Specimen collection: An essential tool

INSIGHTS Edited by Jennifer Sills Specimen collection: An essential tool COLLECTING BIOLOGICAL specimens for biodiversity is hidden deep in its habitat (see image)]. Moreover, identification is often not the most important reason to collect voucher specimens. Studies of morphological diversity and its evolution are impossible without whole specimens. Preserved specimens also provide verifiable data points for monitoring species health, distribution, and phenotypes through time. Both historical and new collections played a key role in understanding the spread of the chytrid fungus infection, one of the greatest current threats to amphibians (5). The decision to ban dichlorodiphenyltrichloroethane (DDT) distract from the primary causes of modern extinction: habitat degradation and loss, unsustainable harvesting, and invasive species (10). It is important to distinguish protecting the lives of individuals from conserving populations and species. Individuals are lost every day to predation, natural death, and anthropogenic factors, hence it is the populations we try to save. Halting collection of voucher specimens by scientists would be detrimental not only to our understanding of Earth’s diverse biota and its biological processes, but also for conservation and management efforts. Species descriptions, biodiversity scientific studies came under scrutiny when B. A. Minteer et al. [“Avoiding (re)extinction,” Perspectives, 18 April, p. 260] suggested that this practice plays a significant role in species extinctions. Based on a small number of examples (rare birds, frogs, and a few plants), the authors concluded that collection of voucher specimens is potentially harmful to many species, and that alternatives— photographs, audio recordings and nonlethal tissue sampling for DNA analysis—are sufficient to document biological diversity. The isolated examples that Minteer et al. cited to demonstrate the negative impact of scientific collecting have been carefully analyzed, and none of these extinction events can be attributed to that cause (1–3). For example, only about 102 Great Auk specimens Undercover. Many Alpheidae shrimps live deep in the reef and are impossible to collect nonlethally. (Pinguinus impennis) exist today in scientific collections, many of which are skeletons obtained after extincand other environmental pollutants was inventories, and the identification of areas tion, whereas millions were harvested the result of the discovery of thinning of of endemism are just some of the basic for food, oil, and feathers over millennia bird eggshells collected over an extended information that can be obtained from (1). Similarly, only nine Mexican elf owls period (6). One of the negative effects of specimens and collections-based research. (Micrathene whitneyi graysoni), endemic climate change, declining body size in Such knowledge, with its rich temporal and to Socorro Island, Mexico, are present in animals, was only discovered with morspatial dimensions, has proven fundamennatural history collections. Field notes phological data from museum specimens tal in designing conservation areas and indicate that this species was common (7). Furthermore, IUCN Red List criteria in making environmental impact assesswhen specimens were collected between require specific and detailed informaments (11). These issues are particularly 1896 and 1932, and the most likely reasons tion about life history and biology (such relevant in many developing nations, which for extinction around 1970 were habitat as longevity and growth rate), especially ideally must seek a balance between the degradation and predation by invasive for widely distributed species; therefore, conservation of their natural (biological) species (2). without specimens, the extinction risk of resources and development. One example Scientists have come a long way from many species cannot be properly assessed comes from the Bird’s Head Peninsula of the days of indiscriminate collecting. (8). Most specimens were not collected New Guinea, Indonesia, where the disModern collecting adheres to strict permitwith these objectives in mind, and this is covery and description of small endemic ting regulations and ethics guidelines, a hallmark of biological collections: They species—undetectable without specimen including the general practice of collecting are often used in ways that the origicollection—directly resulted in the crea number of specimens substantially below nal collector never imagined. With new ation of several new protected areas and levels that would affect population demogtechnologies continuing to emerge (such increased support for marine parks (12). raphy (3, 4). The suggested alternatives as stable isotope analyses, massive parallel With our ever-increasing footprint, to collecting specimens (photographsequencing, and CT-scan tomography), scihumans now affect even the most remote ing, recording calls, or sampling tissue entific collections are becoming even more corners of Earth. Because an estimated nonlethally) are individually problematic, important for studies of ecology, evolution, 86% of species on the planet remain and even together cannot be used to reliand conservation (9). unknown (13), our goal should be to docuably identify or describe the vast majority The arguments of Minteer et al. erronement biodiversity as rigorously as possible of Earth’s biodiversity [for example, a ously portray the critical importance of through carefully planned collections large proportion of the world’s marine scientific collecting in a negative light and so that it can be effectively preserved 814 sciencemag.org SCIENCE 23 MAY 2014 • VOL 344 ISSUE 6186 Published by AAAS PHOTO: ARTHUR ANKER L E T TERS and understood. Specimens from such collections and their associated data are essential for making informed decisions about management and conservation now and in the future. As a community, we advocate the utmost responsibility and care while making scientific collections (4). Furthermore, given increasing rates of habitat loss and global change, we believe that responsibly collecting voucher specimens and associated data and openly sharing this knowledge (for example, through GBIF, iDigBio, and VertNet) are more necessary today than ever before. L. A. Rocha,1* A. Aleixo,2 G. Allen,3 F. Almeda,1 C. C. Baldwin,4 M. V. L. Barclay,5 J. M. Bates,6 A. M. Bauer,7 F. Benzoni,8 C. M. Berns,9 M. L. Berumen,10 D. C. Blackburn,1 S. Blum,1 F. Bolaños,11 R. C. K. Bowie,12 R. Britz,5 R. M. Brown,13 C. D. Cadena,14 K. Carpenter,15 L. M. Ceríaco,16 P. Chakrabarty,17 G. Chaves,11 J. H. Choat,18 K. D. Clements,19 B. B. Collette,20 A. Collins,20 J. Coyne,21 J. Cracraft,22 T. Daniel,1 M. R. de Carvalho,23 K. de Queiroz,4 F. Di Dario,24 R. Drewes,1 J. P. Dumbacher,1 A. Engilis Jr.,25 M. V. Erdmann,26 W. Eschmeyer,1 C. R. Feldman,27 B. L. Fisher,1 J. Fjeldså,28 P. W. Fritsch,1 J. Fuchs,29 A. Getahun,30 A. Gill,31 M. Gomon,32 T. Gosliner,1 G. R. Graves,4 C. E. Griswold,1 R. Guralnick,33 K. Hartel,34 K. M. Helgen,4 H. Ho,35 D. T. Iskandar,36 T. Iwamoto,1 Z. Jaafar,4,37 H. F. James,4 D. Johnson,4 D. Kavanaugh,1 N. Knowlton,4 E. Lacey,12 H. K. Larson,38 P. Last,39 J. M. Leis,40 H. Lessios,41 J. Liebherr,42 M. Lowman,1 D. L. Mahler,25 V. Mamonekene,43 K. Matsuura,44 G. C. Mayer,45 H. Mays Jr.,46 J. McCosker,1 R. W. McDiarmid,4 J. McGuire,12 M. J. Miller,41 R. Mooi,1 R. D. Mooi,47 C. Moritz,48 P. Myers,49 M. W. Nachman,12 R. A. Nussbaum,49 D. Ó Foighil,49 L. R. Parenti,4 J. F. Parham,50 E. Paul,51 G. Paulay,52 J. Pérez-Emán,53 A. Pérez-Matus,54 S. Poe,55 J. Pogonoski,39 D. L. Rabosky,49 J. E. Randall,56 J. D. Reimer,57 D. R. Robertson,41 M.-O. Rödel,58 M. T. Rodrigues,23 P. Roopnarine,1 L. Rüber,59 M. J. Ryan,55 F. Sheldon,17 G. Shinohara,44 A. Short,13 W. B. Simison,1 W. F. Smith-Vaniz,52 V. G. Springer,4 M. Stiassny,22 J. G. Tello,22,60 C. W. Thompson,49 T. Trnski,61 P. Tucker,49 T. Valqui,62 M. Vecchione,20 E. Verheyen,63 P. C. Wainwright,25 T. A. Wheeler,64 W. T. White,39 K. Will,12 J. T. Williams,4 G. Williams,1 E. O. Wilson,34 K. Winker,65 R. Winterbottom,66 C. C. Witt55 Museum, London, SW7 5BD, UK. 6Field Museum of Natural History, Chicago, IL 60605, USA. 7Villanova University, Villanova, PA 19085, USA. 8University of Milano-Bicocca, Milan, 20126, Italy. 9Utica College, Utica, NY 13502, USA. 10King Abdullah University of Science and Technology, Thuwal, 23955, Saudi Arabia. 11Universidad de Costa Rica, San José, 11501-2060, Costa Rica. 12University of California, Berkeley, CA 94720–3161, USA. 13University of Kansas, Lawrence, KS 66045, USA. 14Universidad de los Andes, Bogotá, 4976, Colombia. 15Old Dominion University, Norfolk, VA 23529, USA. 16Museu Nacional de História Natural e da Ciência, Lisbon, 7005638, Portugal. 17Louisiana State University, Baton Rouge, LA 70803, USA. 18James Cook University, Townsville, 4811, Australia. 19University of Auckland, Auckland, 1142, New Zealand. 20NOAA Systematics Laboratory, Washington, DC 20013, USA. 21University of Chicago, Chicago, IL 60637, USA. 22American Museum of Natural History, New York, NY 10024, USA. 23Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil. 24Universidade Federal do Rio de Janeiro, Macaé, RJ, 27965-045, Brazil. 25University of California, Davis, CA 95616, USA. 26Conservation International, Denpasar, Bali, 80235, Indonesia. 27 University of Nevada, Reno, NV 89557–0314, USA. 28 Natural History Museum of Denmark, Copenhagen, DK-2100, Denmark. 29Muséum National d’Histoire Naturelle, Paris, 75005, France. 30Addis Ababa University, Addis Ababa, 1176, Ethiopia. 31University of Sydney, Sydney, NSW, 2006, Australia. 32Museum Victoria, Melbourne, 3001, VIC, Australia. 33University of Colorado, Boulder, CO 80309–0334, USA. 34 Harvard University, Cambridge, MA 02138, USA. 35 National Museum of Marine Biology & Aquarium, Pingtung, 944, Taiwan. 36Institut Teknologi Bandung, Bandung, 40132, Indonesia. 37National University of Singapore, 117543, Singapore. 38Museum and Art Gallery of the Northern Territory, Darwin, 0820, NT, Australia. 39CSIRO Marine & Atmospheric Research, Hobart, TAS, 7000, Australia. 40Australian Museum, Sydney, NSW, 2010, Australia. 41Smithsonian Tropical Research Institute, Balboa, 0843-03092, Panamá. 42Cornell University, Ithaca, NY 14853, USA. 43 Université Marien Ngouabi, Brazzaville, B.P. 69, Republic of Congo. 44National Museum of Nature and Science, Tsukuba, 305-0005, Japan. 45University of Wisconsin-Parkside, Kenosha, WI 53141–2000, USA. 46Cincinnati Museum Center, Cincinnati, OH 45203, USA. 47The Manitoba Museum, Winnipeg, MB, R3B 0N2, Canada. 48Australian National University, Canberra, ACT, 0200, Australia. 49 University of Michigan, Ann Arbor, MI 48109–1079, USA. 50California State University, Fullerton, CA 92831, USA. 51The Ornithological Council, Chevy Chase, MD 20815, USA. 52University of Florida, Gainesville, FL 32611, USA. 53Universidad Central de Venezuela, Caracas, 1041, Venezuela. 54Pontificia Universidad Católica de Chile, Santiago 6513677, Chile. 55University of New Mexico, Albuquerque, NM 87131–0001, USA. 56Bernice P. Bishop Museum, Honolulu, HI 96817, USA. 57University of the Ryukyus, Nishihara, 903-0213, Japan. 58 Museum für Naturkunde, Berlin, 10115, Germany. 59 Naturhistorisches Museum der Burgergemeinde Bern, Bern, CH-3005, Switzerland. 60Long Island University, Brooklyn, NY 11201–8423, USA. 61 Auckland Museum, Auckland, 1142, New Zealand. 62 Centro de Ornitologia y Biodiversidad, Lima, 33, Peru. 63Royal Belgian Institute of Natural Sciences, Brussels, 1000, Belgium. 64McGill University, Montreal, QC, H9X 3V9, Canada. 65University of Alaska Museum, Fairbanks, AK 99775, USA. 66Royal Ontario Museum, Toronto, ON, M5S 2C6, Canada. *Corresponding author. E-mail: LRocha@ calacademy.org R E F E R E N CES 1 California Academy of Sciences, San Francisco, CA 94118, USA. 2Museu Paraense Emílio Goeldi, Belém, PA, 66040-170, Brazil. 3Western Australian Museum, Perth, WA, 6986, Australia. 4Smithsonian Institution, Washington, DC 20560, USA. 5Natural History 1. E. Fuller, The Great Auk (H. N. Abrams, New York, 1999). 2. J. P. Hume, M. Walters, Extinction in Birds (Bloomsbury, London, 2012). 3. N. J. Collar, Bird Cons. Int. 10, 1 (2000). 4. K. Winker et al., Auk 127, 690 (2010). SCIENCE sciencemag.org 5. T. L. Cheng, S. M. Rovito, D. B. Wake, V. T. Vredenburg, Proc. Natl. Acad. Sci. U.S.A. 108, 9502 (2011). 6. R. D. Porter, S. N. Wiemeyer, Science 165, 199 (1969). 7. J. L. Gardner, A. Peters, M. R. Kearney, L. Joseph, R. Heinsohn, Trends Ecol. Evol. 26, 285 (2011). 8. Y. Sadovy de Mitcheson et al., Fish Fish. 14, 119 (2013). 9. K. Bi et al., Mol. Ecol. 22, 6018 (2013). 10. M. Clavero, E. Garcia-Berthou, Trends Ecol. Evol. 20, 110 (2005). 11. B. Collen, N. Pettorelli, J. E. M. Baillie, S. M. Durant, Eds., Biodiversity Monitoring and Conservation: Bridging the Gap between Global Commitment and Local Action (Wiley, Cambridge, UK, 2013). 12. M.V. Erdmann, in Still counting…: Biodiversity Exploration for Conservation – the first 20 years of the Rapid Assessment Program, L. E. Alonso, J. L. Deichmann, S. A. McKenna, P. Naskrecki, S. J. Richards, Eds. (Conservation International, Arlington, VA, 2010). 13. C. Mora, D. P. Tittensor, S. Adl, A. G. B. Simpson, B. Worm, PLOS Biol. 9, e1001127 (2011). Specimen collection: Plan for the future WE WISH THAT B. A. Minteer et al.’s claim that field biologists routinely collect voucher specimens were true [“Avoiding (re)extinction,” Perspectives, 18 April, p. 260]. Any museum curator will tell you that it is a constant struggle to convince them to do so, despite countless publications rendered unreliable because it is impossible to verify species’ identities. The necessity of voucher specimens varies by taxon and region, but in general, it is good practice to deposit them and as much data as possible, including DNA and photos in life. We certainly do not wish to see any species driven to extinction by overcollecting, but submit that this is rare and more associated with commercial or ardent, recreational overcollecting than sensible scientific vouchering (1, 2). If the kill of a single individual increases the extinction risk of a species, then it is well below viable population size and already among the “walking dead.” Dawkins’ description of evolution as improbability on a colossal scale is nowhere more evident than in morphology. Whether or not a species survives, museum specimens represent a window on many of its most remarkable novelties. Molecular data, although helpful in identifications, is neither a panacea nor surrogate for museum specimens, especially when it comes to newly discovered species. Describing a new species without depositing a holotype when a specimen can be preserved borders on taxonomic malpractice. Even given good photographs and a tissue sample, there are reasons to collect one or more complete specimens. We do not know what morphological characters will prove important in future studies of species status, phylogenetic 23 MAY 2014 • VOL 344 ISSUE 6186 Published by AAAS 815