Abstract
The status of the arboreal squirrels of Mexico was analyzed as a model taxon to elucidate the urgent need that exists worldwide to allocate more funding and research effort to less charismatic species. To accomplish this, we surveyed the literature to review their diversity and present distribution, state of scientific knowledge, and conservation status. We also examined diversity patterns and threats to their persistence. There are currently 14 recognized species, of which four are endemic to the country, with the states of Chiapas and San Luis Potosí possessing the greatest diversity. Presently, seven species are federally listed under some category of risk in Mexico. Our survey yielded only 37 peer-reviewed publications, revealing that a critical dearth of information still exists on the arboreal squirrels of Mexico. We found that states with a greater diversity of arboreal squirrels also have a higher annual wood production, possibly posing a serious threat to their persistence. A common threat to all species is habitat loss caused by deforestation with annual rates >1.0% in the country. Like other less charismatic species in the world, information from local populations is needed to establish suitable regional plans to conserve species facing specific anthropogenic threats.
Introduction
Habitat destruction is widely recognized as the most conspicuous and pervasive threat to global biodiversity (Zedler et al. 2001, Jha et al. 2005, Mendoza et al. 2005). However, extinction rates are more severe in the tropics, given the high species richness found in these habitats (Bradshaw et al. 2009, Pyron and Burbrink 2009), and the economic, social, and political problems faced by countries at these latitudes (Mares 1986). Nonetheless, suitable plans to conserve biodiversity require a variety of information, ranging from human population trends and major land ownership patterns, to environmental and biological information on conservation targets (Groves et al. 2002). Unfortunately, because of insufficient funding and support, research attention has focused mainly on charismatic and flagship species, whereas “less charismatic” species often remain poorly studied and more vulnerable to anthropogenic threats (Garnett et al. 2003, Barua et al. 2011).
The group of arboreal squirrels (Rodentia: Sciuridae) comprises 180 species of tree (n=136) and flying (n=44) squirrels worldwide, with the greatest diversity and endemism found in the tropics (Thorington and Hoffmann 2005, Koprowski and Nandini 2008). Because of their dependence on mature forests that provide seeds for food, tree cavities and canopies for nests, and stems and canopies for launch sites, arboreal squirrels may be excellent indicators of forest condition (Koprowski and Nandini 2008). However, compared with other charismatic and flagship species [e.g., brown bear – Ursus arctos (Linnaeus 1758), gray wolf – Canis lupus (Linnaeus 1758), and giant panda – Ailuropoda melanoleuca (David 1869)], arboreal squirrels have received little attention worldwide, resulting in a dearth of information on their ecology, and with about 73% (n=129) of the species listed under some category of risk by the International Union for Conservation of Nature (IUCN) (Koprowski and Nandini 2008, IUCN 2011). These critical knowledge gaps, together with high deforestation rates worldwide (Mares 1986, Food and Agriculture Organization (FAO) 2010), pose serious threats to the conservation of arboreal squirrels particularly in the tropics.
Mexico is considered a megadiverse country, with its mammalian fauna ranking third in species richness worldwide after Indonesia and Brazil (Ceballos et al. 2005). This rich biodiversity is the result of a set of interrelated factors that include the geographic location, topography, diversity and heterogeneity of habitats, and geologic history of the country (Ceballos and Navarro 1991). Mexico also lies in the transition zone between the Nearctic and Neotropical biogeographic regions that cross the central part of the country (Ceballos and Navarro 1991, García-Marmolejo et al. 2008). As a result, species from North and South America converge in the country, contributing to its rich biodiversity. Mexico’s rich mammalian fauna includes 14 species of arboreal squirrels divided into three genera (Ceballos et al. 2005, Ramírez-Pulido et al. 2005). Unfortunately, high annual deforestation rates >1.0%, and an estimated conversion of 90% of the original humid tropical forests into agrosystems or urban settlements, pose serious threats to the persistence of this rich biodiversity in the country (Sánchez-Cordero et al. 2005).
Herein, we examined the status of the arboreal squirrels of Mexico as a model taxon to elucidate the urgent need that exists worldwide to allocate more funding and research effort to less charismatic species. In particular, we were interested in the following questions: What is the diversity and present distribution, state of scientific knowledge, and conservation status of the arboreal squirrels of Mexico? Are there patterns that may account for their diversity? What are the potential threats for their persistence in the country?
Materials and methods
We surveyed the literature to review the diversity (i.e., number of species and subspecies) and present distribution of all the arboreal squirrels of Mexico. Distribution was determined on the basis of historical and recent records for each state of the country. To examine diversity patterns, we conducted a multiple regression analysis to explore relationships between the diversity of arboreal squirrels with the following characteristics of each state of the country: continental area, mean latitude, mean altitude, area of temperate forests, and area of tropical forests (Table 1). Mean annual temperature and mean annual precipitation were excluded from the analysis because of high correlations with mean altitude (r=-0.74, p<0.0001) and mean latitude (r=-0.76, p<0.0001), respectively (McGarigal et al. 2000) (Table 1).
State | Area | % | Latitude | Altitude | °C | mm | Temperate | Tropical | m3r | Population |
---|---|---|---|---|---|---|---|---|---|---|
Aguascalientes | 5617.8 | 0.3 | 21.8 | 2460 | 16.5 | 568.5 | 436.3 | 0 | 4734 | 2.2 |
Baja California | 71,445.9 | 3.6 | 30.0 | 1555 | 19.6 | 169.4 | 1608.6 | 0 | 75 | 2.3 |
Baja California Sur | 73,922.5 | 3.8 | 25.3 | 1055 | 23.3 | 261.7 | 346.1 | 3874.3 | 2554 | 4.0 |
Campeche | 57,924.4 | 3.0 | 19.0 | 200 | 25.8 | 1464.6 | 28.2 | 9200.7 | 77,679 | 1.7 |
Chihuahua | 247,455.3 | 12.6 | 28.4 | 2370 | 17.3 | 370.5 | 58,891.9 | 3921.7 | 1,033,181 | 1.1 |
Chiapas | 73,288.8 | 3.7 | 16.0 | 2300 | 20.3 | 2388.5 | 6601.3 | 7066 | 120,607 | 2.0 |
Coahuila | 151,562.6 | 7.7 | 26.9 | 2655 | 18.6 | 386.6 | 4580.7 | 0 | 137 | 1.8 |
Colima | 5625 | 0.3 | 18.9 | 2165 | 24.9 | 1163 | 291 | 321.2 | 2878 | 1.8 |
Distrito Federal | 1485.5 | 0.1 | 19.2 | 3085 | 13.0 | 965.3 | 172.2 | 0 | 2430 | 0.3 |
Durango | 123,451.3 | 6.3 | 24.4 | 2610 | 16.0 | 597.1 | 38,894.9 | 4451 | 1,741,212 | 1.2 |
Guanajuato | 30,608.4 | 1.6 | 20.5 | 2555 | 18.1 | 590.9 | 2379.1 | 38 | 31,200 | 1.6 |
Guerrero | 63,620.7 | 3.2 | 17.4 | 2125 | 26.3 | 1282.5 | 13,601.5 | 4021.5 | 123,540 | 0.9 |
Hidalgo | 20,846.5 | 1.1 | 20.3 | 2595 | 16.0 | 1332.1 | 2609.6 | 39.36 | 148,507 | 1.7 |
Jalisco | 78,599.2 | 4.0 | 20.5 | 2900 | 25.2 | 989.6 | 14,151.2 | 5000.9 | 322,913 | 1.5 |
México | 22,356.8 | 1.1 | 19.2 | 4080 | 11.6 | 762.6 | 4075.5 | 164 | 145,510 | 1.4 |
Michoacán | 58,643.4 | 3.0 | 18.9 | 2880 | 20.6 | 998.4 | 9446 | 5694.1 | 619,422 | 0.9 |
Morelos | 4892.7 | 0.2 | 18.6 | 3505 | 20.4 | 1170.7 | 308.1 | 40.9 | 3760 | 1.3 |
Nayarit | 27,815.2 | 1.4 | 21.7 | 1840 | 21.7 | 1123.1 | 5640.1 | 3242.3 | 25,905 | 1.6 |
Nuevo León | 64,220.2 | 3.3 | 25.3 | 2125 | 18.1 | 622.2 | 4528.4 | 94.95 | 26,780 | 1.9 |
Oaxaca | 93,793.3 | 4.8 | 16.9 | 2635 | 21.7 | 2020.2 | 8760 | 12,673.7 | 415,049 | 1.0 |
Puebla | 34,289.7 | 1.7 | 19.0 | 3835 | 17.5 | 1260 | 3208.9 | 1382.3 | 223,089 | 1.3 |
Querétaro | 11,683.8 | 0.6 | 20.7 | 2590 | 19.4 | 619.2 | 1149.9 | 623.2 | 9601 | 2.6 |
Quintana Roo | 42,361.0 | 2.2 | 19.5 | 120 | 25.7 | 1301.4 | 4.5 | 11,106.4 | 34,487 | 4.1 |
San Luis Potosí | 60,982.8 | 3.1 | 22.7 | 2510 | 21.3 | 648.7 | 3667.2 | 1498.5 | 2968 | 1.1 |
Sinaloa | 57,377.2 | 2.9 | 24.6 | 1290 | 24.9 | 635.7 | 7827.4 | 15,104 | 44,429 | 0.9 |
Sonora | 179,502.9 | 9.2 | 29.5 | 1415 | 22.0 | 370.2 | 16,205.4 | 23,618 | 162,646 | 1.8 |
Tabasco | 24,737.8 | 1.3 | 17.8 | 455 | 27.2 | 2506 | 14.7 | 839.4 | 17,006 | 1.6 |
Tamaulipas | 80,174.7 | 4.1 | 24.8 | 1800 | 20.6 | 909.8 | 4674.3 | 5904.8 | 138,766 | 1.7 |
Tlaxcala | 3991.1 | 0.2 | 19.3 | 3330 | 15.3 | 670.7 | 361.3 | 0 | 19,789 | 1.9 |
Veracruz | 71,820.4 | 3.7 | 19.7 | 3235 | 17.4 | 1334.3 | 1435.3 | 1420.2 | 264,845 | 1.0 |
Yucatán | 39,612.2 | 2.0 | 20.3 | 110 | 25.8 | 862.7 | 0 | 446.9 | 2195 | 1.6 |
Zacatecas | 75,539.3 | 3.9 | 23.0 | 2715 | 18.3 | 570.9 | 6394 | 456.3 | 41,063 | 0.9 |
Data sources: INEGI 2011, SEMARNAT 2011. Data for temperature and precipitation from 2010, areas of temperate and tropical forests from 2005, wood production from 2009, and population growth rate from 2010.
We reviewed the present state of scientific knowledge of each species by surveying peer-reviewed literature using the search engines JSTOR and BioOne, and restricting our search to articles published from 1930 to 2012. However, because researchers often scan and post old scientific articles on the Internet, we decided to expand our search using the Firefox browser. We assumed that the number of publications reveals how much research attention and biological information exists for each species (e.g., Guevara-Chumacero et al. 2001, Koprowski and Nandini 2008). The scientific and English common names of each species were used in our search (Table 2); however, alternative common names also were used for three species: tassel-eared squirrel (Sciurus aberti, Woodhouse 1853), Mexican gray squirrel (S. aureogaster, Cuvier 1829), and fox squirrel (S. niger, Linnaeus 1758) (Table 2). We did not use Spanish common names because arboreal squirrels in Mexico do not have specific or distinctive common names (Valdés-Alarcón 2003). We only considered publications that focused on species or populations located within the country or that used specimens from Mexico for genetic or morphological analyses. We did not include publications that mentioned species sporadically, such as the distribution of mammals for specific regions of the country. Publications were also classified by specific topics to examine the type of information that has been more prevalent.
English common name | Species | Subspecies | Distribution | SEMARNATa | IUCNb | CITES |
---|---|---|---|---|---|---|
Southern flying squirrel | Glaucomys volans | T | Lc | |||
chontali | Endemic | |||||
goldmani | Endemic | |||||
guerreroensis | Endemic | |||||
herreranus | Endemic | |||||
madrensis | Endemic | |||||
oaxacensis | Endemic | |||||
Abert’s squirrel | Sciurus aberti | Lc | ||||
barberi | Endemic | Sp | ||||
durangi | Endemic | Sp | ||||
phaeurus | Endemic | Sp | ||||
Allen’s squirrel | Sciurus alleni | Endemic | Lc | |||
Arizona gray squirrel | Sciurus arizonensis | T | Dd | |||
huachuca | ||||||
Mexican red-bellied squirrel | Sciurus aureogaster | Lc | ||||
aureogaster | Endemic | |||||
nigrescens | ||||||
Collie’s squirrel | Sciurus colliaei | Lc | ||||
colliaei | Endemic | |||||
nuchalis | Endemic | |||||
sinaloensis | Endemic | |||||
truei | Endemic | |||||
Deppe’s squirrel | Sciurus deppei | Lc | III/w | |||
deppei | ||||||
negligens | Endemic | |||||
vivax | ||||||
Western gray squirrel | Sciurus griseus | T | Lc | |||
anthonyi | ||||||
Mexican fox squirrel | Sciurus nayaritensis | Lc | ||||
apache | Endemic | |||||
nayaritensis | Endemic | |||||
Eastern fox squirrel | Sciurus niger | Lc | ||||
limitis | ||||||
Peters’s squirrel | Sciurus oculatus | Sp | Lc | |||
oculatus | Endemic | |||||
shawi | Endemic | |||||
tolucae | Endemic | |||||
Variegated squirrel | Sciurus variegatoides | Sp | Lc | |||
goldmani | ||||||
Yucatan squirrel | Sciurus yucatanensis | Lc | ||||
baliolus | ||||||
phaeopus | ||||||
yucatanensis | ||||||
Mearns’s squirrel | Tamiasciurus mearnsi | Endemic | T | E |
Data sources: Diersing 1980, Hall 1981, Lindsay 1981, Yensen and Valdés-Alarcón 1999, Villa and Cervantes 2003, Ceballos and Oliva 2005, Ramírez-Pulido et al. 2005, Thorington and Hoffmann 2005, SEMARNAT 2010, CITES 2011, IUCN 2011, Thorington et al. 2012.
aT, threatened; Sp, special protection.
bLc, least concern, Dd, data deficient, E, endangered.
We reviewed the conservation status of each species by consulting information from the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT 2010), the IUCN (2011), the Convention on International Trade in Endangered Species (CITES 2011), and by surveying the literature. We conducted a multiple regression analysis to explore relationships between the IUCN Red List categories for each species with the number of states it occupies (i.e., geographic distribution) and the number of publications for each species (Koprowski and Nandini 2008). The IUCN Red List categories were coded to reflect the following increasing threat level: data deficient=1, least concern=2, near threatened=3, vulnerable=4, endangerment=5, critically endangered=6. To examine potential threats, we conducted a multiple regression analysis to explore relationships between the diversity of arboreal squirrels with annual wood production and human population growth rate for each state of the country (Table 1).
We used the corrected Akaike’s information criterion (AICc) and AICc weights (wi) for model selection in all multiple regression analyses (Burnham and Anderson 2002). We conducted the last literature search in April 2012. All statistical analyses were conducted using SPSS 17.0 (SPSS Inc., Chicago, IL, USA). When necessary, we transformed data to meet the assumptions of normality for all analyses (Zar 1996).
Results
Diversity
There are 14 species of arboreal squirrels currently recognized in Mexico divided into three genera: Glaucomys, Sciurus, and Tamiasciurus (Table 2). Glaucomys and Tamiasciurus only have one species each, whereas Sciurus is the most diverse taxon with 12 species. Twelve of the 14 species are polytypic divided into 30 subspecies, whereas two species are monotypic [i.e., Sciurus alleni (Nelson 1898) and Tamiasciurus mearnsi (Townsend 1897)] (Table 2). At the species level, only four of the 14 species are endemic to Mexico [i.e., S. alleni, S. colliaei (Richardson 1839), S. oculatus (Peters 1863), and T. mearnsi], whereas at the subspecies level 20 of the 30 subspecies are endemic (Table 2). A recent systematic revision of Glaucomys volans (Linnaeus 1758) has reassigned G. v. chontali and G. v. herreranus as subspecies, increasing the number from four (Ceballos and Oliva 2005, Ramírez-Pulido et al. 2005) to six subspecies in Mexico (Thorington and Hoffmann 2005, Thorington et al. 2012) (Table 2). The classification of G. v. madrensis always has been contentious (Goodwin 1961) and recently has been suggested as incorrect (Ceballos and Oliva 2005). Unlike S. aureogaster nigrescens that has been collected in Guatemala, S. a. aureogaster only has been collected in Mexico (Kelson 1952, Musser 1968, Hall 1981), indicating that this subspecies also may be endemic to Mexico (Table 2).
Geographic distribution
Sciurus aureogaster is the species most widely distributed, present in 20 of the 32 states, followed by S. deppei (Peters 1863) and Glaucomys volans found in 13 and 12 states, respectively (Table 3). In contrast, S. arizonensis (Coues 1867), S. griseus (Ord 1818), S.variegatoides (Ogilby 1839), and Tamiasciurus mearnsi have distributions restricted to only one state each (Table 3). Glaucomys volans has a scattered distribution in eastern, central, and southern Mexico (Ceballos et al. 2010) (Table 3). Recent records have confirmed the presence of this species in the states of Hidalgo (Hernández-Flores et al. 2010) and Michoacán (Ceballos et al. 2010). In Michoacán, G. volans only was known from a recorded sighting (Hooper 1952); however, its presence in that state had not been confirmed. Sciurus aberti has a disjunct distribution throughout its range in northwestern Mexico (Table 3), owing to its close association with ponderosa pine (Pinus ponderosa, Douglas ex Lawson), which provides both shelter and food (Nash and Seaman 1977). Sciurus griseus has a restricted distribution in northwestern Mexico (Table 3), with its population apparently disconnected from other populations in southern California (Ceballos and Oliva 2005). In Mexico, the species is known from Sierra de Juárez, but a recent record has expanded its distribution to approximately 258 km farther south (Escobar-Flores et al. 2011). Interestingly, the species is absent in Sierra de San Pedro Mártir (Yensen and Valdés-Alarcón 1999, Koprowski et al. 2006), located south of Sierra de Juárez. Although widely distributed in eastern and central United States (Koprowski 1994), S. niger has a restricted distribution in northeastern Mexico, near the US-Mexico border (Table 3). However, a visual record has been recently reported in the state of Durango where its presence was unknown (Aragón et al. 2009).
State | Code | Species | G. volans | S. aberti | S. alleni | S. arizonensis | S. aureogaster | S. colliaei | S. deppei | S. griseus | S. nayaritensis | S. niger | S. oculatus | S. variegatoides | S. yucatanensis | T. mearnsi |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Aguascalientes | AS | × | ||||||||||||||
Baja California | BC | × | × | |||||||||||||
Baja California Sur | BS | |||||||||||||||
Campeche | CC | × | × | |||||||||||||
Chihuahua | CH | × | × | × | × | |||||||||||
Chiapas | CS | × | × | × | × | × | ||||||||||
Coahuila | CL | × | × | |||||||||||||
Colima | CM | × | × | |||||||||||||
Distrito Federal | DF | × | × | |||||||||||||
Durango | DG | × | × | × | × | |||||||||||
Guanajuato | GT | × | ||||||||||||||
Guerrero | GR | × | × | |||||||||||||
Hidalgo | HG | × | × | × | × | |||||||||||
Jalisco | JC | × | × | × | ||||||||||||
México | MC | × | × | × | ||||||||||||
Michoacán | MN | × | × | |||||||||||||
Morelos | MS | × | ||||||||||||||
Nayarit | NT | × | × | × | ||||||||||||
Nuevo León | NL | × | × | × | × | |||||||||||
Oaxaca | OC | × | × | × | ||||||||||||
Puebla | PL | × | × | × | × | |||||||||||
Querétaro | QT | × | × | × | × | |||||||||||
Quintana Roo | QR | × | × | |||||||||||||
San Luis Potosí | SP | × | × | × | × | × | ||||||||||
Sinaloa | SL | × | × | |||||||||||||
Sonora | SR | × | × | × | × | |||||||||||
Tabasco | TC | × | × | × | ||||||||||||
Tamaulipas | TS | × | × | × | × | |||||||||||
Tlaxcala | TL | × | ||||||||||||||
Veracruz | VZ | × | × | × | × | |||||||||||
Yucatán | YN | × | × | |||||||||||||
Zacatecas | ZS | × | × |
Data sources: Musser 1968, Diersing 1980, Hall 1981, Álvarez-Castañeda 1996, Jiménez-Guzmán et al. 1997, Yensen and Valdés-Alarcón 1999, Villa and Cervantes 2003, Ceballos and Oliva 2005, Núñez-Garduño 2005, Sánchez-Hernández et al. 2005, Aragón et al. 2009, Ceballos et al. 2010.
Chiapas and San Luis Potosí are the states with the greatest diversity of arboreal squirrels with five species each, whereas Baja California Sur has no record of arboreal squirrels (Figure 1). Interestingly, six states along the Gulf of Mexico and three states in the northwestern region of the country display a high diversity of arboreal squirrels (Figure 1). Our analysis revealed that the best-fit model to account for the diversity of arboreal squirrels of Mexico included both temperate and tropical forests but not latitude, altitude, or continental area of each state (Table 4).
Models | Adj R2 | F | df | p-Value | AICc | ΔAICc | wi |
---|---|---|---|---|---|---|---|
A. Diversity patterns | |||||||
Temperate forest+tropical forest+latitude+altitude+area | 0.16 | 2.19 | 5, 26 | 0.09 | 22.02 | 8.13 | 0.01 |
Temperate forest+tropical forest+latitude+altitude | 0.18 | 2.72 | 4, 27 | 0.05 | 19.12 | 5.23 | 0.03 |
Temperate forest+tropical forest+area | 0.20 | 3.54 | 3, 28 | 0.03* | 16.60 | 2.71 | 0.11 |
Temperate forest*+tropical forest | 0.22 | 5.43 | 2, 29 | 0.01* | 13.89 | 0.00 | 0.42 |
Latitude+altitude+area* | 0.09 | 2.02 | 3, 28 | 0.14 | 20.63 | 6.74 | 0.01 |
Latitude+altitude | -0.03 | 0.51 | 2, 29 | 0.61 | 22.95 | 9.06 | 0.00 |
Temperate forest* | 0.14 | 6.17 | 1, 30 | 0.02* | 15.46 | 1.56 | 0.19 |
Tropical forest* | 0.13 | 5.46 | 1, 30 | 0.03* | 16.09 | 2.20 | 0.14 |
Latitude | -0.03 | 0.13 | 1, 30 | 0.72 | 21.30 | 7.41 | 0.01 |
Altitude | -0.01 | 0.77 | 1, 30 | 0.39 | 20.63 | 6.73 | 0.01 |
Area | 0.08 | 3.82 | 1, 30 | 0.60 | 17.60 | 3.71 | 0.07 |
B. Conservation status | |||||||
Geographic distribution+number of publications | -0.06 | 0.63 | 2, 11 | 0.55 | -32.14 | 0.03 | 0.33 |
Geographic distribution | -0.05 | 0.34 | 1, 12 | 0.57 | -32.17 | 0.00 | 0.34 |
Number of publications | -0.05 | 0.33 | 1, 12 | 0.58 | -32.16 | 0.01 | 0.33 |
C. Potential threats | |||||||
Wood production*+population growth rate | 0.16 | 3.91 | 2, 29 | 0.03* | 16.42 | 2.06 | 0.25 |
Wood production* | 0.17 | 7.43 | 1, 30 | 0.01* | 14.36 | 0.00 | 0.70 |
Population growth rate | 0.03 | 2.02 | 1, 30 | 0.17 | 19.36 | 5.00 | 0.06 |
*Indicate significant differences at p<0.05.
State of scientific knowledge
Our search yielded only 37 peer-reviewed publications from 1930 to 2012. During the first 50 years, from 1930 to 1980, the number of publications per decade was three or fewer with not a single one during the 1940s. However, we observed an increase in the number of publications during the 1980s (n=5) and 1990s (n=12), followed by a decrease during the next decade (n=4). Interestingly, between 2010 and 2012, we found five publications compared with previous decades. Glaucomys volans is the species with the greatest number of publications, followed by Sciurus aureogaster and Tamiasciurus mearnsi (Figure 2). In contrast, whereas six species only have one publication, S. niger does not have a single one in Mexico (Figure 2). Most of the publications (70.3%) consisted of mammalian species accounts (which summarize the published literature for each species, except for S. aureogaster, S. griseus, S. niger, and T. mearnsi), articles on systematics (G. volans, n=4; S. aureogaster, n=3; S. variegatoides, n=1; T. mearnsi, n=1), and distribution (G. volans, n=4; S. colliaei, n=1; S. griseus, n=2) (Figure 3); most of the articles (n=8) published during the 1990s correspond to accounts. The remainder of the publications (29.7%) covered topics on genetics (G. volans, n=1; S. aberti, n=1; T. mearnsi, n=1), basic biology (G. volans, n=1), basic ecology (S. aureogaster, n=1; T. mearnsi, n=1), nest-site selection (S. aureogaster, n=1), communal nesting behavior (T. mearnsi, n=1), population density (S. colliaei, n=1), fossils (G. volans, n=1), and parasites (S. aureogaster, n=1) (Figure 3). Interestingly, <30% of all the publications had at least one author associated with a Mexican institution.
Conservation status and potential threats
Presently, seven species are federally listed in Mexico under some category of risk by SEMARNAT (Table 2). Of these, four are listed as threatened and three as subject to special protection, with three subspecies also subject to special protection (Table 2). The IUCN has included all the species under some category of risk, with 12 listed as least concern, 1 as data deficient, and 1 as endangered (Table 2). In contrast, CITES only has one species listed (Table 2). Sciurus aureogaster and S. colliaei are not listed in Mexico under any category of risk owing to their wide distributions and varied diet, whereas S. griseus, S. arizonensis, and Tamiasciurus mearnsi are listed owing in part to their restricted distributions (Ceballos and Oliva 2005). Surprisingly, S. niger is not listed under any category of risk in Mexico, despite its restricted distribution that lies in forests with excessive timber exploitation and conversion to agriculture (Ceballos and Oliva 2005). Other species known to be threatened by deforestation are S. aberti, S. alleni, S. deppei, and S. oculatus (Ceballos and Oliva 2005). It is estimated that only 69.2% and 43.6% of the potential habitats of S. alleni and S. oculatus, respectively, remain unaltered (Sánchez-Cordero et al. 2005). Glaucomys volans is also threatened by habitat destruction, with some populations known to have disappeared from several sites in central Mexico during the last decade (Ceballos and Oliva 2005). Other species such as S. oculatus and S. variegatoides have been considered as “fragile” (Ceballos and Navarro 1991) owing to the destruction of their habitats. The riparian habitats occupied by S. arizonensis also are subject to a strong anthropogenic pressure (Ceballos and Oliva 2005). However, another potential threat to S. arizonensis and S. niger is the US proposal to build a border fence that will prevent free movement of wildlife populations between the United States and Mexico by eliminating biological corridors (Koleff et al. 2007, Lasky et al. 2011). Sciurus variegatoides and S. yucatanensis (Allen 1877) have been suggested to tolerate disturbed areas (Ceballos and Oliva 2005); however, unfortunately, almost nothing is known about their ecology. In portions of its range, S. aureogaster is known to cause damage to crops and is considered a pest species (Nelson 1899, Romero-Balderas et al. 2006, Ramos-Lara and Cervantes 2011). In Chiapas, S. aureogaster and S. deppei are sold as food for human consumption or as pets by the Tzeltal and Lacandon people (Naranjo et al. 2004, Ceballos and Oliva 2005, Barragán et al. 2007). Similarly, S. nayaritensis (Allen 1890) is hunted for sport and human consumption (Ceballos and Oliva 2005). A potential threat to T. mearnsi is the introduction of S. carolinensis (Gmelin 1788) to the Sierra de San Pedro Mártir in 1946 (Yensen and Valdés-Alarcón 1999). However, although S. carolinensis was not observed in the Sierra de San Pedro Mártir during recent studies (Koprowski et al. 2006, Ramos-Lara and Koprowski 2012), its presence or absence still needs to be confirmed particularly at the introduction sites.
We did not find any relationship between the IUCN Red List categories with either the geographic distribution of the arboreal squirrels or the number of publications (Table 4). Nonetheless, the diversity of arboreal squirrels was related to annual wood production but not human population growth rate (Table 4).
Discussion
Mexico harbors a great diversity of species and subspecies of arboreal squirrels. However, we did not find a latitudinal cline similar to that reported for all the arboreal squirrels of the world (Koprowski and Nandini 2008), possibly owing to the number of species distributed in both Nearctic and Neotropical regions of the country. Species with restricted distributions within Mexico have similar IUCN Red List categories than those with wide distributions, owing in part to their wide distributions in North and Central America. Among these species, Sciurus arizonensis, S. griseus, and S. variegatoides are federally listed under some category of risk by SEMARNAT (2010), except for S. niger, which probably also should be listed.
Compared with other countries in North America and Europe, where arboreal squirrels have been studied more often (Steele and Koprowski 2001, Koprowski and Nandini 2008), little is known about the arboreal squirrels of Mexico. For instance, Tamiasciurus hudsonicus (Erxleben 1777) from North America and Sciurus vulgaris (Linnaeus 1758) from Eurasia have more than 260 and 460 publications, respectively (Koprowski and Nandini 2008), far surpassing the number of publications for all the arboreal squirrels of Mexico. Few publications with some authors associated with Mexican institutions also suggest a lack of interest to study this group of mammals, possibly in part because arboreal squirrels in Mexico are considered mostly as pests and not as charismatic as other mammals. The IUCN Red List categories were not related to the number of publications, possibly because of the scarce number of publications for all the species of arboreal squirrels in the country. Endemic species such as S. oculatus and S. alleni are practically unknown and their IUCN Red List categories should be possibly higher than other species. However, in Mexico, only S. oculatus is federally listed under a category of risk by SEMARNAT (2010). Similarly, basically nothing is known about the populations of S. niger in the country.
More information on the ecology of the arboreal squirrels of Mexico is needed to generate suitable regional plans to protect this high biodiversity and the forest ecosystems that they occupy, especially for those endemic and with restricted distributions. In Mexico, endemic mammals face different extirpation risks according to their geographic location, indicating a need to incorporate geographic context when designing both regional and local conservation plans (Sánchez-Cordero et al. 2005). Although arboreal squirrels have been studied more often in North America and Europe (Koprowski and Nandini 2008), it is unclear whether information gleaned from Holarctic species can be effectively used in conservation plans for arboreal squirrels at lower latitudes (Ramos-Lara and Cervantes 2011). For instance, recent publications have revealed that important aspects on the ecology and behavior of Tamiasciurus mearnsi differ from other congeners located at higher latitudes (Koprowski et al. 2006, Ramos-Lara and Koprowski 2012). As a result, using information from other Tamiasciurus to generate conservation plans for T. mearnsi could be uncertain. Like other less charismatic species in the world, information from local populations is needed to establish suitable regional plans to effectively protect species and populations facing specific anthropogenic threats (Smith et al. 2005).
Knowledge on the arboreal squirrels worldwide not only is poor relative to their conservation status, but forested environments also are disappearing rapidly (Koprowski and Nandini 2008). In Mexico, like in other countries of Latin America (Mares 1986, Bradshaw et al. 2009), conservation is a multifaceted problem with the exploitation and management of natural resources usually based on political decisions rather than on scientific data (Ceballos and Navarro 1991). Mexico is among the top five countries, together with Brazil, Gabon, Papua New Guinea, and Indonesia, with the largest decrease in primary forest over the last 20 years (FAO 2010). We found that states with larger areas of temperate and tropical forests harbor a greater diversity of arboreal squirrels. However, annual deforestation rates >1.0% nationwide pose serious threats to the diversity and conservation of arboreal squirrels and other species in the country (Sánchez-Cordero et al. 2005). Furthermore, owing to the lack of permanent monitoring in the country, deforestation rates are difficult to estimate but range between 450,000 and 1,500,000 ha/year (Aguilar et al. 2000, Valdez et al. 2006). Mexico has lost >95% of its tropical forests and >50% of its temperate forests (Céspedes-Flores and Moreno-Sánchez 2010). We also found that states with a greater diversity of arboreal squirrels have a higher annual wood production, possibly posing a threat to their persistence, as it is estimated that 50% of the wood produced annually in the country is illegal (Instituto Nacional de Ecología 2012). In particular, the states of Veracruz, Chiapas, Tabasco, and Colima have the highest deforestation rates >1.0% (Céspedes-Flores and Moreno-Sánchez 2010). In contrast, other states with a great diversity, such as San Luis Potosí, Durango, Sonora, and Chihuahua, have deforestation rates <0.1% (Céspedes-Flores and Moreno-Sánchez 2010). Nonetheless, a species such as Sciurus aberti is at risk by timber exploitation in portions of its range in Sonora, Chihuahua, and Durango (Ceballos and Oliva 2005).
One of the most significant challenges facing conservation and development in Mexico is the need to support rural livelihoods by adequately assessing and capturing the value of environmental services that wildlife provides to ecosystems (Brandon et al. 2005). Although known to cause damage to crops (e.g., Valdés-Alarcón 2003, Romero-Balderas et al. 2006, Ramos-Lara and Cervantes 2011), arboreal squirrels perform considerable ecosystem services such as seed planting and dispersal, pollination, fungal spore dispersal, serve as indicator species in some forests owing to their close associations with specific vegetation types, and are an important food source for many predators (Valdés-Alarcón 2003, Koprowski and Nandini 2008). As a result, arboreal squirrels may be used as indicators of forest condition and in turn protect other species in the ecosystem. However, because regional differences in the ecology of a species may hinder its use as an indicator in other geographic areas (Smith et al. 2005), it is important to generate more biological information from populations found within Mexico to establish suitable plans for their conservation, rather than using solely data from Holarctic arboreal squirrels. Like other countries with a great biodiversity and limited economic resources, national and international efforts may be required to preserve Mexico’s rich biological heritage (Ceballos and Navarro 1991). However, less charismatic species worldwide face conservation concerns similar to those of the arboreal squirrels of Mexico, with little or non-existent biological information to generate the suitable regional plans required for their conservation. Our study shows that more funding and research effort should be allocated to less charismatic species that in most cases face critical conservation concerns and are listed in high categories of risk.
Acknowledgments
The Consejo Nacional de Ciencia y Tecnología (CONACyT) and the Wallace Research Foundation provided financial support to Nicolás Ramos-Lara. Erin E. Posthumus, Jonathan J. Derbridge, Judith L. Bronstein, Melissa J. Merrick, Robert W. Mannan, Seafha J. Blount, William W. Shaw, and two anonymous reviewers provided valuable comments that improved the manuscript.
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