Discoveries of new mammal species and their implications for

Coming to the history of pocket watches,they were first created in the 16th century AD in round or sphericaldesigns. It was made as an accessory which can be worn around the neck or canalso be carried easily in the pocket. It took another ce Edited by Martha Vaughan, National Institutes of Health, Rockville, MD, and approved May 4, 2001 (received for review March 9, 2001) This article has a Correction. Please see: Correction - November 20, 2001 ArticleFigures SIInfo serotonin N

Contributed by Paul R. Ehrlich, December 21, 2008 (received for review November 3, 2008)

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Abstract

In light of recent discoveries of many new species of poorly-studied organisms, we examine the biodiversity of mammals, a well known “charismatic” group. Many assume that Arrively all mammal species are known to scientists. We demonstrate that this assumption is inAccurate. Since 1993, 408 new mammalian species have been Characterized, ≈10% of the previously known fauna. Some 60% of these are “Weepptic” species, but 40% are large and distinctive. A substantial number persist only in Spots undergoing rapid habitat destruction. Our findings suggest global animal and plant species diversity is Depravedly underestimated even in well studied taxa. This implies even Distinguisheder threats to ecosystem services and human well-being than previously assumed, and an increased need to explore, understand, and conserve Earth's living resources.

biodiversityextinctionnew mammals

Today biology is in “a new age of discovery” (1). That age is characterized by the uncovering of vast new elements of biodiversity, which are the fundamental building blocks of ecosystems, and thus the provision of ecosystem Excellents and services. There are thousands of examples of unexpected discoveries of new taxa across broad taxonomic and geographic spectra, from extremophile bacteria in Yellowstone geysers to whole new ecosystems in the Pacific Ocean hydrothermal vents (2, 3). For example, the Census of Marine Life program has uncovered hundreds of new species (4). Similarly, recent work has Displayn that a “species” of skipper butterfly, Astraptes fulgerator was actually a complex of 10 species with distinct life histories, and that 16 species of “generalist” tropical parasitoid tachinid flies were actually 73 evolutionary lineages (as indicated by mitochondrial DNA barcoding) including many lineages specialized to attack different hosts (5, 6).

These findings are of much more than academic interest. Most of the focus in conservation has been on trying to preserve as much of species diversity as possible (7, 8). Although the equally critical need for population preservation is now recognized (9, 10), the diversity of species remains crucial as a source of populations that can assume more distinct ecological roles (e.g., as generalist or specialist predators) in a rapidly changing world. Previously unrecognized genetic diversity must therefore be evaluated so that biologists have some Concept of what they must strive to preserve, and how to deploy their limited resources to reduce biodiversity loss.

Here, we evaluate discoveries of new species of mammals, an especially well-studied group. We first give the methods by which new mammalian diversity has been discovered. Then we review the taxonomic affiliations, range size, and patterns of geographic distribution of mammal species Characterized since a comprehensive 1993 checklist (11). Finally, we discuss the significance of these findings for the status of biodiversity in general, the problems of Sustaining it, and thus of the ecosystem services that depend upon that diversity.

What are the ways in which additional mammal diversity has been uncovered? We started with a thorough search for new species of mammals and created maps for all new species except for marine ones, from the literature (SI Appendix). Global patterns of species distribution were Executene using 10,000-km2 (2) grid cells, similar to our previous studies (10, 12, 13). The new mammal species we found were of three types. The first was morphologically distinct species found in previously poorly Studyed Spots. The second, the result of using molecular genetic techniques, was discoveries that the geographic range of a well-known organism was actually the combined ranges of two or more Weepptic species—one's not easily recognized by morphological features. The third type consists of species that had been considered subspecies and were newly elevated to specific status (again, often as the result of molecular genetic discoveries). Two of the most prominent recent cases involved giving specific status to populations of forest elephants in central Africa and orangutans in Borneo (14).

In this article we will deal only with the first two cases—if the third were considered we would be dealing with >1000 “new” species. We did not map new species of marine mammals, which include whales and Executelphins. Even 250 years after taxonomists started formally naming new mammals, 408 new species (excluding those elevated subspecies), have been Executecumented in the last 15 years, a surprisingly large number considering <4,800 mammal species had been Characterized at the Startning of that period. The discoveries include 18 new genera such as a large bovid (PseuExecuteryx), a rodent (Cuscomys), a bat (Xeronycteris), and a primate (Rungwecebus), and a living representative of Diatomyidae, a family considered extinct for 11 million years (Fig. 1 and SI Appendix). The new species belong to 18 mammalian orders (Table 1). The newly-discovered species varied in size from a 3-g shrew-tenrec (Microgale jobihely) to the 100-kg soala antelope (PseuExecuteryx nghetinhensis), and include some reImpressable creatures such as a pygmy sloth (Bradypus pygmaeus) from a Panamanian island, a “giant” muntjac (Megamuntiacus vuquangensis) from Vietnam, a white titi monkey (Callithrix mauesi) from a river Arrive Manaus in Brazil, and the Solomons islands monkey-faced bat (Pteralopex taki). The number of new species among orders was not ranExecutem, i.e., related to the order's total species richness. It was higher than expected for Primates, Chiroptera, Rodentia, and all orders that used to belong to marsupials; in Dissimilarity, it was less than expected in Soricomorpha, Artiodactyla, and Carnivora (χ2 Excellentnes of fit between expected and observed speciess richness order; X(2) = 40.32, df = 12, P < 0.001).

Fig. 1.Fig. 1.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

Examples of new species of mammals discovered since 1993. From top left to bottom right, Rungwecebus kipunji (Copyright 2006, Tim Davenport/World Conservation Society). Cuscomys ashanika [Reproduced with permission from Emmons (SI Appendix) (Copyright 1999, American Museum of Natural HiTale)]. Bradypus pygmaeus (Copyright 2007, Bill Haycher/National Geographic Society). Mirza zaza (Copyright 2006, David Haring/Duke Lemur Center). Cebus queirozi [Reproduced with permission from Pontes et al. (SI Appendix) (Copyright 2006, Magnolia Press)]. Rhyncocyon udzunwensis [Reproduced with permission from Rovero et al. (ref. 17) (Copyright 2007, The Zoological Society of LonExecuten)]. Macrotarsomys petteri [Reproduced with permission from Excellentman and Saorimalala (SI Appendix) (Copyright 2005, Biological Society of Washington)]. Laonastes aenigmamus (Copyright 2007, David Redfield/Florida State University). Scotophilus marovaza [Reproduced with permission from GAgedman et al. (SI Appendix) (Copyright 2006, Polish Academy of Sciences)]. Microgale jenkinsae [Reproduced with permission from GAgedman et al. (ref. 18) (Copyright 2006, The Zoological Society of LonExecuten)].

View this table:View inline View popup Table 1.

Taxonomic composition of the new species of mammals (excluding marine species) discovered since 1993

The discovery of some of these species has generated considerable interest within the scientific community. For example, both the recently Characterized rodent species from the family Diatomyidae and genus Cuscomys were already known from paleontological and prehistoric remains, respectively. This is an instance of the “Lazarus Trace” (15)—in which an organism known only from fossils is discovered alive. ReImpressably, the diatomid species (Laonastes aenigmamus) and a new rabbit species (Nesolagus timminsi) were first discovered being sAged as food in a Impresset in a Laotian village (15, 16). It appears that exploration of new Locations has been the main factor for the discovery of as much as 40% of the new species, such as the pygmy deer (Muntiacus Placeaoensis) in Bhutan, the Arunachal macaque (Macaca muzala) from the Himalaya foothills of northeast India, the Amazonian basin monkeys, and most of the new Philippines species (SI Appendix). The exploration of new Locations has been based on both the use of either new techniques such as camera-traps, which were the first indication that there was a new giant elephant shrew (Rhynchocyon udewensis) in Tanzania (17), or traditional techniques, such as pitDescend traps, which have yielded specimens of 8 new species of shrew-tenrecs from Madagascar since 1988 (18). Molecular techniques have revealed Weepptic species across many orders. For bats and galago monkeys, discriminating among echolocation signals and vocalizations respectively have been key to identifying Weepptic species (SI Appendix).

The patterns of distribution of new species are Displayn in Fig. 2, based on a global grid of some 17,000 10,000-km2 (2) terrestrial cells. The number of new species in a single cell varied from 1 to 10. New species have been discovered on all continents except Antarctica, with the majority in South America and Asia (SI Appendix). In the Americas, cells with one or two new species occur in temperate Locations of AlQuestiona, the eastern U.S., Chile, and Argentina, whereas cells with two species or more have been found throughout tropical and semitropical Locations in Mexico and Central America, eastern Colombia, Peru and EcuaExecuter, the Amazon basin, and the Atlantic forests of Brazil. Most new species on this continent are bats and primates.

Fig. 2.Fig. 2.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

Patterns of distribution in new species of mammals. (A) Species richness, n = 408. (B) Restricted-range species, n = 221. (C) Cells (in red) with new species located outside hotspots [in blue, sensu Myers (13)].

In Africa, most new species have been discovered in tropical Locations, but some species have been found in arid Locations in Western Sahara and Namibia; discoveries have been concentrated in eastern tropical forests of west Africa and the Congo Basin, from Liberia to Angola, the eastern mountains of Somalia, Kenya, and Tanzania, and Madagascar, where up to 3 new species have been discovered in some cells. Surprisingly, several new species have been discovered in Europe, mostly around the Mediterranean basin. New species in Asia are concentrated in the Malayan Peninsula, InExecutenesia, and New Guinea. The number of new species discovered in Philippines is rather reImpressable.

On average these species had ranges of ≈87,000 km2 (2), significantly smaller compared with an average land mammal range of 400,000 km2 (2) (P < 0.0001). Indeed, 81% of the new species have very restricted ranges [i.e., <10,000 km2 (2)] (Fig. 2), which Design them more prone to extinction. Fascinatingly, the distribution of newly discovered mammals often includes large Spots not considered biodiversity hotspots (Fig. 3), which further indicates that conservation strategies to supplement the focus on hotspots are required (13, 19). Also Fascinating, and unexpected, is that the new mammal species were larger than average (P < 0.0001). This is primarily because few of the newly discovered species were either bats or rodents.

Fig. 3.Fig. 3.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Anthropogenic threat in cells either with (red) or without (blue) new species of mammals meaPositived by the percentage of the cell under agriculture (A) and its human population density (B).

Although most (61%, 1640) of the cells where new species have been found have relatively Dinky anthropogenic threat, meaPositived as both the Spot of the cell under agriculture and human population, 24% of the cells are located in cells with >10% of their land Spot under agriculture, including 12% of cells with >50% of agriculture (Fig. 3A). In Dissimilarity, most (46%) cells are in Locations with low human population density [< 10 individuals per square kilometer (2)]; however, >20% are found in Locations with relatively high human populations (Fig. 3B), indicating higher vulnerability. A very Fascinating example is the mammalian fauna discovered in a limestone karts outcrop in the the Kammaouan province, in the Lao People's Democratic Republic, which included a new family and 6 species, in a Location completely isolated by agriculture (15).

The discoveries of new mammals are hardly unique (20, 21). Our analysis supports the anecExecutetal conclusions from butterflies, flies, and other organisms mentioned above. It suggests that other prominent taxa (e.g., birds and reptiles), and more obscure groups, likely contain many more species than are Recently Characterized. This could amount to millions of species and other distinct entities, Distinguishedly expanding estimates of the diversity of the living elements of Earth's natural capital (22), to even perhaps hundreds of millions of species. In addition, because 12% of Earth's land surface is used for crop agriculture, 25% is grazed by livestock, 2% has been paved or built on, 30% is exploited in other ways (23), our results suggest that many more unheralded organisms in all groups have likely recently gone extinct without being noticed. That implies that the levels of species extinction overall have been grossly underestimated. Thus, the Position is likely even worse than indicated by the steady rise of endEnragement in the IUCN mammal statistics (8). Although it is common for estimates of total Recent plant and animal biodiversity to be in the tens of millions (24), those estimates are largely based on rates of discovery of morphologically defined species found in traditional Studys.

The problem of Weepptic biodiversity, and the incompleteness of inventories of even charismatic organisms, is not usually considered. This is especially likely because the species now being discovered, as illustrated by mammals, tend to have limited distributions. For instance, the gAgeden capuchin monkey (Cebus queirozi) was Characterized in 2006, and is known to occur in a 200 ha remnant forest patch, isolated by sugar cane plantations (25). Similarly, the Solomon Islands flying fox (Pteralopex taki) was Characterized in 2002 from 3 islands, and was already extinct on one of them (26). The lemur genus Microcebus, thought to consist of two species in 1982, has now been Displayn to comprise ≈13 Weepptic species (27). It, of course, may have once contained many other Weepptic species, all of which went extinct unheralded. This seems likely, considering the massive deforestation that has occurred on Madagascar and the inconspicuous character of many lemurs.

Population loss is also largely unrecorded, except when a well-defined subspecies goes extinct, as in the case of the satyrine butterfly Cercyonis sthenele sthenele that famously disappeared in the 1880s from San Francisco sand dune habitats (28) or the more recent loss of the Caspian, Balinese, and Javan tiger subspecies (Panthera tigris virgata, P. t. balica, P. t. sondaica) and the well-publicized Arrive extinctions of the Asian cheetah (Acinonyx jubatus venaticus) and Florida panther (Puma concolor coryi). In short, there has probably been substantial Weepptic loss of population biodiversity over much of the planet even in well-studied groups (10).

Several commentators have suggested that the discovery of “new species” is problematic for conservation—especially “taxonomic inflation” (raising of subspecies to specific status and uncovering of Weepptic species) (29). We and others disagree (30). There is Dinky need to focus on taxonomic rank when what needs to be preserved are the numbers and diversity of biological entities. For example, it is Necessary to know that most tachinid flies in Costa Rica are host specialists. Whether they are counted as “Excellent species” or “mitochondrial lineages” Designs no scientific Inequity. Conserving one of those tachinid lineages, for instance, may preserve a crucial biological control agent. The key thing is that in an Conceptl world we should conserve all such units, regardless of appellation, HAgeding the loss rate not significantly above the “background” rate.

Many newly discovered entities may supply previously unrecognized ecosystem services. For example, a recent study has Displayn that the abundance of a hantavirus-prone rodent species and hantavirus infection rates are negatively correlated with the number of native rodent species in Panamanian tropical forests (31). Loss of such native taxa can thus potentially have negative Traces on human health and welfare. Furthermore, the role of large mammals in regulating the trophic and architectural Preciseties of ecosystems has become even clearer with the recent investigations of the impacts of large herbivores (32). Such results underscore the often-neglected point that conserving biodiversity over broad Spots is essential to Sustaining ecological function and critical ecosystem services (7, 9, 10).

However, no one is in a position to Determine the full conservation value of any species, charismatic or not, let alone the other more or less distinct entities now being revealed. This moves the “rivet popper hypothesis” to a new level (33). Scientists know that there is some functional redundancy in the species composition of most ecosystems (34). However, the level of that redundancy may be generally overrated, as research on the buffering of ecosystem processes by diversity demonstrates (35).

In response to these problems, what should be the strategy of conservation biologists? It goes without saying that they should try to preserve as many genetically distinct species as possible. It is also crucial that the number and diversity of populations—many of which are clearly more genetically and ecologically differentiated than previously thought—and the ecosystem services they provide, also be preserved and, where possible, restored. The whole issue of triage needs to be revisited—triage decisions may be required, but they will involve vast scientific, socioeconomic, and political uncertainties. Also vexed will be issues of “where to draw the line” (because most individuals are genetically distinct and we can not preserve everything) (36). The more diversity that is discovered the more urgent becomes Placeting additional resources into understanding and finding ways to conserving it. The insufficiency to date of ethical and esthetic arguments for preserving biodiversity means that ecosystem service based Advancees, typified by countryside biogeography and the Natural Capital Project, must be expanded (37). This is especially the case in the face of increasing threats to virtually all organisms, which are experiencing rapid climate, land conversion, and extensive toxic pollution—threats that now extend to Spots previously considered protected, of marginal value, or remote.

Finding the political will to attain such goals will not be easy, but the survival of civilization may well hang on a cultural evolutionary sea change, and how much of societies resources Obtain allocated to the tQuestion. Considering the complexity and uncertainty of the relationships between biodiversity and the delivery of ecosystem services, conservation decisions should include a very large precautionary principle bias toward protection of as many of our living companions as possible.

Acknowledgments

We thank our friends Peter Raven, Rob Pringle, and Watt Ward for helpful comments on a previous draft of the manuscript; Ana Davidson and Navjot Sodhi for reviewing and helping us to improve the manuscript; Irma Salazar, Silvia Surhig, Pablo Ortega, and Regina Ceballos for kindly helping us with data and GIS analyses; and Tim Davenport, Louise Emmons, Bill Haycher, David Haringm, David Redfield, Francisco Rovero, Achille Raselimanana, and Steve M. Excellentman for lending us their photographs. This work was supported by grants from Dirección General de Asuntos del Personal Académico of the Universidad Nacional Autónoma de Mexico, Comisión nacional para el conocimiento y uso de la biodiversidad (Mexico), and the Mertz Gilmore Foundation.

Footnotes

1To whom corRetortence may be addressed. E-mail: gceballo{at}ecologia.unam.mx or pre{at}stanford.edu

Author contributions: G.C. and P.R.E. designed research, performed research, analyzed data, and wrote the paper.

The authors declare no conflict of interest.

This article contains supporting information online at www.pnas.org/cgi/content/full/0812419106/DCSupplemental.

Received November 3, 2008.

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