Journal of Mammalogy, 99(1):1–14, 2018 DOI:10.1093/jmammal/gyx147

Invited Paper How many of are there?

Connor J. Burgin,1 Jocelyn P. Colella,1 Philip L. Kahn, and Nathan S. Upham* Department of Biological Sciences, Boise State University, 1910 University Drive, Boise, ID 83725, USA (CJB) Department of Biology and Museum of Southwestern Biology, University of New Mexico, MSC03-2020, Albuquerque, NM 87131, USA (JPC) Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA (PLK) Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511, USA (NSU) Integrative Research Center, Field Museum of Natural History, Chicago, IL 60605, USA (NSU) 1Co-first authors. * Correspondent: [email protected]

Accurate is central to the study of biological diversity, as it provides the needed evolutionary framework for taxon sampling and interpreting results. While the number of recognized species in the class Mammalia has increased through time, tabulation of those increases has relied on the sporadic release of revisionary compendia like the Species of the World (MSW) series. Here, we present the Mammal Diversity Database (MDD), a digital, publically accessible, and updateable list of all mammalian species, now available online: https://mammaldiversity.org. The MDD will continue to be updated as manuscripts describing new species and higher taxonomic changes are released. Starting from the baseline of the 3rd edition of MSW (MSW3), we performed a review of taxonomic changes published since 2004 and digitally linked species names to their original descriptions and subsequent revisionary articles in an interactive, hierarchical database. We found 6,495 species of currently recognized mammals (96 recently extinct, 6,399 extant), compared to 5,416 in MSW3 (75 extinct, 5,341 extant)—an increase of 1,079 species in about 13 years, including 11 species newly described as having gone extinct in the last 500 years. We tabulate 1,251 new species recognitions, at least 172 unions, and multiple major, higher-level changes, including an additional 88 genera (1,314 now, compared to 1,226 in MSW3) and 14 newly recognized families (167 compared to 153). Analyses of the description of new species through time and across biogeographic regions show a long-term global rate of ~25 species recognized per year, with the Neotropics as the overall most species-dense biogeographic region for mammals, followed closely by the Afrotropics. The MDD provides the mammalogical community with an updateable online database of taxonomic changes, joining digital efforts already established for amphibians (AmphibiaWeb, AMNH’s Amphibian Species of the World), birds (e.g., Avibase, IOC World Bird List, HBW Alive), non-avian reptiles (The Reptile Database), and fish (e.g., FishBase, Catalog of Fishes).

Una taxonomía que precisamente refleje la realidad biológica es fundamental para el estudio de la diversidad de la vida, ya que proporciona el armazón evolutivo necesario para el muestreo de taxones e interpretación de resultados del mismo. Si bien el número de especies reconocidas en la clase Mammalia ha aumentado con el tiempo, la tabulación de esos aumentos se ha basado en las esporádicas publicaciones de compendios de revisiones taxonómicas, tales como la serie Especies de mamíferos del mundo (MSW por sus siglas en inglés). En este trabajo presentamos la Base de Datos de Diversidad de Mamíferos (MDD por sus siglas en inglés): una lista digital de todas las especies de mamíferos, actualizable y accesible públicamente, disponible en la dirección URL https://mammaldiversity.org/. El MDD se actualizará con regularidad a medida que se publiquen artículos que describan nuevas especies o que introduzcan cambios de diferentes categorías taxonómicas. Con la tercera edición de MSW (MSW3) como punto de partida, realizamos una revisión en profundidad de los cambios taxonómicos publicados a partir del 2004. Los nombres de las especies nuevamente descriptas (o ascendidas a partir de subespecies) fueron conectadas digitalmente en una base de datos interactiva y jerárquica con sus

© 2018 American Society of Mammalogists, www.mammalogy.org

1

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 2 JOURNAL OF MAMMALOGY

descripciones originales y con artículos de revisión posteriores. Los datos indican que existen actualmente 6,495 especies de mamíferos (96 extintas, 6,399 vivientes), en comparación con las 5,416 reconocidas en MSW3 (75 extintas, 5,341 vivientes): un aumento de 1,079 especies en aproximadamente 13 años, incluyendo 11 nuevas especies consideradas extintas en los últimos 500 años. Señalamos 1,251 nuevos reconocimientos de especies, al menos 172 uniones y varios cambios a mayor nivel taxonómico, incluyendo 88 géneros adicionales (1,314 reconocidos, comparados con 1,226 en MSW3) y 14 familias recién reconocidas (167 en comparación con 153 en MSW3). Los análisis témporo-geográficos de descripciones de nuevas especies (en las principales regiones del mundo) sugieren un promedio mundial de descripciones a largo plazo de aproximadamente 25 especies reconocidas por año, siendo el Neotrópico la región con mayor densidad de especies de mamíferos en el mundo, seguida de cerca por la region Afrotrópical. El MDD proporciona a la comunidad de mastozoólogos una base de datos de cambios taxonómicos conectada y actualizable, que se suma a los esfuerzos digitales ya establecidos para anfibios (AmphibiaWeb, Amphibian Species of the World), aves (p. ej., Avibase, IOC World Bird List, HBW Alive), reptiles “no voladores” (The Reptile Database), y peces (p. ej., FishBase, Catalog of Fishes).

Key words: , conservation, extinction, taxonomy

Species are a fundamental unit of study in mammalogy. Yet spe- behaviorally cryptic (e.g., shrews, burrowing mammals). For cies limits are subject to change with improved understanding of example, the phylogenetic placement of tenrecs and golden geographic distributions, field behaviors, and genetic relation- moles (families: Tenrecidae and Chrysochloridae) has long been ships, among other advances. These changes are recorded in a a point of taxonomic contention, having variously been included vast taxonomic literature of monographs, books, and periodi- within Insectivora, Eulipotyphla, and Lipotyphla. Taxonomic cals, many of which are difficult to access. As a consequence, assignment of this group was only conclusively resolved when a unified tabulation of changes to species and higher taxa has genetic data (Madsen et al. 2001; Murphy et al. 2001), as corrob- become essential to mammalogical research and conservation orated by morphology (Asher et al. 2003), aligned Tenrecidae efforts in mammalogy. Wilson and Reeder’s 3rd edition of and Chrysochloridae in the Afrosoricida and found it Mammal Species of the World (MSW3), published in November allied to other African radiations in the superorder Afrotheria 2005, represents the most comprehensive and up-to-date list of (Macroscelidea, Tubulidentata, Hyracoidea, Proboscidea, mammalian species, with 5,416 species (75 recently extinct, Sirenia). As analytical methods evolve and techniques become 5,341 extant), 1,229 genera, 153 families, and 29 orders. That more refined, mammalian taxonomy will continue to change, edition relied on expertise solicited from 21 authors to deliver making it desirable to create an adjustable list of accepted spe- the most comprehensive list of extant mammals then availa- cies-level designations and their hierarchical placement that can ble. However, the episodic release of these massive anthologies be updated on a regular basis. Such a list is needed to promote (MSW1—Honacki et al. 1982; MSW2—Wilson and Reeder consistency and accuracy of communication among mammalo- 1993; MSW3—Wilson and Reeder 2005) means that taxo- gists and other researchers. nomic changes occurring during or soon after the release of a Here, using MSW3 as a foundation, we provide an up-to- new edition may not be easily accessible for over a decade. For date list of mammal species and introduce access to this spe- example, MSW3, compared to MSW2, resulted in the addition cies list as an amendable digital archive: the Mammal Diversity of 787 species, 94 genera, and 17 families compared to MSW2 Database (MDD), available online at http://mammaldiversity. (Solari and Baker 2007). Since the publication of MSW3, there org. We compare our list to that of MSW3 to quantify changes has been a steady flow of taxonomic changes proposed in peer- in mammalian taxonomy that have occurred over the last reviewed journals and books; however, changes proposed more 13 years and evaluate the distribution of species diversity and than a decade ago (e.g., Carleton et al. 2006; Woodman et al. new species descriptions across both geography and time. We 2006) have yet to be incorporated into a Mammalia-wide refer- intend the MDD as a community resource for compiling and ence taxonomy. This lag between the publication of taxonomic disseminating published changes to mammalian taxonomy in changes and their integration into the larger field of mammal- real time, rather than as a subjective arbiter for the relative ogy inhibits taxonomic consistency and accuracy in mam- strength of revisionary evidence, and hence defer to the peer- malogical research, and—at worst—it can impede the effective reviewed literature for such debates. conservation of mammals in instances where management deci- sions depend upon the species-level designation of distinctive evolutionary units. Materials and Methods The genetic era has catalyzed the discovery of morphologi- Starting from those species recognized in MSW3, we reviewed cally cryptic species and led to myriad intra- and interspecific > 1,200 additional taxonomic publications appearing after revisions, either dividing species (splits) or uniting them (lumps). MSW3’s end-2003 cutoff date in order to compile a list of Many groups of mammals are taxonomically complex and in every recognized mammal species. In addition to evaluating need of further revision, especially those that have received peer-reviewed manuscripts, other major references included the relatively little systematic attention or are morphologically or Handbook of the Mammals of the World volumes 1–6 (Wilson

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 3

and Mittermeier 2009, 2011, 2014, 2015; Mittermeier et al. Seychelles). We grouped the Australasian and Oceanian 2013; Wilson et al. 2016), Mammals of South America volumes realms to include a single category for Australia, New 1 and 2 (Gardner 2007; Patton et al. 2015), Mammals of Africa Zealand, Sulawesi, and the islands east of Sulawesi, including volumes 1–6 (Kingdon et al. 2013), Rodents of Sub-Saharan Melanesia, Polynesia, Micronesia, Hawaii, and Easter Island, Africa (Monadjem et al. 2015), Taxonomy of Australian but excluding the Palearctic Japanese Bonin Islands. There are Mammals (Jackson and Groves 2015), and Ungulate Taxonomy no terrestrial mammal species native to Antarctica. Open-water (Groves and Grubb 2011). We linked each species to its pri- and coastal marine species, including the few Antarctic breed- mary, descriptive publication and if a species was taxonomi- ing species (e.g., leopard seals, Hydrurga), were grouped sep- cally revised since 2004, the associated revisionary publications arately. Freshwater species (e.g., river dolphins, river ) also were linked. The list was curated for spelling errors and were sorted by their resident landmass. compared to the species recognized in MSW3 to determine the Based on our newly curated list, we calculated the number total change in the number of recognized species over the inter- of new species described each decade since the origin of bi- val 1 January 2004 to 15 August 2017; the latter date was our nomial nomenclature (Linnaeus 1758) to determine the major cutoff for reviewing literature. As with MSW3 and the IUCN eras of species discovery and taxonomic description. The year (2017) RedList, species totals for the MDD include mamma- 1758 includes all the species described by Linnaeus that are lian species that have gone extinct during the last 500 years, still currently recognized. For each biogeographic realm, we an arbitrary period of time used to delimit species “recently calculated the total number of mammalian species recognized extinct”. The IUCN taxonomy was downloaded on 28 June and the number of new species recognized since 2004. Note 2017. that the recognition of new species in a particular region can re- We considered “de novo” species descriptions to be those flect greater research efforts per region or taxon and thus cannot species recognized since MSW3 and named with novel spe- be extrapolated to the expected number of undiscovered species cies epithets (post-MSW3 proposal date), whereas “splits” are in that region. We scaled the number of species by regional land species established by resurrecting an existing name (i.e., ele- area (km2—World Atlas 2017) to determine the most species- vated or synonym, and pre-MSW3 proposal). We dense region. based these 2 bins of new species on the epithet authority year to enable downstream analyses of species discovery trends. However, we acknowledge that this categorization is not precise Results regarding the more complex (and biologically interesting) issue The MDD currently lists 6,495 valid species of mammals of how many species were derived from new field discover- (6,399 extant, 96 recently extinct), which is 1,079 more spe- ies of distinctive populations versus the recognition of multiple cies than were recognized in MSW3 (1,058 extant and 21 species within named forms (Patterson 1996). Nevertheless, we extinct) and a 19.9% increase in species during about 13 years expected the de novo category to encompass those field dis- (Table 1). The MDD recognizes 1,251 new species described coveries along with other types of species descriptions, and the since MSW3 in categories of splits (720 species; 58%) and de splits category to encompass instances where existing names novo species descriptions (531 species; 42%), indicating that are elevated or validated, both of which are categories warrant- at least 172 species were lumped together since the release of ing future investigation. MSW3. The MDD documents a total of 1,314 genera (increas- In addition to taxonomic ranks (order, , , species) ing by 88 from MSW3), 167 families (increasing by 14), and and primary data links, MDD species information includes 27 orders (decreasing by 2). The MDD also includes 17 domes- the year of description, scientific authority, and geographic ticated species in the listing to facilitate the association of occurrence by biogeographic region. Here, we approximate the biogeographic realms defined by the World Wildlife Fund Table 1.—Comparison of Mammal Diversity Database (MDD) (Olson and Dinerstein 1998; Olson et al. 2001), with the excep- taxonomic totals and those of Mammal Species of the World (MSW) tion that we classified countries split across multiple biogeo- editions 1–3 and the International Union of Conservation of Nature graphic realms as belonging exclusively to the realm covering (IUCN) RedList, version 2017-1. the majority of that country. We defined the Nearctic realm as Taxa MSW1 MSW2 MSW3 IUCN MDD all of North America, including Florida, Bermuda, and all of 1982 1993 2005 2017 This study Mexico. The Neotropical realm included all of South America, Central America, and the insular Caribbean. The Palearctic Species Total 4,170 4,631a 5,416 5,560 6,495 realm included all of Europe, northern Asia (including all of Extinct NA NA 75 85b 96 China), Japan, and northern Africa (Egypt, Algeria, Tunisia, Living NA NA 5,341 5,475 6,399 Morocco, Western Sahara, Canary Islands, and the Azores). The Living wild NA NA 5,338 5,475 6,382 Indomalayan realm included southern and southeastern Asia Genera 1,033 1,135 1,230 1,267 1,314 (Pakistan, India, Nepal, Bhutan, Vietnam, Laos, Myanmar) Families 135 132 153 159 167 Orders 20 26 29 27 27 and all islands west of Sulawesi including the Greater Sundas and Philippines. The Afrotropical realm included all of sub- aCorrected total per Solari and Baker (2007). Saharan Africa and the Arabian Peninsula, plus Madagascar bExtinct IUCN mammals include both “EX” (extinct) and “EW” (extinct in and the nearby Indian Ocean islands (e.g., Comoros, Mauritius, the wild).

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 4 JOURNAL OF MAMMALOGY

these derivatives of wild populations with their often abundant into 2 (Hipposideridae, Rhinonycteridae—Foley et al. 2015), and trait data (e.g., DNA sequences, reproductive data). Details Bathyergidae into 2 (Bathyergidae, Heterocephalidae—Patterson of the full MDD version 1 taxonomy, including associated and Upham 2014). One family, Diatomyidae, was added based citations and geographic region assignments, are provided in on a species discovery (Laonastes aenigmamus—Jenkins et al. Supplementary Data S1. 2005), although it was already known as a prehistorically extinct The largest mammalian families are in the order Rodentia— family (Dawson et al. 2006). Additional newly recognized Muridae (834 species versus 730 in MSW3) and Cricetidae families are Chlamyphoridae, Cistugidae, Kogiidae, Lipotidae, (792 species versus 681 in MSW3)—followed by the chi- Miniopteridae, Pontoporiidae, Potamogalidae, Prionodontidae, ropteran family Vespertilionidae (493 species versus 407 in and Zenkerellidae. Three families recognized in MSW3 have MSW3) and the eulipotyphlan family Soricidae (440 species since been subsumed: Myocastoridae and Heptaxodontidae inside versus 376 in MSW3). Unsurprisingly, the 2 most speciose Echimyidae (Emmons et al. 2015), and Aotidae inside Cebidae orders (Rodentia and Chiroptera) witnessed the most species (Schneider and Sampaio 2015; Dumas and Mazzoleni 2017). additions: 371 and 304 species, respectively. The most speciose Note that Capromyidae is still recognized at the family level rodent family besides Muridae and Cricetidae is Sciuridae (298 (Fabre et al. 2017). The order Cetacea also experienced major revi- species) and 6 rodent families are monotypic: Aplodontiidae, sions, and is now included within the order Artiodactyla based on Diatomyidae, Dinomyidae, Heterocephalidae, Petromuridae, genetic and morphological data (Gatesy et al. 1999; Adams 2001; and Zenkerellidae. The most speciose chiropteran families Asher and Helgen 2010). Soricomorpha and Erinaceomorpha along with Vespertilionidae are Phyllostomidae (214 species) also are grouped together in the order Eulipotyphla, given their and Pteropodidae (197 species), whereas there is only 1 mono- shared evolutionary history demonstrated by genetic analyses typic bat family: Craseonycteridae. (Douady et al. 2002; Meredith et al. 2011). The increased number of recognized genera to 1,314 (from On average, since 1758, 24.95 species have been described 1,230 in MSW3) results from the demonstrated paraphyly per decade, including 3 major spikes in species recognition in the of several speciose and widely distributed former genera. 1820–1840s, 1890–1920s, and 2000–2010s (Fig. 1). These bursts This includes Spermophilus, which was split into 8 dis- of systematic and taxonomic development were followed by 2 tinct genera (Spermophilus, Urocitellus, Callospermophilus, major troughs from about 1850–1880 and 1930–1990 (Fig. 1). Otospermophilus, Xerospermophilus, Ictidomys, Poliocitellus, Currently, we detect an accelerating rate of species description and Notocitellus—Helgen et al. 2009) and Oryzomys, which per decade, increasing from the 1990s (207 species), 2000s (341 was split into 11 genera (Oryzomys, Aegialomys, Cerradomys, species), and 2010s so far (298 species). A linear regression on Eremoryzomys, Euryoryzomys, Hylaeamys, Mindomys, these data suggests that if trends in mammalian species discov- Nephelomys, Oreoryzomys, Sooretamys, and Transandinomys— ery continue, 120.46 species are yet to be discovered this decade, Weksler et al. 2006). Many smaller generic splits broke 1 genus potentially resulting in a total of 418 new species to be recog- into 2 or more genera and often involved the naming of a new nized between 2010 and 2020 (R2 = 0.97, P < 0.000; Fig. 1). genus, such as with Castoria (formerly Akodon—Pardiñas Across biogeographic regions, the Neotropics harbors the et al. 2016), Paynomys (formerly Chelemys—Teta et al. 2016), greatest number of currently recognized mammalian species and Petrosaltator (formerly Elephantulus—Dumbacher 2016). (1,617 species), followed by the Afrotropics (1,572 species), Other genera were described on the basis of newly discovered and the Palearctic (1,162 species), whereas Australasia-Oceania taxa, such as Laonastes (Jenkins et al. 2005), Xeronycteris has the least (527 species) (Fig. 2). The Neotropics also has (Gregorin and Ditchfield 2005), Rungwecebus (Davenport the most newly recognized species (362 species—169 de novo et al. 2006), Drymoreomys (Percequillo et al. 2011), and and 193 split), again followed by the Afrotropics (357 spe- Paucidentomys (Esselstyn et al. 2012). The most speciose cur- cies—158 de novo and 199 split), and with the fewest new spe- rently recognized genera are Crocidura (197 species), Myotis cies described from Australasia-Oceania (48 species—18 de (126 species), and Rhinolophus (102 species). These also are novo and 30 split). Other categories included the marine (124 the only genera of mammals that currently exceed 100 recog- total species—4 de novo and 5 split), domesticated (17 total spe- nized and living species, with Rhinolophus reaching this level cies—0 de novo and 2 split), and extinct (96 total species—7 de only recently. novo and 4 split; Fig. 2; Table 2) categories. When weighting Higher-level taxonomy also was significantly altered since the biogeographic realms by land area, we find the Neotropics 2004, with the recognition of 14 additional families and 2 and Afrotropics are also the most species-dense biogeographic fewer orders than MSW3. In the MDD, we included 3 families regions (85.1 and 71.1 species per km2, respectively), followed (†Megaladapidae, †Palaeopropithecidae, †Archaeolemuridae) closely by Australasia-Oceania (61.4 species per km2; Table 2). that were not in MSW3 but that may have gone extinct in the In all realms except the Indomalayan, more species were recog- last 500 years (McKenna and Bell 1997; Montagnon et al. 2001; nized via taxonomic splits than by de novo descriptions. Gaudin 2004; Muldoon 2010). The net addition of 11 other families in the MDD are the result of taxonomic splits and new taxon discoveries, as well as families lumped since MSW3. Discussion For example, Dipodidae was split into 3 families (Dipodidae, Mammalogists have a collective responsibility to serve the most Zapodidae, Sminthidae—Lebedev et al. 2013), Hipposideridae current taxonomic information about mammalian biodiversity

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 5

Fig. 1.—Cumulative and decadal descriptions of taxonomically valid extant mammal species from 1758 to 15 August 2017.

Fig. 2.—The number of mammalian species distributed in each biogeographical region: Palearctic, Afrotropic, Indomalayan, Nearctic, Neotropic, and Australasia-Oceania (i.e., Aust-Oceania), with marine, extinct, and domestic species in separate categories. Each group is divided into species recognized in both MSW3 and MDD, and new species in the MDD in categories of newly coined species epithet (de novo) versus existing species epithet (splits). The dot within each bar indicates the relative species density per km2 land area, values are available in Table 2. MDD = Mammal Diversity Database; MSW3 = 3rd edition of Mammal Species of the World.

to the general public. The need for mammalian taxonomy to access to this biodiversity data for purposes of study design, reflect our current understanding of species boundaries and classroom teaching, analyses, and writing. The release of the evolutionary relationships is only expected to grow as efforts to MDD therefore addresses a key need in the mammalogical and synthesize “big data” increase in frequency, scope, and sophis- global biodiversity communities alike. Whether we study the tication. Studies at this macroscale address major questions behavioral ecology of desert rodents or the macroevolution of in evolution, ecology, and biodiversity conservation across tetrapods, biologists collectively need accurate measurements the tree of life (e.g., Rabosky et al. 2012; Hedges et al. 2015; of species diversity—the most commonly assessed (but not the Hinchliff et al. 2015), yielding results relevant to global issues only) dimension of biodiversity (Jarzyna and Jetz 2016). of sustainability that require our best data on biodiversity The MDD represents the most comprehensive taxonomic (Pascual et al. 2017). Mammalogists, in turn, benefit from easy compendium of currently recognized mammals, documenting

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 6 JOURNAL OF MAMMALOGY

Table 2.—The total number of mammal species in the Mammal Diversity Database (MDD) as compared to Mammal Species of the World, vol- ume 3 (MSW3) that live within each biogeographic realm and those belonging to domestic and extinct categories. Numbers correspond to Fig. 2. Note that some species are found within multiple regions, so column totals do not correspond to taxonomic totals.

Category Total species Shared with MSW3 De novo Split Area (million km2) Density (species/km2) Neotropic 1,617 1,255 169 193 19.0 85.1 Afrotropic 1,572 1,215 158 199 22.1 71.1 Palearctic 1,162 938 48 176 54.1 21.5 Indomalaya 954 774 97 83 7.5 12.7 Nearctic 697 628 15 54 22.9 30.4 Aust-Oceania 527 479 18 30 8.6 61.4 Marine 124 115 4 5 Domestic 17 15 2 Extinct 96 85 7 4

6,399 extant species (Tables 1 and 3) as well as 96 recently bats is unsurprising given their existing diversity, these clades extinct species for a total of 6,495 species. This database is may reasonably contain disproportionally high levels of cryptic updateable and digitally searchable, tracking primary sources diversity (e.g., Ruedi and Mayer 2001; Belfiore et al. 2008), of species descriptions and phylogenetic studies of higher-level and thus the application of genetic sequence data may continue (genus or family) taxonomic changes and compiling them into to yield greater insights. Within Eulipotyphla (most particularly a single listing. The MDD thus closes the gap between pro- in shrews), we expect that the discovery of new species will posed taxonomic changes and integration into a broader under- continue given their rate of recent discoveries and frequency of standing of mammalian diversity, and it then distributes this morphological crypsis (Esselstyn et al. 2013). The species rich- information to the scientific community and lay public as it is ness in Sorex (86 species) and Crocidura (197 species) suggests published in scientific literature. We aim for the MDD to build that genus-level revisions are needed and, when conducted, are on this capacity as a record keeper to be a resource for hosting likely to yield further taxonomic rearrangements (Castiglia histories of taxonomic change. For example, the MDD records et al. 2017; Matson and Ordóñez-Garza 2017). both the description of Tapirus kabomani (Cozzuol et al. 2013) The MDD includes a total of 465 species of non-cetacean and the later synonymy of this taxon under T. terrestris (Voss Artiodactyla and Perissodactyla recognized by Groves and et al. 2014). Likewise, the revision of Spermophilus ground Grubb (2011) with select modifications based on taxonomic squirrels into 8 genera (Helgen et al. 2009) altered the binomial refinements published after the release of the latter (e.g., 4 spe- names of 28 species, a rearrangement that usefully established cies of Giraffa [Bercovitch et al. 2017] versus 8 [Groves and generic monophyly, but one that has not been readily summa- Grubb 2011]). This total compares to 240 species in these or- rized for workers without easy access to libraries. The MDD ders recognized in MSW3 (> 93% increase). Although some compiles data on genus transfers published since 2004 across researchers have argued that the changes proposed by Groves all of Mammalia, helping to release researchers from undertak- and Grubb (2011) exemplify an extreme form of taxonomic in- ing piecemeal taxonomic updates for their projects. flation (Lorenzen et al. 2012; Zachos et al. 2013; Harley et al. Preliminary findings from the MDD compilation indicate 2016), the increase in species richness is comparable to concur- that Primates has been a nexus of new species discovery, which rent rates of increase in the richness of Rodentia, Chiroptera, is unexpected given their large body sizes. An incredible 148 Eulipotyphla, and Primates. For now, inclusion of the tax- primate species have been recognized since the publication of onomy of Groves and Grubb (2011) in the MDD ensures that MSW3, including 67 de novo and 81 splits (Tables 1 and 3), a these taxa are vetted by the greater mammalogical community taxonomic outcome that is striking for our closest human rela- using multiple tiers of evidence (de Queiroz et al. 2007; Voss tives. Taxonomic revisions have centered around New World et al. 2014). monkey families (Cebidae—Boubli et al. 2012; Pitheciidae— Following the publication of Linnaeus’s 10th edition of Marsh 2014) and many de novo species descriptions also Systema Naturae in 1758, the number of described species of occurred among Malagasy lemurs (Cheirogaleidae—Lei et al. mammals has increased at various rates, punctuated by factors 2014; Lepilemuridae—Louis et al. 2006). However, persis- including the efforts of prolific systematists and world events tent taxonomic uncertainty within the family Cercopithecidae (Fig. 1). For example, Oldfield Thomas (1858–1929) of the (Groves 2007a, 2007b; Mittermeier et al. 2013) suggests that British Museum (now the Natural History Museum, London), the species-level diversity of Primates is not yet stable and will considered one of the “greatest taxonomists […] who ever continue to fluctuate. lived” (Flannery 2012), was responsible for nearly 3,000 new Among other taxonomic changes, the MDD documents the names for genera, species, and subspecies (Hill 1990). In turn, addition of 371 species of Rodentia, 304 species of Chiroptera, reduced rates of species descriptions in the mid-20th cen- 86 species of Eulipotyphla, and 227 species of Artiodactyla, tury may be linked to periods of political instability and lim- including many species from historically well-studied geo- ited scientific activity during World War I (1914–1918) and II graphic regions (Table 2; Rausch et al. 2007; Castiglia et al. (1939–1945). Methodological innovations such as polymer- 2017). While the addition of > 300 species each of rodents and ase chain reaction (PCR—Mullis et al. 1989) may have driven

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 7

Table 3.—Totals of the genera and species per families and orders currently listed in the Mammal Diversity Database (MDD) online compila- tion, along with new species described since Mammal Species of the World volume 3 (MSW3) in categories of split or de novo, based on whether the specific epithet already existed or was newly coined, respectively.

Genera Species New species since MSW3 Splits De novo Class Mammalia 1,314 6,495 720 531 Subclass Prototheria 3 5 Order Monotremata 3 5 Family Ornithorhynchidae 1 1 Family Tachyglossidae 2 4 Subclass Theria 1,311 6,490 720 531 Infraclass Marsupialia 91 379 32 29 Order Didelphimorphia 18 111 15 18 Family Didelphidae 18 111 15 18 Order Paucituberculata 3 7 1 Family Caenolestidae 3 7 1 Order Microbiotheria 1 3 2 Family Microbiotheriidae 1 3 2 Order Notoryctemorphia 1 2 Family Notoryctidae 1 2 Order Dasyuromorpha 19 78 5 5 Family Dasyuridae 17 76 5 5 Family Myrmecobiidae 1 1 Family †Thylacinidae 1 1 Order Peramelemorphia 8 23 1 1 Family †Chaeropodidae 1 1 Family Peramelidae 6 20 1 1 Family Thylacomyidae 1 2 Order Diprotodontia 41 155 11 2 Family Acrobatidae 2 3 1 Family Burramyidae 2 5 Family Hypsiprymnodontidae 1 1 Family Macropodidae 13 67 3 Family Petauridae 3 12 1 Family Phalangeridae 6 30 3 1 Family Phascolarctidae 1 1 Family Potoroidae 4 12 1 Family Pseudocheiridae 6 20 3 Family Tarsipedidae 1 1 Family Vombatidae 2 3 Infraclass Placentalia 1,220 6,111 684 502 Superorder Afrotheria 34 89 8 6 Order Tubulidentata 1 1 Family Orycteropodidae 1 1 Order Afrosoricida 20 55 1 3 Family Chrysochloridae 10 21 Family Potamogalidaea 2 3 Family Tenrecidae 8 31 1 3 Order Macroscelidea 5 20 2 3 Family Macroscelididae 5 20 2 3 Order Hyracoidea 3 5 1 Family Procaviidae 3 5 1 Order Proboscidea 2 3 Family Elephantidae 2 3 Order Sirenia 3 5 Family Dugongidae 2 2 Family Trichechidae 1 3 Superorder Xenarthra 14 30 Order Cingulata 9 20 Family Chlamyphoridaeb 8 13 Family Dasypodidae 1 7 Order Pilosa 5 10 Family Bradypodidae 1 4 Family Cyclopedidae 1 1 Family Megalonychidae 1 2 Family Myrmecophagidae 2 3

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 8 JOURNAL OF MAMMALOGY

Table 3.—Continued

Genera Species New species since MSW3 Splits De novo Superorder Euarchontoglires 616 3,194 285 249 Order Scandentia 4 24 4 Family Ptilocercidae 1 1 Family Tupaiidae 3 23 4 Order Dermoptera 2 2 Family Cynocephalidae 2 2 Order Primates 84 518 81 67 Family †Archaeolemuridaec 1 2 Family Atelidae 4 25 3 Family Cebidaed 11 89 27 2 Family Cercopithecidae 23 160 24 5 Family Cheirogaleidae 5 40 1 20 Family Daubentoniidae 1 1 Family Galagidae 6 20 2 2 Family Hominidae 4 7 Family Hylobatidae 4 20 3 2 Family Indriidaee 3 19 2 6 Family Lemuridae 5 21 2 Family Lepilemuridae 1 26 16 Family Lorisidae 4 15 6 1 Family †Megaladapidaec 1 1 Family †Palaeopropithecidaec 1 1 Family Pitheciidae 7 58 9 9 Family Tarsiidae 3 13 2 4 Order Lagomorpha 13 98 10 1 Family Leporidae 11 67 5 1 Family Ochotonidae 1 30 5 Family †Prolagidae 1 1 Order Rodentia 513 2,552 190 181 Family Abrocomidae 2 10 Family Anomaluridae 2 6 Family Aplodontiidae 1 1 Family Bathyergidae 5 21 3 4 Family Calomyscidae 1 8 Family Capromyidae 7 17 Family Castoridae 1 2 Family Caviidae 6 21 3 Family Chinchillidae 3 7 1 Family Cricetidae 145 792 75 61 Family Ctenodactylidae 4 5 Family Ctenomyidae 1 69 5 6 Family Cuniculidae 1 2 Family Dasyproctidae 2 15 2 1 Family Diatomyidaef 1 1 1 Family Dinomyidae 1 1 Family Dipodidae 13 37 3 Family Echimyidaeg 25 93 6 3 Family Erethizontidae 3 17 1 2 Family Geomyidae 7 41 8 1 Family Gliridae 9 29 1 Family Heterocephalidaeh 1 1 Family Heteromyidae 5 66 6 2 Family Hystricidae 3 11 Family Muridae 157 834 41 84 Family Nesomyidae 21 68 1 6 Family Octodontidae 7 14 1 Family Pedetidae 1 2 Family Petromuridae 1 1 Family Platacanthomyidae 2 5 2 1 Family Sciuridae 62 298 18 5 Family Sminthidaei 1 14 2

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 9

Table 3.—Continued

Genera Species New species since MSW3 Splits De novo Family Spalacidae 7 28 8 Family Thryonomyidae 1 2 Family Zapodidaei 3 12 6 1 Family Zenkerellidaej 1 1 Superorder 556 2,798 399 247 Order Eulipotyphlak 56 527 23 63 Family Erinaceidae 10 24 Family †Nesophontidae 1 6 Family Solenodontidae 1 3 Family Soricidae 26 440 16 55 Family Talpidae 18 54 7 8 Order Chiroptera 227 1,386 130 174 Family Cistugidael 1 2 Family Craseonycteridae 1 1 Family Emballonuridae 14 54 3 Family Furipteridae 2 2 Family Hipposideridae 7 88 6 8 Family Megadermatidae 5 6 1 Family Miniopteridael 1 35 7 9 Family Molossidae 19 122 12 13 Family Mormoopidae 2 17 8 Family Mystacinidae 1 2 Family Myzopodidae 1 2 1 Family Natalidae 3 11 3 Family Noctilionidae 1 2 Family Nycteridae 1 16 Family Phyllostomidae 62 214 22 37 Family Pteropodidae 45 197 5 12 Family Rhinolophidae 1 102 10 14 Family Rhinonycteridaem 4 9 1 3 Family Rhinopomatidae 1 6 1 1 Family Thyropteridae 1 5 2 Family Vespertilionidae 54 493 55 70 Order 130 305 23 2 Family 1 2 1 Family 13 39 3 Family 7 8 Family 14 42 5 Family Herpestidae 16 36 2 Family Hyaenidae 3 4 Family 4 12 1 Family 23 64 5 1 Family Nandiniidae 1 1 Family Odobenidae 1 1 Family Otariidae 7 16 Family Phocidae 14 19 Family Prionodontidaen 1 2 Family 6 14 2 1 Family Ursidae 5 8 Family 14 37 4 Order Pholidota 3 8 Family Manidae 3 8 Order Perissodactyla 8 21 4 Family Equidae 1 12 4 Family Rhinocerotidae 4 5 Family Tapiridae 3 4 Order Artiodactylao 132 551 219 8 Family Antilocapridae 1 1 Family Balaenidae 2 4 Family Balaenopteridae 2 8 1 Family Bovidae 54 297 152 2 Family Camelidae 2 7 1

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 10 JOURNAL OF MAMMALOGY

Table 3.—Continued

Genera Species New species since MSW3 Splits De novo Family Cervidae 18 93 43 Family Delphinidae 17 40 3 3 Family Eschrichtiidae 1 1 Family Giraffidae 2 5 3 Family Hippopotamidae 2 4 Family Iniidae 1 3 1 1 Family Kogiidaep 1 2 Family Lipotidaeq 1 1 Family Monodontidae 2 2 Family Moschidae 1 7 Family Neobalaenidae 1 1 Family Phocoenidae 3 7 1 Family Physeteridae 1 1 Family Platanistidae 1 1 Family Pontoporiidaeq 1 1 Family Suidae 6 28 11 Family Tayassuidae 3 5 2 Family Tragulidae 3 10 1 1 Family Ziphiidae 6 22 1

aSplit from Tenrecidae. jSplit from Anomaluridae. bSplit from Dasypodidae. kIncludes Soricomorpha and Erinaceomorpha. cRecently extinct families not included in MSW3. lSplit from Vespertilionidae. dIncludes Aotidae and Callitrichidae. mSplit from Hipposideridae. eWas spelled as “Indridae” in MSW3. nSplit from Felidae. fRecognized as extant based on Laonastes aenigmamus. oIncludes Cetacea. gIncludes Heptaxodontidae and Myocastoridae. pSplit from Physeteridae. hSplit from Bathyergidae. qSplit from Iniidae. iSplit from Dipodidae. †Extinct.

later bursts of species descriptions by allowing morphologically contain considerably greater species diversity than is com- cryptic but genetically divergent evolutionary lineages to be monly recognized. Remarkably, the same estimate of ~25 spe- recognized as species. For example, over one-half of the spe- cies/year was derived somewhat independently from tracking cies described since 2004 appear to have stemmed from taxo- 14 estimates of global diversity (1961–1999—Patterson 2001) nomic splits (~58%), many based in part or whole on genetic and from species-level changes between MSW2 and MSW3 data, to go with at least 172 species unions (lumps) during the (Reeder and Helgen 2007), thereby affirming the robustness of same period. As we continue to progress within the genomic era, that estimate across both data sources and eras. where data on millions of independent genetic loci can be read- Assumed in all taxonomic forecasts is the stability of global ily generated for taxonomic studies, there is a growing under- ecosystems, scientific institutions, and natural history collections. standing that hybridization and introgression commonly occur With mammals being disproportionately impacted by human- among mammalian species that may otherwise maintain genetic induced extinctions (Ceballos et al. 2017), especially in insular integrity (e.g., Larsen et al. 2010; Miller et al. 2012; vonHoldt regions like the Caribbean (Cooke et al. in press), efforts to protect et al. 2016). Characterizing species and their boundaries using threatened and their resident mammalian species are key multiple tiers of evidence will continue to be essential given the to the continued persistence, existence, and discovery of mammals. profound impact of species delimitation on legislative decisions The Neotropics is the most species-dense biogeographic region in (e.g., U.S. Endangered Species Act of 1973—Department of the the world, followed closely by the Afrotropics and Australasia- Interior, U.S. Fish and Wildlife Service 1973). Oceania, the latter of which is one of the least explored terrestrial At the current rate of taxonomic description of mammals regions on Earth, with the second fewest de novo species descrip- (~25 species/year from 1750 to 2017), we predict that 7,342 tions (18 species; Table 2). Inventory efforts may thus be fruitfully mammalian species will be recognized by 2050 and 8,590 by prioritized in northern Australia, Melanesia, Sulawesi, and other 2100. Alternatively, if we consider the increased rate of taxo- oceanic islands east of Wallace’s Line. However, we note that nomic descriptions since the advent of PCR (~30 species/year obtaining collecting permissions is a barrier to species description from 1990 to 2017), our estimates increase to 7,509 species in any region. The continued description and discovery of mamma- recognized by 2050 and 9,009 by 2100. These estimates sur- lian species diversity hinges on investment in both natural history pass Reeder and Helgen’s (2007) prediction of > 7,000 total collecting and in the physical collections that house the specimens mammalian species, but echo their observation that mammals essential for taxonomic research. Natural history collections are

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 11

repositories for the genetic and morphological vouchers used to Literature Cited describe every new species listed in the MDD, a fact that high- Adams, D. C. 2001. Are the fossil data really at odds with the molec- lights the indispensable role of museums and universities in under- ular data? Systematic Biology 50:444–453. standing species and the ecosystems in which they live (McLean AmphibiaWeb. 2017. AmphibiaWeb. University of California, et al. 2015). As our planet changes, the need to support geographi- Berkeley. http://amphibiaweb.org. Accessed 12 May 2017. cally broad and site-intensive biological archives only grows in rel- Asher, R. J., and K. M. Helgen. 2010. Nomenclature and placental mammal phylogeny. BMC Evolutionary Biology 10:102. evance. Collections represent time series of change in biodiversity Asher, R. J., M. J. Novacek, and J. H. Geisler. 2003. Relationships and often harbor undiscovered species (e.g., Helgen et al. 2013), of endemic African mammals and their fossil relatives based on including those vulnerable or already extinct. morphological and molecular evidence. Journal of Mammalian Acting under the supervision of the American Society Evolution 10:131–194. of Mammalogists’ Biodiversity Committee, the MDD has Belfiore, N. M., L. Liu, and C. Moritz. 2008. Multilocus phylo- a 2018–2020 plan to further integrate synonym data, track genetics of a rapid radiation in the genus Thomomys (Rodentia: Holocene-extinct taxa, and add links to outside data sources. Geomyidae). Systematic Biology 57:294–310. While full synonymies are not feasible, inclusion of common Bercovitch, F. B., et al. 2017. How many species of giraffe are synonyms will facilitate tracking taxonomic changes through there? Current Biology 27:R136–R137. time, especially within controversial groups (e.g., Artiodactyla Boubli, J. P., A. B. Rylands, I. P. Farias, M. E. Alfaro, and J. and Perissodactyla—Groves and Grubb 2011). Controversial L. Alfaro. 2012. Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys. taxonomic assignments also will be “flagged” as tentative American Journal of Primatology 74:381–393. or pending further scientific investigation. The MDD aims Carleton, M. D., J. C. Kerbis Peterhans, and W. T. Stanley. 2006. to link taxon entries to a variety of relevant per-species and Review of the Hylomyscus denniae group (Rodentia: Muridae) per-higher taxon data pages on other web platforms, includ- in Eastern Africa, with comments on the generic allocation of ing geographic range maps, trait database entries, museum Epimys endorobae Heller. Proceedings of the Biological Society of records, genetic resources, and other ecological information. Washington 119:293–325. Mammalian Species accounts, published by the American Castiglia, R., F. Annesi, G. Amori, E. Solano, and G. Aloise. 2017. Society of Mammalogists since 1969 and consisting of over The phylogeography of Crocidura suaveolens from southern Italy 950 species-level treatments, will be linked to relevant MDD reveals the absence of an endemic lineage and supports a Trans- species pages, including synonym-based links. In this manner, Adriatic connection with the Balkanic refugium. Hystrix, the the MDD’s efforts parallel initiatives in other vertebrate taxa Italian Journal of Mammalogy 28:1–3. Ceballos, G., P. R. Ehrlich, and R. Dirzo. 2017. Biological anni- to digitize taxonomic resources (amphibians—AmphibiaWeb hilation via the ongoing sixth mass extinction signaled by verte- 2017; Amphibian Species of the World—Frost 2017; birds: brate population losses and declines. Proceedings of the National Avibase—LePage et al. 2014; IOC World Bird List—Gill Academy of Sciences 114: E6089–E6096. and Donsker 2017; the Handbook of the Birds of the World Cooke, S. B., L. M. Dávalos, A. M. Mychajliw, S. T. Turvey, and Alive—del Hoyo et al. 2017; non-avian reptiles, turtles, croco- N. S. Upham. 2017. Anthropogenic extinction dominates Holocene diles, and tuatara—Uetz et al. 2016; and bony fish: FishBase— declines of West Indian mammals. Annual Review of Ecology, Froese and Pauly 2017; Catalog of Fishes—Eschmeyer et al. Evolution, and Systematics 48:301–327. 2017). The new mammalian taxonomic database summarized Cozzuol, M. A., et al. 2013. A new species of tapir from the Amazon. herein aims to advance the study of mammals while bringing Journal of Mammalogy 94:1331–1345. it to par with the digital resources available in other tetrapod Davenport, T. R., et al. 2006. A new genus of African monkey, clades, to the benefit of future mammalogists and non-mam- Rungwecebus: morphology, ecology, and molecular phylogenetics. Science 312:1378–1381. malogists alike. Dawson, M., C. Marivaux, C.-K. Li, K. C. Beard, and G. Metais. 2006. Laonastes and the “Lazarus effect” in recent mammals. Science 311:1456–1458. Acknowledgments de Queiroz, K. 2007. Species concepts and species delimitation. We are grateful to the American Society of Mammalogists for Systematic Biology 56:879–886. funding this project, and as well as for logistical support from the del Hoyo, J., A. Elliott, J. Sargatal, D. A. Christie, and E. de NSF VertLife Terrestrial grant (#1441737). We thank J. Cook, Juana. 2017. Handbook of the birds of the world alive. D. Wilson, B. Patterson, W. Jetz, M. Koo, J. Esselstyn, E. Lacey, Edicions, Barcelona, Spain. http://www.hbw.com/. Accessed 12 D. Huckaby, L. Ruedas, R. Norris, D. Reeder, R. Guralnick, J. May 2017. Patton, E. Heske, and other members of the ASM Biodiversity Department of the Interior, U.S. Fish and Wildlife Service. 1973. Committee for advice, support, and input about this initiative. U.S. Endangered Species Act of 1973. http://www.nmfs.noaa.gov/ pr/laws/esa/text.htm. Accessed 12 May 2017. Douady, C. J., et al. 2002. Molecular phylogenetic evidence con- Supplementary Data firming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews. Molecular Phylogenetics and Evolution Supplementary data are available at Journal of Mammalogy online. 25:200–209. Supplementary Data SD1.— Details of the full Mammal Dumas, F., and S. Mazzoleni. 2017. Neotropical primate evolution Diversity Database (MDD) version 1 taxonomy, including and phylogenetic reconstruction using chromosomal data. The associated citations and geographic regions. European Zoological Journal 84:1–18.

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 12 JOURNAL OF MAMMALOGY

Dumbacher, J. P. 2016. Petrosaltator gen. nov., a new genus Helgen, K. M., et al. 2013. Taxonomic revision of the olingos replacement for the North African sengi Elephantulus rozeti (), with description of a new species, the Olinguito. (Macroscelidea; Macroscelididae). Zootaxa 4136:567–579. ZooKeys 324:1–83. Emmons, L. H., Y. L. R. Leite, and J. L. Patton. 2015. Family Helgen, K. M., F. R. Cole, L. E. Helgen, and D. E. Wilson. Echimyidae. Mammals of South America. Vol. 2 (J. L. Patton, U. 2009. Generic revision in the holarctic ground squirrel genus F. J. Pardiñas, and G. D’Elía, eds.). University of Chicago Press, Spermophilus. Journal of Mammalogy 90:270–305. Chicago, Illinois; 877–1022. Hill, J. E. 1990. A memoir and bibliography of Michael Rogers Eschmeyer, W. N., R. Fricke, and R. van der Laan. 2017. Catalog Oldfield Thomas, F.R.S. Bulletin of the British Museum (Natural of fishes: genera, species, references. https://www.calacademy.org/ History). Historical Series 18:25–113. scientists/projects/catalog-of-fishes. Accessed 12 May 2017. Hinchliff, C. E., et al. 2015. Synthesis of phylogeny and taxon- Esselstyn, J. A., A. S. Achmadi, and K. C. Rowe. 2012. Evolutionary omy into a comprehensive tree of life. Proceedings of the National novelty in a rat with no molars. Biology Letters 8:990–993. Academy of Sciences 112:12764–12769. Esselstyn, J. A., Maharadatunkamsi, A. S. Achmadi, C. D. Siler, Honacki, J. H., K. E. Kinman, and J. W. Koeppl. 1982. Mammal and B. J. Evans. 2013. Carving out turf in a biodiversity hotspot: species of the world: a taxonomic and geographic reference. 1st multiple, previously unrecognized shrew species co-occur on Java ed. Allen Press and the Association of Systematics Collections, Island, Indonesia. Molecular Ecology 22:4972–4987. Lawrence, Kansas. Fabre, P. H., et al. 2017. Mitogenomic phylogeny, diversifica- IUCN. 2017. The IUCN Red List of Threatened Species. Version tion, and biogeography of South American spiny rats. Molecular 2017-1. www.iucnredlist.org. Accessed 28 June 2017. Biology and Evolution 34:613–633. Jackson, S. M., and C. Groves. 2015. Taxonomy of Australian mam- Flannery, T. 2012. Among the islands: adventures in the Pacific. mals. CSIRO Publishing, Clayton South, Victoria, Australia. Grove/Atlantic, Inc., New York City, New York. Jarzyna, M. A., and W. Jetz. 2016. Detecting the multiple facets of Foley, N. M., et al. 2015. How and why overcome the impediments biodiversity. Trends in Ecology & Evolution 31:527–538. to resolution: lessons from rhinolophid and hipposiderid bats. Jenkins, P. D., C. W. Kilpatrick, M. F. Robinson, and R. J. Timmins. Molecular Biology and Evolution 32:313–333. 2005. Morphological and molecular investigations of a new family, Froese, R., and D. Pauly. 2017. FishBase. www.FishBase.org. genus and species of rodent (Mammalia: Rodentia: Hystricognatha) Accessed 12 May 2017. from Lao PDR. Systematics and Biodiversity 2:419–454. Frost, D. R. 2017. Amphibian species of the world: an online ref- Kingdon, J., D. Happold, T. Butynski, M. Hoffmann, M. Happold, and erence. Version 6.0. American Museum of Natural History, J. Kalina. 2013. Mammals of Africa (Vol. 1–6). A&C Black, New York. New York. http://research.amnh.org/vz/herpetology/amphibia/. Larsen, P. A., M. R. Marchán-Rivadeneira, and R. J. Baker. 2010. Accessed 28 June 2017. Natural hybridization generates mammalian lineage with species Gardner, A. L. 2007. Mammals of South America: volume 1: marsu- characteristics. Proceedings of the National Academy of Sciences pials, xenarthrans, shrews, and bats. University of Chicago Press, 107:11447–11452. Chicago, Illinois. Lebedev, V. S., A. A. Bannikova, J. Pisano, J. R. Michaux, and G. Gatesy, J., P. O’Grady, and R. H. Baker. 1999. Corroboration among I. Shenbrot. 2013. Molecular phylogeny and systematics of data sets in simultaneous analysis: hidden support for phyloge- Dipodoidea: a test of morphology‐based hypotheses. Zoologica netic relationships among higher level artiodactyl taxa. Cladistics Scripta 42:231–249. 15:271–313. Lei, R., et al. 2014. Revision of Madagascar’s dwarf lemurs Gaudin, T. J. 2004. Phylogenetic relationships among sloths (Cheirogaleidae: Cheirogaleus): designation of species, candidate (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. species status and geographic boundaries based on molecular and Zoological Journal of the Linnean Society 140:255–305. morphological data. Primate Conservation:9–35. Gill, F., and D. Donsker. 2017. IOC World Bird List (v 7.3). www. Lepage, D., G. Vaidya, and R. Guralnick. 2014. Avibase - a database worldbirdnames.org. Accessed 12 May 2017. system for managing and organizing taxonomic concepts. ZooKeys Gregorin, R., and A. D. Ditchfield. 2005. New genus and species 420:117–135. of -feeding bat in the tribe Lonchophyllini (Phyllostomidae: Linnaeus, C. 1758. Systema naturae per regna tria naturae: secundum Glossophaginae) from northeastern Brazil. Journal of Mammalogy classes, ordines, genera, species, cum characteribus, differentiis, 86:403–414. synonymis, locis. Laurentius Salvius, Stockholm, Sweeden. Groves, C. P. 2007a. Speciation and biogeography of Vietnam’s pri- Lorenzen, E. D., R. Heller, and H. R. Siegismund. 2012. Comparative mates. Vietnamese Journal of Primatology 1:27–40. phylogeography of African savannah ungulates. Molecular Ecology Groves, C. P. 2007b. The endemic Uganda mangabey, Lophocebus 21:3656–3670. ugandae, and other members of the albigena-group (Lophocebus). Louis, E. E., Jr., et al. 2006. Molecular and morphological analyses Primate Conservation 22:123–128. of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) Groves, C., and P. Grubb. 2011. Ungulate taxonomy. Johns Hopkins reveals 11 previously unrecognized species. Special Publications University Press/Bucknell University, Baltimore, Maryland. of the Museum of Texas Tech University 49:1–47. Harley, E. H., M. De Waal, S. Murray, and C. O’Ryan. 2016. Madsen, O., M. Scally, C. J. Douady, and D. J. Kao. 2001. Parallel Comparison of whole mitochondrial genome sequences of north- adaptive radiations in two major clades of placental mammals. ern and southern white rhinoceroses (Ceratotherium simum): the Nature 409:610. conservation consequences of species definitions. Conservation Marsh, L. K. 2014. A taxonomic revision of the saki monkeys, Genetics 17:1285–1291. Pithecia Desmarest, 1804. Neotropical Primates 21:1–165. Hedges, S. B., J. Marin, M. Suleski, M. Paymer, and S. Kumar. Matson, J. O., and N. Ordóñez-Garza. 2017. The taxonomic sta- 2015. Tree of life reveals clock-like speciation and diversification. tus of long-tailed shrews (Mammalia: genus Sorex) from Nuclear Molecular Biology and Evolution 32:835–845. Central America. Zootaxa 4236:461–483.

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 INVITED PAPER—MAMMALIAN SPECIES DIVERSITY 13

McKenna, M. C., and S. K. Bell. 1997. Classification of mammals: Percequillo, A. R., M. Weksler, and L. P. Costa. 2011. A new genus above the species level. Columbia University Press, New York City, and species of rodent from the Brazilian Atlantic (Rodentia: New York. Cricetidae: Sigmodontinae: Oryzomyini), with comments on ory- McLean, B. S., et al. 2015. Natural history collections-based zomyine biogeography. Zoological Journal of the Linnean Society research: progress, promise, and best practices. Journal of 161:357–390. Mammalogy 97:287–297. Rabosky, D. L., G. J. Slater, and M. E. Alfaro. 2012. Clade age and Meredith, R. W., et al. 2011. Impacts of the Cretaceous terrestrial species richness are decoupled across the eukaryotic tree of life. revolution and KPg extinction on mammal diversification. Science PLoS Biology 10:e1001381. 334:521–524. Rausch, R. L., J. E. Feagin, and V. R. Rausch. 2007. Sorex rohweri Miller, W., et al. 2012. Polar and brown genomes reveal sp. nov. (Mammalia, Soricidae) from northwestern North America. ancient admixture and demographic footprints of past cli- Mammalian Biology-Zeitschrift für Säugetierkunde 72:93–105. mate change. Proceedings of the National Academy of Sciences Reeder, D. M., and K. M. Helgen. 2007. Global trends and biases 109:E2382–E2390. in new mammal species discoveries. Occasional Papers of the Mittermeier, R. A., A. B. Rylands, and D. E. Wilson. 2013. Museum of Texas Tech University 269:1–35. Handbook of the mammals of the world, volume 3: Primates. Lynx Rowe, K. C., A. S. Achmadi, and J. A. Esselstyn. 2016. A new Edicions, Barcelona, Spain. genus and species of omnivorous rodent (Muridae: Murinae) from Monadjem, A., P. J. Taylor, C. Denys, and F. P. Cotterill. 2015. Sulawesi, nested within a clade of endemic . Journal of Rodents of sub-Saharan Africa: a biogeographic and taxonomic Mammalogy 97:978–991. synthesis. Walter de Gruyter GmbH & Co. KG, Berlin, Germany. Ruedi, M., and F. Mayer. 2001. Molecular systematics of bats of the Montagnon, D., B. Ravaoarimanana, B. Rakotosamimanana, and genus Myotis (Vespertilionidae) suggests deterministic ecomorphologi- Y. Rumpler. 2001. Ancient DNA from Megaladapis edwardsi cal convergences. Molecular Phylogenetics and Evolution 21:436–448. (Malagasy subfossil): preliminary results using partial cytochrome Schneider, H., and I. Sampaio. 2015. The systematics and evolution b sequence. Folia Primatologica 72:30–32. of new world primates - a review. Molecular Phylogenetics and Muldoon, K. M. 2010. Paleoenvironment of Ankilitelo Cave Evolution 82:348–357. (late Holocene, southwestern Madagascar): implications for Solari, S., and R. J. Baker. 2007. Mammal species of the world: a the extinction of giant lemurs. Journal of Human Evolution 58: taxonomic reference by D. E. Wilson; D. M. Reeder. Journal of 338–352. Mammalogy 88:824–839. Mullis, K. B., H. A. Erlich, N. Arnheim, G. T. Horn, R. K. Saiki, and Teta, P., C. Cañón, B. D. Patterson, and U. F. Pardiñas. 2016. S. J. Scharf. 1989. Process for amplifying, detecting, and/or clon- Phylogeny of the tribe Abrotrichini (Cricetidae, Sigmodontinae): ing nucleic acid sequences. Patent US4683195 A. integrating morphological and molecular evidence into a new clas- Murphy, W. J., E. Eizirik, W. E. Johnson, and Y. P. Zhang. 2001. sification. Cladistics 33:153–182. Molecular phylogenetics and the origins of placental mammals. Uetz, P., P. Freed, and J. Hošek. 2016. The reptile database. http:// Nature 409:614–618. reptile-database.org. Accessed 12 May 2017. Olson, D. M., et al. 2001. Terrestrial ecoregions of the world: a new vonHoldt, B. M., et al. 2016. Whole-genome sequence analysis map of life on Earth. Bioscience 51:933–938. shows that two endemic species of North American wolf are admix- Olson, D. M., and E. Dinerstein. 1998. The Global 200: a representa- tures of the coyote and gray wolf. Science Advances 2:e1501714. tion approach to conserving the Earth’s most biologically valuable Voss, R. S., K. M. Helgen, and S. A. Jansa. 2014. Extraordinary ecoregions. Conservation Biology 12:502–515. claims require extraordinary evidence: a comment on Cozzuol Osterholz, M., L. Walter, and C. Roos. 2008. Phylogenetic po- et al. (2013). Journal of Mammalogy 95:893–898. sition of the langur genera Semnopithecus and Trachypithecus Weksler, M., A. R. Percequillo, and R. S. Voss. 2006. Ten new gen- among Asian colobines, and genus affiliations of their species era of oryzomyine rodents (Cricetidae: Sigmodontinae). American groups. BMC Evolutionary Biology 8:58. Museum Novitates 3537:1–29. Pardiñas, U. F., L. Geise, K. Ventura, and G. Lessa. 2016. A new Wilson, D. E., T. E. Lacher, Jr., and R. A. Mittermeier. 2016. genus for Habrothrix angustidens and Akodon serrensis (Rodentia, Handbook of the mammals of the world, volume 6: lagomorphs Cricetidae): again paleontology meets neontology in the legacy of and rodents I. Lynx Edicions, Barcelona, Spain. Lund. Mastozoología Neotropical 23:93–115. Wilson, D. E., and R. A. Mittermeier. 2009. Handbook of the mammals Pascual, U., et al. 2017. Valuing nature’s contributions to people: the of the world, volume 1: carnivores. Lynx Edicions, Barcelona, Spain. IPBES approach. Current Opinion in Environmental Sustainability Wilson, D. E., and R. A. Mittermeier. 2011. Handbook of the mam- 26:7–16. mals of the world, volume 2: hoofed mammals. Lynx Edicions, Patterson, B. D. 1996. The “species alias” problem. Nature Barcelona, Spain. 380:588–589. Wilson, D. E., and R. A. Mittermeier. 2014. Handbook of the mammals Patterson, B. D. 2001. Fathoming tropical biodiversity: the continu- of the world, volume 4: sea mammals. Lynx Edicions, Barcelona, Spain. ing discovery of Neotropical mammals. Diversity and Distributions Wilson, D. E., and R. A. Mittermeier. 2015. Handbook of the mam- 7:191–196. mals of the world, volume 5: monotremes and marsupials. Lynx Patterson, B. D., and N. S. Upham. 2014. A newly recognized fam- Edicions, Barcelona, Spain. ily from the Horn of Africa, the Heterocephalidae (Rodentia: Wilson, D. E., and D. M. Reeder. 1993. Mammal species of the Ctenohystrica). Zoological Journal of the Linnean Society world: a taxonomic and geographic reference. 2nd ed. Smithsonian 172:942–963. Institution Press, Washington, D.C. Patton, J. L., U. F. J. Pardiñas, and G. D’Elías. 2015. Mammals of Wilson, D. E., and D. M. Reeder. 2005. Mammal species of the world: South America, volume 2: rodents. University of Chicago Press, a taxonomic and geographic reference. 3rd ed. Johns Hopkins Chicago, Illinois. University Press/Bucknell University, Baltimore, Maryland.

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 14 JOURNAL OF MAMMALOGY

Woodman, N., R. M. Timm, and G. R. Graves. 2006. Characters Zachos, F. E., et al. 2013. Species inflation and taxonomic artefacts— and phylogenetic relationships of nectar-feeding bats, with a critical comment on recent trends in mammalian classification. descriptions of new Lonchophylla from western South America Mammalian Biology-Zeitschrift für Säugetierkunde 78:1–6. (Mammalia: Chiroptera; Phyllostomidae: Lonchophyllini). Proceedings of the Biological Society of Washington 119: Submitted 21 September 2017. Accepted 12 October 2017. 437–476. World Atlas. 2017. Map and details of all 7 continents. www.worl- datlas.com. Accessed 12 May 2017. Associate Editor was Edward Heske.

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/1/4834091 by University of Wyoming Libraries user on 21 August 2018 MTheammals ConqueredThat the New fossils and DNA analyses elucidate the remarkable

70 SCIENTIFIC AMERICAN COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. “They say the sea is cold, but the sea contains the hottest blood of all, and the wildest, the most urgent.”

—D. H. Lawrence, “Whales Weep Not!”

Dawn breaks over the Tethys Sea, 48 million years ago, and the blue- green water sparkles with the day’s first light. But for one small mammal, this new day will end almost as soon as it has started.

ANCIENT WHALE Rodhocetus (right and left front) feasts on the bounty of the sea, while Ambulocetus (rear) attacks a small land mammal some 48 million years ago in what is now Pakistan.

Seas By Kate Wong evolutionary history of whales

SCIENTIFIC AMERICAN 71 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. Tapir-like Eotitanops has wandered perilously close to the Darwin, these air-breathing, warm-blooded that nurse water’s edge, ignoring its mother’s warning call. For the brute their young with milk distinctly grouped with mammals. And lurking motionless among the mangroves, the opportunity is because ancestral mammals lived on land, it stood to reason simply too good to pass up. It lunges landward, propelled by that whales ultimately descended from a terrestrial ancestor. powerful hind limbs, and sinks its formidable teeth into the calf, Exactly how that might have happened, however, eluded schol- dragging it back into the surf. The victim’s frantic struggling ars. For his part, Darwin noted in On the Origin of Species that subsides as it drowns, trapped in the viselike jaws of its cap- a bear swimming with its mouth agape to catch was a tor. Victorious, the beast shambles out of the water to devour plausible evolutionary starting point for whales. But the propo- its kill on terra firma. At first glance, this fearsome predator re- sition attracted so much ridicule that in later editions of the sembles a crocodile, with its squat legs, stout tail, long snout book he said just that such a bear was “almost like a whale.” and eyes that sit high on its skull. But on closer inspection, it The fossil record of cetaceans did little to advance the study has not armor but , not claws but hooves. And the cusps on of whale origins. Of the few remains known, none were suffi- its teeth clearly identify it not as a reptile but as a mammal. In ciently complete or primitive to throw much light on the mat- fact, this improbable creature is Ambulocetus, an early whale, ter. And further analyses of the bizarre anatomy of living and one of a series of intermediates linking the land-dwelling whales led only to more scientific head scratching. Thus, even ancestors of cetaceans to the 80 or so species of whales, dol- a century after Darwin, these aquatic mammals remained an phins and porpoises that rule the oceans today. evolutionary enigma. In fact, in his 1945 classification of mam- Until recently, the emergence of whales was one of the most mals, famed paleontologist George Gaylord Simpson noted intractable mysteries facing evolutionary biologists. Lacking fur that whales had evolved in the oceans for so long that nothing and hind limbs and unable to go ashore for so much as a sip of informative about their ancestry remained. Calling them “on freshwater, living cetaceans represent a dramatic departure the whole, the most peculiar and aberrant of mammals,” he in- from the mammalian norm. Indeed, their piscine form led Her- serted cetaceans arbitrarily among the other orders. Where man Melville in 1851 to describe Moby Dick and his fellow whales belonged in the mammalian family tree and how they whales as fishes. But to 19th-century naturalists such as Charles took to the seas defied explanation, it seemed. Over the past two decades, however, many of the pieces of this once imponderable puzzle have fallen into place. Paleon- Guide to Terminology tologists have uncovered a wealth of whale fossils spanning the CETACEA is the order of mammals that comprises living Eocene epoch, the time between 55 million and 34 million years whales, dolphins and porpoises and their extinct ancestors, ago when archaic whales, or archaeocetes, made their transi- the archaeocetes. Living members fall into two suborders: the tion from land to sea. They have also unearthed some clues odontocetes, or toothed whales, including sperm whales, pilot from the ensuing Oligocene, when the modern suborders of whales, belugas, and all dolphins and porpoises; and the cetaceans—the mysticetes (baleen whales) and the odontocetes mysticetes, or baleen whales, including blue whales and fin (toothed whales)—arose. That fossil material, along with analy- whales. The term “whale” is often used to refer to all cetaceans. ses of DNA from living animals, has enabled scientists to paint a detailed picture of when, where and how whales evolved from MESONYCHIDS are a group of primitive hoofed, wolflike their terrestrial forebears. Today their transformation—from mammals once widely thought to have given rise to whales. landlubbers to Leviathans—stands as one of the most profound ARTIODACTYLA is the order of even-toed, hoofed mammals evolutionary metamorphoses on record. that includes camels; ruminants such as cows; hippos; and, most researchers now agree, whales. Evolving Ideas

AT AROUND THE SAME TIME that Simpson declared the ) EOCENE is the epoch between 55 million and 34 million relationship of whales to other mammals undecipherable on the years ago, during which early whales made their transition basis of anatomy, a new comparative approach emerged, one from land to sea. that looked at antibody-antigen reactions in living animals. In OLIGOCENE is the epoch between 34 million and 24 million response to Simpson’s assertion, Alan Boyden of Rutgers Uni- preceding pages years ago, during which odontocetes and mysticetes versity and a colleague applied the technique to the whale ques- evolved from their archaeocete ancestors. tion. Their results showed convincingly that among living ani-

mals, whales are most closely related to the even-toed hoofed KAREN CARR (

72 SCIENTIFIC AMERICAN MAY 2002 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. THE WHALE’S CHANGING WORLD

TETHY S S EA

PROTO-INDIA

PROTO- AUSTRALIA

50 Million Years Ago Present FOSSIL LOCATIONS PAKICETIDS AMBULOCETIDS PROTOCETIDS REMINGTONOCETIDS BASILOSAURIDS LLANOCETUS

t might seem odd that 300 million years after vertebrates climate systems brought about radical changes in the first established a toehold on land, some returned to the sea. quantity and distribution of nutrients in the sea, generating IBut the setting in which early whales evolved offers hints as a whole new set of ecological opportunities for the cetaceans. to what lured them back to the water. For much of the Eocene As posited by paleontologist Ewan Fordyce of the University epoch (roughly between 55 million and 34 million years ago), of Otago in New Zealand, that set the stage for the a sea called Tethys, after a goddess of Greek mythology, replacement of the archaeocetes by the odontocetes and stretched from Spain to Indonesia. Although the continents and mysticetes (toothed and baleen whales, respectively). The ocean plates we know now had taken shape, India was still earliest known link between archaeocetes and the modern adrift, Australia hadn’t yet fully separated from Antarctica, and cetacean orders, Fordyce says, is Llanocetus, a 34-million- great swaths of Africa and Eurasia lay submerged under year-old protobaleen whale from Antarctica that may well have Tethys. Those shallow, warm waters incubated abundant trawled for krill in the chilly Antarctic waters, just as living nutrients and teemed with fish. Furthermore, the space baleen whales do. Odontocetes arose at around the same vacated by the plesiosaurs, mosasaurs and other large marine time, he adds, specializing to become echolocators that could reptiles that perished along with the dinosaurs created room hunt in the deep. for new top predators (although sharks and crocodiles still Unfortunately, fossils documenting the origins of provided a healthy dose of competition). It is difficult to mysticetes and odontocetes are vanishingly rare. Low sea imagine a more enticing invitation to aquatic life for a mammal. levels during the middle Oligocene exposed most potential During the Oligocene epoch that followed, sea levels sank whale-bearing sediments from the early Oligocene to erosive and India docked with the rest of Asia, forming the crumpled winds and rains, making that period largely “a fossil interface we know as the Himalayas. More important, wasteland,” says paleontologist Mark Uhen of the Cranbrook University of Michigan paleontologist Philip Gingerich notes, Institute of Science in Bloomfield Hills, Mich. The later fossil Australia and Antarctica divorced, opening up the Southern record clearly shows, however, that shortly after, by about 30 Ocean and creating a south circumpolar current that million years ago, the baleen and toothed whales had eventually transformed the balmy Eocene earth into the ice- diversified into many of the cetacean families that reign over capped planet we inhabit today. The modern current and the oceans today. —K.W.

mammals, or artiodactyls, a group whose members include Leigh Van Valen, then at the American Museum of Natural camels, hippopotamuses, pigs and ruminants such as cows. History in New York City, discovered striking resemblances Still, the exact nature of that relationship remained unclear. between the three-cusped teeth of the few known fossil whales Were whales themselves artiodactyls? Or did they occupy their and those of a group of meat-eating condylarths called mesony- own branch of the mammalian family tree, linked to the artio- chids. Likewise, he found shared dental characteristics between dactyl branch via an ancient common ancestor? artiodactyls and another group of condylarths, the arctocy- Support for the latter interpretation came in the 1960s, onids, close relatives of the mesonychids. Van Valen conclud- from studies of primitive hoofed mammals known as condy- ed that whales descended from the carnivorous, wolflike larths that had not yet evolved the specialized characteristics of mesonychids and thus were linked to artiodactyls through the

SARA CHEN AND EDWARD BELL artiodactyls or the other mammalian orders. Paleontologist condylarths.

www.sciam.com SCIENTIFIC AMERICAN 73 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. 3 meters RODHOCETUS 4.5 meters DORUDON 4.15 meters AMBULOCETUS 1.75 meters PAKICETUS CETACEAN RELATIONS CETACEAN characteristics ofartiodactylankles,suggestingthatwhalesare The anklebonesofthoseancientwhalesbearthedistinctive whales, nowseemsunlikelyinlightofnewfossilwhalediscoveries. wolflike beastsknownasmesonychidsaretheclosestrelativesof ( various hypothesesoftherelationshipwhalestoothermammals PORTIA SLOAN AND EDWARD BELL family orsubfamilyaredepicted( extinct archaeocetes.Representativemembersofeacharchaeocete suborders ofwhales,theodontocetesandmysticetes,from FAMILY TREEOFCETACEANS right ). Theoldmesonychidhypothesis,whichpositsthatextinct 1.75 meters KUTCHICETUS CETACEA 18.2 meters BASILOSAURUS shows thedescentoftwomodern left ). Branchingdiagramsillustrate 55 54 35 40 45 50 55 Millions ofYearsAgo COPYRIGHT 2002SCIENTIFIC AMERICAN,INC. PAKICETIDAE AMBULOCETIDAE REMINGTONOCETIDAE PROTOCETIDAE traits thatcharacterizeallknownartiodactyls. they currentlyreside.Ifso,wouldhavetolosttheankle artiodactyl order,insteadoftheextinctorderCondylarthra,inwhich still bethewhale’sclosestkinifthey,too,wereincludedin the newmesonychidhypothesis,proposesthatmesonychidscould however, remainstobeseen.Afourthscenario,denotedhereas Whether thefossilrecordcansupporthippopotamidhypothesis, related tohippopotamusesthananyotherartiodactylgroup. hypothesis. Molecularstudiesindicatethatwhalesaremoreclosely themselves artiodactyls,asenvisionedbytheartiodactyl BASILOSAURIDAE DORUDONTINAE BASILOSAURINAE EO RISHIPPOS WHALES ARTIOS MESOS RISHPO MESOS WHALES HIPPOS ARTIOS HIPPOS WHALES ARTIOS MESOS MESOS WHALES HIPPOS ARTIOS MESOS =MESONYCHIDS ARTIOS =ARTIODACTYLS OTHER THANHIPPOS HIPPO MYSTICETES ODONTOCETES S =HIPPOPOTAMIDS OL NEW MESONYCHIDNEW HYPOTHESIS HIP ARTIODACTYL HYPOTHESIS D MESONYCHID HYPOTHESIS POPOTAMID HYPOTHESIS — K.W. Walking Whales however. By 1983 Gingerich was no longer able to work there A DECADE OR SO PASSED before paleontologists finally be- because of the Soviet Union’s invasion of Afghanistan. He de- gan unearthing fossils close enough to the evolutionary branch- cided to cast his net in Egypt instead, journeying some 95 miles ing point of whales to address Van Valen’s mesonychid hy- southwest of Cairo to the Western Desert’s Zeuglodon Valley, pothesis. Even then the significance of these finds took a while so named for early 20th-century reports of fossils of archaic to sink in. It started when University of Michigan paleontolo- whales—or zeuglodons, as they were then known—in the area. gist Philip Gingerich went to Pakistan in 1977 in search of Like Pakistan, much of Egypt once lay submerged under Eocene land mammals, visiting an area previously reported to Tethys. Today the skeletons of creatures that swam in that an- shelter such remains. The expedition proved disappointing be- cient sea lie entombed in sandstone. After several field seasons, cause the spot turned out to contain only marine fossils. Find- Gingerich and his crew hit pay dirt: tiny hind limbs belonging ing traces of ancient ocean life in Pakistan, far from the coun- to a 60-foot-long sea snake of a whale known as Basilosaurus try’s modern coast, is not surprising: during the Eocene, the vast and the first evidence of cetacean feet. Tethys Sea periodically covered great swaths of what is now the Earlier finds of Basilosaurus, a fully aquatic monster that Indian subcontinent [see box on page 73]. Intriguingly, though, slithered through the seas between some 40 million and 37 mil- the team discovered among those ancient fish and snail rem- lion years ago, preserved only a partial femur, which its discov- nants two pelvis fragments that appeared to have come from erers interpreted as vestigial. But the well-formed legs and feet relatively large, walking beasts. “We joked about walking revealed by this discovery hinted at functionality. Although at whales,” Gingerich recalls with a chuckle. “It was unthink- less than half a meter in length the diminutive limbs probably able.” Curious as the pelvis pieces were, the only fossil collect- would not have assisted Basilosaurus in swimming and certain- ed during that field season that seemed important at the time ly would not have enabled it to walk on land, they may well have was a primitive artiodactyl jaw that had turned up in another helped guide the beast’s serpentine body during the difficult ac- part of the country. tivity of aquatic mating. Whatever their purpose, if any, the lit- Two years later, in the Himalayan foothills of northern Pak- tle legs had big implications. “I immediately thought, we’re 10 istan, Gingerich’s team found another weird whale clue: a par- million years after Pakicetus,” Gingerich recounts excitedly. “If tial braincase from a wolf-size creature—found in the company these things still have feet and toes, we’ve got 10 million years of 50-million-year-old land mammal remains—that bore some of history to look at.” Suddenly, the walking whales they had distinctive cetacean characteristics. All modern whales have fea- scoffed at in Pakistan seemed entirely plausible. tures in their ears that do not appear in any other vertebrates. Just such a remarkable creature came to light in 1992. A Although the fossil skull lacked the anatomy necessary for hear- team led by J.G.M. (Hans) Thewissen of the Northeastern Ohio ing directionally in water (a critical skill for living whales), it Universities College of Medicine recovered from 48-million- clearly had the diagnostic cetacean ear traits. The team had dis- year-old marine rocks in northern Pakistan a nearly complete covered the oldest and most primitive whale then known—one skeleton of a perfect intermediate between modern whales and that must have spent some, if not most, of its time on land. Gin- their terrestrial ancestors. Its large feet and powerful tail be- gerich christened the creature Pakicetus for its place of origin spoke strong swimming skills, while its sturdy leg bones and and, thus hooked, began hunting for ancient whales in earnest. mobile elbow and wrist joints suggested an ability to locomote At around the same time, another group recovered addi- on land. He dubbed the Ambulocetus natans, the walk- tional remains of Pakicetus—a lower jaw fragment and some ing and swimming whale. isolated teeth—that bolstered the link to mesonychids through strong dental similarities. With Pakicetus showing up around 50 Shape Shifters million years ago and mesonychids known from around the SINCE THEN, Thewissen, Gingerich and others have unearthed same time in the same part of the world, it looked increasingly a plethora of fossils documenting subsequent stages of the likely that cetaceans had indeed descended from the mesonychids whale’s transition from land to sea. The picture emerging from or something closely related to them. Still, what the earliest those specimens is one in which Ambulocetus and its kin—them- whales looked like from the neck down was a mystery. selves descended from the more terrestrial pakicetids—spawned Further insights from Pakistan would have to wait, needle-nosed beasts known as remingtonocetids and the intre- pid protocetids—the first whales seaworthy enough to fan out from Indo-Pakistan across the globe. From the protocetids arose the dolphinlike dorudontines, the probable progenitors of the snakelike basilosaurines and modern whales [see box on opposite page]. In addition to furnishing supporting branches for the whale family tree, these dis- coveries have enabled researchers to chart many of the spectacular anatomical and physiological changes that allowed cetaceans to establish permanent residency in the

www.sciam.com SCIENTIFIC AMERICAN 75 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. BECOMING LEVIATHAN

PAKICETUS AMBULOCETUS

REPRESENTATIVE ARCHAEOCETES in the lineage leading to modern odontocetes and mysticetes trace some of the anatomical changes that enabled these animals to take to the seas (reconstructed bone appears in lavender). In just 15 million years, whales shed their terrestrial trappings and became fully adapted to aquatic life. Notably, the hind limbs diminished, the forelimbs transformed into flippers, and the vertebral column evolved to permit tail-powered swimming. Meanwhile the skull changed to enable underwater hearing, the nasal opening moved backward to the top of the skull, and the teeth simplified into pegs for grasping instead of grinding. Later in whale evolution, the mysticetes’ teeth were replaced with baleen. MODERN MYSTICETE ocean realm. Some of the earliest of these adaptations to emerge, for? Thewissen suspects that much as turtles hear by picking up as Pakicetus shows, are those related to hearing. Sound travels vibrations from the ground through their shields, Pakicetus may differently in water than it does in air. Whereas the ears of hu- have employed its bullae to pick up ground-borne sounds. Tak- mans and other land-dwelling animals have delicate, flat ear- ing new postcranial evidence into consideration along with the drums, or tympanic membranes, for receiving airborne sound, ear morphology, he envisions Pakicetus as an ambush predator modern whales have thick, elongate tympanic ligaments that that may have lurked around shallow rivers, head to the ground, cannot receive sound. Instead a bone called the bulla, which in preying on animals that came to drink. Ambulocetus is even whales has become quite dense and is therefore capable of trans- more likely to have used such inertial hearing, Thewissen says, mitting sound coming from a denser medium to deeper parts because it had the beginnings of a channel linking jaw and ear. ) of the ear, takes on that function. The Pakicetus bulla shows By resting its jaw on the ground—a strategy seen in modern croc- some modification in that direction, but the animal retained a odiles—Ambulocetus could have listened for approaching prey. land mammal–like eardrum that could not work in water. The same features that allowed early whales to receive sounds photograph What, then, might Pakicetus have used its thickened bullae from soil, he surmises, preadapted them to hearing in the water. Zhe-Xi Luo of the Carnegie Museum of Natural History in Pittsburgh has shown that by the time of the basilosaurines and DORUDON, a 4.5-meter-long, dolphinlike archaeocete that patrolled the seas between roughly 40 million and 37 million years ago, may be dorudontines, the first fully aquatic whales, the ropelike tym- the ancestor of modern whales. panic ligament had probably already evolved. Additionally, air ); UNIVERSITY OF MICHIGAN EXHIBIT MUSEUM NATURAL HISTORY ( illustrations PORTIA SLOAN (

76 SCIENTIFIC AMERICAN MAY 2002 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. RODHOCETUS DORUDON

MODERN ODONTOCETE

sinuses, presumably filled with spongelike tissues, had formed tean shift are those that produced its streamlined shape and un- around the middle ear, offering better sound resolution and di- matched swimming abilities. Not surprisingly, some bizarre am- rectional cues for underwater hearing. Meanwhile, with the ex- phibious forms resulted along the way. Ambulocetus, for one, re- ternal ear canal closed off (a prerequisite for deep-sea diving), tained the flexible shoulder, elbow, wrist and finger joints of its he adds, the lower jaw was taking on an increasingly important terrestrial ancestors and had a pelvis capable of supporting its auditory role, developing a fat-filled canal capable of conduct- weight on land. Yet the creature’s disproportionately large hind ing sound back to the middle ear. limbs and paddlelike feet would have made walking somewhat Later in the evolution of whale hearing, the toothed and awkward. These same features were perfect for paddling around baleen whales parted ways. Whereas the toothed whales evolved in the fish-filled shallows of Tethys, however. the features necessary to produce and receive high-frequency Moving farther out to sea required additional modifications, sounds, enabling echolocation for hunting, the baleen whales many of which appear in the protocetid whales. Studies of one developed the ability to produce and receive very low frequen- member of this group, Rodhocetus, indicate that the lower arm cy sounds, allowing them to communicate with one another over bones were compressed and already on their way to becoming vast distances. Fossil whale ear bones, Luo says, show that by hydrodynamically efficient, says University of Michigan paleon- around 28 million years ago early odontocetes already had some tologist Bill Sanders. The animal’s long, delicate feet were prob- of the bony structures necessary for hearing high-pitched sound ably webbed, like the fins used by scuba divers. Rodhocetus also and were thus capable of at least modest echolocation. The ori- exhibits aquatic adaptations in its pelvis, where fusion between gin of the mysticete’s low-frequency hearing is far murkier, even the vertebrae that form the sacrum is reduced, loosening up the though the fossil evidence of that group now dates back to as lower spine to power tail movement. These features, says Gin- early as 34 million years ago. gerich, whose team discovered the creature, suggest that Rod- Other notable skull changes include movement of the eye hocetus performed a leisurely paddle at the sea surface and sockets from a crocodilelike placement atop the head in Pa- a swift combination of otterlike hind-limb paddling and tail kicetus and Ambulocetus to a lateral position in the more propulsion underwater. When it went ashore to breed or perhaps aquatic protocetids and later whales. And the nasal opening mi- to bask in the sun, he proposes, Rodhocetus probably hitched grated back from the tip of the snout in Pakicetus to the top of itself around somewhat like a modern or . the head in modern cetaceans, forming the blowhole. Whale By the time of the basilosaurines and dorudontines, whales morphed, too, turning the complexly cusped, grind- were fully aquatic. As in modern cetaceans, the shoulder re- ing molars of primitive mammalian ancestors into the simple, mained mobile while the elbow and wrist stiffened, forming flip- pronglike teeth of modern odontocetes, which grasp and swal- pers for steering and balance. Farther back on the skeleton, only low their food without chewing. Mysticetes lost their teeth al- tiny legs remained, and the pelvis had dwindled accordingly. together and developed comblike plates of baleen that hang Analyses of the vertebrae of Dorudon, conducted by Mark D. from their upper jaws and strain plankton from the seawater. Uhen of the Cranbrook Institute of Science in Bloomfield Hills, The most obvious adaptations making up the whale’s pro- Mich., have revealed one tail vertebra with a rounded profile.

www.sciam.com SCIENTIFIC AMERICAN 77 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. Modern whales have a similarly shaped bone, the ball vertebra, known. In fact, a recent discovery made by Lawrence G. Barnes at the base of their fluke, the flat, horizontal structure capping the of the Natural History Museum of Los Angeles County hints at tail. Uhen thus suspects that basilosaurines and dorudontines surprisingly well developed hind limbs in a 27-million-year-old had tail flukes and swam much as modern whales do, using so- baleen whale from Washington State, suggesting that whale legs called caudal oscillation. In this energetically efficient mode of persisted far longer than originally thought. Today, however, locomotion, motion generated at a single point in the vertebral some 50 million years after their quadrupedal ancestors first wad- column powers the tail’s vertical movement through the water, ed into the warm waters of Tethys, whales are singularly sleek. and the fluke generates lift. Their hind limbs have shrunk to externally invisible vestiges, and Exactly when whales lost their legs altogether remains un- the pelvis has diminished to the point of serving merely as an an- chor for a few tiny muscles unrelated to locomotion. WATER, WATER EVERYWHERE Making Waves THE FOSSILS UNCOVERED during the 1980s and 1990s ad- MOST MAMMALS—big ones in particular—cannot live without freshwater. For marine mammals, however, freshwater is vanced researchers’ understanding of whale evolution by leaps difficult to come by. Seals and sea lions obtain most of their and bounds, but all morphological signs still pointed to a water from the fish they eat (some will eat snow to get mesonychid origin. An alternative view of cetacean roots was freshwater), and manatees routinely seek out freshwater from taking wing in genetics laboratories in the U.S., Belgium and rivers. For their part, cetaceans obtain water both from their Japan, however. Molecular biologists, having developed so- food and from sips of the briny deep. phisticated techniques for analyzing the DNA of living creatures, When did whales, which evolved from a fairly large (and took Boyden’s 1960s immunology-based conclusions a step fur- therefore freshwater-dependent) terrestrial mammal, develop a ther. Not only were whales more closely related to artiodactyls system capable of handling the excess salt load associated with than to any other living mammals, they asserted, but in fact ingesting seawater? Evidence from so-called stable oxygen whales were themselves artiodactyls, one of many twigs on that isotopes has provided some clues. In nature, oxygen mainly branch of the mammalian family tree. Moreover, a number of occurs in two forms, or isotopes: 16O and 18O. The ratios of these these studies pointed to an especially close relationship between isotopes in freshwater and seawater differ, with seawater whales and hippopotamuses. Particularly strong evidence for containing more 18O. Because mammals incorporate oxygen this idea came in 1999 from analyses of snippets of noncoding from drinking water into their developing teeth and bones, the DNA called SINES (short interspersed elements), conducted by remains of those that imbibe seawater can be distinguished Norihiro Okada and his colleagues at the Tokyo Institute of from those that take in freshwater. Technology. J.G.M. (Hans) Thewissen of the Northeastern Ohio The whale-hippo connection did not sit well with paleontol- Universities College of Medicine and his colleagues thus ogists. “I thought they were nuts,” Gingerich recollects. “Every- analyzed the oxygen isotope ratios in ancient whale teeth to thing we’d found was consistent with a mesonychid origin. I was gain insight into when these animals might have moved from a happy with that and happy with a connection through mesony- freshwater-based osmoregulatory system to a seawater-based chids to artiodactyls.” Whereas mesonychids appeared at the one. Oxygen isotope values for pakicetids, the most primitive right time, in the right place and in the right form to be consid- whales, indicate that they drank freshwater, as would be ered whale progenitors, the fossil record did not seem to contain predicted from other indications that these animals spent much a temporally, geographically and morphologically plausible ar- of their time on land. Isotope measurements from amphibious tiodactyl ancestor for whales, never mind one linking whales Ambulocetus, on the other hand, vary widely, and some and hippos specifically. Thewissen, too, had largely dismissed specimens show no evidence of seawater intake. In the DNA findings. But “I stopped rejecting it when Okada’s explanation, the researchers note that although Ambulocetus is SINE work came out,” he says. known to have spent time in the sea (based on the marine It seemed the only way to resolve the controversy was to find, nature of the rocks in which its fossils occur), it may still have of all things, an ancient whale anklebone. Morphologists have had to go ashore to drink. Alternatively, it may have spent the traditionally defined artiodactyls on the basis of certain features early part of its life (when its teeth mineralized) in freshwater in one of their anklebones, the astragalus, that enhance mobili- and only later entered the sea. ty. Specifically, the unique artiodactyl astragalus has two The protocetids, however, which show more skeletal grooved, pulleylike joint surfaces. One connects to the tibia, or adaptations to aquatic life, exhibit exclusively marine isotope shinbone; the other articulates with more distal anklebones. If values, indicating that they drank only seawater. Thus, just a whales descended from artiodactyls, researchers reasoned, those few million years after the first whales evolved, their that had not yet fully adapted to life in the seas should exhibit descendants had adapted to increased salt loads. This this double-pulleyed astragalus. physiological innovation no doubt played an important role in That piece of the puzzle fell into place last fall, when Gin- gerich and Thewissen both announced discoveries of new prim- facilitating the protocetids’ dispersal across the globe. —K.W. itive whale fossils. In the eastern part of Baluchistan Province,

78 SCIENTIFIC AMERICAN MAY 2002 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. HIND LIMB of an ancient whale, Rodhocetus, preserves a long-sought anklebone 123 known as the astragalus (at right). Shown in the inset beside a mesonychid astragalus (1) and one from a modern artiodactyl (2), the Rodhocetus astragalus (3) exhibits the distinctive double-pulley shape that characterizes all artiodactyl astragali, suggesting that whales descended not from mesonychids as previously thought but from an ancient artiodactyl. ASTRAGALUS

Gingerich’s team had found partially articulated skeletons of whales’ closest relative, and hippos could be their closest living Rodhocetus balochistanensis and a new protocetid genus, Ar- relative [see box on page 74]. Critics of that idea, however, point tiocetus. Thewissen and his colleagues recovered from a bone out that although folding the mesonychids into the artiodactyl bed in the Kala Chitta Hills of Punjab, Pakistan, much of the order offers an escape hatch of sorts to supporters of the mesony- long-sought postcranial skeleton of Pakicetus, as well as that chid hypothesis, it would upset the long-standing notion that the of a smaller member of the pakicetid family, Ichthyolestes. Each ankle makes the artiodactyl. came with an astragalus bearing the distinctive artiodactyl Investigators agree that figuring out the exact relationship characteristics. between whales and artiodactyls will most likely require finding The anklebones convinced both longtime proponents of the additional fossils—particularly those that can illuminate the be- mesonychid hypothesis that whales instead evolved from artio- ginnings of artiodactyls in general and hippos in particular. Yet dactyls. Gingerich has even embraced the hippo idea. Although even with those details still unresolved, “we’re really getting a hippos themselves arose long after whales, their purported an- handle on whales from their origin to the end of archaeocetes,” cestors—dog- to horse-size, swamp-dwelling beasts called an- Uhen reflects. The next step, he says, will be to figure out how thracotheres—date back to at least the middle Eocene and may the mysticetes and odontocetes arose from the archaeocetes and thus have a forebear in common with the cetaceans. In fact, Gin- when their modern features emerged. Researchers may never un- gerich notes that Rodhocetus and anthracotheres share features ravel all the mysteries of whale origins. But if the extraordinary in their hands and wrists not seen in any other later artiodactyls. advances made over the past two decades are any indication, Thewissen agrees that the hippo hypothesis holds much more with continued probing, answers to many of these lingering appeal than it once did. But he cautions that the morphological questions will surface from the sands of time. SA data do not yet point to a particular artiodactyl, such as the hip- po, being the whale’s closest relative, or sister group. “We don’t Kate Wong is a writer and editor for ScientificAmerican.com have the resolution yet to get them there,” he remarks, “but I think that will come.” MORE TO EXPLORE What of the evidence that seemed to tie early whales to The Emergence of Whales: Evolutionary Patterns in the Origin of mesonychids? In light of the new ankle data, most workers now Cetacea. Edited by J.G.M. Thewissen. Plenum Publishing, 1998. suspect that those similarities probably reflect convergent evo- Skeletons of Terrestrial Cetaceans and the Relationship of Whales to lution rather than shared ancestry and that mesonychids repre- Artiodactyls. J.G.M. Thewissen, E. M. Williams, L. J. Roe and S. T. Hussain in Nature, Vol. 413, pages 277–281; September 20, 2001. sent an evolutionary dead end. But not everyone is convinced. Maureen O’Leary of the State University of New York at Stony Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan. Philip D. Gingerich, Munir ul Haq, Iyad S. Brook argues that until all the available evidence—both mor- Zalmout, Intizar Hussain Khan and M. Sadiq Malkani in Science, Vol. 293, phological and molecular—is incorporated into a single phylo- pages 2239–2242; September 21, 2001. genetic analysis, the possibility remains that mesonychids belong The Encyclopedia of Marine Mammals. Edited by W. F. Perrin, Bernd G. at the base of the whale pedigree. It is conceivable, she says, that Würsig and J.G.M. Thewissen. Academic Press, 2002. mesonychids are actually ancient artiodactyls but ones that re- A broadcast version of this article will run on National Geographic Today, a

DAN ERICKSON versed the ankle trend. If so, mesonychids could still be the show on the National Geographic Channel. Please check your local listings.

www.sciam.com SCIENTIFIC AMERICAN 79 COPYRIGHT 2002 SCIENTIFIC AMERICAN, INC. Downloaded from rspb.royalsocietypublishing.org on August 28, 2014

Genetic analysis of hair samples attributed to yeti, bigfoot and other anomalous primates

Bryan C. Sykes, Rhettman A. Mullis, Christophe Hagenmuller, Terry W. Melton and Michel Sartori

Proc. R. Soc. B 2014 281, 20140161, published 2 July 2014

References This article cites 11 articles, 3 of which can be accessed free http://rspb.royalsocietypublishing.org/content/281/1789/20140161.full.html#ref-list-1

Article cited in: http://rspb.royalsocietypublishing.org/content/281/1789/20140161.full.html#related-urls This article is free to access

Subject collections Articles on similar topics can be found in the following collections

evolution (1869 articles) genetics (145 articles) taxonomy and systematics (198 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here

To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on August 28, 2014

Genetic analysis of hair samples attributed to yeti, bigfoot and other anomalous primates rspb.royalsocietypublishing.org Bryan C. Sykes1, Rhettman A. Mullis2, Christophe Hagenmuller3, Terry W. Melton4 and Michel Sartori5,6

1Institute of Human Genetics, Wolfson College, University of Oxford, Oxford OX2 6UD, UK 2PO Box 40143, Bellevue, WA 98005, USA 3NaturAlpes, Annecy-Le-Vieux 74940, France Research 4Mitotyping Technologies, 2565 Park Center Boulevard, State College, PA 16801, USA 5Museum of Zoology, Palais de Rumine, Lausanne 1014, Switzerland Cite this article: Sykes BC, Mullis RA, 6Museum of Zoology and Grindel Biocentre, Hamburg 20146, Germany Hagenmuller C, Melton TW, Sartori M. 2014 Genetic analysis of hair samples attributed to In the first ever systematic genetic survey, we have used rigorous decontami- yeti, bigfoot and other anomalous primates. nation followed by mitochondrial 12S RNA sequencing to identify the species origin of 30 hair samples attributed to anomalous primates. Two Himalayan Proc. R. Soc. B 281: 20140161. samples, one from Ladakh, India, the other from Bhutan, had their closest http://dx.doi.org/10.1098/rspb.2014.0161 genetic affinity with a Palaeolithic polar bear, maritimus. Otherwise the hairs were from a range of known extant mammals.

Received: 21 January 2014 Accepted: 27 March 2014 1. Introduction Despite several decades of research, mystery still surrounds the species identity of so-called anomalous primates such as the yeti in the Himalaya, almasty in central Asia and sasquatch/bigfoot in North America. On the one hand, numer- Subject Areas: ous reports including eye-witness and footprint evidence, point to the existence genetics, taxonomy and systematics, evolution of large unidentified primates in many regions of the world. On the other hand, no bodies or recent fossils of such creatures have ever been authenticated. There Keywords: is no shortage of theories about what these animals may be, ranging from sur- viving populations of collateral hominids such as Homo neanderthalensis, Homo yeti, almasty, bigfoot, sasquatch, floresiensis [1] or Denisovans [2], extinct apes such as Gigantopithecus [3] or even mitochondrial DNA unlikely hybrids between Homo sapiens and other mammals [4]. Modern science has largely avoided this field and advocates frequently complain that they have been ‘rejected by science’ [5]. This conflicts with the basic tenet that science Author for correspondence: neither rejects nor accepts anything without examining the evidence. To apply this philosophy to the study of anomalous primates and to introduce Bryan C. Sykes some clarity into this often murky field, we have carried out a systematic genetic e-mail: [email protected] survey of hair samples attributed to these creatures. Only two ‘tongue-in-cheek’ scientific publications report DNA sequence data from anomalous primates. Milinkovitch et al. [6], after analysis of a Nepalese sample, confirmed Captain Haddock’s suspicions that the yeti was an ungulate [7]. The same conclusion was reached by Coltman et al. [8] after analysis of sasquatch hair from Alaska.

2. Material and methods Hair samples submissions were solicited from museum and individual collections in a joint press release issued on 14 May 2012 by the Museum of Zoology, Lausanne and the University of Oxford. A total of 57 samples were received and subjected to macroscopic, microscopic and infrared fluorescence examination to eliminate obvious non-hairs. This excluded one sample of plant material and one of glass fibre. Of the screened samples, 37 were selected for genetic analysis based on their provenance or historic interest. Lengths (2–4 cm) of individual hair shaft

& 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from rspb.royalsocietypublishing.org on August 28, 2014

Table 1. Origin and GenBank sequence matches of hair samples attributed to anomalous primates. (All sequence matches were 100%.) 2 rspb.royalsocietypublishing.org ref. no. location attribution GenBank sequence match common name

25025 Ladakh, India yeti U. maritimus polar bear 25191 Bhutan yeti/migyhur U. maritimus polar bear 25092 Nepal yeti Capricornis sumatraensis serow 25027 Russia almasty U. arctos brown bear 25039 Russia almasty Equus caballus horse 25040 Russia almasty Bos taurus cow rc .Sc B Soc. R. Proc. 25041 Russia almasty Equus caballus horse 25073 Russia almasty Equus caballus horse 25074 Russia almasty U. americanus American black bear

25075 Russia almasty P. lotor 281

25194 Russia almasty U. arctos brown bear 20140161 : 25044 Sumatra orang pendek Tapirus indicus Malaysian tapir 25035 AZ, USA bigfoot P. lotor raccoon 25167 AZ, USA bigfoot Ovis aries sheep 25104 CA, USA bigfoot U. americanus American black bear 25106 CA, USA bigfoot U. americanus American black bear 25081 MN, USA bigfoot Erethizon dorsatum N. American porcupine 25082 MN, USA bigfoot U. americanus American black bear 25202 OR, USA bigfoot U. americanus American black bear 25212 OR, USA bigfoot C. lupus/latrans/domesticus wolf/coyote/dog 25023 TX, USA bigfoot Equus caballus horse 25072 TX, USA bigfoot Homo sapiens human 25028 WA, USA bigfoot U. americanus American black bear 25029 WA, USA bigfoot C. lupus/latrans/domesticus wolf/coyote/dog 25030 WA, USA bigfoot Bos taurus cow 25069 WA, USA bigfoot Odocoileus virginianus/hemionus white-tailed/mule deer 25086 WA, USA bigfoot Bos taurus cow 25093 WA, USA bigfoot C. lupus/latrans/domesticus wolf/coyote/dog 25112 WA, USA bigfoot Bos taurus cow 25113 WA, USA bigfoot C. lupus/latrans/domesticus wolf/coyote/dog

were thoroughly cleaned to remove surface contamination, identical to the revised Cambridge Reference Sequence [11] ground into a buffer solution in a glass homogenizer then incu- and thus H. sapiens of likely European matrilineal descent. bated for 2 h at 568C in a solution containing proteinase K before Other submitted samples were of known mammals that in extraction with phenol/chloroform/isoamyl alcohol. PCR ampli- most cases were living within their normal geographical fication of the ribosomal mitochondrial DNA 12S fragment range, the exceptions being sample nos. 25025 and 25191 corresponding to bps 1093–1196 of the human mitochondrial (Ursus maritimus, polar bear) from the Himalayas, no. 25074 genome was carried out [9,10]. Recovered sequences were (Ursus americanus, American black bear) and no. 25075 ( compared to GenBank accessions for species identification. lotor, raccoon) that were submitted from Russia even though they are native to North America. Despite the wide range of age and condition of the submit- 3. Results and discussion ted hair shafts, which ranged from fresh to museum specimens The table 1 shows the GenBank species identification of more than 50 years old, the majority yielded mitochondrial sequences matching the 30 samples from which DNA was 12S RNA sequences which allowed species identification with recovered. Seven samples failed to yield any DNA sequences 100% sequence identity. Of the recovered sequences, only one despite multiple attempts. As the sequence of mitochon- (no. 25072) yielded a human sequence, indicating that the drial 12S RNA segment is identical in H. sapiens and rigorous cleaning and extraction protocol had been effective H. neanderthalensis, amplification and sequencing of mitochon- in eliminating extraneous human contamination which often drial DNA hypervariable region 1 (bps 16 000–16 400) of confounds the analysis of old material and may lead to misinter- no. 25072 was carried out and identified the source as being pretation of a sample as human or even as an unlikely and Downloaded from rspb.royalsocietypublishing.org on August 28, 2014

unknown human x mammalian hybrid [4]. The deliberately especially if, as reported by the hunter who shot the Ladakh 3 permissive primer combination used here allowed a wide specimen, they behave more aggressively towards humans rspb.royalsocietypublishing.org range of mammalian DNA to be amplified within a single reac- than known indigenous bear species. tion, although this meant that some identification did not go With the exception of these two samples, none of the sub- beyond the level of genus. For example, no. 25029 was identified mitted and analysed hairs samples returned a sequence that as but did not distinguish between Canis lupus (wolf), could not be matched with an extant mammalian species, Canis latrans (coyote) and Canis domesticus (domestic dog). often a domesticate. While it is important to bear in mind Sequences derived from hair sample nos. 25025 and 25191 that absence of evidence is not evidence of absence and this had a 100% match with DNA recovered from a Pleistocene survey cannot refute the existence of anomalous primates, fossil more than 40 000 BP of U. maritimus (polar bear) [12] neither has it found any evidence in support. Rather than per- but not to modern examples of the species. Hair sample no. sisting in the view that they have been ‘rejected by science’,

25025 came from an animal shot by an experienced hunter in advocates in the cryptozoology community have more work B Soc. R. Proc. Ladakh, India ca 40 years ago who reported that its behaviour to do in order to produce convincing evidence for anomalous was very different from a brown bear Ursus arctos with which primates and now have the means to do so. The techniques he was very familiar. Hair sample no. 25191 was recovered described here put an end to decades of ambiguity about from a high altitude (ca 3500 m) bamboo forest in Bhutan species identification of anomalous primate samples and set 281 and was identified as a nest of a migyhur, the Bhutanese a rigorous standard against which to judge any future claims. equivalent of the yeti. The Ladakh hairs (no. 25025) were 20140161 : golden-brown, whereas the hair from Bhutan (no. 25191) was reddish-brown in appearance. As the match is to a segment Acknowledgements. We thank Reinhold Messner, Peter Byrne, Justin only 104 bp long, albeit in the very conserved 12S RNA gene, Smeja, Bart Cutino, Derek Randles, Dan Shirley, Garland Fields, this result should be regarded as preliminary. Other than Loren Coleman, Betty Klopp, Marcel Cagey, Sam Cagey, Lori these data, nothing is currently known about the genetic affi- Simmons, Adam Davies, Dr Mike Amaranthus, Mike Long, Patrick nity of Himalayan and although there are anecdotal Spell, Maxwell David, Mark McClurkan, Rob Kryder, Jack Barnes, Jeff Anderson, David Ellis, Steve Mattice, Brenda Harris, Stuart reports of white bears in Central Asia and the Himalayas Fleming, Igor Burtsev, Dmitri Pirkulov, Michael Trachtengerts and [13,14], it seems more likely that the two hairs reported here Dmitri Bayanov for submitting samples and for their progressive are from either a previously unrecognized bear species, stance in doing so. Thanks also to, Ray Crowe, Ronnie Roseman, colour variants of U. maritimus,orU. arctos/U. maritimus Greg Roberts and Tom Graham for discussing their experiences hybrids. Viable U. arctos/U. maritimus hybrids are known and to Jeff Meldrum and Anna Nekaris for advice and guidance. We are very grateful to Ken Goddard, Ed Espinoza, Mike Tucker, from the Admiralty, Barayanov and Chicagov (ABC) islands Barry Baker, Bonnie Yates, Cookie Smith and Dyan Straughan of off the coast of Alaska though in the ABC hybrids the mito- the US Fish and Wildlife Service Forensic Laboratory, Ashland, OR, chondrial sequence homology is with modern rather than USA, for help with forensic methods of trace evidence analysis and ancient polar bears [15]. If they are hybrids, the Ladakh and to Charity Holland, Bonnie Higgins, Gloria Dimick and Michele Bhutan specimens are probably descended from a different Yon for technical assistance. Data accessibility. hybridization event during the early stages of species diver- DNA sequences: GenBank accession nos. KJ155696– KJ155724 and KJ607607. Voucher samples of the research materials gence between U. arctos and U. maritimus. Genomic sequence have been deposited in the Heuvelmans Archive at the Museum of data are needed to decide between these alternatives. If these Zoology, Lausanne, Switzerland. bears are widely distributed in the Himalayas, they may well Funding statement. We also thank Harry Marshall and Icon Films for contribute to the biological foundation of the yeti legend, their contribution to the costs of analysis.

References

1. Brown P, Sutikna T, Morwood M, Soejono R, Jatmiko E, Phylogenet. Evol. 31, 1–3. (doi:10.1016/j.ympev. revision of the Cambridge reference sequence for Saptomo E, Awa Due R. 2004 A new small-bodied 2004.01.009) human mitochondrial DNA. Nat. . 23, 147. hominin from the Late Pleistocene of Flores, Indonesia. 7. Herge. 1960 Tintin au Tibet. Tournai, Belgium: (doi:10.1038/13779) Nature 431, 1055–1061. (doi:10.1038/nature02999) Casterman. 12. Linqvist C et al. 2010 Complete mitochondrial 2. Reich D et al. 2010 Genetic history of an archaic 8. Coltman D, Davis C. 2005 Molecular cryptozoology genome of a Pleistocene jawbone unveils the origin hominin group in Denisova Cave in Siberia. Nature meets the Sasquatch. Trends Ecol. Evol. 21, 60–61. of polar bear. Proc. Natl Acad. Sci. USA 107, 468, 1053–1060. (doi:10.1038/nature09710) (doi:10.1016/j.tree.2005.11.010) 5053–5057. (doi:10.1073/pnas.0914266107) 3. Strauss W. 1957 Jaw of Gigantopithecus. Science 9. Melton T, Dimick G, Higgins B, Lindstrom Nelson K. 13. Brunner B. 2007 Bears: a brief history, p. 64. New 125, 685. (doi:10.1126/science.125.3250.685) 2005 Forensic mitochondrial DNA analysis of 691 Haven, CT: Yale University Press. 4. Ketchum M et al. 2013 North American hominins. casework hairs. J. Forensic Sci. 50, 73–80. (doi:10. 14. Smythe F. 1936 The valley of flowers, p. 144. De Novo 1, 1–15. 1520/JFS2004230) London, UK: Hodder and Stoughton. 5. Regal B. 2011 Searching for Sasquatch, p. 5. 10. Melton T, Holland C. 2007 Routine forensic use of the 15. Hailer F, Kutschera V, Hallstron B, Klassert D, Fain S, New York, NY: Palgrave Macmillan. mitochondrial 12S ribosomal RNA genes for species Leonard J, Arnasojn U, Janke A. 2012 Nuclear 6. Milinkovitch MC et al. 2004 Molecular phylogenetic identification. J. Forensic Sci. 52, 1305–1307. genomic sequences reveal that polar bears are an analyses indicate extensive morphological 11. Andrews R, Kubacka I, Chinnery C, Lightowlers RN, old and distinct bear lineage. Science 336, convergence between the ‘yeti’ and primates. Mol. Turnbull DM, Howell N. 1999 Reanalysis and 344–347. (doi:10.1126/science.1216424) The Impact of Conservation on the Status of the World's Vertebrates Michael Hoffmann et al. Science 330, 1503 (2010); DOI: 10.1126/science.1194442

This copy is for your personal, non-commercial use only.

If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here.

The following resources related to this article are available online at www.sciencemag.org (this information is current as of August 25, 2012 ):

Updated information and services, including high-resolution figures, can be found in the online version of this article at: on August 25, 2012 http://www.sciencemag.org/content/330/6010/1503.full.html Supporting Online Material can be found at: http://www.sciencemag.org/content/suppl/2010/10/27/science.1194442.DC1.html A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/330/6010/1503.full.html#related

This article cites 36 articles, 13 of which can be accessed free: www.sciencemag.org http://www.sciencemag.org/content/330/6010/1503.full.html#ref-list-1 This article has been cited by 21 articles hosted by HighWire Press; see: http://www.sciencemag.org/content/330/6010/1503.full.html#related-urls This article appears in the following subject collections: Ecology

http://www.sciencemag.org/cgi/collection/ecology Downloaded from

Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2010 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. RESEARCH ARTICLE

by two to three orders of magnitude (3), with substantial detrimental societal and economic consequences (4). In response to this crisis, 193 The Impact of Conservation on the parties to the Convention on Biological Diversity (CBD; adopted 1992) agreed “to achieve by Status of the World’s Vertebrates 2010 a significant reduction of the current rate of biodiversity loss at the global, regional, and na- tional level as a contribution to poverty alle- Michael Hoffmann,1,2* Craig Hilton-Taylor,3 Ariadne Angulo,4,5 Monika Böhm,6 viation and to the benefit of all life on Earth” (5). Thomas M. Brooks,7,8,9 Stuart H. M. Butchart,10 Kent E. Carpenter,2,5,11 Janice Chanson,5,12 That the target has not been met was borne out Ben Collen,6 Neil A. Cox,5,13 William R. T. Darwall,3 Nicholas K. Dulvy,14 Lucy R. Harrison,14 by empirical testing against 31 cross-disciplinary Vineet Katariya,3 Caroline M. Pollock,3 Suhel Quader,15 Nadia I. Richman,6 Ana S. L. Rodrigues,16 indicators developed within the CBD framework Marcelo F. Tognelli,5,13,17 Jean-Christophe Vié,5 John M. Aguiar,18 David J. Allen,3 itself (1). However, this does not mean that con- Gerald R. Allen,19 Giovanni Amori,20 Natalia B. Ananjeva,21 Franco Andreone,22 Paul Andrew,23 servation efforts have been ineffective. Conser- Aida Luz Aquino Ortiz,24 Jonathan E. M. Baillie,25 Ricardo Baldi,26,27 Ben D. Bell,28 vation actions have helped to prevent extinctions S. D. Biju,29 Jeremy P. Bird,30 Patricia Black-Decima,31 J. Julian Blanc,32 Federico Bolaños,33 (6, 7) and improve population trajectories (8), Wilmar Bolivar-G.,34 Ian J. Burfield,10 James A. Burton,35,36 David R. Capper,37 but there has been limited assessment of the Fernando Castro,38 Gianluca Catullo,39 Rachel D. Cavanagh,40 Alan Channing,41 overall impact of ongoing efforts in reducing Ning Labbish Chao,42,43,44 Anna M. Chenery,45 Federica Chiozza,46 Viola Clausnitzer,47 losses in biodiversity (9, 10). Here, we assess the Nigel J. Collar,10 Leah C. Collett,3 Bruce B. Collette,48 Claudia F. Cortez Fernandez,49 overall status of the world’s vertebrates, deter- Matthew T. Craig,50 Michael J. Crosby,10 Neil Cumberlidge,51 Annabelle Cuttelod,3 mine temporal trajectories of extinction risk for Andrew E. Derocher,52 Arvin C. Diesmos,53 John S. Donaldson,54 J. W. Duckworth,55 Guy Dutson,56 three vertebrate classes, and estimate the degree to S. K. Dutta,57 Richard H. Emslie,58 Aljos Farjon,59 Sarah Fowler,60 Jo¨rg Freyhof,61 which conservation actions have reduced bio- David L. Garshelis,62 Justin Gerlach,63 David J. Gower,64 Tandora D. Grant,65 diversity loss. Geoffrey A. Hammerson,66 Richard B. Harris,67 Lawrence R. Heaney,68 S. Blair Hedges,69 Described vertebrates include 5498 mam- Jean-Marc Hero,70 Baz Hughes,71 Syed Ainul Hussain,72 Javier Icochea M.,73 Robert F. Inger,68 mals, 10,027 birds, 9084 reptiles, 6638 amphib- on August 25, 2012 Nobuo Ishii,74 Djoko T. Iskandar,75 Richard K. B. Jenkins,76,77,78 Yoshio Kaneko,79 ians, and 31,327 fishes (table S1). Vertebrates Maurice Kottelat,80,81 Kit M. Kovacs,82 Sergius L. Kuzmin,83 Enrique La Marca,84 are found at nearly all elevations and depths, John F. Lamoreux,5,85 Michael W. N. Lau,86 Esteban O. Lavilla,87 Kristin Leus,88 occupy most major types, and display Rebecca L. Lewison,89 Gabriela Lichtenstein,90 Suzanne R. Livingstone,91 remarkable variation in body size and life his- Vimoksalehi Lukoschek,92,93 David P. Mallon,94 Philip J. K. McGowan,95 Anna McIvor,96 tory. Although they constitute just 3% of known Patricia D. Moehlman,97 Sanjay Molur,98 Antonio Muñoz Alonso,99 John A. Musick,100 species, vertebrates play vital roles in ecosystems Kristin Nowell,101 Ronald A. Nussbaum,102 Wanda Olech,103 Nikolay L. Orlov,21 (11) and have great cultural importance (12). Theodore J. Papenfuss,104 Gabriela Parra-Olea,105 William F. Perrin,106 Beth A. Polidoro,5,11 Under the auspices of the International Union for Mohammad Pourkazemi,107 Paul A. Racey,108 James S. Ragle,5 Mala Ram,6 Galen Rathbun,109

Conservation of Nature (IUCN) Species Survival www.sciencemag.org Robert P. Reynolds,110 Anders G. J. Rhodin,111 Stephen J. Richards,112,113 Lily O. Rodríguez,114 Commission, we compiled data on the taxonomy, Santiago R. Ron,115 Carlo Rondinini,46 Anthony B. Rylands,2 Yvonne Sadovy de Mitcheson,116,117 distribution, population trend, major threats, con- Jonnell C. Sanciangco,5,11 Kate L. Sanders,118 Georgina Santos-Barrera,119 Jan Schipper,120 servation measures, and threat status for 25,780 Caryn Self-Sullivan,121,122 Yichuan Shi,3 Alan Shoemaker,123 Frederick T. Short,124 vertebrate species, including all mammals, birds, Claudio Sillero-Zubiri,125 Débora L. Silvano,126 Kevin G. Smith,3 Andrew T. Smith,127 amphibians, cartilaginous fishes, and statistically Jos Snoeks,128,129 Alison J. Stattersfield,10 Andrew J. Symes,10 Andrew B. Taber,130 Bibhab K. Talukdar,131 Helen J. Temple,132 Rob Timmins,133 Joseph A. Tobias,134 Katerina Tsytsulina,135 Denis Tweddle,136 Carmen Ubeda,137 Sarah V. Valenti,60

1 Downloaded from 2 138,139 140 10 64 IUCN SSC Species Survival Commission, c/o United Nations Peter Paul van Dijk, Liza M. Veiga, Alberto Veloso, David C. Wege, Mark Wilkinson, Environment Programme World Conservation Monitoring Centre, 141 142 7 143 10 Elizabeth A. Williamson, Feng Xie, Bruce E. Young, H. Resit Akçakaya, Leon Bennun, 219 Huntingdon Road, Cambridge CB3 0DL, UK. 2Conservation Tim M. Blackburn,6 Luigi Boitani,46 Holly T. Dublin,144,145 Gustavo A. B. da Fonseca,146,147 International, 2011 Crystal Drive, Arlington, VA 22202, USA. 3 Claude Gascon,2 Thomas E. Lacher Jr.,18 Georgina M. Mace,148 Susan A. Mainka,149 Species Programme, IUCN, 219c Huntingdon Road, Cambridge CB3 0DL, UK. 4IUCN–CI Biodiversity Assessment Unit, c/o P.O. Jeffery A. McNeely,149 Russell A. Mittermeier,2,149 Gordon McGregor Reid,150 151 2 152 149 Box 19004, 360 A Bloor Street W., Toronto, Ontario M5S 1X1, Jon Paul Rodriguez, Andrew A. Rosenberg, Michael J. Samways, Jane Smart, Canada. 5Species Programme, IUCN, Rue Mauverney 28, 1196, Bruce A. Stein,153 Simon N. Stuart1,2,154,155 Gland, Switzerland. 6Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK. 7NatureServe, 1101 Wilson Boulevard, Arlington, VA 22209, USA. 8World Using data for 25,780 species categorized on the International Union for Conservation of Nature Agroforestry Center (ICRAF), University of the Philippines Los 9 Red List, we present an assessment of the status of the world’s vertebrates. One-fifth of species are Baños, Laguna 4031, Philippines. School of Geography and Environmental Studies, University of Tasmania, Hobart, Tasmania classified as Threatened, and we show that this figure is increasing: On average, 52 species of 7001, Australia. 10BirdLife International, Wellbrook Court, Girton mammals, birds, and amphibians move one category closer to extinction each year. However, this Road, Cambridge CB3 0NA, UK. 11Department of Biological overall pattern conceals the impact of conservation successes, and we show that the rate of Sciences, Old Dominion University, Norfolk, VA 23529, USA. 12 deterioration would have been at least one-fifth again as much in the absence of these. IUCN–CI Biodiversity Assessment Unit, c/o 130 Weatherall Road, Cheltenham 3192, Victoria, Australia. 13IUCN–CI Biodi- Nonetheless, current conservation efforts remain insufficient to offset the main drivers of versity Assessment Unit, Conservation International, 2011 Crystal biodiversity loss in these groups: agricultural expansion, logging, overexploitation, and Drive Ste 500, Arlington, VA 22202, USA. 14IUCN Shark Specialist invasive alien species. Group, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada. 15National Centre for Biological Sciences, Tata Institute of n the past four decades, individual popula- original cover (1, 2) through anthropogenic ac- Fundamental Research, GKVK Campus, Bellary Road, Bangalore tions of many species have undergone declines tivity. These losses are manifested in species ex- 560 065, India. 16Centre d’Ecologie Fonctionnelle et Evolutive, Iand many habitats have suffered losses of tinction rates that exceed normal background rates CNRS UMR5175, 1919 Route de Mende, 34293 Montpellier,

www.sciencemag.org SCIENCE VOL 330 10 DECEMBER 2010 1503 RESEARCH ARTICLE

France. 17IADIZA-CONICET, CCT-Mendoza, CC 507, 5500 Mendoza, Valley Road, Escondido, CA 92027, USA. 66NatureServe, 746 Terrace, Adelaide, South Australia 5000, Australia. 113Rapid Argentina. 18Department of Wildlife and Fisheries Sciences, Middlepoint Road, Port Townsend, WA 98368, USA. 67Depart- Assessment Program, Conservation International, P.O. Box 1024, Texas A&M University, College Station, TX 77843, USA. ment of Ecosystem and Conservation Science, University of Atherton, Queensland 4883, Australia. 114German Technical 19Western Australian Museum, Locked Bag 49, Welshpool DC, Montana, Missoula, MT 59812, USA. 68Field Museum of Nat- Cooperation (GTZ) GmbH, Pasaje Bernardo Alcedo N° 150, piso Perth, Western Australia 6986, Australia. 20CNR–Institute for ural History, Chicago, IL 60605, USA. 69Department of Biol- 4, El Olivar, San Isidro, Lima 27, Perú. 115Museo de Zoología, Ecosystem Studies, Viale dell’Università 32, 00185 Rome, Italy. ogy, Pennsylvania State University, University Park, PA 16802, Escuela de Biología, Pontificia Universidad Católica del Ecuador, 21Zoological Institute, Russian Academy of Sciences, 199034 St. USA. 70Environmental Futures Centre, School of Environment, Av. 12 de Octubre y Veintimilla, Quito, Ecuador. 116School of Petersburg, Universitetskaya nab.1, Russia. 22Museo Regionale Griffith University, Gold Coast campus, Queensland, 4222, Biological Sciences, University of Hong Kong, Pok Fu Lam Road, di Scienze Naturali, Via G. Giolitti, 36, I-10123 Torino, Italy. Australia. 71Wildfowl & Wetlands Trust, Slimbridge, Glos GL2 Hong Kong SAR. 117Society for the Conservation of Reef Fish 23Taronga Conservation Society Australia, Taronga Zoo, P.O. Box 7BT, UK. 72Wildlife Institute of India, Post Box #18, Dehra Dun, Aggregations, 9888 Caroll Centre Road, Suite 102, San Diego, 20, Mosman 2088, Sydney, Australia. 24Martin Barrios 2230 c/ 248001 Uttarakhand, India. 73Calle Arica 371, Dpto U-2, CA 92126, USA. 118School of Earth and Environmental Sciences, Pizarro; Barrio Republicano, Asunción, Paraguay. 25Zoological Miraflores, Lima 18, Perú. 74School of Arts and Sciences, Tokyo Darling Building, University of Adelaide, North Terrace, Adelaide Society of London, Regent’s Park, London, NW1 4RY, UK. Woman’s Christian University, Zempukuji 2-6-1, Suginami-ku, 5005, Australia. 119Departamento de Biología Evolutiva, Facultad 26Unidad de Investigación Ecología Terrestre, Centro Nacional Tokyo 167-8585, Japan. 75School of Life Sciences and de Ciencias, Universidad Nacional Autónoma de México, Circuito Patagónico–CONICET, Boulevard Brown 2915, 9120 Puerto Technologi, Institut Teknologi Bandung, 10, Jalan Ganesa, Exterior S/N, 04510, Ciudad Universitaria, México. 120Big Island Madryn, Argentina. 27Patagonian and Andean Steppe Program, Bandung 40132, Indonesia. 76Durrell Institute of Conservation Invasive Species Committee, Pacific Cooperative Studies Unit, Wildlife Conservation Society, Boulevard Brown 2915, 9120 and Ecology, School of Anthropology and Conservation, University of Hawai’i, 23 East Kawili Street, Hilo, HI 96720, USA. Puerto Madryn, Argentina. 28Centre for Biodiversity & Restora- University of Kent, Canterbury, Kent CT2 7NR, UK. 77School 121Sirenian International, 200 Stonewall Drive, Fredericksburg, tion Ecology, School of Biological Sciences, Victoria University of the Environment and Natural Resources, Bangor University, VA 22401, USA. 122Department of Biology, P.O. Box 8042, of Wellington, P.O. Box 600, Wellington 6140, New Zealand. Bangor LL57 2UW, UK. 78Madagasikara Voakajy, B.P. 5181, Georgia Southern University, Statesboro, GA 30460, USA. 29Systematics Lab, School of Environmental Studies, University Antananarivo (101), Madagascar. 79Iwate Prefectural Uni- 123IUCN SSC Tapir Specialist Group, 330 Shareditch Road, of Delhi, Delhi 110 007, India. 30Center for Biodiversity and versity, Sugo 152-52, Takizawa, Iwate 020-0193, Japan. Columbia, SC 29210, USA. 124Department of Natural Resources Biosecurity Studies, Pacific Institute for Sustainable Develop- 80Route de la Baroche 12, 2952 Cornol, Switzerland. 81Raffles and the Environment, University of New Hampshire, Jackson ment, Jalan Bumi Nyiur 101, Manado, North Sulawesi, Museum of Biodiversity Research, National University of Estuarine Laboratory, Durham, NH 03824, USA. 125Wildlife Indonesia. 31Facultad de Ciencias Naturales e Instituto Miguel Singapore, Department of Biological Sciences, 6 Science Drive Conservation Research Unit, Department of Zoology, University of Lillo, Universidad Nacional de Tucuman, Miguel Lillo 205, 2, #03-01, 117546, Singapore. 82Norwegian Polar Institute, Oxford, Recanati-Kaplan Centre, Tubney House, Tubney OX13 4000 SM de Tucumán, Tucumán, Argentina. 32P.O. Box 47074, 9296 Tromsø, Norway. 83Institute of Ecology and Evolution, 5QL, UK. 126Laboratório de Zoologia, Universidade Católica de Nairobi 00100, Kenya. 33Escuela de Biología, Universidad de Russian Academy of Sciences, Leninsky Prospect, 33, Moscow Brasília, Campus I-Q.S. 07 Lote 01 EPCT-Taguatinga-DF, 71966- Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. 119071, Russia. 84Laboratorio de Biogeografía, Escuela de 700, Brazil. 127School of Life Sciences, Arizona State University, 34Sección de Zoología, Departamento de Biología, Facultad de Geografía, Universidad de Los , Mérida 5101, Vene- Tempe, AZ 85287, USA. 128Royal Museum for Central Africa, Ciencias Naturales y Exactas, Universidad del Valle, Calle 13, No. zuela. 85IUCN Species Programme, c/o 406 Randolph Hill Ichthyology, Leuvensesteenweg 13, B-3080 Tervuren, Belgium. 35 86 129 100-00, Cali, . Earthwatch Institute, 256 Banbury Road, Randolph, NH 03593, USA. Kadoorie Farm & Botanic Katholieke Universiteit Leuven, Laboratory of Animal Diversity on August 25, 2012 Road, Oxford OX2 7DE, UK. 36Veterinary Biomedical Sciences, Garden, Lam Kam Road, Tai Po, New Territories, Hong Kong and Systematics, Charles Deberiotstraat 32, B-3000 Leuven, Royal(Dick)SchoolofVeterinaryStudies,Universityof SAR. 87Instituto de Herpetología, Fundación Miguel Lillo– Belgium. 130Center for International Forestry Research, Jalan Edinburgh, Summerhall, Edinburgh EH9 1QH, Scotland, UK. CONICET, Miguel Lillo 251, 4000 SM de Tucumán, Tucumán, CIFOR, Situ Gede, Bogor Barat 16115, Indonesia. 131Aaranyak 3747B Lewisham Hill, London SE13 7PL, UK. 38Laboratorio de Argentina. 88Conservation Breeding Specialist Group–European and International Rhino Foundation, 50 Samanwoy Path (Survey), Herpetologia, Universidad del Valle,Carrera51,No.8H-15,Cali, Regional Office, p/a Annuntiatenstraat 6, 2170 Merksem, Post Office Beltola, Guwahati-781 028, Assam, India. 132The Colombia. 39WWF Italy–Species Office, Via Po 25/c 00198 Rome, Belgium. 89Biology Department, San Diego State University, Biodiversity Consultancy Ltd., 4 Woodend, Trumpington, Cam- Italy. 40British Antarctic Survey, High Cross, Madingley Road, San Diego, CA 92182, USA. 90Instituto Nacional de Antropologia bridge CB2 9LJ, UK. 1332313WillardAvenue,Madison,WI Cambridge CB3 0ET, UK. 41Biodiversity and Conservation Biology y Pensamiento Latinoamericano, 3 de Febrero 1378, 1426 53704, USA. 134Edward Grey Institute, Department of Zoology, Department, University of the Western Cape, Private Bag X17, Buenos Aires, Argentina. 91Ecology and Evolutionary Biology, University of Oxford, Oxford OX1 3PS, UK. 135Vertebrate Research Bellville 7535, South Africa. 42Bio-Amazonia Conservation Faculty of Biomedical & Life Sciences, Graham Kerr Building, Division, National Institute of Biological Resources, Environmental

International, 1295 William Street, Baltimore, MD 21230, USA. University of Glasgow, Glasgow G12 8QQ, Scotland, UK. Research Complex, Gyoungseo-dong, Seo-gu, Incheon 404-708, www.sciencemag.org 43Universidade Federal do Amazonas, Depto Ciências Pesqueiras, 92Department of Ecology and Evolutionary Biology, University South Korea. 136South African Institute for Aquatic Biodiversity, Manaus, AM 60700, Brazil. 44National Museum of Marine Bi- of California, Irvine, CA 92697, USA. 93ARC Centre of Excel- P/Bag 1015, Grahamstown, 6140, South Africa. 137Departamento ology and aquarium, 2 Houwan Road, Checheng, Pingtung 944, lence for Coral Reef Studies, James Cook University, Townsville, de Zoologia, Centro Regional Universitario Bariloche, Universidad Taiwan, R.O.C. 45United Nations Environment Programme World Queensland, 4811, Australia. 94Department of Biology, Chem- Nacional del Comahue, Quintral 1250, 8400 Bariloche, Conservation Monitoring Centre, 219 Huntingdon Road, Cam- istry and Health Science, Manchester Metropolitan University, Argentina. 138Emilio Goeldi Museum, Av. Perimetral, 1901, bridge CB3 0DL, UK. 46Department of Animal and Human Manchester M1 5GD, UK. 95World Pheasant Association, New- Belém, Pará 66017-970, Brazil. 139Federal University of Pará, Biology, Sapienza Università di Roma, Viale dell’Università 32, castle University Biology Field Station, Close House Estate, Rua Augusto Corrêa, 01, Belém, Pará 66075-110, Brazil. 140De- 00185 Roma, Italy. 47Senckenberg Museum of Natural History Heddon on the Wall, Newcastle upon Tyne NE15 0HT, UK. partamento de Ciencias Ecológicas, Facultad de Ciencias, Goerlitz, PF 300 154, 02806 Goerlitz, Germany. 48National 96115 Suez Road, Cambridge CB1 3QD, UK. 97Wildlife Trust Universidad de Chile, Las Palmeras 3425, Casilla 6553, Santiago,

Marine Fisheries Service Systematics Laboratory, National Alliance, Box 2031, Arusha, Tanzania. 98Zoo Outreach Or- Chile. 141Department of Psychology, University of Stirling, Stirling Downloaded from Museum of Natural History, MRC-0153, Smithsonian Institution, ganisation, 9A Lal Bahadur Colony, Peelamedu, Coimbatore, FK9 4LA, Scotland, UK. 142Chengdu Institute of Biology, the Washington, DC 20013, USA. 49Av.Busch,EdificioGirasoles2, Tamil Nadu 641004, India. 99El Colegio de la Frontera Sur, Chinese Academy of Sciences, Chengdu, 610041, P.R. China. Piso 5, Depto 7, La Paz, Bolivia. 50Department of Marine Apartado postal 63, Carretera Panamericana y Periférico sur 143Department of Ecology and Evolution, Stony Brook University, Sciences, University of Puerto Rico, P.O. Box 9000, Mayagüez, s/n Col. María Auxiliadora, 29290, San Cristóbal de las Casas, Stony Brook, NY 11794, USA. 144IUCN SSC, African Elephant PR 00681, USA. 51Department of Biology, Northern Michigan Chiapas, México. 100Virginia Institute of Marine Science, Specialist Group, c/o IUCN ESARO, P.O. Box 68200, Nairobi University, Marquette, MI 49855, USA. 52Department of Gloucester Point, VA 23062, USA. 101CAT, P.O. Box 332, 00200, Kenya. 145Wildlife Conservation Society, 2300 Southern Biological Sciences, University of Alberta, Edmonton, Alberta Cape Neddick, ME 03902, USA. 102Division of Reptiles and Boulevard, Bronx, NY 10460, USA. 146Global Environment T6G 2E9, Canada. 53Herpetology Section, Zoology Division, Amphibians, Museum of Zoology, University of Michigan, Facility, 1818 H Street NW, G 6-602, Washington, DC 20433, National Museum of the Philippines, Padre Burgos Avenue, Ann Arbor, MI 48109, USA. 103Warsaw University of Life USA. 147Department of Zoology, Federal University of Minas Ermita 1000, Manila, Philippines. 54South African National Sciences, Ciszewskiego 8, 02-786 Warsaw, Poland. 104Museum Gerais, 31270-901, Belo Horizonte, Brazil. 148Centre for Biodiversity Institute, KRC, Private Bag X7, Claremont 7735, of Vertebrate Zoology, University of California, Berkeley, CA Population Biology, Imperial College London, Silwood Park, South Africa. 55P.O. Box 5573, Vientiane, Lao PDR. 56c/o Birds 94720, USA. 105Departamento de Zoologia, Instituto de Ascot, Berks SL5 7PY, UK. 149IUCN, 28 Rue Mauverney, CH-1196 Australia, 60 Leicester Street, Carlton, Victoria 3053, Australia. Biologia, Universidad Nacional Autónoma de México, 04510 Gland, Switzerland. 150North of England Zoological Society, 57North Orissa University, Sriram Chandra Vihar, Takatpur, Ciudad Universitaria, México. 106Southwest Fisheries Science Chester Zoo, Upton-by-Chester, Chester CH2 1LH, UK. 151Centro Baripada 757003, Dist: Mayurbhanj, Orissa, India. 58IUCN SSC Center, National Marine Fisheries Service, NOAA, 3333 North de Ecología, Instituto Venezolano de Investigaciones Científicas, African Rhino Specialist Group, Box 1212, Hilton 3245, South Torrey Pines Court, La Jolla, CA 92037, USA. 107International Apartado 20632, Caracas 1020-A, Venezuela, and Provita, Africa. 59Herbarium, Library, Art & Archives, Royal Botanic Gar- Sturgeon Research Institute, P.O. Box 41635-3464, Rasht, Iran. Apartado 47552, Caracas 1041-A, Venezuela. 152Department of dens,Kew,Richmond,SurreyTW93AB,UK.60NatureBureau, 108Centre for Ecology and Conservation, University of Exeter in Conservation Ecology and Entomology, Stellenbosch University, 36 Kingfisher Court, Hambridge Road, Newbury RG14 5SJ, UK. Cornwall, Penryn TR10 9EZ, UK. 109Department of Ornithology P/Bag X1, Matieland 7602, South Africa. 153National Wildlife 61Leibniz-Institute of Freshwater Ecology and Inland Fisheries, and Mammalogy, California Academy of Sciences (San Fran- Federation, 901 E Street NW, Suite 400, Washington, DC 20004, Müggelseedamm 310, 12587 Berlin, Germany. 62Minnesota cisco),c/oP.O.Box202,Cambria,CA93428,USA.110USGS USA. 154Department of Biology and Biochemistry, University of Department of Natural Resources, Grand Rapids, MN 55744, Patuxent Wildlife Research Center, MRC 111, National Museum Bath, Bath BA2 7AY, UK. 155Al Ain Wildlife Park & Resort, P.O. USA. 63Nature Protection Trust of Seychelles, 133 Cherry Hinton of Natural History, Smithsonian Institution, P.O. Box 37012, Box 45553, Abu Dhabi, United Arab Emirates. Road, Cambridge CB1 7BX, UK. 64Department of Zoology, Washington, DC 20013, USA. 111Chelonian Research Founda- Natural History Museum, London SW7 5BD, UK. 65San Diego tion, 168 Goodrich Street, Lunenburg, MA 01462, USA. *To whom correspondence should be addressed. E-mail: Zoo Institute for Conservation Research, 15600 San Pasqual 112Herpetology Department, South Australian Museum, North [email protected]

1504 10 DECEMBER 2010 VOL 330 SCIENCE www.sciencemag.org RESEARCH ARTICLE

representative samples of reptiles and bony fishes [~1500 species each (13)]. The IUCN Red List is the widely accepted standard for assessing species’ global risk of extinction according to established quantitative criteria (14). Species are categorized in one of eight categories of extinction risk, with those in the categories Critically Endangered, Endangered, or Vulnerable classified as Threatened. Assess- ments are designed to be transparent, objective, and consultative, increasingly facilitated through workshops and Web-based open-access systems. All data are made freely available for consulta- tion (15) and can therefore be challenged and improved upon as part of an iterative process toward ensuring repeatable assessments over time. Status, trends, and threats. Almost one-fifth of extant vertebrate species are classified as Threatened, ranging from 13% of birds to 41% of amphibians, which is broadly comparable with the range observed in the few invertebrate and plant taxa completely or representatively assessed to date (Fig. 1 and table S2). When we incorporate the uncertainty that Data De- ficient species (those with insufficient informa-

tion for determining risk of extinction) introduce, on August 25, 2012 the proportion of all vertebrate species classi- Fig. 1. The proportion of vertebrate species in different Red List categories compared with completely fied as Threatened is between 16% and 33% (or representatively) assessed invertebrate and plant taxa on the 2010 IUCN Red List (15). EW, Extinct in (midpoint = 19%; table S3). [Further details the Wild; CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least of the data and assumptions behind these val- Concern; DD, Data Deficient. Extinct species are excluded. Taxa are ordered according to the estimated ues are provided in (16) and tables S2 and S3.] percentage (shown by horizontal red lines and given in parentheses at tops of bars) of extant species Threatened vertebrates occur mainly in trop- considered Threatened if Data Deficient species are Threatened in the same proportion as data-sufficient ical regions (Fig. 2), and these concentrations species. Numbers above the bars represent numbers of extant species assessed in the group; asterisks are generally disproportionately high even

indicate those groups in which estimates are derived from a randomized sampling approach. when accounting for their high overall species www.sciencemag.org Downloaded from

Fig. 2. Global patterns of threat, for land (terrestrial and freshwater, in brown) and marine (in blue) vertebrates, based on the number of globally Threatened species in total.

www.sciencemag.org SCIENCE VOL 330 10 DECEMBER 2010 1505 RESEARCH ARTICLE

richness (fig. S4, A and B). These patterns with intensive direct and indirect anthropogenic To investigate temporal trends in extinction highlight regions where large numbers of spe- pressures, such as (18)andfish- risk of vertebrates, we used the IUCN Red List cies with restricted distributions (17) coincide eries (19). Index (RLI) methodology (20)thathasbeen

Table 1. Net number of species qualifying for revised IUCN Red List cat- teriorating in status (i.e., moving from a lower to a higher category of threat) egories between assessments owing to genuine improvement or deterioration are indicated by “–”. Species changing categories for nongenuine reasons, in status, for birds (1988 to 2008), mammals (1996 to 2008), and amphibians such as improved knowledge or revised taxonomy, are excluded. In the case of (1980 to 2004). Category abbreviations are as for Fig. 1; CR(PE/PEW) denotes birds, for which multiple assessments have been undertaken, values in Critically Endangered (Possibly Extinct or Possibly Extinct in the Wild). CR parentheses correspond to the sum of all changes between consecutive as- excludes PE/PEW. Species undergoing an improvement (i.e., moving from a sessments; the same species may therefore contribute to the table more than higher to a lower category of threat) are indicated by “+”; species de- once [see (16)].

Red List category at end of period CR EX EW (PE/PEW) CR EN VU NT LC Birds EX 0 0 0 0 0 0 0 EW 0 0 +1 (+1) 0 0 0 0 CR (PE/PEW) 0 0 0 0 0 0 0 CR –2(–2) –2(–2) –7(–7) +16 (+19) +1 (+3) 0 0 EN 0 0 0 –22 (–27) +4 (+5) 0 0 VU 0 0 0 –10 (–11) –34 (–41) +9 (+10) 0 (+1) NT 0 0 0 –4(–4) –5(–2) –40 (–47) +1 (+1) LC 0 0 0 –1(0) –5(–4) –5(–5) –78 (–81) Mammals EX 0 0 0 0 0 0 0

EW 0 0 +1 +1 0 0 0 on August 25, 2012 Red List CR (PE/PEW) 0 0 0 0 0 0 0 category CR 0 –1 –3+3+200 at start of EN 0 0 0 –31 +3 +1 0 period VU 0 0 0 –2 –39 +5 +1 NT 0 0 0 –1 –4 –47 +7 LC 0 0 0 0 –2 –2 –39 Amphibians EX 0 0 0 0 0 0 0 EW 0 0 0 0 0 0 0 – CR (PE/PEW) 20 0 0 0 0 0 www.sciencemag.org CR –3 –1 –34 0 +2 0 0 EN –20–42 –77 0 +2 0 VU –20–19 –51 –45 0 0 NT 0 0 0 –7 –18 –32 0 LC 0 0 0 –3 –8 –20 –92 Downloaded from Fig. 3. (A) Trends in the Red List Index (RLI) for the world’sbirds,mam- mals, and amphibians. (B to D)Ob- served change in the RLI for each group (black) compared with RLI trends that would be expected if species that un- derwent an improvement in status due to conservation action had undergone no change (red). The difference is at- tributable to conservation. An RLI value of 1 equates to all species being Least Concern; an RLI value of 0 equates to all species being Extinct. Improvements in species conservation status lead to increases in the RLI; deteriorations lead to declines. A downward trend in the RLI value means that the net expected rate of species extinctions is increasing. Shading shows 95% confidence inter- vals. Note: RLI scales for (B), (C), and (D) vary.

1506 10 DECEMBER 2010 VOL 330 SCIENCE www.sciencemag.org RESEARCH ARTICLE adopted for reporting against global targets was one of 72 bird species to deteriorate one 2008. Note that the RLI does not reflect on- (1, 2). We calculated the change in RLI for Red List category between 1994 and 2000, from going population changes that are occurring too birds (1988, 1994, 2000, 2004, and 2008), mam- Least Concern to Near Threatened, mainly be- slowly to trigger change to different categories of mals (1996 and 2008), and amphibians (1980 cause of accelerating habitat loss in the Sundaic threat. Other indicators based on vertebrate pop- and 2004); global trend data are not yet avail- lowlands in the 1990s. Such a deterioration in ulation sizes showed declines of 30% between able for other vertebrate groups, although re- a species’ conservation status leads to a decline 1970and2007(1, 2, 22). gional indices have been developed (21). The in the RLI (corresponding to increased aggre- Global patterns of increase in overall ex- RLI methodology is explained in detail in (16), gated extinction risk); an improvement would tinction risk are most marked in Southeast Asia but in summary the index is an aggregated mea- lead to an increase in the RLI. (Fig. 4 and figs. S5A and S6). It is known that sure of extinction risk calculated from the Red Temporal trajectories reveal declining RLIs the planting of perennial export crops (such as List categories of all assessed species in a taxon, for all three taxa. Among birds, the RLI (Fig. oil palm), commercial hardwood timber op- excluding Data Deficient species. Changes in 3A) showed that their status deteriorated from erations, agricultural conversion to rice paddies, the RLI over time result from species changing 1988 to 2008, with index values declining by and unsustainable hunting have been detrimen- categories between assessments (Table 1). Only 0.49%, an average of 0.02% per year (table S4). tal to species in the region (23), but here we real improvements or deteriorations in status For mammals, the RLI declined by 0.8% from show the accelerating rate at which these forces (termed “genuine” changes) are considered; re- 1996 to 2008, a faster rate (0.07% per year) are driving change. In California, Central Amer- categorizations attributable to improved knowl- than for birds. Proportionally, amphibians were ica, the tropical Andean regions of South Amer- edge, taxonomy, or criteria change (“nongenuine” more threatened than either birds or mammals; ica, and Australia, patterns have been driven changes) are excluded (22). Accordingly, the RLI values declined 3.4% from 1980 to 2004 mainly by the “enigmatic” deteriorations among RLI is calculated only after earlier Red List cat- (0.14% per year). Although the absolute and amphibians (24), which have increasingly been egorizations are retrospectively corrected using proportional declines in RLIs for each taxo- linked to the infectious disease chytridiomy- current information and taxonomy, to ensure that nomic group were small, these represent con- cosis, caused by the presumed invasive fungal the same species are considered throughout and siderable biodiversity losses. For example, the pathogen Batrachochytrium dendrobatidis (25). that only genuine changes are included. For ex- deterioration for amphibians was equivalent to Almost 40 amphibians have deteriorated in ample, the greater red musk shrew (Crocidura 662 amphibian species each moving one Red status by three or more IUCN Red List cate- flavescens) was classified as Vulnerable in 1996 List category closer to extinction over the as- gories between 1980 and 2004 (Table 1). and as Least Concern in 2008; however, cur- sessment period. The deteriorations for birds Although chytridiomycosis has been perhaps on August 25, 2012 rent evidence indicates that the species was also and mammals equate to 223 and 156 species, the most virulent threat affecting vertebrates to Least Concern in 1996, and the apparent im- respectively, deteriorating at least one category. emerge in recent years, it is not the only novel provement is therefore a nongenuine change. In On average, 52 species per year moved one Red cause of rapid declines. The toxic effects of the contrast, Hose’s broadbill (Calyptomena hosii) List category closer to extinction from 1980 to veterinary drug diclofenac on Asian vultures have www.sciencemag.org Downloaded from

Fig. 4. Global patterns of net change in overall extinction risk across cosmopolitan distributions (e.g., the humpback whale). Deteriorations on birds, mammals, and amphibians (for the periods plotted in Fig. 3) islands [e.g., the nightingale reed-warbler (Acrocephalus luscinius)inthe mapped as average number of genuine Red List category changes per Northern Mariana Islands] and improvements on islands [e.g., the cell per year. Purple corresponds to net deterioration (i.e., net increase Rarotonga monarch (Pomarea dimidiata) in the Cook Islands] are hard to in extinction risk) in that cell; green, net improvement (i.e., decrease in discern; islands showing overall net improvements are shown in blue. extinction risk); white, no change. The uniform pattern of improvement Note that the intensity of improvements never matches the intensity of at sea is driven by improvements of migratory marine mammals with deteriorations.

www.sciencemag.org SCIENCE VOL 330 10 DECEMBER 2010 1507 RESEARCH ARTICLE

caused estimated population declines exceeding and birds, where the history of conservation ex- of a 1992 U.N. moratorium on large-scale pe- 99% over the past two decades in certain Gyps tends farther back and where the bulk of species- lagic driftnet fisheries]. species, and have resulted in three species moving focused conservation funding and attention is Confronting threats. Species recovery is from Near Threatened to Critically Endangered directed (31). Only four amphibian species un- complex and case-specific, but threat mitigation between 1994 and 2000. Numbers of Tasmanian derwent improvements, because the amphib- is always required. We investigated the main devils (Sarcophilus harrisii)havefallenbymore ian extinction crisis is such a new phenomenon drivers of increased extinction risk by identify- than 60% in the past 10 years because of the and a plan for action has only recently been ing, for each species that deteriorated in status, emergence of devil facial tumor disease (result- developed (32). the primary threat responsible for that change. To ing in three step changes from Least Concern to To estimate the impact of conservation suc- understand which drivers of increased extinction Endangered). Climate change is not yet ade- cesses, we compared the observed changes in risk are being mitigated most successfully, we quately captured by the IUCN Red List (26, 27) the RLI with the RLI trends expected if all 64 identified, for each species that improved in sta- but has been directly implicated in the deterio- species that underwent an improvement in tus, the primary threat offset by successful con- rating status of several vertebrates and may in- status due to conservation action had not done servation (table S6). teract with other threats to hasten extinction (28). so (16). Our explicit assumption is that in the We found that for any single threat, re- However, there is no evidence of a parallel to the absence of conservation, these species would gardless of the taxa involved, deteriorations systemwide deteriorations documented for reef- have remained unchanged in their original cat- outnumber improvements; conservation actions building corals affected by bleaching events egory, although we note that this approach is have not yet succeeded in offsetting any ma- related to El Niño–Southern Oscillation occur- conservative because it is likely that some would jor driver of increased extinction risk (fig. S7). rences (29). have deteriorated [in the sense of (6)]. The re- On a per-species basis, amphibians are in an Most deteriorations in status are reversible, sulting difference between the two RLIs can be especially dire situation, suffering the double but in 13% of cases they have resulted in extinc- attributed to conservation. We show that the in- jeopardy of exceptionally high levels of threat tion. Two bird species—the kamao (Myadestes dex would have declined by an additional 18% coupled with low levels of conservation effort. myadestinus) from Hawaii and the Alaotra grebe for both birds and mammals in the absence of Still, there are conservation successes among (Tachybaptus rufolavatus) from Madagascar— conservation (Fig. 3, B and C, and table S4). There birds and mammals, and here we investigate became extinct between 1988 and 2008, and a was little difference for amphibians (+1.4%; Fig. the degree to which particular threats have been further six Critically Endangered species have 3D) given the paucity of species improvements. addressed.

been flagged as “possibly extinct” during this For birds, conservation action reduced the de- Conservation actions have been relatively on August 25, 2012 period (Table 1 and table S5). At least nine am- cline in the RLI from 0.58% to 0.49%, equivalent successful at offsetting the threat of invasive phibian species vanished during the two decades to preventing 39 species each moving one Red alien species for birds and mammals: For every after 1980, including the golden toad (Incilius List category closer to extinction between 1988 five species that deteriorated in status because periglenes) from Costa Rica and both of Austra- and 2008. For mammals, conservation action of this threat, two improved through its mit- lia’s unique gastric-brooding frog species (genus reduced the RLI decline from 0.94% to 0.8%, igation. These successes have resulted from the Rheobatrachus); a further 95 became possibly equivalent to preventing 29 species moving one implementation of targeted control or eradica- extinct, 18 of them harlequin toads in the Neo- category closer to extinction between 1996 and tion programs [e.g., introduced cats have been tropical genus Atelopus (23% of species). No 2008. eradicated from 37 islands since the mid-1980s

mammals are listed as Extinct for the period These results grossly underestimate the im- (34)] coupled with reintroduction initiatives [e.g., www.sciencemag.org 1996 to 2008, although the possible extinction pact of conservation, because they do not ac- the Seychelles magpie-robin (Copsychus sechel- of the Yangtze River dolphin (Lipotes vexillifer) count for species that either (i) would have larum) population was 12 to 15 birds in 1965 would be the first megafauna vertebrate species deteriorated further in the absence of conser- but had increased to 150 birds by 2005 (fig. extinction since the Caribbean in the vation actions, or (ii) improved numerically, al- S8)]. Many of these improvements have oc- 1950s (30). though not enough to change Red List status. curred on small islands but also in Australia, Estimates of conservation success. These As an example among the former, the black owing in part to control of the red ( results support previous findings that the state stilt (Himantopus novaezelandiae) would have vulpes) (Fig. 4 and fig. S5B). However, among

of biodiversity continues to decline, despite in- gone extinct were it not for reintroduction and amphibians, only a single species—the Mallor- Downloaded from creasing trends in responses such as protected predator control efforts, and its Critically En- can midwife toad (Alytes muletensis)—improved areas coverage and adoption of national legislation dangered listing has thus remained unchanged in status as a result of mitigation of the threat (1, 2). Next, we asked whether conservation (6). Among the latter, conservation efforts im- posed by invasive alien species, compared with efforts have made any measurable contribution proved the total population numbers of 33 Crit- 208 species that deteriorated. This is because to reducing declines or improving the status of ically Endangered birds during the period 1994 there is still a lack of understanding of the path- biodiversity. to 2004, but not sufficiently for any species to ways by which chytridiomycosis is spread and The RLI trends reported here are derived be moved to a lower category of threat (33). As may be controlled, and in situ conservation man- from 928 cases of recategorization on the IUCN many as 9% of mammals, birds, and amphib- agement options are only just beginning to be Red List (Table 1 and table S6), but not all of ians classified as Threatened or Near Threat- identified [e.g., (35)]. Meanwhile, the establish- these refer to deteriorations. In 7% of cases ened have stable or increasing populations (15) ment of select, targeted captive populations with (68/928), species underwent an improvement in largely due to conservation efforts, but it will the goal of reintroducing species in the wild status, all but four due to conservation action. take time for these successes to translate into may offer valuable opportunities once impacts For example, the Asian crested ibis (Nipponia improvements in status. Conservation efforts in their native habitat are brought under control nippon) changed from Critically Endangered have also helped to avoid the deterioration in [e.g., the Kihansi spray toad (Nectophrynoides in 1994 to Endangered in 2000 owing to pro- status of Least Concern species. Finally, con- asperginis), categorized as Extinct in the Wild tection of nesting trees, control of agrochem- servation actions have benefited many other because of drastic alteration of its spray zone icals in rice fields, and prohibition of firearms; Threatened species besides birds, mammals, and habitat]. the four exceptions were improvements result- amphibians, but this cannot yet be quantified For mammals and birds, the threats lead- ing from natural processes, such as unassisted through the RLI for groups that have been ing to habitat loss have been less effectively habitat regeneration (tables S7 and S8). Nearly assessed only once [e.g., salmon shark (Lamna addressed relative to that of invasive alien spe- all of these improvements involved mammals ditropis) numbers have improved as the result cies: For every 10 species deteriorating as a

1508 10 DECEMBER 2010 VOL 330 SCIENCE www.sciencemag.org RESEARCH ARTICLE result of agricultural expansion, fewer than 1 Binding legislation and harvest management in CBD (UNEP, Nairobi, 2002); www.cbd.int/doc/ improved because of mitigation of this threat. strategies also are urgently needed to address meetings/cop/cop-06/official/cop-06-20-en.pdf. 6. S. H. M. Butchart, A. J. Stattersfield, N. J. Collar, Oryx 40, Protected areas are an essential tool to safe- the disproportionate impact of fisheries on 266 (2006). guard biodiversity from habitat loss, but the cartilaginous fishes (fig. S10). 7. A. S. L. Rodrigues, Science 313, 1051 (2006). protected areas network remains incomplete We have no data on the relationship between 8. P. F. Donald et al., Science 317, 810 (2007). and nonstrategic relative to Threatened species expenditure on biodiversity and conservation suc- 9. T. M. Brooks, S. J. Wright, D. Sheil, Conserv. Biol. 23, 1448 (2009). (17), and reserve management can be ineffec- cess. A disproportionate percentage of annual 10. P. J. Ferraro, S. K. Pattanayak, PLoS Biol. 4, e105 tive (36). Numerous Threatened species are re- conservation funding is spent in economically (2006). stricted to single sites, many still unprotected wealthy countries (41), where there are generally 11. J. W. Terborgh, Conserv. Biol. 2, 402 (1988). (37), and these present key opportunities to fewer Threatened species (Fig. 2 and fig. S4B) 12. B. Clucas, K. Mchugh, T. Caro, Biodivers. Conserv. 17, slow rates of extinction. In the broader matrix of and the disparity between success and failure 1517 (2008). 13. J. E. M. Baillie et al., Cons. Lett. 1, 18 (2008). unprotected land, agri-environmental schemes appears less evident (Fig. 4). Southeast Asia, by 14. G. M. Mace et al., Conserv. Biol. 22, 1424 could offer important biodiversity benefits, pro- contrast, has the greatest imbalance between (2008). vided that management policies are sufficient improving and deteriorating trends, emphasizing 15. IUCN Red List of Threatened Species. Version 2010.3 to enhance populations of Threatened species the need there for greater investment of resources (IUCN, 2010; www.iucnredlist.org). 16. See supporting material on Science Online. (38). and effort. 17. A. S. L. Rodrigues et al., Bioscience 54, 1092 Hunting has been relatively poorly addressed Conclusions. Our study confirms previous (2004). in mammals (62 deteriorations, 6 improve- reports of continued biodiversity losses. We 18. M. C. Hansen et al., Proc. Natl. Acad. Sci. U.S.A. 105, ments) when compared with birds (31 deteriora- also find evidence of notable conservation suc- 9439 (2008). 19. B. Worm et al., Science 325, 578 (2009). tions, 9 improvements). In birds, successes have cesses illustrating that targeted, strategic con- 20. S. H. M. Butchart et al., PLoS One 2, e140 (2007). resulted mainly from targeted protection [e.g., servation action can reduce the rate of loss 21. N. K. Dulvy, S. Jennings, S. I. Rogers, D. L. Maxwell, Lear’s macaw (Anodorhynchus leari) changed relative to that anticipated without such ef- Can. J. Fish. Aquat. Sci. 63, 1267 (2006). from Critically Endangered to Endangered as forts. Nonetheless, the current level of action is 22. B. Collen et al., Conserv. Biol. 23, 317 (2009). 23. N. S. Sodhi, L. P. Koh, B. W. Brook, P. K. Ng, Trends Ecol. a result of active protection of the Toca Velha/ outweighed by the magnitude of threat, and Evol. 19, 654 (2004). Serra Branca cliffs in Brazil], but also from en- conservation responses will need to be sub- 24. S. N. Stuart et al., Science 306, 1783 (2004); forcement of legislation (e.g., hunting bans) and stantially scaled up to combat the extinction cri- 10.1126/science.1103538. harvest management measures. Many mammals sis. Even with recoveries, many species remain 25. D. B. Wake, V. T. Vredenburg, Proc. Natl. Acad. Sci. U.S.A. on August 25, 2012 subject to hunting occur at low densities, have conservation-dependent, requiring sustained, 105 (suppl. 1), 11466 (2008). 26. H. R. Akçakaya, S. H. M. Butchart, G. M. Mace, large home ranges, and/or are large-bodied. Al- long-term investment (42); for example, actions S. N. Stuart, C. Hilton-Taylor, Glob. Change Biol. 12, though active site-based protection has contrib- have been under way for 30 years for the golden 2037 (2006). uted to an improvement in the status of some lion tamarin (Leontopithecus rosalia), 70 years 27. B. W. Brook et al., Biol. Lett. 5, 723 (2009). of these species, site protection alone is often for the whooping crane (Grus americana), and 28. W. F. Laurance, D. C. Useche, Conserv. Biol. 23, 1427 (2009). insufficient if not complemented by appropriate 115 years for the white rhinoceros (Ceratothe- 29. K. E. Carpenter et al., Science 321, 560 (2008); legislation, biological management, and effec- rium simum). 10.1126/science.1159196. tive enforcement (39). For example, a combina- Halting biodiversity loss will require coordi- 30. S. T. Turvey et al., Biol. Lett. 3, 537 (2007). 31. N. Sitas, J. E. M. Baillie, N. J. B. Isaac, Anim. Conserv. 12, tion of the Convention on International Trade nated efforts to safeguard and effectively man- www.sciencemag.org 231 (2009). in Endangered Species of Wild Flora and Fauna age critical sites, complemented by broad-scale 32. C. Gascon et al., Eds., Amphibian Conservation Action (CITES) and enactment of the Vicuña Conven- action to minimize further destruction, degra- Plan (IUCN/SSC Amphibian Specialist Group, Gland, tion, which prohibited domestic exploitation and dation, and fragmentation of habitats (37, 39) Switzerland, 2007). mandated the establishment of protected areas, and to promote sustainable use of productive 33. M. de L. Brooke et al., Conserv. Biol. 22, 417 (2008). has helped to improve the status of the vicuña lands and waters in a way that is supportive to 34. M. Nogales et al., Conserv. Biol. 18, 310 (2004). (Vicugna vicugna) from Near Threatened to Least biodiversity. Effective implementation and en- 35. R. N. Harris et al., ISME J. 3, 818 (2009). Concern. forcement of appropriate legislation could deliver 36. L. M. Curran et al., Science 303, 1000 (2004).

The threat of fisheries has been mitigated quick successes; for example, by-catch mitiga- 37. T. H. Ricketts et al., Proc. Natl. Acad. Sci. U.S.A. 102, Downloaded from relatively more effectively for marine mammals tion measures, shark-finning bans, and mean- 18497 (2005). 38. D. Kleijn et al., Ecol. Lett. 9, 243 (2006). (4 deteriorations, 2 improvements) than for birds ingful catch limits have considerable potential 39. C. Boyd et al., Cons. Lett. 1, 37 (2008). (10 deteriorations, 0 improvements), reflecting to reduce declines in marine species (19). The 40. J. Cooper et al., Mar. Ornithol. 34, 1 (2006). both the time when drivers first emerged and the 2010 biodiversity target may not have been met, 41. A. N. James, K. J. Gaston, A. Balmford, Nature 401, past influence of supranational conservation but conservation efforts have not been a failure. 323 (1999). 42. J. M. Scott, D. D. Goble, A. M. Haines, J. A. Wiens, policy. Among historically exploited, long-lived The challenge is to remedy the current shortfall M. C. Neel, Cons. Lett. 3, 91 (2010). mammals, for example, the humpback whale in conservation action to halt the attrition of 43. We are indebted to the more than 3000 species (Megaptera novaeangliae) has benefited from global biodiversity. experts who devoted their knowledge, intellect, and time protection from commercial whaling (since to the compilation of vertebrate data on the IUCN Red List. Full acknowledgments are provided in the supporting 1955) and has improved from Vulnerable to References and Notes online material. Least Concern. Declines among slow-breeding 1. S. H. M. Butchart et al., Science 328, 1164 (2010); seabirds (particularly albatrosses and petrels; fig. 10.1126/science.1187512. S9) are mainly a consequence of increasing 2. Secretariat of the Convention on Biological Diversity, Supporting Online Material www.sciencemag.org/cgi/content/full/science.1194442/DC1 incidental by-catch resulting from the growth of Global Biodiversity Outlook 3 (Convention on Biological Diversity, Montréal, 2010). Materials and Methods commercial fisheries, primarily those that use 3. S. L. Pimm, G. J. Russell, J. L. Gittleman, T. M. Brooks, Figs. S1 to S10 long-line and trawling methods. Legislative Science 269, 347 (1995). Tables S1 to S9 tools, such as the recently enacted multilateral 4. TEEB, The Economics and Ecosystems of Biodiversity: References Acknowledgments Agreement on the Conservation of Albatrosses An Interim Report (European Communities, Cambridge, 2008). and Petrels (40), may yet deliver dividends by 5. UNEP, Report of the Sixth Meeting of the Conference of 29 June 2010; accepted 11 October 2010 coordinating international action to reduce fish- the Parties to the Convention on Biological Diversity Published online 26 October 2010; eries mortality of these highly migratory species. (UNEP/CBD/COP/20/Part 2) Strategic Plan Decision VI/26 10.1126/science.1194442

www.sciencemag.org SCIENCE VOL 330 10 DECEMBER 2010 1509 letters to nature

Received 9 October 2001; accepted 17 January 2002......

1. Sparks, R. S. J., Wilson, L. & Hulme, G. Theoretical modeling of the generation, movement, and emplacement of pyroclastic ¯ows by column collapse. J. Geophys. Res. 83, 1727±1739 Global environmental controls of (1978). 2. Valentine, G. A. & Wolhletz, K. H. Numerical models of Plinian eruption columns and pyroclastic diversity in large herbivores ¯ows. J. Geophys. Res. 94, 1867±1887 (1989). 3. Dobran, F., Neri, A. & Macedonio, G. Numerical simulation of collapsing volcanic columns. Han Olff*, Mark E. Ritchie² & Herbert H. T. Prins* J. Geophys. Res. 98, 4231±4259 (1993). 4. Neri, A. & Macedonio, G. Numerical simulation of collapsing volcanic columns with particles of two sizes. J. Geophys. Res. 101, 8153±8174 (1996). * Tropical Nature Conservation and Vertebrate Ecology Group, Wageningen 5. Oberhuber, J. M., Herzog, M., Graf, H. F. & Schwanke, K. Volcanic plume simulation on large scales. University, Bornsesteeg 69, 6708 PD Wageningen, The Netherlands J. Volcanol. Geotherm. Res. 87, 29±53 (1998). ² Department of Biology, Syracuse University, Syracuse, New York 13244, USA 6. Self, S., Wilson, L. & Nairn, I. A. Vulcanian eruption mechanisms. Nature 277, 440±443 (1979)...... 7. Turcotte, D. L., Ockendon, H., Ockendon, J. R. & Cowley, S. J. A mathematical model of Vulcanian eruptions. Geophys. J. Int. 103, 211±217 (1990). Large mammalian herbivores occupy half of the earth's land 1 8. Fagents, S. A. & Wilson, L. Explosive volcanic eruptionsÐVII. The ranges of pyroclastics ejected in surface and are important both ecologically and economically , transient volcanic explosions. Geophys. J. Int. 113, 359±370 (1993). but their diversity is threatened by human activities2. We inves- 9. Woods, A. W. A model of Vulcanian explosions. Nucl. Eng. Des. 155, 345±357 (1995). tigated how the diversity of large herbivores changes across 10. Kieffer, S. W. Fluid dynamics of the May 18 blast at Mount St. Helens. US Geol. Surv. Prof. Pap. 1250, 379±400 (1981). gradients of global precipitation and soil fertility. Here we show 11. Wohletz, K. H., McGetchin, T. R., Sandford, M. T. & Jones, E. M. Hydrodynamic aspects of caldera- that more plant-available moisture reduces the nutrient content forming eruptions: numerical models. J. Geophys. Res. 89, 8269±8285 (1984). of plants but increases productivity, whereas more plant-available 12. Neri, A., Di Muro, A. & Rosi, M. Mass partition during collapsing and transitional columns by using numerical simulations. J. Volcanol. Geotherm. Res. (in the press). nutrients increase both of these factors. Because larger herbivore 13. Neri, A. Multiphase Flow Modelling and Simulation of Explosive Volcanic Eruptions. Thesis, Illinois Inst. species tolerate lower plant nutrient content but require greater Technol. (1998). plant abundance, the highest potential herbivore diversity should 14. Neri, A., Macedonio, G., Gidaspow, D. & Esposti Ongaro, T. Multiparticle Simulation of Collapsing occur in locations with intermediate moisture and high nutrients. Volcanic Columns and Pyroclastic Flows (Volcanic Simulation Group Report 2001±2, Instituto Nazionale di Geo®sica e Vulcanologia, Pisa, 2001). These areas are dry enough to yield high quality plants and 15. Amsden, A. A. & Harlow, F. H. KACHINA: An Eulerian Computer Program for Multi®eld Fluid Flows support smaller herbivores, but productive enough to support (Report LA-5680, Los Alamos National Laboratory, Los Alamos, 1974). larger herbivores. These predictions ®t with observed patterns of 16. Rivard, W. C. & Torrey, M. D. K-FIX: A Computer Program for Transient, Two-dimensional, Two-¯uid body size and diversity for large mammalian herbivores in North Flow (Report LA-NUREG-6623, Los Alamos National Laboratory, Los Alamos, 1977). 17. Gidaspow, D. Multiphase Flow and Fluidization: Continuum and Kinetic Theory Descriptions America, Africa and Australia, and yield a global map of regions (Academic, New York, 1994). with potentially high herbivore diversity. Thus, gradients of 18. Voight, B. et al. Magma ¯ow instability and cyclic activity at SoufrieÁre Hills Volcano, Montserrat. precipitation, temperature and soil fertility might explain the Science 283, 1138±1142 (1999). 19. Wilson, L., Sparks, R. S. J. & Walker, G. P. L. Explosive volcanic eruptions IV. The control of magma global distribution of large herbivore diversity and help to properties and conduit geometry on eruption column behaviour. Geophys. J. R. Astron. Soc. 63, 117± identify crucial areas for conservation and restoration. 148 (1980). Previous studies have linked rainfall, soil fertility and primary 20. Sparks, R. S. J. Causes and consequences of pressurisation in lava dome eruptions. Earth Planet. Sci. productivity to total herbivore community biomass3±5, plant qual- Lett. 150, 177±189 (1997). 6±8 9±12 21. Devine, J. D., Rutherford, M. J. & Barclay, J. Changing magma conditions and ascent rates during the ity and species richness of herbivores , but have not explained 13 SoufrieÁre Hills eruption on Montserrat. GSA Today 8, 2±7 (1998). why and how these factors affect herbivore diversity . The ability of 22. Barclay, J. et al. Experimental phase equilibria constraints on pre-eruptive storage conditions of the large herbivores (mass . 2 kg) to persist probably changes across SoufrieÁre Hills magma. Geophys. Res. Lett. 25, 3437±3440 (1998). gradients of plant abundance and quality. Plant productivity and 23. Murphy, M. D., Sparks, R. S. J., Barclay, J., Carroll, M. R. & Brewer, T. S. Remobilization of andesite magma by intrusion of ma®c magma at the SoufrieÁre Hills Volcano, Montserrat, West Indies. J. Petrol. quality are in¯uenced by the availability of two principal plant 41, 21±42 (2000). resources, water and nutrients, and thus change across environ- 24. Jaupart, C. & AlleÁgre, C. J. Gas content, eruption rate and instabilities of eruption regime in silicic mental gradients of these resources14. Previous results15 have shown volcanoes. Earth Planet. Sci. Lett. 102, 413±429 (1991). 25. Druitt, T. H. et al. The Explosive Eruptions of August 1997 (Special Report 04, Montserrat Volcano that plant abundance, as measured by the equilibrium biomass of Observatory, Salem, Montserrat, 1998). ungrazed plants, increases linearly with rainfallÐa crude measure 26. Hoblitt, R. P. Observations of the eruptions of July 22 and August 7 1980 at Mount St Helens, of plant-available moisture. This increase is stronger at higher Washington. US Geol. Surv. Prof. Pap. 1335, (1986). nutrient availability (Fig. 1a). However, leaf tissue nitrogen content, 27. Wolf, T. Der Cotopaxi und seine letzte Eruption am 26 Juni 1877. Neues Jb. Miner. Geol. PalaÈont. 113± 167 (1878). an index of plant quality to herbivores, decreases with plant- 28. Taylor, G. A. The 1951 eruption of Mount Lamington, Papua. Aust. Bur. Min. Resour. Geol. Geophys. available moisture even though it also increases with plant-available Bull. 38, 1±117 (1958). nutrients (Fig. 1b). Similar patterns occur with plant phosphorus 29. Formenti, Y. & Druitt, T. H. in Abstracts and Addresses of the IAVCEI General Assembly 2000 232 content15,16. (Volcanological Survey of Indonesia, Bandung, Indonesia, 2000). 30. Melnik, O. & Sparks, R. S. J. Nonlinear dynamics of lava dome extrusion. Nature 402, 37±41 These combined effects imply that plant abundance and nutrient (1999). content show different response surfaces to moisture and nutrients (Fig. 1c, d). Plant abundance is lowest at either low moisture or low nutrient availability, and highest when both are high (Fig. 1c). By Acknowledgements contrast, plant nutrient content is lowest at combinations of high We thank our colleagues at Montserrat Volcano Observatory for their assistance, especially C. Bonadonna, T. Druitt, C. Harford, R. Herd, R. Luckett and R.E.A. Robertson, our plant-available moisture and low nutrients, and highest at combi- colleagues during the August explosions. Support for monitoring was provided by the nations of low plant-available moisture and high nutrients. We Department for International Development (UK), the British Geological Survey (BGS), expect the contours of the response surface for plant nutrient the Seismic Research Unit of the University of the West Indies, and the US Geological content to be concave at low moisture and relatively horizontal at Survey (USGS). A.C. and B.V. acknowledge support from the US NSF. A.N. and G.M. were high moisture (Fig. 1d), because an increase in nutrients will assisted by the Istituto Nazionale di Geo®sica e Vulcanologia, and Gruppo Nazionale per la Vulcanologia INGV, Italy. B.V. was a Senior Scientist at Montserrat in 1997 with BGS, and increase plant nutrient content more strongly at low than at high was also af®liated with the USGS Volcano Hazards Program. We thank M. Rutherford for moisture17 (Fig. 1b). comments. The two response surfaces for plant abundance and nutrient content can be combined to de®ne potential conditions for the Competing interests statement presence of large herbivores. A given herbivore species must The authors declare that they have no competing ®nancial interests. encounter plants of both suf®cient abundance and quality to persist, and therefore may be constrained to persist only under certain Correspondence and requests for materials should be addressed to A.B.C. conditions of plant-available moisture and nutrients. These condi- (e-mail: [email protected]). tions can be de®ned in a graphical model by two proposed

NATURE | VOL 415 | 21 FEBRUARY 2002 | www.nature.com © 2002 Macmillan Magazines Ltd 901 letters to nature thresholds of combinations of moisture and nutrients that allow The plant abundance threshold of larger herbivores will be shifted plants of suf®cient quality and abundance for a herbivore's persis- farther from the origin, but their plant quality threshold will be tence (Fig. 2a). A speci®c contour of the plant abundance response more horizontal and shifted to wetter conditions (Fig. 2b). Smaller surface (Fig. 1c) will correspond to the plant abundance require- herbivores should have abundance thresholds closer to the origin, ments of a herbivore, and represents the `plant abundance thresh- plus more sharply concave quality thresholds shifted towards drier, old' of the herbivore. Similarly, a speci®c contour of the plant more fertile conditions. nutrient content response surface (Fig. 1d) will correspond to the Thus, the occurrence of larger herbivores is expected to increase plant quality requirements of a herbivore, and represents the `plant with greater moisture, but to be relatively independent of plant- quality threshold' of the herbivore. available nutrients. In contrast, smaller herbivores should decrease The plant abundance threshold of a herbivore species is the in occurrence with greater moisture and increase with greater minimum plant-available moisture, for a given nutrient availability, nutrient availability. Therefore, the mean body size for all species above which plant productivity will be suf®ciently high to support a population of that herbivore species. Likewise, the plant quality threshold of a herbivore species is the maximum plant-available moisture, for a given nutrient availability, below which plant tissue is suf®ciently nutrient-rich for that herbivore species to persist. a b Together, the quality and abundance thresholds de®ne a `wedge' of 0 Body combinations of moisture and nutrients at which a herbivore Plant quality 2 mass threshold species can persist (Fig. 2a). 3 small The predicted potential diversity of different-sized herbivores at a 4 Grazer 0 2 3 5 certain combination of moisture and nutrients should re¯ect how persists 5 large many species can persist at those conditions. Larger herbivores 2 Plant abundance threshold Plant-available moisture Plant-available moisture 0 require more abundant plants but can tolerate lower plant quality Plant-available nutrients Plant-available nutrients than smaller herbivores, whereas smaller herbivores can persist on less-abundant plants but only if the plants are of higher c d Elephant Buffalo Zebra Thomson gazelle Klipspringer quality3,8,18±20. Thus, the plant abundance and quality thresholds 1.0 1.0 should differ across orders of magnitude in herbivore body sizes8. 0.8 0.8 0.6 0.6 0.4 0.4

Frequency 0.2 0.2 0 0 1–2 5–6 9–10 >12 0 to 0.50.5 to 1 –3 to –1.5–1.5 to–1 –1 to –0.5–0.5 to 0 Plant-available nutrients index Plant-available moisture index a c Plant abundance e f

) 1,000 1,000 1,500 –2 Fertilized 800 800 600 600 1,000 High 400 400 Unfertilized 200 200 500 0 0

Mean body mass (kg) 1-2 5-6 9-10 0 to 0.50.5 to 1 Plant-available nutrients index 0 –3 to –1.5–1.5 to–1 –1 to –0.5–0.5 to 0 Low Plant-available moisture index Plant biomass (g m 0 400 800 1,200

Rainfall (mm yr –1) Plant-available moisture Plant-available nutrients g h 50 r 2 = 0.16 50 r 2 = 0.28 b 40 40 4 Poor soils d Plant quality 30 30 Rich soils 20 20 3 10 10 species pool 0 0 % of continental 2 Low –3 –2 –1 0 1 2 0 5 10 15 20 Plant-available moisture index Plant-available nutrients index 1

Plant N conc. (%) 0 Figure 2 Predicted and observed patterns of herbivore diversity along gradients of plant- 0 400 800 1,200 available moisture and nutrients. a, Threshold combinations of plant-available moisture High Rainfall (mm yr –1) and nutrients that allow a hypothetical herbivore to persist. Plant abundance and plant Plant-available moisture Plant-available nutrients quality thresholds re¯ect shapes of the contours of the response surfaces for plant biomass and plant nutrient content, respectively. b, Hypothetical regions of persistence Figure 1 Plant biomass and tissue nitrogen content changes across rainfall gradients in for six different species that differ in body mass, as de®ned by plant abundance thresholds Africa. a, Ungrazed plant biomass (V, open circles) increases with rainfall (M) on poor soils (solid curves) and plant quality thresholds (dashed curves). Numbers indicate how many in West Africa (V=-46.32 + 0.34M; n=77, R 2 = 0.70, P , 0.001) and fertilized herbivore species can persist under different conditions of plant-available moisture and patches at the same sites (only the regression line is available)15,16. b, Whole-plant tissue nutrients. Note the greater overlap in regions of persistence at intermediate plant- nitrogen content (N ) at the same sites (open circles) decreases across the same rainfall available moisture and high plant-available nutrients. c, d, Frequency of occurrence of gradient on poor soils (N = 15.99M-0.45; n = 117, R 2 = 0.22, P , 0.001), as it does ®ve different-sized herbivore species (klipspringer, Oreotragus oreotragus; Thomson's on rich soils from East Africa (N = 822.14M-0.95; M 2 = 0.57, P=0.02)26±30. Plant gazelle, Gazella thomsoni; Burchell's zebra, Hippotigris quagga; Cape buffalo, Syncerus tissue phosphorus content on poor West African soils responded similarly to rainfall as caffer; elephant, Loxodonta africana) among 85 African parks in different intervals of tissue nitrogen content15,16. c, d, Hypothetical response surfaces for plant biomass indices for plant-available moisture (c) and plant-available nutrients (d). e, f, Body mass (c; abundance) and plant nutrient content (d) to plant-available moisture (balance of (mean 6 s.e.) of all species present in different intervals of indices for plant-available rainfall and potential evapotranspiration) and plant-available nutrients, inferred from moisture (e) and plant-available nutrients (f). g, h, Observed large herbivore species observed data in a and b. Contour shapes in c re¯ect the joint limitation of plant biomass richness, expressed as a percentage of the continental species pools from 118 sites in by water and soil nutrients. Contour shapes in d re¯ect the observed data in b, which North America and Africa versus indices for plant-available moisture (log10[precipitation/ show that plant nutrient content increases with plant-available nutrients more rapidly at potential evapotranspiration]), y = -3.81x2 - 6.53x + 14.93 (g), and plant-available low than at high plant-available moisture. nutrients (ref. 25, and Methods), y = 1.10x + 6.79 (h).

902 © 2002 Macmillan Magazines Ltd NATURE | VOL 415 | 21 FEBRUARY 2002 | www.nature.com letters to nature is expected ®rst to increase rapidly with plant-available moisture patterns for Africa and North America were similar. This pattern and then to level off, but to decrease continuously with plant- is unlikely to be caused by plant diversity (leading to more resource available nutrients (Fig. 2b). types), because plant diversity is typically highest at low soil The trade-off in requirements for plant quantity and quality for fertility23. It is also unlikely to be caused by non-food differences different-sized herbivores ultimately predicts general patterns of between habitats (for example, shelter to predation) as the patterns herbivore diversity across gradients of water availability and soil shown in Fig. 2g and h did not change substantially when the nutrients. At a given nutrient concentration, herbivore species analysis was restricted to include only sites that were primarily richness is predicted to peak at intermediate moisture because grassland. both small and large species occur together (Fig. 2b). For a given On a global scale, this empirical regression model (Table 1) moisture, however, herbivore species richness should increase con- predicts that there are regions that can support high herbivore tinuously with greater nutrients because more smaller species are diversity when applied to maps of our indices for plant-available added (Fig. 2b). The highest herbivore diversity is thus expected in moisture and nutrients (Methods and Fig. 3). To validate our locations that are not so wet and/or infertile that average plant regression model with independent data, we predicted large herbi- quality would be too low to sustain smaller herbivores, and also not vore species richness (as a percentage of continental pool) for ten so dry and/or infertile that plant productivity would be insuf®cient preserves and natural areas in Australia on the basis of our global to sustain larger herbivores (Fig. 2b). This prediction is insensitive to the shapes of the contours of plant abundance and nutrient content (Fig. 1a±d). We tested our predictions by compiling a data set of the observed occurrence and species richness of all terrestrial mammalian herbi- vores with a mass greater than 2 kg (grazers, mixed feeders and browsers) in 33 different protected natural areas in North America and 85 such areas in sub-Saharan Africa (Methods). For every site, we calculated indices for plant-available moisture and nutrients (Methods), and graphed changes in individual species, mean body mass and species richness along these gradients. We expressed species richness as a proportion of the total species richness per continent to standardize for differences between the two continents in size and biogeographical history21,22. Observed frequencies of occurrence of ®ve different-sized grazing mammals, chosen as representative examples, in 85 parks in Africa support our predictions for individual species (Fig. 2c, d). Large species (Cape buffalo and elephant) peaked in occurrence at higher plant-available moisture than did intermediate-sized herbivores (zebra, Thomson's gazelle), which in turn peaked in occurrence at higher water availability than did a small species (klipspringer). In addition, logistic regression showed that occurrence of the two largest species was independent of plant-available nutrients (P . 0.05), but that occurrence of the smaller three species increased with increasing plant-available nutrients (P , 0.05). As we predicted, the mean body mass of all species present at a site increased with increasing plant-available moisture, and decreased with increasing plant-available nutrients (Fig. 2e, f). Consistent with these results for individual species and mean body mass, and with our predictions of diversity patterns (Fig. 2b), we found that total herbivore species richness (as a percentage of the continental species pool) for Africa and North America together peaked at intermediate plant-available moisture (Fig. 2g) and increased continuously with plant-available nutrients (Fig. 2h). Multiple regression analysis (Table 1) showed that herbivore species richness increased linearly with plant-available nutrients and non- linearly (as a quadratic function) with plant-available moisture, and that each had a signi®cant effect. Separate herbivore diversity

Figure 3 Global distribution of large herbivore diversity, as predicted by indices for plant- available moisture and nutrients using a regression model obtained from data for African Table 1 Dependence of species richness on water and soil and North American parks. a, b, Maps of observed water supply and soil fertility indices, Coef®cient Regression Standard tPrespectively. c, Map of species richness of large herbivores, as a percentage of coef®cient error ...... continental species pool (Methods), predicted from indices for plant-available moisture Constant 8.091 1.483 5.46 , 0.001 and nutrients using the multiple regression model (Table 1, Fig. 2d). Continental species Soil fertility index (linear) 1.031 0.181 5.70 , 0.001 pools are North America, 25; Africa, 99; Central and South America, 18; Europe, 5; Water availability index (linear)² -3.639 1.489 -2.45 0.016 Water availability index (quadratic) -2.897 0.877 -3.30 , 0.001 Middle East, 11; North Africa, 8; India, 10; Northern Asia and Far East, 31; southeast Asia ...... and Indonesian archipelago, 10; Australia, 59. All maps represent a planar projection, at a Results of the multiple regression analysis of the dependence of large herbivore species richness (given as a percentage of the continental species pool; see Methods) on indices of water availability resolution of 0.58 longitude/latitude (a)or18 longitude/latitude (b, c). No data for potential and soil fertility are shown. evapotranspiration are available for the boreal zones in a, hence no diversity predictions ² This linear coef®cient was negative, despite a unimodal relationship (Fig. 2e), because water availability indices were mainly negative (potential evapotranspiration . rainfall). could be made for this region (c).

NATURE | VOL 415 | 21 FEBRUARY 2002 | www.nature.com © 2002 Macmillan Magazines Ltd 903 letters to nature map of plant-available moisture and nutrient indices. We found a crudely standardizes diversity relative to the potential number of species that could be strong correspondence between predicted and observed diversity present theoretically at a site. (R2 = 0.69, P = 0.003, n = 10). Regions of known high herbivore Received 28 September; accepted 6 December 2001. diversity in other regions and continents1,10,22 also seem to corre- spond to areas that are classi®ed as having high potential diversity 1. Owen-Smith, N. Megaherbivores. The In¯uence of Very Large Body Size on Ecology (Cambridge Univ. Press, Cambridge, 1988). by our global map. These include the Argentinian pampa, Gir Forest 2. Prins, H. H. T. The pastoral road to extinction: Competition between wildlife and traditional of India, steppes of Khazakstan and Mongolia, Cordillera of Spain, pastoralism in East Africa. Environ. Conserv. 19, 117±123 (1992). and the coastal region of Morocco and Algeria (Fig. 3c). 3. Bell, R. H. V. in Ecology of Tropical Savannas (eds Huntly, B. J. & Walker, B. H.) 193±216 (Springer, Extrapolating the predictions of our model to the global map Berlin, 1982). 4. East, R. Rainfall, nutrient status and biomass of large African savannah mammals. Afr. J. Ecol. 22, 245± yields potentially important insights about the global status of large 270 (1984). herbivore conservation. For example, the prime regions for large 5. McNaughton, S. J., Oesterheld, M., Frank, D. A. & Williams, K. J. Ecosystem-level patterns of primary herbivore diversity can host potentially more than 25% of the productivity and herbivory in terrestrial habitats. Nature 341, 142±144 (1989). 6. Coe, M. in Nitrogen as an Ecological Factor (eds Lee, J. A., McNeill, J. & Rorison, I. H.) 345±368 species in a continental species pool, but comprise only about 5% (Oxford, Blackwell, 1983). of the investigated land of the world (see Fig. 3c). Fewer than 2% of 7. Du Toit, J. T. & Owen-Smith, N. Body size, population metabolism and habitat specialization among the prime regions for large herbivore diversity overlap with regions large African herbivores. Am. Nat. 133, 736±740 (1989). designated as `general purpose' biodiversity hotspots24. Current 8. Belovsky, G. E. Optimal foraging and community structure: The allometry of herbivore food selection 25 and competition. Evol. Ecol. 11, 641±672 (1997). land-use practices suggest that more than half of the area of 9. Western, D. & Ssemakula, J. The future of savanna ecosystems: ecological islands or faunal enclaves? these prime regions has been already converted to agriculture and Afr. J. Ecol. 19, 7±19 (1981). lost its herbivore diversity. Another 25% of these prime regions may 10. Huston, M. A. Biological Diversity. The Coexistence of Species on Changing Landscapes (Cambridge be converted to agriculture in the next 25 yr. Thus, less than 1.2% of Univ. Press, Cambridge, 1994). 11. Danell, K. L. P. & Niemela, P. Species richness in mammalian herbivores: patterns in the boreal zone. the earth's surface might remain to support uniquely diverse, grazing Ecography 19, 404±409 (1996). ecosystems by 2025. Some regions, such as the northern Great Plains 12. Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, Cambridge, 1995). in North America, might be highly suitable for restoring large 13. Prins, H. H. T. & Olff, H. in Dynamics of Tropical Communities (eds Newbery, D., Prins, H. H. T. & Brown, G.) 449±489 (Blackwell Science, Oxford, 1998). herbivore diversity if agriculture were to be abandoned. 14. Walker, B. H. & Langridge, J. L. Predicting savanna vegetation structure on the basis of plant available Our approach is powerful because it identi®es how plant moisture (PAM) and plant available nutrients (PAN): A case study from Australia. J. Biogeogr. 24, resources constrain the distribution of herbivores of different 813±825 (1997). sizes. We can use this functional relationship to predict patterns 15. Breman, H. & De Wit, C. T. Rangeland productivity and exploitation in the Sahel. Science 221, 1341± 1347 (1983). in large herbivore diversity on a global scale. Similar approaches 16. Breman, H. & Krul, J. M. in La Productivite de PaÃturages SaheÂliens. Une Etude des Sols, des VeÂgeÂtations et might be applied to other groups of organisms to help to identify de l'Explotation de cette Ressource Naturelle (eds Penning de Vries, F. W. T. & Djiteye, M. A.) 322±345 crucial areas for current conservation and future restoration of (Pudoc, Wageningen, 1991). biodiversity. M 17. Milchunas, D. G., Varnamkhasti, A. S., Lauenroth, W. K. & Goetz, H. Forage quality in relation to long-term grazing history, current-year defoliation, and water resource. Oecologia 101, 366±374 (1995). Methods 18. Jarman, P. J. The social organization of antelope in relation to their ecology. Behaviour 48, 215±267 (1974). Data sources 19. Van Soest, P. J. Nutritional Ecology of the Ruminant: Ruminant Metabolism, Nutritional Strategies, Main data sources for species occurrences in protected areas in North America (34 sites) the Cellulolytic Fermentation and the Chemistry of Forages and Plant Fibres (O & B Books, and Africa (85 sites) were the Man and Biosphere Species Database (http://ice.ucdavis. Corvallis, 1982). edu/mab) and the UNEP-WCMC Protected Areas Database (http://www.unep-wcmc. 20. Belovsky, G. E. Generalist herbivore foraging and its role in competitive interactions. Am. Zool. 26, org). Only mammalian herbivores . 2 kg that eat graminoids, forbs and/or woody 51±69 (1986). plants were recorded. We restricted the analysis to this size class because the records of 21. Owen-Smith, N. Pleistocene extinctions: The pivotal role of megaherbivores. Paleobiology 13, 351± smaller herbivores (small mammals, insects) in these areas are incomplete. Species that 362 (1987). eat mostly seeds and were not included as it is unclear whether the food abundance 22. Eisenberg, J. F. The Mammalian Radiations. An Analysis of Trends in Evolution, Adaptation, and and quality patterns shown in Fig. 1a and b also hold for these food types. We included Behaviour (Athlone, London, 1981). 23. Huston, M. A. Biological diversity, soils and economics. Science 262, 1676±1680 (1993). only wilderness areas, national parks and national monuments and wildlife management 24. Myers, N., Mittelmeier, R. A., Mittelmeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots areas (International Union for the Conservation of Nature (IUCN)) categories I, II or III for conservation priorities. Nature 403, 853±858 (2000). or IV). 25. Alcamo, J. et al. Modeling the global society-biosphere-climate system: Part 2. Computed scenarios. Water Air Soil Poll. 76, 37±78 (1994). Plant-available moisture index 26. Murray, M. G. in Serengeti II. Dynamics, Management and Conservation of an Ecosystem (eds Sinclair, The plant-available moisture index for each protected area was calculated as the monthly A. R. E. & Arcese, P.) 231±256 (Univ. Chicago Press, Chicago, 1995). 27. Kinyamario, J. I. & Macharia, J.-N. M. Aboveground standing crop, protein content and dry matter average of the log10 of the ratio of actual rainfall over potential evapotranspiration using published maps26. Data of potential evapotranspiration and therefore our moisture index digestibility of a tropical grassland range in the Nairobi National Park, Kenya. Afr. J. Ecol. 30, 33±41 and diversity prediction were not available for the polar region, as the calculation method (1992). is inappropriate for areas with long-term snow cover. 28. Prins, H. H. T. Ecology and Behaviour of the African Buffalo. Social Inequality and Decision Making (Chapman & Hall, London, 1996). 29. van Wijngaarden, W. Elephants±Trees±Grass±Grazers, relationships between climate, soils, vegeta- Plant-available nutrients index tion and large herbivores in a semi-arid savanna ecosystem (Tsavo, Kenya). (ITC Publication no. 4, Data on plant-available nutrients are based on the FAO-UNESCO Soil Map of the World, Enschede, 1985). assigned25 to 18 by 18 cells. Plant-available nutrients were assumed to be proportional to 30. Voeten, M. M. Living with wildlife. Coexistence of wildlife and livestock in an East African savanna the sum of soil cations Ca2+,Mg2+,Na+ and K+ or total exchangeable bases (TEB), which is ecosystem. Tropical Resource Management Papers no. 29 (Wageningen Univ., Wageningen, 1999). calculated from base saturation, BS% = [(TEB/CECsoil) ´ 100], and soil exchange capacity (soil CEC) according to TEB = (BS%/100) ´ 3.5OC% + [(Clay% x CECclay)/ Acknowledgements 100)], where OC% is the percentage of organic carbon in the soil, Clay% is the percentage of clay content and CECclay is the approximate cation exchange capacity for the dominant We thank E. S. Bakker, J. P. Bakker, W. J. Bond, F. S. Chapin III, G. E. Belovsky, clay mineral. S. J. McNaughton, D. Milchunas, N. Owen-Smith, F. J. Weissing and D. Tilman for comments; M. A. Huston for soil fertility data; and R. Leemans for temperature and rainfall data. Financial support was provided by the Dutch NWO (WOTRO and ALW), Species frequency of occurrence Wageningen University, the NSF, the Utah Agricultural Experiment Station, and the Utah The frequency of occurrence of individual herbivore species is the proportion of parks that State University Ecology Center. contain a particular species in each of six intervals of plant-available moisture index, and seven intervals of plant-available nutrients index. Patterns were robust to our choice of interval sizes. For each interval, we also calculated the mean body mass of all species Competing interests statement present. Because Africa (99 large herbivore species) and North America (25 large herbivore The authors declare that they have no competing ®nancial interests. species) differ in their continental species pools and local species richness, owing in part to extinction of 50% of the species in North America since the last glaciation, the species Correspondence and requests for materials should be addressed to H.O. richness at each park was expressed as a percentage of the continental species pool. This (e-mail: [email protected]).

904 © 2002 Macmillan Magazines Ltd NATURE | VOL 415 | 21 FEBRUARY 2002 | www.nature.com

RESEARCH

MIGRATION Thus, if migration does not stem primarily from a genetically inherited suite of traits, individuals should fail to migrate when first translocated into novel landscapes where migration would be Is ungulate migration culturally a profitable strategy (21). To test this prediction, we affixed global po- transmitted? Evidence of social sitioning system (GPS) collars on 129 bighorn sheep sampled from four populations that had learning from translocated animals been extant for >200 years (herein termed “his- torical populations”) (Fig. 1) and 80 bighorn sheep when the sheep were first translocated into novel Brett R. Jesmer1,2*, Jerod A. Merkle2, Jacob R. Goheen1, Ellen O. Aikens1,2, landscapes (table S1). We defined migration as Jeffrey L. Beck3, Alyson B. Courtemanch4, Mark A. Hurley5, Douglas E. McWhirter4, movement between distinct seasonal ranges and Hollie M. Miyasaki5, Kevin L. Monteith2,6, Matthew. J. Kauffman7 classified the movement of each collared individ- ual as migratory or resident by using net-squared Ungulate migrations are assumed to stem from learning and cultural transmission of displacement (22) [supplementary materials (SM)]. information regarding seasonal distribution of forage, but this hypothesis has not been We then quantified how green waves of forage tested empirically. We compared the migratory propensities of bighorn sheep and moose propagated across individual landscapes (1000 translocated into novel habitats with those of historical populations that had persisted to 3600 km2)bymeasuringthedateeachpixelin for hundreds of years. Whereas individuals from historical populations were largely a rasterized time series of the normalized differ-

migratory, translocated individuals initially were not. After multiple decades, however, Downloaded from ence vegetation index (250-m spatial resolution, translocated populations gained knowledge about surfing green waves of forage (tracking 8-day temporal resolution) peaked in forage qual- plant phenology) and increased their propensity to migrate. Our findings indicate that ity (SM) (23).Usingthisrasterizedmeasureof learning and cultural transmission are the primary mechanisms by which ungulate peak forage quality, we quantified the semivar- migrations evolve. Loss of migration will therefore expunge generations of knowledge about iance (the magnitude of the wave) in the date of the locations of high-quality forage and likely suppress population abundance. peak forage quality across a range of spatial lags

(the distance the wave traveled) (SM). Within http://science.sciencemag.org/ rom tropical savannas to the Arctic tundra, neurological, morphological, physiological, and historical populations, 65 to 100% of individuals the migrations of ungulates (hooved mam- behavioral traits (5, 10, 11). When behavior is pri- migrated, whereas few (<9%; 7 of 80) individ- mals) can span more than 1000 km and are marily a consequence of social learning and per- uals translocated into novel landscapes migrated considered among the most awe inspiring sists across generations—a phenomenon known (Fig. 2A). The migratory propensity of a popula- F — of natural phenomena. Migration allows as culture information is transmitted from gen- tion was not related to the magnitude of the green ungulatestomaximizeenergyintakebysynchro- eration to generation (12). Culture is therefore wave or the distance it traveled (fig. S1), meaning nizing their movements with the emergence of regarded as a “second inheritance system,” anal- that landscape characteristics alone did not ex- high-quality forage across vast landscapes (1). ogous to the inheritance of genes that underlie plain differences in migratory propensity among Consequently, migration often bolsters fitness innate behaviors (13–15). Thus, if social learning is populations. The seven translocated individuals and results in migratory individuals’ greatly out- the primary mechanism allowing animals to gain that migrated were translocated into existing

numbering residents (2, 3). Despite their critical information regarding the seasonal distribution of populations of bighorn sheep (<200 individuals) on September 7, 2018 importance, migrations are increasingly imperiled high-quality forage, cultural transmission may be that had been reestablished three decades before by human activities (4). Thus, understanding how theprincipalforcebywhichungulatemigrations (SM), suggesting cultural transmission of mi- migrations are developed and maintained is criti- have evolved in landscapes conducive to migration. gratory behavior among conspecifics (horizontal calfortheconservationofthisglobalphenomenon Ungulate migration is a strategy for exploiting transmission). Because individuals from migra- (5). Ecologists have long speculated that memory altitudinal, longitudinal, and other topographic tory populations failed to migrate when trans- and social learning underlie ungulate migration gradients of plant phenology that determine located into landscapes where they had no prior (6–8). Bison (Bison bison) remember the locations forage quality (16, 17). The ability of ungulates experience, genes are unlikely to be the primary of high-quality forage and transmit such informa- to synchronize their movements with phenolog- agent underlying ungulate migration. Instead, tion to conspecifics (9), whereas moose (Alces alces) ical waves of nutritious, green plants—abehavior migration may require extended periods of time for and white-tailed deer (Odocoileus virginianus) known as “green-wave surfing” (18)—can result social learning and cultural transmission to occur. adopt the movement strategies of their mothers in migratory movements far beyond an individ- To evaluate the hypothesis that green-wave (6, 7). Nevertheless, the hypothesis that social ual’s perceptual range (19). Ungulates also can surfing is a learned behavior, we first calculated learning underlies the development and mainte- surf green waves of forage within year-round the surfing ability of each GPS-collared individ- nance of ungulate migration has not been tested ranges, even in the absence of migration (1). ual as the absolute difference between the day with empirical data. Green-wave surfing may therefore represent a an individual occupied a location and the day Animal migrations arise through a combina- learned behavior that underlies migration, and forage quality peaked at that location (23). We tion of learned behavior and genetically inherited such knowledge may accumulate over genera- then controlled for the influence that local dif- tions via cultural transmission (15, 20). ferences in latitudinal, elevational, and topo- 1 Program in Ecology, Department of Zoology and Physiology, Across the American West, many bighorn sheep graphical features may have on an individual’s University of Wyoming, Laramie, WY 82071, USA. 2Wyoming Cooperative Fish and Wildlife Research Unit, Department of (Ovis canadensis) populations were extirpated in ability to surf the green wave (23)bycomparing Zoology and Physiology, University of Wyoming, Laramie, the late 1800s because of market hunting and observed green-wave surfing ability with those WY 82071, USA. 3Department of Ecosystem Science and transmission of disease from domestic sheep of a “naïve forager” that moved at random and an Management, University of Wyoming, Laramie, WY 82071, (O. aries) (Fig. 1). To restore lost populations, “omniscient forager” that had complete knowl- USA. 4Wyoming Game and Fish Department, Jackson, WY 83001, USA. 5Idaho Department of Fish and Game, Boise, wildlife managers translocated individuals from edge of phenological patterns (SM). By doing so, ID 83712, USA. 6Haub School of Environment and Natural extant, migratory populations into vacant land- we were able to quantify how much knowledge Resources, University of Wyoming, Laramie, WY 82072, USA. scapes where extirpated populations once existed individuals possessed about local patterns of 7 U. S. Geological Survey, Wyoming Cooperative Fish and (Fig. 1). These individuals therefore had no knowl- phenology (fig. S2). We found that the surfing Wildlife Research Unit, Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, USA. edge about the landscapes into which they were knowledge of bighorn sheep from historical popu- *Corresponding author. Email: [email protected] translocated (herein termed “novel landscapes”). lations was approximately twice that of transplanted

Jesmer et al., Science 361, 1023–1025 (2018) 7 September 2018 1of3 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/

on September 7, 2018

Fig. 1. Bighorn sheep and moose translocation history. (A) The subset events in the history of these species since the settlement of western of historical and translocated populations of bighorn sheep and moose North America by European Americans. See SM for further details used to assess the cultural basis of ungulate migration. (B) Timeline about translocation history. (Cartography by InfoGraphics Lab, of bighorn sheep and moose translocations as well as other important University of Oregon.) individuals (Fig. 2B), suggesting that knowledge tions of bighorn sheep (an additional 58 individ- habitat loss, and increased predation (25, 26). about local green waves may improve over time as uals) and five populations of moose (Alces alces; Together, these results demonstrate that un- animals learn and culturally transmit information 189 individuals) that were GPS collared ~10 to gulates accumulate knowledge of local pheno- about the seasonal distribution of high-quality forage. 110 years after either translocation or natural logical patterns over time via the “ratcheting The hypothesis that ungulate migration is es- colonization (Fig. 1, table S1, and SM). We found effect,” wherein each generation augments cul- tablished and maintained by cultural transmis- that the surfing knowledge of both bighorn sheep turally transmitted information with information sion predicts that green-wave surfing knowledge and moose increased as time since population gained from their own experience, a process and, subsequently, the propensity to migrate establishment increased (Fig. 3A). As time passed known as cumulative cultural evolution (15, 20). should increase as animals learn how to exploit and bighorn sheep and moose increased their Cultural transmission therefore acts as a second landscapes and transmit that foraging informa- surfing knowledge, their migratory propensities (nongenetic) inheritance system for ungulates, tion across generations (vertical transmission of also increased (Fig. 3, B and C). Although pop- shaping their foraging and migratory behavior information). To evaluate the influence of verti- ulation density and migratory propensity are and ultimately providing the primary mechanism cal transmission on surfing knowledge and mi- sometimes correlated positively (24), migratory by which their migrations have evolved. gratory propensity, we expanded our analysis to propensity did not change with substantial de- Across the globe, anthropogenic barriers have include individuals from four additional popula- creases in population density caused by epizootics, disrupted ungulate migrations, triggered declines

Jesmer et al., Science 361, 1023–1025 (2018) 7 September 2018 2of3 RESEARCH | REPORT

5. D. T. Bolger, W. D. Newmark, T. A. Morrison, D. F. Doak, Ecol. Lett. 11,63–77 (2008). 6. M. E. Nelson, Can. J. Zool. 76, 426–432 (1998). 7. P. Y. Sweanor, F. Sandegren, J. Appl. Ecol. 26,25–33 (1989). 8. R. B. Boone, S. J. Thirgood, J. G. C. Hopcraft, Ecology 87, 1987–1994 (2006). 9. J. A. Merkle, M. Sigaud, D. Fortin, Ecol. Lett. 18,799–806 (2015). 10. T. Mueller, R. B. O’Hara, S. J. Converse, R. P. Urbanek, W. F. Fagan, Science 341, 999–1002 (2013). 11. T. Alerstam, Science 313, 791–794 (2006). 12. S. J. Shettleworth, in Cognition, Evolution, and Behavior (Oxford University Press, 2010), pp. 417–464. 13. S. A. Keith, J. W. Bull, Ecography 40, 296–304 (2017). 14. A. Whiten, Nature 437,52–55 (2005). 15. C. Tennie, J. Call, M. Tomasello, Philos. Trans. R. Soc. London Ser. B 364, 2405–2415 (2009). 16. M. Hebblewhite, E. Merrill, G. McDermid, Ecol. Monogr. 78, 141 –166 (2008). 17. J. M. Fryxell, Am. Nat. 138, 478–498 (1991). 18. S. A. J. van der Graaf, J. Stahl, A. Klimkowska, J. P. Bakker, R. H. Drent, Ardea 94, 567–577 (2006). 19. C. Bracis, T. Mueller, Proc. R. Soc. London Ser. B 284, 20170449 (2017). 20. T. Sasaki, D. Biro, Nat. Commun. 8, 15049 (2017).

21. K. N. Laland, V. M. Janik, Trends Ecol. Evol. 21,542–547 (2006). Downloaded from 22. N. Bunnefeld et al., J. Anim. Ecol. 80, 466–476 (2011). 23. E. O. Aikens et al., Ecol. Lett. 20, 741–750 (2017). 24. W. Peters et al., Ecol. Monogr. 87, 297–320 (2017). 25. P. A. Hnilicka et al., in Northern Wild Sheep and Goat Council 13 (Northern Wild Sheep and Goat Council, 2003), pp. 69–94. 26. B. A. Oates, thesis, University of Wyoming, Laramie, WY (2016). Fig. 2. Migratory propensities and green-wave 27. H. Sawyer, M. J. Kauffman, J. Anim. Ecol. 80,1078–1087 (2011). surfing knowledge of seven translocated 28. H. Sawyer et al., J. Appl. Ecol. 50,68–78 (2013). http://science.sciencemag.org/ 29. H. Whitehead, Learn. Behav. 38, 329–336 (2010). and historical populations of bighorn sheep. 30. B. R. Jesmer et al., Dataset for “Is ungulate migration (A) Migratory propensities (±SEM) of bighorn culturally transmitted?” Dryad (2018); https://doi.org/ sheep translocated into novel landscapes 10.5061/dryad.8165qv5. compared with those of historical populations ACKNOWLEDGMENTS (>200 years old). Asterisks indicate landscapes Data used in this analysis were collected by, or in collaboration where naïve individuals were translocated with, biologists at the Wyoming Game and Fish Department into populations previously established via and the Idaho Department of Fish and Game who have been translocation ~30 years before. (B) Relative working for over half a century to restore and conserve ungulate to omniscient and naïve foragers on the same populations. We thank these biologists for their hard work and dedication. We also thank M. Festa-Bianchet and two landscape, surfing knowledge was lower for anonymous reviewers for providing helpful comments on drafts translocated (yellow) bighorn sheep than for of the manuscript (see SM for additional acknowledgments). on September 7, 2018 individuals from historical populations (green). Funding: This research was financially supported by the Mean surfing knowledge (black horizontal bars) Fig. 3. Green-wave surfing knowledge and Wyoming Governor’s Big Game License Coalition (A.B.C., B.R.J., D.E.M., J.L.B., J.R.G., K.L.M., M.J.K.), the Wyoming Game and relative to that of an omniscient forager (set at migratory propensity over time. (A) After Fish Department (D.E.M.), the Idaho Department of Fish and translocation, populations of bighorn sheep 1.0) and associated 95% confidence intervals Game (M.A.H., H.M.M.), the Wyoming NASA Space Grant (white boxes) are presented. The surfing (orange circles) and moose (purple circles) Consortium (B.R.J., J.R.G., M.J.K.), the American Society of knowledge of individuals (black circles) in historical require decades to learn and culturally transmit Mammalogists (B.R.J.), the Safari Club International Foundation (M.J.K.), the Idaho Safari Club (M.A.H., H.M.M.), the Idaho populations was significantly higher than that information about how to best surf green waves, Transportation Department (M.A.H., H.M.M.), the Bureau of (B) eventually leading to the establishment of translocated individuals (Mann-Whitney U Test, Land Management (M.A.H., H.M.M.), the U.S. Forest Service W = 5863, P <0.001). of migration, which (C) takes many generations (M.A.H., H.M.M., A.B.C., J.R.G., M.J.K.), Pittman-Robertson (the generation time for bighorn sheep and Wildlife Restoration funds (M.A.H., H.M.M.), the Wild Sheep moose is ~7 years). Circles represent estimates Foundation (H.M.M., M.A.H.), the Wyoming Wild Sheep Foundation (A.B.C., D.E.M., J.L.B., K.L.M., M.J.K.), the Teton in population abundance, and even caused local of surfing knowledge and migratory propensity extirpations (4). Our results provide empirical Conservation District (A.B.C., M.J.K.), the Grand Teton National for a given population in a given year (i.e., a Park Foundation (A.B.C., M.J.K.), the Wyoming Wildlife- evidence that learning and cultural transmission migratory event). Circle size depicts the amount of Livestock Disease Research Partnership (K.L.M.), and the Alces underlie the establishment and maintenance of confidence (inverse variance) in each estimate. Society (B.R.J.). Author contributions: B.R.J., J.A.M., J.R.G., and M.J.K. conceived the study and wrote and revised the ungulate migration. Because ungulate migra- Black lines and gray shaded areas illustrate fitted tions stem from decades of social learning about manuscript; B.R.J., E.O.A., and J.A.M. analyzed the data; generalized linear model predictions and their and all coauthors assisted with data collection. Competing spatial patterns of plant phenology, loss of migra- 95% confidence intervals. All relationships are interests: All authors declare that they have no competing tion will result in a marked decrease in the knowl- significant at P <0.01. interests. Data and materials availability: Data reported in this edge ungulates possess about how to optimally paper are archived in Dryad (30). exploit their habitats. Hence, restoring migratory populations after extirpation or the removal of and culture that migratory animals use to bolster SUPPLEMENTARY MATERIALS barriers to movement will be hindered by poor fitness and sustain abundant populations (13, 29). www.sciencemag.org/content/361/6406/1023/suppl/DC1 Materials and Methods foraging efficiency, suppressed fitness, and re- Supplementary Text REFERENCES AND NOTES duced population performance (2, 3). Thus, con- Figs. S1 and S2 servation of existing migration corridors, stopover 1. J. A. Merkle et al., Proc.R.Soc.LondonSer.B283, 20160456 (2016). Tables S1 to S3 2. J.M.Fryxell,J.Greever,A.R.E.Sinclair,Am. Nat. 131,781–798 (1988). – sites, and seasonal ranges not only protects the References (31 78) 3. C. M. Rolandsen et al., Oikos 126, 547–555 (2017). landscapes that ungulates depend on (27, 28); such 4. G. Harris, S. Thirgood, J. G. C. Hopcraft, J. P. Cromsigt, 26 January 2018; accepted 6 August 2018 efforts also maintain the traditional knowledge J. Berger, Endangered Species Res. 7,55–76 (2009). 10.1126/science.aat0985

Jesmer et al., Science 361, 1023–1025 (2018) 7 September 2018 3of3 Is ungulate migration culturally transmitted? Evidence of social learning from translocated animals Brett R. Jesmer, Jerod A. Merkle, Jacob R. Goheen, Ellen O. Aikens, Jeffrey L. Beck, Alyson B. Courtemanch, Mark A. Hurley, Douglas E. McWhirter, Hollie M. Miyasaki, Kevin L. Monteith and Matthew. J. Kauffman

Science 361 (6406), 1023-1025. DOI: 10.1126/science.aat0985

Learning where and when

Large ungulate migrations occur across continents and inspire curiosity about how these animals know when to Downloaded from leave and where to go. Jesmer et al. took advantage of regional extinctions and reintroductions of several North American ungulate species to determine the role of learning in migrations (see the Perspective by Festa-Bianchet). Reintroduced populations of bighorn sheep and moose did not migrate as historical herds had. However, after several decades, newly established herds were better able to track the emergence of vegetation in the environment and were increasingly migratory. Thus, newly introduced animals learned about their environment and shared the information through social exchange. Science, this issue p. 1023; see also p. 972 http://science.sciencemag.org/

ARTICLE TOOLS http://science.sciencemag.org/content/361/6406/1023

SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2018/09/05/361.6406.1023.DC1 MATERIALS

on September 7, 2018

RELATED http://science.sciencemag.org/content/sci/361/6406/972.full CONTENT

REFERENCES This article cites 51 articles, 6 of which you can access for free http://science.sciencemag.org/content/361/6406/1023#BIBL

PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions

Use of this article is subject to the Terms of Service

Science (print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. 2017 © The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. The title Science is a registered trademark of AAAS. REPORTS

might also relieve resource constraints and cause Density Triggers Maternal Hormones resource-mediated or permissive parental effects (7). Identification and experimental manipulation of the mechanisms that mediate parental effects That Increase Adaptive Offspring requires a combination of field physiology, exper- imental ecology, and longitudinal studies of nat- Growth in a Wild Mammal ural selection that have not been achieved to date. We identified and experimentally manipu- Ben Dantzer,1*† Amy E. M. Newman,2 Rudy Boonstra,3 Rupert Palme,4 Stan Boutin,5 lated the social density cues and stress hormones Murray M. Humphries,6 Andrew G. McAdam1,2 responsible for an adaptive maternal effect in a natural population of North American red squir- In fluctuating environments, mothers may enhance the fitness of their offspring by adjusting rels (Tamiasciurus hudsonicus). offspring phenotypes to match the environment they will experience at independence. In Individual male and female red squirrels de- free-ranging red squirrels, natural selection on offspring postnatal growth rates varies according fend exclusive territories around a central mid- to population density, with selection favoring faster-growing offspring under high-density den (9, 10) containing cached white spruce cones conditions. We show that exposing mothers to high-density cues, accomplished via playbacks [Picea glauca (11, 12)], and juveniles that fail of territorial vocalizations, led to increased offspring growth rates in the absence of additional to acquire a territory before their first winter do food resources. Experimental elevation of actual and perceived density induced higher not survive (13). Red squirrels experience recur- maternal glucocorticoid levels, and females with naturally or experimentally increased rent fluctuations in population density because glucocorticoids produced offspring that grew faster than controls. Therefore, social cues of pronounced episodic fluctuations in the avail-

reflecting population density were sufficient to elicit increased offspring growth through an ability of white spruce seeds (Fig. 1A) (11, 12). Downloaded from adaptive hormone-mediated maternal effect. Increased autumn spruce cone production is as- sociated with increased squirrel density in the luctuations in food availability and the re- cues that predict the direction or the magnitude following spring (Fig. 1B) (14). In our 23-year sultant changes in the population density of these agents of selection (3, 4). Phenotypic study in the Yukon, Canada, we found that these Fof consumers are thought to be important plasticity is beneficial in such changing environ- changes in density have notable effects on red squir- ecological agents of natural selection in many ments because it enables individuals to track rels because we documented density-dependent http://science.sciencemag.org/ animal populations (1, 2). Temporal variation in fluctuating fitness optima (5, 6). Similarly, if the selection on offspring postnatal growth rates. In natural selection characterized by recurrent pulses parental environment or phenotype provides re- years when spring density was high, females that in food or density can favor the evolution of adapt- liable cues of the conditions that offspring will produced faster-growing offspring had more off- ive phenotypic plasticity when there are reliable experience, parents may induce adaptive changes spring survive their first winter and recruit into in offspring that increase both parental and off- the adult population, whereas when density was low spring fitness [adaptive parental effects (7, 8)]. there was no benefit to producing faster-growing 1Department of Zoology, Michigan State University, East Lansing, The role of parental effects in the adaptation of offspring [n = 463 females, offspring growth × MI 48824, USA. 2Department of Integrative Biology, Univer- 3 offspring to changing environments is intriguing, density, t726 = 2.15, P = 0.016 (table S1)]. sity of Guelph, Guelph, ON N1G 2W1, Canada. Centre for the but little is known about their importance in free- In such variable environments, the evolution Neurobiology of Stress, University of Toronto Scarborough, Toronto, ON M1C 1A4, Canada. 4Department of Biomedical living animals. Not only do the agents of natural of adaptive maternal effects may be favored, but

Sciences/Biochemistry, University of Veterinary Medicine, selection on offspring phenotype need to be iden- this requires the presence of reliable cues that on August 14, 2019 A-1210 Vienna, Austria. 5Department of Biological Sciences, tified, but the cues parents use to predict changes enable an accurate prediction of natural selection 6 University of Alberta, Edmonton, AB T6G 2E9, Canada. Nat- in the agent of selection, and the mechanism that on offspring (3, 4). Therefore, cues of population ural Resource Sciences, Macdonald Campus, McGill University, Ste-Anne-de-Bellevue, QC H9X 3V9, Canada. mediates the parental effect, also need to be density in red squirrels might induce adaptive *Corresponding author. E-mail: [email protected] known. This is further complicated when con- increases in offspring growth when density is †Present address: Department of Zoology, University of sidering population density as a cue because it is high. Red squirrels emit territorial vocalizations Cambridge, Cambridge CB2 3EJ, UK. often confounded with food availability, which called rattles to defend their territories, and the

Fig. 1. Population density of North American red squirrels in the study areas (b =0.24T 0.05, t53 =4.3,P < 0.0001) and one study area Yukon, Canada, fluctuates annually in response to the availability of (Food-add) where squirrels have been provided with supplemental food since spruce cones. (A) Yukon red squirrels experience recurrent fluctuations in autumn 2004 (b =0.20T 0.19, t53 = –0.22, P > 0.5). Autumn spruce cone population density (squirrels/ha) because of interannual variation in white production is an index on a ln scale (11). Regression lines from a linear spruce cone abundance (11, 12). (B) Spruce cone production in the previous mixed-effects model. (C) Red squirrel extracting seeds from a white spruce autumn is associated with increased spring population density in two control cone. [Photo credit: R. W. Taylor]

www.sciencemag.org SCIENCE VOL 340 7 JUNE 2013 1215 REPORTS

frequency with which they hear rattles in their Fig. 2. Female red squir- neighborhood accurately predicts density (10). rels experiencing increased We hypothesized that territorial vocalizations perceived or actual densi- provide a cue of density that allows females to ty produced faster-growing adaptively adjust offspring growth in antici- offspring than controls. pation of the density-dependent selection that Female red squirrels experienc- they will experience. We tested this hypothe- ing experimentally increased sis by simulating high-density conditions using perceived population densi- n audio playbacks of red squirrel rattles (9, 10). ty (rattle playbacks, =19 females, 67 pups) produced This corresponded to a perceived density of offspring that grew significant- 4.92 squirrels/ha, which was sixfold higher than ly faster than those produced the perceived density of females exposed to a con- by controls (n = 19 females, trol stimulus (bird vocalizations, 0.81 squirrel/ha) 65 pups) but similar to those and similar to the maximum historical density produced by food-supplemented (Fig. 1A) (10). Such a high-density environment females (n = 16 females, would typically be associated with a strong 55 pups) experiencing in- positive relationship between offspring growth creased actual density. Val- and fitness (table S1), whereas offspring growth ues on the y axis represent Residual pup growth rate does not affect fitness in the low-density control residuals from a linear mixed- environment. effects model (table S2). High food & density

As predicted, offspring produced by females High perceived density Downloaded from experiencing experimentally heightened perceived Control

density grew significantly faster than those produced -2.5 -2.0 -1.5 -1.0 -0.5 0.0 by control females (Fig. 2). Consistent with life- 123456 history theory (15), the growth rates of offspring Litter size produced by control females declined significant- ly as litter size increased, but this effect was at- http://science.sciencemag.org/ tenuated by 67% in females exposed to playbacks of territorial vocalizations [playback × litter size, A B C n = 25 n = 66 t186 = 1.98, P = 0.024 (table S2 and Fig. 2)]. In fact, the trade-off between litter size and growth rate in females exposed to playbacks of territo-

– 7.2 7.4 rial vocalizations was greatly reduced (r = 0.12, n = 24 – t66 = 1.57, P = 0.06) compared with that in con- ** * trol females (r = –0.37, t64 = –4.43, P < 0.0001). 7.0 Female red squirrels, therefore, increase offspring n = 97 growth in response to conspecific density because

on August 14, 2019

of the fitness benefits of doing so in high-density Fecal cortisol metabolites Fecal cortisol metabolites years. These growth-enhancing maternal effects 6.8 6.8 7.0 7.2 7.4 t=3.63, P=0.0002 Residual fecal cortisol metabolites in high-density years are adaptive for mothers -0.5 0.0 0.5 1.0 1.5 2.0 and offspring by increasing the probability that 01234 Control High density Control High density their offspring will survive their first winter (16), Local density (squirrels/ha) Actual density treatment Perceived density treatment which is a major component of their lifetime fit- Fig. 3. Female red squirrels experiencing higher population density had higher glucocorticoid ness (17). However, faster offspring growth rates levels. (A) Female red squirrels living under high-density conditions had higher concentrations of FCM. are not favored under low-density conditions Squirrels experiencing experimentally increased (B) actual density resulting from long-term food sup- [≤1 squirrel/ha (table S1)], and in some years plementation or (C) perceived density (rattle playbacks) had significantly higher concentrations of FCM than there is significant negative selection on off- controls. Values on the y axis represent either (A) residuals from a linear mixed-effects model (table S4) or spring growth (16). Increased reproductive ef- [(B) and (C)] raw FCM (ln ng/g of dry feces). Sample sizes refer to the number of fecal samples analyzed. P P T fort does not appear to incur a survival cost to ** <0.01and* < 0.05 (table S4). Error bars indicate SE. mothers (18, 19). However, offspring born in high- density years have a reduced adult life span (20), S4 and Fig. 3A)]. Females from a study area In mammalian species, increases in mater- suggesting that faster offspring growth, which with experimentally increased density result- nal glucocorticoid levels can cause profound enhances recruitment when density is high, might ing from food supplementation [75% higher changes in offspring phenotype (22) and may incur a cost to offspring later in life. Such con- density than control study areas (Fig. 1)] had provide offspring with reliable hormonal cues ditions will promote the evolution of plasticity concentrations of FCM that were 49% higher about their future environment. Three lines of evi- in maternal effects, whereby increased offspring [t162 = 3.82, P < 0.0001 (table S4 and Fig. dence indicate that increases in maternal gluco- growth coincides with the high-density condi- 3B)] than those of females in control study areas. corticoid levels are responsible for the adaptive tions under which it enhances fitness. Females experiencing increased perceived den- increase in offspring growth under high-density These adaptive maternal effects on offspring sity through the playback experiment had con- conditions. First, females exposed to heightened were mediated by the physiological stress re- centrations of FCM that were 30% higher than perceived density had increased concentrations sponses of females experiencing heightened pop- those of control females [t48 = 2.24, P = 0.015 of FCM during pregnancy (Fig. 3C) and also ulation density. Across 6 years (2006 to 2011), (table S4 and Fig. 3C)]. These results confirm produced faster-growing offspring than controls we found a positive relationship between local that increases in concentrations of FCM were (Fig. 2). Second, increased maternal FCM con- density and concentrations of fecal cortisol me- driven by perceived density rather than by food centrations were positively associated with off- tabolites [FCM; t155 =3.63,P = 0.0002 (table abundance (21). spring growth in females measured over a 6-year

1216 7 JUNE 2013 VOL 340 SCIENCE www.sciencemag.org REPORTS

ment. In fact, offspring produced by females ex- 11. J. M. LaMontagne, S. Boutin, J. Ecol. 95, 991 (2007). posed to high-density cues but with no access to 12. Q. E. Fletcher et al., Ecology 91, 2673 (2010). 13. K. W. Larsen, S. Boutin, Ecology 75, 214 (1994). additional food grew as fast as those produced 14. S. Boutin et al., Science 314, 1928 (2006). n = 15 by food-supplemented females that were also 15. C. C. Smith, S. D. Fretwell, Am. Nat. 108, 499 (1974). experiencing increased density [1.79 T 0.09 16. A. G. McAdam, S. Boutin, Evolution 57, 1689 (2003). squirrels/ha (Fig. 2 and table S2)]. Therefore, some 17. A. G. McAdam, S. Boutin, A. K. Sykes, M. M. Humphries, Écoscience 14, 362 (2007). *** of the plasticity in female life history traits is 18. M. M. Humphries, S. Boutin, Ecology 81, 2867 (2000). due to the expected fitness benefits of produc- 19. S. Descamps, S. Boutin, A. G. McAdam, D. Berteaux, ing faster-growing offspring under high-density J.-M. Gaillard, Proc. Biol. Sci. 276, 1129 (2009). conditions rather than only reflecting a relaxa- 20. S. Descamps, S. Boutin, D. Berteaux, A. G. McAdam, n = 12 tion of food limitation. J.-M. Gaillard, J. Anim. Ecol. 77, 305 (2008). 21. S. Creel, B. Dantzer, W. Goymann, D. R. Rubenstein, Pup growth rate (g/day) Experimental increases in food resources that Funct. Ecol. 27, 66 (2013). result in increased reproductive output are typical- 22. A. Harris, J. Seckl, Horm. Behav. 59, 279 (2011).

1.4 1.6 1.8 2.0 2.2 ly interpreted as evidence for resource limitations 23. O. P. Love, T. D. Williams, Am. Nat. 172, E135 (2008). on reproduction (29). However, if animals use food 24. R. Boonstra, Funct. Ecol. 27, 11 (2013). 25. A. Catalani et al., Neuroscience 100, 319 (2000). Control Fed GCs abundance as a cue of upcoming density-mediated Treatment 26. C. L. Moore, K. L. Power, Dev. Psychobiol. 19, 235 selection, then reproductive responses to food sup- (1986). Fig. 4. Offspring produced by female red squir- plementation might reflect not only relaxation of 27. C. M. Kuhn, J. Pauk, S. M. Schanberg, Dev. Psychobiol. rels provisioned with cortisol grew significantly food limitation but also an adaptive adjustment 23, 395 (1990). 28. C. S. Elton, Br. J. Exp. Biol. 2, 119 (1924). faster than those from controls. Raw offspring to an anticipated change in natural selection re- 29. S. Boutin, Can. J. Zool. 68, 203 (1990). T y growth rates (mean SE) are shown on axis. sulting from an impending increase in density. Downloaded from Sample sizes denote number of pups. Fed GCs Cues of population density may be a general signal Acknowledgments: We thank Agnes Moose and family for corresponds to provisioning with three different that animals use to make adaptive reproductive access to their traditional trapping area; F. E. Stewart, S. E. Evans, cortisol concentrations (fig. S2). ***P < 0.0001 adjustments in anticipation of density-dependent S. E. McFarlane, Q. E. Fletcher, S. Hossain, R. W. Taylor, and all (table S6). squirrelers for assistance; A. Sykes and E. Anderson for data natural selection on offspring phenotypes. management; and A. Charmantier, T. Getty, K. E. Holekamp, J. S. Lonstein, C. T. Williams, T. D. Williams, and three anonymous period [t = 1.94, P = 0.028 (table S5)]. Last, References and Notes reviewers for incisive comments. Funded by Natural Sciences

98 http://science.sciencemag.org/ offspring born to females with experimentally in- 1. M. J. Wade, S. Kalisz, Evolution 44, 1947 (1990). and Engineering Research Council of Canada, NSF (DEB-0515849 2. A. D. C. MacColl, Trends Ecol. Evol. 26, 514 (2011). and IOS-1110436), and Ontario Ministry of Research creased glucocorticoid levels during pregnancy [fed 3. R. Levins, Evolution in Changing Environments Innovation. Data have been deposited in the Dryad Repository cortisol (fig. S1)] grew 41% faster than those (Princeton Univ. Press, Princeton, NJ, 1968). (http://dx.doi.org/10.5061/dryad.b3h4q). This is publication 4. N. A. Moran, Am. Nat. 139, 971 (1992). no. 69 of the Kluane Red Squirrel Project. produced by control females [t26 = 4.98, P < 0.0001 (table S6 and Fig. 4)]. 5. D. Réale, A. G. McAdam, S. Boutin, D. Berteaux, Supplementary Materials Proc. Biol. Sci. 270, 591 (2003). www.sciencemag.org/cgi/content/full/science.1235765/DC1 Our results suggest that elevated maternal 6. A. Charmantier et al., Science 320, 800 (2008). Materials and Methods glucocorticoid levels in response to heightened 7. T. A. Mousseau, C. A. Fox, Eds., Maternal Effects as Figs. S1 to S3 Adaptations (Oxford Univ. Press, Oxford, 1998). population density induced an adaptive hormone- Tables S1 to S7 8. D. J. Marshall, T. Uller, Oikos 116, 1957 (2007). mediated maternal effect on offspring growth. References (30–54) 9. Materials and methods are available as supplementary In contrast to the widespread assumption that materials on Science Online. 28 January 2013; accepted 5 April 2013 heightened maternal glucocorticoid levels are 10. B. Dantzer, S. Boutin, M. M. Humphries, A. G. McAdam, Published online 18 April 2013; on August 14, 2019 detrimental to offspring (22), our results empha- Behav. Ecol. Sociobiol. 66, 865 (2012). 10.1126/science.1235765 size that in free-living animals they can instead lead to adaptive adjustments in offspring (23, 24). Under high-density conditions, squirrels spend less time feeding and in the nest (10), suggesting The Cross-Bridge Spring: Can Cool that increased offspring growth is not a simple outcome of increased maternal care or milk pro- Muscles Store Elastic Energy? visioning. Alternatively, elevated exposure to glu- cocorticoids early in life (22, 25) could increase N. T. George,1 T. C. Irving,2 C. D. Williams,1,3 T. L. Daniel1* offspring growth by directly influencing off- spring physiology or behavior (22, 26) and sub- Muscles not only generate force. They may act as springs, providing energy storage to drive sequent changes in growth hormone secretion locomotion. Although extensible myofilaments are implicated as sites of energy storage, we in offspring (27). show that intramuscular temperature gradients may enable molecular motors (cross-bridges) to For nearly 100 years, food availability has store elastic strain energy. By using time-resolved small-angle x-ray diffraction paired with beenconsideredtobeauniversalvariableaffect- in situ measurements of mechanical energy exchange in flight muscles of sexta,we ing population dynamics and life-history traits produced high-speed movies of x-ray equatorial reflections, indicating cross-bridge association (28). Increased food availability also increases with myofilaments. A temperature gradient within the flight muscle leads to lower cross-bridge the population density of consumers, which has cycling in the cooler regions. Those cross-bridges could elastically return energy at the extrema made it difficult to distinguish whether the plas- of muscle lengthening and shortening, helping drive cyclic wing motions. These results suggest ticity in life-history traits after periods of high that cross-bridges can perform functions other than contraction, acting as molecular links for food availability is due to relaxation of food lim- elastic energy storage. itation or to adaptive reproductive adjustments to changes in density-mediated selection. Our re- lastic energy storage is heralded as a critical berlike protein in cuticle (1, 2). Elastic sults provide evidence that female red squirrels design characteristic of animal movement, energy storage is particularly important to flying can produce faster-growing offspring in the ab- Ebecause it promotes efficient locomotion. insects, reducing the otherwise prohibitive iner- sence of additional resources but only do so when Canonical examples of elastic energy-storage sites tial power costs of accelerating and decelerat- the fitness prospects warrant this increased invest- include tendons of mammals and resilin, the rub- ing the wings (3, 4). Two main sites of elastic

www.sciencemag.org SCIENCE VOL 340 7 JUNE 2013 1217 Density Triggers Maternal Hormones That Increase Adaptive Offspring Growth in a Wild Mammal Ben Dantzer, Amy E. M. Newman, Rudy Boonstra, Rupert Palme, Stan Boutin, Murray M. Humphries and Andrew G. McAdam

Science 340 (6137), 1215-1217. DOI: 10.1126/science.1235765originally published online April 18, 2013

Thank Your Mother Maternal effects and influence can sometimes prepare unborn offspring for some of the environmental conditions they may face. Dantzer et al. (p. 1215, published online 18 April) monitored a population of red squirrels and found that both natural and artificially induced increases in the number of conspecific calls increased the growth rate of pups Downloaded from because of increased glucocorticoid levels in the mother. The density stress experienced by mothers thus appears to stimulate them to produce pups that will grow faster and hopefully outcompete the many other pups expected to be produced in the dense population. http://science.sciencemag.org/

ARTICLE TOOLS http://science.sciencemag.org/content/340/6137/1215

SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2013/04/17/science.1235765.DC1 MATERIALS

RELATED http://stke.sciencemag.org/content/sigtrans/6/279/ec134.abstract CONTENT on August 14, 2019

REFERENCES This article cites 47 articles, 3 of which you can access for free http://science.sciencemag.org/content/340/6137/1215#BIBL

PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions

Use of this article is subject to the Terms of Service

Science (print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. 2017 © The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. The title Science is a registered trademark of AAAS. RESEARCH | REPORTS xylem sap were high under N-starved conditions TROPHIC CASCADES but lower under N-rich conditions. Altogether, the available evidence from molec- ular and physiological analyses of CEP–CEPR ligand Large carnivores make savanna tree receptor pairs suggests that CEP acts as a root- derived ascending N-demand signal to the shoot, where its perception by CEPR leads to the pro- communities less thorny duction of a putative shoot-derived descending signal that up-regulates nitrate transporter genes Adam T. Ford,1,2* Jacob R. Goheen,2,3 Tobias O. Otieno,2 Laura Bidner,2,4 in the roots. This mechanism supports N acqui- Lynne A. Isbell,2,4 Todd M. Palmer,2,5 David Ward,6 Rosie Woodroffe,2,7 Robert M. Pringle2,8 – sition, especially when NO3 is unevenly distrib- uted within the soil. CEP family peptides induced Understanding how predation risk and plant defenses interactively shape plant on one side of the roots by local N starvation distributions is a core challenge in ecology. By combining global positioning system mediate up-regulation of nitrate transporter genes telemetry of an abundant antelope (impala) and its main predators (leopards and wild in the distant part of the roots exposed to N-rich ) with a series of manipulative field experiments, we showed that herbivores’ conditions to compensate for N deficiency. risk-avoidance behavior and plants’ antiherbivore defenses interact to determine tree ThesystemicmodeofactionofCEPfamilypep- distributions in an African savanna. Well-defended thorny Acacia trees (A. etbaica) were tides in N-demand signaling is reminiscent of that abundant in low-risk areas where impala aggregated but rare in high-risk areas that of Rhizobium-induced, xylem-mobile CLE pep- impala avoided. In contrast, poorly defended trees (A. brevispica) were more abundant in tidesthatsuppressexcessnodulationinlegume high- than in low-risk areas. Our results suggest that plants can persist in landscapes plants, although CEP plays a role opposite to that characterized by intense herbivory, either by defending themselves or by thriving in risky of CLE in terms of lateral organ formation (5, 12, 13). areas where carnivores hunt. Plants, as sessile organisms, continuously face a complex array of environmental fluctuations he observation that most ecosystems sup- to explain the structure of this food web: (i) and have evolved sophisticated responses to cope port abundant plant life, despite the ex- Predation risk drives habitat selection by impala; with them. Given that CEP family peptides are istence of herbivores that eat plants, has (ii) impala prefer to eat less-thorny tree species, conserved throughout vascular plants except for T motivated a great deal of research and de- thereby suppressing their abundance; and (iii) ferns (8, 9), peptide-mediated root-to-shoot-to- bate in ecology. Two broad hypotheses predation risk thus differentially influences the root long-distance signaling is likely to be a gen- have been advanced to explain this phenome- distribution of thorny versus less-thorny Acacia eral strategy employed by all higher plants for non. The green world hypothesis (1)positsthat trees (table S1). environmental adaptation. predators indirectly benefit plants by suppress- To test our first hypothesis, we quantified hab- ing herbivory; such trophic cascades occur when itat selection by impala, using resource selection carnivores consumptively reduce herbivore den- functions, global positioning system (GPS) te- REFERENCES AND NOTES sities or trigger risk-avoidance behaviors (such lemetry, and high-resolution (0.36-m2)satellite 1. B. G. Forde, Annu. Rev. Plant Biol. 53, 203–224 as increased vigilance or refuge-seeking) that imagery (10) (fig. S2). Specifically, we quantified (2002). reduce plant consumption (2, 3). In contrast, the selection of woody cover, which represents 2. X. Gansel, S. Muños, P. Tillard, A. Gojon, Plant J. 26, 143–155 (2001). the plant defense hypothesis contends that forage for impala (9) but could also increase risk 3. S. Ruffel et al., Plant Physiol. 146, 2020–2035 (2008). the world is green because plants have evolved by concealing predators (11, 12). We also tracked 4. S. Ruffel et al., Proc. Natl. Acad. Sci. U.S.A. 108, 18524–18529 structural and chemical defenses that inhibit how impala used two discrete habitat features (2011). consumption (4, 5), often at a cost to their typified by low versus high woody cover (fig. S3): 5. D. E. Reid, B. J. Ferguson, S. Hayashi, Y. H. Lin, “ ” P. M. Gresshoff, Ann. Bot. (Lond.) 108, 789–795 (2011). growth and competitive ability (6, 7). Although (i) glades, which are ~0.5-ha clearings (with 8% 6. Y. Matsubayashi, Annu. Rev. Plant Biol. 65, 385–413 traditionally viewed as alternatives, these hy- mean tree cover) derived from abandoned cattle (2014). potheses are no longer thought to be mutually corrals, covered with nutrient-rich grasses, and – 7. K. Ohyama, M. Ogawa, Y. Matsubayashi, Plant J. 55, 152 160 exclusive (7, 8). A key challenge for contempo- maintained through grazing by wildlife (13, 14); (2008). “ ” 8. I. Roberts et al., J. Exp. Bot. 64, 5371–5381 (2013). rary ecology is to understand how plant de- and (ii) thickets, which are <100-m-wide strips 9. C. Delay, N. Imin, M. A. Djordjevic, J. Exp. Bot. 64, 5383–5394 fense and predation interact across landscapes of woody vegetation (with 25% cover) along the (2013). to shape a green world (8). edges of dry channels. We then quantified the 10. A. C. Bryan, A. Obaidi, M. Wierzba, F. E. Tax, Planta 235, We evaluated how the combination of plant relationship between woody cover and two com- 111–122 (2012). 11. E. A. Vidal, R. A. Gutiérrez, Curr. Opin. Plant Biol. 11, 521–529 defense and risk avoidance by a common African ponents of risk: (i) relative probability of encoun- (2008). ungulate (impala, Aepyceros melampus) deter- tering predators, assessed using resource-selection 12. N. Imin, N. A. Mohd-Radzman, H. A. Ogilvie, M. A. Djordjevic, mined the outcome of a trophic cascade in an functions of leopards and wild dogs for woody J. Exp. Bot. 64, 5395–5409 (2013). East African savanna. Impala consume a mixture cover; and (ii) per-capita risk of mortality from 13. S. Okamoto, H. Shinohara, T. Mori, Y. Matsubayashi, of grasses and trees (“browse”)(9) and are preyed predation, measured as the spatial distribution M. Kawaguchi, Nat. Commun. 4, 2191 (2013). upon by several carnivores, especially leopards of kill sites relative to the spatial distribution of ACKNOWLEDGMENTS ( pardus)andAfricanwilddogs(Lycaon impala (10). This research was supported by a Grant-in-Aid for Scientific pictus) (fig. S1). We tested three hypotheses (Fig. 1) Impala avoided woody cover (Fig. 2A) and Research (S) from the Ministry of Education, Culture, Sports, aggregated in glades and other open habitats, Science, and Technology (no. 25221105). The supplementary 1 especially during times of the day when their materials contain additional data. Department of Zoology, University of British Columbia, Vancouver, BC, Canada. 2Mpala Research Centre, Post Office predators are most active (tables S2 and S3). Box 555, Nanyuki, Kenya. 3Department of Zoology and Both the relative probability of encountering SUPPLEMENTARY MATERIALS Physiology, University of Wyoming, Laramie, WY, USA. predators (Fig. 2A) and the per-capita risk of 4Department of Anthropology, University of California, Davis, www.sciencemag.org/content/346/6207/343/suppl/DC1 CA, USA. 5Department of Biology, University of Florida, mortality from predation (Fig. 2B) increased Materials and Methods Gainesville, FL, USA. 6School of Life Sciences, University of with increasing woody cover. Leopards and Figs. S1 to S11 KwaZulu-Natal, Scottsville, South Africa. 7Institute of Table S1 wild dogs accounted for 83% of impala kills (52 Zoology, Zoological Society of London, Regent's Park, References (14–18) and 31% respectively; fig. S1), and kill sites from London, UK. 8Department of Ecology and Evolutionary 23 June 2014; accepted 3 September 2014 Biology, Princeton University, Princeton, NJ, USA. all species occurred in areas with similar 10.1126/science.1257800 *Corresponding author. E-mail: [email protected] amounts of woody cover (F2,51 =0.765,P =0.47).

346 17 OCTOBER 2014 • VOL 346 ISSUE 6207 sciencemag.org SCIENCE RESEARCH | REPORTS

Thus, a single cue—woody cover—integrated two Although impala avoided risky areas, this be- and open habitats (14). We tested this alter- components of risk (encounters and mortalities) havior might be explained by selection for the native hypothesis by experimentally removing arising from the two major predators of impala. nutrient-rich grasses that characterize glades all woody cover from five 0.5-ha plots, thereby

Fig. 1. Food web hypotheses tested in our study. Solid and dashed arrows represent direct and indirect effects, respectively. Red arrows represent negative effects, green arrows represent positive effects, and gray arrows represent either neutral or positive effects. Hypothesis 1: The risk of predation from large carnivores drives habitat selection of impala. Hypothesis 2: Impala both prefer and suppress the densities of poorly defended plants. Hypothesis 3: Predation risk increases the abundance of poorly defended trees in high-risk areas.

Fig. 2. Impala avoid risky areas, characterized by increasing woody cover. ance of woody cover, respectively. (B) The predicted per-capita risk of (A) Habitat selection by impala (green, b = –1.99 T 0.14, n =20impala,P < mortality from predation [1.70 + 0.228 × ln(woody cover)], coefficient of 0.001), leopards (red, b =3.42T 0.14, n =4leopards,P <0.001),andwild determination based on pooled kill sites from all large carnivores (fig. S2). dogs (pink, b =1.64T 0.19, n = 5 wild dogs, P < 0.001), where the bsrep- Values <1 and >1 indicate that kill sites occur less or more than expected, resent population-level coefficients from resource selection functions for respectively, relative to the spatial distribution of impala. Shading indicates woody cover. Positive and negative coefficients indicate selection and avoid- 95% prediction intervals.

SCIENCE sciencemag.org 17 OCTOBER 2014 • VOL 346 ISSUE 6207 347 RESEARCH | REPORTS

Fig. 3. Impala both preferentially consume and sup- Acacia brevispica Acacia etbaica press Acacia spp. lacking large thorns. The presence of long thorns significantly reduced impala’spreference for (A) A. brevispica and (B) A. etbaica in feeding experiments [likelihood ratio (LR)=4.76,P =0.029)]. The effects of species and species × thorns on pref- erence were nonsignificant (10). A value of 1 (dashed line) indicates that diet preference (leaf consumption) occurred randomly among the four treatments, whereas values >1 indicate selection and values <1 indicate avoidance. Over a 5-year impala exclusion experiment, the net density (stems/ha) of (C) A. brevispica, which lacks long thorns, increased in plots where impala 2 2.0 2.0 were absent (LR: c 1 =127.13,P < 0.001); in contrast, (D) A. etbaica decreased in plots where impala were 2 1.5 1.5 absent (LR: c 1 =158.88,P < 0.001). Error bars in- T dicate 1SEM. 1.0 1.0

0.5 0.5

Diet preference availability Use: 0.0 0.0 Control Thorn Control Thorn addition removal

250 250 -1 200 200 150 150 100 100 50 50 Net stems ha stems Net Abundance 0 0 Impala Impala Impala Impala present absent present absent mimicking the lowered risk of glades, but with- Fig. 4. Tree-community out potential confounds associated with forage composition as a quality. We monitored the movements of five function of predation GPS-collared impala herds for 60 days before risk. Impala avoid and after creating these clearings. Impala’s use woody cover because it of these areas increased by 160 to 576% after increases the risk of the removal of woody cover (table S4), indicat- predation (Fig. 1), ing that forage quantity and quality cannot fully thereby shifting tree explain impala’s selection of open areas. Addi- communities toward tionally, impala typically increase their consump- dominance by the tion of woody plants during the dry season when less thorny species grass quality is poor (9), yet we detected no sig- (A. brevispica) as woody nificant influence of season on their use of open cover increases. Shown habitat (tables S2 and S3). Hence, risk avoidance are (left) the mean appears to drive habitat selection by impala. proportions of GPS We next tested our second hypothesis: that relocations per individual impala prefer and consequently reduce the abun- (n = 20 adult female dance of poorly defended plants. We started by impala located at 20-min quantifying the effect of plant defenses on diet intervals in 2011–2012) preference, focusing on two common Acacia within each of four species (A. brevispica and A. etbaica) that to- classes of woody cover; gether constitute ~80% of trees in the study area the proportions of poorly (13) and differ in traits that may affect the diet defended A. brevispica preference of herbivores (4–8): A. brevispica has (middle left) and well-defended A. etbaica (middle right) among the total number of trees within 108 shorter thorns (≤0.6 cm versus ≤6.0 cm) but randomly located 200 m2 transects; and (right) the availability of woody cover within impala home ranges. higher condensed-tannin concentrations than Additionally, in Poisson regressions, woody cover had a positive effect on the number of A. brevispica A. etbaica (table S5). To measure the impact of stems [1.96 + exp(3.74 × woody cover); P < 0.001] and a negative effect on the number A. etbaica stems these traits on diet preference, we removed thorns [1.52 + exp(–1.03 × woody cover); P = 0.011]. Error bars indicate T1SEM. from A. etbaica branches and attached them to A. brevispica branches; we then presented both impala in a cafeteria-style feeding experiment. than for unmanipulated A. etbaica (Fig. 3, A types of manipulated branches alongside unma- Mean leaf selection by impala was 1.4 times and B). This preference for A. brevispica was nipulated controls of each species to free-ranging greater for unmanipulated A. brevispica branches due to differential thorniness: The removal of

348 17 OCTOBER 2014 • VOL 346 ISSUE 6207 sciencemag.org SCIENCE RESEARCH | REPORTS

A. etbaica’s long thorns increased leaf selection thorny trees. Consequently, the thorniness of tree 6. O. J. Schmitz, Proc.Natl.Acad.Sci.U.S.A.91,5364–5367 to levels commensurate with that of unmanipu- communities decreased across the landscape be- (1994). lated A. brevispica, whereas selection for thorn- cause of the way in which impala responded to 7. K. A. Mooney, R. Halitschke, A. Kessler, A. A. Agrawal, Science 327, 1642–1644 (2010). addition A. brevispica was roughly equal to that spatial variation in predation risk, and also be- 8. O. J. Schmitz, Resolving Ecosystem Complexity,vol.47 of unmanipulated A. etbaica (Fig. 3, A and B). causeofthewayplantdefensesaffectedimpala’s of Monographs in Population Biology,S.A.Levin, Thus, we conclude that A. brevispica is preferred diet preference. H. S. Horn, Eds. (Princeton Univ. Press, Princeton, relative to A. etbaica and that this preference is Human activities—both past and present— NJ, 2010). 9. D. J. Augustine, Afr. J. Ecol. 48, 1009–1020 (2010). determined by thorns rather than tannins or exert a major influence on the interactions be- 10. Materials and methods are available as supplementary other species-specific attributes. tween carnivores, impala, and the tree community. materials on Science Online. Next, we considered whether the diet pref- Glades represent the legacy of traditional live- 11. R. Underwood, Behaviour 79,81–107 1982). – erence of impala could alter the abundance stock production (17), generating a constellation 12. M. Thaker et al., Ecology 92, 398 407 (2011). 13. T. P. Young, N. Patridge, A. Macrae, Ecol. Appl. 5,97 of Acacia species. We therefore measured the of refugia that has shaped the spatial distribution (1995). netchangeinthedensityoftreestemsfrom of impala herbivory. However, the loss of large 14. D. J. Augustine, J. Wildl. Manage. 68, 916–923 (2004). 2009–2014 within nine replicate sets of 1-ha herbi- carnivores will make landscapes less risky (18), 15. J. R. Goheen et al., PLOS ONE 8, e55192 (2013). – vore exclosures that independently manipu- decoupling the spatial interplay of risk avoidance 16. J. L. Orrock, R. D. Holt, M. L. Baskett, Ecol. Lett. 13,11 20 (2010). lated megaherbivores [elephants (Loxodonta and herbivory. The loss of carnivores will also 17. K. E. Veblen, J. Arid Environ. 78, 119–127 (2012). africana)andgiraffes(Giraffa camelopardalis)], render obsolete the need for pastoralists to corral 18. J. Berger, J. E. Swenson, I.-L. Persson, Science 291, 1036–1039 mesoherbivores [impala and eland (Taurotragus their cattle nightly, eliminating the formation of (2001). oryx)], and small browsers [dik-dik (Madoqua glades. Consequently, human-driven extirpation 19. W. J. Ripple et al., Science 343, 1241484 (2014). guentheri)], using electrified wires at different of large carnivores from African savannas (2)will ACKNOWLEDGMENTS heights (15). We isolated the effects of impala on reduce spatial variation in plant communities, This research was supported by grants from Canada’s Natural Acacia species by comparing the megaherbivore leading to a world that is thornier, but still green. Sciences and Engineering Research Council (A.T.F., J.R.G.), the and mesoherbivore-exclusion treatments; we at- As large-carnivore populations continue to de- University of British Columbia (A.T.F.), the University of Wyoming tributed mesoherbivore-driven effects on tree cline globally, understanding the context in which (J.R.G.), the American Society of Mammalogists (A.T.F.), Keren Keyemet I’Israel (D.W.), the U.S. National Science Foundation density to impala because they account for ~87% predators shape key ecosystem processes is an (L.A.I.), and the Wenner-Gren Foundation (L.B.). We thank S. Lima, of browser biomass in this size class (9). The ex- urgent priority (19). Studies integrating risk of M. Kinnaird, M. Littlewood, B. Agwanda, C. Forbes, J. Estes, clusion of impala increased the net stem density predation and plant defenses will constitute a M. Kauffman, R. Ostfeld, S. Buskirk, C. Martinez del Rio, C. Riginos, of the preferred and poorly defended A. brevispica major step toward this goal. and the Kenya Wildlife Service. Comments from three anonymous reviewers greatly improved the manuscript. by 233% (Fig. 3C). Conversely, net stem density of well-defended A. etbaica increased by 692% REFERENCES AND NOTES in plots accessible to impala as compared to 1. N. G. Hairston, F. E. Smith, L. B. Slobodkin, Am. Nat. 94, 421 SUPPLEMENTARY MATERIALS (1960). impala-exclusion plots (Fig. 3D). This increase www.sciencemag.org/content/346/6207/346/suppl/DC1 2. J. A. Estes et al., Science 333, 301–306 (2011). Materials and Methods in A. etbaica in plots where impala were present 3. E. L. Preisser, D. I. Bolnick, M. F. Benard, Ecology 86, 501–509 Figs. S1 to S4 is perhaps due to reduced competition with (2005). Tables S1 to S5 4. W. W. Murdoch, Am. Nat. 100, 219 (1966). A. brevispica (15, 16). Thus, although impala References consumed leaves from both Acacia species (Fig. 3, 5. S. L. Pimm, The Balance of Nature?: Ecological Issues in the Conservation of Species and Communities (Univ. of Chicago 28 February 2014; accepted 15 September 2014 A and B), the long thorns of A. etbaica enabled Press, Chicago, 1991). 10.1126/science.1252753 them to avoid suppression by impala. To evaluate our third and final hypothesis, we related spatial patterns in the abundance of these two Acacia species to satellite-derived esti- CLIMATE CHANGE mates of woody cover. We counted all trees in 108 transects (200 m2) located near randomly se- lected glades and thickets throughout our 140-km2 Increased variability of tornado study area. The abundance of A. brevispica in- creased monotonically with satellite-derived es- timates of woody cover (i.e., risk) across these occurrence in the United States transects, whereas A. etbaica became scarcer as 1 2 2 woody cover increased (Fig. 4 and fig. S4). Risk Harold E. Brooks, * Gregory W. Carbin, Patrick T. Marsh avoidance by impala (Fig. 2) was functionally analogous to impala exclusion by electrified Whether or not climate change has had an impact on the occurrence of tornadoes in the fences (Fig. 3, C and D): Our results consistently United States has become a question of high public and scientific interest, but changes showed that the absence of impala herbivory in how tornadoes are reported have made it difficult to answer it convincingly. We show increased the prevalence of poorly defended trees that, excluding the weakest tornadoes, the mean annual number of tornadoes has remained but not the prevalence of well-defended trees. Thus, relatively constant, but their variability of occurrence has increased since the 1970s. This is treecommunitiesbecamelessthornyaspreda- due to a decrease in the number of days per year with tornadoes combined with an tion risk arising from large carnivores increased increase in days with many tornadoes, leading to greater variability on annual and monthly (Fig. 4). time scales and changes in the timing of the start of the tornado season. Collectively, our results show that the nature of trophic control is contingent on biotic context: eparating nonmeteorological effects in the collecting reports, and from how tornadoes are namely predation risk and plant defenses (Fig. 1). official database of tornadoes in the United observed. The mean occurrence of well-reported Both mechanisms enable plants to thrive in dif- States from actual meteorological ones aspects of the database, such as the mean annual ferent parts of the landscape: Where risk is high, has made interpreting the existence and S 1National Oceanic and Atmospheric Administration poorly defended trees are released from brows- causes of long-term physical changes in tor- ing, resulting in a trophic cascade; where risk is nado occurrence extremely difficult (1). Non- (NOAA)/National Severe Storms Laboratory, Norman, OK 73072, USA. 2NOAA/National Weather Service Storm Prediction low, intense herbivory increases the benefit of meteorological effects in the database result from Center, Norman, OK 73072, USA. defenses, creating communities dominated by changes in the emphasis on, and methodology of, *Corresponding author. E-mail: [email protected]

SCIENCE sciencemag.org 17 OCTOBER 2014 • VOL 346 ISSUE 6207 349 A syndrome of mutualism reinforces the lifestyle of a sloth

Jonathan N. Pauli1, Jorge E. Mendoza1, Shawn A. Steffan2, Cayelan C. Carey3,5, Paul J. Weimer4 and M. Zachariah Peery1 rspb.royalsocietypublishing.org 1Department of Forest and Wildlife Ecology, 2USDA-ARS, Department of Entomology, 3Center for Limnology, and 4USDA-ARS, Department of Bacteriology, University of Wisconsin–Madison, Madison, WI 53706, USA 5Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA

Arboreal herbivory is rare among mammals. The few species with this lifestyle Research possess unique adaptions to overcome size-related constraints on nutritional energetics. Sloths are folivores that spend most of their time resting or eating Cite this article: Pauli JN, Mendoza JE, in the forest canopy. A three-toed sloth will, however, descend its tree Steffan SA, Carey CC, Weimer PJ, Peery MZ. weekly to defecate, which is risky, energetically costly and, until now, inexplic- 2014 A syndrome of mutualism reinforces the able. We hypothesized that this behaviour sustains an ecosystem in the fur of lifestyle of a sloth. Proc. R. Soc. B 281: sloths, which confers cryptic nutritional benefits to sloths. We found that the 20133006. more specialized three-toed sloths harboured more phoretic , greater concentrations of inorganic nitrogen and higher algal biomass than the gener- http://dx.doi.org/10.1098/rspb.2013.3006 alist two-toed sloths. density was positively related to inorganic nitrogen concentration and algal biomass in the fur. We discovered that sloths con- sumed algae from their fur, which was highly digestible and lipid-rich. By descending a tree to defecate, sloths transport moths to their oviposition Received: 16 November 2013 sites in sloth dung, which facilitates moth colonization of sloth fur. Moths Accepted: 20 December 2013 are portals for nutrients, increasing nitrogen levels in sloth fur, which fuels algal growth. Sloths consume these algae-gardens, presumably to augment their limited diet. These linked mutualisms between moths, sloths and algae appear to aid the sloth in overcoming a highly constrained lifestyle. Subject Areas: ecology, evolution 1. Introduction Keywords: While herbivory is the predominant foraging strategy among mammals, arboreal commensalism, Costa Rica, Cryptoses, herbivores are exceedingly rare. Indeed, less than 4% of all mammalian genera con- Trichophilus tain species that are, to some extent, arboreal and herbivorous, and only 10 species of mammals (or less than 0.2% of mammalian diversity) are considered specialized arboreal herbivores [1]. Species that forage on plant matter in trees possess a highly constrained lifestyle. On one hand, they must be small and light to be supported in Author for correspondence: the canopy; on the other hand, small body size limits digestive capacity, especially Jonathan N. Pauli for processing plant matter, which is rich in fibre but low in digestible nutrients. e-mail: [email protected] So, although the evolution towards arboreal herbivory is found in taxonomically disparate mammalian groups, including primates, tree sloths and marsupials, all weigh between 1 and 14 kg [2]. Thus, the rarity of this lifestyle and convergence of body size among herbivorous and arboreal mammals appears to reflect con- straints of nutritional energetics on body size [3]. To overcome such constraints, arboreal herbivores have evolved dramatic anatomical (e.g. ruminant-like pre- gastric digestive organs), physiological (e.g. depressed metabolic rates) and behavioural (e.g. strict dietary preferences) adaptations. Sloths, or los perezosos (‘the lazies’) in Spanish, are slow-moving Neotropical mammals. The two phylogenetic groups, two- (Choloepus spp.) and three-toed (Bradypus spp.) sloths (figure 1a,b), diverged around 40 Ma [4] and are ecologi- cally quite different. Although both are mid-sized foregut fermenting arboreal mammals [2], two-toed sloths possess relatively large home-ranges (x ¼ 18:7 ha, Electronic supplementary material is available but up to 140 ha) [5] and a comparatively diverse diet of animal matter, fruits at http://dx.doi.org/10.1098/rspb.2013.3006 or and leaves, whereas three-toed sloths have highly restricted home-ranges  ¼ via http://rspb.royalsocietypublishing.org. (x ¼ 5:4 ha, range 0.3–15.0 ha) [6] and are regarded as strict folivores [7]. Fur- thermore, individual three-toed sloths are specialists, roosting and consuming

& 2014 The Author(s) Published by the Royal Society. All rights reserved. (c) 12 ** 2

(a) rspb.royalsocietypublishing.org 10 sloth) –1 8

6

4

2 moth biomass (mg kg

0 B Soc. R. Proc. (d) ** 200

150 281 20133006 : (ppm) +

4 100

(b) 50

0

(e) 140 *

120 )NH –1 100 (mg l

a 80

60

40 chlorophylla 20

0 three-toed two-toed sloth sloth Figure 1. Both (a) three- and (b) two-toed sloths harbour a diverse ecosystem in their fur. (c–e) The more sedentary three-toed sloths (black bars) possessed (c)a þ greater number of moths, (d) more inorganic nitrogen in the form of NH4 and (e) greater algal biomass on their fur compared with two-toed sloths (grey bars). Error bars represent +1 s.e.; *p , 0.05, **p , 0.001. leaves from only a few tree species within the forest [6,7]. canopy to defecate constitutes approximately 8% of a Because of their nutritionally poor and toxic diet, three-toed sloth’s daily energetic budget (see the electronic supplemen- sloths possess the slowest rate of digestion for any mammal tary material for details). Given the heightened risk and [8,9]. To account for this low-energy accrual, three-toed energetic cost for a sloth to defecate on the forest floor, one sloths possess an exceedingly low metabolic rate, less than would expect it to be an important fitness-enhancing behav- half of that expected for their mass [3,10]. iour. Suggested benefits of this behaviour to three-toed sloths About once a week, three-toed sloths descend from the include fertilizing their preferred trees, communicating with canopy to the base of their modal tree, where they create a other sloths via latrines or avoiding detection from predators depression in the ground with their vestigial tail, and deposit [13]. Given the nutritional constraints imposed by the lifestyle their dung. After defecation, sloths cover their latrine with of tree sloths, we hypothesized that this behaviour could be leaf litter and ascend to the canopy [7]. Two-toed sloths defe- driven by a cryptic, yet important, nutritional input. cate from the canopy or on the ground, especially when Both species of sloths harbour a diverse assemblage of switching trees (which they do frequently) [7], and their rou- symbiotic microorganisms in their fur, including species of tine, in terms of both frequency and site fidelity, is far less algae, and detritivorous fungi, many of which constrained [11]. Descending a tree is both risky and energe- only exist within the phoretic ecosystem residing in sloth tically costly for any sloth. Indeed, it is the leading cause of fur. Green algae (Trichophilus spp.) are especially abundant mortality for a sloth; more than one-half of all adult sloth [14]. Individual hairs of three-toed sloths possess unique mortalities we have documented were depredation events transverse cracks, which allow the hair shaft to become satu- when sloths were at or near the ground [12]. Furthermore, rated with rainwater, and which algae then colonize and we estimate that the average cost of descending from the grow hydroponically [15]. A commensal relationship has also been ascribed to sloths and pyralid moths (Cryptoses Ministerio de Ambiente, Energia y Telecomunicaciones, Sistema 3 spp.) [16], in which moths require the association (þ), but Nacional de A´ reas de Conservacio´n, Costa Rica. All samples rspb.royalsocietypublishing.org because they do not feed on sloths, impose no consequence were imported to the United States with CITES and United (0) on their host [17]. When a sloth descends a tree and defe- States Fish and Wildlife Service approval. To document the cates, gravid female moths leave the sloth and oviposit in the moth and algal community, as well as quantify levels of inor- ganic nitrogen and phosphorus in sloth fur, we captured fresh excrement. Larvae are copraphagous, developing previously marked adult two- (n ¼ 14) and three-toed (n ¼ 19) entirely within the dung, and adults emerge and fly to the sloths following standard procedures [5,6] in August 2012. canopy to seek their mating grounds in sloth fur to continue Because young sloths are often devoid of algae and appear to their life cycle. Although three-toed sloths regularly auto- acquire their algal community from their mother [14], we did groom [18], they are ineffective in removing sloth moths not include juveniles in our analyses. We cut a lock of hair from [19]. Because the life cycle of pyralid moths is entirely depen- the dorsum of each sloth and collected all moths from the sloth dent on these otherwise inexplicable behaviours in three-toed with an invertebrate vacuum. On average, we collected 15.2 B Soc. R. Proc. sloths, we posited that the moth–sloth interaction might (+2.9; range ¼ 4–39) and 4.5 (+1.3; range ¼ 0–21) moths from actually be an important mutualism, where sloths are also three- and two-toed sloths, respectively. To quantify the concen- benefiting by virtue of their association (þ/þ). trations of inorganic nitrogen and phosphorus, we sampled Mutualisms—jointly beneficial interactions between mem- (0.1 g) of sloth fur, and washed it with 15 ml of de-ionized water for 15 min. The wash was filtered through a 0.45 mm syringe mem- 281 bers of different species—are ubiquitous in nature, and þ

brane filter, and analysed for NO and NH using a flow 20133006 : among the most important of all ecological interactions [20]. 3 4 injection analyser (Quickchem 8000 FIA, Lachat Instruments) Ranging from diffuse and indirect to tightly coevolved direct and total phosphorus using an ICP/OES (Iris Advantage, interactions among multiple species [20,21], mutualisms Thermo-). Moths were identified (Cryptoses choloepi Dyar; have previously been invoked to account for otherwise Pyralidae: Chrysauginae) at the Systematic Entomology Labora- unexplained behaviours, such as ‘cleaner fish’ removing ecto- tories (USDA, Agricultural Research Service). We weighed each parasites from client reef fish [22], or ants defending acacia moth (+0.1 mg), and divided the total biomass of moth infestation trees [23], and as a mechanism by which nutritionally limited by the mass of the sloth (+0.1 kg) to account for individual differ- organisms cultivate and maintain a food source, like those ences in body size; even without scaling, however, we detected a þ observed in fungicultural systems of leaf cutter ants [24]. significant relationship between NH4 and both number of Given the ostensibly unrewarded risks the sloth appears to moths and total moth biomass (see electronic supplementary material, figure S1). be enduring on behalf of the moths, we hypothesized that We measured the chlorophyll a concentration of the microbial the phoretic symbionts, previously believed to possess a com- biomass in the fur of each sloth via fluorometry. Briefly, 0.01 g of mensal relationship with sloths, were in fact reinforcing this fur from each sloth was sonicated in ddH2O1 and methanol relationship by providing nutritional inputs to their hosts. 3 (for approx. 30 min each) to separate algal cells from the To explore the relationship of sloths with their phoretic fur (see electronic supplementary material, figure S2); the filtrate symbionts, we captured adult two- and three-toed sloths from the wash was centrifuged and measured on a fluorometer and quantified the number of pyralid moths infesting each to calculate the concentration of chlorophyll. Our estimates of individual, as well as other important ecosystem components algal biomass were corroborated by the change in mass of the within sloth fur, including the concentration of inorganic fur after sonication (i.e. the decrease in fur mass after algal nitrogen and phosphorus, and algal biomass on their fur. removal was related to chlorophyll a concentration). We used We also collected digesta from the forestomach of sloths to that change in mass of the fur following sonication to approxi- mate the biomass of algae in each sample. We then scaled our determine whether community members within the fur estimate of algal biomass from the sample to approximate the were being consumed. We predicted that the rigid behaviour total mass of algae on the entire sloth by assuming that 20% of observed in three-toed sloths promoted moth infestation, and the sloth’s body mass was fur [9] and that the observed percentage moth density would be greater compared with two-toed change in fur samples from cleaning was constant across the ani- sloths. We further predicted that, because moths are one of mal’s surface area. We compared differences between two- and þ the only portals of exogenous organic material to this ecosys- three-toed sloths in scaled moth biomass, NH4 concentrations tem, increasing moth density would promote nutrient and algal biomass with t-tests, and explored the relationship þ þ availability and productivity within sloth fur, and potentially between moth biomass and NH4 , and between NH4 with species provide nutritional inputs to ease some of the constraints as a categorical variable. Because the interaction for species and faced by this specialized arboreal herbivore. the predictor variable were non-significant for both moth species þ (t ¼ 1.09, p ¼ 0.28) and NH4 species (t ¼ 1.40, p ¼ 0.17), we reported the simple linear regression model with the continuous þ variable (e.g. moth biomass or NH4 ). 2. Material and methods (a) Describing the ecosystem on a sloth (b) In vitro fermentation experiments We conducted fieldwork approximately 85 km northeast of San To quantify the digestibility of the algae in the fur to organic Jose´, Costa Rica (10.328 N, 283.598 W). Both brown-throated acids from pregastric microbial fermentation, in vitro fermenta- three-toed sloths (Bradypus variegatus) and Hoffmann’s two- tions were conducted using a ruminal inoculum, a readily toed sloths (Choloepus hoffmanni) are relatively abundant across available microbial community with the capacity to degrade a our study site. Fieldwork was conducted as stipulated and auth- wide variety of plant components. The inoculum was compos- orized by IACUC protocol A01424 by the University of ited from two Holstein dairy cows (Bos taurus) and prepared as Wisconsin-Madison, and adhered to the guidelines for the use described previously [25], except that the squeezed ruminal of mammals in research set forth by the American Society of fluid was diluted to an OD525 of 5.0 using reduced buffer [26] Mammalogists. Access was granted by the private landowner, that contained 1 g trypticase peptone per litre. Fermentations and our project and sample collection was approved by the were conducted in 5 ml glass serum vials (Wheaton Scientific) that contained 150 mg of air-dried sloth fur from two- (n ¼ 10) (a) 4 ¼ 400 y = 116.2 + 5.78x and three-toed sloths (n 10). To assess the contribution of 2 r = 0.315 rspb.royalsocietypublishing.org algae and organic matter to the fermentation, we included 350 F1,31 = 14.3 ; p < 0.001 vials of fur from the same sloths, but which had been washed and sonicated in methanol to remove algae and other associa- 300 ted organic matter. Four blank vials with only ruminal 250

inoculum and reduced buffer were also analysed. Vials first (ppm) + 4 were gassed vigorously with CO2 for 2 min, and then sealed 200 tightly with #00 butyl rubber stoppers. Diluted ruminal inocu- NH 150 lum (2.00 ml) was added under CO2 gassing, and the vial was sealed with a flanged butyl rubber stopper and secured with 100 an aluminium crimp seal; these inoculations were performed in a398C room after temperature equilibration of the diluted rum- 50 B Soc. R. Proc. 0 510152025 inal fluid. Except for vigorous hand shaking at approximately moth biomass (mg kg–1) 0, 1, 2, 4 and 16 h, vials were incubated in an upright position (b) without shaking. After 24 h of incubation, vials were uncapped 250 y = 47.9 + 0.377x and 1.00 ml of deionized water was added. The liquid contents r2 = 0.245 281 ) F = 10.1 ; p = 0.003 were mixed several times with a micropipetter, and 1.00 ml of 200 1,31 –1

the liquid was removed for microcentrifugation (12 000g, 20133006 : 10 min, 48C). The supernatant was analysed for organic acids (mg l 150 by HPLC [27]. Net production of individual and total volatile a fatty acids (VFA; after subtraction of concentrations in blanks) was analysed by a mixed model in SAS v. 9.2 with sloth species 100 and fur treatment (washed versus unwashed) as class variables,

a species treatment interaction, and with individual animal chlorophylla 50 as random variable. The data (see electronic supplementary material, table S1) revealed that C2 –C5 straight-chain VFA 0 (acetic through valeric) derived primarily from carbohydrate 50 100 150 200 250 300 350 400 + fermentation were produced in higher amounts from unwashed NH4 (ppm) fur than from washed fur, and in fur from three-toed sloths than from two-toed sloths. By contrast, the production of Figure 2. Within the fur of sloths, an increasing number of moths led to branched-chain VFA (isobutyric, 2-methylbutyric and isovaleric), greater concentration of nitrogen, which is related to the biomass of þ which are uniquely derived from amino acid fermentations algae. Relationship between (a) pyralid moth infestation and NH4 concen- þ (specifically, the branched-chain amino acids leucine, isoleucine tration, and (b) amount of NH4 and algal biomass, in the fur of two- (grey) and valine), was low and did not differ between species or and three-toed (black) sloths. with treatment ( p . 0.30), suggesting minimal capacity for pregastric fermentation of algal protein. (d) Identifying algae in the digesta of sloths We collected digesta from the forestomach of two- (n ¼ 16) and (c) Compositional analysis of algae and plants three-toed sloths (n ¼ 12) via gastric gavage to determine whether algae had been consumed by sloths. We filtered a 2 ml We conducted compositional analyses for carbohydrates, pro- aliquot of digesta through a 60 mm sieve to exclude large par- teins and lipids of algal samples extracted from the fur of ticles. We then prepared microscope slides using 30 mlof two- (n ¼ 10) and three-toed (n ¼ 10) sloths, as well as leaf filtered digesta, and viewed each slide with a compound light samples from the six most commonly consumed plant species microscope at 400 magnification. We counted 100 cells of as percentage of dry matter content. For carbohydrate and algal or cyanobacterial material for each slide, and photographed protein analysis, samples (1–7 mg, weighed to 0.001 mg) were each cell detected. Algae and cyanobacteria were identified to the suspended in 200–600 ml of 0.2 M NaOH, heated at 808C for highest taxonomic resolution possible, and representative algal 40 min with frequent mixing by inversion, and cooled to and cyanobacterial groups were photographed (see electronic room temperature. After neutralization with 0.38 volumes of supplementary material, figure S3). 10% (v/v) glacial acetic acid, protein was assayed by the We compared the algal community detected in the digesta to Bradford method [28] using Coomassie Plus reagent (BioRad) that on the fur of two- (n ¼ 5) and three-toed (n ¼ 5) sloths. Fur with lysozyme as standard; carbohydrates were analysed by from these individuals were placed in a microcentrifuge tube the phenol-sulfuric acid method [29], using glucose as standard. containing 1 ml of ddH O and soaked for 1 h, agitated every For lipid extractions [30], air-dried (608C) algae (approx. 50 mg) 2 15 min for 5 min. Fur was removed from vials while the super- and leaves (100–200 mg) were suspended in 2 ml CHCl ,2ml 3 natant was used for microscope mounts. Microscope slides methanol and 1 ml H O in screw-cap tubes with Teflon liners. 2 were prepared using 30 ml of supernatant, viewed using a After vortexing for 2 min, the tubes were centrifuged (2500g, compound light microscope at 400 magnification and ident- 10 min, room temperature) and the chloroform phase recovered. ified as described above. Photographs of 100 algal and The remaining material was extracted three additional times, cyanobacterial cells from each slide were collected. each with 2 ml chloroform. The four chloroform extracts were pooled and treated with 3 ml of saturated NaCl in water. After the final centrifugation, the chloroform phase was recovered, and evaporated to approximately 0.5 ml volume under N2. The 3. Results and discussion concentrated extracts were quantitatively transferred with As predicted, three-toed sloths harboured more moths (figure 1c), CHCl3 washes to preweighed 1.5 ml microfuge tubes and the þ CHCl3 evaporated. The microfuge tubes were then air-dried as well as greater concentrations of NH4 (figure 1d)and overnight at 608C prior to weighing. Blank tubes were used to increased biomass of algae (figure 1e) in their fur than correct for weight loss of empty microfuge tubes on drying. two-toed sloths. We found a similar trend, but did not detect 5 rspb.royalsocietypublishing.org

(c)

algae (Trichophilus spp.)

+ 3– – NH4 PO4 NO3 (d)

(a) B Soc. R. Proc.

fungi (Ascomycota spp.) 281

mineralized sloth hair

(b) 20133006 :

sloth moths (Cryptoses spp.)

Figure 3. Postulated linked mutualisms (þ) among sloths, moths and algae: (a) sloths descend their tree to defecate, and deliver gravid female sloth moths (þ) to oviposition sites in their dung; (b) larval moths are copraphagous and as adults seek sloths in the canopy; (c) moths represent portals for nutrients, and via decomposition and mineralization by detritivores increase inorganic nitrogen levels in sloth fur, which fuels algal (þ) growth, and (d) sloths (þ) then consume these algae-gardens, presumably to augment their limited diet.

a significant ( p . 0.05) difference, in NO3 or total phos- algae between sloth species. Regardless, a food item with this 3 phorus (principally in the form of PO4 ) between the high lipid composition would provide an especially rich species (see electronic supplementary material, figure S4). (over twice that compared with protein or carbohydrate per However, as commonly observed in soils, these nutrients are gram) and rapid source of energy to sloths, as lipids would likely to be rapidly acquired by photosynthetic organisms or typically bypass the pregastric fermentation process. leached during rain showers [31]. Regardless of sloth species, Unsurprisingly, the same species of alga occurred in the þ NH4 concentration was positively related to the number of fur and digesta of both two- and three-toed sloths. Specifically, pyralid moths in the fur (figure 2a), and the biomass of algae we identified Trichophilus spp. in the digesta of two of the þ also increased with the concentration of NH4 in the fur of three-toed sloths (or 17%) and six of the two-toed sloths sloths (figure 2b). sampled (or 38%)—this symbiotic alga is only known to We estimate that the sloths on average harbour 125.5 g inhabit the fur of sloths (see electronic supplementary material, (+14.8 g, +1 s.e.) of microbial biomass (principally algae) in figure S3) [14]. The fact that the algae are readily digestible yet their fur, which translates into approximately 2.6% (+0.2%) were detected in our limited sample size suggests that the of their body mass. Our in vitro fermentation experiments frequency of ingested algae is likely to be high. revealed that algae in sloth fur are also highly digestible, that VFA production from algal digestion is primarily associated with carbohydrate fermentation, and that fur of three-toed sloths contains organic material sufficient to yield 24.4 mg of 4. Conclusion VFAs.(g fur21) from pregastric fermentation (see electronic Our data suggest that a series of linked mutualisms occurs supplementary material, table S1), nearly twice the amount between sloths, moths and algae (figure 3). Specifically, compared with two-toed sloths ( p , 0.001). Compositional sloths appear to promote pyralid moth infestation by des- analysis of algae and leaves of plant species preferred by cending to the base of the tree to defecate and assisting the sloths revealed that both items were rich in carbohydrates life cycle of moths [16,19], even in the face of heightened pre- (25.7% + 1.4 for algae versus 42.4% + 3.5 for plants; see elec- dation risk and significant energetic costs [12]. Moths in the tronic supplementary material, table S2), and possessed fur of sloths, in turn, act as a portal for nutrients, linking equivalent amounts of protein (5.0% + 0.39). Compared with the ecosystem within sloth fur to the surrounding environ- plant leaves, however, microalgae were three to five times ment. Within the sloth’s ecosystem, fungi are common [14] richer in lipid content—algae from two- and three-toed sloths and we postulate that moths are being mineralized by this were 45.2% (+4.0) and 27.4% (+0.8) lipid, respectively (see abundant community of decomposers. Alternatively, moths electronic supplementary material, table S2). Lipid content of could be directly transporting organic waste from the dung microalgae is inversely related to inorganic nitrogen levels pile to the fur. Regardless of the mechanism, increasing [32], which could explain the difference in lipid content of moth biomass increased inorganic nitrogen levels, which appeared to augment the growth of algal communities on though they presumably face similar predation pressure in 6 sloth fur. Sloths consume algae, presumably via autogroom- the forest canopy. Indeed, two- and three-toed sloths from rspb.royalsocietypublishing.org ing, for nutritional benefit. Our VFA and compositional data the same geographical area harbour phylogenetically distinct suggest that algae on the fur of sloths are especially rich in groups of Trichophilus spp., suggesting a long coevolutionary digestible carbohydrates and lipids. In short, we propose relationship between sloths and their algal community [14]. that sloths are grazing the ‘algae-gardens’ they have derived Whatever advantage algae confer to sloths, this complex from a three-way mutualism (figure 3). syndrome of mutualisms—among moths, sloths and algae— In addition to providing nutrition, it is possible that algal appears to have locked three-toed sloths into an evolutionary cultivation enhances sloth survival via camouflage reducing trade-off that requires it to face increased predation risk in mortality from aerial predators [13]. These two ultimate order to preserve linked mutualisms. Supporting the life mechanisms of algal cultivation are not mutually exclusive, cycle of moths may explain why three-toed sloths possess a but we speculate that the camouflage provided by algae is high fidelity to only a few modal trees, and a marked willing- B Soc. R. Proc. secondary to nutritional supplementation. First, the advan- ness to defecate in what is, for a sloth, the most dangerous part tage of increased concealment within the canopy would of the forest. These mutualisms could also contribute to have to be very strong to offset the high predation rates the sloth’s success as an arboreal herbivore, one of the most encountered when descending the tree to defecate, yet the constrained and rarest foraging strategies among vertebrates 281 algae–sloth symbiosis appears unrelated to the distribution [1]. Our study is the first to suggest that unique ecological of the primary aerial predator of sloths, the harpy eagle interactions, in addition to physiological and anatomical adap- 20133006 : (Harpia harpyja). Second, previously constructed energy tations, may foster an arboreal and herbivorous lifestyle; future budgets for three-toed sloths suggests that daily energy experiments that test the mechanistic linkages and putative expenditure can actually exceed intake [3], which might be benefits of the interactions between sloths, moths and algae from computational error [10] or because a cryptic food will help tease apart the exact nature of these linkages. item, like algae, has been missed. An unaccounted food source would help to explain why three-toed sloths are diffi- Acknowledgements. cult to keep well nourished in sanitized captive facilities [33]. Many thanks to E. Stanley and B. Zuckerberg for helpful discussions and comments on the manuscript, and to Finally, the mutualisms associated with the two-toed sloth, A. Solis for moth identifications. which is the more vagile and less restricted forager, were Funding statement. Funding was provided by the National Science Foun- more equivocal. Two-toed sloths possessed significantly dation (DEB-1257535), the Milwaukee Public Museum, the University fewer moths, and less inorganic nitrogen and algae, even of Wisconsin–Madison and the American Society of Mammalogists.

References

1. Eisenberg JF. 1978 The evolution of arboreal 7. Montgomery GG, Sunquist ME. 1978 Habitat 14. Suutari M, Majaneva M, Fewer DP, Voirin B, Aiello herbivores in the class mammalia. In The ecology of selection and use by two-toed and three-toed A, Friedl T, Chiarello AG, Blomster J. 2010 Molecular arboreal folivores (ed. GG Montgomery), pp. 135– sloths. In The ecology of arboreal folivores evidence for a diverse green algal community 152. Washington, DC: Smithsonian Institution Press. (ed. GG Montgomery), pp. 329–359. Washington, growing in the hair of sloths and a specific 2. Cork SJ, Foley WJ. 1991 Digestive and metabolic DC: Smithsonian Institution Press. association with Trichophilus welckeri (Chlorophyta, strategies of arboreal folivores in relation to 8. Foley WJ, Engelhardt WV, Charles-Dominique P. Ulvophyceae). BMC Evol. Biol. 10, e86. (doi:10.1186/ chemical defences in temperate and tropical . 1995 The passage of digesta, particle size, and in 1471-2148-10-86) In Plant defenses against mammalian herbivory (eds vitro fermentation rate in the three-toed sloth 15. Aiello A. 1985 Sloth hair: unanswered questions. In RT Palo, CT Robbins), pp. 166–175. Boca Raton, FL: Bradypus tridactylus (Edentata: Bradypodidae). The evolution and ecology of armadillos, sloths, and CRC Press. J. Zool. 236, 681–696. (doi:10.1111/j.1469-7998. vermilinguas (ed. GG Montgomery), pp. 213–218. 3. McNab BK. 1978 Energetics of arboreal folivores: 1995.tb02739.x) Washington, DC: Smithsonian Institution Press. physiological problems and ecological consequences 9. Britton SW. 1941 Form and function in the sloth 16. Waage JK, Montgomery GG. 1976 Cryptoses of feeding on an ubiquitous food supply. In The (concluded). Q. Rev. Biol. 16, 190–207. (doi:10. choloepi: a coprophagous moth that lives on a sloth. ecology of arboreal folivores (ed. GG Montgomery), 1086/394628) Science 193, 157–158. (doi:10.1126/science.193. pp. 153–162. Washington, DC: Smithsonian 10. Nagy KA, Montgomery GG. 1980 Field metabolic 4248.157) Institution Press. rate, water flux, and food consumption in three- 17. Odum E. 1953 Fundamentals of ecology. 4. Gaudin TJ. 2004 Phylogenetic relationships among toed sloths (Bradypus variegatus). J. Mammal. 61, Philadelphia, PA: WB Saunders Company. sloths (Mammalia, Xenarthra, Tardigrada): the 465–472. (doi:10.2307/1379840) 18. Chiarello AG. 1998 Activity budgets and ranging craniodental evidence. Zool. J. Linnean Soc. 140, 11. Goffart M. 1971 Function and form in the sloth. patterns of the Atlantic forest maned sloth Bradypus 255–305. (doi:10.1111/j.1096-3642.2003.00100.x) Oxford, UK: Pergamon Press. torquatus (Xenarthra: Bradypodidae). J. Zool. 246, 5. Peery MZ, Pauli JN. 2012 The mating system of a 12. Peery MZ, Pauli JN. In press. Shade-grown cacao 1–10. (doi:10.1111/j.1469-7998.1998.tb00126.x) ‘lazy’ mammal, Hoffmann’s two-toed sloth. Anim. supports a self-sustaining population of two-toed 19. Waage JK, Best RC. 1985 associates of Behav. 84, 555–562. (doi:10.1016/j.anbehav.2012. but not three-toed sloths. J. Appl. Ecol. (doi:10. sloths. In The evolution and ecology of armadillos, 06.007) 1111/1365-2664.12182) sloths, and vermilinguas (ed. GG Montgomery), 6. Pauli JN, Peery MZ. 2012 Unexpected strong 13. Chiarello AG. 2008 Sloth ecology: an overview of pp. 297–311. Washington, DC: Smithsonian polygyny in the brown-throated three-toed sloth. field studies. In The biology of the Xenarthra Institution Press. PLoS ONE 7, e51389. (doi:10.1371/journal.pone. (eds SF Vizcaino, WJ Loughry), pp. 269–280. 20. Herre EA, Knowlton N, Mueller UG, Rehner SA. 1999 0051389) Gainesville, FL: University Press of Florida. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. the fermentability of cellulosic biomass to ethanol. 29. Dubois M, Gilles KE, Hamilton JK, Rebers PA, Smith 7 14, 49–53. (doi:10.1016/S0169-5347(98)01529-8) Appl. Microbiol. Biotechnol. 67, 52–58. (doi:10. F. 1956 Colorimetric method for determination of rspb.royalsocietypublishing.org 21. Kiers ET, Palmer TD, Ives AR, Bruno JF, Bronstein JL. 1007/s00253-004-1844-7) sugars and related substances. Anal. Chem. 28, 2010 Mutualisms in a changing world: an 26. Goering HK, Van Soest PJ. 1970 Forage 350–356. (doi:10.1021/ac60111a017) evolutionary perspective. Ecol. Lett. 13, 1459–1474. fiber analysis: apparatus, reagents, procedures, 30. Huang G-H, Chen G, Chen F. 2009 Rapid screening (doi:10.1111/j.1461-0248.2010.01538.x) and some applications. Agricultural Handbook method for lipid production in alga based on Nile 22. Bshary R, Grutter AS, Willener AST, Leimar O. 2008 No. 379. Washington, DC: US Department of red fluorescence. Biomass Bioenergy 33, 1386– Pairs of cooperating cleaner fish provide better Agriculture. 1392. (doi:10.1016/j.biombioe.2009.05.022) service quality than singletons. Nature 455, 27. Weimer PJ, Shi Y, Odt CL. 1991 A segmented gas/ 31. Nadelhoffer KJ, Aber JD, Melillo JM. 1984 Seasonal 964–966. (doi:10.1038/nature07184) liquid delivery system for continuous culture of patterns of ammonium and nitrate uptake in nine 23. Janzen DH. 1966 Coevolution of mutualism between microorganisms on insoluble substrates and its use temperate forest ecosystems. Plant Soil 80,

ants and acacias in Central America. Evolution 20, for growth of Ruminococcus flavefaciens on 321–335. (doi:10.1007/BF02140039) B Soc. R. Proc. 249–275. (doi:10.2307/2406628) cellulose. Appl. Microbiol. Biotechnol. 36, 178–183. 32. Williams PJ le B, Laurens LML. 2010 Microalgae as 24. Currie CR, Mueller UG, Malloch D. 1999 The (doi:10.1007/BF00164416) biodiesel and biomass feedstocks: review and analysis agricultural pathology of ant fungus gardens. Proc. 28. Bradford MM. 1976 A rapid and sensitive of the biochemistry, energetics and economics. Energy Natl Acad. Sci. USA 96, 7998–8002. (doi:10.1073/ method for quantitation of microgram quantities Environ. Sci. 3, 554–590. (doi:10.1039/b924978h) pnas.96.14.7998) of protein utilizing the principle of protein-dye 33. Diniz LS, Oliveira PM. 1999 Clinical problems of 281 25. Weimer PJ, Dien BS, Springer TL, Vogel KP. 2005 In binding. Anal. Biochem. 72, 248–254. (doi:10. sloths (Bradypus sp. and Choloepus sp.) in captivity. 20133006 : vitro gas production as a surrogate measurement of 1016/0003-2697(76)90527-3) J. Zoo Wildl. Med. 30, 76–80. Quaternary Science Reviews 211 (2019) 1e16

Contents lists available at ScienceDirect

Quaternary Science Reviews

journal homepage: www.elsevier.com/locate/quascirev

Invited review The accelerating influence of humans on mammalian macroecological patterns over the late Quaternary

* Felisa A. Smith a, , Rosemary E. Elliott Smith b, S. Kathleen Lyons c, Jonathan L. Payne d, Amelia Villasenor~ a a Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA b Department of Mathematics, University of Chicago, Chicago, IL, 60637, USA c School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA d Department of Geological Sciences, Stanford University, Stanford, CA, 94305, USA article info abstract

Article history: The transition of hominins to a largely meat-based diet ~1.8 million years ago led to the exploitation of Received 10 August 2018 other mammals for food and resources. As hominins, particularly archaic and modern humans, became Received in revised form increasingly abundant and dispersed across the globe, a temporally and spatially transgressive extinction 24 February 2019 of large-bodied mammals followed; the degree of selectivity was unprecedented in the Cenozoic fossil Accepted 25 February 2019 record. Today, most remaining large-bodied mammal species are confined to Africa, where they co- Available online 13 March 2019 evolved with hominins. Here, using a comprehensive global dataset of mammal distribution, life his- tory and ecology, we examine the consequences of ‘body size downgrading’ of mammals over the late Keywords: fi Anthropocene Quaternary on fundamental macroecological patterns. Speci cally, we examine changes in species di- Paleogeography versity, global and continental body size distributions, allometric scaling of geographic range size with Body size downgrading body mass, and the scaling of maximum body size with area. Moreover, we project these patterns toward Size-selective extinction a potential future scenario in which all mammals currently listed as vulnerable on the IUCN's Red List are Megafauna extirpated. Our analysis demonstrates that anthropogenic impact on earth systems predates the terminal Macroecology Pleistocene and has grown as populations increased and humans have become more widespread. Terminal pleistocene megafauna extinction Moreover, owing to the disproportionate influence on ecosystem structure and function of megafauna, past and present body size downgrading has reshaped Earth's biosphere. Thus, macroecological studies based only on modern species yield distorted results, which are not representative of the patterns present for most of mammal evolution. Our review supports the concept of benchmarking the ‘Anthropocene’ with the earliest activities of Homo sapiens. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction et al., 2016a). On average, a modern industrial human metabo- lizes more than 40 times the amount of energy used by a hunter- More than any other single species in Earth history, humans gatherer (Decker et al., 2000); per capita energy consumption in have shaped their environment. The growth and of the USA is now equal to that of a 30,000 kg primate (Moses and the global human population over time has been fueled by resource Brown, 2003). Indeed, we are now in an ecological deficit (Burger extraction, which in turn has led to intense habitat alteration, et al., 2012), with annual anthropogenic demand for resources far species extinctions, and changes in climate and biogeochemical exceeding what Earth can regenerate each year (https://www. cycling (e.g., Vitousek et al., 1997; Decker et al., 2000; Myers and footprintnetwork.org/our-work/ecological-footprint/). Thus, the Knoll, 2001; Thomas et al., 2004; Barnosky, 2008; Burger et al., evolution of the genus Homo was a watershed event in Earth 2012; Smith et al., 2010a; Burnside et al., 2012; Braje and history. Erlandson, 2013; Dirzo et al., 2014; Boivin et al., 2016; Smith Around ~2 Ma ago, hominins transitioned from a mostly plant- based diet to one more dependent on meat, much of it provi- sioned from other mammals (Aiello and Wheeler, 1995; Foley, 2001; Aiello and Wells, 2002; Bunn, 2007; Anton et al., 2014; * Corresponding author. fi E-mail address: [email protected] (F.A. Smith). Zink and Lieberman, 2016). The adoption of re may have occurred https://doi.org/10.1016/j.quascirev.2019.02.031 0277-3791/© 2019 Elsevier Ltd. All rights reserved. 2 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 as early as half a million years after this dietary change (Wrangham occupied a variety of habitats within the temperate and tropical et al., 1999; Wrangham, 2009; Berna et al., 2012; Gowlett, 2016) zones, spanning some ~47 degrees of latitude (e.g., 400 Nto70 S; while the more sophisticated and regular use of tools occurred even Anton et al., 2014). Anthropologists do not yet agree on the routes, earlier (Roebroeks and Villa, 2011; Joordens et al., 2015; Shea, 2017). exact timing or number of initial migrations, but early members of The morphology of species such as Homo erectus reflected their our own species probably left Africa in pulses ca. 100 ka (Stringer more diverse diet and increased consumption of animal products and Andrews, 1988; Stringer, 2000; Walter et al., 2000; Carto (Andrews and Martin, 1991; Milton, 1999; Watts, 2008; Anton et al., et al., 2009; Groucutt et al., 2015, Fig. 1); an exodus likely driven 2014); associated physiological traits included a reduction in tooth and/or facilitated by changing environmental conditions (Anton, and gut size and increased body and brain size (McHenry, 1992; 2003; Carto et al., 2009; Larrasoana~ et al., 2013; Jennings et al., Aiello and Wheeler, 1995; Anton, 2003; Braun et al., 2010). How 2015; Parton et al., 2015; Breeze et al., 2016; Timmermann and these early hominins obtained animal resources is still in debate Friedrich, 2016; Tierney and Zander, 2017; Muttoni et al., 2018). (Domínguez-Rodrigo, 2002; Bunn, 2007), but it was likely through Specifically, the migration of humans from Africa may have been a combination of hunting and passive or active scavenging (Bunn tied to Heinrich events -climate episodes driven by the massive et al., 1986; Blumenschine, 1995; Domínguez-Rodrigo and Barba, release of icebergs due to ice sheet instability and the subsequent 2006; Luca et al., 2010; Anton et al., 2014). Some of the oldest addition of large volumes of fresh water to the North Atlantic (Carto uncontested evidence for these activities comes from Olduvai et al., 2009). These episodes, coupled with increasing aridity and Gorge in Tanzania where in situ butchered mammals ranging from the onset of glaciation, likely contributed to abrupt changes in hedgehogs to elephants were found at several sites dating to climate and vegetation and opened migration corridors (Carto et al., ~1.8 Ma (Blumenschine and Pobiner, 2006; Domínguez-Rodrigo 2009; Tierney and Zander, 2017). Hominins may also have been et al., 2007; Pante et al., 2017). following migrating prey into Eurasia (Carto et al., 2009; Muttoni Later hominins developed even more successful hunting and et al., 2018). In any case, by ca. 80e100 ka, Eurasia housed several scavenging technologies, allowing them to target large-bodied species of hominins, including Neanderthals, archaic humans, and prey. The earliest clear evidence of spear points dates from ~500 the enigmatic Denisovans (Stringer, 2000; Walter et al., 2000; Carto ka, and more complex projectile weapons were employed by 71 ka et al., 2009; Krause et al., 2010). The expansion of Homo sapiens into (Brown et al., 2012; Wilkins et al., 2012). Paleolithic cave paintings Melanesia and Australia likely occurred around 50e60 ka, and the depicting bison, horses, mammoth and reindeer, highlight the New World was colonized around 13e15 ka (Fig. 1; Dixon, 1999; importance of these animals to early hunters (Whitley, 2009). Bowler et al., 2003; O’Connell and Allen, 2004; Goebel et al., 2008; Stable isotope analysis of some Neanderthals, for example, in- Oppenheimer, 2012; Timmermann and Friedrich, 2016). Impor- dicates that their bone collagen was heavily enriched in 15N, tantly, the migration of humans around the world was accompa- indicative of a high degree of carnivory (Fizet et al., 1995; Richards nied by rapid increases in population density (Carto et al., 2009; et al., 2000; Bocherens et al., 2001; Sponheimer et al., 2007, 2013). Timmermann and Friedrich, 2016, Fig. 1b). Thus, in the late Quaternary, hominins had evolved to become Considerable work has focused on the pattern of extinction that wide-ranging generalist carnivores that predated on a broad array followed the migration of humans into Australia and the New of mammal species. Indeed, by the early to mid-Pleistocene, they World, with much of it focused on the issue of causation (e.g., may even have outcompeted other carnivores, resulting in a drastic Martin, 1967, 1984; 2005; Barnosky et al., 2004; Lyons et al., 2004; decline in carnivore functional richness in African ecosystems Miller et al., 2005; Koch and Barnosky, 2006; Ripple and Van (Werdelin and Lewis, 2013). Valkenburgh, 2010; Barnosky et al., 2011; Zuo et al., 2013). The migration of hominins out of Africa began ~2 million years Although still contentious, most scientists now agree that humans ago with the expansion of Homo erectus into Eurasia (Stiner, 2002; had a large contributing role to the terminal Pleistocene extinctions Anton et al., 2014; Rightmire et al., 2017). By 1.5 Ma, hominins (Martin, 1967, 1984, 2005; Martin and Steadman, 1999; Roberts

Fig. 1. Trends in extinction and human population growth over the late Quaternary. A) The cumulative loss of global mammal biodiversity over time. B) Estimated human pop- ulation growth over time. C) Human migration patterns over the late Quaternary. Shown are approximate dates; panel modified after Oppenheimer (2012). Data for human population over time from Hern (1999); data for biodiversity loss from Smith et al. (2018). F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 3 et al., 2001; Lyons et al., 2004; Miller et al., 2005; Koch and data for the Future interval are somewhat conservative because we Barnosky, 2006; Haynes, 2009; Sandom et al., 2014); there is also ignore mammals falling into the ‘data deficient’ category. These are consensus about the culpability of humans in Holocene extinctions species so poorly studied or rare that their conservation status is (Burney and Flannery, 2005; Turvey, 2009; Turvey and Fritz, 2011), unclear; many likely fall into a threat category. For some analyses, and in the ongoing biodiversity crisis and ecosystem degradation paleo data are too coarse to assign to specific time bins, so we (Vitousek et al., 1997; Cardillo et al., 2005; Schipper et al., 2008; subsume the LP, EP and TP into a single ‘LQ’ category, which rep- Barnosky et al., 2011; Estes et al., 2011; Dirzo et al., 2014; Ceballos resents 125e10 ka, or the late Quaternary up until the early et al., 2015; Ripple et al., 2015, 2016). Holocene. Moreover, there is a large and growing literature on modern and future human mediated influences on ecosystems, which makes 2. Materials and methods clear the rapid expansion of our ecological footprint over recent time (e.g., Decker et al., 2000; Purvis et al., 2000; Balmford et al., 2.1. Biodiversity loss 2004; Dirzo et al., 2014; Young et al., 2016; Ceballos et al., 2015; Ripple et al., 2015, 2016). However, we are just now beginning to Data employed were from Smith et al. (2018) and represent an appreciate the long prehistorical influence of hominins in general updated version of MOM v10 (Smith et al., 2003), which was on ecological communities (Braje and Erlandson, 2013; Werdelin revised to reflect mammalian taxonomy as of September 2017 and Lewis, 2013; Lyons et al., 2016a; Malhi et al., 2016; Smith (Mammal Species of the World v3.0; Wilson and Reeder, 2003). et al., 2016b, 2018; Bibi et al., 2017, Fig. 1a). These influences pre- Information included continental distribution, body mass, IUCN date the terminal Pleistocene; middle to late-Pleistocene extinc- Red List conservation status (www.iucnredlist.org), last occurrence tions of large-mammal fauna in Africa, for example, may have been dates for extinct species, and trophic affiliation for all mammals of linked to a combination of hominin behavioral and climate changes the late Quaternary (last ~125 ka). Because our focus was on non- (Bibi et al., 2017). Moreover, they follow the movement patterns of volant, terrestrial mammals, bats, marine or oceanic species, insular hominins, particularly humans, across the globe (Smith et al., 2018). mammals, and introductions were excluded for most analyses. As Indeed, the extra mortality experienced by large mammals as novel discussed above, extinct species were binned into one of five time and efficient human predators grew in abundance and dispersed intervals representing the approximate date of their extinctiond across the earth led to a temporally and spatially transgressive late Pleistocene (125e70 ka), end Pleistocene (70e20 ka), terminal pattern of size-biased extinction (Smith et al., 2018. Pleistocene (20e10 ka), Holocene (10e0 ka) and Future (þ200 Here, we explore the prehistoric influence of hominins on other years) for threatened taxa; this latter category included those mammals over the late Quaternary. Note that our review does not considered near-threatened, vulnerable, endangered, critically en- focus on the abundant evidence suggesting hominins were the dangered, or extinct in the wild on the IUCN Red List. Following main driver of these extinctions, but rather we focus on the con- Smith et al. (2018), we ignored speciation and assumed extant sequences of these events. Moreover, we do not differentiate be- mammal species were also present at the late Pleistocene. This tween the different hominin species that were present. We suspect assumption is reasonable because the average species ‘lifespan’ of a that Neanderthals, Denisovans and archaic and modern humans mammal is ~1e2 million years (Foote and Raup, 1996; Alroy, 2000; may all have been effective predators on other mammals, including Vrba and DeGusta, 2004). We collapsed trophic information into each other. However, it is clear that by the terminal Pleistocene, four general guilds (herbivore, carnivore, insectivore and omni- humans were the main drivers of these extinctions. Thus, here we vore) to reflect the major dietary mode. The statistical moments, review how size-selective exploitation of other mammals influ- degree of biodiversity loss, and changes in body mass were enced continental and global body size distributions, and illustrate computed globally and for each continent for each time interval. how this changed the energy flow through ecosystems and several We also characterized losses at different levels of the taxonomic fundamental macroecological patterns (e.g., Brown, 1995; Maurer, hierarchy. Distributional changes over time were assessed using 1999; Gaston and Blackburn, 2000; Gaston, 2003). We focus on Kolomorgorov-Smirnov tests; all analyses were conducted in R (R macroecological patterns because this is the domain where ecology, Core Team, 2015; R Studio, 2015). biogeography, paleobiology, and evolution overlap, and where the Data for human population growth over the late Quaternary connections between individuals, populations, communities and were extracted from Hern (1999). While these are admittedly ecosystems are evident (Smith et al., 2008). While these influences imprecise, his estimates were derived from the paleontological and likely began with the spread of hominins within Africa several archeological literature and extend far enough into the fossil record million years ago (e.g., Werdelin and Lewis, 2013; Bibi et al., 2017; for useful comparisons. Here, we compare human population es- Smith et al., 2018), data are limited for this time frame. Thus, our timates with extinction dynamics of other mammals over the late analyses focus on five time intervals that roughly correspond to Quaternary. important shifts in the demography and distribution of humans. These are: 1) the late Pleistocene (LP), around 125e70 ka, which 2.2. Extinction patterns roughly coincides with the initial migration of humans out of Africa into Eurasia; 2) the end Pleistocene (EP), about 70e20 ka, a time 2.2.1. Selectivity of extinctions period encompassing the colonization of Australasia; 3) the ter- The sudden loss of many species of large-bodied mammals at minal Pleistocene (TP), about 20e10 ka, an interval that represents the terminal Pleistocene has drawn considerable attention over the the migration of humans into the New World; 4) the Holocene (H), years (e.g., Guilday, 1967; Lundelius, 1967; Martin, 1967, 1984; about 10e0 ka, a time that represents the continued expansion of Graham and Lundelius, 1984; Graham and Grimm, 1990; Guthrie, humans across the Earth; and 5) the Future, about 200 years in the 1990; Murray, 1991; Lessa and Farina, 1996; Flannery and future, where we assume that mammals characterized as ‘vulner- Schouten, 2001; Martin and Steadman, 1999; Stuart, 1999; able’ by the IUCN actually become extinct. Because the conserva- Barnosky et al., 2004; Lyons et al., 2004; Koch and Barnosky, 2006; tion status of many species in the IUCN threat categories have Sandom et al., 2014), with later authors quantifying the degree of deteriorated rapidly over recent decades, it is likely that many, if selectivity across the taxonomic hierarchy and across continents not most, will go extinct (e.g., Cardillo et al., 2005, 2008; Barnosky (Lyons et al., 2004; Sandom et al., 2014). Similarly, the greater et al., 2011; Dirzo et al., 2014; Ceballos et al., 2015). We note that extinction risk of Holocene and modern IUCN Red Listed mammals 4 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 also has been quantified (Cardillo, 2003, Cardillo et al., 2003, 2005, mammals without regard to historic and prehistoric anthropogenic 2008; Schipper et al., 2008; Barnosky et al., 2011; Ceballos et al., extinctions, which have disproportionately targeted larger-bodied 2015, 2017; Ripple et al., 2015, 2016). However, only recently mammals (Smith et al., 2010a; Smith and Boyer, 2012). Only a have earlier extinctions been characterized and the change in few studies have examined shifts in range sizes over time (Ceballos extinction bias over time examined (Smith et al., 2018). Our dis- and Ehrlich, 2002; Morrison et al., 2007; Lyons and Smith, 2013; cussion of extinction selectivity is based largely on the data and Faurby and Svenning, 2015), and they have not quantified the in- results of Smith et al. (2018). As detailed above, data employed fluence on the ‘shape’ of the constraint envelope. included body mass estimates for extant and recently extinct Thus, we examined differences in the geographic range using mammals, last occurrence dates, continental distribution and tro- both historic and modern data extracted from two compilations phic guild. For each temporal interval, extinction selectivity by (Ceballos and Ehrlich, 2002; Morrison et al., 2007). We focused on group (i.e., global, continent, trophic guild) was quantified by taxa from four terrestrial mammal orders (Artiodactyla, Carnivora, calculating the difference in mean (log10-transformed) body mass Perissodactyla, and Proboscidea; N ¼ 275), because these groups between victims and survivors as well as by determining the co- experienced substantial range reductions over the past few cen- efficient of association between log10-transformed body mass and turies (Ceballos and Ehrlich, 2002; Morrison et al., 2007). We survival status using logistic regression. Smith et al. (2018) exam- computed future range size based on species status within the IUCN ined extinction selectivity globally, by continent, and by trophic Red List; as was done earlier, those mammals listed as vulnerable, group. We extend this to assess extinction selectivity for each tro- near-threatened, threatened, or endangered were assumed to phic group on each continent in each time interval. become extinct and removed. We assumed that ongoing range constriction would continue in to the future period. Thus, for the 2.2.2. Comparisons with deep time Cenozoic record future time bin, we further reduced surviving species’ ranges by the There has been a long and acrimonious debate in the literature percent lost between historic and modern periods. Body mass was about the role of climate in driving extinction in mammals, derived from MOM v10 (Smith et al., 2003). For each time bin, we particularly those of the terminal Pleistocene (e.g., Barnosky et al., plotted geographic range and body size by trophic guild (carnivore, 2004; Lyons et al., 2004; Koch and Barnosky, 2006; Grayson, or herbivore). “Constraint envelopes” (e.g., Brown and Maurer, 2007; Wroe et al., 2006, 2013; Sandom et al., 2014). More recent 1987) in the form of convex hulls (minimum bounding polygons) studies generally agree that human activities had a pivotal role, were fit to herbivores, carnivores and to describe the although climate shifts may have contributed to some extent energetic and/or environmental limits to the distribution of species (Barnosky et al., 2004; Lyons et al., 2004; Koch and Barnosky, 2006; in bivariate space. We characterized the upper constraint in two Haynes, 2009; Sandom et al., 2014). However, the idea that rapid ways: first, we ran a regression through the largest geographic changes in climate and vegetation at the PleistoceneeHolocene range for each 0.25 log body size bin across the 8 orders of transition led to mammal extinctions (Guilday, 1967; Lundelius, magnitude span of size; a similar analysis was done for the lower 1967; Graham and Lundelius, 1984; Graham and Grimm, 1990; constraint line. Second, we ran an upper quartile regression; doing Guthrie, 1990; Grayson, 2007) has not completely disappeared so for the lower quartile was non-informative because of the con- from the recent literature (e.g., Wroe et al., 2013; Meltzer, 2015). centration of values at small body masses and ranges. Constraint Thus, to robustly examine the potential role of climate on extinction envelopes were used to visualize the change in the relationship patterns, we compared turnover in the Cenozoic terrestrial between body mass and geographic range through time. Species mammal record and paleotemperature (Zachos et al., 2001) for the included in the modern range estimates were also included in an past 65 Ma. Our analyses followed the initial work reported by analysis of population trendsdbased on IUCN population estima- Smith et al. (2018) where extinction selectivity was computed for tesdto determine the proportion within four taxonomic orders 1 Ma intervals across the Cenozoic. Mammal turnover was (Artiodactyla, Carnivora, Perissodactyla, and Proboscidea), which compared to the global climate state (mean temperature), climate have decreasing, increasing or stable population size. variability (within 1 Ma intervals; using the standard deviation) and climate change (the change in these measures between 1 Ma 2.3.2. Area, species richness and body mass intervals) using linear regression. Further details regarding the The relationship between the area of a land mass and the largest methods are available in Smith et al. (2018). Mammalian turnover species present has received surprisingly little attention in the over the Cenozoic was characterized here using Foote's boundary macroecological literature. The few studies conducted to date crosser method (Foote, 2000), which takes into account sampling demonstrate a log linear relationship with the mass of the largest intensity. species increasing with increasing land area; reported values for the slope range considerably from 0.5 to 0.8 (Marquet and Taper, 2.3. Changes in macroecological patterns over time 1998; Burness et al., 2001; Smith et al., 2010a; Smith and Boyer, 2012). Explanations for the pattern vary, but generally relate to 2.3.1. Geographic range size some aspect of resource availability. For example, because large The relationship between species body mass and the size of the mammals have low population densities and large home ranges geographic range has been quantified by a number of workers (Damuth, 1981, 1987; Brown and Maurer, 1987, 1991), maximum (Anderson, 1977; Brown, 1995; Gaston and Blackburn, 1996; Rundle size may be limited by the number of home ranges that can fit into a et al., 2007; Lyons and Smith, 2013), who demonstrate that it is given land area (Burness et al., 2001; Maurer, 2013). roughly triangle-shaped for most groups. While small mammals Here, we re-evaluated this relationship in two important ways. may have either larger or small geographic ranges depending on First, we dramatically increased sample size by collecting temporal their degree of habitat specialization, large-bodied mammals data on the body size of the largest species for 97 different land- require a large range to maintain an effective population size masses, including islands, the major continents and ocean basins (Brown, 1995; Smith et al., 2008). Moreover, there is a dispropor- (http://biology.unm.edu/fasmith/Datasets/). We also conducted the tionately greater risk of extinction for animals that have small analysis with and without inclusion of marine mammals, which as ranges for their body size (Brown, 1995). This is considered a classic the largest-bodied mammals anchor the upper end of the regres- pattern in macroecology (Brown, 1995). However, it - like other sion. Area ranged in size from 1 km2 for the smallest islands (e.g., apparently fundamental relationships-was based on extant Todos Santos), to 5,451,700 km2 for Eurasia, and 266,702,000 km2 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 5 for the Atlantic, Pacific, Artic, and Southern ocean basins combined. Second, we investigated the influence of size-selective extinction on this relationship. Here, data limitations led us to focus on four time periods: LQ (125e10 ka), Holocene (10e0 ka), Modern (0 ka) and the Future (þ200 yrs). Note that our sample size of landmasses is not completely consistent over time. For example, we had fewer landmasses for the LQ because some were landbridge islands that only formed in with the rising of sea levels at the terminal Pleis- tocene. Both body mass and land area were logged prior to analyses and then evaluated using ordinary least squares regression.

2.3.3. Trophic structure Trophic downgrading of modern ecosystems is ongoing (Estes et al., 2011). The loss of the apex consumers in ecosystems has many direct and indirect consequences, including the potential to change vegetation structure and composition, unravel food webs, and change processes such as fire regimes (Estes et al., 2011; Ripple et al., 2014). We are just beginning to develop an appreciation for the integral role of large consumers in Earth systems (Smith et al., 2016a,b). Here, we examine the influence of the size-selective trophic downgrading across the Quaternary within two major terrestrial trophic groups, carnivores and herbivores. These are the groups that have suffered the greatest biodiversity losses over the late Quaternary (Smith et al., 2018). Fig. 2. The taxonomic sensitivity of extinction over time. A) Cumulative degree of As with the biodiversity analyses, we employed body mass, the extinction within each level of the taxonomic hierarchy. B) The distribution of extinction over various taxonomic levels. Note the sharp increase in both the extent IUCN Red List conservation status (www.iucnredlist.org), last and the breadth of extinction in the future time bin; while extinctions were once fi occurrence dates for extinct species, and trophic af liation for all confined to particular clades, they are now widespread across the taxonomic hierarchy. mammals of the late Quaternary from Smith et al. (2018). All members of the order Carnivora were classified as carnivores, regardless of the degree or source of meat consumption. We hundred years (Table 1; Fig. 2). This value may be conservative grouped species identified as being predominately browsers or because we ignored ‘data deficient’ mammals in the future pro- grazers as herbivores. We then characterized the distributions of jections. However, our cumulative estimate is in line with many these two trophic groups for the six time bins: prior (>125 ka), late recent projections, which focus on the change in biodiversity from Pleistocene (125-70ka), end Pleistocene (70e20 ka), terminal the modern to the future (Cardillo et al., 2005; Schipper et al., 2008; Pleistocene (20e10 ka), Holocene (10e0 ka), Modern (0 ka), and Hoffmann et al., 2010; Barnosky et al., 2011; Dirzo et al., 2014; Future (þ200 years), where all species listed as threatened, Ceballos et al., 2015; Ripple et al., 2015, 2016, 2017). Moreover, vulnerable, and extinct by the IUCN Red List were removed. while past extinctions were concentrated in particular taxonomic Changes in the range of body size and in the shapes of the distri- groups (e.g., the Holocene and late Pleistocene extinctions were butions over time were tested using Kolomorgorov-Smirnov tests; confined to 7 and 11 orders, respectively; Table 1), suggesting that all analyses were conducted in R. conserved biological traits made some clades more susceptible to extinction (Purvis et al., 2000; Turvey and Fritz, 2011), the magni- tude of future extinctions means they will necessarily become more 3. Results and discussion widespread across the taxonomic hierarchy (Fig. 2). Our computa- tions suggest that in the Future, for example, more than 88% of 3.1. Biodiversity loss orders could experience at least one extinction (Fig. 2). Moreover, extinctions could lead to considerable loss of phylogenetic and The extinction rate of mammals has increased dramatically over functional diversity with as many as ~27% of terrestrial nonvolant the last ~125,000 years (Fig. 1a), concomitant with the growth and families and 25% of mammalian orders lost (Table 1). spread of human populations (Fig. 1b and c). To date, we have lost Interestingly, these past and future extinction events have not approximately 8% of the world's mammals; without intervention changed the canonical ‘hollow curve’ pattern of species among the cumulative biodiversity loss could reach ~30% within a few

Table 1 Global alpha diversity of terrestrial nonvolant mammals by taxonomic level and time interval.

Interval Time Interval Cumulative Biodiversity loss (%) Extant at end of interval Species extinctions during interval

Species Genus Family Order Species Genus Family Order

Before 125 ka unknown 3305 891 126 32 Late Pleistocene 125-70 ka 0.5 3292 889 126 32 13 10 8 5 End Pleistocene 70-20 ka 2.1 3241 869 124 32 51 33 16 6 Terminal Pleistocene 20-10 ka 6.8 3084 792 115 30 157 101 33 11 Holocene 10e0 8.0 3043 785 112 29 41 28 12 7 Future 200 yrs 29.6 2328 604 92 24 711 349 82 21 Change from LP to Future 29.6 973 287 34 8

Higher level taxonomic information provided for extinct species showing the extent of loss; it does not represent the actual generic, family or ordinal losses. Those can be obtained by subtracting between temporal intervals. 6 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 genera (i.e., the S/G ratio), where a few lineages are species rich and bodied mammals will lead to increases in abundance or distribu- most are species poor (Fig. 3); a pattern ubiquitous across biology tion of survivors and/or changes in species compensation (Ernest (Willis and Yule, 1922; Anderson, 1977; Maurer and Brown, 1988; and Brown, 2001b). Brown and Maurer, 1989; Williams and Gaston, 1994; Roy et al., The loss of large-bodied mammals across the globe occurred in a 1996; Hilu, 2007). Because S/G ratios are sensitive to diversity spatially and temporally transgressive manner (Smith et al., 2018, (Simberloff, 1970), the null expectation would be a monotonic Fig. 5), co-incident with human migration patterns (Fig. 1c). Each decrease in the ratios with declining number of species (Jarvinen,€ time humans entered a new continent, extinctions followed. The 1982; Gotelli and Colwell, 2001). That we do not find this predic- downgrading of mean mammal body size was severe: at ~125 ka, tion borne out is interesting because late Quaternary extinctions the average global mass of terrestrial nonvolant mammals was were phylogenetically non-random (Lyons et al., 2004; Smith and ~81 kg (Fig. 5b). Today, it is about 16.8 kg. We predict that in the Lyons, 2011; Turvey and Fritz, 2011; Smith et al., 2018), and future future it will fall to ~6.9 kg, the lowest average global body mass of losses will also likely disproportionately target certain clades (e.g., mammals in ~55 million years (Smith et al., 2010b, Fig. 5a). A Cardillo et al., 2005, 2008; Schipper et al., 2008; Davidson et al., similar trajectory of body size downgrading is evident for 2009; Fritz et al., 2009; Dirzo et al., 2014; Pimm et al., 2014). maximum body mass on the continents (Smith et al., 2018). When Hence, we might anticipate that a higher proportion of monotypic mean global body mass of mammals is plotted against estimated genera, representing unique functional diversity, would be lost population size of H. sapiens over the late Pleistocene and Holocene, (e.g., Purvis et al., 2000). However, projected extinction intensity at we find a strong and significant correlation: the near exponential the genus level is only slightly higher than that of the species level growth of human populations has led to a near exponential (~32 vs 30%; Table 1, Fig. 2). decrease in mean body size over the Earth (Fig. 6). While the fundamental S/G ratios did not alter, late Quaternary and Future extinctions did and will lead to significant changes in 3.2. Extinction patterns the body size distribution (BSD) of mammal species over time (Fig. 4). On each continent (Fig. 4aee), and globally (Fig. 4f), there Late Quaternary extinctions and current extinction threat were has been a selective loss of the largest mammals from ecosystems, strongly biased against large-bodied terrestrial mammals leading to an approximate 2 orders of magnitude truncation in the (Fig. 5def; Fig. 7). A striking and highly significant size bias was range. Moreover, these changes, particularly since the terminal evident both globally (Fig. 7a and b), as well as when data were Pleistocene, have also meant reduced mean mass and the loss of stratified by continent (Fig. 7c and d) or by trophic group (Fig. 7e multi-modality in New World fauna (Lyons et al., 2004; Smith et al., and f; Smith et al., 2018). The average victim of Late Quaternary 2004; Smith and Lyons, 2011; Smith and Boyer, 2012; Lyons and extinctions was more than three orders of magnitude larger in body Smith, 2013), leading to a largely unimodal right-skewed distri- mass than the average surviving species (Fig. 7a). While several bution. The BSD of mammals first became bimodal ~40 Ma (Lyons authors have quantified the size selectivity of the terminal Pleis- and Smith, 2013), concomitant with the evolution of very large tocene megafauna extinction (e.g., Alroy, 1999; Lyons et al., 2004; body size and remained that way until the late Quaternary (Lyons Sandom et al., 2014), the realization that this event was part of a and Smith, 2013). Thus, the modern BSD of mammals on conti- long-term global trajectory is relatively recent (Koch and Barnosky, nents is unlike that seen earlier in Earth history. Because the dis- 2006; Braje and Erlandson, 2013; Smith et al., 2018). Strikingly, the tribution of body sizes regulates energy flow through communities, size selectivity of the Late Quaternary extinctions was completely restructuring of the BSD has important implications in terms of unprecedented in the previous fossil mammal record (Fig. 5c vs. 5d; ecological function. For example, the right skewed BSD observed see Alroy, 1999 for North America). No interval in the past 65 Ma for mammals (and many other taxa) reflects that there are more has resulted in the same level of extinction bias against large- species of small animals than large ones, suggesting that small bodied mammals seen in the late, end or terminal Pleistocene, things can or do more finely divide resources in the environment and even the Holocene and Future intervals are outliers in terms of (Hutchinson and MacArthur, 1959; Van Valen, 1973; Brown and the Cenozoic fossil record (Fig. 5d; Smith et al., 2018). These were Maurer, 1987; Dial and Marzluff, 1988; Brown and Nicoletto, unusual events. 1991; Fenchel, 1993; Brown, 1995). This pattern might suggest Interestingly, although large-bodied mammals still suffer(ed) competitive interactions are stronger or more important in struc- disproportionately, the selectivity of extinction decreased over the turing these size classes. Ecological homeostasis theory predicts Holocene and into the Future (Figs. 5 and 7); indeed, the difference that unused energy in an ecosystem resulting from the loss of large- in body mass between victims and survivors drops to approxi- mately one order of magnitude for extinctions during the Holocene and for projected future losses (Fig. 7a). This change in the selec- tivity likely reflects the reduced diversity of large-bodied mammals extant (e.g., fewer to go extinct) as well as a change in the nature of threats. However, the simple truncation of the size distribution does not explain the reduced association between size and extinction observed over time in the regression analysis (Fig. 7b, d, f, h). While direct exploitation was probably the main driver of the late Quaternary extinctions (Alroy, 2001; Zuo et al., 2013), a more complex suite of stresses including hunting, extermination (of carnivores in areas with livestock), fragmentation and/or land use change, and climate change, are driving Holocene and future ex- tinctions (Vitousek et al., 1997; Barnosky et al., 2004, 2011; Cardillo et al., 2005, 2008; Schipper et al., 2008; Estes et al., 2011; Dirzo Fig. 3. The pattern of species diversity within genera. Note that despite phylogenetic et al., 2014; Ceballos et al., 2015; Ripple et al., 2015, 2016). selectivity, extinctions during the late Quaternary did not change the fundamental Indeed, future extinctions target not only large-bodied mammals, ‘Hollow curve’ pattern of the number of species per genus. Both curves are concate- nated at 50 species per genus; there are a few genera in both time intervals that are but also small, often highly specialized or geographically localized much more speciose. species (Lyons et al., 2016b; Ripple et al., 2017; Smith et al., 2018). F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 7

Fig. 4. Body size downgrading over the late Quaternary. Redrawn from Smith et al. (2018)..

Fig. 5. Body size and extinction selectivity of mammals over the Cenozoic. A) Mean body size (kg) from 66 to 1 Ma. B) Mean body mass over the late Quaternary (last ~125 ka years). C) Body size selectivity of extinctions over the Cenozoic era, D) Body size selectivity over the late Quaternary, E) Difference in body mass between victims and survivors (in log units) over the Cenozoic, and, F) Difference in body mass between victims and survivors (in log units) over the late Quaternary. Note the temporally and spatially transgressive decrease in body mass; this corresponds with human migration patterns (Panels aed redrawn after Smith et al., 2018). 8 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16

The larger size bias observed in data when stratified by conti- nent rather than by trophic group (Fig. 7) suggested that the esti- mation of bias was reduced in the global analyses. This reduction may have occurred because global analyses mixed extinction pat- terns on continents that, at least prior to the Late Quaternary, hosted many of the largest species (e.g., Africa, Eurasia, North America) with continents that hosted fewer extremely large- bodied species (e.g., Australia). The size bias reported by Smith et al. (2018) persisted when further stratified both by continent and by trophic group (Fig. 7 g, h). In general, the size bias was greatest for herbivores, followed by carnivores, and smaller in omnivores and insectivores. This led to striking changes in the global distribution of herbivores and carnivores over time (Fig. 8). Note that we focus here on the consequences and not the causes Fig. 6. The mean body mass of mammals across the late Quaternary plotted against of late Quaternary extinctions. The evidence is overwhelming for a estimated human population size. Data for human population growth from Hern strong contributing role of humans in each of these time periods (1999). Mean body mass for each interval from Smith et al. (2018). The estimate (e.g., Alroy, 2001; Lyons et al., 2004; Koch and Barnosky, 2006; (and standard error) of the coefficients: Intercept ¼ 2.902 (0.1829), slope ¼ -0.208 (0.0279); Multiple R-squared: 0.9171, P < 0.001, df ¼ 5. Haynes, 2009; Surovell and Waguespack, 2009; Turvey, 2009; Barnosky et al., 2011; Turvey and Fritz, 2011; Zuo et al., 2013;

Fig. 7. Extinction selectivity patterns with respect to body size from the Late Quaternary through the near future. A) Differences in mean (log10-transformed) body mass between victims and survivors globally for the Late Pleistocene (LP), end-Pleistocene (EP), terminal Pleistocene (TP), Holocene (H), and near future (F) scenarios. B) Logistic regression coefficients with 95% confidence intervals from logistic regression of extinction status as a function of body mass, globally. C) Size differences between victims and survivorsby continent. D) Logistic regression coefficients by continent. E) Size differences by trophic group. F) Logistic regression coefficients by trophic group. G) Size differences by continent and trophic group. H) Logistic regression coefficients by continent and trophic group. F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 9

difference in size between the mean size of victim and survivor) or extinction rate (turnover). These results argue that climate change in the past was not a key driver of extinction in mammals (Smith et al., 2018). While climate shifts led to changes in abundance, distribution, and likely morphological adaptation (Smith et al., 1995, 1998; 2010b; Smith and Betancourt, 2003), most mammals were able to cope with the changing environments of the Cenozoic through these mechanisms. Finally, the trophic bias we find is consistent with the exploi- tation of mammals for food. The bias of extinction is greatest for herbivores, which have tended to be the most important hominin prey, moderate against carnivores, which tend to compete with hominin hunters for large prey (or, more recently, livestock), and weakest against omnivores and insectivores, which tend to have less value as prey and less competition with hominins over food resources (Fig. 7e and f; Fig. 8). Moreover, the greater selectivity of extinction after controlling for continent suggests that it is relative size within a continent rather than absolute size that has influenced extinction probability (Fig. 7g and h). This finding is more consis- tent with an effect of hunting, which acts on the availability species pool, than of a physiological response to climate change or an ecological response associated with a fundamental scaling property. Changes in macroecological patterns over time.

3.2.1. Geographic range Elucidating the factors constraining and shaping the geographic range of animals has captivated naturalists since they began exploring the planet (Humboldt et al., 2009). Darwin (1859) wrote: ‘I have lately been especially attending to Geograph. Distrib., and most splendid it is, a grand game of chess with the world for a Board’. Despite centuries of research, understanding the constraints on geographic ranges remains one of the fundamental aims of bioge- ography (Brown and Lomolino, 1998). Anthropogenic climate

Fig. 8. Histograms of log body-size are plotted for species classified as carnivores (A) change has led to geographic shifts in the range extent of many and herbivores (B) at six different time-bins within which extinctions occur. Within species, with northern hemispheric species shifting ranges toward the future time bin, predicted extinctions occur within species classified as vulnerable, the north pole and southern hemispheric species shifting towards threatened, or endangered. the south pole (Parmesan and Yohe, 2003); future warming may lead to the contraction of ranges as well. Human activities have also led to declines and/or fragmentation of the distribution of many Sandom et al., 2014; Surovell et al., 2016; Smith et al., 2018) and species, especially in Africa and Eurasia (Ceballos and Ehrlich, 2002; thus, we do not debate the issue of causation. Nonetheless, we note Morrison et al., 2007; Crooks et al., 2017). Not surprisingly, we find that our work both highlights the influential role of humans, and that the body size downgrading of the late Quaternary has funda- contravenes a role for climate as a driver of mammal biodiversity mentally changed the relationship between the body size of loss in several important ways. mammal species and their geographic range (Fig. 10). For some First, as we noted above, we find no evidence in the fossil record large-bodied herbivores, for example, the modern range has shrunk prior to the evolution of hominins for the type of dramatic size more than three orders of magnitude relative to historic time pe- selectivity observed over the past 125 ka (Figs. 5e7). It was riods (Fig. 10d). Overall, the average geographic range of mammals completely unprecedented in 65 Ma of mammal evolution; body has decreased by 48%, although the impact was much greater for size did not normally influence extinction risk (Alroy, 1999; Tomiya, herbivores than carnivores (60% vs. 30%, respectively; Fig. 10c and 2013; Smith et al., 2018). The pattern of size-selectivity was both d). This enhanced dataset confirms earlier work suggesting large- temporally and spatially transgressive (Fig. 5b), and closely fol- bodied mammals have lost at least 30% of their range since his- lowed human migration patterns (Fig. 1c; Smith et al., 2018). toric times, and that ~40% have experienced 80% or more of range Moreover, the mean body size of mammals globally was inversely contraction (Ceballos et al., 2017). and significantly related to human population size (Fig. 6). Mammal range-size loss was not randomly distributed across Second, the lack of relationship between extinction selectivity, space or dietary affiliation. From historic to modern time, the de- or the rate of extinction, and Cenozoic climate is remarkable (Fig. 9). clines were greatest for Africa and Asia (Ceballos and Ehrlich, 2002). Neither the selectivity nor the rate of mammalian extinction in the The largest contractions were generally seen for species whose Cenozoic fossil record was significantly correlated with the mean ranges overlapped with areas of particularly high human density or global climate state or with the trend in global climate as measured modification of landscapes such as agricultural fields (Ceballos and through the marine oxygen isotope record (Smith et al., 2018). Ehrlich, 2002; Morrison et al., 2007). Generalists have been more Whether measured in terms of mean temperature, temperature successful than specialists in coping with the consequences of variability, or change in temperature (Fig. 9), there was no corre- human impacts on ecosystems such as invasive species and biotic lation between any of the climate variables and either extinction homogenization (Olden et al., 2004; Davidson et al., 2009; Clavel selectivity (measured as the logistic regression coefficient or as the et al., 2011; Longman et al., 2018). And of course, an extreme 10 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16

Fig. 9. Scatterplots of extinction patterns versus measures of climate across the Cenozoic at million-year intervals. Extinction is quantified as: first row) the negative of the natural log of the number of the number of species ranging through the interval divided by the number of species entering the stage from the previous interval but not surviving into the subsequent interval (Foote, 2000); second row) the logistic regression coefficient measuring the association between body mass and extinction; and third row) the difference in mean size between victims and survivors. Climate is measured in terms of mean, standard deviation, and interval-to-interval change in mean oxygen isotope paleoclimate proxy values from planktic foraminifera. generalist, Homo sapiens, has been the most significant invasive bodied mammals suffer disproportionately from human activities species and ecological engineer of the late Quaternary (Marean, (Crooks et al., 2017). 2015). Not surprisingly, some mammals with small geographic ran- The shape of the ‘constraint space’ that characterizes the rela- gesdoften specialistsdare at risk owing to wide-scale habitat tionship between geographic range and body size (Brown, 1995) restructuring by humans (Flannery and Schouten, 2001; Ripple has also altered significantly over time (Fig. 10). In the past, the et al., 2017). The bottom portion of the constraint envelope drop- upper constraint limit between geographic range and body size was ped an order of magnitude across body size classes from historic to well-described statistically (Table 2), reflecting the general pattern modern times (Fig. 10e and f). Indeed, it is the bottom of the that species with larger body sizes also had larger ranges. However, constraint envelope where species may be most vulnerable to range fragmentation and constriction have influenced the largest extinction in the future (Brown and Maurer, 1987). Our future mammals disproportionately; they have lost on average ~70% of polygons (Fig. 10g and h) confirm this prediction; while mammals their former range, as compared to 22e35% for mammals of smaller larger than ~130 kg have lost 50e70% of their range since historic sizes (Fig. 11). Thus, the slope of the relationship has decreased times (N ¼ 78 species), the smallest mammals (<3 kg) have on from the historic into the modern, and moreover, is no longer average experienced a 71% range contraction (N ¼ 3 species; distinguishable from zero (Fig. 10; Table 2). The decline in the Fig. 11). Whether this is a universal pattern is unclear (but see geographic ranges of large mammals is a direct consequence of Ripple et al., 2017). their large range, which brings animals into greater contact, and Some species have benefited from the changes in ecosystem thus conflict, with humans on an increasingly fragmented earth structure. Today, as large carnivores decline, mesocarnivores, such (Cardillo et al., 2005; Barnosky et al., 2012; Tucker et al., 2018). The as the coyote (Canis latrans) are increasing both their range and geographic range is an amalgamation of the home ranges of the population size, presumably owing to a reduction in competitive individuals within the species. Because large-bodied mammals are pressures (Ritchie and Johnson, 2009). Mesocarnivore release may generally constrained to have low population densities, their also have occurred with the extinction of larger-bodied carnivores effective population size will be small unless they have a large earlier in earth history (Pardi and Smith, 2016). The transformation geographic range (Brown, 1995). Thus, reductions in their of mesocarnivores into apex carnivores may influence the popula- geographic range will lead to reduced densities, which increases tion dynamics of smaller mammals in communities (Prugh et al., the probability of extinction (MacArthur and Wilson, 1967; Brown, 2009; Pardi and Smith, 2016). Indeed, across trophic guilds, we 1995). Habitat fragmentation is yet another way in which large- find that medium-sized mammals show the lowest range F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 11

Fig. 11. Geographic range reductions from historic to future time intervals by body size.

We find that body size downgrading over the late Quaternary

Fig. 10. Influence of humans on pattern of geographic range and body mass of changed the scaling relationship between maximum size and area mammals. Range size for the largest (50% percentile) taxa from four mammal orders (Table 3). Although the relationship remained highly significant (Artiodactyla, Carnivora, Perissodactyla, and Proboscidea) plotted against body size as even into the future, the slope shifted slightly and the intercept in Brown and Maurer (1987). Rows represent time bins (historic, historic to modern, decreased as mammals were extirpated from islands. While the modern, and future projections), while columns represent trophic guilds. Triangles in largest Cetacean is endangered (e.g., the blue whale, Balaenoptera panels A and B represent the triangular envelope for the historic range of the entire large mammal community. Panels C and D show the transformation of range size from musculus), other large whales are currently considered of Least historic (squares) to modern (circles) time bins, while arrows represent the direction of Concern by the IUCN (e.g., the bowhead whale, Balaena mysticetus). change. In panels E and F, light gray triangles represent modern range envelopes for Thus, the upper end of the relationship did not change appreciably large mammals and overlay the dark gray triangles that represent the historic range. going into the Future interval. Nor does the regression change Panels G and H show historic, modern, and future range triangular envelopes, note that the major axis of change is the bottom right leg of the triangle. substantially when marine mammals were eliminated altogether (Table 3). However, the y-intercept decreased by ~50% from the Pleistocene into the Future (Table 3), translating to slightly more contractions from the historic to modern (Fig. 11). Moreover, ex- than an order of magnitude decrease in the size of the largest amination of the terminal Pleistocene to modern demonstrated mammal supported by a given land area. For example, the largest that smaller mammals displayed greater variation in range size mammal on the Greek island of Rhodes (1410 km2) during the shifts than did other mammals (Lyons et al., 2010). Pleistocene was predicted to be ~10.8 kg; in the future, the largest mammal would ~0.8 kg. 3.2.2. Area, species richness and body mass As with other macroecological patterns affected by body size As has been reported elsewhere, there is a highly significant downgrading, these results suggest that relationships characterized relationship between the size of the largest mammal species and using only modern data should be interpreted with caution and the size of the land or ocean basin where it is found (Marquet and reevaluated after the inclusion of fossil data. More importantly, Taper, 1998; Burness et al., 2001; Smith et al., 2010b; Smith and continued body size downgrading is likely to have cascading effects Boyer, 2012). This is not a statistical artifact of larger areas having on island ecosystems. Mammals on islands provide a prey base for more species and thus increasing the probability of the evolution of other species including other mammals, reptiles, and birds. Carni- fl larger animals (Marquet and Taper, 1998). Rather, it likely results vores in particular, are strongly in uenced by extinctions. More- from the positive scaling of resource availability and diversity with over, the size of carnivores is correlated with the size of their prey area, which provides more energy to maintain viable populations of (Raia and Meiri, 2006; Forsman, 1991; Goltsmann et al., 2005; large, low density, mammals (Marquet and Taper, 1998; Burness Jessop et al., 2006). Such patterns have been documented for rep- et al., 2001; McNab, 2010). tiles and mammals (Forsman, 199; Raia and Meiri, 2006). As the size

Table 2 ‘Constraint lines’ characterizing the upper limit of mammal body mass and geographic range.

Time Bin Aspect of Geographic Range Slope Intercept (þ/ stdev) r2adj p-value

Historic Maximum 0.24 12.1 0.11 0.04 Modern Maximum 0.36 8.8 0.037 0.16 Historic Upper quartile 0.19 14.8 e 0.04 Modern Upper quartile 0.14 17.5 e 0.5

‘Maximum’ represents an OLS regression conducted through the largest geographic range in each 0.25 log unit across the 8 orders of magnitude span of mammal body size; Upper quartile regression used tau ¼ 0.9; significant values indicated in bold. df ¼ 168 in all cases. 12 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16

Table 3 The relationship between the maximum size of mammals and area.

Interval Age With whales Without whales

N Slope Intercept p-value R2 N Slope Intercept p-value R2

Pleistocene Before 10 ka 92 0.77 1.59 <0.001 0.51 90 0.77 1.57 <0.001 0.47 Holocene 10e0 92 0.70 1.39 <0.001 0.56 90 0.68 1.47 <0.001 0.51 Modern 78 0.70 1.24 <0.001 0.56 76 0.66 1.34 <0.001 0.49 Future þ200 yrs 60 0.61 1.26 <0.001 0.54 58 0.54 1.50 <0.001 0.45

OLS regressions were conducted on log island area (km2) and log body mass (g). Regressions were done with and without whales.

of prey decrease, the size and growth rate of carnivores dependent colleges. Until recently, the fossil record was not typically incor- on them will be influenced, perhaps leading to restructuring of the porated into ecological work. Yet, what is ‘past is prologue” carnivore guild (Goltsmann et al., 2005). Such changes have im- (Shakespeare, The Tempest, Act 2, Scene 1). Thus, incorporating plications for the structure and energy flow through island eco- studies of past extinction events can help bring about a synoptic systems. Predicting just how ecosystem structure and function will understanding of what the decline and ultimate extinction of large- change is complicated by other human impacts, including habitat bodied animals may mean in terms of lost ecosystem function (e.g., alteration and human population density on islands. Malhi et al., 2016; Smith et al., 2016a,b). This is now a vibrant area of Our analysis highlights the widespread extinctions on islands. research (e.g., Zimov et al., 1995; Johnson, 2009; Doughty et al., Although 78% of the landmasses still contain mammals, most lost 2010; Smith et al., 2010a, 2015, 2016a,b, 2018; Werdelin and their largest species. These losses were widespread across islands of Lewis, 2013; Gill, 2014; Bakker et al., 2016; Pardi and Smith, all sizes and were not a result of differential losses of large species 2016; Doughty et al., 2016a, b; Van Valkenburgh et al., 2016; on small islands. Moreover, 21% of the areas lost all of their native Lyons et al., 2016a; Galetti et al., 2017; Pires et al., 2017; Bibi et al., mammals entirely. In the future, ~40% of the islands we examined 2017). will contain no native mammals. Island faunas of the future are Here, we have explored a few of the large-scale patterns relating likely to be very different as a result of the combined effects of mammal body mass to diversity, energy use and community extirpation and body size downgrading. composition. We demonstrate that these macroecological patterns have been altered in fundamental ways with the increased density and expansion of humans over the late Quaternary, and subsequent 4. Conclusion and outlook loss of megafauna. However, there were likely many other emer- gent properties of ecosystems impacted that we do not discuss. The loss of large-bodied mammals over the late Quaternary was Certainly, late Quaternary and future extinctions led, and will severe, unique in Earth history, and occurred in a temporally and continue to lead, to the reorganization of ecological communities spatially transgressive manner. Moreover, body size downgrading and shifts in the foraging niches of surviving species (e.g., Gill et al., was significantly related to increased human population density 2009; Estes et al., 2011; Dirzo et al., 2014; Gill, 2014; Keesing and (e.g., Fig. 6) and not to changing climate (Fig. 9). As humans have Young, 2014; Bakker et al., 2016; Smith et al., 2016b). But, the migrated across Earth, from continent to continent, and from impact has been almost certainly much more widespread (Myers continents to islands, extinctions of large-bodied mammals have and Knoll, 2001). For example, the transition from the vast followed. Whether by default or design, humans have manipulated ‘mammoth steppe’ of the Pleistocene to the more waterlogged the environment since they became a dominant species on the habitats of the Holocene is at least partially owing to the absence of planet (e.g., Decker et al., 2000; Purvis et al., 2000; Balmford et al., grazing and other activities by large-bodied mammals such as 2004; Lyons et al., 2004; Donlan et al., 2005, 2006; Dirzo et al., mammoth (Zimov et al., 1995; Johnson, 2009). Contemporary 2014; Young et al., 2016; Ceballos et al., 2015; Ripple et al., 2015, studies demonstrate an important role of elephants in maintaining 2016, 2017). While the pace of extinctions has increased over time grasslands and inhibiting woodland regeneration (Owen-Smith, (Fig. 2), the size selectivity has decreased (Figs. 5 and 7), presum- 1989; Cumming et al., 1997; Whyte et al., 2003; Pringle, 2008; ably owing to a change in the nature of the threats. Keesing and Young, 2014; Asner et al., 2016; Bakker et al., 2016); While considerable work has focused on the causes of some of because modern elephants are generally smaller than their Pleis- these extinctions, particularly those at the terminal Pleistocene, tocene congeners, this suggests extinct megaherbivores played an what has been largely overlooked until fairly recently were the even more substantial role. Similarly, extant equids play a signifi- consequences of the loss of millions of large-bodied mammals on cant role in the dispersal of large-seeded plants (Western and ecological landscapes (Smith et al., 2016b). Interestingly, it is only Maitumo, 2004), and presumably did so in the past. The cascade recently that we have begun appreciating the extent to which even of effects probably also influenced the distribution of smaller near-time human activities have altered fundamental macro- mammals (Pardi and Smith, 2016; Smith et al., 2015; Van ecological patterns (Smith and Boyer, 2012). For example, the Valkenburgh et al., 2016). And, the absence of large herbivores original studies on BSD were based on extant ecosystems and hence likely altered biogeochemical cycling of nutrients such as carbon, did not include historical and/or prehistorical extinctions (e.g., sodium and nitrogen (Schmitz et al., 2014; Doughty et al., 2016a, b), Hutchinson and MacArthur, 1959; Brown and Maurer, 1987; Brown, as well as methane, an important greenhouse gas with global 1995). To a large extent, this exclusive use of modern data reflected climate implications (Smith et al., 2010a, 2016a). In the absence of the considerable difficulty of compiling large datasets in the pre/ heavy grazing, water tables may have risen, leading to a slowdown early internet days and a lack of computing power (Smith et al., in the rate of nutrient breakdown and recycling, an increase in 2008). Indeed, the first global database of mammals (e.g., MOM organic matter accumulation and a decrease in soil fertility. Vege- v1.0; Smith et al., 2003), which was constructed solely from the tative shifts influenced the albedo of the landscape changing heat literature, was not released until 2003. But, it also reflected a lack of absorption and reflectivity (Doughty et al., 2010). Many other po- communication between biologists and paleontologists, who were tential unpredictable ‘emergent novelties’ may arise owing to the traditionally housed in separate departments and sometimes even F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 13 absence of megafauna, including changes in the transmission and/ References or frequency of disease, ecosystem homogenization, biodisparity impoverishment, and even changes in the evolutionary process Aiello, L.C., Wells, J.C., 2002. Energetics and the evolution of the genus Homo. Annu. Rev. Anthropol. 31, 323e338. itself (Myers and Knoll, 2001). Aiello, L.C., Wheeler, P., 1995. The expensive-tissue hypothesis: the brain and the Our interest in characterizing fundamental macroecological digestive system in human and primate evolution. Curr. Anthropol. 36, patterns goes beyond an exercise in demonstrating how they have 199e221. Alroy, J., 2001. A multispecies overkill simulation of the end-Pleistocene megafauna been altered by human activities over the late Quaternary. Modern mass extinction. Science 292, 1893e1896. ecological science informs conservation and management de- Alroy, J., 1999. Putting North America's end-Pleistocene megafaunal extinction in cisions (Kingsland, 2002). Conservation biologists are especially context: large-scale analyses of spatial patterns, extinction rates, and size dis- concerned with maintaining large-bodied species, characterizing tribution. In: MacPhee, R. (Ed.), Extinctions in Near Time: Causes, Contexts and Consequences. Kluwer Academic, New York, pp. 105e143. their role in communities, and developing an understanding of how Alroy, J., 2000. New methods for quantifying macroevolutionary patterns and their loss may ‘unravel’ contemporary ecosystems. Coherent man- processes. Paleobiology 26, 707e733. agement decisions often employ quantitative data extracted from Anderson, S., 1977. Geographic ranges of North American terrestrial mammals. Am. Mus. Novit. 2629, 1e15. fundamental macroecological patterns. For example, the size of a Andrews, P., Martin, L., 1991. Hominoid dietary evolution. Phil. Trans. Roy. Soc. Lond. wildlife reserve might be determined based on consideration of the B 334, 199e209. body size-range size relationship of a target species. As we have Anton, S.C., Potts, R., Aiello, L., 2014. Evolution of early Homo: an integrated bio- logical perspective. Science 345, 1236828. shown, if this is done with modern data without regard to the Anton, S.C., 2003. Natural history of Homo erectus. Yearbk. Phys. Anthropol. 46, prehistorical pattern, a distorted picture may emerge. Indeed, 126e170. modern or future geographic ranges of mammals based on Asner, G.P., et al., 2016. Ecosystem-scale effects of megafauna in African savannas. Ecography 39, 240e252. contemporary patterns actually may not be large enough to sustain Bakker, E.S., et al., 2016. Combining paleo-data and modern exclosure experiments viable populations (Ceballos and Ehrlich, 2002). Thus, an appreci- to assess the impact of megafauna extinctions on woody vegetation. Proc. Natl. ation of deeper ecological history becomes increasingly imperative Acad. Sci. U.S.A. 113, 847e855. Balmford, A., et al., 2004. The worldwide costs of marine protected areas. Proc. Natl. for conservation efforts. Acad. Sci. U.S.A. 101, 9694e9697. The influence of humans on Earth ecosystems and biogeo- Barnosky, A.D., 2008. Megafauna biomass tradeoff as a driver of Quaternary and chemical processes has increased over time as our species has future extinctions. Proc. Natl. Acad. Sci. U.S.A. 105, 11543e11548. become more abundant, more widespread, and more technologi- Barnosky, A.D., et al., 2011. Has the Earth's sixth mass extinction already arrived? Nature 471, 51e57. cally sophisticated. The advent of agriculture and the domestication Barnosky, A.D., et al., 2012. Approaching a state shift in Earth's biosphere. Nature of plants and animals transformed the landscape (Smith and Zeder, 486, 52e58. 2013); today, more than 55% of the Earth's surface is urbanized Barnosky, A.D., et al., 2004. Assessing the causes of late Pleistocene extinctions on the continents. Science 306, 70e75. (Ellis et al., 2010). Moreover, there has been a fundamental shift Berna, F., et al., 2012. Microstratigraphic evidence of in situ fire in the Acheulean over the late Quaternary from a world of wild mammals to one strata of Wonderwerk cave, northern Cape province, South Africa. Proc. Natl. e dominated by humans and our domesticated livestock (Barnosky, Acad. Sci. U.S.A. 109, E1215 E1220. Bibi, F., et al., 2017. Paleoecology of the Serengeti during the Oldowan-Acheulean 2008; Smith et al., 2016a,b); today wildlife make up less than 10% transition at Olduvai Gorge, Tanzania: the mammal and fish evidence. J. Hum. of terrestrial mammal biomass (Smith et al., 2016b). Largely owing Evol. 120, 48e75. to ongoing human activities (Vitousek et al., 1997; Estes et al., 2011; Blumenschine, R.J., Pobiner, B.L., 2006. Zooarchaeology and the ecology of Oldowan hominin carnivory. In: Ungar, P. (Ed.), Early Hominin Diets: the Known, the Dirzo et al., 2014), the remaining species of large-bodied mammals Unknown, and the Unknowable. Oxford University Press, Oxford, pp. 167e190. on Earth are either vulnerable or endangered (http://www. Blumenschine, R.J., 1995. Percussion marks, tooth marks, and experimental de- iucnredlist.org). Here, we show that body size and trophic down- terminations of the timing of hominid and carnivore access to long bones at FLK Zinjanthropus, Olduvai Gorge, Tanzania. J. Hum. Evol. 29, 21e51. grading has been ongoing since at least the late Pleistocene, and Bocherens, H., Billiou, D., Mariotti, A., 2001. New isotopic evidence for dietary habits moreover, that the loss of large-bodied mammals has already had of Neanderthals from Belgium. J. Hum. Evol. 40, 497e505. many consequences on ecosystems. Future extinctions, if not hal- Boivin, N.L., et al., 2016. Ecological consequences of human niche construction: ted, will likely lead to any number of unanticipated effects (Estes examining long-term anthropogenic shaping of global species distributions. Proc. Natl. Acad. Sci. U.S.A. 113, 6388e6396. et al., 2011; Dirzo et al., 2014). Our analysis and review suggest Bowler, J.M., et al., 2003. New ages for human occupation and climatic change at that human activities measurably influenced global macro- Lake Mungo, Australia. Nature 421, 837. ecological patterns, biogeochemical processes and even potentially Braje, T.J., Erlandson, J.M., 2013. Human acceleration of animal and plant extinc- tions: a Late Pleistocene, Holocene, and Anthropocene continuum. Anthro- climate long before the development of agriculture, complex civi- pocene 4, 14e23. lizations and the industrial age. Indeed, the start of the Anthro- Braun, D.R., et al., 2010. Early hominin diet included diverse terrestrial and aquatic pocene arguably began with the evolution of our genus, Homo. animals 1.95 Ma in East Turkana, Kenya. Proc. Natl. Acad. Sci. U.S.A. 107, 10002e10007. Breeze, P.S., et al., 2016. Palaeohydrological corridors for hominin dispersals in the e e Acknowledgements Middle East similar to 250 70,000 years ago. Quat. Sci. Rev. 144, 155 185. Brown, J.H., Maurer, B.A., 1987. Evolution of species assemblages: effects of ener- getic constraints and species dynamics on the diversification of the North We thank P. Wagner with assistance in computing mammalian American avifauna. Am. Nat. 130, 1e17. turnover rates over the Cenozoic. Funding was provided by NSF Brown, J.H., 1995. Macroecology. University of Chicago Press, Chicago, Illinois. Brown, J.H., Maurer, B.A., 1989. Macroecology: the division of food and space among DEB-1555525 (F.A. Smith, PI). species on continents. Science 243, 1145e1150. Brown, J.H., Nicoletto, P.F., 1991. Spatial scaling of species composition: body masses of North American land mammals. Am. Nat. 138, 1478e1512. Appendix A. Supplementary data Brown, J.H., Lomolino, M.V., 1998. Biogeography, second ed. Sinauer Associates, Sunderland, Mass. Supplementary data related to this article can be found at: Brown, K.S., et al., 2012. An early and enduring advanced technology originating 71,000 years ago in South Africa. Nature 491, 590e593. http://biology.unm.edu/fasmith/Datasets/and www.sciencemag. Bunn, H.T., et al., 1986. Systematic butchery by plio-pleistocene hominids at Olduvai org/content/360/6386/310/suppl/DC1. Gorge, Tanzania. Curr. Anthropol. 27, 431e452. Bunn, H.T., 2007. Meat made us human. In: Ungar, P. (Ed.), Early Hominin Diets: the Known, the Unknown, and the Unknowable. Oxford University Press, Oxford, Declarations of interest pp. 191e211. Burger, J.R., et al., 2012. The macroecology of sustainability. PLoS Biol. 10 e1001345. Burness, G.P., Diamond, J., Flannery, T., 2001. Dinosaurs, dragons, and dwarfs. The None. 14 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16

evolution of maximal body size. Proc. Natl. Acad. Sci. U.S.A. 98, 14518e14523. Fritz, S.A., Bininda-Emonds, O.R.P., Purvis, A., 2009. Geographical variation in pre- Burney, D.A., Flannery, T.F., 2005. Fifty millennia of catastrophic extinctions after dictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. human contact. Trends Ecol. Evol. 20, 395e401. Lett. 12, 538e549. Burnside, W.R., et al., 2012. Human macroecology: linking pattern and process in Galetti, M., et al., 2017. Ecological and evolutionary legacy of megafauna extinctions. big-picture human ecology. Biol. Rev. 87, 194e208. Biol. Rev. 93, 845e862. Cardillo, M., 2003. Biological determinants of extinction risk: why are smaller Gaston, K.J., Blackburn, T.M., 1996. Range size body size relationships: evidence of species less vulnerable? Anim. Conserv. 6, 63e69. scale dependence. Oikos 75, 479e485. Cardillo, M., Huxtable, J.S., Bromham, L., 2003. Geographic range size, life history Gaston, K.J., 2003. The Structure and Dynamics of Geographic Ranges. Oxford and rates of diversification in Australian mammals. J. Evol. Biol. 16, 282e288. University Press, Oxford. Cardillo, M., et al., 2005. Multiple causes of high extinction risk in large mammal Gaston, K.J., Blackburn, T.M., 2000. Pattern and Process in Macroecology. Blackwell species. Science 309, 1239e1241. Science, Oxford. Cardillo, M., et al., 2008. The predictability of extinction: biological and external Gill, J.L., 2014. Ecological impacts of the late Quaternary megaherbivore extinctions. correlates of decline in mammals. In: Proceedings of the Royal Society B, vol New Phytol. 201, 1163e1169. 275, pp. 1441e1448. Gill, J.L., et al., 2009. Pleistocene megafaunal collapse, novel plant communities, and Carto, S.L., et al., 2009. Out of Africa and into an ice age: on the role of global climate enhanced fire regimes in North America. Science 326, 1100e1103. change in the late Pleistocene migration of early modern humans out of Africa. Goebel, T., et al., 2008. The late Pleistocene dispersal of modern humans. Science J. Hum. Evol. 56, 139e151. 319, 1497e1502. Ceballos, G., Ehrlich, P.R., 2002. Mammal population losses and the extinction crisis. Goltsmann, M., et al., 2005. “Island syndrome” in a population of Arctic Science 296, 904e907. (Alopex lagopus) from Mednyi island. J. Zool. 267, 405e481. Ceballos, G., et al., 2015. Accelerated modern humaneinduced species losses: Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in entering the sixth mass extinction. Sci. Adv. 1, 1400251e1400255 e1400253. the measurement and comparison of species richness. Ecol. Lett. 3, 379e391. Ceballos, G., Ehrlich, P.R., Dirzo, R., 2017. Population losses and the sixth mass Gowlett, J.A., 2016. The discovery of fire by humans: a long and convoluted process. extinction. Proc. Natl. Acad. Sci. U.S.A. 114, E6089eE6096. Phil. Trans. Roy. Soc. Lond. B 371, 20150164. Clavel, J., Julliard, R., Devictor, V., 2011. Worldwide decline of specialist species: Graham, R.W., Grimm, E.C., 1990. Effects of global climate change on the patterns of toward a global functional homogenization? Front. Ecol. Environ. 9, 222e228. terrestrial biological communities. Trends Ecol. Evol. 5, 289e292. Crooks, K.R., et al., 2017. Quantification of habitat fragmentation reveals extinction Graham, R.W., Lundelius, E.L., 1984. Coevolutionary disequilibrium and Pleistocene risk in terrestrial mammals. Proc. Natl. Acad. Sci. U.S.A. 114, 7635e7640. extinctions. In: Martin, P.S., Klein, R.G. (Eds.), Quaternary Extinctions: a Pre- Cumming, D.H., et al., 1997. Elephants, woodlands and biodiversity in southern historic Revolution. University of Arizona Press, Tucson, pp. 223e249. Africa. South Afr. J. Sci. 93, 231e236. Grayson, D.K., 2007. Deciphering north American pleistocene extinctions. Damuth, J.D., 1981. Population density and body size in mammals. Nature 290, J. Anthropol. Res. 63, 185e213. 699e700. Groucutt, H.S., et al., 2015. Rethinking the dispersal of Homo sapiens out of Africa. Damuth, J.D., 1987. Interspecific allometry of population density in mammals and Evol. Anthropol. Issues News Rev. 24, 149e164. other animals: the independence of body mass and population energy-use. Biol. Guilday, J., 1967. Differential extinction during late-Pleistocene and Recent times. In: J. Linn. Soc. 31, 193e246. Martin, P.S., Wright Jr., H.E. (Eds.), Pleistocene Extinctions: the Search for a Damuth, J.D., 1991. Of size and abundance. Nature 351, 268e269. Cause. Yale University Press, New Haven, pp. 121e140. Darwin, C., 1859. The Origin of Species. John Murray, London, UK. Guthrie, R.D., 1990. Frozen Fauna of the Mammoth Steppe: the Story of Blue Babe. Davidson, A.D., et al., 2009. Multiple ecological pathways to extinction in mammals. University of Chicago Press, Chicago. Proc. Natl. Acad. Sci. U.S.A. 106, 10702e10705. Haynes, G., 2009. American Megafaunal Extinctions at the End of the Pleistocene. Decker, E.H., et al., 2000. Energy and material flow through the urban ecosystem. Springer, Dordrecht, Netherlands. Annu. Rev. Energy Environ. 25, 685e740. Hern, W.M., 1999. How many times has the human population doubled? Compar- Dial, K.P., Marzluff, J.M., 1988. Are the smallest organisms the most diverse? Ecology isons with Cancer. Popul. Environ. 21, 59e80. 69, 1620e1624. Hilu, K., 2007. Skewed distribution of species number in grass genera: is it a Dirzo, R., et al., 2014. Defaunation in the Anthropocene. Science 345, 401e406. taxonomic artifact? In: Hodkinson, T.R., Parnell, J.A.N. (Eds.), Reconstructing the Dixon, E.J., 1999. Bones, Boats and bison: Archeology and the First Colonization of Tree of Life: Taxonomy and Systematics of Large and Species Rich Taxa. CRC Western North America. University of New Mexico Press, Albuquerque. Press, Boca Raton, pp. 165e176. Domínguez-Rodrigo, M., Barba, R., Egeland, C.P. (Eds.), 2007. Deconstructing Old- Hoffmann, M., et al., 2010. The impact of conservation on the status of the world's uvai: A Taphonomic Study of the Bed I Sites. Springer, Netherlands. vertebrates. Science 330, 1503e1509. Domínguez-Rodrigo, M., 2002. Hunting and scavenging by early humans: the state Humboldt, A., Bonpland, A., Jackson, S.T., Romanowski, S., 2009. Reprint of Hum- of the debate. J. World PreHistory 16, 1e54. boldt's 1807.Essay on the Geography of Plants. Chicago University Press, Domínguez-Rodrigo, M., Barba, R., 2006. New estimates of tooth mark and per- Chicago. cussion mark frequencies at the FLK Zinj site: the carnivore-hominid-carnivore Hutchinson, G.E., MacArthur, R.J., 1959. A theoretical ecological model of size dis- hypothesis falsified. J. Hum. Evol. 50, 170e194. tributions among species of animals. Am. Nat. 93, 117e125. Donlan, C.J., et al., 2005. Rewilding north America. Nature 436, 913e914. Jarvinen,€ O., 1982. Species-to-genus ratios in biogeography: a historical note. Donlan, C.J., et al., 2006. Pleistocene Rewilding: an optimistic agenda for twenty- J. Biogeogr. 9, 363e370. first century conservation. Am. Nat. 168, 660e681. Jennings, R.P., et al., 2015. The greening of Arabia: Multiple opportunities for human Doughty, C.E., Wolf, A., Field, C.B., 2010. Biophysical feedbacks between the Pleis- occupation of the Arabian Peninsula during the Late Pleistocene inferred from tocene megafauna extinction and climate: the first human-induced global an ensemble of climate model simulations. Quat. Int. 382, 181e199. warming? Geophys. Res. Lett. 37, 1e5. Jessop, T.S., et al., 2006. Maximum body size among insular Komodo dragon pop- Doughty, C.E., et al., 2016a. Global nutrient transport in a world of giants. Proc. Natl. ulations covaries with large prey density. Oikos 112, 422e429. Acad. Sci. U.S.A. 113, 868e873. Johnson, C.N., 2009. Ecological consequences of Late Quaternary extinctions of Doughty, C.E., et al., 2016b. Interdependency of plants and animals in controlling megafauna. Proc. Roy. Soc. Lond. B 276, 2509e2519. the sodium balance of ecosystems and the impacts of global defaunation. Joordens, J.C., et al., 2015. Homo erectus at Trinil on Java used shells for tool pro- Ecography 39, 204e212. duction and engraving. Nature 518, 228e231. Ellis, E.C., et al., 2010. Anthropogenic transformation of the biomes, 1700 to 2000. Keesing, F., Young, T.P., 2014. Cascading consequences of the loss of large mammals Glob. Ecol. Biogeogr. 19, 589e606. in an African Savanna. Bioscience 64, 487e495. Ernest, S.K.M., Brown, J.H., 2001. Homeostasis and compensation: the role of re- Kingsland, S., 2002. Designing nature reserves: adapting ecology to real-world sources in ecosystem stability. Ecology 82, 2118e2132. problems. Endeavour 26, 9e14. Estes, J.A., et al., 2011. Trophic downgrading of planet earth. Science 333, 301e306. Koch, P.L., Barnosky, A.D., 2006. Late Quaternary extinctions: state of the debate. Faurby, S., Svenning, J.C., 2015. Historic and prehistoric human-driven extinctions Annu. Rev. Ecol. Evol. Syst. 37, 215e250. have reshaped global mammal diversity patterns. Divers. Distrib. 21, 1155e1166. Krause, J., et al., 2010. The complete mitochondrial DNA genome of an unknown Fenchel, T., 1993. There are more small than large species? Oikos 68, 375e378. hominin from southern Siberia. Nature 464, 894e897. Fizet, M., et al., 1995. Effect of diet, physiology and climate on carbon and nitrogen Larrasoana,~ J.C., Roberts, A.P., Rohling, E.J., 2013. Dynamics of green Sahara periods isotopes of collagen in a late Pleistocene anthropic paleoecosystem. J. Archaeol. and their role in hominin evolution. PLoS One 8 e76514. 22, 67e79. Lessa, E.P., Farina, R.A., 1996. Reassessment of extinction patterns among the late Flannery, T.F., Schouten, P., 2001. A Gap in Nature: Discovering the World's Extinct Pleistocene mammals of South America. Palaeontology 39, 651e662. Animals. Atlantic Monthly Press, New York. Longman, E.K., Rosenblad, K., Sax, D.F., 2018. Extreme homogenization: the past, Foley, R.A., 2001. The evolutionary consequences of increased carnivory in homi- present and future of mammal assemblages on islands. Glob. Ecol. Biogeogr. 27, nids. In: Stanford, C.B., Bunn, H.T. (Eds.), Meat-eating and Human Evolution. 77e95. Oxford University Press, Oxford, pp. 305e331. Luca, F., Perry, G.H., Di Rienzo, A., 2010. Evolutionary adaptations to dietary changes. Foote, M., 2000. Origination and extinction components of taxonomic diversity: Annu. Rev. Nutr. 30, 291e314. general problems. Paleobiology 26, 74e102. Lundelius Jr., E.L., 1967. Late-Pleistocene and Holocene faunal history of central Foote, M., Raup, D.M., 1996. Fossil preservation and the stratigraphic ranges of taxa. Texas. In: Martin, P.S., Wright Jr., H.E. (Eds.), Pleistocene Extinctions: the Search Paleobiology 22, 121e140. https://doi.org/10.1017/S0094837300016134. for a Cause. Yale University Press, New Haven, pp. 288e319. Forsman, A., 1991. Variation in sexual size dimorphism and maximum body size Lyons, S.K., Smith, F.A., Brown, J.H., 2004. Of mice, mastodons, and men: human among adder populations: effects of prey size. J. Anim. Ecol. 60, 253e267. mediated extinctions on four continents. Evol. Ecol. Res. 6, 339e358. F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16 15

Lyons, S.K., Wagner, P.J., Dzikiewicz, K., 2010. Ecological correlates of range shifts of Foundation Statistical Company. Late Pleistocene mammals. Phil. Trans. Biol. Sci. 365, 3681e3693. R Studio Team, 2015. R Studio. Integrated Development for R. R Foundation Sta- Lyons, S.K., Smith, F.A., 2013. Macroecological patterns of body size in mammals tistical Company. across time and space. In: Smith, F.A., Lyons, S.K. (Eds.), Body Size: Linking Raia, P., Meiri, S., 2006. The island rule in large mammals: paleontology meets Pattern and Process across Space, Time and Taxonomy. University of Chicago ecology. Evolution 60, 1731e1742. Press, Chicago, pp. 114e142. Richards, M.P., et al., 2000. Neanderthal diet at Vindija and Neatherthal predation: Lyons, S.K., et al., 2016a. Holocene shifts in the assembly of plant and animal the evidence from stable isotopes. Proc. Natl. Acad. Sci. U.S.A. 97, 7663e7666. communities implicate human impacts. Nature 529, 80eU183. Rightmire, G.P., et al., 2017. Skull 5 from Dmanisi: descriptive anatomy, comparative Lyons, S.K., et al., 2016b. The changing role of mammal life histories in late Qua- studies, and evolutionary significance. J. Hum. Evol. 104, 50e79. ternary extinction vulnerability on continents and islands. Biol. Lett. 12, Ripple, W.J., Van Valkenburgh, B., 2010. Linking top-down forces to the Pleistocene 20160342. megafaunal extinctions. Bioscience 60, 516e526. MacArthur, R.H., Wilson, E.O., 1967. z Theory of Island Biogeography. Princeton Ripple, W.J., et al., 2014. Status and ecological effects of the world's largest carni- University Press, Princeton. vores. Science 343 (6167), 1241484. Malhi, Y., et al., 2016. Megafauna and ecosystem function from the pleistocene to Ripple, W.J., et al., 2015. Collapse of the world's largest herbivores. Sci. Adv. 1, the Anthropocene. Proc. Natl. Acad. Sci. U.S.A. 113, 838e846. 31400103. Marean, C.W., 2015. The most invasive species of all. Sci. Am. 313, 33e39. Ripple, W.J., et al., 2016. Saving the world's terrestrial megafauna. Bioscience 66, Marquet, P.A., Taper, M.L., 1998. On size and area: patterns of mammalian body size 807e812. extremes across landmasses. Evol. Ecol. 12, 127e139. Ripple, W.J., et al., 2017. Extinction risk is most acute for the world's largest and Martin, P.S., 1967. Prehistoric overkill. In: Martin, P.S., Wright Jr., H.E. (Eds.), Pleis- smallest vertebrates. Proc. Natl. Acad. Sci. Unit. States Am. 114, 10678e10683. tocene Extinctions: the Search for a Cause. Yale University Press, New Haven, Ritchie, E.G., Johnson, C.N., 2009. Predator interactions, mesopredator release and pp. 75e120. biodiversity conservation. Ecol. Lett. 12, 982e998. Martin, P.S., 1984. Prehistoric overkill: the global model. In: Martin, P.S., Klein, R.G. Roberts, R.G., et al., 2001. New ages for the last Australian megafauna: continent- (Eds.), Quaternary Extinctions: A Prehistoric Revolution. University of Arizona wide extinction about 46,000 years ago. Science 292, 1888e1892. Press, Tucson, pp. 354e403. Roebroeks, W., Villa, P., 2011. On the earliest evidence for habitual use of fire in Martin, P.S., 2005. Twilight of the Mammoths: Ice Age Extinctions and Rewilding Europe. Proc. Natl. Acad. Sci. U.S.A. 108, 5209e5214. America. University of California Press, Berkley. Roy, K., Jablonski, D., Valentine, J.W., 1996. Higher taxa in biodiversity studies: Martin, P.S., Steadman, D.W., 1999. Prehistoric extinctions on islands and conti- patterns from eastern Pacific marine molluscs. Phil. Trans. Biol. Sci. 351, nents. In: MacPhee, R.D.E. (Ed.), Extinctions in Near Time: Causes, Contexts, and 1605e1613. Consequences. Kluwer Academic/Plenum Press, New York, pp. 17e55. Rundle, S.D., Bilton, D.T., Abbott, J.C., Foggo, A., 2007. Range size in North American Maurer, B.A., Brown, J.H., 1988. Distribution of energy use and biomass among Enallagma damselflies correlates with wing size. Freshw. Biol. 52, 471e477. species of North American terrestrial birds. Ecology 69, 1923e1932. Sandom, C., et al., 2014. Global late Quaternary megafauna extinctions linked to Maurer, B.A., 1999. Untangling Ecological Complexity: the Macroscopic Perspective. humans, not climate change. Proc. Roy. Soc. Lond. B 281, 20133254. University of Chicago Press, Chicago. Schipper, J., et al., 2008. The status of the world's land and marine mammals: di- Maurer, B.A., 2013. Geographic variation in body size distributions of continental versity, threat, and knowledge. Science 322, 225e230. avifauna. In: Smith, F.A., Lyons, S.K. (Eds.), Body Size: Linking Pattern and Schmitz, O.J., et al., 2014. Animating the carbon cycle. Ecosystems 17, 344e359. Process across Space, Time and Taxonomy. University of Chicago Press, Chicago, Shea, J.J., 2017. Occasional, obligatory, and habitual stone tool use in hominin pp. 83e94. evolution. Evol. Anthropol. Issues News Rev. 26, 200e217. McHenry, H.M., 1992. Body size and proportions in early hominids. Am. J. Phys. Simberloff, D., 1970. Taxonomic diversity of island biotas. Evolution 24, 23e47. Anthropol. 87, 407e431. Smith, B.D., Zeder, M.A., 2013. The onset of the Anthropocene. Anthropocene 4, McNab, B.K., 2010. Geographic and temporal correlations of mammalian size 8e13. reconsidered: a resource rule. Oecologica 164, 13e23. Smith, F.A., Boyer, A.G., 2012. Losing time? Incorporating a deeper temporal Meltzer, D.J., 2015. Pleistocene overkill and North American mammal extinctions. perspective into modern ecology. Front. Biogeogr. 4, 27e39. Annu. Rev. Anthropol. 44, 33e53. Smith, F.A., Betancourt, J.L., 2003. The effect of late Holocene temperature fluctu- Miller, G.H., et al., 2005. Ecosystem collapse in Pleistocene Australia and a human ations on the evolution and ecology of woodrats (Neotoma) in Idaho and role in megafaunal extinction. Science 309, 287e290. northwestern Utah. Quat. Res. 59, 160e171. Milton, K., 1999. A hypothesis to explain the role of meat-eating in human evolu- Smith, F.A., Betancourt, J.L., Brown, J.H., 1995. Evolution of woodrat body size tracks tion. Evol. Anthropol. 8, 11e21. 20,000 years of climate change. Science 270, 2012e2014. Morrison, J.C., et al., 2007. Persistence of large mammal faunas as indicators of Smith, F.A., Browning, H., Shepherd, U.L., 1998. The influence of climatic change on global human impacts. J. Mammal. 88, 1363e1380. the body mass of woodrats (Neotoma albigula) in an arid region of New Mexico, Moses, M.E., Brown, J.H., 2003. Allometry of human fertility and energy use. Ecol. USA. Ecography 21, 140e148. Lett. 6, 295e300. Smith, F.A., Elliott, S.M., Lyons, S.K., 2010a. Methane emissions from extinct Murray, P., 1991. The Pleistocene megafauna of Australia. In: Vickers-Rich, P., megafauna. Nat. Geosci. 3, 374e375. Mongahan, J.M., Baird, R.F., Rich, T.H. (Eds.), Vertebrate Palaeontology of Aus- Smith, F.A., Lyons, S.K., 2011. How big should a mammal be? A macroecological look tralasia. Pioneer Design Studio, Melbourne, pp. 1070e1164. at mammalian body size over space and time. Proc. R. Soc. Ser. B 366, Muttoni, G., Scardia, G., Kent, D.V., 2018. Early hominins in Europe: the Galerian 2364e2378. migration hypothesis. Quat. Sci. Rev. 180, 1e29. Smith, F.A., et al., 2003. Body mass of late Quaternary mammals. Ecology 84, 3402. Myers, N., Knoll, A.H., 2001. The biotic crisis and the future of evolution. Proc. Natl. Smith, F.A., et al., 2004. Similarity of mammalian body size across the taxonomic Acad. Sci. U.S.A. 98, 5389e5392. hierarchy and across space and time. Am. Nat. 163, 672e691. O'Connell, J., Allen, J., 2004. Dating the colonization of Sahul (Pleistocene Australia- Smith, F.A., et al., 2008. Macroecology: more than the division of food and space New Guinea): A review of recent research. J. Archaeol. Sci. 31 (6), 835e853. among species on continents. Prog. Phys. Geogr. 32, 115e138. Olden, J.D., et al., 2004. Ecological and evolutionary consequences of biotic ho- Smith, F.A., et al., 2010b. The evolution of maximum body size of terrestrial mogenization. Trends Ecol. Evol. 19, 18e24. mammals. Science 330, 1216e1219. Oppenheimer, S., 2012. Out-of-Africa, the peopling of continents and islands: Smith, F.A., et al., 2015. Unraveling the consequences of the terminal Pleistocene tracing uniparental gene trees across the map. Phil. Trans. Biol. Sci. 367, megafauna extinction on mammal community assembly. Ecography 39, 770e784. 223e239. Owen-Smith, N., 1989. Megafaunal extinctions: the conservation message from Smith, F.A., et al., 2016a. Exploring the influence of ancient and historic mega- 11,000 years B.P. Conserv. Biol. 3, 405e412. herbivore extirpations on the global methane budget. Proc. Natl. Acad. Sci. Pante, M.C., et al., 2017. The carnivorous feeding behavior of early Homo at HWK EE, U.S.A. 113, 874e879. Bed II, Olduvai Gorge, Tanzania. J. Hum. Evol. 120, 215e235. Smith, F.A., et al., 2016b. Megafauna in the earth system. Ecography 39, 99e108. Pardi, M.I., Smith, F.A., 2016. Biotic responses of canids to the terminal Pleistocene Smith, F.A., et al., 2018. Body size downgrading of mammals over the late Quater- megafauna extinction. Ecography 39, 141e151. nary. Science 360, 310e313. Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change Sponheimer, et al., 2013. Isotopic evidence of early hominin diets. Proc. Natl. Acad. impacts across natural systems. Nature 421, 37e42. Sci. U.S.A. 110, 10513e10518. Parton, A., et al., 2015. Orbital-scale climate variability in Arabia as a potential motor Sponheimer, M.J., Lee-Thorp, de Ruiter, D., 2007. Icarus, isotopes and australopith for human dispersals. Quat. Int. 382, 82e97. diets. In: Ungar, P.S. (Ed.), Evolution of the Human Diet: the Known, the Un- Pimm, S.L., et al., 2014. The biodiversity of species and their rates of extinction, known and the Unknowable. Oxford University Press, Oxford, pp. 132e149. distribution, and protection. Science 344, 1246752. Stiner, M., 2002. Carnivory, coevolution, and the geographic spread of the genus Pires, M.M., et al., 2017. Pleistocene megafaunal extinctions and the functional loss Homo. J. Archaeol. Res. 10, 1e63. of long-distance seed-dispersal services. Ecography 41, 153e163. Stringer, C., 2000. Paleoanthropology: coasting out of Africa. Nature 405, 24e27. Pringle, R.M., 2008. Elephants as agents of habitat creation for small vertebrates at Stringer, C., Andrews, P., 1988. Genetic and fossil evidence for the origins of modern the patch scale. Ecology 89, 26e33. humans. Science 239, 1263e1268. Prugh, L.R., et al., 2009. The rise of the mesopredator. Bioscience 59, 779e791. Stuart, A.J., 1999. Late Pleistocene megafaunal extinctions: a European perspective. Purvis, A., et al., 2000. Nonrandom extinction and the loss of evolutionary history. In: MacPhee, R.D.E. (Ed.), Extinctions in Near Time: Causes, Contexts, and Science 288, 328e330. Consequences. Kluwer Academic/Plenum, New York, pp. 257e270. R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Surovell, T.A., et al., 2016. Test of Martin's overkill hypothesis using radiocarbon 16 F.A. Smith et al. / Quaternary Science Reviews 211 (2019) 1e16

dates on extinct megafauna. Proc. Natl. Acad. Sci. U.S.A. 113, 886e891. 20-year experiment. Afr. J. Ecol. 42, 111e121. Surovell, T.A., Waguespack, N.M., 2009. Human prey choice in the late Pleistocene Whitley, D.S., 2009. Cave Paintings and the Human Spirit: the Origin of Creativity and its relation to megafaunal extinctions. In: Haynes, G. (Ed.), American and Belief. Prometheus, Amherst. Megafaunal Extinctions at the End of the Pleistocene. Springer-Verlag, New Whyte, I.J., et al., 2003. Kruger's elephant population: its size and consequences for York, pp. 77e105. ecosystem heterogeneity. In: Du Toit, J.T., Rogers, K.H., Biggs, H.C. (Eds.), The Thomas, C.D., et al., 2004. Extinction risk from climate change. Nature 427, 145e148. Kruger Experience: Ecology and Management of Savanna Heterogeneity. Island Tierney, J.E., Zander, P.D., 2017. A climatic context for the out-of-Africa migration. Press, Washington, D.C, pp. 332e348. Geology 45, 1023e1026. Wilkins, J., et al., 2012. Evidence for early hafted hunting technology. Science 338, Timmermann, A., Friedrich, T., 2016. Late Pleistocene climate drivers of early human 942e946. migration. Nature 538, 92e95. Williams, P.H., Gaston, K.J., 1994. Measuring more of biodiversity: can higher-taxon Tomiya, S., 2013. Body size and extinction risk in terrestrial mammals above the richness predict wholesale species richness? Biol. Conserv. 67, 211e217. species level. Am. Nat. 182, 196eE214. Willis, J.C., Yule, G.U., 1922. Some statistics of evolution and geographical distri- Tucker, M.A., et al., 2018. Moving in the Anthropocene: global reductions in bution in plants and animals, and their significance. Nature 109, 177e179. terrestrial mammalian movements. Science 359, 466e469. Wilson, D.E., Reeder, D.M., 2003. Mammal Species of the World. A Taxonomic and Turvey, S.T., 2009. Holocene Extinctions. Oxford University Press, Oxford. Geographic Reference. John Hopkins University Press, Baltimore. Turvey, S.T., Fritz, S.A., 2011. The ghosts of mammals past: biological and Wrangham, R.W., et al., 1999. The raw and the stolend cooking and the ecology of geographical patterns of global mammalian extinction across the Holocene. human origins. Curr. Anthropol. 40, 567e594. Phil. Trans. Biol. Sci. 366, 2564. Wrangham, R.W., 2009. Catching Fire: How Cooking Made Us Human. Basic Books, Van Valen, L., 1973. A new evolutionary law. Evol. Theory 1, 1e30. New York. Van Valkenburgh, B., et al., 2016. The impact of large terrestrial carnivores on Wroe, S., et al., 2013. Climate change frames debate over the extinction of mega- Pleistocene ecosystems. Proc. Natl. Acad. Sci. U.S.A. 113, 862e867. fauna in Sahul (Pleistocene Australia-New Guinea). Proc. Natl. Acad. Sci. U.S.A. Vitousek, P.M., et al., 1997. Human domination of earth's ecosystems. Science 277, 110, 8777e8781. 494e499. Wroe, S., Field, J., Grayson, D.K., 2006. Megafaunal extinction: climate, humans, and Vrba, E.S., DeGusta, D., 2004. Do species populations really start small? New per- assumptions. Trends Ecol. Evol. 21, 61e62. spectives from the Late Neogene fossil record of African mammals. Phil. Trans. Young, H.S., et al., 2016. Patterns, causes, and consequences of Anthropocene Biol. Sci. 359, 285e292. defaunation. Annu. Rev. Ecol. Evol. Syst. 47, 333e358. Walter, R.C., et al., 2000. Early human occupation of the Red sea coast of Eritrea Zachos, J., et al., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to during the last interglacial. Nature 405, 65e69. present. Science 292, 686e693. Watts, D.P., 2008. Scavenging by chimpanzees at Ngogo and the relevance of chim- Zimov, S.A., et al., 1995. Steppe-tundra transition: a herbivore- driven biome shift at panzee scavenging to early hominin behavioral ecology. J. Hum. Evol. 54,125e133. the end of the Pleistocene. Am. Nat. 146, 765e794. Werdelin, L., Lewis, M.E., 2013. Temporal change in functional richness and even- Zink, K.D., Lieberman, D.E., 2016. Impact of meat and Lower Palaeolithic food pro- ness in the eastern African plio-Pleistocene carnivoran guild. PLoS One 8 cessing techniques on chewing in humans. Nature 531, 500e503. e57944. Zuo, W., et al., 2013. A life-history approach to the Late Pleistocene megafaunal Western, D., Maitumo, D., 2004. Woodland loss and restoration in a savanna park: a extinction. Am. Nat. 182, 524e531. Brain size predicts problem-solving ability in mammalian carnivores

Sarah Benson-Amrama,b,1, Ben Dantzerc,d, Gregory Strickere, Eli M. Swansonf, and Kay E. Holekampe,g aDepartment of Zoology and Physiology, University of Wyoming, Laramie, WY 82071; bProgram in Ecology, University of Wyoming, Laramie, WY 82071; cDepartment of Psychology, University of Michigan, Ann Arbor, MI 48109; dDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109; eDepartment of Integrative Biology, Michigan State University, East Lansing, MI 48824; fDepartment of Ecology, Evolution, and Behavior, University of Minnesota, Twin Cities, St. Paul, MN 55108; and gEcology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI 48824

Edited by Karen B. Strier, University of Wisconsin, Madison, WI, and approved December 16, 2015 (received for review March 25, 2015)

Despite considerable interest in the forces shaping the relationship environment (17). In this study, we investigate whether larger- between brain size and cognitive abilities, it remains controversial brained animals do, indeed, exhibit enhanced problem-solving whether larger-brained animals are, indeed, better problem-solvers. abilities by conducting a standardized experiment in which we Recently, several comparative studies have revealed correlations present a novel problem-solving task to individuals from a large between brain size and traits thought to require advanced cognitive array of species within the mammalian order Carnivora. abilities, such as innovation, behavioral flexibility, invasion success, Carnivores often engage in seemingly intelligent behaviors, such and self-control. However, the general assumption that animals with as the cooperative hunting of prey (18, 19). Nevertheless, with the larger brains have superior cognitive abilities has been heavily exception of domestic dogs, carnivores have largely been ignored in criticized, primarily because of the lack of experimental support for the animal cognition literature (20). Mammalian carnivores com- it. Here, we designed an experiment to inquire whether specific prise an excellent taxon in which to assess the relationship between neuroanatomical or socioecological measures predict success at brain size and problem-solving ability and test predictions of hy- solving a novel technical problem among species in the mammalian potheses forwarded to explain the evolution of large brains and superior cognitive abilities, because they exhibit great variation in order Carnivora. We presented puzzle boxes, baited with food and their body size, their brain size relative to body size, their social scaled to accommodate body size, to members of 39 carnivore species structure, and their apparent need to use diverse behaviors to solve from nine families housed in multiple North American zoos. We found ecological problems. Although most carnivores are solitary, many that species with larger brains relative to their body mass were more species live in cohesive or fission–fusion social groups that closely successful at opening the boxes. In a subset of species, we also used resemble primate societies (21–23). Furthermore, experiments with virtual brain endocasts to measure volumes of four gross brain re- both wild spotted (24) andwildmeerkats(25)showthat gions and show that some of these regions improve model prediction members of these species are able to solve novel problems, and in of success at opening the boxes when included with total brain size spotted hyenas, those individuals that exhibit the greatest behav- and body mass. Socioecological variables, including measures of social ioral diversity are the most successful problem-solvers (24). complexity and manual dexterity, failed to predict success at opening Here, we presented steel mesh puzzle boxes, scaled according to the boxes. Our results, thus, fail to support the social brain hypothesis subject body size, to 140 individuals from 39 species in nine families but provide important empirical support for the relationship between of zoo-housed carnivores and evaluated whether individuals in each relative brain size and the ability to solve this novel technical problem. species successfully opened the boxes to obtain a food reward inside (Fig. 1A and Dataset S1). In addition to testing whether larger- brain size | problem-solving | carnivore | social complexity | intelligence brained carnivores are better at solving a novel technical problem, we inquired whether species that live in larger social groups exhibit nimals exhibit extreme variation in brain size, with the sperm enhanced problem-solving abilities compared with species that are Awhale’s brain weighing up to 9 kg (1), whereas the brain of the solitary or live in smaller social groups. We also asked whether desert ant weighs only 0.00028 g (2). Although body mass is the species exhibiting greater behavioral diversity are better at solving single best predictor of brain size (1, 3), some species have much larger brains than expected given their body size (e.g., humans and Significance dusky dolphins), whereas other species have much smaller brains than expected (e.g., hippopotamus and blue whale) (1). Brain tissue Intelligence presents evolutionary biology with one of its greatest is energetically costly (4–6), and therefore, large brains are presumed challenges. It has long been thought that species with relatively to have been favored by natural selection, because they confer ad- large brains for their body size are more intelligent. However, vantages associated with enhanced cognition (3). However, despite despite decades of research, the idea that brain size predicts great interest in the determinants of brain size, it remains controversial cognitive abilities remains highly controversial; little experimental whether brain size truly reflects an animal’s cognitive abilities (7–9). support exists for a relationship between brain size and the ability Several studies have found an association between absolute or to solve novel problems. We presented 140 zoo-housed members relative brain size and behaviors thought to be indicative of complex of 39 mammalian carnivore species with a novel problem-solving cognitive abilities. For example, brain size has been found to cor- task and found that the species’ relative brain sizes predicted relate with bower complexity in bower birds (10), success at building problem-solving success. Our results provide important support food caches among birds (11), numerical abilities in guppies (5), and for the claim that brain size reflects an animal’s problem-solving two measures of self-control in a comparative study of 36 species of abilities and enhance our understanding of why larger brains mammals and birds (12). Additionally, larger-brained bird species evolved in some species. have been found to be more innovative, more successful when in- vading novel environments, and more flexible in their behavior (13– Author contributions: K.E.H. designed research; G.S. performed research; B.D., E.M.S., and S.B.-A 16). Although there is circumstantial evidence suggesting an asso- analyzed data; S.B.-A., B.D., E.M.S., and K.E.H. wrote the paper; and S.B.-A. extracted video data. ciation between problem-solving ability and brain size, experimental The authors declare no conflict of interest. evidence is extremely rare. To experimentally assess the relationship This article is a PNAS Direct Submission. between brain size and any cognitive ability across a number of 1To whom correspondence should be addressed. Email: [email protected]. species in a standardized way is challenging because of the unique This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. adaptations each species has evolved for life in its particular 1073/pnas.1505913113/-/DCSupplemental.

2532–2537 | PNAS | March 1, 2016 | vol. 113 | no. 9 www.pnas.org/cgi/doi/10.1073/pnas.1505913113 AB

Fig. 1. (A) We tested the performance of zoo- housed individuals in 39 species from nine carnivore families by exposing them to our puzzle box prob- lem, with the box scaled to accommodate body size. (B) The relationship between body mass (kilograms) and brain volume (milliliters) in 39 mammalian car- nivore species. (A) Species in gray and (B) family names in gray represent species in which no tested subjects opened the box. Note that, in B, two species in the family Felidae (Panthera pardus and concolor) have overlapping points. problems than species exhibiting less behavioral diversity. Addi- considerably among families, with species in the families Ursidae tionally, carnivores exhibit an impressive range of manual dexterity (69.2% of trials), Procyonidae (53.8% of trials), and Mustelidae from the famously dexterous and to the much less (47.1% of trials) being most successful at opening the puzzle box dexterous hyenas and cheetahs (26). Therefore, to ensure that our and those within the family Herpestidae (0%) being the least suc- measure of problem-solving ability was not solely determined by cessful (Table S1). Total brain volume corrected for body mass manual dexterity and ensure that our problem-solving test was varied among the species that we tested, with Canid and Ursid equivalently difficult across a range of species, we also examined the species having the largest brains for their body mass and Viverrid, impact of manual dexterity on problem-solving success in this study. Hyaenid, and Herpestid species having the smallest brains for their Finally, the relative sizes of specific brain regions might be more body mass (Fig. 1B and Table S1). strongly predictive of problem-solving ability than overall brain size It appeared that the majority of subjects in our study actually relative to body size. Recently, Swanson et al. (27) used virtual brain gained an understanding of the puzzle and how to open it. If indi- endocasts to show that, although mammalian carnivore species with viduals were only using brute force to open the box or emitting a higher degree of social complexity did not have larger total brain exploratory behaviors without any understanding of how the puzzle volumes relative to either body mass or skull size, they did have works, then we should not have seen any evidence of learning the significantly larger cerebrum volumes relative to total brain volume. solution over time. To investigate whether the test subjects were Therefore, we used deviance information criterion (DIC) model actually learning the solution to the problem, we ran a non- selection analysis to inquire whether any of four gross regional brain phylogenetically corrected generalized linear mixed-effects model to volumes (total cerebrum, posterior cerebrum, anterior cerebrum, examine how work time changed over successive trials for successful and hindbrain) better predicted performance in our puzzle box trials individuals. Work time significantly decreased as trial number in- than total brain size in a subset of 17 carnivore species for which creased (F9,97 = 2.57; P = 0.01), indicating that successful individuals these data were available from virtual brain endocasts (Dataset S1). improved their performance with experience. We retrieved data on brain size and the sizes of gross brain regions The top model based on DIC model selection was one that con- from published literature and used phylogenetic comparative statistics tained brain volume, body mass, latency to approach the puzzle box, to assess relationships among these measures, social complexity, be- time spent trying to open the box, manual dexterity, behavioral di- havioral diversity, manual dexterity, and performance measures versity, and group size (Table 1). The only statistically indistinguish- obtained during box trials. We used social group size as our proxy for able model (i.e., ΔDIC < 2) did not include group size but was social complexity, because in an earlier comparative study of mam- otherwise the same (Table 1). Individuals from carnivore species with malian carnivores, Swanson et al. (27) found that group size was just both larger absolute brain volumes and larger brain volumes relative as effective of a proxy as the first axis from a principal component to their overall body mass were better than others at opening the analysis of several different measures of social complexity in carni- puzzle box, but only relative brain volume was a statistically significant vores. We used an established measure of behavioral diversity, which predictor [P value from Markov Chain Monte Carlo (pMCMC) = we obtained by calculating the number of different behaviors ex- 0.013] (Figs. 2 and 3, Table 2, and Table S2). Our results were in- hibited by individuals from each species while interacting with the sensitive to variation in both the total number of individuals tested puzzle box (24, 28–30). To assess manual dexterity, we recorded oc- per species and the minimum number of trials conducted per indi- currences of 20 types of forelimb movements following the work by vidual. Specifically, we obtained the same qualitative results if we Iwaniuk et al. (26). Finally, we used measures taken from virtual limited our analyses to only species in which at least three (398 trials brains to analyze the effects of the size of specific gross brain regions on 112 individuals from 23 species) (Table S3) or four individuals on performance in puzzle box trials. These measures allowed us to (348 trials on 97 individuals from 18 species) (Table S4)weretested inquire whether specific neuroanatomical or socioecological measures per species, and if we restricted our analyses only to individuals to can help explain variation in problem-solving ability across species. which we administered at least three separate trials (total number of trials per individual was 3–10) (Table S5). Additionally, if we restricted Results our analyses only to trials 1–3 for individuals that were tested at least We tested one to nine individuals in each of 39 species (mean = 4.9 three times (388 trials with 39 species), we found that individuals from individuals; median = 5) (Table S1). Of 140 individuals tested, 49 species with a larger brain volume for their body mass tended to be individuals (35%) from 23 species succeeded at opening the puzzle more likely to open the puzzle box (pMCMC = 0.052) (Table S6). box (Fig. 1A, Table S1,andMovie S1). The proportion of individ- Individuals from species with large average group sizes, such as COGNITIVE SCIENCES uals within each species that succeeded at opening the box varied banded (average group size = 23.7 individuals), were PSYCHOLOGICAL AND

Benson-Amram et al. PNAS | March 1, 2016 | vol. 113 | no. 9 | 2533 Table 1. Model comparisons using DIC model selection analysis to investigate the predictors of success in opening the puzzle box in 39 carnivore species Fixed effects λ-Posterior mode λ-Mean (95% credible interval) DIC ΔDIC

BV + BM + L + WT + D + BD + GS 0.94 0.85 (0.49–0.99) 283.2 0 BV + BM + L + WT + D + BD 0.93 0.82 (0.33–0.99) 284.9 1.7 L + WT + D + BD + GS 0.95 0.87 (0.62–0.99) 286.4 3.2 L + WT + D + BD 0.96 0.85 (0.56–0.99) 288.5 5.3 WT + D + BD 0.93 0.84 (0.54–0.99) 288.5 5.3 BV + BM + L + GS 0.97 0.91 (0.76–0.99) 293.3 10.1 BV + BM + L 0.95 0.88 (0.65–0.99) 294.3 11.1 BV + BM + GS 0.98 0.91 (0.73–0.99) 294.5 11.3 L + GS 0.97 0.92 (0.78–0.99) 296.4 13.2 BV + BM 0.96 0.88 (0.65–0.99) 296.6 13.4 GS 0.97 0.91 (0.73–0.99) 298.1 14.9 Intercept 0.96 0.90 (0.71–0.99) 299.9 16.7

Model terms are behavioral diversity (BD), body mass (BM), brain volume (BV), dexterity (D), group size (GS), latency to approach puzzle box (L), and time spent working trying to open the puzzle box (WT). no more successful at opening the puzzle box (pMCMC = 0.79) DIC values (Table 3). However, models containing hindbrain volume (Table 2) than individuals from solitary species, such as black (which includes both cerebellum and brainstem volumes; ΔDIC = bears (group size = 1) or (group size = 1). To further 0.2) or total cerebrum volume (ΔDIC = 0.3) were not considerably test whether social complexity affected carnivores’ ability to open worse. Notably, models containing body mass and total brain volume the puzzle box, we also compared success at opening the puzzle in addition to the volume of one of four specific brain regions all had box between solitary species (group size = 1) and social species lower DIC values than a model containing only body mass and total (group size > 1) where group size was a binary predictor. This brain volume (ΔDIC ranged from 1.9 to 2.2) (Table 3). This result comparison indicated that social species were no better at opening suggests that the addition of the volume of a brain region to the the puzzle box than solitary species (pMCMC = 0.99) (Table S7). model improved its ability to predict performance in the puzzle box Surprisingly, individuals from species with larger body sizes were trials over a model containing only total brain volume (Table 3). In less successful than smaller-bodied species at opening the puzzle box none of the models using the reduced dataset were the relative sizes (pMCMC = 0.036) (Table 2). Individuals that were more dexterous of any specific brain region associated with success in opening the (pMCMC = 0.08) (Table 2) and those that spent more time puzzle box (Table S9). attempting to open the puzzle box (pMCMC = 0.08) (Table 2) tended to be more successful, although neither of these were statistically Discussion significant. Individuals that more quickly approached the puzzle box The connection between brain size and cognitive abilities has been (pMCMC = 0.57) (Table 2) or those that used a greater diversity called into question by both a study pointing out the impressive of behaviors when interacting with the puzzle box (pMCMC = 0.39) cognitive abilities of small-brained species, such as bees and ants (7), (Table 2) were no more successful than others at opening the box. In and another study doubting that overall brain size is a valid proxy for nine of the puzzle box trials, individuals opened the box door but did cognitive ability (9). In the former case, Chittka and Niven (7) argue not retrieve the food reward, which might reflect underlying differ- that larger brains are partially a consequence of the physical need ences in motivation. We included these trials in our main analyses for larger neurons in larger animals and partially caused by in- (Table 2), but also, we ran our analyses without these nine trials and creased replication of neuronal circuits, which confers many ad- obtained the same qualitative results (Table S8). vantages for larger-brained species, such as enhanced perceptual In our brain region analyses, there was no obvious top model that abilities and increased memory storage. Chittka and Niven (7) best explained success at opening the puzzle box (Table 3). Models conclude that neither of these properties of larger brains necessarily containing relative anterior cerebrum volume (anterior to the cru- enhance cognitive abilities. Interestingly, our results actually show ciate sulcus; ΔDIC = 0) and posterior cerebrum volume (posterior to that carnivore species with a larger average body mass performed thecruciatesulcus;ΔDIC = 0) were the two models with the lowest worse than smaller-bodied species on the task that we presented to

F C A Ailuridae CF A C Canidae B F Felidae PM H Herpestidae P M Y Hyaenidae M M Mustelidae M F P Procyonidae F M U Ursidae M Fig. 2. (A) Carnivore species with larger brain volumes U V Viverridae U for their body mass were better than others at opening V U V U the puzzle box. (B) There was no significant relationship F C CF between absolute brain volume and success at opening

0.4 0.6 0.8F 1.0 F the puzzle box in carnivore species when body mass Y F F Y was excluded from the statistical model. Data pre- A C A C sented represent the average proportion of puzzle box 0.2 UU U U trials in which species were successful and are for pre- F PF P F F F F sentation purposes only, whereas statistical results from HFMPYFHFCCFCFV C U HFMPHFCVFCFCCYF U our full model used for our inferences are shown in 0.0 0.0 0.2 0.4 0.6 0.8 1.0

Prop. Trials Successful Opening Puzzle Box Table 2. Mass-corrected brain volume in A is from a -0.5 0.0 0.5 23456general linear model and for presentation purposes only; statistical results from the full model are shown in Mass-corrected Brain Volume log (Brain Volume) Table 2.

2534 | www.pnas.org/cgi/doi/10.1073/pnas.1505913113 Benson-Amram et al. 1.00 1.00 whichthebraincandevelop(32).Inadditiontofunctionallyspe- cialized modules, the brain also contains broad areas, such as the A B mammalian neocortex, that control multiple processes. Thus, there are reasons to believe that overall brain size may be an informative 0.75 0.75 proxy for cognitive abilities, despite the modular nature of the brain. Here we examined relationships between relative brain size, size of specific brain regions, and problem-solving success. Although none of the regional brain volumes that we examined significantly predicted 0.50 0.50 success on this task (Table S9), the addition of the volume of these brain regions improved the ability of our models to explain perfor- mance in the puzzle box task over a model containing only total brain volume (Table 3). We emphasize, however, that only 17 species were 0.25 0.25 included in that analysis. Nevertheless, relative brain size was a sig- Success at Opening Puzzle Box nificant predictor of problem-solving success across species, and this result was robust in all of our analyses. Thus, our data provide im-

0.00 0.00 portant support for the idea that relative brain size can be useful in examining evolutionary relationships between neuroanatomical and -0.5 0.0 0.5 1.0 23456 Residual Brain Volume log(Brain Volume) cognitive traits and corroborate results from artificial selection ex- periments showing that larger brain size is associated with enhanced Fig. 3. (A) Individuals from carnivore species with larger brain volumes relative problem solving (5). It will be important in future work to use more to their body mass were significantly better than others at opening the puzzle detailed noninvasive brain imaging methods rather than endocasts to box (Table 2). (B) There was no significant relationship between absolute brain evaluate whether hypothetically important brain areas, such as pre- volume and success at opening the puzzle box in our individual-level analyses in frontal and cingulate cortexes, contribute to the relationship between which body mass was excluded (Table S2). Individuals with success equal to one brain size and performance during problem solving. opened the box, whereas those with success equal to zero did not. Mass-cor- Assessment of the ecological and neuroanatomical predictors of rected brain volume in A is from a general linear model and for presentation problem-solving ability has some important implications for hy- purposes only; full statistical results are shown in Table 2 and Table S2.Re- potheses proposed to explain the adaptive value of large brains and gression lines represent predicted relationships from statistical models in- sophisticated cognition. One such hypothesis that has garnered vestigating the association between (A) brain volume relative to body mass or (B) much support in primate studies is “the social brain hypothesis” (33, log (brain volume) and success at opening the puzzle box. 34), which proposes that larger brains evolved to deal with chal- lenges in the social domain. This hypothesis posits that selection them. Thus, it truly does seem that a larger brain size relative to favored those individuals best able to anticipate, respond to, and body size is an important determinant of performance on this task, perhaps even manipulate the actions of conspecific group members. However, a major shortcoming of the social brain hypothesis (35, and it is not the case that larger animals are more successful simply 36) is its apparent inability to explain the common observation that because their brains are larger than those of smaller species. species with high sociocognitive abilities also excel in general in- Regarding whether overall brain size is a valid proxy for cognitive telligence (37, 38). There is, in fact, a long-standing debate as to abilities, the use of whole-brainsizeasapredictorofcognitive whether animal behavior is mediated by cognitive specializations complexity in comparative studies is questioned, because the brain that have evolved to fulfill specific ecological functions or instead, has different functional areas, some of which are devoted to partic- domain-general mechanisms (38, 39). If selection for social agility ular activities, such as motor control or sensory processing. Given this has led to the evolution of domain-general cognitive abilities, then high degree of modularity in the brain, Healy and Rowe (8, 9) argue species living in social groups should solve technical problems better that overall brain size is unlikely to be a useful measure when ex- than solitary species. However, we found that carnivore species amining how evolution has shaped the brains of different species living in social groups performed no better on our novel technical to perform complex behaviors. Although the brain has functional problem than solitary species. Thus, whereas social complexity may modules, such as the hippocampus or the olfactory bulbs, which may select for enhanced ability to solve problems in the social domain be under specific selection pressures (31), these modules may also (40), at least in carnivores, greater social complexity is not associated exhibit coordinated changes in size because of constraints on ways in with enhanced ability to solve a novel technical problem.

Table 2. Results from Bayesian phylogenetic generalized linear mixed-effects models to investigate the predictors of success in opening the puzzle box in 39 mammalian carnivore species Effective sample size Posterior mean (95% CI) Posterior mode pMCMC

Random effect Species 3,094 13.8 (0.0007–40.4) 4.3 — Individual identification 2,791 21 (7.6–38.2) 16.1 — Fixed effect Intercept* 3,284* −36.5 (−60.7 to −16.1)* −30.6* 0.0003* Brain volume* 3,284* 8.5 (1.3–16.3)* 7.8* 0.013* Body mass* 3,720* −4.6 (−9.2 to −0.2)* −4.9* 0.036* Latency to approach 3,284 −0.12 (−0.5–0.3) −0.1 0.57 Work time 2,493 0.34 (−0.04–0.7) 0.4 0.08 Behavioral diversity 3,018 1.7 (−1.9–6) 1.2 0.39 Dexterity 3,284 2.7 (−0.3–5.8) 2.2 0.08 Group size 3,284 −0.04 (−0.3–0.2) −0.02 0.79

pMCMC is the Bayesian P value. Sample sizes are 495 trials on 140 individuals from 39 different species. 95% CI, 95% credible interval. COGNITIVE SCIENCES *Statistically significant. PSYCHOLOGICAL AND

Benson-Amram et al. PNAS | March 1, 2016 | vol. 113 | no. 9 | 2535 Table 3. Model comparisons using DIC model selection to investigate whether the volumes of specific brain regions better predicted success in opening the puzzle box than total brain volume in 17 mammalian carnivore species Model name Fixed effects λ-Posterior mode λ-Mean (95% CI) DIC ΔDIC

Anterior cerebrum AC + BM + BV 0.006 0.42 (0.0003–0.99) 88.4 0 Posterior cerebrum PC + BM + BV 0.004 0.37 (0.0002–0.98) 88.4 0 Brainstem/cerebellum BS/CL + BM + BV 0.006 0.42 (0.004–0.99) 88.6 0.2 Cerebrum C + BM + BV 0.006 0.41 (0.0003–0.99) 88.7 0.3 Brain BV + BM 0.005 0.36 (0.0002–0.98) 90.6 2.2

Model terms are volume of anterior cerebrum (AC), body mass (BM), volume of brainstem and cerebellum (BS/ CL), volume of total brain (BV), volume of total cerebrum (C), and volume of posterior cerebrum (PC). 95% CI, 95% credible interval.

Our results are similar to those obtained in the work by MacLean body mass = 50 kg) and wild dogs (species average body mass = 22.05 kg), both et al. (12), which examined relationships among brain size, social large and small boxes were used with some subjects, but their performance complexity, and self-control in 23 species of primates. In both that did not vary with box size (additional details are given in SI Text). study and our own study, species with the largest brains showed the We videotaped all trials and extracted performance measures from videotapes best performance in problem-solving tasks. However, in neither pri- using methods described elsewhere (24, 28, 45) (Movie S1). Extracted behaviors mates nor carnivores did social complexity predict problem-solving included the latency to approach the puzzle box, the total time spent trying to success. This finding is also consistent with results obtained in the open the box, the number of different behaviors used in attempting to open work by Gittleman (41), with analysis of 153 carnivore species that the box, and a measure of manual dexterity (all described in SI Text). We then revealed no difference in brain size relative to body size between brought together data on success and performance measures during zoo trials social and solitary species. Nevertheless, in this study, we were only with previously published data on total brain size and body mass (46). able to present carnivores with a single problem-solving task, and we We used Bayesian phylogenetic generalized linear mixed-effects models were only able to test one to nine individuals per species. Ideally, based on a Markov Chain Monte Carlo algorithm implemented in the R future studies will present a large array of carnivores with additional package MCMCglmm (47–49) to identify the variables predicting success or cognitive challenges and will test more individuals per species. failure in solving this puzzle. These models allowed us to assess the effects of A second hypothesis forwarded to explain the evolution of larger predictor variables on carnivores’ success at opening the puzzle box after and more complex brains, the cognitive buffer hypothesis (42, 43), controlling for shared phylogenetic history. posits that large brains evolved to allow animals to cope with For our analyses of how brain volume affected the ability of carnivores to open socioecological challenges and thus, reduce mortality in changing the puzzle box, we constructed 12 different models containing different com- environments. Previous work has shown convincingly that diet is a binations of the morphological, behavioral, and social characteristics of tested significant predictor of brain size in carnivores (27), as it is in pri- species or individuals (Table 1). In all models except that shown in Table S2,we mates (12), and this study shows that carnivore species with larger included species’ average body mass as a covariate so that we could assess the brains are more likely to solve a novel technical problem. However, effects of brain volume on puzzle box performance relative to body mass (50, an explicit test of the cognitive buffer hypothesis has not yet been 51). We used DIC (51) to examine the relative degree of fit of the different attempted with mammalian carnivores. models. DIC is analogous to Akaike’s information criterion (52), and lower values Overall, our finding that enhanced problem solving is related to for DIC suggest a better fit. We present DIC values for all models (Table 1) but disproportionally large brain size for a given body mass is important only present results from the model with the lowest DIC (Table 2) (53). for several reasons. First, although there is correlational evidence for In separate analyses, we performed five different Bayesian phylogenetic an association between absolute or relative brain size and problem- generalized linear mixed-effects models to determine whether the volume of any solving abilities, experimental evidence is extremely rare. The lack of specific brain region better predicted success in opening the puzzle box than experimental evidence has led to criticisms of the use of brain size as overall endocranial volume (Table 3). These models also included species’ aver- a proxy for problem-solving abilities (8, 9, 44). We offer experimental age body mass and total brain volume as covariates (27). Computed tomogra- evidence that brain size is, indeed, a useful predictor of performance, phy data were available documenting both total endocranial volume and the at least in the single problem-solving task that we posed to our volumes of specific brain regions from 17 different carnivore species in six carnivore subjects. Although only brain size relative to body mass was families (Dataset S1). Overall endocranial volume was subdivided into (i) cere- a significant predictor of success with our puzzle box, species with brum anterior to the cruciate sulcus, (ii) cerebrum posterior to the cruciate larger absolute brain volumes also tended to be better than others at sulcus, (iii) total cerebrum, and (iv) hindbrain, which includes both cerebellum opening the puzzle box (Figs. 2 and 3 and Table S2). Second, the vast and brainstem. The cerebrum anterior to the cruciate sulcus is comprised mainly majority of work on this topic has focused on primates, fish, and birds of frontal cortex. Additional methodological details on the estimation of these (5, 10, 11, 13–16). Our results offer new evidence for the relationship brain region volumes can be found elsewhere (54–56) (SI Text). between brain size and problem-solving abilities in mammalian car- Our response variable was binary (did or did not open puzzle box); therefore, nivores. The previous lack of support for this relationship across a we used a categorical error structure in MCMCglmm, and we fixed the prior for diverse set of taxa has limited both its validity and its generality. the residual variance to one (V = 1; fix = 1). We included random effects for species Thus, the findings presented here represent an important step for- and individual identity in these models. We used weakly informative inverse ward in our understanding of why some animals have evolved large γ-priors with a low degree of belief (V = 1; μ = 0.002) for the random effect brains for their body size. variance. All models were run for appropriate numbers of iterations, burn-ins, and thinning intervals to generate a minimum effective sample size of >2,000 for all Materials and Methods parameters in all of the different models. We provide the mean, mode, and 95% credible interval from the posterior distribution of each parameter. We considered From 2007 to 2009, we presented puzzle boxes to myriad carnivores housed in nine North American zoos (Fig. 1A and Dataset S1). Because we were testing parameters to be statistically significant when the 95% credible intervals did not < animals that ranged in size from roughly 2 to 300 kg, we used two steel mesh overlap zero and pMCMC was 0.05 (47). Detailed statistical methods are in SI Text. puzzle boxes; the larger box was 63.5 × 33 × 33 cm, and the smaller box was Appropriate ethical approval was obtained for this work. This work was one-half that size. The smaller box was presented to species with an average approved by Michigan State University Institutional Animal Care and Use body mass of <22 kg, such as river otters, kinkajous, sand cats, and other Committee (IACUC) Approval 03/08-037-00 and also, the IACUCs at all nine zoos small-bodied carnivores (Dataset S1). The larger box was presented to species (St. Louis Zoo, Bergen County Zoo, Binder Park Zoo, Potter Park Zoo, Columbus with an average body mass >22 kg, including snow leopards, wolves, bears, Zoo, The Living Desert, Wild Canid Survival and Research Center, Turtle Back and other large-bodied species (Dataset S1). For cheetahs (species average Zoo, and Denver Zoo) where testing was done.

2536 | www.pnas.org/cgi/doi/10.1073/pnas.1505913113 Benson-Amram et al. ACKNOWLEDGMENTS. We thank Steve Glickman for inspiring this work and Science Foundation (NSF) Grants IOS 1121474 (to K.E.H.) and DEB 1353110 Adam Overstreet for help with data extraction. We thank Dorothy Cheney, (to K.E.H.) and NSF Cooperative Agreement DBI 0939454 supporting the Robert Seyfarth, Jeff Clune, and three anonymous reviewers for many BEACON Center for the Study of Evolution in Action. E.M.S. was supported helpful suggestions and discussions. This work was supported by National by NSF Postdoctoral Fellowship 1306627.

1. Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9(5): 38. Reader SM, Hager Y, Laland KN (2011) The evolution of primate general and cultural 250–257. intelligence. Philos Trans R Soc Lond B Biol Sci 366(1567):1017–1027. 2. Wehner R, Fukushi T, Isler K (2007) On being small: Brain allometry in ants. Brain 39. Thornton A, Clayton NS, Grodzinski U (2012) Animal minds: From computation to Behav Evol 69(3):220–228. evolution. Philos Trans R Soc Lond B Biol Sci 367(1603):2670–2676. 3. Striedter GF (2005) Principles of Brain Evolution (Sinauer, Sunderland, MA). 40. Maclean EL, et al. (2013) Group size predicts social but not nonsocial cognition in 4. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: The brain and the di- lemurs. PLoS One 8(6):e66359. gestive system in human and primate evolution. Curr Anthropol 36(2):199–221. 41. Gittleman JL (1986) Carnivore brain size, behavioral ecology, and phylogeny. 5. Kotrschal A, et al. (2013) Artificial selection on relative brain size in the guppy reveals J Mammal 67(1):23–36. costs and benefits of evolving a larger brain. Curr Biol 23(2):168–171. 42. Sol D (2009) Revisiting the cognitive buffer hypothesis for the evolution of large 6. Isler K, van Schaik CP (2009) The expensive brain: A framework for explaining evo- brains. Biol Lett 5(1):130–133. lutionary changes in brain size. J Hum Evol 57(4):392–400. 43. Sol D (2009) The cognitive-buffer hypothesis for the evolution of large brains. Cognitive 7. Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19(21):R995–R1008. Ecology II, eds Dukas R, Ratcliffe RM (Chicago Univ Press, Chicago), pp 111–136. 8. Healy SD, Rowe C (2013) Costs and benefits of evolving a larger brain: Doubts over the 44. Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25(6):1287–1292. evidence that large brains lead to better cognition. Anim Behav 86(4):e1–e3. 45. Benson-Amram S, Heinen VK, Gessner A, Weldele ML, Holekamp KE (2014) Limited social 9. Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc Biol Sci learning of a novel technical problem by spotted hyenas. Behav Processes 109(Pt B):111–120. 274(1609):453–464. 46. Finarelli JA, Flynn JJ (2009) Brain-size evolution and sociality in Carnivora. Proc Natl 10. Madden J (2001) Sex, bowers and brains. Proc Biol Sci 268(1469):833–838. Acad Sci USA 106(23):9345–9349. 11. Garamszegi LZ, Eens M (2004) The evolution of hippocampus volume and brain size in 47. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed – relation to food hoarding in birds. Ecol Lett 7(12):1216 1224. models: The MCMCglmm R package. J Stat Softw 33(2):1–22. 12. MacLean EL, et al. (2014) The evolution of self-control. Proc Natl Acad Sci USA 111(20): 48. Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for compar- – E2140 E2148. ative biology: Phylogenies, taxonomies and multi-trait models for continuous and 13. Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced categorical characters. J Evol Biol 23(3):494–508. cognition, and response of birds to novel environments. Proc Natl Acad Sci USA 49. Garamszegi LZ (2014) Modern Phylogenetic Comparative Methods and Their – 102(15):5460 5465. Application in Evolutionary Biology (Springer, Berlin). 14. Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in 50. Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22(7): – birds. Anim Behav 63(3):495 502. 1367–1375. 15. Sol D, Lefebvre L, Rodríguez-Teijeiro JD (2005) Brain size, innovative propensity and 51. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: – migratory behaviour in temperate Palaearctic birds. Proc Biol Sci 272(1571):1433 1441. A test and review of evidence. Am Nat 160(6):712–726. 16. Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds in- 52. Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of troduced to New Zealand. Oikos 90(3):599–605. model complexity and fit. J R Stat Soc Series B Stat Methodol 64(4):583–639. 17. Kotrschal A, Corral-Lopez A, Amcoff M, Kolm N (2015) A larger brain confers a benefit 53. Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: in a spatial mate search learning task in male guppies. Behav Ecol 26(2):527–532. A Practical Information-Theoretic Approach (Springer Science and Business Media, Berlin). 18. Mech LD (2007) Possible use of foresight, understanding, and planning by wolves 54. Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011) Brain size and social com- hunting muskoxen. Arctic 60(2):145–149. plexity: A computed tomography study in Hyaenidae. Brain Behav Evol 77(2):91–104. 19. Bailey I, Myatt JP, Wilson AM (2013) Group hunting within the Carnivora: Physio- 55. Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011) Virtual endocasts: An ap- logical, cognitive and environmental influences on strategy and cooperation. Behav plication of computed tomography in the study of brain variation among hyenas. Ecol Sociobiol 67(1):1–17. Ann N Y Acad Sci 1225(Suppl 1):E160–E170. 20. Vonk J, Jett SE, Mosteller KW (2012) Concept formation in American black bears, 56. Arsznov BM, Lundrigan BL, Holekamp KE, Sakai ST (2010) Sex and the frontal cortex: Ursus americanus. Anim Behav 84(4):953–964. A developmental CT study in the spotted . Brain Behav Evol 76(3-4):185–197. 21. Gittleman JL (1989) Carnivore group living: Comparative trends. Carnivore Behaviour, 57. Barrett L (2014) What counts as (non) cognitive?: A comment on Rowe and Healy. Ecology and Evolution, ed Gittleman JL (Cornell Univ Press, Ithaca, NY), pp 183–208. Behav Ecol 25(6):1293–1294. 22. Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator de- 58. Shettleworth SJ (2010) Cognition, Evolution, and Behavior (Oxford Univ Press, New York). fenses in carnivores. Evolution 68(5):1415–1425. 59. Cole EF, Morand-Ferron J, Hinks AE, Quinn JL (2012) Cognitive ability influences re- 23. Holekamp KE, Dantzer B, Stricker G, Shaw Yoshida KC, Benson-Amram S (2015) productive life history variation in the wild. Curr Biol 22(19):1808–1812. Brains, brawn and sociality: A hyaena’s tale. Anim Behav 103:237–248. 60. Isden J, Panayi C, Dingle C, Madden J (2013) Performance in cognitive and problem- 24. Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted solving tasks in male spotted bowerbirds does not correlate with mating success. hyenas. Proc R Soc Lond B Biol Sci 279(1744):4087–4095. Anim Behav 86(4):829–838. 25. Thornton A, Samson J (2012) Innovative problem solving in wild . Anim 61. Bergman TJ, Beehner JC (2015) Measuring social complexity. Anim Behav 103:203–209. Behav 83(6):1459–1468. 62. Dunbar RIM (1992) Neocortex size as a constraint on group size in primates. J Hum 26. Iwaniuk AN, Pellis SM, Whishaw IQ (1999) Brain size is not correlated with forelimb – dexterity in fissiped carnivores (Carnivora): A comparative test of the principle of Evol 22(6):469 493. proper mass. Brain Behav Evol 54(3):167–180. 63. White DJ, Gersick AS, Snyder-Mackler N (2012) Social networks and the development – 27. Swanson EM, Holekamp KE, Lundrigan BL, Arsznov BM, Sakai ST (2012) Multiple of social skills in cowbirds. Philos Trans R Soc Lond B Biol Sci 367(1597):1892 1900. determinants of whole and regional brain volume among terrestrial carnivorans. 64. Bininda-Emonds ORP, et al. (2007) The delayed rise of present-day mammals. Nature – PLoS One 7(6):e38447. 446(7135):507 512. 28. Benson-Amram S, Weldele ML, Holekamp KE (2013) A comparison of innovative 65. Fritz SA, Bininda-Emonds ORP, Purvis A (2009) Geographical variation in predictors of – problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta. mammalian extinction risk: Big is bad, but only in the tropics. Ecol Lett 12(6):538 549. Anim Behav 85(2):349–356. 66. R Development Core Team (2014) R: A Language and Environment for Statistical 29. Griffin AS, Guez D (2014) Innovation and problem solving: A review of common Computing (R Found Stat Comput). Available at https://www.r-project.org. Accessed mechanisms. Behav Processes 109(Pt B):121–134. June 1, 2015. 30. Griffin AS, Diquelou M, Perea M (2014) Innovative problem solving in birds: A key role 67. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: Investigating of motor diversity. Anim Behav 92:221–227. evolutionary radiations. Bioinformatics 24(1):129–131. 31. Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 68. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 405(6790):1055–1058. 401(6756):877–884. 32. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution 69. Housworth EA, Martins EP, Lynch M (2004) The phylogenetic mixed model. Am Nat of mammalian brains. Science 268(5217):1578–1584. 163(1):84–96. 33. Brothers L (1990) The social brain: A project for integrating primate behaviour and 70. Plummer M, Best N, Cowles K, Vines K (2006) CODA: Convergence diagnosis and neurophysiology in a new domain. Concepts Neurosci 1:27–51. output analysis for MCMC. R News 6(1):7–11. 34. Barton RA, Dunbar RIM (1997) Evolution of the social brain. Machiavellian Intelligence II: 71. Geweke J (1992) Evaluating the accuracy of sampling-based approaches to calculating Extensions and Evaluations, eds Whiten A, Byrne RW (Cambridge Univ Press, Cambridge, posterior moments. Bayesian Statistics, ed Jm B (Clarendon, Oxford). United Kingdom), pp 240–263. 72. Gelman A, Rubin D (1992) Inference from iterative simulation using multiple se- 35. Holekamp KE (2007) Questioning the social intelligence hypothesis. Trends Cogn Sci quences. Stat Sci 7(4):457–511. 11(2):65–69. 73. Brooks SPB, Gelman AG (1998) General methods for monitoring convergence of it- 36. van Schaik CP, Isler K, Burkart JM (2012) Explaining brain size variation: From social to erative simulations. J Comput Graph Stat 7(4):434–455. cultural brain. Trends Cogn Sci 16(5):277–284. 74. Gelman AG (2006) Prior distributions for variance parameters in hierarchical models. 37. Byrne RW (1997) The technical intelligence hypothesis: An additional evolutionary Bayesian Anal 1(3):515–533. stimulus to intelligence? Machiavellian Intelligence II: Extensions and Evaluations, eds 75. Hadfield J (2015) MCMCglmm Course Notes. Available at cran.us.r-project.org/web/ Whiten A, Byrne RW (Cambridge Univ Press, Cambridge, United Kingdom), pp 289–311. packages/MCMCglmm/vignettes/CourseNotes.pdf. Accessed October 13, 2014. COGNITIVE SCIENCES PSYCHOLOGICAL AND

Benson-Amram et al. PNAS | March 1, 2016 | vol. 113 | no. 9 | 2537