Saimiri Oerstedii Research Articles

Survey of medium-sized and large mammals of Piedras Blancas National Park, Costa Rica

Piedras Blancas National Park, in southern Costa Rica, is an important component of two biological corridors connecting the Osa Peninsula (Corcovado National Park) and La Amistad International Park. Understanding the mammal community composition of Piedras Blancas will provide baseline data to evaluate the success of conservation efforts. We used camera traps and opportunistic observations to describe the medium-sized and large mammals of the park. We deployed camera traps for 1,440 trap nights (2016-2018). We detected 19 mammal species from seven orders and 13 families. Five species are globally threatened: Leopardus wiedii (Schinz, 1821), Saimiri oerstedii (Linnaeus, 1758), Ateles geoffroyi (Kuhl, 1820), Alouatta palliata (Gray, 1849), and Tapirus bairdii (Gill, 1865). We did not detect two locally threatened species, Panthera onca (Linnaeus, 1758) and Tayassu pecari (Link, 1795). Our research highlights a need for critical conservation work within the proposed biological corridor to support Costa Rica’s most threatened wildlife.

Conservation in human-dominated landscapes: Lessons from the distribution of the Central American squirrel monkey

It is becoming increasingly evident that many species can tolerate different degrees of habitat perturbation and that we often underestimate the capacity of some human-modified landscapes to support populations of declining species. We provide new insights into the distribution of the endangered Central American squirrel monkey and habitat changed over the last 20 years. The species has shown an approximate 60% decrease between the historic and the present extent of occurrence, with an area of occupancy of also about 60% of the present extent of occurrence. Despite the large habitat alteration, our results show surprisingly that this endangered monkey can persist in highly perturbed landscapes. This offers opportunities to improve its long-term chances of survival through conservation actions to protect and restore its habitat on the one hand, and to reduce the monkey's direct mortality on the other. Surprisingly we found several troops in 16 localities in a large area along the Rio Coto Brus where the Central American squirrel monkey was previously unrecorded. Some of our observations were made in cloud forests at a record high altitude for this species. We speculate the monkeys are using these highland areas as a corridor between suitable lowland habitats in the Coto Brus and the Rio Sierpe-Osa Peninsula regions. In response, we suggest strategies to help in the monkey's long-term conservation, that can be used as an example for other endangered species.

Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences.

Some previous genetic studies have been performed to resolve the molecular phylogenetics of the squirrel monkeys (Saimiri). However, these studies did not show consensus in how many taxa are within this genus and what the relationships among them are. For this reason, we sequenced 2,237 base pairs of the mt COI and COII genes in 218 Saimiri individuals. All, less 12 S. sciureus sciureus from French Guyana, were sampled in the wild. These samples represented all the living Saimiri taxa recognized. There were four main findings of this study. (1) Our analysis detected 17 different Saimiri groups: albigena, cassiquiarensis, five polyphyletic macrodon groups, three polyphyletic ustus groups, sciureus, collinsi, boliviensis, peruviensis, vanzolinii, oerstedii and citrinellus. Four different phylogenetic trees showed the Central American squirrel monkey (S. oerstedii) as the most differentiated taxon. In contrast, albigena was indicated to be the most recent taxon. (2) There was extensive hybridization and/or historical introgression among albigena, different macrodon groups, peruviensis, sciureus and collinsi. (3) Different tests showed that our maximum likelihood tree was consistent with two species of Saimiri: S. oerstedii and S. sciureus. If no cases of hybridization were detected implicating S. vanzolinii, this could be a third recognized species. (4) We also estimated that the first temporal splits within this genus occurred around 1.4-1.6 million years ago, which indicates that the temporal split events within Saimiri were correlated with Pleistocene climatic changes. If the biological species concept is applied because, in this case, it is operative due to observed hybridization in the wild, the number of species within this genus is probably more limited than recently proposed by other authors. The Pleistocene was the fundamental epoch when the mitochondrial Saimiri diversification process occurred.

Subspecies of the Central American Squirrel Monkey (Saimiri oerstedii) as Units for Conservation

The accurate diagnosis of conservation units now typically includes recognition of genetic diversity and unique evolutionary lineages and is necessary to inform the conservation management of endangered species. We evaluated whether the two currently recognized subspecies of the endangered Central American squirrel monkey (Saimiri oerstedii) in Costa Rica are evolutionarily significant units (ESUs) that should be managed separately in conservation efforts. We used previously published sequences of 50 individuals of Saimiri oerstedii for 880 bp of the mtDNA d-loop and genotypes of 244 individuals for 16 microsatellites and conducted novel analyses to characterize genetic differentiation between subspecies of Saimiri oerstedii. We measured sequence differentiation and inferred an intraspecific molecular phylogeny and a haplotype network, and found consistent results supporting statistically significant divergence and reciprocal monophyly between subspecies. A population aggregation analysis also supported Saimiri oerstedii citrinellus and S. o. oerstedii as diagnosably distinct units. These results confirm previous genetic studies with smaller sample sizes and are consistent with other factors including differences in pelage and morphology and divergence at nuclear markers. Conservation managers should manage these subspecies separately to prevent the loss of genetic diversity via artificially induced outbreeding. High levels of genetic diversity may buffer populations against outside extinction pressures, to which Saimiri oerstedii are vulnerable because of their dwindling habitat and small population size.

Scale-Dependent Effects of a Heterogeneous Landscape on Genetic Differentiation in the Central American Squirrel Monkey (Saimiri oerstedii)

Landscape genetic studies offer a fine-scale understanding of how habitat heterogeneity influences population genetic structure. We examined population genetic structure and conducted a landscape genetic analysis for the endangered Central American Squirrel Monkey (Saimiri oerstedii) that lives in the fragmented, human-modified habitats of the Central Pacific region of Costa Rica. We analyzed non-invasively collected fecal samples from 244 individuals from 14 groups for 16 microsatellite markers. We found two geographically separate genetic clusters in the Central Pacific region with evidence of recent gene flow among them. We also found significant differentiation among groups of S. o. citrinellus using pairwise FST comparisons. These groups are in fragments of secondary forest separated by unsuitable “matrix” habitats such as cattle pasture, commercial African oil palm plantations, and human residential areas. We used an individual-based landscape genetic approach to measure spatial patterns of genetic variance while taking into account landscape heterogeneity. We found that large, commercial oil palm plantations represent moderate barriers to gene flow between populations, but cattle pastures, rivers, and residential areas do not. However, the influence of oil palm plantations on genetic variance was diminished when we restricted analyses to within population pairs, suggesting that their effect is scale-dependent and manifests during longer dispersal events among populations. We show that when landscape genetic methods are applied rigorously and at the right scale, they are sensitive enough to track population processes even in species with long, overlapping generations such as primates. Thus landscape genetic approaches are extremely valuable for the conservation management of a diverse array of endangered species in heterogeneous, human-modified habitats. Our results also stress the importance of explicitly considering the heterogeneity of matrix habitats in landscape genetic studies, instead of assuming that all matrix habitats have a uniform effect on population genetic processes.

Genetic evidence for dispersal by both sexes in the Central American Squirrel Monkey, Saimiri oerstedii citrinellus

Sex-biased dispersal (SBD) is common in many vertebrates, including primates. However, dispersal patterns in New World primates may vary among closely related taxa or populations in different local environments. Here, we test for SBD in an endangered New World primate, the Central American Squirrel Monkey (Saimiri oerstedii citrinellus). Previous studies of behavioral ecology suggest predominantly female dispersal in S.o. oerstedii in the Southern Pacific region of Costa Rica. However, our genetic data do not support strongly female-biased dispersal in S.o. citrinellus in the Central Pacific region. Our tests for SBD using microsatellite data including comparisons of isolation-by-distance, AI(c) , and F(ST) values between males and females were not significant. Also, we found greater population genetic structure in mitochondrial markers than in microsatellite markers, indicative of predominantly male dispersal. We conclude that both sexes disperse in S.o. citrinellus, and that males probably disperse over longer distances. We discuss how spatial and temporal variation among local populations should be taken into account when studying dispersal patterns and especially sex bias.

Anthropochorous Wild Mammal Taxa and Conservation Lists

Invasions of nonindigenous species, especially on oce-anic or oceanic-like islands, are one of the major causesof species extinction and ecosystem alteration at a glo-bal scale (Schofield 1989; Clout & Lowe 1997). It is notoften recognized, however, that humans have played anactive role in the dispersal of many mammals during thelast 10,000 years. Such ancient introductions on islands,sometimes coupled with interbreeding of different lin-eages, gave rise to the formation of morphologically rec-ognized “subspecies”or “species,” as described by earlytaxonomists. In turn, taxonomic recognition and in-ferred endemicity prompted special focus on theseforms by conservationists and their inclusion on nationaland international Red Lists.The focus of modern conservation biology is the pres-ervation of all natural biota and the identification of trulyevolutionarily significant units (ESUs) or potential unitsof conservation (Moritz 1994) as targets for action. It isevident that introduced populations, even if taxonomi-cally recognized, fail to represent divergent phyloge-netic units and do not deserve conservation efforts com-parable to those of ESUs.There is no general consensus on the treatment of an-thropochorous taxa—populations whose ancient dis-persal to new areas was mediated by humans—in con-servation priority assessment. In other words, thisquestion has not been properly addressed or has beenleft to the “sensibility”of individual scholars. In one in-teresting case the conservation of a highly threatenedspecies, the Central American squirrel monkey (Saimirioerstedii), has been hampered because it was errone-ously considered a hybrid population deriving from apre-Hispanic introduction (Cropp & Boinski 2000).Probably no other place in the world has been soheavily affected for such a prolonged period of time byhuman activities as the Mediterranean region. On theMediterranean islands, human appearance in the earlyNeolithic caused a complete turnover of the mammalianfauna, with extinction of native species and gradual in-troduction of new species (Blondel & Vigne 1993). Inva-sions by nonindigenous mammals also affected conti-nental lands. On islands, however, the absence of earlyfossil records of these mammals offers unequivocal evi-dence of anthropogenic introductions (cf. Vigne 1992).Species may have been introduced more than once fromdifferent localities, as has been demonstrated for the Sar-dinian fox (Vulpes vulpes ichnusae) (Frati et al. 1997).Until now, no particular criteria have been developedfor taxonomic treatment of introduced mammals andthus for their inclusion in threatened-species categories.

The Central American Squirrel Monkey (Saimiri oerstedii): Introduced Hybrid or Endemic Species?

Although squirrel monkeys (Saimiri spp., Primates: Cebidae) are abundant and widespread in South America, the disjunct Central American species, Saimiri oerstedii, has been restricted to the Pacific wet lowlands of Costa Rica and Panama since the earliest historical records. This taxon is now endangered in Costa Rica and nearly extinct in Panama because of habitat loss, development, and the pet trade. Conservation efforts have been hampered because of the influential, but untested, speculation that S. oerstedii represents a hybrid species introduced by prehispanic Amerind traders from multiple localities in South America. Using nuclear and mitochondrial DNA sequence data to reconstruct the phylogenetic relationships among Saimiri from Central and South America, we reexamine the taxonomic status of squirrel monkeys from different geographic regions. The sequence data support P. Hershkovitz's (1984, Am. J. Primatol. 6: 257–281) taxonomy advocating four distinct species. Combining this information with evidence from the fossil record to date the divergence times among sister taxa, we test and reject the hypothesis that Central American squirrel monkeys are the result of human introduction.

Positional behavior and vertebral morphology in atelines and cebines.

Atelines are of particular interest to primate evolutionary studies because they converge with hominoids in postcranial anatomy, including the vertebral column. Currently, our understanding of ateline vertebral morphology is limited to mainly qualitative descriptions and functional interpretations based on general categories of positional behavior. Even less is known about the vertebrae of other platyrrhines. This study more closely examines vertebral form and function in atelines and cebines by combining direct field observations of axial postures and movements, assessments of spinal loading regimes, and a detailed vertebral morphometric analysis. Field observations (Corcovado, Costa Rica) on Ateles geoffroyi, Alouatta palliata, Cebus capucinus, and Saimiri oerstedii were quantified in conjunction with a morphometric analysis of ateline and cebine lumbar vertebrae. Hylobates was also included for comparison. Compared to Cebus and Saimiri, atelines engage more frequently in postures and locomotor behaviors that induce pronounced bending loads on the spine. All atelines share lumbar adaptations for resisting bending, including ventrodorsally elongated vertebral bodies and perpendicularly oriented transverse processes. Among atelines, lumbar region lengths and vertebral bodies are shortest in Ateles and Brachyteles, longest in Alouatta (resembling Cebus), and intermediate in Lagothrix. Compared to Cebus and all atelines, Saimiri has a relatively longer lumbar region, longer and less ventrodorsally expanded vertebral bodies, and more ventrally oriented transverse processes. These features accentuate bending loads, but increase the sagittal flexibility required for leaping. Vertebral convergence between hylobatids and atelines is more readily interpretable as a product of shared spinal loading patterns than shared positional behaviors.

Feeding behaviour and predation of a bat by Saimiri sciureus in a semi-natural Amazonian environment.

A free-ranging group of Saimiri sciureus was studied in a semi-natural forest habitat in eastern Amazonia, where behaviour patterns were broadly similar to those recorded for the species in the wild. According to focal-animal samples, the monkeys spent the vast majority of their time foraging and feeding, in particular for arthropod prey, which contributed almost half of identified food items. The predation of a small-bodied bat was also observed, although the study animals did not appear to forage systematically for chiropterans in the manner recorded for Saimiri oerstedi.

Male residence and association patterns in Costa Rican squirrel monkeys (Saimiri oerstedi).

A model is developed to interpret the evolution of the unusual pattern of male residence and social structure in the Costa Rican squirrel monkey (Saimiri oerstedi). Observations of a wild population document that males 1) maintain close spatial and social associations with other males, especially other males in their birth cohort, but not females and infants; 2) exhibit negligible within-troop male-male aggression, high levels of antipredator vigilance, and frequent predator deterrence; 3) cooperate in aggressive olfactory investigation of females; and 4) maintain residence in their natal troop with their male birth cohort, eventually succeeding to reproductive positions in their natal troop. Less commonly, male age-cohorts leave the troop well past reproductive maturity and usurp the reproductive male cohort in another troop. We suggest that this divergence from the social structure typical of male squirrel monkeys in Peru (males transient between troops, weak male-male bonds, high within-troop male aggression, little investment in anti-predator behavior) arose because female S. oerstedi in Costa Rica are not philopatric. In Costa Rica, long term reproductive cooperation is likely advantageous to males, because of the frequent movement of female S. oerstedi between troops; the potential costs of inbreeding are reduced. Male S. oerstedi of all ages residing in the same troop, but especially those of the same age cohort, are predicted to have a much higher degree of genetic relatedness than adult females. © 1994 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.

Neotropical primate conservation

The greatest threat to Neotropical primates is the loss of tropical forest for agriculture, ranching, commercial logging and hydroelectric projects. Hunting of primates for consumption or sale and live capture for the pet trade and for biomedical purposes is also a threat to certain species. Twenty-eight of the 76 Neotropical primate species are considered endangered and the highest density of endangered taxa occurs in Brazil's Atlantic forest, followed by Amazonia and Middle America. The most endangered Neotropical primate genera are Brachyteles and Leontopithecus, followed by some species of Ateles, Lagothrix, Saguinus and the Central American squirrel monkey ( Saimiri oerstedii citrinellus). Solutions to the problems of primate conservation are discussed, including habitat conservation, protection against poaching and international primate trade, education, research and captive propagation, and examples of successful conservation efferts are provided.

Preliminary observations on squirrel monkey (Saimiri oerstedi) vocalizations in Costa Rica.

This study was an initial attempt to analyze quantitatively vocalizations from the Central American squirrel monkey, Saimiri oerstedi. Vocalizations were recorded in the wild at P. N. Corcovado (S. o. oerstedi). and at P. N. Manuel Antonio (S. o. citrinellus). Additional recordings were made from captive individuals of both subspecies. The acoustic structure of analyzed vocalizations resembled most closely the vocal repertoire of South American Saimiri with the "gothic arch" phenotype, in agreement with the prominent gothic arch facial pattern of S. oerstedi. New structural subtypes of the twitter ("dog-tooth twitter") and the chuck ("bent-mast chuck") not previously found in an extensive library of South American Saimiri sound spectrograms were documented. Calls used by older infants when socially separated and when approaching an adult male were essentially identical (sharing typical "isolation peep" structural features) but had significantly different duration and peak frequency. Analysis of recordings from an escaped captive female calling outside her compound over a 3-day period indicated the presence of numerous structural intermediates between typical chuck, twitter, and peep calls.

Prevalence of Malaria in Panamanian Primates

Over a 35-year period, 1,994 Panamian primates representing seven species have been examined for malaria at the Gorgas Memorial Laboratory. Plasmodium brasilianum was the only species found. The prevalence rates for the various species were: Ateles geoffroyi (30.3%), A. fusciceps (10.6%), Alouatta villosa (4.0%), and Cebus capucinus (2.2%). No infections were found in Saimiri iierstedii, Aotus trivirgatus, and Saguinus geoffroyi. Malaria in primates has interested workers at Gorgas Memorial Laboratory for the past 35 years. Clark (1930, 1931) surveyed Panamanian primates for malaria and other parasites. Clark and Dunn (1931) reported an attempt to transfer the malaria parasite of Ateles geoffroyi to man. Taliaferro and Taliaferro (1934a, b, c, 1944) and Taliaferro and Kluver (1940a, b) studied Plasmodium brasilianum in Panamanian primates. Taliaferro and Taliaferro (1934d) and Taliaferro and Cannon (1934) attempted the transmission of P. falciparum to the Panamanian howler monkey (Alouatta villosa). Since these early reports, much additional information has been obtained. Nearly 2,000 Panamanian primates have been examined on receipt at the laboratory from 1931 to 1957 and during the past year. The purpose of this paper is to summarize the information on the prevalence of malaria in these animals. MATERIALS AND METHODS Records kept at the laboratory include information on species, geographic origin, age, and sex of the primate. Primates examined were Ateles fusciceps (black spider monkey), Ateles geoffroyi (red spider monkey), Cebus capucinus (whiteface monkey), Alouatta villosa (black howler monkey), Saimiri oerstedii (squirrel monkey), Aotus trivirgatus (night monkey), and Saguinus geoffroyi (titi marmoset). Weight was the principal factor used in separating infants from juveniles. One thousand grams was used as a separation weight for Ateles and Alouatta, 750 g for Cebus, 300 g for Saimiri and Aotus, and 200 g for Saguinus. Juveniles were separated from adults by lack of sexual maturity. Received for publication 27 April 1966. * During the past year, these studies have been supported in part by the United States Army Medical Research and Development Command, grant DA-MD-49-193-65-G-165. Until last year, all primates entering Gorgas Memorial Laboratory were examined on at least 5 consecutive weekdays for malaria parasites and monthly thereafter. In most cases, the initial period of five daily examinations now is followed by weekly examinations. Thick blood films are made, stained with Giemsa, and examined microscopically.