Notes on Lagothrix flavicauda (Primates: Atelidae): oldest known specimen and the importance of the revisions of museum specimens

José Eduardo Serrano-Villavicencio Luís Fábio Silveira About the authors

ABSTRACT

The yellow-tailed woolly monkey, Lagothrix flavicauda (Humboldt, 1812), is a large atelid endemic to the cloud forests of Peru. The identity of this species was uncertain for at least 150 years, since its original description in 1812 without a voucher specimen. Additionally, the absence of expeditions to the remote Peruvian cloud forests made it impossible to collect material that would help to confirm the true identity of L. flavicauda during the 19th and first half of the 20th century. Until now, the specimens of L. flavicauda collected by H. Watkins, in 1925, in La Lejía (Amazonas, Peru) were thought to be the oldest ones deposited in any scientific collection. Nevertheless, after reviewing the databases of the several international museums and literature, we found one specimen of L. flavicauda deposited at the Muséum National d’histoire Naturelle (Paris, France) collected in 1900 by G.A. Baër, in the most eastern part of San Martín (Peru), where the presence of this species was not confirmed until 2011. Thus, Baër’s specimen represents the oldest known specimen of the yellow-tailed woolly monkey and the only one coming from the eastern part of the species’ distribution. Finally, we highlight the importance of online scientific databases for easily diagnosable species. However, caution needs to be taken when using them. We also discuss the value of scientific collections as sources of new discoveries.

KEY WORDS:
Distribution; history; taxonomy; yellow-tailed woolly monkey

Brief taxonomic history of Lagothrix flavicauda

The yellow-tailed woolly monkey, Lagothrix flavicauda (Humboldt, 1812Humboldt A (1812) Tableau synoptique des singes de l’ Amerique. In: Humboldt A, Bonpland A. Recueil d’observations de zoologie et d’anatomie comparée. Faites Dan l’océan Atlantique, dans l’interieur du nouveocontinent at dans la mer de Sud pedant les annés 1799-1803. Premier volume Deuxieme partie. Observations de zoologie et d’anatomie comparee. Paris, Schoell and Dofour & Co, 368 pp.), endemic to the Peruvian cloud forest in the Departments of Amazonas, San Martín, Loreto, and Huánuco (Leo Luna 1989Leo Luna M (1989) Biología y conservación del mono choro de cola amarilla (Lagothrix flavicauda), especie en peligro de extinción. In: Saavedra CJ, Mittermeier RA, Santos IB (Eds) La Primatologia en Latinoamérica. Washington DC, World Wildlife Fund, 23-30., Shanee 2011Shanee S (2011) Distribution survey and threat assessment of the yellow-tailed woolly monkey (Oreonax flavicauda; Humboldt 1812), Northeastern Peru. International Journal of Primatology 32: 691-707. https://doi.org/10.1007/s10764-011-9495-x
https://doi.org/10.1007/s10764-011-9495-...
), is one of the rarest and most threatened primates in the Neotropics. The yellow-tailed woolly monkey is also poorly-represented in scientific collections. For more than 150 years after the original description of the species, nothing was known beyond what was written in specimen’s labels and naturalists’ field notes.

The taxonomic history of L. flavicauda began with Humboldt (1812Humboldt A (1812) Tableau synoptique des singes de l’ Amerique. In: Humboldt A, Bonpland A. Recueil d’observations de zoologie et d’anatomie comparée. Faites Dan l’océan Atlantique, dans l’interieur du nouveocontinent at dans la mer de Sud pedant les annés 1799-1803. Premier volume Deuxieme partie. Observations de zoologie et d’anatomie comparee. Paris, Schoell and Dofour & Co, 368 pp.) who reported “Le choro de la province de Jaen” during his travel with Aimé Bonpland through South America (1799-1803). Humboldt (1812Humboldt A (1812) Tableau synoptique des singes de l’ Amerique. In: Humboldt A, Bonpland A. Recueil d’observations de zoologie et d’anatomie comparée. Faites Dan l’océan Atlantique, dans l’interieur du nouveocontinent at dans la mer de Sud pedant les annés 1799-1803. Premier volume Deuxieme partie. Observations de zoologie et d’anatomie comparee. Paris, Schoell and Dofour & Co, 368 pp.) described this species as a brownish-black monkey, with arms and thighs a tone more obscure than the back, a yellowish-brown face, a prehensile tail shorter than the body, of an olive black and laterally adorned with two yellow stripes. However, no specimen was collected on that expedition. Humboldt (1812Humboldt A (1812) Tableau synoptique des singes de l’ Amerique. In: Humboldt A, Bonpland A. Recueil d’observations de zoologie et d’anatomie comparée. Faites Dan l’océan Atlantique, dans l’interieur du nouveocontinent at dans la mer de Sud pedant les annés 1799-1803. Premier volume Deuxieme partie. Observations de zoologie et d’anatomie comparee. Paris, Schoell and Dofour & Co, 368 pp.) originally considered L. flavicauda as an unknown species of howler monkey (genus Alouatta), naming it as Simia flavicauda. This author also reported that this species was traded in the region of Jaén and Maynas in the Departments of Cajamarca and Loreto (both in Peru), respectively. Although not supported by any voucher specimen, Humboldt’s (1812Humboldt A (1812) Tableau synoptique des singes de l’ Amerique. In: Humboldt A, Bonpland A. Recueil d’observations de zoologie et d’anatomie comparée. Faites Dan l’océan Atlantique, dans l’interieur du nouveocontinent at dans la mer de Sud pedant les annés 1799-1803. Premier volume Deuxieme partie. Observations de zoologie et d’anatomie comparee. Paris, Schoell and Dofour & Co, 368 pp.) description leaves no doubt about the uniqueness of L. flavicauda but, based solely on this description, several authors reproduced the erroneous idea that L. flavicauda would represent a howler monkey species. Thus, L. flavicauda was listed as a member of Mycetes (Kuhl 1820Kuhl H (1820) Beiträge zur Zoologie und vergleichenden Anatomie. Frankfurt am Main, Hermannschen Buchhandlung, 212 pp., Wagner 1840Wagner JA (1840) Schreber’s Die Säugthiere. Suppl. Vol. l. Expedition des Schreber’schen Säugthier- und des Esper’schen Schmetterlingswerkes, etc. Erlangen, xiv+551 pp., Lesson 1840Lesson RP (1840) Species des mammifères: Bimanes et quadrumanes. París, J.B. Balliere, xiv+292 pp., von Tschudi 1844Von Tschudi JJ (1844) Untersuchungen über die Fauna Peruana. Part 1 (Therologie). Scheitlin and Zollikofer, St. Gallen, xxx+262 pp., I. Geoffroy Saint-Hilaire 1851Geoffroy Saint-Hilaire I (1851) Catalogue méthodique de la collection des mammifères, de la collection des oíseaux et des collections annexes, Part. 1 (Catalogue des Primates). París, Gide et Baudry, Libraires-Éditeurs, xv+96 pp., Schlegel 1876Schlegel H (1876) Les singes: Simiae. Leiden, Muséum d’Histoire Naturelle du Pays-Bas, vol. 7, monograph 40, 356 pp.), Stentor (É. Geoffroy Saint-Hilaire 1812Geoffroy Saint-Hilaire É (1812) Tableau des quadrumanes ou des animaux composant le premier ordre de la class des mammifères. Annales du Muséum d’histoire naturelle 19: 85-122., Cuvier 1837Cuvier G (1837) The animal kingdom, arranged according to its organization, serving as a foundation for the natural history of animals: and an introduction to comparative anatomy. Volume I. G. Henderson, 1834-37. London, 408 pp.), and Alouatta (Forbes 1896Forbes HO (1896) A hand-book to the primates. London, Edward Lloyd, vol. 1, xiv+286 pp., Elliot 1913Elliot DG (1913) [dated 1912]. A Review of the Primates. New York, American Museum of Natural History, vol. 1, 596 pp., Tate 1939Tate GHH (1939) The mammals of the Guiana region. Bulletin of the American Museum of Natural History 76: 151-229.), being the two former genera junior synonyms of the latter.

The misunderstanding about the real identity of Humboldt’s Simia flavicauda increased with the description of Lagothrix (Oreonax) hendeii (Thomas 1927aThomas O (1927a) A remarkable new monkey from Peru. The Annals and Magazine of Natural History 9(19): 156-157.). This same author claimed that the morphological differences of the monotypic subgenus Oreonax deserved a generic distinction from Lagothrix, containing O. hendeii (Thomas 1927bThomas O (1927b) The Godman-Thomas Expedition to Peru - V. On mammals collected by Mr. R. W. Hendee in the Province of San Martín, N. Peru, mostly at Yurac Yacu. The Annals and Magazine of Natural History 9(19): 361-375.,cThomas O (1927c) The Godman-Thomas Expedition to Peru - VI. On mammals from the upper Huallaga and neighbouring highlands. The Annals and Magazine of Natural History 9(20): 594-608.). Thomas (1927aThomas O (1927a) A remarkable new monkey from Peru. The Annals and Magazine of Natural History 9(19): 156-157.,bThomas O (1927b) The Godman-Thomas Expedition to Peru - V. On mammals collected by Mr. R. W. Hendee in the Province of San Martín, N. Peru, mostly at Yurac Yacu. The Annals and Magazine of Natural History 9(19): 361-375.,cThomas O (1927c) The Godman-Thomas Expedition to Peru - VI. On mammals from the upper Huallaga and neighbouring highlands. The Annals and Magazine of Natural History 9(20): 594-608.) based his description on material collected by R.W. Hendee in Puca Tambo (San Martín, Peru) in January 1926. In Thomas’ vision, his Oreonax hendeii clearly represented a different species of Humboldt’s Simia flavicauda. Thomas (1927bThomas O (1927b) The Godman-Thomas Expedition to Peru - V. On mammals collected by Mr. R. W. Hendee in the Province of San Martín, N. Peru, mostly at Yurac Yacu. The Annals and Magazine of Natural History 9(19): 361-375.) concluded that Humboldt’s S. flavicauda was probably nothing more than “a local Lagothrix, perhaps L. lagothricha”. This taxonomic confusion led Tate (1939Tate GHH (1939) The mammals of the Guiana region. Bulletin of the American Museum of Natural History 76: 151-229.: 214, 217) to consider Humboldt’s Simia flavicauda a composite taxon containing two different species, [Lagothrix] hendeii and [Alouatta] flavicauda. On the other hand, Cabrera (1958Cabrera A (1958) Catálogo de los mamíferos da América del Sur. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Ciencia Zoologica, Buenos Aires 4: 1-307.: 153, 183) stated that Humboldt’s Simia flavicauda could be a valid but undeterminable species of Alouatta and recognized Thomas’ Lagothrix hendeii as a valid species. Hill (1962Hill W (1962) Primates. Comparative Anatomy and Taxonomy. IV. Cebidae Part A. Edinburgh, Edinburgh University Press, 537 pp.: 250) also considered L. hendeii as a valid species making no mention to Humboldt’s Simia flavicauda. Nevertheless, these two latter authors considered that the characters presented by Thomas (1927bThomas O (1927b) The Godman-Thomas Expedition to Peru - V. On mammals collected by Mr. R. W. Hendee in the Province of San Martín, N. Peru, mostly at Yurac Yacu. The Annals and Magazine of Natural History 9(19): 361-375.,cThomas O (1927c) The Godman-Thomas Expedition to Peru - VI. On mammals from the upper Huallaga and neighbouring highlands. The Annals and Magazine of Natural History 9(20): 594-608.) to sustain Oreonax as full genus had no more than specific value and retained hendeii within Lagothrix. Fooden (1963Fooden J (1963) A revision of the Woolly Monkeys (Genus Lagothrix). Journal of Mammalogy 44: 213-247. https://doi.org/10.2307/1377454
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) performed the first comprehensive taxonomic revision of the genus Lagothrix, finally resolving the identity of Humboldt’s Simia flavicauda. After reviewing the available literature and comparing museum specimens, Fooden (1963Fooden J (1963) A revision of the Woolly Monkeys (Genus Lagothrix). Journal of Mammalogy 44: 213-247. https://doi.org/10.2307/1377454
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) found that Humboldt’s Simia flavicauda and Thomas’ Oreonax hendeii represented the same species of woolly monkey.

Fooden’s (1963Fooden J (1963) A revision of the Woolly Monkeys (Genus Lagothrix). Journal of Mammalogy 44: 213-247. https://doi.org/10.2307/1377454
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) taxonomic arrangement was largely accepted (Napier 1976Napier PH (1976) Catalogue of Primates in the British Museum (Natural History). Part I: Families Callitrichidae and Cebidae. London, British Museum (Natural History), 121 pp., Eisenberg and Redford 1999Eisenberg JF, Redford KH (1999) Mammals of the Neotropics. Chicago, The University of Chicago Press, vol. 3, 609 pp., Nowak 1999Nowak R (1999) Walker’s Mammals of the World, Baltimore, The Johns Hopkins University Press, vol. 1, 642 pp.), until Groves (2001Groves CP (2001) Primate Taxonomy. Washington DC, Smithsonian Institution Press, 350 pp.) tested the phylogeny of the atelids. This latter author, based on a 50% majority rule consensus tree estimated via a parsimony analysis of only 20 cranial characters and an undetermined number of species, found out that Lagothrix flavicauda was more closely related to species of Ateles than to L. lagothricha. These low-supported results (bootstrap support <70%) led Groves to resurrect Thomas’ Oreonax for flavicauda. Groves’ (2001Groves CP (2001) Primate Taxonomy. Washington DC, Smithsonian Institution Press, 350 pp.) proposal was rapidly accepted (Groves 2005Groves CP (2005) Order Primates. In: Wilson DE, Reeder DM (Eds) Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore, John Hopkins University Press, 3rd ed., 111-184., DeLuycker and Heymann 2007DeLuycker AM, Heymann EW (2007) Peruvian yellow-tailed woolly monkey Oreonax flavicauda (Humboldt, 1812). In: Primates in peril: the world’s 25 most endangered primates, 2006-2008, R. A. Mittermeier et al. (eds.), pp.20-21, 32. Primate Conservation (22): 1-40., Rylands and Mittermeier 2009Rylands AB, Mittermeier RA (2009) The Diversity of the New World Primates (Platyrrhini). In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (Eds) South American Primates: Comparative Perspectives in the Study of Bahavior, Ecology, and Conservation. New York, Springer, 23-54. https://doi.org/10.1007/978-0-387-78705-3_2
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); nevertheless, the use of Oreonax as a formal genus for flavicauda was also criticized. Matthews and Rosenberger (2008Matthews LJ, Rosenberger AL (2008) Taxon combinations, parsimony analysis (PAUP*), and the taxonomy of the Yellow-Tailed Woolly Monkey, Lagothrix flavicauda. American Journal of Physical Anthropology 137(3): 245-55. https://doi.org/10.1002/ajpa.20859
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) and Rosenberger and Matthews (2008Rosenberger A, Matthews L (2008) Oreonax- not a genus. Neotropical Primates 15(1): 8-12. https://doi.org/10.1896/044.015.0102
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) replicated and extended Groves’ (2001Groves CP (2001) Primate Taxonomy. Washington DC, Smithsonian Institution Press, 350 pp.) study and showed that his results were probably a sampling artifact, which undermined the logic of reviving Oreonax as a formal genus for flavicauda. However, as noted by Pacheco et al. (2009Pacheco V, Cadenillas R, Salas E, Tello C, Zeballos H (2009) Diversidad y endemismo de los mamíferos del Perú. Revista Peruana de Biología 16(1): 5-32. https://doi.org/10.15381/rpb.v16i1.111
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), these authors did not provide a phylogeny that placed flavicauda within Lagothrix. More recently, molecular evidence has also refuted Groves’ (2001Groves CP (2001) Primate Taxonomy. Washington DC, Smithsonian Institution Press, 350 pp.) results. Ruiz-Garcia et al. (2014Ruiz-García M, Pinedo-Castro M, Shostell JM (2014) How many genera and species of woolly monkeys (Atelidae, Platyrrhine, Primates) are there? The first molecular analysis of Lagothrix flavicauda, an endemic Peruvian primate species. Molecular Phylogenetics and Evolution 79: 179-198. https://doi.org/10.1016/j.ympev.2014.05.034
https://doi.org/10.1016/j.ympev.2014.05....
) and Di Fiore et al. (2015Di Fiore A, Chaves PB, Cornejo FM, Schmitt CA, Shanee S, Corté-Ortiz L, Fagundes V, Roos C, Pacheco V (2015) The rise and fall of a genus: Complete mtDNA genomes shed light on the phylogenetic position of yellow-tailed woolly monkeys, Lagothrix flavicauda, and on the evolutionary history of the family Atelidae (Primates: Platyrrhini). Molecular Phylogenetics and Evolution 82: 495-510. https://doi.org/10.1016/j.ympev.2014.03.028
https://doi.org/10.1016/j.ympev.2014.03....
) presented the first molecular phylogenetic analyses of Lagothrix flavicauda. The results of both studies were similar, supporting a monophyletic Lagothrix that included flavicauda and the other woolly monkey species, agreeing with Fooden’s (1963Fooden J (1963) A revision of the Woolly Monkeys (Genus Lagothrix). Journal of Mammalogy 44: 213-247. https://doi.org/10.2307/1377454
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) taxonomic arrangement.

The oldest known specimen of Lagothrix flavicauda

As a part of an ongoing study, we were looking for specimens of Lagothrix flavicauda deposited in scientific collections or cited in the literature. We found 17 skins and 8 skulls deposited in the following collections: Museo de Historia Natural, Lima, Peru (11 skins, 3 skulls); American Museum of Natural History, New York, USA (AMNH; 2 skins, 2 skulls); Natural History Museum, London, UK (NHM; 3 skins, 3 skulls); and The Museum of Vertebrate Zoology, Berkeley, USA (MVZ; 1 skin). All these specimens have been referenced in the literature somehow. Additionally, Kuhl (1820Kuhl H (1820) Beiträge zur Zoologie und vergleichenden Anatomie. Frankfurt am Main, Hermannschen Buchhandlung, 212 pp.: 30) stated that one specimen of Mycetes flavicaudatus (a synonym of Lagothrix flavicauda) was held at the Muséum National d’histoire Naturelle (MNHN, Paris - France). Nonetheless, Elliot (1913Elliot DG (1913) [dated 1912]. A Review of the Primates. New York, American Museum of Natural History, vol. 1, 596 pp.: 277) said that this must have been a mistake since he could not find that specimen in the collection and É. Geoffroy Saint-Hilaire (1812Geoffroy Saint-Hilaire É (1812) Tableau des quadrumanes ou des animaux composant le premier ordre de la class des mammifères. Annales du Muséum d’histoire naturelle 19: 85-122.) never mentioned it either. Nevertheless, we found one skin at the MNHN, collected in 1900 by G.A. Baër, which until now had not been mentioned in the literature.

Between 1900 and 1901, G.A. Baër traveled throughout South America collecting several animals, most of which were birds. He also collected a considerable number of mammals, including rodents, marsupials, and primates. While in Peru, he traveled to some inhospitable areas between June and December of 1900. One of the specimens collected by Baër was an adult individual of Lagothrix flavicauda (Figs 1-4). This specimen was collected at the Hacienda Nuevo Loreto in the Department of San Martín in September 1900 (Simon 1902Simon E (1902) Étude sur les Trochilidés observés an Perou par G. A. Baer (1900-1901). Novitates Zoologicae. Band 9, S. 177-183., Stephens and Traylor Jr 1983Stephens L, Traylor Jr MA (1983) Ornithological gazetteer of Peru. Cambridge, Museum of Comparative Zoology, Harvard University, 271 pp.). Simon (1902Simon E (1902) Étude sur les Trochilidés observés an Perou par G. A. Baer (1900-1901). Novitates Zoologicae. Band 9, S. 177-183.) described this locality as a warm forest region of the Río Mixiollo (= Río Mishollo) valley, three days East of Tayabamba, and at an altitude of 1200 m.a.s.l. (Fig. 5). All of Baër’s material was shipped to Paris and housed in the collection of the MNHN. At the MNHN, this specimen was identified as a Cebus sp. under the catalog number MNHN-ZM-MO-1901-1602. The skin deposited at this museum represents, chronologically, the oldest known specimen of L. flavicauda deposited in a scientific institution.

Figures 1-4
Lagothrix flavicauda (MNHN-ZM-MO-1901-1602) collected by G.A. Baër in September 1900 in the Hacienda Nuevo Loreto (San Martín - Peru): (1) complete skin; (2) close-up of the tail showing the diagnostic yellow-golden hairs surrounding the tail’s digital patch; (3) close-up of the face showing the white circumbuccal patch; (4) original Baër’s label of the specimen. Photographs provided by Jacques Cuisin (MNHN).

Figure 5
Map showing the historical confirmed records of the Lagothrix flavicauda specimens deposited in scientific collections. MUSM (circle). AMNH (square), NHM (triangle), and MNHN (star). For locality data, see Table 1.

Table 1
Summary of the historical records of Lagothrix flavicauda, arranged in latitudinal order.

After 50 years without any records, Mittermeier et al. (1977Mittermeier RA, de Macedo-Ruiz H, Luscombe BA, Cassidy J (1977) Rediscovery and conservation of the Peruvian yellow-tailed woolly monkey (Lagothrix flavicauda). In: Prince Rainier III, Bourne GH (Eds) Primate Conservation . New York, Academic Press, 95-116.) registered L. flavicauda in Pedro Ruiz Gallo (Amazonas, Peru) and, without knowing Baër’s record, they stated that the first specimens collected of L. flavicauda were those held at the AMNH. These two specimens were provided by H. Watkins, who collected them at La Lejía (Amazonas, Peru) in April 1925. In 1926, R.W. Hendee, a collector for the Godman-Thomas Expedition to Peru, collected three more specimens, those used by Thomas (1927aThomas O (1927a) A remarkable new monkey from Peru. The Annals and Magazine of Natural History 9(19): 156-157., bThomas O (1927b) The Godman-Thomas Expedition to Peru - V. On mammals collected by Mr. R. W. Hendee in the Province of San Martín, N. Peru, mostly at Yurac Yacu. The Annals and Magazine of Natural History 9(19): 361-375., cThomas O (1927c) The Godman-Thomas Expedition to Peru - VI. On mammals from the upper Huallaga and neighbouring highlands. The Annals and Magazine of Natural History 9(20): 594-608.). Based on the available data at that time, Mittermeier et al. (1977Mittermeier RA, de Macedo-Ruiz H, Luscombe BA, Cassidy J (1977) Rediscovery and conservation of the Peruvian yellow-tailed woolly monkey (Lagothrix flavicauda). In: Prince Rainier III, Bourne GH (Eds) Primate Conservation . New York, Academic Press, 95-116.) proposed that the distribution range of L. flavicauda would encompass the southern part of Amazonas and the mountainous western part of San Martin.

The northern limit of the distribution of L. flavicauda was confirmed in several studies after its Mittermeier et al.’s (1977Mittermeier RA, de Macedo-Ruiz H, Luscombe BA, Cassidy J (1977) Rediscovery and conservation of the Peruvian yellow-tailed woolly monkey (Lagothrix flavicauda). In: Prince Rainier III, Bourne GH (Eds) Primate Conservation . New York, Academic Press, 95-116.) record (Leo Luna 1980Leo Luna M (1980) First field study of the yellow-tailed woolly monkey. Oryx 15: 386-389., Butchart et al. 1995Butchart SM, Barnes R, Davies CWN, Fernandez M, Seddon N (1995) Observations of two threatened primates in the Peruvian Andes. Primate Conservation 16: 15-19.). Nonetheless, its Southern limit remained uncertain for several decades. N. Shanee et al. (2007Shanee N, Shanee S, Maldonado AM (2007) Conservation assessment and planning for the yellow tailed woolly monkey (Oreonax flavicauda) in Peru. Wildlife Biology in Practice 3: 73-82.), based on information given by local guides, informed that this species inhabits the eastern portion of San Martín (40 km west of Tocache, approximately). A few years later, S. Shanee (2011) confirmed the presence of L. flavicauda in eastern San Martín. Recently, Aquino et al. (2016Aquino R, Charpentier E, García G, López L (2016) First Record of Lagothrix flavicauda on the eastern side of the Río Huallaga: An expansion of its known geographic distribution. Primate Conservation 30: 15-20.) recorded five groups of L. flavicauda on the eastern side of the Huallaga River, between Oso Mayo and Palizada (Huánuco, Peru) expanding its southern limits. Although Baër’s specimen remained unnoticed, its importance is remarkable. It is not only the first record of Lagothrix flavicauda in eastern San Martín, more than 100 years before S. Shanee’s (2011Shanee S (2011) Distribution survey and threat assessment of the yellow-tailed woolly monkey (Oreonax flavicauda; Humboldt 1812), Northeastern Peru. International Journal of Primatology 32: 691-707. https://doi.org/10.1007/s10764-011-9495-x
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) survey, but also, as far as we know, it is the only specimen coming from that region in any scientific collection. Furthermore, if this specimen had been discovered before, the area where it was collected could have been taken into account in the early conservation programs developed for L. flavicauda. For example, this area could have been considered to be protected in the buffer zone of the Río Abiseo National Park created in 1990.

The importance of reviewing museum specimens

The specimen of Lagothrix flavicauda collected by Baër represents a good example of the importance of thoroughly revising specimens in scientific collections. There are notable examples of new species that were described based on museum material long after the type specimens were collected: Pithecia vanzoliniiHershkovitz, 1987Hershkovitz P (1987) The taxonomy of South American sakis, genus Pithecia (Cebidae, Platyrrhini): a preliminary report and critical review with the description of a new species and a new subspecies. American Journal Primatology 12(4): 387-468., Callicebus vieiraiGualda-Barros, Nascimento & Amaral, 2012Gualda-Barros J, Nascimento FO, Amaral MK (2012) A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia 52(23): 261-279. https://doi.org/10.1590/S0031-10492012002300001
https://doi.org/10.1590/S0031-1049201200...
and Mico marcai (Alperin, 1993Alperin R (1993) Callithrix argentata (Linnaeus, 1771): considerações taxonômicas e descrição de subespécie nova. Boletim do Museu Paraense Emilio Goeldi Série Zoologia 9(2): 317-328.).

Vanzolini’s bald-faced saki, P. vanzolinii, was described based on a large set of samples that remained unnoticed in at least three different Brazilian collections: the Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP); the Museu Nacional Universidade Federal do Rio de Janeiro, Rio de Janeiro (MNRJ); and the Museu Paraense Emílio Goeldi, Belém (MPEG). The majority of samples of P. vanzolinii were collected in 1936 by A.M. Olalla and other two samples were collected in 1956 by F. Novaes and M.M. Moreira, held at the MPEG (Nunes and Serrano-Villavicencio, 2017Nunes A, Serrano-Villavicencio J (2017) Rediscovery of Vanzolini’s Bald-Faced Saki, Pithecia vanzolinii Hershkovitz, 1987 (Primates, Pitheciidae): first record since 1956. Check List 13(1): 2048. https://doi.org/10.15560/13.1.2048
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). De Vivo (1985De Vivo M (1985) On some monkeys from Rondônia, Brazil (Primates: Callitrichidae, Cebidae). Papéis Avulsos de Zoologia 36(11): 103-110.) was the first to notice that the material of Pithecia collected by Olalla and held at the MZUSP possessed a particular phenotype; nevertheless, he did not recognize this material as a different taxon. It was not until Hershkovitz (1987Hershkovitz P (1987) The taxonomy of South American sakis, genus Pithecia (Cebidae, Platyrrhini): a preliminary report and critical review with the description of a new species and a new subspecies. American Journal Primatology 12(4): 387-468.) that this species was formally described, originally as a subspecies of P. irrorata.

Another example is Gualda-Barros et al.’s (2012Gualda-Barros J, Nascimento FO, Amaral MK (2012) A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia 52(23): 261-279. https://doi.org/10.1590/S0031-10492012002300001
https://doi.org/10.1590/S0031-1049201200...
) C. vieirai. The holotype and the paratypes of Vieira’s titi were collected in 1997 by Marília Kerr and in 1988 by J.L. Silva-Filho, respectively. All these specimens were kept in the collection of the MZUSP. Gualda-Barros et al. (2012Gualda-Barros J, Nascimento FO, Amaral MK (2012) A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia 52(23): 261-279. https://doi.org/10.1590/S0031-10492012002300001
https://doi.org/10.1590/S0031-1049201200...
), after revising the collection of Callicebus of the MZUSP, noticed that the phenotype of those specimens, deposited there for at least 15 years, was different, and described it as a new species.

As a final example, Marca’s Marmoset, M. marcai, was described using material collected by the Comissão Rondon in 1914 and held at the MNRJ. This material remained unnoticed in various revisions of callithricids (Hershkovitz 1975Hershkovitz P (1975) Comments on the taxonomy of Brazilian marmosets (Callithrix, Callitrichidae). Folia Primatologica 24: 137-172., 1977Hershkovitz P (1977) Living New World Monkeys (Platyrrhini): With an Introduction to Primates. Chicago, The University of Chicago Press , vol.1, 1132 pp., Ávila-Pires 1969Ávila-Pires FD (1969) Taxonomia e zoogeografia do gênero Callithrix (Erxleben, 1777) (Primates: Callitrichidae). Revista Brasileira de Biologia 29: 49-64., de Vivo 1991De Vivo M (1991) Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Fundação Biodiversitas para Conservação da Diversidade Biológica, Belo Horizonte, Brazil, 105 pp.); Alperin (1993Alperin R (1993) Callithrix argentata (Linnaeus, 1771): considerações taxonômicas e descrição de subespécie nova. Boletim do Museu Paraense Emilio Goeldi Série Zoologia 9(2): 317-328.) noticed that these specimens represented a different taxon describing it as Callithrix argentata marcai. Van Roosmalen et al. (2000Van Roosmalen M, van Roosmalen T, Mittermeier RA, Rylands AB (2000) Two new species of marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates) from the Tapajós/Madeira interfluvium, south central Amazonia, Brazil. Neotropical Primates 8: 2-18.) described the marmoset Mico manicorensis (Roosmalen, Roosmalen, Mittermeier & Rylands, 2000); nevertheless, the authors did not analyze the type material of M. marcai and this later species was found to be a synonym of the former (Garbino 2014Garbino GST (2014) The Taxonomic Status of Mico marcai (Alperin 1993) and Mico manicorensis (van Roosmalen et al. 2000) (Cebidae, Callitrichinae) from Southwestern Brazilian Amazonia. International Journal of Primatology 35(2): 529-546. https://doi.org/10.1007/s10764-014-9766-4
https://doi.org/10.1007/s10764-014-9766-...
).

This kind of ‘museum discovery’ it is not unusual, but the lack of thorough reviews of scientific collections, especially the old ones, is alarming and may also have important consequences for conservation, as in the case of critically endangered species. The revision of scientific material brings not only new data and even new species in the middle of the present biodiversity crisis, but also has a tremendous potential to discover new or historical localities which must be viewed as opportunities to evaluate the real conservation status of a species over time (Graham et al. 2004Graham CH, Ferrier S, Huettman F, Moritz C, Peterson AT (2004) New developments in museum-based informatics and applications in biodiversity analysis. Trends in Ecology & Evolution 19: 497-503. https://doi.org/10.1016/j.tree.2004.07.006
https://doi.org/10.1016/j.tree.2004.07.0...
). These historical distributional records provide unique opportunities to trace distributional changes in relation to threatening processes and thereby anticipate future impacts (Drost and Fellers 1996Drost CA, Fellers GM (1996) Collapse of a regional frog fauna in Yosemite area of the California Sierra Nevada USA. Conservation Biology 10: 414-425., Shaffer et al. 1998Shaffer HB, Fisher R, Davidson C (1998) The role of natural history collections in documenting species declines. Trends in Ecology & Evolution 13: 27-30. https://doi.org/10.1016/S0169-5347(97)01177-4
https://doi.org/10.1016/S0169-5347(97)01...
, Ponder et al. 2001Ponder WF, Carter GA, Flemons P, Chapman RR (2001) Evaluation of museum collection data for the use in biodiversity assessment. Conservation Biology 15: 648-657. https://doi.org/10.1046/j.1523-1739.2001.015003648.x
https://doi.org/10.1046/j.1523-1739.2001...
, Graham et al. 2004Graham CH, Ferrier S, Huettman F, Moritz C, Peterson AT (2004) New developments in museum-based informatics and applications in biodiversity analysis. Trends in Ecology & Evolution 19: 497-503. https://doi.org/10.1016/j.tree.2004.07.006
https://doi.org/10.1016/j.tree.2004.07.0...
).

Scientific collections have proved to be a source of new discoveries (Funk 2018Funk VA (2018) Collections‐based science in the 21st Century. Journal of Systematics and Evolution 56: 175-193. https://doi.org/10.1111/jse.12315
https://doi.org/10.1111/jse.12315...
); in this context, the efforts of all the museums worldwide to make their collections available in digi tal media should be highlighted and celebrated. However, we recommend that specialists, whenever possible, review these collections carefully to avoid identification mistakes and the posterior uncontrolled misuse of the museum’s data. Finally, a proper maintenance of these collections must be guaranteed for future generations of scientists to have access to the valuable material and unfinished source of information that is deposited in them.

ACKNOWLEDGEMENTS

We would like to thank especially Jacques Cuisin from the MNHN, Paris, for kindly providing the information and images needed for this work; Cindy Hurtado for editing the images and for the comments; Victor Pacheco for the access to the database of the Museo de Historia Natural (Lima); João Pedro Souza-Alves and Guilherme Garbino for the valuable comments of the manus cript. Fabio O. do Nascimento and the another anonymous reviewer for the valuable comments on the manuscript. Finally, we thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Finance Code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 302291/2015-6) for the grants to JESV and LFS, respectively.

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Publication Notes

  • Available online:

    July 5, 2019
  • Zoobank Register:

    http://zoobank.org/B29AF1E9-F78A-475D-AF1F-3AECEBABA626
  • Publisher:

    © 2019 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Publication Dates

  • Publication in this collection
    22 July 2019
  • Date of issue
    2019

History

  • Received
    24 Sept 2018
  • Accepted
    11 Dec 2018
  • Published
    05 July 2019
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