily distributed resources throughout the forest and matrix. Lemur catta at Anja occupy smaller home ranges; have shorter daily path lengths (DPLs); and spend less time foraging and more time resting, locomoting, and engaging in social and territorial behavior. In contrast, groups at Tsaranoro occupy larger home ranges, have longer DPLs, rely heavily on the matrix, and expend most of their energy in foraging behavior. These differences point to variation in the relative habitat quality of the two fragments and are thus an important consideration for conservation managers when assessing the capacity of forest fragments to sustain populations.     

Neuropathogenesis of Japanese Encephalitis in a Primate Model

Background

Japanese encephalitis (JE) is a major cause of mortality and morbidity for which there is no treatment. In addition to direct viral cytopathology, the inflammatory response is postulated to contribute to the pathogenesis. Our goal was to determine the contribution of bystander effects and inflammatory mediators to neuronal cell death.

Methodology/Principal Findings

Material from a macaque model was used to characterize the inflammatory response and cytopathic effects of JE virus (JEV). Intranasal JEV infection induced a non-suppurative encephalitis, dominated by perivascular, infiltrates of mostly T cells, alongside endothelial cell activation, vascular damage and blood brain barrier (BBB) leakage; in the adjacent parenchyma there was macrophage infiltration, astrocyte and microglia activation. JEV antigen was mostly in neurons, but there was no correlation between intensity of viral infection and degree of inflammatory response. Apoptotic cell death occurred in both infected and non-infected neurons. Interferon-α, which is a microglial activator, was also expressed by both. Tumour Necrosis Factor-α, inducible nitric oxide synthase and nitrotyrosine were expressed by microglial cells, astrocytes and macrophages. The same cells expressed matrix metalloproteinase (MMP)-2 whilst MMP-9 was expressed by neurons.

Conclusions/Significance

The results are consistent with JEV inducing neuronal apoptotic death and release of cytokines that initiate microglial activation and release of pro-inflammatory and apoptotic mediators with subsequent apoptotic death of both infected and uninfected neurons. Activation of astrocytes, microglial and endothelial cells likely contributes to inflammatory cell recruitment and BBB breakdown. It appears that neuronal apoptotic death and activation of microglial cells and astrocytes play a crucial role in the pathogenesis of JE.     

Confusion Effect in a Reptilian and a Primate Predator

The confusion effect is claimed to be one benefit of group living with respect to predator avoidance: it is more difficult for predators to capture prey that is surrounded by other conspecifics than to capture an isolated individual. So far, the predictions of the confusion effect have been tested mainly in aquatic predators. As the confusion effect is seen to be a general problem for predators, terrestrial predators of two different vertebrate classes were used to test it. The prey (mealworms and black beetles, Tenebrio molitor ) was harmless and had no chance of predator avoidance. Thus, confounding effects of group defence and enhanced vigilance were controlled. Both leopard geckos ( Eublepharis macularius ) and common marmosets ( Callithrix jacchus ) took longer to catch one out of several prey compared to one single prey. Leopard geckos showed more fixations (changing of head position) when confronted with 20 mealworms than when confronted with only one mealworm, thus showing indications of being 'confused'.     

Spread of an introduced vector-borne banana virus in Hawaii

Emerging diseases are increasing in incidence; therefore, understanding how pathogens are introduced into new regions and cause epidemics is of importance for the development of strategies that may hinder their spread. We used molecular data to study how a vector-borne banana virus, Banana bunchy top virus (BBTV), spread in Hawaii after it was first detected in 1989. Our analyses suggest that BBTV was introduced once into Hawaii, on the island of Oahu. All other islands were infected with isolates originating from Oahu, suggesting that movement of contaminated plant material was the main driving factor responsible for interisland spread of BBTV. The rate of mutation inferred by the phylogenetic analysis (1.4 × 10⁻⁴ bp/year) was similar to that obtained in an experimental evolution study under greenhouse conditions (3.9 × 10⁻⁴ bp/year). We used these values to estimate the number of infections occurring under field conditions per year. Our results suggest that strict and enforced regulations limiting the movement of banana plant material among Hawaiian islands could have reduced interisland spread of this pathogen.