Associations Between Golden-Headed Lion Tamarins and the Bird Community in the Atlantic Forest of Southern Bahia

We examined the presence of birds accompanying and foraging in proximity to golden-headed lion tamarins at Una Biological Reserve, Bahia, Brazil. We followed 3 groups of golden-headed lion tamarins over 3 yr. We noted all birds ≤5 m of a lion tamarin during 20-min observation periods. We found 11 different bird species in the presence of the lion tamarins. We most often found insectivores, such as woodcreepers and nunbirds, in association with them, eating prey the tamarins flushed. Associations were most frequent in mature and shade-cocoa forests. The group that spent most of its time in mature and shade-cocoa forest was also the group that foraging birds followed most frequently. Differences in resource availability among forest types, such as the abundance of microforaging environments, may affect the frequency and diversity of birds seen in association with golden-headed lion tamarins.     

Diet, foraging, and use of space in wild golden-headed lion tamarins

Lion tamarins (Callitrichidae: Leontopithecus) are small frugi-faunivores that defend large home ranges. We describe results from the first long-term investigation of wild golden-headed lion tamarins (L. chrysomelas; GHLTs). We present data about activity budgets, daily activity cycles, diet, daily path length, home range size, home range overlap, and territorial encounters for three groups of GHLTs that were studied for 1.5-2.5 years in Una Biological Reserve, Bahia State, Brazil, an area characterized by aseasonal rainfall. We compare our results to those from other studies of lion tamarins to identify factors that may influence foraging and ranging patterns in this genus. Ripe fruit, nectar, insects, and small vertebrates were the primary components of the GHLT diet, and gums were rarely eaten. Fruit comprised the majority of plant feeding bouts, and the GHLTs ate at least 79 different species of plants from 32 families. The most common foraging sites for animal prey were epiphytic bromeliads. The GHLTs defended large home ranges averaging 123 ha, but showed strong affinities for core areas, spending 50% of their time in approximately 11% of their home range. Encounters with neighboring groups averaged two encounters every 9 days, and they were always aggressive. Data about time budgets and daily activity cycles reveal that the GHLTs spent most of their time foraging for resources or traveling between foraging sites distributed throughout their home ranges. The GHLTs spent much less time consuming exudates compared to lion tamarins in more seasonal environments. Additionally, the GHLTs had much larger home ranges than golden lion tamarins (L. rosalia), and did not engage in territorial encounters as frequently as L. rosalia. GHLT ranging patterns appear to be strongly influenced by resource acquisition and, to a lesser extent, by resource defense.     

Mycophagy and its influence on habitat use and ranging patterns in Callimico goeldii

Mycophagy has been documented in a number of species of marmosets and lion tamarins (Callitrichinae) but its effect on ranging behavior is not known. We present the results of 10 years of research on five groups of Goeldi's monkey (Callimico goeldii) at a field site in northwestern Bolivia. We studied the diet and ranging behavior of two of the groups. On average, groups contained 4.5 individuals (range 2.0–9.0), but they gradually decreased in size until only the breeding female remained in the home range. The annual diet was composed of fungi (31.1–34.9%), fruits (34.0–40.6%), prey (17.4–30.1%), and exudates (1.0–10.9%). They had large home ranges (114–150 ha) and over time individuals tended to shift their core areas of use. They used secondary and bamboo forest and forest with dense understories more than expected based on availability. We suggest that the large home ranges and shifting core areas used by C. goeldii are components of a foraging strategy to track patchy, low density, and ephemeral fungal fruiting bodies. Our results, along with data published on other callitrichines, indicate that groups of Leontopithecus, Callithrix, and Callimico that eat fungi have larger home ranges than those that do not. Mycophagy is one of the several factors that evidently affect home range size in callitrichines. Fungi are clearly an important food source for a number of populations, but additional studies are needed to determine why some eat fungi frequently while others do not. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Forest type affects prey foraging of saddleback tamarins,Saguinus nigrifrons

Callitrichids can persist in secondary forests where they may benefit from elevated prey abundance. However, how tamarins forage for prey in secondary forest compared to primary forest has not been examined. Using scan and focal sampling, we compared prey foraging and capture success of two groups of Saguinus nigrifrons in north-eastern Peru: one ranging in primary forest, the other with access to a 10-year-old anthropogenic secondary forest. There was a trend for more prey search in the secondary forest, but prey feeding, capture success and size were lower compared to the primary forest. Tamarins avoided the forest floor, used vertical supports less often and searched on a lower variety of substrates in the secondary forest. In the secondary forest, tamarins did not capture flushed prey, which make up a substantial part of the total prey captures biomass in primary forests. Reduced prey capture success is unlikely to reflect reduced prey availability, since more Orthoptera were found in secondary forest through ultrasonic surveys. Therefore, the prey search activity of S. nigrifrons in young secondary forests seemed rather opportunistic, presumably influenced by altered predation patterns, vegetation structure, as well as prey diversity.     

Golden lion tamarin sleeping-site use and pre-retirement behavior during intense predation

Sleeping sites, their patterns of use, and cryptic pre-retirement behavior mitigate predation risk at sleeping sites and could influence prey fitness. We evaluated sleeping-site usage for 10 groups of golden lion tamarins (GLTs) from a population that recently suffered a substantial decline due to predation at sleeping sites. We recorded the average number of nights that groups spent at their different sleeping sites to determine whether patterns of sleeping-site use were influenced by predation risk, as measured by the rate of encounters with predators, or the availability of suitable sleeping sites, as measured by the size of a group's home range and amount of mature forest within their home range. In addition, we measured travel speed to sleeping sites and compared this speed with that recorded at other times of day. GLT groups spent more nights on average at each of their sleeping sites compared to other callitrichid species for which data are available. Predation risk and habitat characteristics were not significant predictors of how many times groups used each of their different sleeping sites. Groups significantly increased their travel speed just before entering the sleeping site. Rapid locomotion to secure tree cavities may help GLTs avoid crepuscular and nocturnal predators; however, we speculate that this strategy failed numerous GLTs in our study population during the previous decade because they used sleeping sites that were accessible to predators.     

Ecological correlates of lion social organization (Panthers, leo)

Data on lion home range size, pride size, density, group size, cub survival, litter size and adult sex ratio were extracted from studies carried out in 10 habitats. The data were compared with five measures of food supply: mean prey biomass, prey biomass during the season of greatest abundance, prey biomass during the season of least abundance, biomass of middle-sized prey species (i.e. those with mean adult live-weights between 50 and 250 kg), and the mean size of carcasses fed on by lions. The results indicated that range size is inversely correlated with the abundance of prey during the period of least abundance, but not with overall prey abundance. Range size showed no consistent variation with pride size or with minimum metabolic requirements. Pride size (measured in terms of average number of animals per pride and average number of adult females) and cub survival strongly correlated with lean season food abundance. No relationship was found between group size or litter size and any of the measures of food supply Adult sex ratio did not vary consistently with food supply or lion density, although the data did suggest that prides inhabiting small, circumscribed reserves may experience less inter-male competition and this, in turn, may affect the adult sex ratio.     

Prey-mediated avoidance of an intraguild predator by its intraguild prey

Intraguild (IG) predation is an important factor influencing community structure, yet factors allowing coexistence of IG predator and IG prey are not well understood. The existence of spatial refuges for IG prey has recently been noted for their importance in allowing coexistence. However, reduction in basal prey availability might lead IG prey to leave spatial refuges for greater access to prey, leading to increased IG predation and fewer opportunities for coexistence. We determined how the availability of prey affected space-use patterns of bobcats (Lynx rufus, IG prey) in relation to coyote space-use patterns (Canis latrans, IG predators). We located animals from fall 2007 to spring 2009 and estimated bobcat home ranges and core areas seasonally. For each bobcat relocation, we determined intensity of coyote use, distance to water, small mammal biomass, and mean small mammal biomass of the home range during the season the location was collected. We built generalized linear mixed models and used Akaike Information Criteria to determine which factors best predicted bobcat space use. Coyote intensity was a primary determinant of bobcat core area location. In bobcat home ranges with abundant prey, core areas occurred where coyote use was low, but shifted to areas intensively used by coyotes when prey declined. High spatial variability in basal prey abundance allowed some bobcats to avoid coyotes while at the same time others were forced into more risky areas. Our results suggest that multiple behavioral strategies associated with spatial variation in basal prey abundance likely allow IG prey and IG predators to coexist.     

Assessment of Competition between Fisheries and Steller Sea Lions in Alaska Based on Estimated Prey Biomass,Fisheries Removals and Predator Foraging Behaviour

A leading hypothesis to explain the dramatic decline of Steller sea lions (Eumetopias jubatus) in western Alaska during the latter part of the 20th century is a change in prey availability due to commercial fisheries. We tested this hypothesis by exploring the relationships between sea lion population trends, fishery catches, and the prey biomass accessible to sea lions around 33 rookeries between 2000 and 2008. We focused on three commercially important species that have dominated the sea lion diet during the population decline: walleye pollock, Pacific cod and Atka mackerel. We estimated available prey biomass by removing fishery catches from predicted prey biomass distributions in the Aleutian Islands, Bering Sea and Gulf of Alaska; and modelled the likelihood of sea lions foraging at different distances from rookeries (accessibility) using satellite telemetry locations of tracked animals. We combined this accessibility model with the prey distributions to estimate the prey biomass accessible to sea lions by rookery. For each rookery, we compared sea lion population change to accessible prey biomass. Of 304 comparisons, we found 3 statistically significant relationships, all suggesting that sea lion populations increased with increasing prey accessibility. Given that the majority of comparisons showed no significant effect, it seems unlikely that the availability of pollock, cod or Atka mackerel was limiting sea lion populations in the 2000s.     

Seasonal Variation in Seed Dispersal by Tamarins Alters Seed Rain in a Secondary Rain Forest

Reduced dispersal of large seeds into degraded areas is one of the major factors limiting rain forest regeneration, as many seed dispersers capable of transporting large seeds avoid these sites with a limited forest cover. However, the small size of tamarins allows them to use small trees, and hence to disperse seeds into young secondary forests. Seasonal variations in diet and home range use might modify their contribution to forest regeneration through an impact on the seed rain. For a 2-yr period, we followed a mixed-species group of tamarins in Peru to determine how their role as seed dispersers in a 9-yr-old secondary-growth forest varied across seasons. These tamarins dispersed small to large seeds of 166 tree species, 63 of which were into a degraded area. Tamarins’ efficiency in dispersing seeds from primary to secondary forest varied across seasons. During the late wet season, high dietary diversity and long forays in secondary forest allowed them to disperse large seeds involved in later stages of regeneration. This occurred precisely when tamarins spent a more equal amount of time eating a high diversity of fruit species in primary forest and pioneer species in secondary forest. We hypothesized that well-balanced fruit availability induced the movement of seed dispersers between these 2 habitats. The noteworthy number of large-seeded plant species dispersed by such small primates suggests that tamarins play an important, but previously neglected, role in the regeneration and maintenance of forest structure.     

Environmental factors influencing spotted hyena and lion population biomass across Africa

The spotted hyena (Crocuta crocuta Erxleben) and the lion (Panthera leo Linnaeus) are two of the most abundant and charismatic large mammalian carnivores in Africa and yet both are experiencing declining populations and significant pressures from environmental change. However, with few exceptions, most studies have focused on influences upon spotted hyena and lion populations within individual sites, rather than synthesizing data from multiple locations. This has impeded the identification of over‐arching trends behind the changing biomass of these large predators. Using partial least squares regression models, influences upon population biomass were therefore investigated, focusing upon prey biomass, temperature, precipitation, and vegetation cover. Additionally, as both species are in competition with one other for food, the influence of competition and evidence of environmental partitioning were assessed. Our results indicate that spotted hyena biomass is more strongly influenced by environmental conditions than lion, with larger hyena populations in areas with warmer winters, cooler summers, less drought, and more semi‐open vegetation cover. Competition was found to have a negligible influence upon spotted hyena and lion populations, and environmental partitioning is suggested, with spotted hyena population biomass greater in areas with more semi‐open vegetation cover. Moreover, spotted hyena is most heavily influenced by the availability of medium‐sized prey biomass, whereas lion is influenced more by large size prey biomass. Given the influences identified upon spotted hyena populations in particular, the results of this study could be used to highlight populations potentially at greatest risk of decline, such as in areas with warming summers and increasingly arid conditions.     

A field study on the red-bellied tamarin,Saguinus l. labiatus,in Bolivia

A 5-month field study was conducted on red-bellied tamarins,Saguinus labiatus labiatus, in the Pando Department of northern Bolivia. Group sizes ranged from 5 to 10 animals, and each group associated with a group of saddle-backed tamarins,Saguinus fuscicollis weddelli. Members of three groups were trapped and marked and data were collected by radiolocation. The average range size used over 10 days was 19 ha. On average the groups entered about 29% of their range each day and had a mean daily path length of about 1487 m. The groups used a number of different sleeping sites within their ranges. They fed on a variety of different fruits and also on nectar from flowers, resin, and insects. Areas within the home range which were used significantly more than expected were generally those in which one or more of the following existed: a sleeping site, an intergroup encounter site, or a site where the group took shelter during an extended period of heavy rain.     

Progressive parenting behavior in wild golden lion tamarins

Young primates in the family Callitrichidae (the marmosets and tamarins) receive extensive and relatively prolonged care from adults. Of particular note, callitrichid young are routinely provisioned until well after weaning by parents and helpers, which is in stark contrast to typical juvenile primates, who must acquire most of their food independently once they are weaned. Adults of some callitrichid species produce a specialized vocalization that encourages immature group members to take proffered food from the caller. Here, I report that wild adult golden lion tamarins (Leontopithecus rosalia) not only used this food-offering call to encourage young, mobile offspring to approach and take captured prey from them, but as the young began to spend significant time foraging for themselves and to acquire prey by independent means, the frequency of these vocalizations in the context of food transfer declined. Adults then began to use food-offering calls in a novel context: to direct juveniles to foraging sites that contained hidden prey that the adults had found but not captured. During the period of these most frequent adult-directed prey captures, the independent prey-capture success rates of juveniles improved. Thus, adults modified their provisioning behavior in a progressive developmentally sensitive manner that may have facilitated learning how to find food. I hypothesize that as a result of these demonstrations by adults, juveniles either may be encouraged to continue foraging despite low return rates or to learn the properties of productive prey-foraging substrates in a complex environment.     

Tree and forest characteristics influence sleeping site choice by golden lion tamarins

Lion tamarin monkeys are among a small number of primates that repeatedly use a few tree holes for the majority of their sleeping sites. To better understand why lion tamarins rely on tree holes as sleeping sites, we compared the physical characteristics of frequently used sleeping sites, infrequently used sleeping sites, and randomly selected forest locations at multiple spatial scales. From 1990 to 2004, we recorded 5,235 occurrences of sleeping site use by 10 groups of golden lion tamarins (Leontopithecus rosalia) in Poço das Antas Reserve, Rio de Janeiro State, Brazil. Of those, 63.6% were tree holes. Bamboo accounted for an additional 17.5% of observations. Frequently used tree holes were more likely to be found in living trees and their entrances were at lower canopy heights than infrequently used tree holes. We also found that frequently used sleeping sites, in comparison to random sites, were more likely to be found on hillsides, be close to other large trees, have a lower percent of canopy cover, and have larger diameter at breast height. Topography and small‐scale variables were more accurate than were habitat‐level classifications in predicting frequently used sleeping sites. There are ample tree holes available to these lion tamarins but few preferred sites to which they return repeatedly. The lion tamarins find these preferred sites wherever they occur including in mature forest and in relics of older forest embedded in a matrix of secondary forest. Am. J. Primatol. 69:976–988, 2007. © 2007 Wiley‐Liss, Inc.     

Changes in home range size of African lions in relation to pride size and prey biomass in a semi‐arid savanna

Within‐population studies are needed to investigate the extent of, and the factors underlying, intraspecific variation in home range size. We used data from 12 female and 8 male adult lions instrumented with GPS radio‐collars to describe the ranging behaviour of lions in a population from a dystrophic semi‐arid savanna, Hwange National Park, Zimbabwe. We measured prey availability at the home range scale in 2003, 2004, and 2005. For females, home range size increased as pride biomass increased, which is strongly suggestive of expansionism. Once controlled for pride biomass, home range size decreased as prey biomass increased. Pride ranges responded to changes in food abundance on an annual timescale rather than on a seasonal timescale. Female home range size was influenced by the abundance of kudu in the early dry season, whereas it was influenced by buffalo and young elephant abundance in the late dry season. This study shows that female home range size is mainly driven by the size of the pride, but also by prey abundance. Furthermore, female seasonal home range size may be determined, not only by prey abundance, but also by prey dispersion in the landscape. Home range size of males was driven by both prey biomass and the density of female prides.     

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (<Emphasis Type="Italic">Saguinus fuscicollis</Emphasis>)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.     

Multichannel feeding by spider functional groups is driven by feeding strategies and resource availability

Multichannel feeding, whereby consumers feed across resource channels such as upon herbivore and detritivore resources, acts to link discrete compartments of a food web with implications for ecosystem functioning and stability. Currently however, we have little understanding which feeding strategies of consumers underlie multichannel feeding. We therefore link spider functional group and resource density‐dependent or density‐independent feeding strategies to multichannel feeding by quantifying not only consumer diet, but also the relative availability of resources. Here we analysed herbivore (green) and detritivore (brown) prey use by spider communities in grasslands, and tested if available prey biomass proportions were linked to observed spider dietary proportions. Different spider functional groups each linked green and brown resource channels, but while green prey were always consumed in proportion to their relative biomass, brown prey were consumed independently of proportion by some functional groups. Additionally, we found greater intraguild predation by cursorial spiders when green resources were relatively scarcer, suggesting green prey was preferred, and needed to be compensated for when rare. Overall, we observed a stronger consumer connection to the green than brown resource channel, yet this green connection was more variable due to greater range in green resource availability across grasslands and density‐dependent consumption on green prey. Consequently, multichannel feeding by spiders was determined by density‐dependent and density‐independent feeding strategies that varied by spider functional group and across resources channels. Our results demonstrate that the role of multichannel feeding by spiders in linking separate food web compartments is a dynamic component of food web structure in these wild grasslands.     

Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest

Forming interspecific associations is one of many strategies adopted by primates in order to avoid predation. In addition to improved predator detection and avoidance, benefits of interspecific associations relate to improved foraging efficiency. In this study we tested these two hypotheses explaining associations between the endangered golden-headed lion tamarin, Leontopithecus chrysomelas and the sympatric Wied's marmoset, Callithrix kuhlii. We estimated predation risk by recording the number of encounters between lion tamarins and potential predators in cabruca agroforest (shaded cacao plantation) and in mosaic forest (a mix of cabruca, primary and secondary forest). To evaluate if the association between the two species was related to foraging benefits we recorded the number of associations between the two species when the lion tamarins were eating and when they were not eating. To test if the association occurred to improve predator detection and avoidance, we evaluated if associations between the species were more frequent in areas with higher predation risk and during the part of the day when predation risk is higher. We also compared the number of associations 3 months before birth events and 3 months after, when the lion tamarins are more susceptible to predation. Predation risk, mainly by raptors, was significantly higher in cabruca than in mosaic forest (0.17 and 0.05 encounters with predators per hour of observation, respectively). Associations were significantly more frequent after birth events and during the part of the day when predation risk was also higher (5-6 am until noon). We did not observe any direct evidence of foraging-related advantages of interspecific associations for the lion tamarins. The tamarins did not associate more when they were foraging. Our findings suggest that lion tamarins are more exposed to predation in cabruca than in mosaic forest and associations between lion tamarins and Wied's marmosets are related to predation avoidance.     

Diet of Eurasian lynx <Emphasis Type="Italic">Lynx lynx</Emphasis> in the northern Dinaric Mountains (Slovenia and Croatia)

The Eurasian lynx Lynx lynx (Linnaeus 1758) is an opportunistic predator that usually selects the smallest ungulate available. Its diet varies considerably among different regions; therefore it is important to study lynx diet in different parts of the species’ range. We studied the diet of lynx from the endangered Dinaric population in Slovenia and Croatia by analyzing lynx scats, prey remains, and stomach contents. Dinaric lynx mainly killed European roe deer Capreolus capreolus (0.64 frequency of occurrence, 79% of all consumed biomass), which were used more frequently during winter and spring. Ungulates were killed more often by adult males than by lynx of other age and sex groups. In contrast to studies from other regions, lynx in the northern Dinaric Mountains also frequently fed on the edible dormice Glis glis (0.18 frequency of occurrence, 7% of all consumed biomass). This large rodent appears to be an important alternative prey, especially for females and young lynx, and was the reason for the highest use of rodents reported so far for the Eurasian lynx. Edible dormice in Dinaric forests have highly variable numbers of active animals. Seasonal and possibly annual variation in dormouse availability obviously affects lynx diet. This is a rare example where variability in the availability of the alternative prey and not the preferred prey leads to the dietary shift. This study confirms the opportunistic nature of Eurasian lynx and the regional variability of its diet.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

Census and distribution of the golden lion tamarin (Leontopithecus rosalia)

During 1990–1992, a survey of the golden lion tamarin, Leontopithecus rosalia, was carried out throughout its known distribution area. Forest remnants were identified by visual interpretation of Landsat‐TM satellite images. Localities occupied by L. rosalia were first identified by interviews with local people. All forests more than 20 ha in size, and for which two or more interviews suggested the presence of the species, were surveyed using “play‐back” recordings of lion tamarin long calls. The total wild population of L. rosalia, including that of the Poço das Antas Biological Reserve, was estimated to be 562 individuals in 109 groups. The lion tamarins were generally found in four major areas of forest (six or more groups per forest, not including Poço das Antas), with a further 12 groups isolated in small forest patches. Currently the species' distribution is restricted to just four municipalities in the state of Rio de Janeiro: Silva Jardim, Cabo Frio, Saquarema, and Araruama. Although they are typically confined to lowland forest of <300 m altitude, L. rosalia was recorded at an altitude of 550 m in one locality. Average group size varied from 3.6 to 5.7 individuals, and densities from 0.39 groups/km² to 2.35 groups/km² (2.17 individuals/ km² to 8.53 individuals/km²). Six of the isolated groups found during the survey were successfully translocated to a forest of 2,400 ha. There is now also a significant population of reintroduced lion tamarins. Overall, however, the possibilities for further expansion of the wild population are severely limited. Am. J. Primatol. 59:29–44, 2003. © 2003 Wiley‐Liss, Inc.