Introduction: New World Primates


With an evolutionary history dating back 30 million years, the Neotropical primates now present a remarkable radiation of monkeys, comprising some 200 extant taxa (c. 150 species), and ranging in size from the smallest anthropoid, the Pygmy marmoset Cebuella pygmaea at c. 100 g, to the muriquis (Brachyteles) and spider monkeys (Ateles) weighing more than 10 kg. They occur throughout the American tropics – the Mexican spider monkey Ateles geoffroyi just north of the Tropic of Cancer, and the Southern brown howler Alouatta guariba extends some distance south of the Tropic of Capricorn to (31°S), where the Atlantic forest gives way to the Pampas. There are three biogeographic communities for these primates, each having considerable endemism: (1) southern Mexico, Central America, and central and northern Colombia and Venezuela, with 45 taxa (spp and subspp); (2) the Amazon basin, including the Guianas and the eastern slopes of the Andes, with 135 taxa (spp and subspp); (3) the non-Amazonian tropical savannah (Cerrado), dry forests in north-east Brazil (Caatinga), southern Bolivia and Paraguay, the Chaco, and the lowland, montane, evergreen and semi-deciduous Atlantic forest in Brazil, Paraguay and Argentina, with 31 taxa (spp and subsp).

Rosenberger (1992, 2011) neatly summarized the four principal adaptive zones of these primates using an ‘ecophylogenetic model’ of size, diet and locomotion. The first is occupied by the Callitrichidae (marmosets, Goeldi's monkey Callimico goeldii, lion tamarins and tamarins); small (100–750 g) insectivore-frugivore-exudativores of the middle to lower canopy and understorey of the forest. They have specific adaptations for moving about on tree trunks, for vertical clinging and leaping (extreme in Pygmy marmosets and Goeldi's monkey) and, in the case of the marmosets, for tree gouging and feeding on plant exudates such as gums (Coimbra-Filho & Mittermeier, 1978; Garber et al., 2009; Youlatos & Meldrum, 2011). The second is that of the Cebidae (squirrel monkeys and capuchin monkeys); small to middle-sized (750–3500 g), dextrous, canopy insectivore-omnivores that are quadrupedal walkers and leapers (Fragaszy et al., 2004; Jack, 2007). The smaller squirrel monkeys are dextrous in the sense of being agile, small-branch, foliage gleaners, whereas the larger capuchin monkeys are manipulative and destructive foragers, and extraordinarily creative in processing and obtaining a wide variety of animal and plant foods. Then come the Pitheciidae; small to middle-sized (750–3000 g), hard-fruit eaters and seed predators, with a specialized anterior dentition to suit, and including quadrupedal walkers and leapers (canopy species: uakaris Cacajao and bearded sakis Chiropotes), and vertical clingers and leapers (lower canopy: sakis Pithecia) (Norconk, 2007; Norconk & Veres, 2011). The titi monkeys (Callicebus), also pitheciids, are small, understorey, quadrupedal walkers and leapers that specialize on small, sometimes hard, fruits and seeds, besides leaves and insects. Their charm and unusualness comes from them living in small monogamous families, and the ♂ shows extensive care of the young; a social and mating system also found in the similar-sized night monkeys (Aotus), the only nocturnal anthropoid. Consensus has still to be reached concerning the phylogenetic affiliation of Aotus; over the years, it has been placed in the Atelidae, Pitheciidae and Cebidae (Fernandez-Duque, 2007). Molecular genetic evidence aligns Aotus with the Cebidae but, in his most recent review of the functional morphology of the platyrrhines, Rosenberger (2011) places them in the subfamily Homunculinae in the Pitheciidae, along with the titi monkeys. Groves (2001) and Rylands & Mittermeier (2008) place them in their own family, the Aotidae. Their diets are poorly known; they are frugivores, eating leaves, insects, flowers and fungi, but there are no morphological traits to indicate seed predation and the exploitation of hard fruits. The fourth adaptive zone is that of the Atelidae (howler, woolly and spider monkeys, and muriquis); large (5–10 kg), suspensory (prehensile-tailed) frugivore-folivores. The muriquis and howler monkeys are the most folivorous, having dental adaptations for crushing leaves, and an enlarged caecum to ferment them. The woolly monkeys (Lagothrix) and spider monkeys are the most frugivorous, eating a wide array of ripe fruits, and occupying large home ranges as a result (Rosenberger & Strier, 1989; Di Fiore & Campbell, 2007).

The first field study of a primate was by Carpenter (1934); a study of Mantled howlers Alouatta palliata on the island of Barro Colorado, Panama. Despite this auspicious start, in 1972, the year of the first International Zoo Yearbook dedicated to the New World monkeys (Volume 12), published field studies of New World primates were still scarce and largely restricted to the four occurring on Barro Colorado (spider monkeys, howler monkeys, White-faced capuchins Cebus capucinus and Geoffroy's tamarin Saguinus geoffroyi), with just a smattering of field observations elsewhere: Weeper capuchins Cebus olivaceus in the Venezuelan llanos (Oppenheimer & Oppenheimer, 1973), and squirrel monkeys in Panama and Colombia (Thorington, 1967; Baldwin & Baldwin, 1972). A report on titi monkey territoriality in Colombia by Mason (1968) was the sole platyrrhine entry in a book dedicated to discussing adaptation and variability in primates.

From the 1940s, there was regular trade in New World primates for pets, zoos and research centres but there was a dramatic increase in the use of New World monkeys for biomedical research in the mid-1950s. Enormous numbers began to be shipped to Florida from Barranquilla, Colombia, and the Amazon ports of Iquitos (Peru) and Letícia (Colombia). The volume of trade – annual registered imports through Miami, FL, USA, increased from 26 872 in 1961 to 52 501 in 1967 – resulted in alarm calls concerning widespread extirpation, even in the Amazon (Heltne, 1967a,b), and the recognition of the need to regulate the sources, housing and transport conditions of the animals; predominantly squirrel monkeys, capuchin monkeys, Peruvian and Colombian tamarins, and night monkeys (Cooper, 1968). Interest in having for medical research small non-prosimian primates that were fast-breeding, and easy and cheap to maintain, resulted in massive exports of callitrichids, mainly tamarins (especially Cotton-top tamarin Saguinus oedipus) to the United States, but Common marmosets Callithrix jacchus from Brazil, Guyana and French Guiana to the United Kingdom and Europe. Accordingly, the first New World primate volume of the Yearbook, edited by Philip Hershkovitz (1972), was ‘designed for a discussion of New World monkeys from the time of capture and use in the wild to their confinement and use in seminatural, simulated natural, and artificially controlled environments’ (p. 3). Four of the articles addressed capture, housing and transport, two discussed social communication (marmosets and capuchins), four described case studies of maintenance procedures and breeding in zoos, and another two reviewed the parasites being imported with the monkeys. Hershkovitz dedicated his introductory article to a review of their taxonomy and zoogeography following his letter to Science in which he ridiculed the lack of attention given then to this fundamental aspect of the use and study of primates (Hershkovitz, 1965). Coimbra-Filho (1972) argued for the establishment of breeding colonies for endangered Atlantic forest species, such as the lion tamarins, but otherwise only three pages were dedicated to conservation: a review of the status of the Latin American primates, of which practically nothing was known (Warland, 1972).

In 1976, the principal countries exporting primates – Colombia, Peru and Brazil – banned or severely restricted the trade, resulting in the establishment of breeding and primate research centres in the countries themselves. In Peru particularly there were major efforts to survey primate populations, assess ‘stocks’ and evaluate the effects of trapping (e.g. PAHO, 1976; Proyecto Peruano de Primatologia ‘Manuel Moro Sommo’, 1990). The Pan American Health Organization (PAHO) sponsored countrywide primate surveys (PAHO, 1976; Muckenhirn & Eisenberg, 1978; Freese et al., 1982). In 1976, Miranda Stevenson achieved the first ever study of the Common marmoset in the wild (Stevenson & Rylands, 1988), and in a benchmark volume, edited by Devra G. Kleiman, the first field studies of tamarins (S. geoffroyi and S. oedipus) were published, along with the results of a number of pioneer field surveys and reviews of major advances in callitrichid breeding biology, behaviour and maintenance in captivity (Kleiman, 1978; see also Rothe et al., 1978).

The second volume of the Yearbook dedicated to New World primates, published 10 years later (Volume 22, 1982), clearly reflects these developments. Edited by Russell A. Mittermeier and John P. Hearn, the first six articles, covering 68 pages, discussed the conservation status and threats to primates in Venezuela, the Brazilian Atlantic forest, and in the Amazon in Brazil, Peru and Suriname. The remaining articles reported on the status and conservation of the long-lost Peruvian Yellow-tailed woolly monkey Lagothrix flavicauda, the use of reintroduction for the conservation of endangered primates, and the significant progress achieved in the breeding and maintenance of an array of New World monkeys from Pygmy marmosets to Goeldi's monkey, squirrel monkeys and spider monkeys. There were also reports on reproductive physiology and reproductive parameters – owl monkeys, saki monkeys, capuchin monkeys and marmosets – that reflected efforts to maximize reproductive performance and survival in breeding colonies to supply biomedical laboratories (see also Hearn, 1983). The reproductive physiology of the Common marmoset (twinning, chimaerism and reproductive suppression) was of sufficient interest in itself to inspire research initiatives in a number of laboratories (Hearn, 1983).

So, here we have the third volume of the International Zoo Yearbook dedicated to these primates, 40 years on from the first New World Primate volume in 1972. It starts with a brief review of the taxonomy, so changed since 1972 and in very large part owing to the scholarship and dedication of Hershkovitz himself. Rylands et al. (2012) took to heart not only Hershkovitz's (1965) appeal that taxonomy precedes research on captive primates, but also Collar's (1997) insistence that it precedes conservation. The initial idea was to have conservation status reviews of the countries or regions. The task, relatively easy in 1982, is now too onerous with the enormous amount of information available and the complexity of the issues. Meanwhile, the situations described in the 1982 reviews have not really changed in essence, only in degree. The destruction of the Amazon forests, for example, proceeds apace. In 1972, the Brazilian Amazon was estimated to have lost about 1% of its forest, now more than 20% has been lost – but the destruction is not uniform. Ecuador has suffered most particularly through highway construction, colonization and petroleum drilling, and the report by de la Torre (2012) is severely disturbing, with 20 of its 21 primate species and subspecies now found to be nationally threatened or near threatened. Thirty years on the balance for the Atlantic forest has been positive overall. The extraordinary upsurge of conservation non-governmental organizations in the Atlantic forest, its listing as a Biosphere Reserve (1992–1993) and the expansion of the protected-areas system mean that now a large proportion of the remaining forest is protected. There are ongoing long-term programmes to protect the most threatened primates there, supported by zoos and zoo associations, using them as flagship species to promote a conservation ethic and protect wide expanses of the forests where they live (e.g. Jerusalinsky et al., 2011).

The first two articles in Volume 46 have their predecessors in 1972 and 1982, but the rest really do not and that paradoxical expression ‘quantum leap’ comes to mind. They bring to the Yearbook clear examples, perhaps just glimpses, of the extraordinary progress in our understanding of the diversity, phylogeny and evolution of the New World monkeys (Martin, 2012; Rylands et al., 2012), and their functional sociobiology, indicating how this has influenced their management and husbandry in captivity (Anzenberger & Falk, 2012). Captive management of the New World primates has benefited from an understanding of their lives in the wild and, most significantly, has begun to overcome, through the remarkable, tireless, intelligent and thoughtful efforts of many (represented here by Barnes, 2012; Barnes & Cronin, 2012; Buchanan-Smith, 2012; Jens et al., 2012; Price et al., 2012), the entirely utilitarian, industrial-scale approach to breeding that was pre-eminent from the 1950s to the 1980s (e.g. Schmidt, 1972). A further four articles (Bairrão Ruivo & Wormell, 2012; Kierulff et al., 2012; Lernould et al., 2012; Savage & Guillen, 2012) provide clear examples of the successful development of threatened species programmes for primates that combine in situ and ex situ initiatives – pioneered by The Durrell Wildlife Park, Jersey, British Channel Islands, championed and developed by the International Union for Conservation of Nature/Species Survival Commission Conservation Breeding Specialist Group, and put into action with or by the various regional, national and international zoological park and aquarium associations, and their conservation committees. Lastly, Fernandez-Duque (2012) demonstrates the benefits of an integrated captive–field approach in providing insights into the private lives and ecological needs of New World primates, and most especially the difficult-to-study nocturnal owl monkeys.

In the second edition of Wild Mammals in Captivity, Devra Kleiman pointed out that ‘the past decade has […] seen an explosion in concern about animal welfare’ (Kleiman et al., 2010: p. xi). Techniques for measuring welfare, and those for environmental and social enrichment for captive mammals, are emphasized in that book, and addressed here in the articles reporting on free-ranging callitrichids at the Durrell Wildlife Park and Zürich Zoo, Switzerland (Price et al., 2012), and cebids at Apenheul Primate Park, the Netherlands (Jens et al., 2012), and the article by Buchanan-Smith (2012), who discusses techniques, successes and problems in the maintenance and exhibition of mixed groups of tamarins as well as those of squirrel monkeys and tufted capuchin monkeys. This surely must be the superlative social and environmental enrichment for these species. These articles report on major leaps and bounds in zoo practices for these primates, quantum or otherwise.

The development of threatened species conservation programmes for primates, a zoo–field combination, is another of those subatomic jumps in progress. In Volume 12 of the Yearbook, Coimbra-Filho (1972) reported on the plight of the Golden lion tamarin Leontopithecus rosalia, emphasizing the role of, and need for, a captive-breeding programme. In Volume 22 of the Yearbook, Kleiman et al. (1982) reported that the previously chaotic captive population of the Golden lion tamarin, suffering constantly high morbidity and mortality, had been taken in hand. This was achieved through behavioural and physiological research, and the development of an international studbook, with an international cooperative breeding programme and its accompanying committee – a strategy for rationalizing, organizing and optimizing captive breeding that, to use an apt modern phrase, ‘became viral’. Organized, collaborative and ethically strong breeding programmes are now in place for 31 Neotropical primate taxa, managed through European Endangered Species Programmes (EEPs) and Species Survival Plans (SSPs) – 11 callitrichids, seven cebids, six pitheciids and seven atelids (11/7/6/7). Fourteen of these programmes span the Atlantic Ocean. In addition, EEPs exist for a further ten species (3/3/2/2) and SSPs for a further seven species (1/2/2/2). This sort of progress has led to, for example, the guidelines for the husbandry of callitrichids produced by the Association of Zoos and Aquariums (Sodaro & Saunders, 1999) and the European Association of Zoos and Aquaria (Bairrão Ruivo, 2010).

Kleiman et al. (1982) also reported on the ongoing efforts to develop an in situ conservation programme for the Golden lion tamarin, including research and monitoring, reintroduction (captive to wild) and environmental education. Eventually added to that was translocation (wild to wild), and it is poignant that Kierulff et al. (2012) are able to report here that efforts spanning some 30 years have resulted in an immense and ongoing success in saving the species. The Golden Lion Tamarin Conservation Programme, developed through the Smithsonian Institution's National Zoological Park, Washington, DC, USA, is considered exemplary, and long-term initiatives for the other three lion tamarins – Golden-headed lion tamarin Leontopithecus chrysomelas, Black lion tamarin Leontopithecus chrysopygus and Black-faced lion tamarin Leontopithecus caissara – emulating the original programme have also proven successful (Kleiman & Rylands, 2002; Holst et al., 2006). Three other remarkable initiatives of this nature are reported in this Volume: in situ/ex situ conservation programmes for the Cotton-top tamarin (Savage & Guillen, 2012) and the White-footed tamarin Saguinus leucopus (Bairrão Ruivo & Wormell, 2012) in the devastated forests of northern Colombia, and the Yellow-breasted capuchin Cebus xanthosternos (Lernould et al., 2012) surviving, like the Golden lion tamarin, in the desperately fragmented and destroyed remnants of the Atlantic forest in Brazil.

We are most grateful to the authors for reporting on these important trends and quantum leaps but most especially for their contributions to our understanding of New World primates. These articles on evolution and behaviour, the establishment of humane and enriched care and the well-being of Neotropical primates in captivity, and the struggle for the conservation of these taxa in the wild call attention to the huge amount of work that has been carried out already and point us in the right direction for the future.