Emergent Group Level Navigation: An Agent-Based Evaluation of Movement Patterns in a Folivorous Primate

The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus), testing for: the effects of memory type (Euclidian or landmark based), amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led). Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group’s step length, whereas the type of memory had the highest impact on a group’s path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.     

Playing it safe? Solitary vervet monkeys (Chlorocebus pygerythrus) choose high‐quality foods more than those in competition

An important goal in foraging ecology is to determine how biotic and abiotic variables impact the foraging decisions of wild animals and how they move throughout their multidimensional landscape. However, the interaction of food quality and feeding competition on foraging decisions is largely unknown. Here we examine the importance of food quality in a patch on the foraging decisions of wild vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda using a multidestination platform array. The overall nutritional composition of the vervet diet was assessed and found to be low in sodium and lipids, thus we conducted a series of experimental manipulations in which the array was varied in salt and oil content. Although vervets prioritized platforms containing key nutrients (i.e., sodium and lipids) overall, we found that solitary vervets prioritized nutrient‐dense platforms more strongly than competing vervets. This finding was opposite to those in a similar experiment that manipulated food site quantity, suggesting that large, salient rewards may be worth competing over but slight differences in nutritional density may be only chosen when there are no potentially negative social consequences (i.e., aggression received). We also found that vervets chose platforms baited with oil‐only, and oil combined with salt, but not salt‐only, suggesting that energy was an important factor in food choice. Our findings demonstrate that when wild vervets detect differences in feeding patches that reflect nutritional composition, they factor these differences into their navigational and foraging decisions. In addition, our findings suggest that these nutritional differences may be considered alongside social variables, ultimately leading to the complex strategies we observed in this study.     

Proximity and grooming patterns reveal opposite-sex bonding in Rwenzori Angolan colobus monkeys (<Emphasis Type="Italic">Colobus angolensis ruwenzorii</Emphasis>)

Close proximity and social grooming are important bonding mechanisms in primates. These behaviors show the social structure of a species and many studies have found positive correlations between the degree of kinship and grooming and proximity. We used 1 year of data collected via instantaneous scan sampling on a large “supertroop” of Colobus angolensis ruwenzorii at Lake Nabugabo, Uganda, to examine partner preferences for grooming and nearest neighbors in each age-sex class. Little is known about this species, so we based our hypotheses on congeners. Of the five species of black-and-white colobus, data on sex-biased dispersal patterns are available for three (C. guereza, C. vellerosus, and C. polykomos), all of which show male-biased dispersal with occasional female dispersal. We thus predicted that female C. a. ruwenzorii would be more strongly bonded than males, showing greater proximity and grooming. We did not expect bonding between the sexes since congeners do not show this pattern. We found that among adult dyads, males and females were more likely to be found in loose proximity, and to groom, than would be expected given group composition. Conversely, both males and females had relatively weak same-sex relationships. Between the sexes, adult males had higher proximity and grooming indices with adult females without infants than with females with infants. These observations indicate that this subspecies is cross-bonded and that both sexes may disperse. Furthermore, our findings suggest that the social organization and social structure of C. a. ruwenzorii differ greatly from other black-and-white colobus species.     

Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng‐Fiema,Ghana: Possible anthropozoonotic transmission

Parasite richness and prevalence in wild animals can be used as indicators of population and ecosystem health. In this study, the gastrointestinal parasites of ursine colobus monkeys (Colobus vellerosus) at the Boabeng‐Fiema Monkey Sanctuary (BFMS), Ghana, were investigated. BFMS is a sacred grove where monkeys and humans have long lived in relatively peaceful proximity. Fecal samples (n = 109) were collected opportunistically from >27 adult and subadult males in six bisexual groups and one all‐male band from July 2004 to August 2005. Using fecal floatation, we detected three protozoans (two Entamoeba sp., Isospora sp.), five nematodes (Ascaris sp., Enterobius sp., Trichuris sp., two strongyle sp.), and one digenean trematode. Using fluorescein labeled antibodies, we detected an additional protozoan (Giardia sp.), and with PCR techniques, we characterized this as G. duodenalis Assemblage B and also identified a protistan (Blastocystis sp., subtype 2). The most prevalent parasite species were G. duodenalis and Trichuris sp. Parasites were more prevalent in the long wet season than the long dry. Parasite prevalence did not vary by age, and average parasite richness did not differ by rank for males whose status remained unchanged. However, males that changed rank tended to show higher average parasite richness when they were lower ranked. Individuals that spent more time near human settlements had a higher prevalence of Isospora sp. that morphologically resembled the human species I. belli. The presence of this parasite and G. duodenalis Assemblage B indicates possible anthropozoonotic and/or zoonotic transmission between humans and colobus monkeys at this site. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Vervet monkeys use paths consistent with context‐specific spatial movement heuristics

Animal foraging routes are analogous to the computationally demanding “traveling salesman problem” (TSP), where individuals must find the shortest path among several locations before returning to the start. Humans approximate solutions to TSPs using simple heuristics or “rules of thumb,” but our knowledge of how other animals solve multidestination routing problems is incomplete. Most nonhuman primate species have shown limited ability to route plan. However, captive vervets were shown to solve a TSP for six sites. These results were consistent with either planning three steps ahead or a risk‐avoidance strategy. I investigated how wild vervet monkeys (Chlorocebus pygerythrus) solved a path problem with six, equally rewarding food sites; where site arrangement allowed assessment of whether vervets found the shortest route and/or used paths consistent with one of three simple heuristics to navigate. Single vervets took the shortest possible path in fewer than half of the trials, usually in ways consistent with the most efficient heuristic (the convex hull). When in competition, vervets' paths were consistent with different, more efficient heuristics dependent on their dominance rank (a cluster strategy for dominants and the nearest neighbor rule for subordinates). These results suggest that, like humans, vervets may solve multidestination routing problems by applying simple, adaptive, context‐specific “rules of thumb.” The heuristics that were consistent with vervet paths in this study are the same as some of those asserted to be used by humans. These spatial movement strategies may have common evolutionary roots and be part of a universal mental navigational toolkit. Alternatively, they may have emerged through convergent evolution as the optimal way to solve multidestination routing problems.     

Social correlates of fecal testosterone in male ursine colobus monkeys (Colobus vellerosus): the effect of male reproductive competition in aseasonal breeders

Male testosterone (T) levels are thought to be linked with the mating system, degree of parental care, and male–male aggression in reproductive contexts (The ‘challenge hypothesis’; Wingfield et al., 1990). In many species though, T increases associated with mating behavior cannot be separated from those associated with male–male aggression. We tested the challenge hypothesis on aseasonally breeding ursine colobus (Colobus vellerosus), where male–male competition is intense outside of mating contexts. Fecal samples (N = 109) were collected from > 27 subadult and adult males in seven groups during 13-months of research in Ghana in 2004–2005. Fecal T (fT) levels were determined by enzyme immunosorbant assays. Behavioral data was collected using focal-animal and ad libitum sampling. The number of receptive females in each group did not positively correlate with male fT. There was a trend for adult males to have higher fT than subadult males; however there was no effect of rank on fT. The level of male–male aggression experienced was positively correlated with fT and individual males showed higher mean fT during ‘challenge’ than during ‘non-challenge’ periods. The number of male incursions experienced positively correlated with fT whereas the number of between-group encounters did not. Males attempt to gain reproductive opportunities during incursions, thus these results support the ‘challenge hypothesis’ in C. vellerosus. Outside of mating contexts, higher male fT levels are associated with increased aggression. Male parental investment in the form of infant defense was associated with increased fT, rather than the decline expected from other forms of paternal care.     

Preliminary assessment of natal attraction and infant handling in wild Colobus vellerosus

This study describes natal attraction and infant handling in wild ursine colobus (Colobus vellerosus). Focal animal samples were collected from five infants of 1-16 weeks of age (mean: 14.5 focal hours per infant). Group members may be attracted to an infant, but unable to handle it because of resistance from the mother. We thus measured natal attraction independently from infant handling by the number of interactive approaches received. The youngest infants were most attractive. Immature females were attracted to and handled infants more than other group members. Mothers were tolerant of most handling attempts and infant-directed aggression was rare. A sixth infant was attacked by members of an all-male band, which allowed us to record the expression of natal attraction and infant handling in the context of an acute threat of infanticide. This infant was carried by non-mothers less frequently than the other infants, and its mother resisted handling attempts more often.     

Individuals' behaviors following dye-marking in wild black-and-white colobus (Colobus vellerosus)

The ability to recognize individuals is a prerequisite for analyzing social relationships. We marked five adult and subadult Colobus vellerosus (three in 2002, and two in 2003) at the Boabeng Fiema Monkey Sanctuary, Ghana, to assess the feasibility of dye-marking black-and-white colobus, describe their reactions, and compare some of their behaviors with those of unmarked individuals. We used Nyanzol-D, a nontoxic black dye sprayed on the white tail (or white thigh) of the animal with a spray gun or a tree sprayer. Reactions to the marking procedure ranged from moving away and staring at the observer, without interruption in feeding (in one subject), to fleeing about 5 m away (in four subjects). In 234 hr of ad libitum observations (in 2002 and 2003), marks were scratched or otherwise were the object of attention from the bearer or other individuals on only one occasion. In 2002 we collected 22 hr of observations on the three marked monkeys and some unmarked monkeys in 10-min focal samples. Neither the marked nor the unmarked animals attended to the marks during focal samples. Marked and unmarked individuals displayed similar rates of displacement activities (autogrooming, scratching, and yawning). The proportion of scans with at least one near neighbor varied between marked and unmarked subjects, but the direction of the difference was not the same between males and females. The only aggression observed was displacements, and only in one comparison (out of four) did a difference emerge: the marked subadult male received more displacements than the unmarked males. Overall, marked and unmarked individuals did not differ consistently in our measures. Examination of the potential effects of marking should continue, since changes in pelage coloration may have longer-term social effects in species that rely largely on vision.     

The Function of Male Agonistic Displays in Ursine Colobus Monkeys (Colobus vellerosus): Male Competition,Female Mate Choice or Sexual Coercion?

Male agonistic displays may allow males to assess competitors, females to assess mates, or could be directed at cycling females to sexually coerce them. We analysed the display output of 26 male ursine colobus monkeys (Colobus vellerosus) in four groups over 13‐mo at the Boabeng‐Fiema Monkey Sanctuary, Ghana. Display indices (including three behaviours, loud calls, stiff‐legs, and jump‐displays) were calculated for males in each group. Males vary in their expression of these behaviours suggesting they are sexually selected signals. We investigated the target of displays and whether display indices varied in relation to male dominance rank, eviction of other males, copulation rate, and proceptive behaviours received from females, to assess the primary function of these behaviours. Male displays decreased in vigour over time and were targeted to other groups and males. High‐ranking males displayed more than low‐ranking males. Alpha male display indices correlated with the number of other males evicted from the group. Display rates were generally higher when cycling females were present in the group. However, neither male display index nor rank correlated with copulation rates. Alpha and non‐alpha males gave cycling females equal rates of sexual solicitations; likewise cycling females showed no difference in the rates of proceptive behaviours directed towards alpha and non‐alpha males. Females mated promiscuously and did not seem to base mating decisions on male display output, although data on female hormones is needed to determine if they mate with strongly displaying males more in the periovulatory period. The male–male competition hypothesis received the greatest support, with some support for the female mate choice hypothesis. Although behaviours that appeared sexually coercive were observed, the function of male displays did not seem to be sexual coercion. Displays were rarely directed at females and males that displayed more did not have greater mating success.