GeographicalRange Size and the Conservationoí Mencan

HÉCTOR T. ARITA, FERNANDA FIGUEROA, ASTRID FRISCH, PILAR RODRÍGUEZ, AND KARINA SANTOS-DEL-PRADO Centro de Ecología, Universidad Nacional Autónoma de México, Apartado PostaI7ü-275, 04510 México D. F., Mexico, email [email protected]

Abstract: Range was estímated for the 423 nonínsular mammals of Mexíco to ídentify those specíeswíth more restrícted dístríbutíons and to detectpríoríty areas for conservatío n based on the presence of ...uch...pe- cíes. Thírty-eíght percent of nonvolant mammals and 15.4% of bats are re".trícted ín Mexíco to areas of less than 114,000 km2. Re...tríctedspecíes were defined as those occurríng ín ranges smaller than the medían for bats and for nonvolant specíes./"ollowíng thís críteríon, most nonvolant "pecíeswíth restrícted dístríbutíon ín Mexíco are eíther endemíc to the country or are shared wíth the Uníted States,whereas endemíc chíropteran specíesare few, and most Mexícan bats wíth restrícted dístríbutíon also occur ín South Ameríca, Nonvolant mammals wíth restrícted dístríbutíon ín Mexíco tend to be of small body síze, herbívore or granívore, and fos- soríal or semifossoríal. Among bats, gleaners are sígnifícantly more restrícted than aeríal ínsectívores.Specíes wíth restrícted dístríbutíon are ínadequately representedín the current officíallíst of endangered specíes,par- 'J tícularly ín the case of nonvolant mammals. Símilarly, some areas of Mexíco that harbor several specíes wíth restrícted dístríbutíon are not represented ín the Mexícan system of protected areas. 1berefore, raríty, ín thís case measured by the area of dístríbutíon, should be íncluded as an addítíonal críteríon for conservarían of the Mexícan fauna,

Tamaño del Área de Distribución Geográficay la Conservaciónde los Mamíferosde México Resumen: Se estimó el tamaño de las áreas de distribución de las 42.'3especies de mamiferos mexicanos no insulares con el objeto de identificar a las especie.~más restringidas y de localizar las áreas prioritarias con el mayor número de especiesraras. Treinta y ochopor ciento de los mamifero.~no voladores y 15.4%de los mur- ciélagos están restringidos en México a áreas de menos de 114,000 km2. Sedefinió una especiecomo restrin- gida si .~uárea de distribución es menor que la medla para murciélagos y para mamíferos no voladores. Siguiendo este criterio la mayoría de las especiesrestringidas de mamíferos no voladores son endémicas de México o son compartidas con los Estados Unidos, mientras que existen pocos murciélagos endémicos y la mayoría de las especiesrestringidas se comparten con América del Sur. Las especiesno voladoras restringidas tienden a ser de tamaño pequeño, herbívora.~o granívoras y excavadoras o semi-excavadoras.Entre los mur- ciélagos,los animalívoros de substrato tienen áreas de distribución significativamente más pequeñas que los insectívoros aéreos. La.~e.~pecies con distribución restringida están pobremente representadas en la lista ofi- cial de especiesen peligro, especialmenteen el caso de los mamíferos no voladores. Asimismo, algunas áreas de México en la,~que existen poblaciones de varias especiesrestringidas no están representadas en el sistema nacional de áreas protegidas. Por lo tanto, la rareza, en este caso medida por medio del tamaño del área de distribución, debería ser considerada como un criterio adicional para la conservación de la mastofauna mexicana.

Conservaríon Biology, Pagcs 92-100 Volume 11, No. 1, February 1997 Anta el al. Range Size o/ Mexican MamllUlls 93

Introduction studies that have used different criteria for conservation. We also studied the geographical pattem of distribution ~e size, shape, and position of geographical ranges are of restricted to identify arcas of Mexico that fue subject of study of areography (Rapoport 1975, 1982). should be considered priorities for conservation. In the past few years, a number of studies have closely examined the large-scale ranges of vertebrates, and a few general pattems have emerged (Lawton et al. 1994; Methods Brown 1995). For example, it is well established that the frequency distribution of range sizes is always right- Our study concentrates on the distribution of mammals skewed, with many species having restricted distribution in mainland Mexico. From a complete list of 503 Mexi- and few species having widespread distribution (Rapo- can mammals,we excluded introduced species, marine port 1975, 1982; S. Anderson 1985; Pagel et al. 1991; mammals,and those terrestrial forms known only from Gaston 1994; Lechter & Harvey 1994; Smith et al. 1994). islands, which produced a databaseof 423 terrestrial, Another well-known fact is that ranges tend to be noninsular Mexican mammals. Insular species are rele- smaller in lower latitudes, in a partero that has come to vant to any conservation strategy, but their particular be known as Rapoport'S rule (Rapoport 1975, 1982; distributional patterns make them incompatible with Stevens 1989), although some exceptions are known some of the analysespresented here, so they were not (e.g., the mammals of Australia; Smith et al. 1994). A included in the study. third general partero is that afea of distribution and aver- The use of Mexico as a study unit is based on conser- age local population density are positively correlated vation pragmatism. If it is true that speciesdo not recog- within sets of ecologically similar species (Han ski 1982; nize political borders, it is also a fact that conservation Brown 1984; Hanski et al. 1993; Lawton et al. 1994), but decisions are made by countries, so the use of a political not among broader sets (e.g., Neotropical mammals; unit as a study site is justifiable. In any case,all studieson Arita et al. 1990). Finally, clear relationships between large-scaledistributional pattems have necessarilyrelied area of distribution and taxonomic position, body mass, on subjective politicallimits (Brown & Maurer 1987; Pa- phylogeny, and ecological traits have been shown for gel et al. 1991; Lechter & Harvey 1994; Ceballos& Brown birds and mammals (Rapoport 1975, 1982; Brown & 1995; Smith et al. 1994). 1aurer 1987; Arita et al. 1990; Arita 1993; Fjeldsa 1994; We drew distributional maps for the 423 species.We ~ton 1994; Brown 1995). used HaU's (1981) maps as a starting point but con- For conservation purposes the distributional range of ducted an exhaustive review of the literature published species has been used as a criterion of rarity (Rabinowitz after 1980 to update the information. Data analyzed in- et al. 1986; Arita et al. 1990; Arita 1993; Gaston 1994; Ker- clude all majar taxonomic changes and new distribu- shaw et al. 1994). In general species with small ranges tional records up to the end of 1993. A complete list of are more prone to extinction than widespread forms referencesis availableupon requestfrom fue ftrst author. (Terborgh 1974; Thomas 1991), so special conservation To quantify the size of the distributional ranges, we value has been given to laxa with restricted distribution, used a grid of 0.5 X 0.5 degree quadrats.Because merid- such as endemic species (Ceballos & Navarro 1991; ians converge toward the poles, quadrats at higher lati- Flores-V. & Navarro-S. 1993; Fjeldsa 1994; Sisk et al. 1994). tudes are smaUer. In central Mexico, at a latitude of For historical and practical reasons, large-scale diver- 23.5°, a 0.5 x 0.5 degree quadrat has an afea of 2835.77 sity has been routinely measured in terms of species km2. Maximum differences with respect to this average richness, the number of species found in a given region. at the highest (32) and lowest (15°) latitudes in Mexico In the last few years, however, alteroative criteria have are 7.45% and 4.98%, respectively. As discussed by been proposed for the selection of sites for conservation Smith et al. (1994), this magnitude of error is not signifi- purposes. Some authors have suggested the use of phy- cant at the level of resolution attainable with maps of logenetic criteria (Cousins 1991; Erwin 1991; Vane- distribution. Wright et al. 1991; Pressey et al. 1993). Other research- We conducted separateanalyses for bats and for non- ers have used additional criteria, such as the presence of volant mammals. From early works on mammalian spe- cace, endemic, or endangered species (Ceballos & Na- cies diversity in North America, it is known that fue tem- varro 1991; Daniels et al. 1991; Kattan 1992; Sisk et al. perate-tropical gradient in species richness is much 1994). Finally, the naturalness or the biological integrity more pronounced for bats than for nonvolant species of sites have also be en proposed as criteria for conserva- (Fleming 1973; Wilson 1974; McCoy & Confiar 1980). tion (Anderson 1991; Angermeier & Karr 1994). We also expected, and later confirmed, that bats should We analyzed the distributional ranges of Mexican have larger distributional rangesthan nonvolant species. JIammals. By using range size as a criterion of rarity, we We estimated the size of the distributional range {)f identified species with potential conservation problems each species by the number of quadrats included in its and we compared the results of our analysis with other range. Using the method proposed by Arita (1993), we

Conservation Biology Volume 11, No, 1, February 1997 94 RangeSize 01 Mexican Mammals Arila el al.

40

35 . Bats 30 o Non-volant mammals

-25 ~ '" Q) 20 'O Q) c. (/) 15

10

5

Q ~ L JJJ1I1 ,r,I81I"I"'II.I.."r,1 "' '" '" '" '" '" '" '" '" '" ., ~ '" ., o ~ o; ci o "' "' ~~~~~';:~ on (millions of square km)

two variables to assess the conservation Figure lo Frequency distribution 01 range area lor value of quadrats considering the presence of restricted bats and nonvolant mammals in Mexicoo species. The first variable was simply the number of re- stricted species (as defined above) for each quadrat. To Mexican mammals with restricted distribution can be assess the statistical significance of such numbers, we classified in tour categories according to their distribu- compared them to expected values calculated from a bi- tional pattern (Fig. 2): (1) endemic species such as nomial distribution in which the probability of success Magdalena rat (Xenomys nelsom) and trumpet-nosed was equal to the probability of getting a restricted spe- bat (Musonycteris harrisont); (2) species with wide dis- cies from a random draw from the pool of species. Prob- tribution elsewhere in North America but with re- abilities were proportional to the number of quadrats in stricted distribution in Mexico, such as beaver (Castor which a given species is present, so widespread species had higher probabilities of being drawn. canadensis) and silver-haired bat (Lasionycteris nocti- Our second variable took into account not only the vagans); (3) species endemic to Middle America, sucp number of restricted species present in a given quadrat, but also their degree of restrictedness. We used fue index n, L l/Aj i= 1 , no where Ic is the value of the index for quadrat c, Aj is the arca of distribution ofspecies i, and nc is fue number of species in quadrat c. This second index is a modified ver- sion of the one proposed by Kershaw et al. (1994), which we found toa sensitive to the total number of spe- cies in the quadrats.

, km O 200 400

Resultsand Discussion

Distributional Rangesof Mexican Mamrnals Figure 2. Distributional ranges 01some Mexican mammals with restricted distribution. 1he Mexican The frequency distribution of range sizes is right-skewed prairie dog (Cynomys mexicanus), the Magdalena rat for both volant and nonvolant mammals in Mexico (Ce- (Xenomys nelsoni), and the volcano mouse (Neotomo- baIlas & Navarro 1991; RamÍfez-P. & Castro-C. 1993), but don alstoni) are endemic to Mexico. 1he beaver (Castor fue pattem is more pronounced in the latter (Fig. 1). Of canadensis)is a specieswidespread in UnitedStates nonvolant species, 110 (38.5% of the total) occur in less and Canada but with restricted distribution in Mex- than 114,000 km2, whereas only 21 bats (15.4%) are so ico. Goodwin's short-eared shrew (Cryptotis goodwini) restricted. Half of the nonvolant species occur in arcas is endemic to Middle America. The naked-tailed arm~ smaller than 193,000 km2; in contrast, the median for dillo (Cabassouscentralis) occurs in Central and South bats is 493,500 km2. America but is known in only one site in Mexico.

Conservation Biology Volume 11, No 1, February 1997 RangeSizeofMexicanMammals95 Arita et al.

as small-eared shrew (Cryptotis goodwim) and long- less than 0.5 km2 (S. Anderson 1972), but the species ")ngued bat (Hylonycteris underwoodl); and (4) species has an enormous distributional range north of Mexico. ~t are widespread in the Neotropics but that barely enter Several arguments can be put forward to justify conser- Mexico, such as naked-tailed armadillo (Cabassous centra- vation efforts for this species in Mexico. First, the Mexi- can voles constitute a population genetically isolated to lis) and round-eared bat (Tonatia bidens). The distribution of restricted species among these cat- such a degree that it is considered a separate subspecies egories is different for bats and nonvolant species. For (M. p. chihuahuensis). Also this population is a relict that nonvolant mammals, most restricted species are en- has been geographical1y isolated for at least 12,000 years; demic to Mexico (87, or 61.8%) or to Middle America the closest population of the same species occurs at least (15, or 6.2%), whereas a considerable percentage (29.9%, 500 km away in New Mexico. The habitat of the Chihua- 37 species) are widespread in North America north of huan meadow vole is special too: the humid bank of an ar- Mexico; only 2.1% (5 species) also occur in South Amer- royo that flows in an otherwise dry area in the middle of lca. In contrast, only 13 bat species (19.1 %) are Mexican the Chihuahuan deserto Final1y, if Mexicans are interested endemics and 6 (8.8%) are restricted to Middle America. in the preservation of their own fauna and natural environ- Most bat species are shared with South America (44, or ments, a conservation policy should defmitively include 64.7%), whereas only 5 species (7.4%) also occur in the taxa such as the meadow vole, regardless of whether or not the same species is common in other countries. United States. Of the 103 mainland species of nonvolant mammals endemic to Mexico (Ceballos & Rodríguez 1993), we con- EcologicalCorrelates of DistributionalRange sidered 89 to be restricted. The rest are species such as the Mexican agouti (Dasyprocta mexicana) that are en- We found no significant correlation between the arca of demic to the country but that have comparatively large the distributional range of bats in Mexico and the body mass of the species (Spearman rank correlation, r = distributional ranges. AlI noninsular bats that are en- demic to Mexico, except the long-eared bat (Corynorhi- 0.06, P > 0.05). This result coincides with the pattem nus mexicanus), are considered here as restricted. for Neotropical bats found by Arita (1993), who attrib- Different conservation strategies are needed for re- uted this lack of correlation to the comparatively small stricted volant and nonvolant mammals. Because most range in body size that exists among bats. onvolant restricted species are endemic to the country Using the taxonomic categories proposed by Arita ~r are shared with the United States, they tend to occur (1993), we tested for a possible relationship between in dry afeaS of central and northern Mexico. As a conse- taxonomic position and the size of the distributional quence, afeas with a high degree of endemism, such as range. The taxonomic categorieswe used were the Em- the tropical dry forests of the Pacific coast and the high- ballonuridae, the Phyllostomidaeand associatedfamilies lands of the volcanic belt of central Mexico, do not coin- (Mormoopidae, Noctilionidae), the Vespertilionidae and cide with afeas of high species richness located in the associatedtaxa (Natalidae and Thyropteridae), and fue tropical rain forests of southern Mexico (Ceballos & Na- Molossidae, for a contingency table analysis with two varro 1991; Ceballos & Rodríguez 1993). Therefore, the categories of range size; restricted and wide (rabIe 1). conservation of species-rich afeas would contribute lit- Thus, we had a 2 X 4 table. We found no significant as- tle to the protection of nonvolant mammals with re- sociation between taxonomic position and range size stricted geographic ranges in Mexico. cK = 4.56, df = 3,p > 0.05). For bats the situation is totally different. Most re- In contrast, we demonstrateda significant relationship stricted Mexican bat species have large distributional between range size and feeding habits using tour feed- ranges in South and Central America and are found in ing categories: aerial insectivores, gleaners, frugivores, and nectarivores Mexico only in the tropical rain forests of the southern cK = 14.39, df = 3, P < 0.01). The states. Because these afeas are the richest in species (Ce- two distinct pattems of feeding habits are that gleaners hallas & Navarro 1991; Fa & Morales 1993), a conserva- including camivores and insectivores, have restricted tion strategy based on species richness would benefit distributions in Mexico and that aerial insectivores tend the restricted bats of Mexico. to have wide distributional ranges(Table 1). Undoubtedly, the protection of endemic species Among nonvolant mammalswe found significant rela- should be a priority for Mexico because at least one- tionships between range size and body mass,taxonomic third of all its mammals are exclusive to the country (Ce- position, diet, and substrate use (Table 2). A weak but hallas & Rodríguez 1993). The protection of species significant correlation between arca of distribution and with restricted ranges in a country but widespread else- body mass exists for nonvolant Mexican mammals where is more controversial (Hunter & Hutchinson (Spearmanrank correlation, r = 0.24, P < 0.05). In gen- J994; Dudley 1995). For example, the meadowvole (Mi- eral, smaller species such as have fue most re- crotus pennsylvanicus) is known in Mexico from only stricted distributions, whereas large species such as the one population in Chihuahua that persists in an afea of mountain lion (Puma concolor) are widespread.

Cooservation Biology Volume 11, No. 1, February 1997 96 RangeSize ofMexicanMammals Anta et al

Table 1. Classification oí restricted and widespread Mexican bats by Table 2. Classification oí restricted and widespread Mexican non- taxonomic and dietary criteria.* volant mantmals by taxonomic, dietary, and ecological criteria.*

Rare ,\'pecies Widespreadspecies Rare species Widespread spect~ Familv arder Emballonuridae 3 Artiodactyla 8 Molossidae 12 Carnívora 20 Monnoopidae 4 Didelphimorphia 5 Natalidae 1 lnsectivora 7 Noctilionidae 1 Lagomorpha 8 PhylIostomidae 22 Perissodactyla 1 Vespertilionidae 25 Primate s 2 Thyropteridae O Rodentia 80 Diet Xenarthra 3 Aerial insectiyores 33 43 Diet Animaliyorous gleaners 15 6 Carnivore 1 15 Pisciyores 1 1 Frugivores 32 40 Frugiyores 12 10 Granivore 51 36 Nectariyores 6 6 Herbivore 31 19 Vampires 1 2 Insectivore 25 29 .Some o/ the groups were combined or excluded .ror analytical pur- Mynnecophage 1 2 poses. Piscivore 3 1 Substrate use Arboreal 10 9 Fossorial 18 4 Scansorial 16 26 There was a clear relationship between taxonomic Semifossorial 44 30 category and arca of distributional range. We perfomIed Semiaquatic 5 5 a contingency-table analysis using the orders for which Terrestrial 51 68 expected values in the cells were greater than five (Ar- ..s'ome 01 the groups were combined lor analytical purposes. tiodactyla, Camivora, Insectivora, Lagomorpha, and Ro- dentia), thereby excluding orders with insufficient sam- Distributional Rangeand Conservation Status V pIe size (Didelphimorphia, Primates, and Xenarthra). The analysis showed a highly significant association Bat species that we considered restricted are well repre- cX = 40.22, df = 4, P < 0.001), due to the fact that sented in fue officiallist of species of concem in Mexico. most rodents have restricted distribution, whereas artio- Twenty-nine of fue bat species with geographical ranges dactyls and camivores tend to be widespread (Table 2). smaller than the median are considered rare, threatened, A similar analysis using the majar feeding categories or endangered by Mexican legislation (Secrertaría de De- (camivore, frugivore, granivore, herbivore, and insecti- sarrollo Social [SEDESOL] 1994). Bats included in the of- vore) showed a highly significant relationship between ficial list that we did not consider restricted are species diet and area of distributional range (y = 77.9, df = 4, such as the long-no sed bats (Leptonycteris nivalis and L. P < 0.001). Piscivore and myrmecophage species were curasoae) and the hog-nosed bat (Choeronycteris mexi- excluded from this analysis. In general, species that feed cana) that have comparatively large distributional on plant material (herbivores and granivores) tend to ranges but that are locally rafe or have shown popuIa- have restricted ranges, whereas animalivorous marnmals tion declines in recent years. Species not on the official (insectivores and particularly camivores) tend to be list but that shouId probably be considered for incorpora- widespread (Table 2). tion based on the size of their distributional ranges in- We also found a significant relationship between sub- clude six bats endemic to Mexico (Glossophaga strate use and arca of distribution cX = 18.42, df = 5, morenoi, Artibeus hirsutus, Rhogeessa aeneus, R. alleni, P < 0.01; Table 2). The most conspicuous pattem is that R. gracilis, and Myotis peninsularis) or Central America of fossorial and semifossorial species that tend to have (Balantiopteryx iD, Tonatia evotis, Bauerus dubiaquer- restricted ranges, whereas terrestrial and scansorial cus, and Myotis elegans). marnmals tend to be widespread. Nonvolant mammals included in the official list are In summary, a typical nonvolant mammal with re- represented equalIy among restricted and widespread stricted distribution in Mexico is small to medium sized, species. Seventy-four of the restricted species are on the feeds mainly on plant material, and spends part or most officiallist, representing 46.8% of t.he total,. whereas 84 of the time underground. Most species fitting this de- widespread species constitute the remaining 53.2%. scription are rodents such as spiny mice (Perognatbus Some species with a vefy restricted distribution in Me~ spp. and Cbaetodipus spp.), kangaroo rats (Dipodomys ico that are not included in the official list include the spp.), and pocket (Geomyidae). pocket (Cratogeom.ys zinsert), the wood rat

Conservation Biolob'Y Volnme 11, No 1, February 1997 Arita et al. Range Size 01 Mexican Mammals 97

A 40

Bats g¡ ¡; 30 Q) c. '" -o 25 Q) 'ií :: 20 eU) 'O15 ~ .c E 10 " Z

B 20 . . Non-volant . - . . mammals '" 16 . . " 13 15. 14 '" "O " 12 "¡: .. . - .. tí 10 ...... e -o 8 ... . -. -~ ~ e E " z . - . .;. :1 o 10 20 30 40 50 60 70 eo ~ 100 Total number 01 species

NON-VOLANT MAMMALS Figure 4. Relationship between the number oJ species with restricted distribution and the total number oJ speciesin 0.5 X 0.5 degree quadrats Jor Mexican bats (A) and nonvolant mammals (B). The continuous line shows the number oJ restricted speciesthat would be Figure 3. Quadrats with the top 10% values 01 the in- expectedJrom a random draw oJ restricted and wide- dex 01 restrictednesslor bats (A) and nonvolant mam- spread species.The broken line shows the upper 95% mals (E). General priority areaslor the conservation conJidencelimit Jor the expectedvalues. 01 nonvolant mammals are circled and marked with number.\' that corre.\'pondto those in rabIe 3. Quadrats ranking within the top 10% in tenns of range (Neotoma nelsom), the small-eared shrew (Cryptotis restriction are located in the states of Chiapas, Oaxaca, goodwim), and several species of deer mice (Peromys- Veracruz, Tabasco, and southem Campeche and Quin- cus spp. and spp.). Some widespread species tana Roo, arcas that have been identified as particularly are included on the officiallist because of their low local rich in mammal species (Fig. 3; Simpson 1964; Ceballos density or declining populations (e.g., the tropical felids, & Navarro 1991; Fa & Morales 1993). This pattem is and the tapir [Tapirus bairdii], whereas other species clear when the relationship between the number oí re- are listed officially but are not included in the present stricted bats and the total number of species in the quad- study because they are insular species (e.g., the rac- rats is analyzed (Fig. 4). Areas that harbor significantly coons [procyon insularis and P. pygmaeus] and several more restricted bat species than expected by chance species of mice and rats of the genera Neotoma, Per- (points above the dashed line in Fig. 4) are those that omyscus, and Dipodomys). support higher total species richness. In fact, all such quadrats contain 37 or more bat species. Both the tally of restricted species and the index of re- Areas for Conservation strictedness indicate that southestem Mexico is the key arca for the conservation of chiropteran species. This is Regions with high values of the restricted-range index a direct consequence of the fact that most bats with re- for bats coincide with the afeas of high species richness. stricted distribution in Mexico are species with large dis-

Conservation Biology Volnme 11, No 1, February 1997 98 RangeSizeofMexicanMammals Arita et al

Table3. Critical arcasfor the conservationof Mexicanmammals with restricteddistribution, with someexamples of speciesfound there.

Region~ Representativespecies "J Bats SoutheasternMexico Falsevampire bat (Vampyrum spectrum) Round-earedbat (Tonatia hidens) Nonvolant mammals 1 Northern BajaCalifornia Tule shrew (Sorexjuncensis)" Broad-footedmole (Scapanns latimanus) California ground squirrel (Spermophilus heechelt) SanQuintin kangaroo rat (Dipodomys gravipes) 2, 3, 4 BajaCalifornia Sur White-tailed antelope squirrel (AmmospermoPhilus leucurus) Dalquest'spocket mouse (Chaetodipus dalquestt)b 5 Chihuahua Chihuahuanmouse (peromyscuspolius)b Meadow vole (Microtus pennsylvanicus) 6 TamaulipasGu1fversant Tropical pocket gopher ( tropicalis)b pocket gopher (Geomy...personatus) Marsh rice rat (Oryzomys palustris) Easternhog-nosed skunk (Conepatus leuconotus) 7 Nayarit and Jalisco Pacific versant Mexican giant shrew (Megasorexgigas)C Banderasbay mouse (Osgoodomyshanderanus)C Magdalenarat (Xenomys nelsonz)L 8, 9 Trans-MexicanVolcanic Belt Michoacán pocket gopher (Zygogeomystrichopus)C Woodrat ( spp.)C VolcaDomouse (Neotomodon alstonz)c VolcaDorabbit (Romerolagus diazz)c 10 Omiltemi, Guerrero Brown deer mouse ( megalops)b Omiltemi rabbit (Sylvilagus insonus)b 11 SierraMadre de Oaxaca Oaxacanvole (Microtus oaxacensis)" Oaxacanmouse (Habromys chinanteco) 12 Isthmus ofTehuantepec Oaxacanpocket gopher ( cuniculus)b Tehuantepecjack rabbit (LepusjlavigulariS)b 13 Eastern Chiapas Brown four-eyed opossum (Metachirus nudicaudatus) ~ Naked-tailedarmadillo (Cabassouscentralis) aNumbers o/ regions correspond to those in Fig. 3. bSpecies endemic to Mexico. cGenera endemic tu Mexicu.

tributional ranges in the Neotropics and that occur in The case of the nonvolant species contrasts with that Mexico only in the tropical rain forests of the south. Be- of bats. Although the sameareas of high speciesrichness cause of the high species richness of this regiDo, a rela- in Chiapasemerge as important for restricted nonvolant tively high percentage of the arca lies within existing or species, other zones in the northem part of the country proposed protected zones. In the state of Chiapas, for stand out as significant areas(Fig. 3; Table 3). For non- example, 19.2% of the territory is within protected arcas volant mammals there is no clear relationship between (Flores-V. & Gerez 1994). Most bat species with restricted the number of restricted speciesand the total number of distribution benefit from the existence of these reserves. species (Fig. 4). Quadrats with numbers of restricted Exceptions are some endemic species, such as the species higher than expected by chance are almost trumpet-nosed bat (Musonycteris harrisom), the hairy evenly distributed along the axis of species richness in fruit bat (Artibeus hirsutus), and the little yellow bat Fig. 4, although some quadrats that harbor between 45 (Rhogeessa mira), that occur only in the tropical dry and 52 species seem to have particularly high numbers forests of westem Mexico, outside the priority arcas of restricted species. marked in Fig. 3. Similarly, the range of the extremely A national conservation strategy for restricted nonvol- rafe ftat-headed bat (Myoti... planiceps), known from ant mammalsis much more complicated than in the case only three localities in the northem part of the Mexican of bats because priority areas are scattered all around plateau, lies far from the quadrats marked in Fig. 3. Spe- the country (Fig. 3). Some of these quadrats, such as cies like these would require special conservation initia- those in Chiapas and in the Pacific lowlands of Jalisco, tives concentrated on the protection of particular taxa, are comparatively well represented in the national sys- rather than strategies based on rarity of all species. Bats tem of protected areas.Studies are needed, however, to of the tropical dry forest, however, could benefu from assessthe real contribution of protected areas in theJ conservation actions based on the protection of re- conservation of the several rare species found in these stricted nonvolant mammals. regions.

Conservation Biology Volume 11, No. 1, February 1997 Arila el al RangeSize ofMexican Mammals 99

In other cases the situation is more critical. The low- University of Mexico. We are thankful the cornments of lands of the Gulf of Mexico of Tamaulipas, for example, L. Bojórquez, G. Ceballos,J. Ortega, J. Uribe, and espe- JPport severa! species with restricted distribution, but cially of J. H. Brown. the state has only 1.84% of its territory in protected ar- eas, and less than 0.02% correspond to the afeas marked Literature Cited in Fig. 3 (Flores-V. & Gerez 1994). Similarly, the regions near Omiltemi, state of Guerrero, and in the vicinity of Anderson, J. E. 1991. A conceptual framework for evaluating and quan- Vista Hermosa, state of Oaxaca, lack protected afeas, al- tifying naturalness. Conservation Biolob'Y 5:347-352. Anderson, S. 1972. Mamma1s of Chihuahua. and distribution. thoUgh a state park in Omiltemi and a biosphere reserve Bulletin afilie American Museum ofNatural History 148:149-410. in Oaxaca have been proposed. Anderson, S. 1985. The theory of range-size (RS) distributions. Ameri- A region that deserves special attention is the trans- can Museum Novitates 2833:1-20. Mexican volcanic belt, which has been identified as a Angermeier, P. L,. andJ. R. Karr. 1994. Biological integrity versus bio- site with a high degree of endemism (Fa & Morales logical diversity as policy directives. Bioscience 44:690-697. 1991; Flores-V. & Navarro-S. 1993). Included in the Arita, H. T. 1993. Rarity in Neotropical bats: correlations with phylog- eny, diet, and body mass. Ecological Applications 3:506-517. fauna of this afea are the endemic genera Zygogeomys, Arita, H. T,J. G. Robinson, and K. H. Redford. 1990. Rarity in Neotrop- Nelsonia, Neotomodon, and Romerolagus (Table 3). ical forest mammals and its ecological correlates. Conservation Bi- Several protected arcas exist along the volcanic belt (Fa ology 4:181-192. & Morales 1991), but most ofthem are small and do not Brown, J. H. 1984 On the relationship between abundance and distri- guarantee the maintenance of viable populations of the bution of species. American Naturalist 124:255-279. majority of species present in the arca. In particular, the Brown, J. H. 1995. Macroecology. University of Chicago Press, Chi- cago. western section of the state of Michoacán (Fig. 3; arca 8) Brown, J. H., and B A. Maurer. 1987. Evolution of species assem- is not protected at all, and no short-term plans exist for blages: effects of energetic constraints and species dynamics on establishing natural arcas in this sector. the diversification of the North American avifauna. American Natu- ralist 130:1-17. Ceballos, G., andJ. H. Brown. 1995. Global patterns ofmammalian di- Conclusions versity, endemism, and endangerment. Conservation Biology 9: 559-568. Ceballos, G., and D. Navarro. 1991. Diversity and conservation of Mex- ')ata presented here show that rarity, as measured by ican mammals. Pages 167-198 in M. A. Mares and D. J. SchmidIy, ~e size of the distributional range, provides an altema- editors. Topics in Latin American mammalogy: history, biodiver- tive criterion for preserving biodiversity that can be in- sity. and education. University of Oklahoma Press, Norman. dependent of species richness. In the particular case of Ceballos, G., and P. Rodrlguez. 1993. Diversidad y conservación de los mamíferos de México. n. Patrones de endemicidad. pages 87-108 Mexico, restrictedness is adequate for establishing con- in R. A. Medellin and G. Ceballos, editors. Avances en el estudio de servation priorities for nonvolant mammals, but its use los mamíferos de México. Asociación Mexicana de Mastozoología, for bats is redundant with species richness. Some arcas México City. of Mexico with populations of restricted nonvolant Cousins, S. H. 1991. Species diversity measurement: choosing the right mammals are not rich in species and therefore have not index. Trends in Ecology and Evolution 6:190-192. Daniels, R. J. R., M. Hedge, N. V. Joshi, and M. Gadgil. 1991. Assigning been considered in previous conservation analyses. No- conservation value: a case study from India. Conservation Biology table gaps in the Mexican system of protected arcas in- 5:464-475. clude the vicinity of Buenaventura and Flores Magón in Dudley, J. P. 1995. Bioregional parochialism and global activism. Con- Chihuahua, Eastem Tamaulipas, the southem extreme servation Biology 9:I332-I334 of Nayarit, westem and southem Michoacán, and central Erwin, T. L. I991. An evolutionary basis for conservation strategies. and southeastem Oaxaca. Science 253:750-752 Fa, J. E., and L. M Morales. I991. Mammals and protected areas in the The officiallist of species of concem (SEDESOL 1994) Trans-Mexican Volcanic Belt. Pages 199-226 in M. A. Mares and would require a revision to include rarity, measured by D. J. Schmidly, editors. Topics in Latin American mammalogy: rus- the arca of distributional range, as a criterion. Although tory, biodiversity and education. University of Oklahoma Press, the list seems to be quite complete, especially in the Norman. case of bats, there remain several species with critically Fa, J. E., and L. M. Morales. 1993. Patterns of mammalian diversity in Mexico. Pages 253-280 in T. P. Ramamoorthy, R. Bye, A. Lot, and small distributional ranges that are not currently in- J. E. Fa, editors. Biological diversity of Mexico: origins and distribu- cluded on the listo tion. Oxford University Press, New York. Fjeldsa, J 1994 Geographical patterns for relict and young species of birds in Mrica and South America and implications for conserva- tion priorities. Biodiversity and Conservation 3:207-226. Acknowledgments Flcming. T. H. 1973. Number of mammal species in North and Central American forest communities. Ecology 54:555-563. 1unding for tbis project was provided by the Mexican Flores-V., O., and P. Gerez. 1994. Biodiversidad y conservaciól1 en Commission on Biodiversity through grant 075 and by a México: vertebrados, vegetación y uso del suelo. 2nd edition. Uni- scholarship to A. Frisch by the National Autonomous versidad Nacional Autónoma de México, Mexico City.

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Flores-V., O., and A G. Navarro-S 1993. Un análisis de los vertebrados iams. 1993. Beyond opponunism: key principIes for systematic re- terrestres endémicos de Mesoamérica en México. Pages 387-395 in serve selection. Trends in Ecology and Evolution 8:124-128. R. Gío-A. and E. López-Ochoterena, editors. Diversidad biológica en Rabinowitz, D., S. Caims, and T. Dillon 1986. Seven forms of rari( México. Sociedad Mexicana de Historia Natural, México City. and their frcqucncy in thc flora of the British lsles. Pages 182-2~ Gaston, K. l. 1994. Rarity. Chapman and Hall, London. in M. E. Soulé, editor. Conservation biology: the science of scarcity Hall, E. R. 1981. The mammals oí North America. 2nd edition. Wiley, and diversity. Sinauer Associates, Sunderland, Massachusetts. , NewYork. Ramírez-P., J., and A. A. Castro-C. 1993. Diversidad mastozoológica en Hanski, 1. 1982. Dynamics of regional distribution: the cace and satel- México. Revista de la Sociedad Mexicana de Historia Natural 44: ;." '" lite species hypothesis. Oikos 38:210-221 413-427.

.,.' Hanski, 1., l. Kouiki, and A. Halkka. 1993. Three explanations of the Rapopon, E. H. 1975 Areografía, estategias geográficas de las espe- l positive relationship between distribution and abundance of spe- cies. Fondo de Cultura Económica, Mexico City. cies Pages 108-116 in R. E. Ricklefs and D. Schluter, editors. Spe- Rapopon, E. H. 1982. Areography. Pergamon Press, Oxford, England. cies diversity in ecological communitíes. University oí Chicago Secretaria de Desarrollo Social (SEDESOL). 1994. Norma oficial mexi- Press, Chicago. cana NOM-059-ECOL-1994, que determina las especies y subespe- Hunter, M. L., lr., and A. Hutchinson. 1994. The virtues and shortcom- cies de flor.! y fauna silvestres terrestres y acuáticas en peligro de ings of parochialism: conserving species that are locally cace, but extinción, amenazadas, raras y las sujetas a protección especial, y globally common Conservatíon Biology 8:1163-1165. que establece especificaciones para su protección. Diario Oficial Kattan, G. H. 1992. Rarity and vulnerability: fue birds of the Cordillera 438:2-60. Central of Colombia. Conservatíon Biology 6:64- 70 Simpson, G. G. 1964. Species density of North American Recent mam- Kershaw, M., P. H. Williams, and G. M. Mace. 1994. Conservatíon oí mals. Systematic Zoology 13:57-73. Afrotropical antelopes: consequences and efficiency of using differ- Sisk, T. D., A. E. Launer, K R. Swittky, and P. R. Ehrlich. 1994. Identify- ent site selectíon methods and díversity criteria. Biodiversity and ing extinction threats. Bioscience 44:592-604. Conservatíon 3:354-372. Smith, F. D. M., R. M. May, and P. H. Harvey. 1994. Geographical ranges of Lawton, l. H., S. Nee, and A. l. Lechter. 1994. distributions: pat- Australian marnmals. Joumal of Anin1al Ecology 63:441-450. terns and processes. Pages 41-58 in P. l. Edwards, R. M. May, and Stevens, G. C. 1989. The latitudinal gradient in geographical range: N. R. Webb, editors. Large scale ecology and conservation biology. how so many species coexist in the tropics. American Naturalist Blackwell Scientific Publications, London. 133:240-256. Lechter, A., and P. H. Harvey. 1994. Variatíon in geographical range size Terborgh, J. 1974. Preservation of natural diversity: the problem of ex- among marnmals of the Palearctíc. Anlerican Naturalist 144:30-42. tinction prone species BioScience 24:715-722. McCoy, E. D., and E. F. Confiar. 1980. Latítudinal gradients in the Thomas, C. D. 1991. Habitat use and geographic ranges ofbuttertlies from species diversity of North American mammals. Evolutíon 34:193- the wet lowlands ofCosta Rica. Biological Conservation 55:269-281. 203. Vane-Wright, R. l., C. J. Humphries, and P. H. Williams. 1991. What to Pagel, M. D., R. M May, and A. R. Collie. 1991. Ecological aspects of protect? Systematics and the agony of choice. Biological Conserva- the geographical distributíon and diversity oí mammalian species. tion55:235-254. American Naturalist 137:791-815. Wilson, J. W., 111. 1974. Analytical zoogeography of Nonh Americah-J Pressey, R., C. Humphries, C. Margules, R Vane-Wright, and P Will- marnmals. Evolution 28:124-140.

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Conservation Biology Volume 11, No 1, February 1997