Ecology of the Endemic Mearns's Squirrel (Tamiasciurus Mearnsi) in Baja California, Mexico
Item Type text; Electronic Dissertation
Authors Ramos-Lara, Nicolas
Publisher The University of Arizona.
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Download date 02/10/2021 17:04:27
Link to Item http://hdl.handle.net/10150/228171 ECOLOGY OF THE ENDEMIC MEARNS’S SQUIRREL ( TAMIASCIURUS MEARNSI ) IN BAJA CALIFORNIA, MEXICO
by
Nicolas Ramos Lara
A Dissertation Submitted to the Faculty of the
SCHOOL OF NATURAL RESOURCES AND THE ENVIRONMENT
In Partial Fulfillment of the Requirements For the Degree of
DOCTOR OF PHILOSOPHY WITH A MAJOR IN WILDLIFE AND FISHERIES SCIENCE
In the Graduate College
THE UNIVERSITY OF ARIZONA
2012
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THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Nicolas Ramos Lara
entitled: Ecology of the endemic Mearns’s squirrel ( Tamiasciurus mearnsi ) in Baja California, Mexico and recommend that it be accepted as fulfilling the dissertation requirement for the
Degree of Doctor of Philosophy
______Date: 10 April 2012 John L. Koprowski
______Date: 10 April 2012 Judith L. Bronstein
______Date: 10 April 2012 R. William Mannan
______Date: 10 April 2012 William W. Shaw
Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement.
______Date: 10 April 2012 Dissertation Director: John L. Koprowski
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STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.
Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author.
SIGNED: Nicolas Ramos Lara
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ACKNOWLEDGEMENTS
I am indebted to my advisor John Koprowski for his advice, encouragement and support, and for giving me the opportunity to embark in this journey. I thank my committee members Judy Bronstein, Bill Mannan, and Bill Shaw for their guidance and for being part of this journey.
I thank all the people in the squirrel lab for their help and friendship during all this time: Bret Pasch, Claire Zugmeyer, Debbie Buecher, Erin Posthumus, Geoff Palmer, Hsiang Ling Chen, Jonathan Derbridge, Kate Leonard, Margaret Rheude, Melissa Merrick, Nathan Gwinn, Nichole Cudworth, Rebecca Minor, Rosa Jessen, Sandy Doumas, Sarah Hale, Seafha Blount, Shari Ketcham, Tim Jessen, and Vicki Greer. I also thank Alberto Macias Duarte and all the people who directly or indirectly contributed to this research.
This research was possible thanks to the financial support provided by the Desert Southwest Cooperative Ecosystem Studies Unit, the Intermountain Region International Conservation Office (IMRICO) of the National Park Service, the Arizona Agricultural Experiment Station, T&E, Inc., the Consejo Nacional de Ciencia y Tecnología (CONACYT) of Mexico, and the Wallace Research Foundation.
This research was conducted under permits from the University of Arizona Institutional Animal Care and Use Committee, Dirección Forestal y de la Fauna Parque Nacional Sierra de San Pedro Mártir, and Dirección General de Vida Silvestre.
The Observatorio Astronómico Nacional of the Universidad Nacional Autónoma de México facilitated housing logistics. The Servicio Meteorológico Nacional provided temperature and precipitation data of the region. I thank William Shaw, R. William Mannan, Bret Pasch, Melissa Merrick, Nicole Tautfest, Chris Schvarcz, Claire Zugmeyer, and Geoff Palmer for their assistance in the field. I also thank Sam Drake for processing the satellite imagery of the Sierra de San Pedro Mártir.
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DEDICATION
This dissertation is dedicated to the loving memory of my mother,
Ana María Lara Meza
¡Gracias Madre!
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TABLE OF CONTENTS
LIST OF TABLES ...... 7
LIST OF FIGURES ...... 10
ABSTRACT ...... 13
CHAPTER 1. INTRODUCTION ...... 15
CHAPTER 2. PRESENT STUDY ...... 21
REFERENCES ...... 24
APPENDIX A. DEFORESTATION AND KNOWLEDGE GAPS THREATEN CONSERVATION OF THE ARBOREAL SQUIRRELS OF MEXICO ...... 31
APPENDIX B. NEST SITE CHARACTERISTICS OF THE MONTANE ENDEMIC MEARNS’S SQUIRREL ( TAMIASCIURUS MEARNSI ): AN OBLIGATE CAVITY NESTER? ...... 70
APPENDIX C. HOME RANGE AND HABITAT USE OF MEARNS’S SQUIRRELS ( TAMIASCIURUS MEARNSI ) WITHOUT THE CONSTRAINTS OF LARDERHOARDING...... 114
APPENDIX D. A STRANGER IN THE GENUS: LIFE HISTORY AND BEHAVIORAL TACTICS OF MEARNS’S SQUIRRELS (TAMIASCIURUS MEARNSI ) ...... 162
APPENDIX E. DISTRIBUTION OF ACTUAL AND RANDOM HOME RANGES OF ADULT MALE AND FEMALE MEARNS’S SQUIRRELS (TAMIASCIURUS MEARNSI ) IN THE NORTHERN PART OF THE SIERRA DE SAN PEDRO MÁRTIR...... 216
APPENDIX F. DETECTED PRESENCE OF MEARNS’S SQUIRRELS (TAMIASCIURUS MEARNSI ) DURING THE STUDY IN DIFFERENT AREAS OF THE SIERRA DE SAN PEDRO MÁRTIR ...... 218
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LIST OF TABLES
TABLE A1. Continental area for each state of Mexico (km 2), its relative size in the country (%), mean latitude, mean altitude (meters above sea level), mean annual temperature ( oC), mean annual precipitation (mm), area size of temperate forests (km 2), area size of tropical forests (km 2), annual wood production (m 3r), and human population growth rate ...... 56
TABLE A2. List of species and subspecies of arboreal squirrels currently recognized in Mexico, their distribution, and their conservation status according to Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT), International Union for Conservation of Nature (IUCN), and Convention on International Trade in Endangered Species (CITES). Protection is specified for species and subspecies accordingly ...... 59
TABLE A3. Presence of the 14 species of arboreal squirrels ( Glaucomys , Sciurus , and Tamiasciurus ) recognized in Mexico by state based on published records ...... 63
TABLE B1. Habitat characteristics used in univariate analyses to compare nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests, in a coniferous forest of the Sierra de San Pedro Mártir, Baja California, Mexico ...... 101
TABLE B2. Correlations between original characteristics selected in stepwise discriminant function analysis to compare nest sites of Mearns’s squirrels (Tamiasciurus mearnsi ) with random sites (availability), and nest sites of males and females, in the Sierra de San Pedro Mártir, Baja California, Mexico. Significance ( P < 0.017) is marked with an asterisk ...... 103
TABLE B3. Habitat characteristics used in stepwise discriminant function analyses to compare nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests, in a coniferous forest of the Sierra de San Pedro Mártir, Baja California, Mexico ...... 104
TABLE B4. Principal component (PC) analysis used to compare nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests in the Sierra de San Pedro Mártir, Baja California, Mexico ...... 106
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LIST OF TABLES Continued
TABLE B5. Relative dominance ( Rdo ), relative density ( Rde ) and relative frequency ( Rfr ) for each species of tree found at nest sites of Mearns’s squirrels (Tamiasciurus mearnsi ), random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests, in coniferous forests of the Sierra de San Pedro Mártir, Baja California, Mexico. Letters meaning: Sp (species of trees), J (Jeffrey pine―Pinus jeffreyi ), L (Lodgepole pine—P. contorta ), S (Sugar pine—P. lambertiana ), F (White fir—Abies concolor ), A (Quaking aspen—Populus tremuloides ) ...... 109
TABLE C1. Results of two way ANOVAs used to compare home range size of Mearns’s squirrels ( Tamiasciurus mearnsi ) between sexes, years of study, seasons, and their respective interactions, in Baja California, Mexico, from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk. MCP: minimum convex polygon ...... 148
TABLE C2. Results of two way ANOVAs used to compare percentage of male and female 95% fixed kernel home ranges overlapped by male and female conspecifics, number of individuals overlapped by male and female conspecifics, and maximum distance traveled by male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating and nonmating seasons, from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk ...... 149
TABLE C3. Mean (± SD ) percentage of male and female 95% fixed kernel home range overlapped by male and female conspecifics, and number of individuals overlapped by male and female conspecifics, during mating and nonmating seasons for Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, from May 2006 November 2007 ...... 150
TABLE C4. Results of stepwise multiple logistic regression used to compare cover composition characteristics between 95% fixed kernel home ranges of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random home ranges in Baja California, Mexico, from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk ...... 151
TABLE C5. Cover composition for male and female 95% fixed kernel home ranges and random home ranges of Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating and nonmating seasons, from May 2006 November 2007, using satellite imagery. Means (± SD ) are provided ...... 152
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LIST OF TABLES Continued
TABLE C6. Annual density estimates (squirrel/ha) and sex ratios (male:female) of adult (>240 g) and juvenile Mearns’s squirrels (Tamiasciurus mearnsi ) in the Sierra de San Pedro Mártir, Baja California, Mexico, from May 2006 November 2007 ...... 154
TABLE D1. Behaviors of adult Mearns’s squirrels ( Tamiasciurus mearnsi ) recorded during radio telemetric observations in the Sierra de San Pedro Mártir, Baja California, Mexico, from May 2006 November 2007 ...... 199
TABLE D2. Results of the multivariate Cox proportional hazards model to explore relationship between survival of adult male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) with predictor variables, in the Sierra de San Pedro Mártir, Baja California, Mexico, using radio telemetry from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk ...... 200
TABLE D3. Comparison of life history and behavioral traits among Mearns’s squirrels ( Tamiasciurus mearnsi ), Douglas’s squirrels ( T. douglasii ), and red squirrels ( T. hudsonicus ) ...... 201
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LIST OF FIGURES
FIGURE A1. Number of species of arboreal squirrels recognized in Mexico by state. For meaning of the state codes see Table 2 ...... 67
FIGURE A2. Number of publications ( N = 37) from 1930 to 2012 for each species of arboreal squirrel ( Glaucomys , Sciurus , and Tamiasciurus ) recognized in Mexico. Each publication focused completely on a species located within Mexico or included specimens collected from Mexico ...... 68
FIGURE A3. Percentage of topics for all the publications ( N = 37) on arboreal squirrels recognized in Mexico from 1930 to 2012 ...... 69
FIGURE B1. Number of Jeffrey pines ( Pinus jeffreyi ), lodgepole pines ( P. contorta ), and white firs ( Abies concolor ) used by Mearns’s squirrels (Tamiasciurus mearnsi ) for nesting ( n = 115), compared to random sites (n = 115), nest sites of males ( n = 47) and females ( n = 48), and nest sites of females with maternity ( n = 21) and nonmaternity nests ( n = 32) in the Sierra de San Pedro Mártir, Baja California, Mexico ...... 111
FIGURE B2. Number of live and dead trees used by Mearns’s squirrels (Tamiasciurus mearnsi ) for nesting ( n = 115) compared to random sites (n = 115), nest sites of males ( n = 47) and females ( n = 48), and nest sites of females with maternity ( n = 21) and nonmaternity nests ( n = 32) in the Sierra de San Pedro Mártir, Baja California, Mexico ...... 112
FIGURE B3. Comparison of principal component scores on PC 1 and PC 2 for nest sites (open circles) of Mearns’s squirrels with random sites (solid circles) in the Sierra de San Pedro Mártir, Baja California, Mexico. Bivariate means for both sites are the same and are represented by a triangle ...... 113
FIGURE C1. Mean (± SD ) home range size estimates of adult male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating and nonmating seasons from May 2006 November 2007. MCP: minimum convex polygon ...... 157
FIGURE C2. Intraspecific relationship between 95% minimum convex polygon (MCP) home range size and body mass of adult male (A) and female (B) Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating seasons from May 2006 November 2007 ...... 158
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LIST OF FIGURES Continued
FIGURE C3. Interspecific relationship between mean home range size and adult body mass for seven species of tree squirrels monitored with telemetry. Acronyms and data sources: Sar (Sciurus arizonensis —Brown 1984; Cudworth and Koprowski 2010), Sgr (S. griseus —Carraway and Verts 1994; Linders et al. 2004), Sna (S. nayaritensis —Brown 1984; Pasch and Koprowski 2006), Sab (S. aberti —Brown 1984; Edelman and Koprowski 2006), Svu (S. vulgaris ―Lurz et al. 2000; Wauters and Dhondt 1989), Thu (Tamiasciurus hudsonicus —Zugmeyer and Koprowski 2009; Brown 1984), Tme (T. mearnsi —Herein). All authors used 95% fixed kernel estimates, except for Lurz et al. (2000): 85% core area ...... 159
FIGURE C4. Maximum distance traveled by adult male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) from their cavity nests in Baja California, Mexico, during mating and nonmating seasons from May 2006 November 2007 ...... 160
FIGURE C5. Interspecific relationship between male home range size and density for ten species of tree squirrels. Acronyms and data sources: Sar (Sciurus arizonensis —Cudworth and Koprowski 2010), Sna (S. nayaritensis — Pasch and Koprowski 2005; Pasch and Koprowski 2006), Sab (S. aberti — Heaney 1984), Sgn (S. granatensis —Heaney 1984), Sgr (S. griseus —Heaney 1984), Sca (S. carolinensis —Heaney 1984), Sni (S. niger —Pasch and Koprowski 2005; Sheperd and Swihart 1995), Svu (S. vulgaris —Lurz et al. 2000), Thu (Tamiasciurus hudsonicus —Heaney 1984; Zugmeyer and Koprowski 2009), Tme (T. mearnsi —Herein). Methods used to estimate home range size may differ among authors ...... 161
FIGURE D1. Mean monthly temperature (A) and precipitation (B) recorded by Servicio Meteorológico Nacional during 2005 2007 at ejido San Matías, located ca. 25 km north of the Sierra de San Pedro Mártir, Baja California, Mexico. Dark bars show reproductive events recorded for radio collared female Mearns’s squirrels ( Tamiasciurus mearnsi ) ...... 207
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LIST OF FIGURES Continued
FIGURE D2. Latitude (A), precipitation (B), temperature (C), body mass (D), length of head and body (E), number of plant species eaten (F), percentage of year frost free (G), and female home range size (H) versus litter size illustrating life history trends in Tamiasciurus and Sciurus squirrels. Acronyms and data sources: Sab (S. aberti —Edelman and Koprowski 2006; Hayssen 2008; Heaney 1984), Sal (S. alleni —Hayssen 2008; Heaney 1984), Sar (S. arizonensis —Cudworth and Koprowski 2010; Hayssen 2008; Heaney 1984; Pasch and Koprowski 2005), Sau (S. aureogaster —Hayssen 2008; Heaney 1984), Sca (S. carolinensis —Hayssen 2008; Heaney 1984), Sco (S. colliaei —Hayssen 2008; Heaney 1984), Sde (S. deppei —Hayssen 2008; Heaney 1984), Sgn (S. granatensis —Hayssen 2008; Heaney 1984), Sgr (S. griseus —Hayssen 2008; Heaney 1984; Linders et al. 2004), Sna (S. nayaritensis —Hayssen 2008; Heaney 1984; Pasch and Koprowski 2005; Pasch and Koprowski 2006), Sni (S. niger —Hayssen 2008; Heaney 1984), Sri (S. richmondi —Hayssen 2008; Heaney 1984), Svu (S. vulgaris —Hayssen 2008; Lurz et al. 2000), Syu (S. yucatanensis —Hayssen 2008; Heaney 1984), Thu (Tamiasciurus hudsonicus —Hayssen 2008; Heaney 1984; Humphries and Boutin 2000; Leonard and Koprowski 2009; Zugmeyer and Koprowski 2009), Tdo (T. douglasii —Hayssen 2008; Heaney 1984; Smith 1981; Steele 1999), Tme (T. mearnsi —Heaney 1984; Herein) ...... 208
FIGURE D3. Survival curves for adult male ( n = 20) and female ( n = 18) Mearns’s squirrels ( Tamiasciurus mearnsi ) in the Sierra de San Pedro Mártir, Baja California, Mexico, using radio telemetry from May 2006 November 2007 ...... 212
FIGURE D4. Mean (± SD ) body mass of adult male ( n = 20) and female ( n = 18) Mearns’s squirrels ( Tamiasciurus mearnsi ) captured in the Sierra de San Pedro Mártir, Baja California, Mexico, from May 2006 November 2007 ...... 213
FIGURE D5. Percentage (± SD ) of time spent by adult Mearns’s squirrels (Tamiasciurus mearnsi ) feeding on different types of food in the Sierra de San Pedro Mártir, Baja California, Mexico from May November 2006 (A) and 2007 (B). Dotted lines indicate the three categories used in the analysis: tree seeds (TS), tree parts (TP), and other food types (O) ...... 214
FIGURE D6. Percentage (± SD ) of time spent by adult Mearns’s squirrels (Tamiasciurus mearnsi ) in different behaviors in the Sierra de San Pedro Mártir, Baja California, Mexico during 2006 (A) and 2007 (B). Dotted lines indicate the three categories used in the analysis: foraging (F), idle (I), and movement (M) ...... 215 13
ABSTRACT
One of the major environmental concerns in the world is the loss of biological diversity due to anthropogenic activities. Of special concern is the conservation of endemic species that are particularly vulnerable to extinction. The Mearns’s squirrel
(Tamiasciurus mearnsi ) is endemic to the Sierra de San Pedro Mártir, Baja California.
Federally listed as threatened in Mexico and as endangered by the International Union for
Conservation of Nature (IUCN), little is known about the ecology of this southernmost
Tamiasciurus . Interestingly, Mearns’s squirrels exhibit deviations from common behaviors observed in other congeners such as lack of leaf nests (dreys) and larderhoards
(middens), suggesting potentially unique adaptations. Herein, I reviewed the diversity and conservation status of the arboreal squirrels of Mexico. Using radio telemetry and satellite imagery, I examined if the lack of dreys and middens may be associated with differences observed in nesting behavior, home range dynamics, and life history and behavioral tactics between Mearns’s squirrels and other arboreal squirrels.
Mexico harbors 14 species of arboreal squirrels, of which four are endemic, with the states of Chiapas and San Luis Potosí possessing the greatest diversity.
Unfortunately, high deforestation rates in Mexico, and a dearth of information on their ecology, pose serious threats to the persistence of this squirrel diversity. Mearns’s squirrels apparently are obligate secondary cavity nesters with specific nesting requirements and their population possibly limited by the low occurrence of tree cavities in their habitat. The species seems to have lost the territorial behavior that is characteristic of the genus Tamiasciurus . Home range dynamics of Mearns’s squirrels 14 are similar to nonterritorial Sciurus squirrels. Although reproduction and survival are similar to other Tamiasciurus , the species is heavier and apparently larger while exhibiting important variations in their behavior compared to other congeners. The lack of dreys and middens appears to be associated with the unique tactics adopted by
Mearns’s squirrels to persist in the Sierra de San Pedro Mártir. The species provides an important opportunity to learn more about geographic variation in nesting behavior and the evolution of territoriality. Large trees and snags that facilitate cavity formation are critical for the conservation of this species. 15
CHAPTER 1. INTRODUCTION
One of the major environmental concerns in the world is the loss of biological diversity (Ceballos et al. 1998). Habitat loss brought about by anthropogenic activities is widely recognized as the most conspicuous and pervasive threat to biodiversity, especially in the tropics (Mendoza et al. 2005). Of special concern for ecologists, is the conservation of endemic species due to their vulnerability to extinction. Extinction rates are more acute in the tropics, given the high species richness found in these habitats
(Bradshaw et al. 2009; Pyron and Burbrink 2009). Mexico is considered a megadiverse country with its mammalian fauna ranking second in species richness at the global level
(Ceballos et al. 1998). This rich mammalian fauna is represented by the great number of species of arboreal squirrels present in the country (Ramírez Pulido et al. 2005).
Arboreal squirrels are of special interest as they may be excellent indicators of forest condition due to their dependence on mature forests that provide tree tissues and seeds for food, cavities and canopies for nest sites, and stems and canopies for launch sites
(Koprowski and Nandini 2008). Unfortunately, annual rates of deforestation over 1.0%, and an estimated conversion of 90% of the original humid tropical forests into agrosystems or urban settlements, pose serious threats to the conservation of this biodiversity in Mexico (Sánchez Cordero et al. 2005). Although previous works have assessed the diversity and conservation status of Mexican mammals (e.g., Ramírez
Pulido et al. 1996; Arita and Ceballos 1997; Ceballos et al. 2002; Ceballos and Oliva
2005; Ramírez Pulido et al. 2005), only one non peer reviewed publication focused on terrestrial and arboreal squirrels (Valdés Alarcón 2003). Thus, assessing the status of the 16 arboreal squirrels of Mexico and their current state of scientific knowledge will be important to learn more about the threats faced by this diverse group of mammals.
Of all the arboreal squirrels in Mexico, the Mearns’s squirrel ( Tamiasciurus mearnsi ) is the only species endemic to the country that is federally listed as threatened
(SEMARNAT 2010). The species is also listed as endangered by the International Union for Conservation of Nature (IUCN—de Grammont and Cuarón 2008). Endemic to the coniferous forests of the Sierra de San Pedro Mártir, Baja California (Lindsay 1981), little is known about the ecology of this southernmost Tamiasciurus (Ceballos and
Navarro 1991; Yensen and Valdés Alarcón 1999). Mearns’s squirrels have been isolated from red squirrels ( T. hudsonicus ) and Douglas’s squirrels ( T. douglasii ) by almost
12,000 years and its exact distribution in the Sierra de San Pedro Mártir is unknown, except for three locations where the species has been collected in the past for museum specimens (Lindsay 1981; Yensen and Valdés Alarcón 1999). Interestingly, recent information has revealed that Mearns’s squirrels exhibit deviations from common behaviors observed in other congeners (Koprowski et al. 2006; Ramos Lara and
Koprowski 2012), suggesting potentially unique adaptations. For instance, whereas other
Tamiasciurus use leaf nests (known as dreys), tree cavities, and underground burrows for nesting (Steele 1998, 1999), Mearns’s squirrels use tree cavities (Koprowski et al. 2006).
Similarly, whereas other Tamiasciurus build and defend larderhoards (known as middens) to store food throughout most of their range (Steele 1998, 1999), Mearns’s squirrels do not exhibit this behavior apparently due to the open and xeric forests in the
Sierra de San Pedro Mártir Mountains (Ramos Lara and Koprowski 2012). 17
In forest ecosystems, cavity nesting species comprise a structured community that interacts through the creation and competition for nest sites (Martin et al. 2004). In particular, densities of secondary cavity nesters are assumed to be primarily limited by nest sites (Miller 2010). Nests are critical for raising young, rest, predator avoidance, and shelter from adverse weather (Steele and Koprowski 2001). However, because males and females have specific but often divergent biological needs, especially in mammals where pair bonding is rare (Curley and Keverne 2005), nesting requirements may differ between sexes (e.g., Edwards and Guynn 1995; Hanski et al. 2000; Meek and Barclay 1996;
Thogmartin 1999). Unfortunately, differences in nesting behavior between sexes have been rarely examined. Quality of nest sites is also associated with fitness correlates such as probability of predation and nesting success (Cain et al. 2003; Li and Martin 1991).
As a result, information on nesting requirements may allow researchers to assess habitat suitability and management (Ramos Lara and Cervantes 2007). However, because of their reliance on tree cavities, nesting requirements of Mearns’s squirrels may differ from other congeners. Thus, information on nesting requirements of Mearns’s squirrels will be important for their conservation and to learn more about the sources of geographic variation in nesting behavior in Tamiasciurus and other species.
Resources such as food, shelter, and mates are distributed in space so space itself often becomes an important resource (Gurnell 1987). Home range, defined as the area traversed by an individual in its normal activities of food gathering, mating, and caring for young (Burt 1943), is a useful measure of space use and is considered an important indicator of animal behavior and resource requirements (Perry and Garland 2002). 18
Similarly, home range overlap may be used to assess interaction among individuals or to infer territoriality when behaviors cannot be observed adequately (Harless et al. 2009).
Characteristics within home ranges also may be used to evaluate habitat suitability, especially for endangered species (e.g., Aebischer et al. 1993; Katnik and Wielgus 2005;
Perkins et al. 2008; Wood et al. 2007; Zugmeyer and Koprowski 2009). In Tamiasciurus , their spatial and social organization is believed to be dependent upon habitat and resource availability (Gurnell 1987). But because of their territorial behavior (Steele 1998, 1999), middens play an important role in the home range dynamics of red and Douglas’s squirrels (Gurnell 1984). However, without middens and territories to defend, home range dynamics and habitat use of Mearns’s squirrels may differ from other congeners.
Thus, information on the space use by Mearns’s squirrels will be important for their conservation and to learn more about the role played by middens in the territorial behavior of Tamiasciurus .
Life history traits are used to measure both the direction and rate of evolutionary change (Dobson and Oli 2007). As a result, comparative analyses of life history variation have provided an important insight into adaptation in diverse taxa (e.g., Lewis and Storey 1984; Charnov 1991; Kirk 1997; Chiaraviglio et al. 2003; Sears 2005; Karl et al. 2008; Quadros et al. 2009; Camfield et al. 2010). Life history variation is created and maintained by differences in the availability and quality of resources among habitats, and is often considered to be evidence of adaptive strategies for dealing with disparate environments (Sears and Angilleta 2003). Therefore, availability and access to resources such as food, space, and nesting sites may affect the life history traits of many animals 19
(Monson et al. 2000; Wiebe et al. 2006). Similarly, because of resource limitation, varying the time budget is used as a means of coping with a changing environment
(Armitage et al. 1996). In Tamiasciurus , middens are important sources of food necessary to survive during winter (Gurnell 1987). However, defending a territory around middens is costly in energy and time and may interfere with other behaviors such as courtship, mating, feeding, and rearing young (Smith 1992; Descamps et al. 2009). In
Mearns’s squirrels, the lack of dreys and middens may be associated with differences observed in life history and behavioral tactics with other congeners. Thus, information on the life history and behavioral tactics of Mearns’s squirrels will be important for their conservation and to learn more about variations in adaptive strategies in Tamiasciurus and other species.
My dissertation is comprised of four manuscripts and two additional maps. The first manuscript (Appendix A): “Deforestation and knowledge gaps threaten conservation of the arboreal squirrels of Mexico” assesses the diversity, distribution, and conservation status of the arboreal squirrels of Mexico. The manuscript also examines the current state of scientific knowledge for this diverse group of mammals. The second manuscript
(Appendix B): “Nest site characteristics of the montane endemic Mearns’s squirrel
(Tamiasciurus mearnsi ): an obligate cavity nester?” examines if Mearns’s squirrels have specific nesting requirements compared to other congeners. The manuscript also assesses if nesting requirements differ between sexes and between breeding and nonbreeding females. The third manuscript (Appendix C): “Home range and habitat use of Mearns’s squirrels ( Tamiasciurus mearnsi ) without the constraints of larderhoarding” examines if 20 home range size, overlap, and movements of Mearns’s squirrels differ between sexes and seasons compared to other congeners. The manuscript also evaluates habitat suitability for the species in remote areas of the Sierra de San Pedro Mártir and if population densities differ from other species of tree squirrels. The fourth manuscript (Appendix D):
“A stranger in the genus: life history and behavioral tactics of Mearns’s squirrels
(Tamiasciurus mearnsi )” assesses if the lack of middens and dreys may be associated
with differences observed in reproduction, survival, body mass, nesting and feeding behavior, and time budgets between Mearns’s squirrels and other Tamiasciurus and
Sciurus squirrels. The manuscript also examines if interyear variation in weather and food supply strongly influences fitness related traits and behavior of male and female
Mearns’s squirrels. The first manuscript is intended for submission to Conservation
Biology , whereas the remainder of the manuscripts are intended for submission to
Journal of Mammalogy . The first map (Appendix E): “Distribution of actual and random home ranges of adult male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) in the northern part of the Sierra de San Pedro Mártir” shows the locations of the home ranges of Mearns’s squirrels used to evaluate habitat suitability for the species in remote areas of the Sierra de San Pedro Mártir. The second map (Appendix F): “Detected presence of
Mearns’s squirrels ( Tamiasciurus mearnsi ) during the study in different areas of the
Sierra de San Pedro Mártir” shows the locations where Mearns’s squirrels were directly
(presence) or indirectly (feeding signs) detected during the study, including visits made to remote areas of the Sierra de San Pedro Mártir.
21
CHAPTER 2. PRESENT STUDY
The study was conducted in the Sierra de San Pedro Mártir National Park located ca. 100 km southeast of Ensenada, Baja California, with elevations averaging 2,600 m in the north and decreasing to 1,800 m in the southern portion of the mountain range
(Stephens et al. 2003). The park comprises 65,000 ha of which coniferous forests cover ca. 40,655 ha (Minnich et al. 2000). Forests are composed of Jeffrey pine ( Pinus jeffreyi ), sugar pine ( P. lambertiana ), lodgepole pine ( P. contorta ), white fir ( Abies concolor ), and limited amounts of quaking aspen ( Populus tremuloides ) and incense cedar ( Calocedrus decurrens ). The most common forest types are Jeffrey pine, Jeffrey pine–mixed conifer, and mixed white fir forests, respectively (Stephens et al. 2003).
Methods, results, and conclusions of this study are contained in the manuscripts and additional maps appended to this dissertation. The following is a summary of the most important findings.
In Mexico, there are 14 recognized species of arboreal squirrels of which four are endemic, with the states of Chiapas and San Luis Potosí possessing the greatest diversity.
Recent records have extended the geographic distribution of three species. States with larger areas of temperate forests also have a greater diversity of arboreal squirrels.
Presently, all species are listed under some category of risk by the International Union for
Conservation of Nature (IUCN), seven species by the Secretaría de Medio Ambiente y
Recursos Naturales (SEMARNAT) of Mexico, and only one species by the Convention on International Trade in Endangered Species (CITES). Our survey yielded 37 publications revealing that a dearth of scientific information still exists for the arboreal 22 squirrels of Mexico. Common threats to all species are deforestation and timber exploitation. States with a greater diversity of arboreal squirrels also have higher annual wood productions, which may pose a serious threat to their persistence.
Compared to other congeners, Mearns’s squirrels apparently are obligate secondary cavity nesters with specific nesting requirements. However, tree cavities are scarce structures in the Sierra de San Pedro Mártir Mountains, possibly limiting the population and distribution of Mearns’s squirrels. Nest tree species, nest tree condition, nest tree size (DBH), canopy cover, and occurrence of white firs (Abies concolor ) are important
characteristics for nesting. Nest sites of males did not differ from those of females except
for nest tree condition. Females apparently do not have specific nesting requirements for
rearing young. Unlike other congeners that also build leaf nests (dreys) and underground burrows for nesting, large trees and snags that facilitate cavity formation are critical for
the conservation of this montane species.
Home range dynamics of Mearns’s squirrels are similar to nonterritorial squirrels in
the genus Sciurus , with males having larger home ranges than females throughout the
year, suggesting that the lack of larderhoards (middens) is associated with the unique
strategies adopted by Mearns’s squirrels to persist in these mountains. Compared to other
species of tree squirrels, home range overlap between females is greater during mating
seasons, similar to that of males. Population densities of Mearns’s squirrels were similar
to other species of tree squirrels. Remote areas in the Sierra de San Pedro Mártir appear
to have suitable habitat for the species. 23
Reproduction and survival of Mearns’s squirrels are similar to other congeners.
However, despite occupying a warmer and drier habitat, mean litter size of Mearns’s squirrels is similar to other Tamiasciurus and Sciurus squirrels located in cold and mesic forests at higher latitudes. Survival of adult squirrels was influenced by sex and body mass. Mearns’s squirrels are heavier and apparently also larger than other congeners, possibly in part as an adaptation to feed on large pine cones ( Pinus ). Interyear variation in weather and food supply strongly influenced fitness related traits and behavior of
Mearns’s squirrels. The lack of middens and dreys seems to be associated with tactics adopted by Mearns’s squirrels that are similar to those found in tree squirrels of the genus
Sciurus , suggesting important adaptive implications. 24
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APPENDIX A
DEFORESTATION AND KNOWLEDGE GAPS THREATEN CONSERVATION OF
THE ARBOREAL SQUIRRELS OF MEXICO
Manuscript prepared for submission to Conservation Biology
32
Review
Deforestation and Knowledge Gaps Threaten Conservation of the Arboreal
Squirrels of Mexico
N. RAMOS LARA* AND J. L. KOPROWSKI
Wildlife and Fisheries Science, School of Natural Resources and the Environment,
University of Arizona, Tucson, AZ 85721, U.S.A.
Abstract: Loss of biodiversity is one of the major environmental concerns in the world.
Mexico is considered a megadiverse country with a great diversity of species. However,
high deforestation rates are posing serious threats to this biodiversity. We assessed the
diversity, distribution, conservation status, and current state of scientific knowledge of
the arboreal squirrels of Mexico. There are 14 recognized species, of which four are
endemic to the country, with the states of Chiapas and San Luis Potosí possessing the greatest diversity. Recent records have extended the geographic distribution of three species. States with larger areas of temperate forests also have a greater diversity.
Presently, all species are listed under some category of risk by the IUCN, seven species
by SEMARNAT, and only one species by CITES. Our survey yielded 37 publications
revealing that a dearth of information exists for the arboreal squirrels of Mexico.
Neither distribution nor publications for each species were associated with the IUCN
categories of endangerment. Common threats to all species are deforestation and timber
exploitation. States with a greater diversity of squirrels also have higher annual wood 33 productions, which may pose a threat to their persistence. Because of their close association with forest ecosystems, arboreal squirrels may be indicators of forest condition. However, using information from arboreal squirrels at higher latitudes to create conservations plans for species located in the tropics may be uncertain.
Therefore, it is important to generate information from populations of arboreal squirrels in Mexico to create suitable plans to preserve this rich biological heritage.
Keywords: deforestation, endemic species, geographical distribution, Glaucomys ,
mammals, Sciurus , squirrels, Tamiasciurus
Resumen: La pérdida de la biodiversidad es una de las mayores preocupaciones
ambientales en el mundo. México es considerado un país megadiverso con una gran
diversidad de especies. Sin embargo, altas tasas de deforestación están planteando serias amenazas para esta biodiversidad. Revisamos la diversidad, distribución, estado
de conservación y estado actual del conocimiento científico de las ardillas arbóreas de
México. Hay 14 especies reconocidas, de las cuales cuatro son endémicas para el país,
con los estados de Chiapas y San Luis Potosí ostentando la diversidad más grande.
Registros recientes han extendido la distribución geográfica de tres especies. Estados
con áreas más grandes de bosques templados también tienen una diversidad más alta.
Actualmente, todas las especies están listadas bajo alguna categoría de riesgo por la
IUCN, siete especies por la SEMARNAT y solamente una especie por CITES. Nuestro
estudio dio 37 publicaciones revelando que existe una escasez de información para las 34 ardillas arbóreas de México. Ni la distribución ni las publicaciones para cada especie estuvieron asociadas con las categorías de riesgo de la IUCN. Amenazas comunes para todas las especies son la deforestación y la explotación forestal. Estados con una diversidad más grande de ardillas también tienen producciones maderables anuales más altas, lo cual puede plantear una amenaza para su persistencia. Debido a su estrecha asociación con ecosistemas de bosque, las ardillas arbóreas pueden ser indicadoras de la condición del bosque. Sin embargo, usar información de ardillas arbóreas en latitudes más altas para crear planes de conservación para especies ubicadas en los trópicos puede ser incierto. Por lo tanto, es importante generar información de las poblaciones de ardillas arbóreas en México para crear planes adecuados para preservar esta rica herencia biológica.
Palabras Clave: ardillas, deforestación, distribución geográfica, especies endémicas,
Glaucomys , mamíferos, Sciurus , Tamiasciurus
*email: [email protected]
Introduction
One of the major environmental concerns in the world is the loss of biological diversity
(Ceballos et al. 1998). Species diversity is being lost in habitats that are increasingly
diminished by development, fragmentation, and urban waste (Zedler et al. 2001). Habitat
loss brought about by anthropogenic activities is widely recognized as the most 35 conspicuous and pervasive threat to biodiversity, especially in the tropics (Mendoza et al.
2005). Extinction rates will continue to increase unless effective conservation strategies are implemented (Ceballos 2007), especially for endemic species which are more vulnerable (Sánchez Cordero et al. 2005). Extinction rates from habitat loss and overexploitation are more acute in the tropics, given the high species richness found in these habitats (Bradshaw et al. 2009; Pyron & Burbrink 2009) and the economic problems faced by countries at these latitudes (Mares 1984).
Mexico is considered a megadiverse country with its mammalian fauna ranking
second in species richness at the global level (Ceballos et al. 1998). The country harbors
475 species of mammals, of which 169 are endemic (Ramírez Pulido et al. 2005). The
uniqueness of this rich mammalian fauna is the result of a set of interrelated factors
including geographic location, topography, habitat diversity and heterogeneity, and
geologic history (Ceballos & Navarro 1991). Mexico also lies in a transition zone between the Nearctic and Neotropical biogeographic regions, crossing the central part of the country from the Pacific to the Gulf coastal plains (Ceballos & Navarro 1991; García
Marmolejo et al. 2008). As a result, species from North and South America merge in the country contributing to this rich diversity, distributed in a wide range of terrestrial habitats or ecological zones. The largest of these ecological zones is the arid and semiarid zone of scrub and grasslands occupying an estimated area of 99 million (M) ha, followed by the subhumid tropic zone of deciduous forest with 40 M ha, subhumid temperate zone of pine, oak, and mixed forest with 33 M ha, humid tropic zone of evergreen forests and savannahs with 22 M ha, humid temperate zone of mixed forests 36 with 1 M ha, and alpine zone with 0.3 M ha (Valdez et al. 2006). In particular, this rich mammalian fauna is represented by a great number of species of arboreal squirrels present in the country (Ramírez Pulido et al. 2005). Unfortunately, annual rates of deforestation over 1.0%, and an estimated conversion of 90% of the original humid tropical forests into agrosystems or urban settlements, pose serious threats to the conservation of this biodiversity in Mexico (Sánchez Cordero et al. 2005).
Previous works have assessed the diversity and conservation status of Mexican mammals (e.g., Ramírez Pulido et al. 1996; Arita & Ceballos 1997; Ceballos et al. 2002;
Ceballos & Oliva 2005; Ramírez Pulido et al. 2005), with only one non peer reviewed publication focused on terrestrial and arboreal squirrels (Valdés Alarcón 2003). In particular, arboreal squirrels are of special interest as they may be excellent indicators of forest condition due to their dependence on mature forests that provide tree tissues and seeds for food, cavities and canopies for nest sites, and stems and canopies for launch sites (Koprowski & Nandini 2008). Nonetheless, besides the continuous loss of forests in the country, other important events have occurred since the publication of these works, especially for the diverse group of arboreal squirrels. For instance, the NOM 059, which lists species under specific categories of risk at the federal level, has been recently updated by the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT
2010). Similarly, the geographic distribution of some species of arboreal squirrels have been extended due to recent records (Aragón et al. 2009; Hernández Flores et al. 2010;
Escobar Flores et al. 2011), their taxonomy also has been revised (Thorington &
Hoffmann 2005; Kerhoulas & Arbogast 2010), and more information on some species of 37 arboreal squirrels has been published (e.g., Koprowski et al. 2006; Ramos Lara &
Cervantes 2007; Ceballos et al. 2010; Ramos Lara & Cervantes 2011; Ramos Lara &
Koprowski 2012). Herein, we assessed the diversity, distribution, and conservation status of the arboreal squirrels of Mexico. We also examined the current state of scientific knowledge in the country for this diverse group of mammals.
Methods
We surveyed the literature to assess the diversity and current distribution of all the species of arboreal squirrels of Mexico. Distribution was determined based upon historical and recent records reported in the literature for each state. We used stepwise multiple regression ( F, entry = 0.05 and removal = 0.10) to examine effect of continental area of each state, mean latitude, mean altitude, area of temperate forests, and area of tropical forests on the diversity of arboreal squirrels (Table A1). Mean annual temperature and mean annual precipitation were excluded from the analysis due to high correlations with mean altitude ( r = 0.74, p < 0.0001) and mean latitude ( r = 0.76, p <
0.0001) respectively.
To assess the current state of scientific knowledge of all the arboreal squirrels of
Mexico, we surveyed the literature using the search engines JSTOR and BioOne, and
restricted our search to papers published from 1930 to 2012. The scientific and common
names of each species were used in our search, but we only considered papers that
focused on each species of arboreal squirrel from Mexico or that used specimens from
Mexico for genetic or morphological analyses. We discarded publications that mentioned 38 a species of arboreal squirrel sporadically such as the distribution of a group of species for a specific region. Each paper was classified by topic to evaluate what information has been more prevalent in the publications.
Information on the conservation status of each species was obtained from Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT 2010), the International Union for Conservation of Nature’s Red List of Threatened Species (IUCN 2011), the
Convention on International Trade in Endangered Species (CITES—www.cites.org), and surveying the literature. We used stepwise multiple regression ( F, entry = 0.05 and removal = 0.10) to explore relationship between the IUCN categories of endangerment with geographic distribution (number of states present) and number of publications for each species. The IUCN categories of endangerment were coded to reflect the following increasing level: data deficient = 1, least concern = 2, near threatened = 3, vulnerable = 4, endangerment = 5, critically endangered = 6. Similarly, stepwise multiple regression ( F, entry = 0.05 and removal = 0.10) was used to explore relationship between species richness with annual wood production and human population growth rate for each state
(Table A1). When necessary, data were transformed to meet the assumptions of normality for all analyses (Zar 1996).
Results
What is the diversity and distribution of the arboreal squirrels of Mexico?
There are currently 14 recognized species of arboreal squirrels in Mexico divided into three genera: Glaucomys , Sciurus , and Tamiasciurus (Table A2). Glaucomys and 39
Tamiasciurus are represented only by 1 (7.1%) species each, whereas Sciurus is the most diverse taxon with 12 (85.8%) species. Of these 14 species, 12 are polytypic divided into
30 subspecies and two are monotypic (i.e., S. alleni and T. mearnsi —Table A2). At the
species level only 4 (28.6%) of the 14 species are endemic to Mexico (i.e., S. alleni , S. colliaei , S. oculatus , and T. mearnsi ), whereas at the subspecies level 20 (66.7%) of the
30 subspecies are endemic (Table A2). A recent taxonomic revision of G. volans has reassigned G. v. chontali and G. v. herreranus as subspecies, increasing the number of recognized subspecies in Mexico (Thorington & Hoffmann 2005; Table A2). The subspecies G. v. madrensis always has been contentious (Goodwin 1961) and recently
has been suggested as incorrect (Ceballos & Oliva 2005). However, this may result in a
reduction in the number of recognized subspecies for the country as only two specimens
are known (Goodwin 1961; Kerhoulas & Arbogast 2010). Unlike S. auregoaster nigrescens , which also has been collected in Guatemala, S. a. aureogaster only has been collected in Mexico (Kelson 1952; Musser 1968; Hall 1981), suggesting that this subspecies may be endemic to Mexico (Table A2). Sciurus alleni has been considered a subspecies of S. oculatus due to their similarities (Best 1995a), whereas S. nayaritensis and S. arizonensis have been suggested to be subspecies of S. niger due to their close relatedness (Best 1995b). Similarly, the status of T. mearnsi has been contentious and it has been suggested to be a subspecies of T. douglasii (Arbogast et al. 2001).
Sciurus aureogaster is the species most widely distributed, present in 20 (62.5%) of the 32 states in the country, followed by S. deppei and G. volans found in 13 (40.6%) and
12 (37.5%) states respectively (Table A3). In contrast, S. arizonensis , S. griseus , S. 40 variegatoides , and T. mearnsi have limited geographic distributions restricted to 1 (3.1%) state each (Table A3). Glaucomys volans has a scattered distribution in eastern, central, and southern Mexico (Ceballos et al. 2010; Table A3). 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; Table A3). In Michoacán, G. volans only was known previously from a recorded sighting (Hooper 1952), but its presence in that state had not been confirmed. Sciurus aberti has a disjunct distribution throughout its range due to its close association with ponderosa pine, which provides both shelter and food (Nash &
Seaman 1977). However, recent information suggests that the species is not strictly dependent on ponderosa pine as previously believed (Edelman & Koprowski 2005).
Sciurus griseus has a limited distribution to northwestern Mexico (Table A3), with its population apparently disconnected from other populations in southern California
(Ceballos & Oliva 2005). In Mexico, S. griseus is known from Sierra de Juárez, but a
recent record has extended its distribution to ca. 258 km farther south of the previously
known localities (Escobar Flores et al. 2011). Interestingly, the species is absent in the
Sierra de San Pedro Mártir (Yensen & Valdés Alarcón 1999; Koprowski et al. 2006),
located south of Sierra de Juárez; however, information on its exact distribution in
Mexico is scarce (Escobar Flores et al. 2011). Although widely distributed in eastern and
central United States (Koprowski 1994), S. niger has a limited distribution to
northwestern Mexico (Table A3). However, a recent record has extended its distribution
to the state of Durango where its presence was unknown (Aragón et al. 2009). 41
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 (Fig. A1); despite the presence of temperate and tropical forests in the southern portion of the state (Table A1). Other states such as Aguascalientes, Guanajuato,
Morelos, and Tlaxcala only have a single species recorded (Fig. A1). The states along the Gulf of Mexico and in the northwestern region present high diversity of arboreal squirrels (Fig. A1). Our analysis revealed that states with larger areas of temperate forests also have a greater diversity of arboreal squirrels (β = 0.41, F1, 30 = 6.17, p =
0.019). In contrast, continental area of a state (p = 0.397), mean latitude ( p = 0.644), mean altitude ( p = 0.618), and area of tropical forests ( p = 0.609) were not associated
with diversity of arboreal squirrels.
What is the state of knowledge of the arboreal squirrels of Mexico?
Our search yielded 37 publications on the arboreal squirrels of Mexico from 1930 to 2012
(Fig. A2). Glaucomys volans has the greatest number of publications, followed by S.
aureogaster and T. mearnsi (Fig. A2). In contrast, whereas six species have only one publication, S. niger has not a single publication (Fig. A2). Most of the publications
(70.3%) consisted primarily of accounts (which summarized the current literature for each species except for S. aureogaster , S. griseus , S. niger , and T. mearnsi ), and papers
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; Fig.
A3). The remainder of the publications (29.7%) covered briefly topics on genetics (G. 42 volans , n = 1; S. aberti , n = 1; T. mearnsi , n = 1), biology ( G. volans , n = 1), 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; Fig. A3). Nonetheless, this still leaves a void in other important topics such as feeding behavior, habitat use, population dynamics, home range dynamics, life histories, and competition. Of the 37 publications, <30% had at least one researcher associated with a Mexican Institution in the states of Baja California (Universidad Autónoma de Baja California [UABC], n = 1;
Centro de Investigación Científica y de Educación Superior de Ensenada [CICESE], n =
1), Distrito Federal (Universidad Autónoma Metropolitana [UAM], n = 1, Universidad
Nacional Autónoma de México [UNAM], n = 6), Hidalgo (Universidad Autónoma del
Estado de Hidalgo [UAEH], n = 1), Puebla (Benemérita Universidad Autónoma de
Puebla [BUAP], n = 1), and Veracruz (Instituto de Ecología, A. C., n = 1).
What is the conservation status of the arboreal squirrels of Mexico?
Presently, seven of the 14 species of arboreal squirrels are federally listed in Mexico
under some category of risk (Table A2). Of these, four are listed as threatened and three
as subject to special protection; with only three subspecies also subject to special protection (Table A2). The IUCN has all 14 species included under some category of
risk, with 12 species listed as least concern, one as data deficient, and one as endangered
(Table A2). In contrast, CITES only has a single species listed (Table A2). Sciurus
aureogaster and S. colliaei are not listed in Mexico under any category of risk due to 43 their wide distribution and varied diet, whereas S. griseus , S. arizonensis , and T. mearnsi are listed due in part to their restricted distributions (Ceballos & Oliva 2005).
Surprisingly, S. niger is not listed under any category of risk, despite its restricted
distribution that lies in forests with excessive timber exploitation and conversion to
agriculture and possibly making it vulnerable (Ceballos & Oliva 2005). Other species
known to be threatened by timber exploitation and deforestation are S. aberti , S. alleni , S.
deppei , and S. oculatus (Ceballos & Oliva 2005). It has been 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 not only is threatened by
habitat destruction, but the species also has disappeared from several sites in central
Mexico during the last decade (Ceballos & Oliva 2005). Species such as S. oculatus and
S. variegatoides have been considered as ‘fragile’ by Ceballos and Navarro (1991) due to the destruction of their habitats. Riparian habitats occupied by S. arizonensis also are subject to a strong anthropogenic pressure (Ceballos & Oliva 2005). However, another potential threat for S. arizonensis is the United States proposal to build a border fence that
will prevent free movement of wildlife populations between the United States and
Mexico by eliminating biological corridors in a critical conservation state (Koleff et al.
2007). Sciurus variegatoides and S. yucatanensis have been suggested to tolerate disturbed areas (Ceballos & Oliva 2005), but unfortunately nothing is known about their ecology (Fig. A2). In portions of its range, S. aureogaster is known to cause damage to crops and is considered a pest species (Nelson 1899; Ramos Lara & Cervantes 2011). In
Chiapas, S. aureogaster and S. deppei are sold as food for human consumption or as pets 44 by the Tzeltal and Lacandon communities (Naranjo et al. 1994; Ceballos & Oliva 2005;
Barragán et al. 2007). Similarly, S. nayaritensis is hunted for sport and human
consumption (Ceballos & Oliva 2005). In Baja California, a potential threat to T.
mearnsi is the introduction of S. carolinensis to the Sierra de San Pedro Mártir (Yensen
& Valdés Alarcón 1999). However, S. carolinensis was not observed in the Sierra during a recent survey (Koprowski et al. 2006).
Our analysis revealed that neither the geographic distribution of arboreal squirrels nor the number of publications were associated with the IUCN categories of endangerment ( F2, 11 = 0.631, p = 0.550). Nonetheless, states with a greater diversity of
arboreal squirrels also have higher annual wood productions (β = 0.451, F1, 30 = 6.17, p =
0.011). In contrast, human population growth rate in each state was not associated with
diversity of arboreal squirrels ( p = 0.480).
Conclusions
Mexico harbors a high diversity of arboreal squirrels with a great number of endemic species and subspecies. However, we did not observe a latitudinal cline like that reported for all arboreal squirrels together at a global scale (Koprowski & Nandini 2008), possibly due to the high diversity recorded in both Nearctic and Neotropical regions of Mexico.
Our analysis revealed that states with larger areas of temperate forests also have a greater diversity of arboreal squirrels. Unfortunately, the recent records of G. volans , S. griseus , and S. niger at new locations clearly show that the exact distribution of arboreal squirrels is still unknown, especially in temperate forests of the country. Species with restricted 45 distributions in Mexico have similar IUCN categories of endangerment than those with wide distributions, possibly due to their wide distributions in North and Central America.
Among these species, S. arizonensis , S. griseus , and S. variegatoides also are federally listed under some category of risk by SEMARNAT (2010) due to their restricted distributions; except for S. niger , which perhaps should be listed also under a category of risk in the country.
Compared to other countries in North America and Europe, where arboreal squirrels have been studied extensively (e.g., Steele & Koprowski 2001; Koprowski & Nandini
2008), little is known about the arboreal squirrels in Mexico. For instance, T. hudsonicus from North America and S. vulgaris from Eurasia have more than 260 and 460 publications, respectively, far surpassing the number of publications for all the arboreal squirrels in Mexico collectively (Koprowski & Nandini 2008; Fig. A2). Few publications with at least one researcher associated with a Mexican institution suggest that a lack of interest exists for studying this group of mammals; especially in the states of Chiapas and
San Luis Potosí. Number of publications was not associated with the IUCN categories of endangerment, possibly due to 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 categories of risk possibly should be higher than other species of arboreal squirrels. However, only S. oculatus is federally listed under a category of risk by SEMARNAT (2010). Similarly, practically nothing is known about the populations of S. niger in the country. 46
More information on the ecology of these species is necessary to establish suitable plans to protect Mexico’s high diversity of arboreal squirrels and their habitats; especially
for those endemic and with restricted distributions. In Mexico, populations of 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 extensively studied in North America and Europe (Koprowski & 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 & Cervantes
2011). For instance, recent publications have revealed that important aspects of the
ecology of T. mearnsi differ from other congeners located at higher latitudes (Koprowski
et al. 2006; Ramos Lara & Koprowski 2012). As a result, using information from other
Tamiasciurus located at higher latitudes to create conservation plans for T. mearnsi could be uncertain and problematic.
Worldwide, our knowledge on arboreal squirrels not only is poor relative to their
conservation status, but forested environments also are disappearing rapidly (Koprowski
& Nandini 2008). In Mexico, like in other countries of Latin America (Mares 1986;
Bradshaw et al. 2009), conservation is a multi faceted problem with the exploitation and
management of natural resources usually based on political decisions rather than on
scientific data (Ceballos & Navarro 1991). Annual rates of deforestation over 1%
nationwide pose threats to biodiversity and conservation in the country (Sánchez Cordero
et al. 2005). Mexico has lost more than 95% of its tropical forests and more than 50% of 47 its temperate forests (Céspedes Flores & Moreno Sánchez 2010). Our analysis revealed that states with the greatest diversity of arboreal squirrels also have the highest annual wood productions, possibly posing a threat to their persistence in the country. In particular, the states of Veracruz, Chiapas, Tabasco, and Colima have the highest rates of deforestation over 1.0% (Céspedes Flores & Moreno Sánchez 2010); both Veracruz and
Chiapas with a high diversity of arboreal squirrels. In contrast, other states with a high diversity such as San Luis Potosí, Durango, Sonora, and Chihuahua have deforestation rates under 0.1% (Céspedes Flores & Moreno Sánchez 2010). Nonetheless, species such as S. aberti may be threatened by timber exploitation in portions of its range in Sonora,
Chihuahua, and Durango (Ceballos & 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 (Brandon et al. 2005) that arboreal squirrels provide to ecosystems. Although known to cause damage to crops (Valdés Alarcón 2003; Ramos
Lara & 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 due to their close associations with specific vegetation types, and are an important food source for many predators (Valdés Alarcón 2003; Koprowski &
Nandini 2008). As a result, arboreal squirrels may be used to monitor forest condition
and in turn protect other species. However, because regional differences in the ecology
of a species may hinder its use as an indicator in other geographical areas (Smith et al.
2005), it is vital to obtain relevant ecological data from the arboreal squirrels of Mexico 48 to establish suitable plans for their conservation, rather than use solely data from
Holarctic arboreal squirrels. As in other countries with high biological diversity and limited financial resources, national and international efforts may be required to preserve the biological heritage of Mexico (Ceballos & Navarro 1991).
Acknowledgments
The Consejo Nacional de Ciencia y Tecnología (CONACYT) and the Wallace Research
Foundation provided financial support to N. R L. E. E. Posthumus, J. J. Derbridge, J. L.
Bronstein, M. J. Merrick, R. W. Mannan, S. J. Blount, and W. Shaw provided helpful comments that improved the manuscript.
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56
Table A1. Continental area for each state of Mexico (km 2), its relative size in the country (%), mean latitude, mean altitude (meters above sea level), mean annual temperature ( oC), mean annual precipitation (mm), area size of temperate forests
(km 2), area size of tropical forests (km 2), annual wood production (m 3r), and human population growth rate.
State Area % Latitude Altitude oC 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 71445.9 3.6 30.0 1555 19.6 169.4 1608.6 0 75 2.3
Baja California Sur 73922.5 3.8 25.3 1055 23.3 261.7 346.1 3874.3 2554 4.0
Campeche 57924.4 3.0 19.0 200 25.8 1464.6 28.2 9200.7 77679 1.7
Chihuahua 247455.3 12.6 28.4 2370 17.3 370.5 58891.9 3921.7 1033181 1.1
Chiapas 73288.8 3.7 16.0 2300 20.3 2388.5 6601.3 7066 120607 2.0
Coahuila 151562.6 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 123451.3 6.3 24.4 2610 16 597.1 38894.9 4451 1741212 1.2
Guanajuato 30608.4 1.6 20.5 2555 18.1 590.9 2379.1 38 31200 1.6 57
Guerrero 63620.7 3.2 17.4 2125 26.3 1282.5 13601.5 4021.5 123540 0.9
Hidalgo 20846.5 1.1 20.3 2595 16.0 1332.1 2609.6 39.36 148507 1.7
Jalisco 78599.2 4.0 20.5 2900 25.2 989.6 14151.2 5000.9 322913 1.5
México 22356.8 1.1 19.2 4080 11.6 762.6 4075.5 164 145510 1.4
Michoacán 58643.4 3.0 18.9 2880 20.6 998.4 9446 5694.1 619422 0.9
Morelos 4892.7 0.2 18.6 3505 20.4 1170.7 308.1 40.9 3760 1.3
Nayarit 27815.2 1.4 21.7 1840 21.7 1123.1 5640.1 3242.3 25905 1.6
Nuevo León 64220.2 3.3 25.3 2125 18.1 622.2 4528.4 94.95 26780 1.9
Oaxaca 93793.3 4.8 16.9 2635 21.7 2020.2 8760 12673.7 415049 1.0
Puebla 34289.7 1.7 19.0 3835 17.5 1260 3208.9 1382.3 223089 1.3
Querétaro 11683.8 0.6 20.7 2590 19.4 619.2 1149.9 623.2 9601 2.6
Quintana Roo 42361.0 2.2 19.5 120 25.7 1301.4 4.5 11106.4 34487 4.1
San Luis Potosí 60982.8 3.1 22.7 2510 21.3 648.7 3667.2 1498.5 2968 1.1
Sinaloa 57377.2 2.9 24.6 1290 24.9 635.7 7827.4 15104 44429 0.9
Sonora 179502.9 9.2 29.5 1415 22.0 370.2 16205.4 23618 162646 1.8 58
Tabasco 24737.8 1.3 17.8 455 27.2 2506 14.7 839.4 17006 1.6
Tamaulipas 80174.7 4.1 24.8 1800 20.6 909.8 4674.3 5904.8 138766 1.7
Tlaxcala 3991.1 0.2 19.3 3330 15.3 670.7 361.3 0 19789 1.9
Veracruz 71820.4 3.7 19.7 3235 17.4 1334.3 1435.3 1420.2 264845 1.0
Yucatán 39612.2 2.0 20.3 110 25.8 862.7 0 446.9 2195 1.6
Zacatecas 75539.3 3.9 23.0 2715 18.3 570.9 6394 456.3 41063 0.9
Data sources: Instituto Nacional de Estadística y Geografía (INEGI—www.inegi.gob.mx), Secretaría de Medio Ambiente y
Recursos Naturales (SEMARNAT—www.semarnat.gob.mx). 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. 59
Table A2. List of species and subspecies of arboreal squirrels currently recognized in Mexico, their distribution, and their conservation status according to Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT), International Union for Conservation of Nature (IUCN), and Convention on International Trade in Endangered Species (CITES). Protection is specified for species and subspecies accordingly.
Species Subspecies Distribution SEMARNAT IUCN CITES
Glaucomys volans Threatened Least concern
chontali Endemic
goldmani Endemic
guerreroensis Endemic
herreranus Endemic
madrensis Endemic
oaxacensis Endemic
Sciurus aberti Least concern
barberi Endemic Subject to special protection
durangi Endemic Subject to special protection 60
phaeurus Endemic Subject to special protection
Sciurus alleni Endemic Least concern
Sciurus arizonensis Threatened Data deficient
huachuca
Sciurus aureogaster Least concern
aureogaster Endemic
nigrescens
Sciurus colliaei Least concern
colliaei Endemic
nuchalis Endemic
sinaloensis Endemic
truei Endemic
Sciurus deppei Least concern III/w
deppei
negligens Endemic 61
vivax
Sciurus griseus Threatened Least concern
anthonyi
Sciurus nayaritensis Least concern
apache Endemic
nayaritensis Endemic
Sciurus niger Least concern
limitis
Sciurus oculatus Subject to special protection Least concern
oculatus Endemic
shawi Endemic
tolucae Endemic
Sciurus variegatoides Subject to special protection Least concern
goldmani
Sciurus yucatanensis Least concern 62
baliolus
phaeopus
yucatanensis
Tamiasciurus mearnsi Endemic Threatened Endangered
Data sources: Diersing 1980; Hall 1981; Lindsay 1981; Yensen & Valdés Alarcón 1999; Villa & Cervantes 2003; Ceballos
& Oliva 2005; Ramírez Pulido et al. 2005; Thorington & Hoffmann 2005; SEMARNAT 2010; IUCN 2011; CITES
(www.cites.org). 63
Table A3. Presence of the 14 species of arboreal squirrels ( Glaucomys , Sciurus , and Tamiasciurus ) recognized in
Mexico by state based on published records.
Species
State Code volans G. aberti S. alleni S. arizonensis S. aureogaster S. collieries S. deppei S. griseus S. nayaritensis S. niger S. oculatus S. variegatoides S. yucatanensis S. T.mearnsi Aguascalientes AS x
Baja California BC x x
Baja California Sur BS
Campeche CC x x
Chihuahua CH x x x x
Chiapas CS x x x x x
Coahuila CL x x
Colima CM x x
Distrito Federal DF x x 64
Durango DG x x x x
Guanajuato GT x
Guerrero GR x x
Hidalgo HG x x x x
Jalisco JC x x x
México MC x x x
Michoacán MN x x
Morelos MS x
Nayarit NT x x x
Nuevo León NL x x x x
Oaxaca OC x x x
Puebla PL x x x x
Querétaro QT x x x x
Quintana Roo QR x x
San Luis Potosí SP x x x x x 65
Sinaloa SL x x
Sonora SR x x x x
Tabasco TC x x x
Tamaulipas TS x x x x
Tlaxcala TL x
Veracruz VZ x x x x
Yucatán YN x x
Zacatecas ZS x x
Data sources: Musser 1968; Diersing 1980; Hall 1981; Álvarez Castañeda 1996; Jiménez Guzmán et al. 1997; Yensen &
Valdés Alarcón 1999; Villa & Cervantes 2003; Ceballos & Oliva 2005; Núñez Garduño 2005; Sánchez Hernández et al. 2005;
Aragón et al. 2009; Ceballos et al. 2010.
66
Figure Legends
Figure A1. Number of species of arboreal squirrels recognized in Mexico by state.
For meaning of the state codes see Table 2.
Figure A2. Number of publications ( N = 37) from 1930 to 2012 for each species of
arboreal squirrel ( Glaucomys , Sciurus , and Tamiasciurus ) recognized in Mexico. Each publication focused completely on a species located within Mexico or included specimens collected from Mexico.
Figure A3. Percentage of topics for all the publications ( N = 37) on arboreal squirrels recognized in Mexico from 1930 to 2012.
67 Figure A1
68 Figure A2
69 Figure A3
70
APPENDIX B
NEST SITE CHARACTERISTICS OF THE MONTANE ENDEMIC MEARNS’S
SQUIRREL ( TAMIASCIURUS MEARNSI ): AN OBLIGATE CAVITY NESTER?
Manuscript prepared for submission to Journal of Mammalogy
71
Send proofs to: Nicolas Ramos Lara Wildlife and Fisheries Science School of Natural Resources and the Environment 325 Biological Sciences East Building The University of Arizona Tucson, AZ 85721 USA Email: [email protected]
Running Heading: Nest sites of Tamiasciurus mearnsi
Nest-site characteristics of the montane endemic Mearns’s squirrel ( Tamiasciurus
mearnsi ): an obligate cavity-nester?
NICOLÁS RAMOS LARA ,* JOHN L. KOPROWSKI , AND DON E. SWANN
Wildlife and Fisheries Science, School of Natural Resources and the Environment,
University of Arizona, Tucson, AZ 85721, USA (NR L, JLK)
Saguaro National Park, Rincon Mountain District, 3693 South Old Spanish Trail,
Tucson, AZ 85730, USA (DES)
Many animals depend on nests for their survival and reproduction, with some species considered obligate tree cavity nesters. The Mearns’s squirrel ( Tamiasciurus mearnsi ) is a species endemic to the Sierra de San Pedro Mártir, Baja California, which relies on tree cavities for nesting. Federally listed as threatened in Mexico, and as endangered by the International Union for Conservation of Nature (IUCN), the ecology of this southernmost Tamiasciurus is poorly known. We examined if Mearns’s squirrels 72 have specific nesting requirements compared to other arboreal squirrels. We also assessed if nesting requirements differ between sexes and between breeding and nonbreeding females. We used telemetry to locate the nests and 10 m radius circular plots to compare habitat characteristics between nest sites and random sites. Tree cavities are scarce structures in the Sierra de San Pedro Mártir, possibly limiting the population and distribution of Mearns’s squirrels. Nest tree species, nest tree condition, nest tree size (DBH), canopy cover, and occurrence of white firs ( Abies concolor ) are important
characteristics for nesting. Nest sites of males did not differ from those of females except
for nest tree condition. Females apparently do not have specific nesting requirements for
rearing young. Unlike other congeners that also build leaf nests and underground burrows for nesting, large trees and snags that facilitate cavity formation are critical for
the conservation of this species. Mearns’s squirrels provide an important opportunity to
learn more about the mechanism of geographic variation in nesting behavior.
Key words: Baja California, cavity nests, endemic species, Mexico, nest sites, Sciurus , secondary cavity nester, Sierra de San Pedro Mártir, tree cavities
*Correspondent: [email protected]
In forest ecosystems, cavity nesting species comprise a structured community that interacts through the creation and competition for nest sites (Martin et al. 2004). Cavity nesters are commonly grouped as weak excavators, strong excavators, and secondary cavity nesters (Steeger and Dulisse 2002). Weak and strong excavators build their own 73 cavities, whereas secondary cavity nesters always use old, existing cavities (Wiebe et al.
2007). Secondary cavity nesters include a variety of passerines, ducks, birds of prey, and small mammals that require but cannot excavate cavities. Thus, they rely on nests created by excavators or a limited number of naturally occurring holes (Martin et al.
2004). In particular, densities of secondary cavity nesters are often assumed to be primarily limited by nest sites (Miller 2010). Nests are critical for raising young, rest, predator avoidance, and shelter from adverse weather (Steele and Koprowski 2001).
Because males and females have specific but often divergent biological needs, especially in mammals where pair bonding is rare (Curley and Keverne 2005), nesting requirements are expected to differ between sexes (e.g., Edwards and Guynn 1995; Hanski et al. 2000;
Meek and Barclay 1996; Thogmartin 1999); however, this seldom has been examined.
Quality of nest sites also has been associated with fitness correlates such as probability of predation and nesting success (Cain et al. 2003; Li and Martin 1991). As a result, information on nest site characteristics may allow researchers to assess habitat suitability and management (Ramos Lara and Cervantes 2007).
In mammals, few cavity using animals are obligates (Carey 2002). Tree squirrels in particular use three types of nests for resting and rearing young: spherical constructed from leaves and twigs (known as dreys), cavities within live trees and snags, and occasionally holes in the ground (Gurnell 1987). However, some female tree and flying squirrels prefer to rear young in tree cavities rather than dreys (Edelman and Koprowski
2006), indicating that female squirrels may have specific nesting requirements compared to males. This seems to be the case of the tree squirrels in the genus Tamiasciurus . The 74 genus contains three species (Thorington and Hoffmann 2005): Douglas’s squirrels ( T. douglasii ), red squirrels ( T. hudsonicus ), and Mearns’s squirrels ( T. mearnsi ). Douglas’s and red squirrels prefer natural tree cavities for nesting, but where suitable cavities are lacking, squirrels construct dreys and occasionally underground burrows (Edelman et al.
2009; Hamilton 1939; Layne 1954; Leonard and Koprowski 2009; Merrick et al. 2007;
Steele 1998; Verts and Carraway 1998). In contrast, Mearns’s squirrels use tree cavities for nesting (Koprowski et al. 2006; Ramos Lara and Koprowski 2012), suggesting that unlike other congeners, Mearns’s squirrels may be obligate secondary cavity nesters. As a result, Mearns’s squirrels may have specific nesting requirements compared to
Douglas’s and red squirrels that also use dreys and underground nests (Arsenault 2004;
Edelman et al. 2009; Robb et al. 1996; Thogmartin 1999). However, no further information on the nesting requirements of Mearns’s squirrels exists to date (Koprowski et al. 2006; Ramos Lara and Koprowski 2012; Yensen and Valdés Alarcón 1999), despite the 100 years since the species was described (Allen 1893; Townsend 1897).
Besides food, few other resources are more important to tree squirrels than nests (Steele and Koprowski 2001), with tree cavities considered an important and potentially limiting resource. However, the importance of nests in different forest types and tree species is also unknown (Edelman and Koprowski 2006).
Tamiasciurus mearnsi is an endemic species that occurs only in the coniferous forests of the Sierra de San Pedro Mártir (SSPM), Baja California (Lindsay 1981).
Mearns’s squirrels are separated from the nearest populations of Douglas’s and red squirrels by ca. 600 km of mostly nonforested lowlands (Yensen and Valdés Alarcón 75
1999). However, the exact distribution of Mearns’s squirrels in the SSPM Mountains is unknown, except for three collection locations <10 km apart reported in the literature
(Lindsay 1981; Yensen and Valdés Alarcón 1999). Mearns’s squirrels likely became isolated from Douglas’s squirrels most recently about 12,000 years ago (Arbogast et al.
2001; Lindsay 1981; Yensen and Valdés Alarcón 1999). The species is known from ca.
2,100 m to 2,750 m elevation in the coniferous forests of SSPM (Yensen and Valdés
Alarcón 1999). Considered a rare species (Huey 1964), Mearns’s squirrels are federally listed as threatened in Mexico (SEMARNAT 2010), due to their restricted distribution, low population density, and isolation, and as endangered by the International Union for
Conservation of Nature (IUCN—de Grammont and Cuarón 2008). Herein, we examined if Mearns’s squirrels have specific nesting requirements compared to other congeners that also use dreys and underground nests. We predicted that habitat characteristics used by
Mearns’s squirrels would facilitate the formation of tree cavities compared to random sites. We also predicted different nesting requirements between males and females and between breeding and nonbreeding females.
MATERIALS AND METHODS
Study area.—SSPM is located ca. 100 km southeast of Ensenada, Baja California,
Mexico (Stephens et al. 2003). SSPM was established as a Forest Reserve in 1932, as a
National Park in 1947, and has been proposed as a Biosphere Reserve (Bojórquez Tapia
et al. 2004). SSPM National Park comprises 65,000 ha of which coniferous forests cover
ca. 40,655 ha (Minnich et al. 2000). Forests are composed of Jeffrey pine ( Pinus jeffreyi ), sugar pine ( P. lambertiana ), lodgepole pine ( P. contorta ), white fir ( Abies 76 concolor ), and limited amounts of quaking aspen ( Populus tremuloides ) and incense cedar ( Calocedrus decurrens ). The most common forest types are Jeffrey pine, Jeffrey pine–mixed conifer, and mixed white fir forests, respectively (Stephens et al. 2003).
Mixed conifer forest on the summit plateau is replaced by chaparral and Sonoran Desert scrub at lower elevations. The most striking feature of the mixed conifer forests is an open park like aspect that consists of mature trees reaching 30–45 m, with few pole sized trees and saplings, and an open shrub cover (Bojórquez Tapia et al. 2004). Elevation averages 2,600 m in the north and decreases to 1,800 m in the southern portion of the range with the highest peaks over 3,000 m (Stephens et al. 2003). Compared to other forests in North America, forests in SSPM have not experienced disturbance from logging and fires have spread without human interference (Minnich et al. 2000).
Summers are dry except for afternoon thunderstorms of the North American monsoon
(Minnich et al. 2000). According to data recorded by Servicio Meteorológico Nacional at ejido San Matías, located ca. 25 km north of SSPM, mean (± SD ) monthly temperature in the region remained similar throughout the study (19.2 °C ± 6.59). In contrast, mean monthly precipitation in 2005 (22.8 mm ± 25.7) was greater than 2006 (9.0 mm ± 16.5) and 2007 (10.7 mm ± 13.5). Hairy woodpeckers ( Picoides villosus ) and northern flickers
(Colaptes auratus ) are the most common species of tree cavity excavators recorded above 2,600 m in SSPM (Gómez de Silva 2002).
Large scale surveys.—During 2005, we surveyed ca. 2,500 ha of forest in the margins of the Vallecitos Meadow, where the species was collected previously for museum specimens (Lindsay 1981; Yensen and Valdés Alarcón 1999), to detect direct 77
(animal sighting) and indirect (remnants of food with characteristic gnawing) occurrence of Mearns’s squirrels and to establish potential capture sites. We explored the area on foot systematically using a topographic map (Centra Publications 1988).
Trapping and telemetry.―We used telemetry to locate the cavity nests of Mearns’s squirrels. Animals were captured during May August 2006 and 2007. Live traps (Model
201; Tomahawk Live Trap Co., Wisconsin) were placed at the base of large diameter trees, baited with peanuts and peanut butter, covered with tree bark, and checked at 1 hr intervals. Captured squirrels were transferred to a cloth handling cone (Koprowski 2002) where we collected data on sex, age class, reproductive condition, and body mass. Adult animals (≥240 g) were fitted with radio collars (Model SOM 2190; Wildlife Materials
International, Inc., Carbondale, Illinois) and uniquely numbered Monel ear tags (Style
#1005 1; National Band and Tag Co., Newport, Kentucky) with colored plastic washers
(Style #1842; National Band and Tag Co., Newport, Kentucky) on both ears. We distinguished adults and juveniles based on reproductive condition and body mass of captured animals. All squirrels were released at the capture site after ≤8 min of handling time; no animals were injured during the study. Trapping and handling procedures were conducted with approval from The University of Arizona Institutional Animal Care and
Use Committee (protocol # 05 038), in accordance with guidelines of the American
Society of Mammalogists (Gannon et al. 2007), and with permits from the following
Mexican authorities: Dirección Forestal y de la Fauna Parque Nacional Sierra de San
Pedro Mártir and Dirección General de Vida Silvestre. 78
Nest identification .―We tracked squirrels to their nests using a 3 element yagi directional antenna (Wildlife Materials International, Inc., Carbondale, Illinois) and receiver (Model R 1000, Communications Specialists, Inc., Orange, California) in spring
(April) and fall (September November) and weekly during summer (May August); we did not monitor animals during winter (December March) due to snow and limited access. Based on the presence of litters and the reproductive condition of radio collared females, we recorded tree cavities that were used by breeding females (known as maternity nests) and nonbreeding females (hereafter referred to as nonmaternity nests).
Habitat characteristics.―For each cavity nest, we recorded height and aspect
(degrees). For each nest tree, we recorded species, height, diameter at breast height
(DBH), condition (live/dead), crown size of live trees (radius of 4 cardinal directions averaged), and number of trees (≥5 cm DBH) with interlocked crowns to the nest tree.
For each nest site, we recorded distance to nearest tree (≥5 cm DBH), total number of trees (≥5 cm DBH), total number of logs (≥15 cm diameter and ≥1.5 m length), slope
(degrees), slope aspect (degrees), and percentage canopy cover at 0 m, 5 m, and 10 m from the nest tree in the 4 cardinal directions (north, south, west, and east); measurements were averaged for each distance (percentage canopy cover at 0 m, 5 m, and 10 m) and for the entire nest site (percentage canopy cover). In addition, we recorded species, condition, and DBH of all trees (≥5 cm DBH) at each nest site. Tree condition was classified using the following classes: live (class 1), dead with intact branches (class 2), and snag with trunk broken (class 3). Based on the habitat characteristics recorded at nest sites, we calculated the following variables (number per hectare): small trees/ha (trees 79 with ≥5 cm DBH and <40 cm DBH), medium trees/ha (trees with ≥40 cm DBH and <85 cm DBH), large trees/ha (trees with ≥85 cm DBH), Jeffrey pines/ha, lodgepole pines/ha, white firs/ha, trees/ha, live trees/ha, dead trees/ha, snags/ha, logs/ha, basal area of all trees (m 2/ha), and species richness. Relative dominance, relative density, and relative
frequency of each species of tree were determined for all nest sites (Muller Dombois and
Ellenberg 1974). The Shannon diversity index ( H’ ) and evenness ( E) also were calculated for all nest sites (Magurran 1988).
We measured nest site characteristics using 10 m radius circular plots (0.03 ha) with the nest tree at the center (Muller Dombois and Ellenberg 1974). Nest height, nest tree height, and slope were measured using a Haglöf electronic clinometer (Haglöf
Sweden; Forestry Suppliers, Inc., Mississippi). Crown size, DBH, and distances were measured using a metric fabric diameter tape (Model: 283D; Forestry Suppliers, Inc.,
Mississippi). Distances were marked using plain vinyl stake wire flags (Forestry
Suppliers, Inc., Mississippi). Percentage canopy cover was measured using a GRS
Densitometer (Forestry Suppliers, Inc., Mississippi). For comparison with nest sites, we used random trees to measure habitat availability for nesting. Randomly generated numbers were used to denote distance and direction, and the nearest tree with ≥40 cm
DBH was used as the center of a 10 m radius circular plot from which the same data were collected. Focal random trees with ≥40 cm DBH are large enough to contain cavities that may be used by Mearns’s squirrels for nesting (Gurnell 1987).
Data analysis.—We used unpaired t tests, Mann Whitney ( U), and the Mardia
Watson Wheeler ( W) test for circular analysis (Magurran 1988; Zar 1996) to examine 80 differences between nest sites and random sites, nest sites of males and females, and nest sites of females with maternity and nonmaternity nests. Rayleigh’s (Z) test was used to analyze random distributions around 360º for both nest aspect and slope aspect (Zar
1996). We used chi square (χ 2) to compare categorical variables between sites, with subsequent Bonferroni simultaneous confidence intervals to establish selection (Marcum and Loftsgaarden 1980; Neu et al. 1974). Pearson correlation ( r) was used to explore
relationship between nest tree height and cavity nest height. We used stepwise
discriminant function analyses (DFA) to determine the habitat characteristics that best
discriminated between nest sites and random sites, nest sites of males and females, and
nest sites of females with maternity and nonmaternity nests (McGarigal et al. 2000).
Selection criteria for entry and removal of variables for nest sites and random sites were:
F, entry = 3.0 and removal = 2.5, and for nest sites of males and females and nest sites of
females with maternity and nonmaternity nests: F, entry = 2.0 and removal = 1.5. Prior
to stepwise DFA, we removed highly correlated variables (r > 0.70) to prevent
multicollinearity. For each pair of highly correlated variables, only the variable that best
discriminated (higher F value in one way ANOVA) was used in stepwise DFA
(McGarigal et al. 2000). We used principal component analyses (PCA) to assess the
variables that accounted for most of the variance between nest sites and random sites,
nest sites of males and females, and nest sites of females with maternity and
nonmaternity nests (McGarigal et al. 2000). Unpaired t tests were used to compare principal component scores between nest sites and random sites, nest sites of males and
females, and nest sites of females with maternity and nonmaternity nests. 81
We conducted all statistical analyses with SPSS 17.0 (SPSS Inc., Chicago) and
Oriana 3.0 (Kovach 2009). When necessary, variables were log transformed to better meet the assumptions of univariate and multivariate tests (McGarigal et al. 2000; Zar
1996); however, means ± SD shown in the results are from untransformed values.
Because the same data were used for multiple comparisons, we adjusted our alpha level to 0.017 with a Bonferroni correction for all our analyses (Pallant 2007).
RESULTS
We captured 38 adult Mearns’s squirrels (20 males, 18 females). Squirrels used
tree cavities in 424 of 426 (99.5%) nesting events, with only one adult male nesting
underground on 2 (0.5%) occasions during August 2007. In total, we located 115 cavity
nests of which 21 were used as maternity nests. As a result, we used 115 random trees to
measure habitat availability for nesting to maintain equal sample sizes.
Only 3 (2.6%) of the 115 random trees contained cavities. On average, cavity nests
were located higher than tree cavities found in random trees (Table B1). However, cavity
height was not correlated with nest tree height ( r = 0.12, n = 79, P = 0.29). Entrances to cavities in nest trees ( Z = 0.48, n = 76, P = 0.62) and random trees ( Z = 0.13, n = 2, P =
0.90) were not oriented in any particular direction (Table B1). Tree species were not
2 used relative to their availability (χ 2 = 13.019, P = 0.0015); Jeffrey pines were used
similarly to their availability (98% CI = 0.70 0.90), whereas lodgepole pines were used
7.5 times less (98% CI = 0.00 0.11) and white firs 14.0 times more (98% CI = 0.06 0.23;
Fig. B1). Because dead trees (class 2) and snags (class 3) did not differ within nest trees
(U = 6098.5, n1 = 115, n2 = 115, P = 0.07) and focal random trees ( U = 6437.0, n1 = 115, 82
n2 = 115, P = 0.42), we pooled both classes into a single variable, hereafter referred to as
2 dead trees. Live and dead trees were not used relative to their availability (χ 1 = 48.79, P
< 0.0001); live trees were used 1.7 times less than their availability whereas dead trees were used 8.7 times more (Fig. B2). Nest trees had crowns 1.7 times greater than focal trees at random sites ( t170 = 9.67, P < 0.0001; Table B1). Slope aspect at nest sites was not oriented in any particular direction (Z = 1.48, n = 115, P = 0.23) and did not differ from random sites ( W = 2.58, P = 0.28; Table B1). Percentage canopy cover, trees/ha, live trees/ha, and small trees/ha did not differ between nest sites and random sites (all P >
0.05; Table B1).
Four of the 17 characteristics used in stepwise DFA differed between nest sites and
2 random sites (Wilks’ λ = 0.48, χ 7 = 164.24, P < 0.001; Table B2). Nest sites had nest
trees 1.5 times larger (DBH), with 1.8 times fewer interlocked trees, 1.2 times less
canopy cover at 0 m, and 5.0 times more occurrence of white firs/ha than those at random
2 sites (eigenvalue = 1.08, χ 7 = 164.24, P < 0.001; Table B3). High PC 1 loadings at nest sites (variance = 30.8%) and random sites (variance = 25.1%) were associated with density of small Jeffrey pines and white firs (Table B4), but this component did not differentiate between sites ( t228 = 9.2E 09, P > 0.99; Fig. B3). High PC 2 loadings at nest
sites (variance = 15.7%) and random sites (variance = 13.4%) were associated with
canopy cover (Table B4), with no difference between sites (t228 = 1.1E 05, P > 0.99; Fig.
B3). Tree diversity ( H’ ) at nest sites ( H’ = 0.72, S = 5, E = 0.45, n = 609) was 2.3 times higher than that at random sites ( H’ = 0.32, S = 5, E = 0.20, n = 742; H’ max = 1.61; t1318 =
8.60, P < 0.0001). This difference was due to the absence of sugar pines and quaking 83 aspens at nest sites and random sites, respectively, and to the difference in abundance among tree species (Table B5). Jeffrey pines had the greatest relative dominance, relative density, and relative frequency at nest sites and random sites. However, unlike
Jeffrey pines, white firs at nest sites had higher relative dominance, relative density, and relative frequency than those at random sites (Table B5).
2 Nest sites of males and females only differed in nest tree condition (χ 1 = 8.98, P =
0.003), with no differences in any other of the characteristics analyzed using univariate
tests (all P > 0.06; Table B1). Females used 1.8 times more live trees for nesting,
whereas males used 2.1 times more dead trees (Fig. B2). In contrast, tree species used for
2 nesting did not differ between males and females (χ 2 = 0.08, P = 0.96; Fig. B1).
2 Stepwise DFA indicated a difference between sexes (Wilks’ λ = 0.85, χ 4 = 14.53, P =
0.006), but none of the variables included in the model were significant after the
Bonferroni correction (Table B2). High PC 1 loadings at nest sites of males (variance =
31.1%) and females (variance = 28.5%) were associated with density of small Jeffrey pines and white firs (Table B4), with no difference between sites (t93 = 1.3E 06, P >
0.99). High PC 2 loadings at nest sites of males (variance = 16.3%) and females
(variance = 17.2%) were associated with canopy cover (Table B4), with no difference between sites (t93 = 6.8E 07, P > 0.99). Similarly, tree diversity did not differ between
nest sites of males ( H’ = 0.77, E = 0.48) and females ( H’ = 0.69, E = 0.43; t542 = 1.62, P =
0.24; Table B5).
Nest sites of females with maternity and nonmaternity nests did not differ in any of
the habitat characteristics analyzed using univariate tests (all P > 0.18; Table B1) and 84
2 2 stepwise DFA (Wilks’ λ = 0.91, χ 2 = 4.80, P = 0.09; Table B3). Tree species (χ 2 = 0.43,
2 P = 0.81; Fig. B1) and tree condition (χ 1 = 0.001, P = 0.97; Fig. B2) did not differ between sites. High PC 1 loadings at sites with maternity (variance = 35.7%) and
nonmaternity nests (variance = 27.1%) were associated with density of small Jeffrey pines and white firs (Table B4), with no difference between sites ( t51 = 3.0E 06, P >
0.99). High PC 2 loadings at sites with maternity (variance = 16.0%) and nonmaternity
nests (variance = 17.8%) were associated with canopy cover (Table B4), with no
difference between sites ( t51 = 1.8E 05, P > 0.99). Similarly, tree diversity did not differ between sites with maternity ( H’ = 0.59, E = 0.37) and nonmaternity nests ( H’ = 0.74, E
= 0.46; t239 = 1.62, P = 0.11; Table B5).
DISCUSSION
Mearns’s squirrels use primarily tree cavities for nesting (Koprowski et al. 2006;
Ramos Lara and Koprowski 2012); although one adult nested underground, this behavior
is rare. As potentially obligate secondary cavity nesters, low occurrence of tree cavities
in SSPM may limit population growth and distribution of Mearns’s squirrels (Boyle et al.
2008; Edelman and Koprowski 2006; Kantola and Humphrey 1990; Loeb 1993). To
compensate for lack of suitable tree cavities, other species of arboreal squirrels construct
dreys and underground burrows (Brown 1986; Edelman et al. 2009; Edwards and Guynn
1995; Gurnell 1987; Hackett and Pagels 2003; Hanski et al. 2000; Layne 1954; Verts and
Carraway 1998). However, the reason for the lack of dreys in Mearns’s squirrels
compared to other arboreal squirrels remains unknown. Reported as rare and occurring
in limited numbers (Huey 1964; Yensen and Valdés Alarcón 1999), Mearns’s squirrel 85 population may be possibly influenced by access to suitable nest sites as suggested for other secondary cavity nesters (Miller 2010).
Mearns’s squirrels have specific nesting requirements with white firs, large trees, and snags, being important resources for nesting, similar to other species of arboreal squirrels (Merrick et al. 2007; Meyer et al. 2005). As secondary cavity nesters, large snags are expected to be important resources for Mearns’s squirrels as cavity nests are typically found in large diseased or damaged trees, but particularly in large snags
(Holloway and Malcolm 2007). However, large snags are not common resources in the study area, which may account for the high use of cavities in live trees. Because woodpeckers use mostly live trees and hard snags for nesting (Steeger and Dulisse
2002), Mearns’s squirrels may depend strongly on these primary cavity nesters for suitable nest sites. Higher frequency of cavity nests in live trees also has been reported in other species of tree and flying squirrels (Bendel and Gates 1987; Edelman and
Koprowski 2006). Contrary to dead trees, live trees may be more suitable as nest sites for cavity nesters because overhead branches provide protection from weather, increased cover, and structural complexity for predator avoidance (Cotton and Parker 2000).
Cavities in larger trees may provide more stability and protection from the effects of wind and cold temperatures (Halloran and Bekoff 1994). Larger trees also have more time to develop suitable cavities and thick trunks facilitate formation of natural cavities
(Edelman and Koprowski 2006) and by other primary cavity nesters. Nonetheless, density of large trees in SSPM is low compared to small and medium trees, possibly limiting excavation of cavities by birds such as woodpeckers. Largest trees within 86 younger stands are known to limit Northern flying squirrel ( Glaucomys sabrinus ) populations in British Columbia (Cotton and Parker 2000). Nest trees with larger crowns also may provide more routes to escape from predators (Ramos Lara and Cervantes
2007) and more access to food sources. Larger trees with larger crowns produce more cones than younger conifers (Holimon et al. 1998). Although nest trees with larger crowns may be selected initially by primary cavity nesters such as northern flickers, which tend to excavate their cavities in sites surrounded by denser forest (Arsenault
2004), Mearns’s squirrels also may benefit from nesting in these trees.
Fewer interlocked trees at nest sites possibly was due to the open forests in the
SSPM Mountains (Bojórquez Tapia et al. 2004). Similarly, the higher proportion of dead trees used by Mearns’s squirrels for nesting also may account for less canopy cover at 0 m. Interlocked trees and more canopy cover in other forests commonly provide routes to escape from predators, easy access to food sources, and allow squirrels to travel through the trees rather than on the ground where they are more exposed to aerial and terrestrial predators (Edelman and Koprowski 2005; Ramos Lara and Cervantes 2007).
However, because of the open forests in SSPM, Mearns’s squirrels commonly travel on the ground from tree to tree in search of food and potential tree cavities, increasing the time exposed to terrestrial and aerial predators. Nest sites with higher density of white firs may provide Mearns’s squirrels with more cavity nests, safer sites for resting and hiding from aerial predators, and easy access to more sources of food. Basidiomycete fungi, such as veiled polypores ( Cryptoporus volvatus ), commonly grow on the trunks of white firs and are an important source of food for Mearns’s squirrels (Koprowski et al. 87
2006). Similarly, cavity nests located at sites with greater diversity of trees may increase the variety of foods nearby. For instance, lodgepole pines were rarely used for nesting but their cones were heavily consumed by Mearns’s squirrels throughout the study.
Nesting near favored food trees during the summer also has been reported in other species of tree squirrels (Edwards and Guynn 1995).
Distribution of animals is influenced by factors such as the abundance and competition for resources, predation pressure, tactics of mate acquisition, and breeding systems (Brock and Harvey 1978; Clutton Brock and Harvey 1978; Meek and Barclay
1996). Differential reproductive investment is more pronounced in polygynous mammals that lack parental male care (Curley and Keverne 2005). As a result, differences in nesting requirements may be expected between sexes (e.g., Edwards and
Guynn 1995; Hanski et al. 2000; Meek and Barclay 1996; Thogmartin 1999). However, nests sites of male and female Mearns’s squirrels only differed in nest tree condition, suggesting that both sexes have similar nesting requirements. Using more live trees for nesting may provide female Mearns’s squirrels with more protection against predators
(Wiebe et al. 2006), and easier access to cavities and food sources (Holimon et al. 1998), especially during the breeding season. In other species such as eastern fox squirrels
(Sciurus niger ), use of dreys and cavities by males and females is proportional within seasons, whereas in eastern gray squirrels ( S. carolinensis ) it differs between sexes
(Edwards and Guynn 1995). More studies are still needed to learn more about the sources of variation in nesting behavior between sexes in arboreal squirrels. 88
Nest sites of females did not differ between maternity and nonmaternity nests, suggesting that female Mearns’s squirrels do not have specific nesting requirements for raising litters. Suitable cavities in live and dead trees seem to be the primary nesting requirement for females during both breeding and nonbreeding seasons. Female eastern fox squirrels and eastern gray squirrels use tree cavities more often during the winter reproductive period to increase the survival of their nestlings (Edwards and Guynn
1995). Other characteristics such as cavity size also are known to influence use by secondary cavity nesters (Boyle et al. 2008; Martin et al. 2004; Robb et al. 1996); however, the importance for Mearns’s squirrels is still unknown.
Evidence indicates that Mearns’s squirrels may be obligate secondary cavity nesters (Koprowski et al. 2006; Ramos Lara and Koprowski 2012) with specific nesting requirements. As a result, conservation of Mearns’s squirrels requires both suitable nest sites and healthy populations of primary cavity nesters such as woodpeckers and flickers.
Large trees and snags that facilitate cavity formation are primarily important for the conservation of this endemic species. Dominance of large snags in forests of SSPM is presumed to be due to the lack of fire suppression (Stephens 2004). In other parts of
North America, fire suppression has altered wildfire patterns increasing the frequency of stand replacing crown fires and greatly reducing standing snags (Dwyer and Block
2000). Because Mearns’s squirrels strongly rely on dead trees for nesting, fire suppression in SSPM may impact the occurrence of these structures and consequently of tree cavities. Low occurrence of tree cavities in SSPM may account in part for multiple
Mearns’s squirrels nesting in different cavities of the same tree and their communal 89 nesting behavior (Ramos Lara and Koprowski 2012), which are uncommon in
Tamiasciurus (Gurnell 1987; Munroe et al. 2009; Steele 1998; Verts and Carraway
1998). However, more studies are still needed to understand the causes for the lack of dreys in Mearns’s squirrels compared to other squirrels and the implications of this behavior in their ecology and conservation. Mearns’s squirrels also provide an excellent opportunity to learn more about the mechanisms of geographic variation in nesting behavior in other species (Knapp et al. 2006).
RESUMEN
Muchos animales dependen de nidos para su sobrevivencia y reproducción, con
algunas especies consideradas anidadoras de cavidad obligadas. La ardilla de Mearns
(Tamiasciurus mearnsi ) es una especie endémica de la Sierra de San Pedro Mártir, Baja
California, la cual depende de cavidades de árbol para anidar. Listada federalmente
como amenazada en México, y como en peligro por la Unión Internacional para la
Conservación de la Naturaleza (UICN), la ecología de esta Tamiasciurus sureña es pobremente conocida. Examinamos si las ardillas de Mearns tienen requerimientos de
anidación específicos comparados con otras ardillas arbóreas. También examinamos si
los requerimientos de anidación difieren entre sexos y entre hembras con crías y sin
crías. Utilizamos telemetría para localizar los nidos y cuadrantes circulares de 10 m de
radio para comparar características del hábitat entre sitios de anidación y sitios al azar.
Las cavidades de árbol son estructuras escasas en la Sierra de San Pedro Mártir, posiblemente limitando la población y distribución de las ardillas de Mearns. La especie
del árbol de anidación, la condición del árbol de anidación, el tamaño (DBH) del árbol de 90 anidación, la cobertura del dosel y la abundancia de abetos blancos ( Abies concolor ) son características importantes para anidar. Los sitios de anidación de los machos no difirieron de las hembras excepto por la condición del árbol de anidación. Las hembras aparentemente no tienen requerimientos de anidación específicos al tener crías. A diferencia de otros congéneres que también construyen nidos de hoja y madrigueras subterráneas para anidar, los árboles grandes y tocones que facilitan la formación de cavidades son críticos para la conservación de esta especie. Las ardillas de Mearns proveen una oportunidad importante para aprender más del mecanismo de variación geográfica en el comportamiento de anidación.
ACKNOWLEDGMENTS
We thank the Desert Southwest Cooperative Ecosystem Studies Unit, the
Intermountain Region International Conservation Office of the National Park Service, the
Arizona Agricultural Experiment Station, and T&E, Inc. for funding. The Consejo
Nacional de Ciencia y Tecnología and the Wallace Research Foundation provided financial support to N. Ramos Lara. L. Norris and N. Kline of the National Park Service and W. Zúñiga, Á. López, and M. Valles of Sierra de San Pedro Mártir National Park supported the concept of the project. J. Franco, P. Strittmatter, B. Powell, J. Sasian, J.
Bohigas, D. Hiriart, D. Carrasco, A. García, I. González, and E. Valdés facilitated housing logistics at Observatorio Astronómico Nacional. The Servicio Meteorológico
Nacional provided temperature and precipitation data of the region. W. Shaw, R. W.
Mannan, B. Pasch, M. Merrick, N. Tautfest, C. Schvarcz, C. Zugmeyer, and G. Palmer assisted with fieldwork. L. Bojórquez, S. Stephens, R. Minnich, J. Vargas, C. Porras, E. 91
Meling, E. Mellink, E. Salgado, B. Mackintosh, and G. Mackintosh graciously shared their knowledge of the Sierra de San Pedro Mártir. J. Bronstein, R. W. Mannan, and W.
Shaw provided valuable comments that improved the manuscript.
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TABLE B1.—Habitat characteristics used in univariate analyses to compare nest sites of Mearns’s squirrels (Tamiasciurus
mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests, in a coniferous forest of the Sierra de San Pedro Mártir, Baja California, Mexico.
Use Sex Reproduction
Habitat Nests Random Males Females Maternity Nonmaternity
characteristics n = 115 n = 115 n = 47 n = 48 n = 21 n = 32
Cavity
Height (m) 14.8 ± 6.1 10.0 ± 10.2 12.8 ± 5.0 15.6 ± 6.5 16.7 ± 6.1 16.5 ± 5.9
Aspect (degrees) 286.8 ± 128.9 305.0 ± 94.2 285.1 ± 95.3 153.0 ± 128.9 323.4 ± 114.6 194.0 ± 88.3
Focal tree
Crown size (m) 4.5 ± 1.3 2.7 ± 1.0 4.8 ± 1.4 4.2 ± 1.3 4.3 ± 1.4 4.3 ± 1.2
Site
% Canopy cover a 41.6 ± 15.9 43.8 ± 9.8 39.6 ± 14.8 45.0 ± 16.4 45.3 ± 16.2 46.0 ± 16.2
Slope aspect (degrees) 246.8 ± 119.5 261.5 ± 101.7 209.1 ± 101.9 310.8 ± 105.0 324.3 ± 124.0 295. 8 ± 114.5
Trees/ha 176.5 ± 167.1 215.1 ± 268.3 180.1 ± 171.5 202.8 ± 180.0 190.5 ± 175.2 199.0 ± 177.5 102
Live trees/ha 167.0 ± 163.1 210.4 ± 268.4 169.5 ± 166.8 193.1 ± 176.7 182.5 ± 172.4 189.6 ± 173.6
Small trees/ha b 130.1 ± 161.5 166.1 ± 271.1 128.4 ± 164.5 161.1 ± 174.3 152.4 ± 177.5 153.1 ± 169.1
a All distances combined (0 m, 5 m, and 10 m)
b ≥5 cm DBH and <40 cm DBH
103
TABLE B2.—Correlations between original characteristics selected in stepwise discriminant function analysis to compare nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random sites (availability), and nest sites of males and females, in the
Sierra de San Pedro Mártir, Baja California, Mexico. Significance ( P < 0.017) is marked with an asterisk.
Correlation with
Habitat discriminant function
characteristics r P
Use vs. Random
Focal tree DBH 0.659 <0.0001*
% Canopy cover 0 m 0.247 <0.0001*
White firs/ha 0.241 <0.0001*
Interlocked trees 0.185 0.004*
% Canopy cover 5 m 0.141 0.028
Large trees/ha a 0.138 0.031
Focal tree height 0.022 0.734
Males vs. Females
% Canopy cover 0 m 0.510 0.043
Species richness (trees) 0.478 0.058
Focal tree height (m) 0.456 0.070
Lodgepole pines/ha 0.146 0.559
a ≥85 cm DBH
104
TABLE B3.—Habitat characteristics used in stepwise discriminant function analyses to compare nest sites of Mearns’s
squirrels ( Tamiasciurus mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests, in a coniferous forest of the Sierra de San Pedro Mártir, Baja California, Mexico.
Use Sex Reproduction
Habitat Nests Random Males Females Maternity Nonmaternity
characteristics n = 115 n = 115 n = 47 n = 48 n = 21 n = 32
Focal tree
Height (m) 24.6 ± 9.0 25.0 ± 6.4 22.6 ± 9.2 26.0 ± 8.7 28.1 ± 10.4 25.4 ± 7.5
DBH 95.6 ± 26.9 65.3 ± 17.5 92.7 ± 26.9 94.6 ± 28.2 103. 5 ± 34.1 92.0 ± 22.0
Interlocked trees 1.3 ± 2.5 2.4 ± 3.6 1.3 ± 2.3 1.5 ± 2.8 1.1 ± 1.6 1.7 ± 3.2
Site
Nearest tree (m) 5.1 ± 3.3 4.15 ± 2.6 5.2 ± 3.2 4.8 ± 3.4 5.3 ± 3.3 4.6 ± 3.3
% Canopy cover 0 m 75.1 ± 26.4 86.4 ± 16.7 70.1 ± 26.7 80.7 ± 23.8 78.1 ± 25.6 83.3 ± 21.9
% Canopy cover 5 m 30.9 ± 23.3 24.9 ± 17.8 28.3 ± 22.2 35.5 ± 25.2 36.5 ± 24.4 36.7 ± 25.3
% Canopy cover 10 m 18.8 ± 17.18 20.0 ± 14.5 20.4 ± 18.6 18.7 ± 17.7 21.2 ± 13.6 17.9 ± 19.4
Medium trees/ha a 37.1 ± 46.3 44.1 ± 43.6 45.4 ± 54.0 33.3 ± 42.4 22.2 ± 35.5 38.5 ± 44.1 105
Large trees/ha b 9.3 ± 17.4 4.9 ± 12.7 6.4 ± 15.0 8.3 ± 16.1 15.9 ± 20.1 7.3 ± 16.4
Jeffrey pines/ha 134.8 ± 128.4 198.6 ± 271.2 131.9 ± 114.8 156.3 ± 150.5 155.6 ± 151.4 147.9 ± 144.7
Lodgepole pines/ha 18.3 ± 51.5 11.6 ± 33.1 23.4 ± 70.5 16.7 ± 36.4 11.1 ± 26.5 20.8 ± 40.4
White firs/ha 23.2 ± 53.2 4.6 ± 18.7 24.8 ± 66.1 29.9 ± 48.3 23.8 ± 38.2 30.2 ± 51.8
Dead trees/ha 9.6 ± 20.1 4.6 ± 12.4 10.6 ± 22.1 9.7 ± 19.4 7.9 ± 14.6 9.4 ± 21.1
Logs/ha c 62.3 ± 58.8 47.8 ± 40.3 70.2 ± 63.4 63.2 ± 58.9 46.0 ± 46.5 67.7 ± 63.6
Basal area (m 2/ha) 21.8 ± 20.7 20.7 ± 16.5 21.9 ± 21.9 21.3 ± 19.5 24.3 ± 19.2 21.5 ± 21.1
Slope (degrees) 22.2 ± 13.0 19.9 ± 10.9 23.0 ± 14.0 23.8 ± 13.1 22.5 ± 11.6 23.2 ± 14.0
Species richness (trees) 1.4 ± 0.8 1.2 ± 0.6 1.3 ± 0.8 1.6 ± 0.8 1.5 ± 0.7 1.6 ± 0.9
a ≥40 cm DBH and <85 cm DBH
b ≥85 cm DBH
c ≥15 cm diameter and ≥1.5 m length
106
TABLE B4.—Principal component (PC) analysis used to compare nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random sites (availability), nest sites of males and females, and nest sites of females with maternity and nonmaternity nests in the Sierra de San Pedro Mártir, Baja California, Mexico.
Use Sex Reproduction
Habitat Nests Random Males Females Maternity Nonmaternity
characteristics n = 115 n = 115 n = 47 n = 48 n = 21 n = 32
PC 1 PC 2 PC 1 PC 2 PC 1 PC 2 PC 1 PC 2 PC 1 PC 2 PC 1 PC 2
Nest tree
Height (m) 0.41 0.55 0.32 0.40 0.49 0.60 0.47 0.42 0.62 0.23 0.24 0.51
DBH 0.51 0.38 0.38 0.19 0.49 0.61 0.49 0.26 0.70 0.24 0.27 0.25
Interlocked trees 0.21 0.60 0.63 0.27 0.28 0.41 0.09 0.57 0.12 0.63 0.05 0.65
Nest site
Nearest tree (m) 0.65 0.17 0.58 0.22 0.74 0.21 0.40 0.10 0.52 0.29 0.28 0.23
Trees/ha 0.96 0.10 0.93 0.20 0.90 0.26 0.92 0.15 0.86 0.13 0.98 0.01
Live trees/ha 0.93 0.13 0.92 0.22 0.88 0.22 0.94 0.18 0.92 0.16 0.96 0.02
Small trees/ha a 0.80 0.03 0.78 0.41 0.76 0.39 0.85 0.04 0.82 0.05 0.90 0.09 107
Medium trees/ha b 0.53 0.05 0.45 0.40 0.55 0.32 0.40 0.30 0.23 0.57 0.44 0.25
Large trees/ha c 0.04 0.28 0.09 0.43 0.04 0.11 0.01 0.40 0.18 0.58 0.05 0.40
Jeffrey pines/ha 0.90 0.07 0.88 0.16 0.85 0.04 0.87 0.11 0.83 0.17 0.92 0.00
White firs/ha 0.62 0.01 0.15 0.23 0.65 0.31 0.68 0.03 0.76 0.07 0.64 0.19
Lodgepole pines/ha 0.23 0.10 0.02 0.03 0.19 0.43 0.05 0.31 0.18 0.18 0.19 0.28
Basal area (m2/ha) 0.59 0.27 0.63 0.51 0.65 0.20 0.47 0.55 0.18 0.79 0.51 0.46
Species richness (trees) 0.75 0.04 0.26 0.08 0.69 0.25 0.75 0.05 0.66 0.06 0.79 0.08
% Canopy cover 0 m 0.31 0.69 0.12 0.29 0.39 0.70 0.23 0.66 0.50 0.36 0.13 0.65
% Canopy cover 5 m 0.10 0.83 0.40 0.68 0.13 0.74 0.29 0.73 0.63 0.52 0.03 0.78
% Canopy cover 10 m 0.31 0.43 0.10 0.37 0.31 0.04 0.21 0.64 0.14 0.72 0.33 0.57
% Canopy cover d 0.12 0.93 0.36 0.76 0.17 0.77 0.21 0.90 0.62 0.64 0.03 0.90
Slope (degrees) 0.49 0.00 0.41 0.32 0.56 0.11 0.53 0.17 0.69 0.05 0.44 0.32
Dead trees/ha 0.38 0.06 0.20 0.17 0.38 0.22 0.29 0.24 0.39 0.19 0.28 0.25
Logs/ha e 0.33 0.19 0.01 0.40 0.33 0.09 0.37 0.21 0.74 0.01 0.16 0.19
Eigenvalue 6.5 3.3 5.3 2.8 6.5 3.4 6.0 3.6 7.5 3.4 5.7 3.7
% Accumulated variance 30.8 46.5 25.1 38.5 31.1 47.4 28.5 45.7 35.7 51.7 27.1 44.9
a ≥5 cm DBH and <40 cm DBH 108 b ≥40 cm DBH and <85 cm DBH c ≥85 cm DBH d All distances combined (0 m, 5 m, and 10 m) e ≥15 cm diameter and ≥1.5 m length 109
TABLE B5.—Relative dominance ( Rdo ), relative density ( Rde ) and relative frequency ( Rfr ) for each species of tree found
at nest sites of Mearns’s squirrels ( Tamiasciurus mearnsi ), random sites (availability), nest sites of males and females, and nest
sites of females with maternity and nonmaternity nests, in coniferous forests of the Sierra de San Pedro Mártir, Baja California,
Mexico. Letters meaning: Sp (species of trees), J (Jeffrey pine―Pinus jeffreyi ), L (Lodgepole pine—P. contorta ), S (Sugar pine—P. lambertiana ), F (White fir—Abies concolor ), A (Quaking aspen—Populus tremuloides ).
Use Sex Reproduction
Nests Random Males Females Maternity Nonmaternity Sp n = 115 n = 115 n = 47 n = 48 n = 21 n = 32
Rdo Rde Rfr Rdo Rde Rfr Rdo Rde Rfr Rdo Rde Rfr Rdo Rde Rfr Rdo Rde Rfr
J 84.8 76.4 64.0 89.5 92.3 77.3 87.3 73.2 66.2 76.8 77.1 60.6 73.3 81.7 61.3 84.8 74.3 60.4
L 2.9 10.3 16.3 7.2 5.4 15.6 2.4 13.0 16.9 4.0 8.2 15.5 0.8 5.8 12.9 5.4 10.5 18.8
S 0 0 0 0.6 0.1 0.7 0 0 0 0 0 0 0 0 0 0 0 0
F 12.3 13.1 19.0 2.7 2.2 6.4 10.3 13.8 16.9 19.2 14.7 23.9 25.9 12.5 25.8 9.8 15.2 20.8
A 0 0.2 0.7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
% 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
110
FIGURE LEGENDS
FIG . B1.―Number of Jeffrey pines ( Pinus jeffreyi ), lodgepole pines ( P. contorta ), and white firs ( Abies concolor ) used by Mearns’s squirrels ( Tamiasciurus mearnsi ) for
nesting ( n = 115), compared to random sites ( n = 115), nest sites of males ( n = 47) and
females ( n = 48), and nest sites of females with maternity ( n = 21) and nonmaternity
nests ( n = 32) in the Sierra de San Pedro Mártir, Baja California, Mexico.
FIG . B2.―Number of live and dead trees used by Mearns’s squirrels ( Tamiasciurus mearnsi ) for nesting ( n = 115) compared to random sites ( n = 115), nest sites of males ( n
= 47) and females ( n = 48), and nest sites of females with maternity ( n = 21) and
nonmaternity nests ( n = 32) in the Sierra de San Pedro Mártir, Baja California, Mexico.
FIG B3.—Comparison of principal component scores on PC 1 and PC 2 for nest
sites (open circles) of Mearns’s squirrels with random sites (solid circles) in the Sierra de
San Pedro Mártir, Baja California, Mexico. Bivariate means for both sites are the same
and are represented by a triangle.
111
FIG . B1
112
FIG . B2
113
FIG . B3
114
APPENDIX C
HOME RANGE AND HABITAT USE OF MEARNS’S SQUIRRELS ( TAMIASCIURUS
MEARNSI ) WITHOUT THE CONSTRAINTS OF LARDERHOARDING
Manuscript prepared for submission to Journal of Mammalogy
115
Send proofs to: Nicolas Ramos Lara Wildlife and Fisheries Science School of Natural Resources and the Environment 325 Biological Sciences East Building The University of Arizona Tucson, AZ 85721 USA Email: [email protected]
Running Heading: Home ranges of Tamiasciurus mearnsi
Home range and habitat use of Mearns’s squirrels ( Tamiasciurus mearnsi ) without the constraints of larderhoarding
NICOLÁS RAMOS LARA * AND JOHN L. KOPROWSKI
Wildlife and Fisheries Science, School of Natural Resources and the Environment,
University of Arizona, Tucson, AZ 85721, USA
Throughout most of their range, tree squirrels in the genus Tamiasciurus defend
exclusive territories centered on large caches of cones, known as middens, which play a
vital role in their home range dynamics. The Mearns’s squirrel ( T. mearnsi ) is the southernmost species in the genus, known from only three locations in the Sierra de San
Pedro Mártir (SSPM), Baja California, Mexico. Unlike other congeners, the species does not build middens and therefore provides an excellent opportunity to assess space use without the constraints of larderhoarding. We used telemetry and satellite imagery to examine if home range dynamics and population densities of Mearns’s squirrels differ 116
from other congeners. We also assessed habitat suitability for the species in remote areas
of SSPM by comparing habitat characteristics within home ranges with random locations.
Overall, home range dynamics of Mearns’s squirrels are similar to nonterritorial squirrels
in the genus Sciurus , with males having larger home ranges than females throughout the
year, suggesting that the lack of middens is associated with the unique strategies adopted by Mearns’s squirrels to persist in these mountains. Compared to other species of tree
squirrels, home range overlap between females is greater during mating seasons, similar
to that of males. Population densities of Mearns’s squirrels were similar to other species
of tree squirrels. Remote areas in SSPM appear to have suitable habitat for the species.
Mearns’s squirrels provide an excellent opportunity to learn more about the evolution of
territoriality. Similarly, conservation plans must include the unique space use pattern and
enlarged home ranges observed in the species.
Key words: Baja California, cover composition, endemic species, habitat use, home
range, larderhoards, middens, overlap, Sierra de San Pedro Mártir
*Correspondent: [email protected]
Resources such as food, shelter, and mates are distributed in space so space itself
often becomes an important resource (Gurnell 1987). Home range, defined as the area
traversed by an individual in its normal activities of food gathering, mating, and caring
for young (Burt 1943), is a useful measure of space use and is likely influenced by
multiple factors such as habitat characteristics (Anich et al. 2010), body mass, seasons 117
(Hanski et al. 2000), population density (Heaney 1984), operational sex ratio (Michener
and McLean 1996), and food availability (Ostfeld 1985). In general, home range size of
an animal is considered an important indicator of its behavior and resource requirements
in relation to the availability of the resources in the environment (Perry and Garland
2002). However, because home ranges of females are more dependent on food and nest
resources whereas home ranges of males are more dependent on the spatial distribution of
females, differences in resource requirements may exist between sexes (Hanski et al.
2000). Within a population, home ranges of individuals may be overlapped considerably by other conspecifics. Therefore, home range overlap may be used to assess the degree
of interaction among individuals within a population or to infer territoriality when behaviors cannot be observed adequately (Harless et al. 2009). Similarly, habitat
characteristics within home ranges may be used to evaluate habitat suitability, especially
for endangered species (e.g., Aebischer et al. 1993; Katnik and Wielgus 2005; Perkins et
al. 2008; Wood et al. 2007; Zugmeyer and Koprowski 2009a).
The spatial and social organization of the tree squirrels in the genus Tamiasciurus is believed to be dependent upon habitat and resource availability (Gurnell 1987). The
genus contains three species (Thorington and Hoffmann 2005): red squirrels ( T.
hudsonicus ), Douglas’s squirrels ( T. douglasii ), and Mearns’s squirrels ( T. mearnsi ). Red
squirrels are the most widely distributed of the three species, with a geographic
distribution that extends from Alaska in the northwest through the Great Lakes region to
the southern Appalachians in the southeast, and southward along the Rocky Mountains
into northern Arizona (Arbogast et al. 2001). The geographic distribution of Douglas’s 118 squirrels is limited to western North America in British Columbia, Washington, Oregon, and California, primarily west of the Cascades and the Sierra Nevada (Arbogast et al.
2001). Red and Douglas’s squirrels are known to defend exclusive territories throughout most of their range against conspecifics and other competitors (Steele 1998, 1999). Each territory is centered on a large cache of cones, known as larderhoard or midden, and the territory owners have exclusive use of this important food resource (Gurnell 1987). As a result, middens play an important role in the territoriality and home range dynamics of red and Douglas’s squirrels (Gurnell 1984). The territories, which are nonoverlapping and contiguous, are defended by vocalizations and the chasing of intruding squirrels
(C.C. Smith 1968). However, for the construction of middens, squirrels require specific characteristics such as cool surface temperatures associated with high basal area, log volume, and canopy cover necessary to prevent cones from opening (Zugmeyer and
Koprowski 2009a).
In contrast to the other two congeners, Mearns’s squirrels are endemic to the coniferous forests of the Sierra de San Pedro Mártir (SSPM), Baja California, Mexico
(Lindsay 1981). The species is separated from the nearest populations of red and
Douglas’s squirrels by ca. 600 km of mostly nonforested lowlands (Yensen and Valdés
Alarcón 1999). However, the exact distribution of Mearns’s squirrels in SSPM is unknown, except for three locations reported in the literature, which includes Vallecitos and La Grulla Meadows, where the species has been collected for museum specimens
(Lindsay 1981; Yensen and Valdés Alarcón 1999). The species is known from ca. 2,100 m to 2,750 m elevation (Yensen and Valdés Alarcón 1999). Unlike other Tamiasciurus , 119
Mearns’s squirrels do not construct middens to store cones, apparently due to the open
and xeric conditions of the SSPM forests (Koprowski et al. 2006), nor exhibit territorial behavior (Ramos Lara and Koprowski 2012). Whereas other Tamiasciurus larderhoard
throughout most of their range (Steele 1998, 1999), Mearns’s squirrels scatterhoard food
items (Ramos Lara and Koprowski 2012) similar to other squirrels in the genus Sciurus
(Gurnell 1987). Without middens and territories to defend, home range dynamics and
habitat use of Mearns’s squirrels may differ from those of other congeners. Although red
squirrels in the northeastern portion of their range do not build middens, they defend
small feeding stations (Layne 1954) and the forests are diverse and provide a suitable and
varied diet (Hamilton 1939), contrary to forests in SSPM (Koprowski et al. 2006).
Considered a rare species (Huey 1964), Mearns’s squirrels are federally listed as
threatened in Mexico (SEMARNAT 2010), due to their restricted distribution, low population density, and isolation, and as endangered by the International Union for
Conservation of Nature (IUCN—de Grammont and Cuarón 2008). Herein, we examined
if the lack of middens and territories may be associated with differences observed in
home range dynamics between Mearns’s squirrels and other congeners. In particular, we
assessed if home range size, overlap, and movements differ between sexes and seasons.
Because Mearns’s squirrels are known from only three locations in the SSPM Mountains,
we evaluated habitat suitability for the species in remote areas. Described as occurring
only in limited numbers (Yensen and Valdés Alarcón 1999), we also examined if population densities of Mearns’s squirrels differ from other tree squirrels. 120
MATERIALS AND METHODS
Study area.—SSPM is located ca. 100 km southeast of Ensenada, Baja California,
Mexico (Stephens et al. 2003). SSPM was established as a Forest Reserve in 1932, as a
National Park in 1947, and has been proposed as a Biosphere Reserve (Bojórquez Tapia
et al. 2004). SSPM National Park comprises 65,000 ha of which coniferous forests cover
ca. 40,655 ha (Minnich et al. 2000). Forests are composed of Jeffrey pine ( Pinus jeffreyi ), sugar pine ( P. lambertiana ), lodgepole pine ( P. contorta ), white fir ( Abies
concolor ), and limited amounts of quaking aspen ( Populus tremuloides ) and incense
cedar ( Calocedrus decurrens ). The most common forest types are Jeffrey pine, Jeffrey pine–mixed conifer, and mixed white fir forests, respectively (Stephens et al. 2003).
Mixed conifer forest on the summit plateau is replaced by chaparral and Sonoran Desert
scrub at lower elevations. The most striking feature of the mixed conifer forests is an
open park like aspect that consists of mature trees reaching 30–45 m, with few pole sized
trees and saplings, and an open shrub cover (Bojórquez Tapia et al. 2004). Elevation
averages 2,600 m in the north and decreases to 1,800 m in the southern portion of the
range with the highest peaks over 3,000 m (Stephens et al. 2003). Soils in SSPM are
unclassified; however, the most common parent material is granite with some soils
derived from metamorphic quartz schists (Stephens 2004). Forests have not experienced
disturbance from logging, and fires have spread without human interference (Minnich et
al. 2000). Summers are dry except for afternoon thunderstorms of the North American
monsoon (Minnich et al. 2000). According to data recorded by Servicio Meteorológico
Nacional at ejido San Matías, located ca. 25 km north of SSPM, mean (± SD ) monthly 121
temperature in the region remained similar throughout the study (19.2 °C ± 6.59). In
contrast, mean monthly precipitation in 2005 (22.8 mm ± 25.7) was greater than 2006
(9.0 mm ± 16.5) and 2007 (10.7 mm ± 13.5).
Large scale surveys.—During 2005, we surveyed ca. 2,500 ha of forest in the
margins of the Vallecitos Meadow, where the species was collected previously for
museum specimens (Lindsay 1981; Yensen and Valdés Alarcón 1999), to detect direct
(animal sighting) and indirect (remnants of food with characteristic gnawing) occurrence
of Mearns’s squirrels and to establish potential capture sites. We explored the area on
foot systematically using a topographic map (Centra Publications 1988).
Trapping and telemetry .—We captured Mearns’s squirrels during May August
2006 and 2007. Live traps (Model 201; Tomahawk Live Trap Co., Wisconsin) were placed at the base of large diameter trees, baited with peanuts and peanut butter, covered
with tree bark, and checked at 1 h intervals. Captured squirrels were transferred to a
cloth handling cone (Koprowski 2002) where we collected data on sex, age class,
reproductive condition, and body mass. Adult animals (≥240 g) were fitted with radio
collars (Model SOM 2190; Wildlife Materials International, Inc., Carbondale, Illinois)
and uniquely numbered Monel ear tags (Style #1005 1; National Band and Tag Co.,
Newport, Kentucky) with colored plastic washers (Style #1842; National Band and Tag
Co., Newport, Kentucky) on both ears; however, juveniles only were marked with ear
tags. We distinguished adults and juveniles based on reproductive condition and body
mass of captured animals. All squirrels were released at the capture site after ≤8 min of
handling time; no animals were injured during the study. We calculated trap effort by 122
counting the total number of days and hours employed for trapping during 2006 and
2007, as well as the total number of Mearns’s squirrels captured during the same period
of time. Trapping and handling procedures were conducted with approval from The
University of Arizona Institutional Animal Care and Use Committee (protocol # 05 038),
in accordance with guidelines of the American Society of Mammalogists (Gannon et al.
2007), and with permits from the following Mexican authorities: Dirección Forestal y de
la Fauna Parque Nacional Sierra de San Pedro Mártir and Dirección General de Vida
Silvestre.
We used a 3 element yagi directional antenna (Wildlife Materials International,
Inc., Carbondale, Illinois) and receiver (Model R 1000, Communications Specialists,
Inc., Orange, California) to locate squirrels from 0700 2000 h at >2 h intervals to avoid
spatial autocorrelation (White and Garrott 1990). We tracked squirrels by homing
monthly in spring (April) and autumn (September November) and weekly during summer
(May August); we did not monitor animals during winter (December March) due to snow
and limited access. Each location was recorded using a global positioning system (eTrex
Legend GPS unit; Garmin International, Inc., Olathe, Kansas). Location error (± 6 m)
was reduced by tracking squirrels until sighted or by triangulation around the tree (Farías
et al. 2006; White and Garrott 1990).
Data analysis .―We stratified years by mating (January through mid July) and nonmating (mid July through December) seasons based upon detection of scrotal males, lactating females, and emergence of litters. We used the Home Range Analysis extension
(Rodgers and Carr 1998) for ArcView 3.2a (ESRI, Inc., Redlands, California) to estimate 123
home range sizes using 95% minimum convex polygons (MCP) for comparison with
other studies, and 95% and 50% core fixed kernels with smoothing parameters chosen
via least squares cross validation (Powell 2000; Seaman et al. 1999). High correlation ( r
= 0.901, P < 0.0001) between 95% MCP and 95% fixed kernel estimates indicated low effect of sample size and estimation techniques (Powell 2000). A plot of home range sizes versus number of locations (Edelman and Koprowski 2006) reached asymptote between 20 25 fixes (location points). Therefore, we only used individuals with ≥22 fixes to estimate home range size, overlap, and maximum distance traveled for both sexes and seasons. Unpaired t tests were used to compare total number of fixes between sexes and seasons. We used two way ANOVAs to compare home range size estimates between sexes and years of study or seasons. Linear regressions were used to explore intraspecific association between home range size estimates and body mass of Mearns’s squirrels (Hanski et al. 2000; Harestad and Bunnell 1979; Wauters and Dhondt 1992), and to explore interspecific association among closely related Tamiasciurus and Sciurus squirrels (Gurnell 1987), also monitored with telemetry and similar home range estimators. However, because most Mearns’s squirrels were captured during mating seasons, we only used this season in the intraspecific analysis.
We used XTools extension (DeLaune 2000) to estimate home range overlap and maximum distance traveled for both sexes and seasons. We used 95% fixed kernel estimates to explore variations in home range overlap (Linders et al. 2004; Powell 2000).
We estimated overlap by measuring total percentage of an animal’s 95% area overlapped by squirrels of the same and opposite sex (Pasch and Koprowski 2006). Percentage 124
overlap was averaged by sex for both seasons (Linders et al. 2004). Maximum distance
traveled by an individual was defined as the distance from its nocturnal nest to the
farthest location recorded since the animal was fitted with the radio collar or during a particular season. When squirrels used more than one nocturnal nest for the period of
time analyzed, we selected the nest used for the most nights. Juvenile squirrels
recaptured in 2007 as adults permitted assessment of natal dispersal (Kemp and Keith
1970; Koprowski 1996; Larsen and Boutin 1994; Sun 1997) by calculating the distance
from their natal nest to their nocturnal nest used as adults. We used two way ANOVAs
to compare percentage overlap, number of individuals overlapped, and maximum
distance traveled between sexes and seasons. Linear regression was used to explore
association between male 95% fixed kernel home range size and number of females
overlapped during both seasons (Cudworth and Koprowski 2010).
To examine habitat use of both sexes of Mearns’s squirrels within home ranges, we
used high resolution satellite imagery (0.6 m Quickbird) and XTools extension (DeLaune
2000) to evaluate cover composition of male and female 95% fixed kernel home ranges
during both seasons. Within each home range, we measured the following habitat
characteristics: percentage of open forest with soil, percentage of open forest with
granite, percentage of closed forest, number of logs per hectare, number of dead trees per
hectare, number of saplings per hectare, and number of trees per hectare. The open
nature of the forest structure in SSPM facilitated the quantification of these
characteristics. Using the actual 95% fixed kernel home ranges ( n = 50), we created
identical home ranges ( n = 50) in shape and size (Perkins et al. 2008) to compare cover 125
composition with random locations and evaluate habitat suitability for Mearns’s squirrels
in remote areas of SSPM. However, we restricted the analysis to the northern part of
SSPM (ca. 20,000 hectares), which included Vallecitos and La Tasajera Meadows, within
the UTM coordinates N: 3438266.52, S: 3425053.33, W: 636263.56, and E: 651058.04
(Appendix E). Random Point Generator extension (Jenness 2005) was used to generate
random point locations upon which we centered each duplicated seasonal home range
(Katnik and Wielgus 2005; Zugmeyer and Koprowski 2009b). We used stepwise
multiple logistic regression (entry = 0.05 and removal = 0.10) to determine the cover
composition characteristics that best discriminated between actual home ranges (coded 0)
and random home ranges (coded 1). Percentage of open forest with soil was correlated
with percentage of closed forest ( r = 0.88, P < 0.0001) and was excluded from the
analysis to prevent multicollinearity (Pallant 2007). We used two way MANOVAs to
examine differences in cover composition between sexes and seasons for actual and
random home ranges (Pallant 2007; Stewart et al. 2002). Data for number of logs per
hectare (all P > 0.28) and number of dead trees per hectare (all P > 0.46) did not differ between seasons, and were pooled due to sample size constraints, and were analyzed
using one way MANOVAs. We used stepwise multiple regression ( F, entry = 0.05 and
removal = 0.10) to explore association of cover composition, sex, and season with 95%
fixed kernel home range size. Percentage of open forest with soil and number of saplings per hectare were highly correlated with percentage of closed forest ( r = 0.88, P <
0.0001) and number of trees per hectare ( r = 0.80, P < 0.0001), respectively, and were
excluded from the analysis. We explored association of number of logs per hectare and 126
number of dead trees per hectare with home range size using nonparametric Spearman’s
rank correlation.
To estimate population densities of Mearns’s squirrels during each year of study,
we overlaid the location points corresponding to the first capture of each individual over
the satellite image. Polygons were created around points covering the same areas used
for trapping squirrels in the margins of the Vallecitos Meadow. Each polygon was
created systematically by leaving the same buffer of a linear distance (150 m) between
the outer points in each trapping area and the margins of the polygon. We used XTools
extension (DeLaune 2000) to calculate the area of each polygon. We estimated population densities by counting the number of adult and juvenile individuals within each polygon (squirrels/ha). Combining information with other species of tree squirrels, we
used linear regression to explore interspecific association between male home range size
and population density (Heaney 1984).
We used unpaired t test and Mann Whitney ( U) to examine differences in number
of recaptures between sexes (Zar 1996). All statistical analyses were conducted using
SPSS 17.0 (SPSS Inc., Chicago). When necessary, we log transformed variables to meet
the assumptions of parametric tests (Zar 1996); however, means (± SD ) reported in the
results are from untransformed values.
RESULTS
We captured 79 Mearns’s squirrels (adults: 20 males, 18 females; juveniles: 23
males, 18 females). Number of times an individual was recaptured did not differ between
adult males (3.10 ± 2.77 individuals) and females (3.61 ± 3.87 individuals; t36 = 0.47, P = 127
0.640) or between juvenile males (1.83 ± 0.98 individuals) and females (1.78 ± 1.63
individuals; U = 174.0, n1 = 23, n2 = 18, P = 0.329). Trap effort was 5.76 trap hours/squirrel in 2006 and 7.25 trap hours/squirrel in 2007. Number of fixes per individual did not differ between adult males (66.55 ± 25.78 fixes) and females (68.31 ±
27.69 fixes; t34 = 0.197 , P = 0.845) or between mating (46.52 ± 19.67 fixes) and
nonmating seasons (40.57 ± 18.37 fixes; t48 = 1.099 , P = 0.277).
Home range metrics.—Home range size estimates differed between sexes but not years of study (Table C1). During the two years, male 95% MCP home ranges (17.06 ±
17.37 ha, n = 20) were 3.4 times larger than those of females (4.96 ± 2.34 ha, n = 16), male 95% fixed kernel home ranges (3.91 ± 3.60 ha, n = 20) were 2.5 times larger than those of females (1.58 ± 1.14 ha, n = 16), and male 50% core fixed kernel home ranges
(0.55 ± 0.60 ha, n = 20) were 2.6 times larger than those of females (0.21 ± 0.25 ha, n =
16). Similarly, home range size estimates differed between sexes but not seasons; except for 95% MCP (Table C1). Whereas female home ranges varied little between seasons, male home ranges were ≥2.7 times larger during mating seasons and ≥3.8 times larger than those of females (Fig. C1). We did not find intraspecific association between home range size estimates and body mass of Mearns’s squirrels (all P > 0.170); except for
2 female 95% MCP ( R = 0.506, F1,11 = 11.28, P = 0.006; Fig. C2). In contrast, a strong interspecific association between home range size and body mass was found using other
2 species of tree squirrels ( R = 0.832, F1,5 = 24.75, P = 0.004; Fig. C3).
Home range overlap.—Percentage overlap of male and female 95% fixed kernel home ranges by conspecifics differed between seasons but not sexes (Table C2). Male 128
and female home ranges were overlapped by more conspecifics of either sex during
mating seasons than during nonmating seasons (Table C3). Female home ranges were
overlapped by more conspecifics of either sex during mating seasons than male home
ranges (Table C3). In contrast, number of individuals overlapping the homes ranges of
conspecifics differed between sexes and seasons for males but only between sexes for
females (Table C2). Males were overlapped by a greater number of males than females
during mating seasons than during nonmating seasons (Table C3). Conversely, females
were overlapped by a greater number of conspecifics of either sex during mating seasons
than during nonmating seasons (Table C3). Male 95% fixed kernel home ranges were
2 not associated with number of females overlapped during mating ( R = 0.0003, F1,12 =
2 0.003, P = 0.955) or nonmating seasons ( R = 0.018, F1,13 = 0.243, P = 0.630).
Distance traveled.—Maximum distance traveled by adult squirrels from nocturnal nests differed between sexes and seasons (Table C2). Males traveled greater distances during mating seasons (613.57 ± 305.81 m, n = 14) than during nonmating seasons
(307.33 ± 183.20 m, n = 15; Fig. C4). In contrast, females traveled similar distances between mating (329.23 ± 186.57 m, n = 13) and nonmating seasons (328.75 ± 159.77 m, n = 8; Fig. C4). Although males and females traveled similar distances during nonmating seasons, males traveled a distance 1.9 times greater than that of females during mating seasons (Fig. C4). Eight juvenile squirrels born in 2006 and recaptured in 2007 provided information on natal dispersal. Males (737.5 ± 763.7 m, range = 120 1,800 m, n = 4)
traveled a distance 7.8 times greater than that of females (95.0 ± 70.0 m, range = 20 180
m, n = 4) before settling in other areas of the forest. 129
Habitat use.—Three cover composition characteristics differed between actual and
2 random home ranges (χ 3 = 51.03, n = 100, P < 0.0001; Table C4). Actual home ranges had less open forest with granite (2.26 ± 4.90 %, n = 50) than random home ranges
(11.69 ± 10.15 %, n = 50), less closed forest (40.87 ± 9.43 %, n = 50) than random home ranges (53.57 ± 15.29 %, n = 50), and fewer trees per hectare (101.54 ± 48.42 individuals, n = 50) than random home ranges (129.60 ± 60.55 individuals, n = 50; Table
C4). Number of logs per hectare (1.43 ± 1.23 individuals, n = 100, P = 0.572), number of dead trees per hectare (1.13 ± 1.0 individuals, n = 100, P = 0.892), and number of saplings per hectare (38.08 ± 23.07 individuals, n = 100, P = 0.899) did not differ between actual and random home ranges. In contrast, percentage of open forest with soil
(Wilks’ λ = 0.85, F2,45 = 3.97, P = 0.026), number of dead trees per hectare (Wilks’ λ =
0.80, F2,47 = 5.84, P = 0.005), and number of saplings per hectare (Wilks’ λ = 0.85, F2,45
= 4.05, P = 0.024) differed between sexes. Home ranges of males had less open forest with soil ( F1,46 = 7.75, P = 0.008) and fewer saplings per hectare ( F1,46 = 5.66, P = 0.022)
than home ranges of females (Table C5); number of dead trees only differed between
random home ranges ( F1,48 = 9.71, P = 0.003). No other cover composition
characteristics differed between sexes, seasons, or their interactions (Wilks’ λ, all P >
0.05). Cover composition and seasons appear to influence home range size of Mearns’s
squirrels ( F3,46 = 48.82, P < 0.0001). Percentage of closed forest (β = 0.64, P < 0.0001) was positively associated, whereas number of trees per hectare (β = 0.49, P < 0.0001) and seasons (β = 0.17, P = 0.023) were negatively associated with home range size. In
contrast, percentage of open forest with granite ( P = 0.707), sex ( P = 0.572), number of 130
logs per hectare ( r = 0.026, P = 0.858), and number of dead trees per hectare ( r = 0.132,
P = 0.361) were not associated.
Density of juvenile squirrels was lower in 2007, whereas density of adults was
greater during the same year (Table C6). With slight variations, sex ratios remained
similar for the two years of study with more presence of adult males than females (Table
C6). An interspecific association between population density and male home range size
2 was found combining the information with other species of tree squirrels ( R = 0.464, F1,9
= 7.79, P = 0.021; Fig. C5).
DISCUSSION
Overall, home range size of Mearns’s squirrels was larger than those reported for
red (Goheen and Swihart 2005; Gurnell 1984; Koprowski et al. 2007; Layne 1954;
Leonard and Koprowski 2009; Rusch and Reeder 1978; C.C. Smith 1968) and Douglas’s
squirrels (Koford 1982). Food availability is suggested as one of the main factors
influencing home range size (Herfindal et al. 2005; Ostfeld 1985). In red squirrels,
territory size may be inversely proportional to food availability (C.C. Smith 1968).
During 2006, we observed a clear decline in pine cone production compared to the previous year and consequently expected larger home ranges; similar to that reported for
red squirrels following a seed crop failure (M.C. Smith 1968). However, home ranges of
males and females did not differ between years. In areas with high variation in rainfall
and food availability, species such as Arizona gray squirrels ( Sciurus arizonensis ) and
Eurasian red squirrels ( S. vulgaris ) apparently respond to this variation by maintaining
large home ranges (Cudworth and Koprowski 2010; Lurz et al. 2000). Without middens 131
or predictable feeding stations to defend as in other Tamiasciurus (Gurnell 1987; Layne
1954), Mearns’s squirrels appear to have adopted a strategy similar to that used by tree
squirrels in the genus Sciurus . Interestingly, female home ranges remained constant between seasons, similar to space use patterns of nonterritorial Sciurus squirrels
(Cudworth and Koprowski 2010; Gurnell 1987; Pasch and Koprowski 2006) and polygynous mammals in general (Ostfeld 1985). In territorial red squirrels, female home
range sizes commonly differ among seasons, with a considerable increase during the
summer (Koprowski et al. 2007). In other words, while home range size of territorial red
squirrels is influenced by season, in Mearns’s squirrels the primary influence is sex.
Lack of sexual dimorphism in tree squirrels (Gurnell 1987) suggests that resource
requirements should be similar for both sexes during nonmating seasons (Pasch and
Koprowski 2006). However, since female reproductive success in mammals is limited by
their ability to acquire food and convert it into weaned offspring, whereas male
reproductive success is limited by access to females (Ostfeld 1985), male home range
size is expected to be larger during mating seasons. Male Mearns’s squirrels had larger
home ranges than those of females, particularly during mating seasons, consistent with
the space use pattern observed in other nonterritorial Sciurus squirrels (Cudworth and
Koprowski 2010; Hanski et al. 2000; Kantola and Humphrey 1990; Lurz et al. 2000;
Pasch and Koprowski 2006; Taulman and Smith 2004).
Home range size only was positively associated with body mass for female 95%
MCP but not for males. Similar positive associations have been reported for male
Eurasian red squirrels where increased home range size was positively related to 132 reproductive success (Wauters and Dhondt 1992). Our findings seem to corroborate that species of tree squirrels with larger body sizes also tend to have larger home ranges, similar to other carnivores and herbivores (Harestad and Bunnell 1979). Mearns’s squirrels have a larger body mass than red and Douglas’s squirrels (Steele 1998, 1999), which may account in part for their larger home ranges (Harestad and Bunnell 1979) necessary to meet their resource requirements (Gurnell 1987).
Percentage overlap of Mearns’s squirrels was influenced primarily by seasons, suggesting that space use is similar for both sexes within seasons with squirrels overlapped by more conspecifics of either sex during mating seasons. In other
Tamiasciurus , the defense of territories around middens restricts overlap to mating seasons when males travel long distances in search of estrous females (Gurnell 1987), whereas overlap between females remains minimal during all seasons (Koprowski et al.
2007). In Sciurus , overlap is frequently lower and constant for females through seasons, whereas it is greater for males and enlarges during mating seasons (Linders et al. 2004;
Lurz et al. 2000). In contrast, overlap between female Mearns’s squirrels was greater during mating seasons, possibly as a result of females searching more widely for food in the open and xeric forests of SSPM, and thus increasing overlap with other males and females; further suggesting lack of territoriality in this species. In Eurasian red squirrels, overlap between females is known to increase with depletion of available seed food through cone consumption and seed shed (Lurz et al. 2000). Mearns’s squirrels also rely on tree cavities for nesting (Ramos Lara and Koprowski 2012). As a result, males and females were observed frequently exploring potential tree cavities which may have 133
contributed to the overlap with other conspecifics, especially in breeding females (Hanski
et al. 2000; Peterson and Gauthier 1985). This also may account in part for the decrease
in overlap between females during nonmating seasons when individuals use this time to
recover fat reserves lost to reproduction (Thompson 1977). Home range size of male
Arizona gray squirrels is positively associated with number of females overlapped during
mating seasons (Cudworth and Koprowski 2010). However, lack of this association in
Mearns’s squirrels may be due to females maintaining large home ranges and
consequently overlapping numerous males.
In general, distances traveled by Mearns’s squirrels during their daily activities
were similar to those reported for other Tamiasciurus (Rusch and Reeder 1978) and
Sciurus squirrels (Edelman and Koprowski 2006; Pasch and Koprowski 2006). Distances traveled by males during nonmating seasons were similar to distances traveled by females during both seasons. This space use pattern also has been reported in other tree squirrels
(Edelman and Koprowski 2006; Linders et al. 2004), supporting the hypothesis of similarity of resource requirements between the sexes in tree squirrels with no sexual dimorphism (Gurnell 1987; Pasch and Koprowski 2006). Greater distances traveled and larger home ranges by nonterritorial male squirrels may be a mechanism to maximize contact with potential mates during mating seasons and to find richer feeding patches during nonmating seasons to recover energy stores lost during mating seasons
(Koprowski 1998; Koprowski 2007; Wauters and Dhondt 1998). Similar distances traveled during both seasons suggest that adult female Mearns’s squirrels have resource requirements similar to those of males during nonmating seasons. Juvenile dispersal in 134
Mearns’s squirrels is similar to other species of tree squirrels with males traveling greater distances from their natal areas before settling and females being more philopatric
(Gurnell et al. 2001; Gurnell 1987; Koprowski 1996). However, more studies are still needed to determine if the mechanism of juvenile dispersal in Mearns’s squirrels without the constraint of middens is similar to other territorial Tamiasciurus (Larsen and Boutin
1994; Price and Boutin 1993).
Home ranges of Mearns’s squirrels were characterized by less granitic soil and fewer trees than random home ranges. However, Mearns’s squirrels have been collected in remote areas such as La Grulla (Lindsay 1981), and La Corona de Abajo (Yensen and
Valdés Alarcón 1999), and observed at Punta San Pedro (J. Vargas, pers. comm.), where granitic soils are common (Appendix F). Tree canopy cover within home ranges was on average 40.9% closed supporting the hypothesis that lack of middens may be due to the open and xeric forests in SSPM (Koprowski et al. 2006). Other Tamiasciurus depend on forests with shaded areas and cool temperatures to construct and maintain middens
(Brown 1984; Zugmeyer and Koprowski 2009a). For instance, areas where disturbances such as fire and insects have killed trees and opened up the forests reduced occupancy of midden sites by red squirrels (Wood et al. 2007). In SSPM, the granitic and sandy soils have excessive drainage with extreme water deficits and do not retain sufficient moisture to support a shallow rooted perennial plant cover (Evett et al. 2007). Male and female
Mearns’s squirrels had similar access to important habitat characteristics such as mature trees, dead trees, logs, and closed forest; required for tree cavity nesting (Ramos Lara and Koprowski 2012). Male and female home ranges were apparently influenced by tree 135
density with larger home range sizes in areas with high occurrence of saplings but low presence of mature trees. Because trees provide food and shelter to arboreal squirrels, their abundance and distribution may affect both population density and home range sizes (Gurnell 1987; Lurz et al. 2000; Rusch and Reeder 1978).
Density estimates of Mearns’s squirrels were similar to those reported for other species of tree squirrels (Carey 1995; Pasch and Koprowski 2005; Rusch and Reeder
1978). Sex ratios also were similar to other tree squirrels with more males than females
(Gurnell 1987; Kemp and Keith 1970; Layne 1954; Rusch and Reeder 1978). Our findings support the hypothesis that home range size in tree squirrels may be influenced by population density (Heaney 1984). Mearns’s squirrels seem to fall in this pattern with larger home ranges but lower population density than other red squirrel populations.
The lack of middens appears to be associated with the loss of territorial behavior in
Mearns’s squirrels that is characteristic of the genus Tamiasciurus (Gurnell 1987;
Ramos Lara and Koprowski 2012). Consequently, this may have altered the home range dynamics of Mearns’s squirrels, which seem to have adopted strategies similar to nonterritorial squirrels in the genus Sciurus to persist in the open and xeric forests of
SSPM. Mearns’s squirrels provide an important opportunity to learn more about the evolution of territoriality in arboreal squirrels and other species. But more importantly, conservation of Mearns’s squirrels must include the unique space use pattern and enlarged home ranges observed in this study. Our findings suggest that remote areas in
SSPM have suitable habitat for Mearns’s squirrels, although possibly in low population densities. The three known locations where the species has been collected for museum 136
specimens: Vallecitos, La Grulla, and La Corona de Abajo (Yensen and Valdés Alarcón
1999; Appendix F), are the primary areas to be protected for the conservation of the
species. However, it is important to verify if other areas in SSPM also maintain Mearns’s
squirrel populations as our model suggests (Appendix E).
RESUMEN
A lo largo de la mayoría de su rango, las ardillas arborícolas en el género
Tamiasciurus defienden territorios exclusivos centrados en grandes resguardos de conos,
conocidos como basurales, los cuales juegan un papel vital en su dinámica de ámbito
hogareño. La ardilla de Mearns ( T. mearnsi ) es la especie más sureña en el género, conocida de solamente tres lugares en la Sierra de San Pedro Mártir (SSPM), Baja
California, México. A diferencia de otros congéneres, la especie no construye basurales y por tanto proporciona una excelente oportunidad para evaluar el uso de espacio sin las restricciones de resguardar alimento. Utilizamos telemetría e imágenes de satélite para examinar si la dinámica de ámbito hogareño y las densidades poblacionales de las ardillas de Mearns difieren de otros congéneres. También evaluamos lo adecuado del hábitat para la especie en áreas remotas de la SSPM al comparar características del hábitat dentro de los ámbitos hogareños con lugares al azar. En general, la dinámica de ámbito hogareño de las ardillas de Mearns es similar a las ardillas no territoriales en el género
Sciurus , con los machos teniendo ámbitos hogareños más grandes que las hembras todo el año, sugiriendo que la ausencia de basurales está asociada con las estrategias únicas adoptadas por las ardillas de Mearns para persistir en estas montañas. Comparado con otras especies de ardillas arborícolas, el sobrelapamiento del ámbito hogareño entre 137
hembras es más grande durante las temporadas reproductivas, similar al de los machos.
Las densidades poblacionales de las ardillas de Mearns fueron similares a otras especies
de ardillas arborícolas. Áreas remotas en la SSPM parecen tener hábitat adecuado para la
especie. Las ardillas de Mearns proporcionan una excelente oportunidad para aprender
más sobre la evolución de la territorialidad. Asimismo, planes de conservación deben
incluir el patrón único de uso de espacio y ámbitos hogareños engrandecidos observados
en la especie.
ACKNOWLEDGMENTS
We thank the Desert Southwest Cooperative Ecosystem Studies Unit, the
Intermountain Region International Conservation Office of the National Park Service, the
Arizona Agricultural Experiment Station, and T&E, Inc. for funding. The Consejo
Nacional de Ciencia y Tecnología and the Wallace Research Foundation provided financial support to N. Ramos Lara. L. Norris, D. Swann, and N. Kline of the National
Park Service and W. Zúñiga, Á. López, and M. Valles of the Sierra de San Pedro Mártir
National Park supported the concept of the project. J. Franco, P. Strittmatter, B. Powell,
J. Sasian, J. Bohigas, D. Hiriart, D. Carrasco, A. García, I. González, and E. Valdés facilitated housing logistics at Observatorio Astronómico Nacional. The Servicio
Meteorológico Nacional provided temperature and precipitation data of the region. W.
Shaw, R. W. Mannan, B. Pasch, M. Merrick, N. Tautfest, C. Schvarcz, C. Zugmeyer, and
G. Palmer assisted with fieldwork. S. Drake assisted with the orthocorrection of the satellite imagery. L. Bojórquez, S. Stephens, R. Minnich, J. Vargas, C. Porras, E.
Meling, E. Mellink, E. Salgado, B. Mackintosh, and G. Mackintosh graciously shared 138
their knowledge of the Sierra de San Pedro Mártir. E. E. Posthumus, J. L. Bronstein, M.
J. Merrick, R. W. Mannan, and W. Shaw provided valuable comments that improved the
manuscript.
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148
TABLE C1.―Results of two way ANOVAs used to compare home range size of Mearns’s squirrels ( Tamiasciurus mearnsi ) between sexes, years of study, seasons, and their respective interactions, in Baja California, Mexico, from May 2006
November 2007. Significance (P < 0.05) is marked with an asterisk. MCP: minimum convex polygon.
95% MCP 95% Fixed kernels 50% Fixed kernels
df F P F P F P
Between years
Sex 1 6.434 0.016 * 4.581 0.039 * 3.218 0.081
Years 1 0.004 0.951 0.028 0.868 0.040 0.843
Years x sex 1 0.005 0.947 0.411 0.526 0.593 0.446
Between seasons
Sex 1 18.496 0.000 * 7.435 0.009 * 4.256 0.045 *
Seasons 1 6.421 0.015 * 3.999 0.051 3.120 0.084
Seasons x sex 1 6.155 0.017 * 2.256 0.140 1.560 0.218
149
TABLE C2.―Results of two way ANOVAs used to compare percentage of male and female 95% fixed kernel home ranges overlapped by male and female conspecifics, number of individuals overlapped by male and female conspecifics, and maximum distance traveled by male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating and nonmating seasons, from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk.
Overlap (%) No. individuals
Males Females Males Females Distance (m)
df F P F P F P F P F P
Sex 1 0.678 0.414 0.477 0.494 5.818 0.019 * 3.661 0.063 4.098 0.049 *
Seasons 1 12.928 0.001 * 8.582 0.006 * 88.538 0.000 * 24.005 0.000 * 5.577 0.022 *
Seasons x sex 1 0.629 0.431 0.121 0.730 3.527 0.066 0.165 0.687 5.542 0.023 *
150
TABLE C3.―Mean (± SD ) percentage of male and female 95% fixed kernel home range overlapped by male and female conspecifics, and number of individuals overlapped by male and female conspecifics, during mating and nonmating seasons for Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, from May 2006 November 2007.
Overlap (%) Number of individuals
Mating n Nonmating n Mating n Nonmating n
Males overlapped by
Males 7.06 ± 4.32 14 2.59 ± 5.60 15 6.57 ± 3.30 14 0.93 ± 0.96 15
Females 9.63 ± 9.12 14 2.64 ± 4.00 15 4.43 ± 1.60 14 0.67 ± 0.72 15
Females overlapped by
Males 14.05 ± 6.27 13 6.20 ± 10.81 8 4.77 ± 3.49 13 1.25 ± 1.65 8
Females 13.01 ± 12.26 13 3.04 ± 7.39 8 3.23 ± 0.83 13 0.25 ± 0.46 8
151
TABLE C4.—Results of stepwise multiple logistic regression used to compare cover composition characteristics between
95% fixed kernel home ranges of Mearns’s squirrels ( Tamiasciurus mearnsi ) with random home ranges in Baja California,
Mexico, from May 2006 November 2007. Significance ( P < 0.05) is marked with an asterisk.
Variables Coefficient SE χ2 df P Odds ratio
% Open forest with granite 0.190 0.054 12.474 1 0.0001* 1.209
% Closed forest 0.069 0.022 10.329 1 0.001* 1.072
No. trees/ha 0.011 0.005 3.899 1 0.048* 1.011
Constant 5.408 1.286 17.675 1 0.0001 0.004
152
TABLE C5.—Cover composition for male and female 95% fixed kernel home ranges and random home ranges of
Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating and nonmating seasons, from May
2006 November 2007, using satellite imagery. Means (± SD ) are provided.
Sex and Mating season Nonmating season
characteristics Actual ranges n Random ranges n Actual ranges n Random ranges n
Males
% Open forest with soil 51.07 ± 11.24 14 32.86 ± 18.53 14 55.79 ± 11.48 15 32.88 ± 20.51 15
% Open forest with granite 1.55 ± 2.03 14 10.32 ± 10.14 14 5.12 ± 8.06 15 13.74 ± 8.79 15
% Closed forest 47.38 ± 10.93 14 56.83 ± 15.63 14 39.09 ± 10.09 15 53.38 ± 16.55 15
No. logs/ha 1.49 ± 1.75 14 0.86 ± 0.91 14 0.96 ± 1.08 15 0.91 ± 1.35 15
No. dead trees/ha 0.75 ± 0.56 14 0.78 ± 0.61 14 0.69 ± 0.83 15 1.04 ± 1.84 15
No. saplings/ha 23.22 ± 15.77 14 25.56 ± 16.44 14 36.76 ± 21.13 15 40.41 ± 26.03 15
No. trees/ha 87.20 ± 33.11 14 114.41 ± 47.93 14 90.98 ± 53.13 15 115.17 ± 47.02 15
Females
% Open forest with soil 62.99 ± 5.58 13 36.54 ± 18.00 13 59.08 ± 5.02 8 38.62 ± 20.34 8 153
% Open forest with granite 0.58 ± 1.43 13 10.44 ± 9.98 13 0.90 ± 0.78 8 12.27 ± 13.76 8
% Closed forest 36.43 ± 5.25 13 53.02 ± 14.80 13 40.02 ± 4.59 8 49.11 ± 14.64 8
No. logs/ha 1.08 ± 0.93 13 0.70 ± 1.25 13 1.08 ± 1.54 8 0.06 ± 0.18 8
No. dead trees/ha 0.43 ± 0.75 13 0.22 ± 0.46 13 0.79 ± 1.45 8 0.11 ± 0.32 8
No. saplings/ha 47.53 ± 25.91 13 49.68 ± 23.30 13 41.99 ± 21.76 8 46.00 ± 21.95 8
No. trees/ha 119.43 ± 56.81 13 163.25 ± 78.40 13 117.35 ± 40.83 8 128.53 ± 58.53 8
154
TABLE C6.—Annual density estimates (squirrel/ha) and sex ratios (male:female) of adult (>240 g) and juvenile Mearns’s squirrels ( Tamiasciurus mearnsi ) in the Sierra de San Pedro Mártir, Baja California, Mexico, from May 2006 November 2007.
2006 2007
Density Sex ratio Density Sex ratio
Adults 0.12 1.25:1 0.35 1.25:1
Juveniles 0.31 1.29:1 0.01 0.00:1
All age classes 0.43 1.28:1 0.37 1.15:1
155
FIGURE LEGENDS
FIG . C1.―Mean (± SD ) home range size estimates of adult male and female
Mearns’s squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating
and nonmating seasons from May 2006 November 2007. MCP: minimum convex polygon.
FIG . C2.—Intraspecific relationship between 95% minimum convex polygon
(MCP) home range size and body mass of adult male (A) and female (B) Mearns’s
squirrels ( Tamiasciurus mearnsi ) in Baja California, Mexico, during mating seasons from
May 2006 November 2007.
FIG . C3.—Interspecific relationship between mean home range size and adult body mass for seven species of tree squirrels monitored with telemetry. Acronyms and data sources: Sar (Sciurus arizonensis —Brown 1984; Cudworth and Koprowski 2010), Sgr (S. griseus —Carraway and Verts 1994; Linders et al. 2004), Sna (S. nayaritensis —Brown
1984; Pasch and Koprowski 2006), Sab (S. aberti —Brown 1984; Edelman and
Koprowski 2006), Svu (S. vulgaris ―Lurz et al. 2000; Wauters and Dhondt 1989), Thu
(Tamiasciurus hudsonicus —Zugmeyer and Koprowski 2009; Brown 1984), Tme (T. mearnsi —Herein). All authors used 95% fixed kernel estimates, except for Lurz et al.
(2000): 85% core area.
156
FIG . C4.—Maximum distance traveled by adult male and female Mearns’s squirrels
(Tamiasciurus mearnsi ) from their cavity nests in Baja California, Mexico, during mating
and nonmating seasons from May 2006 November 2007.
FIG . C5.—Interspecific relationship between male home range size and density for
ten species of tree squirrels. Acronyms and data sources: Sar (Sciurus arizonensis —
Cudworth and Koprowski 2010), Sna (S. nayaritensis —Pasch and Koprowski 2005;
Pasch and Koprowski 2006), Sab (S. aberti —Heaney 1984), Sgn (S. granatensis —
Heaney 1984), Sgr (S. griseus —Heaney 1984), Sca (S. carolinensis —Heaney 1984), Sni
(S. niger —Pasch and Koprowski 2005; Sheperd and Swihart 1995), Svu (S. vulgaris —
Lurz et al. 2000), Thu (Tamiasciurus hudsonicus —Heaney 1984; Zugmeyer and
Koprowski 2009), Tme (T. mearnsi —Herein). Methods used to estimate home range size may differ among authors.
157 FIG . C1 FIG . C2 158
A)
B)
159 F IG . C3
160 FIG . C4
161 FIG . C5
162
APPENDIX D
A STRANGER IN THE GENUS: LIFE HISTORY AND BEHAVIORAL TACTICS OF
MEARNS’S SQUIRRELS ( TAMIASCIURUS MEARNSI )
Manuscript prepared for submission to Journal of Mammalogy
163
Send proofs to: Nicolas Ramos Lara Wildlife and Fisheries Science School of Natural Resources and the Environment 325 Biological Sciences East Building The University of Arizona Tucson, AZ 85721 USA Email: [email protected]
Running Heading: Life history of Tamiasciurus mearnsi
A stranger in the genus: life-history and behavioral tactics of Mearns’s squirrels
(Tamiasciurus mearnsi )
NICOLÁS RAMOS LARA * AND JOHN L. KOPROWSKI
Wildlife and Fisheries Science, School of Natural Resources and the Environment,
University of Arizona, Tucson, AZ 85721
Comparative analyses of variation in life history and behavior have provided
insight into adaptation among taxa. In mammals, red squirrels ( Tamiasciurus hudsonicus ) and Douglas’s squirrels (T. douglasii ) often are used as models to assess life history variation. In contrast, the southernmost member of the genus, the Mearns’s squirrel ( T. mearnsi ), has remained poorly studied. However, the species exhibits important deviations from common behaviors observed in other congeners such as lack of middens and dreys. Using telemetric monitoring, we examined if the absence of these structures may be associated with differences observed in life history and behavioral 164
tactics between Mearns’s squirrels and other congeners. We also examined if interyear
variation in weather and food supply strongly influences fitness related traits and behavior of the species. Overall, reproduction and survival of Mearns’s squirrels are
similar to other congeners. However, despite occupying a warmer and drier habitat,
mean litter size of Mearns’s squirrels is similar to other tree squirrels located in cold and
mesic forests at higher latitudes. Survival of adult squirrels was influenced by sex and body mass. Mearns’s squirrels are heavier and apparently also larger than other
congeners, possibly in part as an adaptation to feed on large pine cones ( Pinus ). Interyear
variation in weather and food supply strongly influenced fitness related traits and behavior of Mearns’s squirrels. The lack of middens and dreys seems to be associated
with tactics adopted by Mearns’s squirrels that are similar to those found in Sciurus
squirrels such as scatterhoarding, communal nesting behavior, and loss of territoriality,
suggesting important adaptive implications.
Key words: adaptation, Baja California, endemic species, fitness, Mexico, reproduction,
Sierra de San Pedro Mártir, survival, territoriality, time budget
*Correspondent: [email protected]
Life history traits (i.e., patterns of growth, reproduction, and survival) are used to
measure both the direction and rate of evolutionary change (Dobson and Oli 2007). As a
result, comparative analyses of life history variation have provided an important insight
into adaptation in diverse taxa (e.g., Lewis and Storey 1984; Charnov 1991; Kirk 1997; 165
Chiaraviglio et al. 2003; Sears 2005; Karl et al. 2008; Quadros et al. 2009; Camfield et al.
2010). Life history variation is created and maintained by differences in the availability and quality of resources among habitats, and is often considered to be evidence of adaptive strategies for dealing with disparate environments (Sears and Angilleta 2003).
Comparative analyses of life history variation at the interspecific level demonstrate that vertebrates rank along a fast slow continuum, from small, short lived species with high fecundity to large, long lived animals with low fecundity (Focardi et al. 2008). Similarly, availability and access to resources such as food, space, and nest sites may affect the life history traits of many animals (Monson et al. 2000; Wiebe et al. 2006). Nests are especially critical for survival of nestlings, protection from predators, resting, and shelter from adverse weather conditions (Steele and Koprowski 2001; Ramos Lara and
Cervantes 2007). In birds, nest sites are often assumed to be the primary factor limiting densities of secondary cavity nesters (Miller 2010). Therefore, individuals with high quality nesting sites will realize increased fitness relative to those nesting in poor quality areas. Food limitation also may influence clutch size and other life history traits in terrestrial vertebrates (Koskela et al. 1998; Ferretti et al. 2005). Because of resource limitation, a successful energetic strategy for any animal requires allocation of finite resources toward maintenance, growth, and reproduction in an ever changing environment (Greer and Koprowski 2009). Sex differences in fitness limiting resources are known to have profound effects on the ecology of the sexes (Koprowski and Corse
2005). Therefore, time budget variation in animals with diets of different quality is determined by a trade off between energetic value of food consumed and time and 166
energetic costs for food acquisition and processing (Khokhlova et al. 2003). Varying the
time budget is a means of coping with a changing environment. Because time is limited,
time spent in one activity decreases the time available for some other activity (Armitage
et al. 1996). Sex differences in time budgets and activity patterns also may suggest
differential constraints that affect each sex (Koprowski and Corse 2005).
In mammals, squirrels (Rodentia: Sciuridae) provide an excellent opportunity to
examine adaptive strategies (e.g., Hayssen 2008; Heaney 1984; Lord 1960). In tree
squirrels, the genus Tamiasciurus contains three species (Thorington and Hoffmann
2005): red squirrels ( T. hudsonicus ), Douglas’s squirrels ( T. douglasii ), and Mearns’s squirrels ( T. mearnsi ). Red squirrels are the most widely distributed of the three species occurring across much of boreal Canada and the northern United States (Steele 1998), whereas Douglas’s squirrels are found in coniferous forests of the Pacific Coast (Steele
1999). The two species are sympatric in parts of British Columbia, Washington, and
Oregon (Arbogast et al. 2001). In contrast to these two Tamiasciurus , Mearns’s squirrels are endemic to the coniferous forests of the Sierra de San Pedro Mártir (SSPM), Baja
California, Mexico (Lindsay 1981). The species is separated from the nearest populations of red and Douglas’s squirrels by ca. 600 km of mostly nonforested lowlands
(Yensen and Valdés Alarcón 1999). Mearns’s squirrels likely became isolated from
Douglas’s squirrels almost 12,000 years ago (Arbogast et al. 2001; Lindsay 1981; Yensen and Valdés Alarcón 1999). The species is known from 2,100 m to 2,750 m elevation in the coniferous forests of SSPM (Yensen and Valdés Alarcón 1999). Considered a rare species (Huey 1964), Mearns’s squirrels are federally listed as threatened in Mexico 167
(SEMARNAT 2010), due to their restricted distribution, low population density, and
isolation, and as endangered by the International Union for Conservation of Nature
(IUCN—de Grammont and Cuarón 2008). Although the species was described more
than 100 years ago (Allen 1893; Townsend 1897), little is known about the ecology of
this southernmost Tamiasciurus (Koprowski et al. 2006).
Interestingly, Mearns’s squirrels exhibit important deviations from common behaviors observed in other congeners, possibly due to the open and xeric characteristics
of the forests in SSPM and to the long period of isolation in these mountains. For
instance, red and Douglas’s squirrels build and defend larderhoards (known as middens)
to store food throughout most of their range (Steele 1998, 1999), whereas Mearns’s
squirrels do not exhibit this behavior (Koprowski et al. 2006). Defending a territory
around middens is costly in energy and time for red and Douglas’s squirrels and may
interfere with other behaviors such as courtship, mating, feeding, and rearing young
(Smith 1992; Descamps et al. 2009). Similarly, red and Douglas’s squirrels use leaf nests
(known as dreys), tree cavities, and underground burrows for nesting (Flyger and Gates
1982; Steele 1998), whereas Mearns’s squirrels rely on tree cavities (Ramos Lara and
Koprowski 2012). Herein, we examined if the lack of middens and dreys may be
associated with differences observed in life history and behavioral tactics between
Mearns’s squirrels and other Tamiasciurus and Sciurus squirrels. In particular, we
assessed reproduction, survival, body mass, nesting and feeding behavior, and time budgets. We also examined if interyear variation in weather and food supply strongly
influences fitness related traits and behavior of Mearns’s squirrels. 168
MATERIALS AND METHODS
Study area .―SSPM is located ca. 100 km southeast of Ensenada, Baja California,
Mexico (Stephens et al. 2003). SSPM was established as a Forest Reserve in 1932, as a
National Park in 1947, and has been proposed as a Biosphere Reserve (Bojórquez Tapia et al. 2004). SSPM National Park comprises 65,000 ha of which coniferous forests cover ca. 40,655 ha (Minnich et al. 2000). Forests are composed of Jeffrey pine ( Pinus jeffreyi ), sugar pine ( P. lambertiana ), lodgepole pine ( P. contorta ), white fir ( Abies concolor ), and limited amounts of quaking aspen ( Populus tremuloides ) and incense cedar ( Calocedrus decurrens ). The most common forest types are Jeffrey pine, Jeffrey pine–mixed conifer, and mixed white fir forests, respectively (Stephens et al. 2003).
Mixed conifer forest on the summit plateau is replaced by chaparral and Sonoran Desert scrub at lower elevations. The most striking feature of the mixed conifer forests is an open park like aspect that consists of mature trees reaching 30–45 m, with few pole sized trees and saplings, and an open shrub cover (Bojórquez Tapia et al. 2004). Elevation averages 2,600 m in the north and decreases to 1,800 m in the southern portion of the range with the highest peaks over 3,000 m (Stephens et al. 2003). Forests have not experienced disturbance from logging, and fires have spread without human interference
(Minnich et al. 2000). Summers are dry except for afternoon thunderstorms of the North
American monsoon (Minnich et al. 2000). According to data recorded by Servicio
Meteorológico Nacional at ejido San Matías, located ca. 25 km north of SSPM, mean
(± SD ) monthly temperature in the region remained similar throughout the study (19.2 °C
± 6.59; Fig. D1). In contrast, mean monthly precipitation in 2005 (22.8 mm ± 25.7) was 169
2.5 times greater than 2006 (9.0 mm ± 16.5) and 2.1 times greater than 2007 (10.7 mm ±
13.5; Fig. D1).
Large scale surveys.—During 2005, we surveyed ca. 2,500 ha of forest in the
margins of the Vallecitos Meadow, where the species was collected previously for
museum specimens (Lindsay 1981; Yensen and Valdés Alarcón 1999), to detect direct
(animal sighting) and indirect (remnants of food with characteristic gnawing) occurrence
of Mearns’s squirrels and to establish potential capture sites. We explored the area on
foot systematically using a topographic map (Centra Publications 1988).
Trapping and telemetry .―We captured Mearns’s squirrels during May August
2006 and 2007. Live traps (Model 201; Tomahawk Live Trap Co., Wisconsin) were placed at the base of large diameter trees, baited with peanuts and peanut butter, covered
with tree bark, and checked at 1 h intervals. Captured squirrels were transferred to a
cloth handling cone (Koprowski 2002) where we collected data on sex, age class,
reproductive condition, and body mass. Adult animals (≥240 g) were fitted with radio
collars (Model SOM 2190; Wildlife Materials International, Inc., Carbondale, Illinois)
and uniquely numbered Monel ear tags (Style #1005 1; National Band and Tag Co.,
Newport, Kentucky) with colored plastic washers (Style #1842; National Band and Tag
Co., Newport, Kentucky) on both ears; however, juveniles only were marked with ear
tags. We distinguished adults and juveniles based on reproductive condition and body
mass of captured animals. All squirrels were released at the capture site after ≤8 min of
handling time; no animals were injured during the study. We calculated trap effort by
counting the total number of days and hours employed for trapping during 2006 and 170
2007, as well as the total number of Mearns’s squirrels captured during the same period
of time. Trapping and handling procedures were conducted with approval from The
University of Arizona Institutional Animal Care and Use Committee (protocol # 05 038),
in accordance with guidelines of the American Society of Mammalogists (Gannon et al.
2007), and with permits from the following Mexican authorities: Dirección Forestal y de
la Fauna Parque Nacional Sierra de San Pedro Mártir and Dirección General de Vida
Silvestre.
We used a 3 element yagi directional antenna (Wildlife Materials International,
Inc., Carbondale, Illinois) and receiver (Model R 1000, Communications Specialists,
Inc., Orange, California) to locate squirrels from 0700 2000 h at >2 hr intervals to avoid
spatial autocorrelation (White and Garrott 1990). We tracked squirrels by homing
monthly in spring (April) and autumn (September November) and weekly during summer
(May August); animals were not monitored during winter (December March) due to
snow and limited access.. When sighted, we recorded reproductive condition, diet, and
different behaviors (Table D1) of squirrels with the aid of binoculars (Bushnell 10x50;
Forestry Suppliers, Inc., Jackson, Mississippi). We conducted all observations from ≥10
m and for a period <30 min to avoid interfering with the natural behavior of squirrels;
however, we also tracked squirrels to their nests to document their behavior and detect presence of litters. Number of nests used by each squirrel and the maximum number of days a nest was used by an individual also were recorded.
Data analysis.—We conducted all statistical analyses with SPSS 17.0 (SPSS Inc.,
Chicago). When necessary, variables were log transformed to better meet the 171
assumptions of parametric tests; however, mean ± SD shown in results are from untransformed values. We used unpaired t tests and Mann Whitney ( U) to examine differences in number of recaptures and body mass between sexes (Zar 1996). To examine life history variation between Mearns’s squirrels with other species of tree squirrels, we used linear regression to explore interspecific association between litter size with temperature, precipitation, percentage of year frost free, latitude, body mass, length of head and body, plant species, and female home range size (Hayssen 2008; Heaney
1984). However, because of the multiple comparisons, we adjusted the level of significance in our analyses to P < 0.006 with a Bonferroni correction. We used the
Kaplan Meier method (Kaplan and Meier 1958) with log rank test to compare survival of adult male and female Mearns’s squirrels. Animals entered the analysis the day following capture and were censored upon loss of the radio signal (Conner 2001) and counted as dead when the radio collar or the remains of an individual were found. A cohort of 8 juvenile squirrels (4 males and 4 females), captured in 2006 and recaptured in
2007 as adults, entered the survival analysis until the second year; however, we also analyzed their survival curves separately for both years. Multivariate Cox proportional hazard modeling was used to explore relationship between survival with mean body mass of squirrels, number of cavities used, maximum number of days using the same cavity nest, sex, and their interactions. Survival was analyzed from May November, when trapping efforts started and animals were radio tracked for the last time each year respectively. We used two way ANOVA to compare body mass, number of nests used, and maximum number of days a nest was used by a squirrel, between sexes and years of 172
study. Chi square (χ 2) was used to examine differences in diet and time budgets between sexes and years (Zar 1996); adjusting the level of significance in our analyses to P <
0.017 due to multiple comparisons. Consequently, we used Bonferroni simultaneous
confidence intervals (Marcum and Loftsgaarden 1980; Neu et al. 1974) to assess
differences among chi square categories. However, because of small sample sizes, we
subdivided diet into three categories for the analysis (tree seeds: Jeffrey pines, lodgepole pines, firs; tree parts: pollen, twigs, branch tips, pine needles; and other food types: fungi, birds, bone, salt, water). Similarly, we subdivided behaviors into three categories:
foraging, idle, and movement (Table D1).
RESULTS
We captured 79 Mearns’s squirrels (adults: 20 males, 18 females; juveniles: 23
males, 18 females). Number of times an individual was recaptured did not differ between
adult males (3.10 ± 2.77 individuals) and females (3.61 ± 3.87 individuals; t36 = 0.47, P =
0.640) or between juvenile males (1.83 ± 0.98 individuals) and females (1.78 ± 1.63 individuals; U = 174.0, n1 = 23, n2 = 18, P = 0.329). Trap effort was 5.76 trap hours/squirrel in 2006 and 7.25 trap hours/squirrel in 2007.
Reproduction .—We observed males with scrotal testes during 21 May to 21 July
2005, 17 May to 7 August 2006, and 22 April to 16 July 2007. However, mating chases were observed during 22 May to 22 July 2005 ( n = 4), 15 May to 25 July 2006 ( n = 21),
and 21 April to 24 June 2007 ( n = 18). Copulations lasted <30 seconds and occurred on the ground, hidden in rock piles, inside hollow logs, and in the branches of trees. We observed a male copulating with a female on 18 June 2007 and a female copulating with 173
multiple males (1 4 individuals) on 24 June 2007. Pregnant females were detected on 21
May 2006 and 22 April 2007. In total, we recorded 14 litters during the three years of
study (3.4 ± 0.8 young/litter); three litters during 15 16 October 2005, 10 litters during 19
May to 24 July 2006, and one litter on 23 May 2007.
Reproductive output was higher in 2006 than 2007. Six (75%) of the eight females
monitored in 2006 were lactating during 20 May to 23 September; two were killed by predators. Of these six squirrels, 2 (25%) were lactating in May and June and again in
August and September, suggesting two litters per year; one in spring and another in
summer. In contrast, only 2 (16.7%) of the 12 females monitored in 2007 were lactating
during 5 8 August; both also produced litters in 2006. Similarly, most juvenile squirrels
were captured in 2006 ( n = 40) compared to 2007 ( n = 1). Whereas four males
recaptured and radio collared in 2007 possessed scrotal testes when ≥10 12 months of
age, none of four females recaptured and radio collared in 2007 were lactating at the
same age. However, one of these females was lactating on 16 May 2008 during our last
visit to the study area when ca. two years of age.
2 Litter size was negatively associated with temperature ( R = 0.416, F1, 15 = 10.69, P
2 = 0.005) and percentage of year frost free ( R = 0.581, F1, 15 = 20.79, P < 0.0001), and
2 positively with latitude ( R = 0.336, F1, 20 = 10.11, P = 0.005) across Tamiasciurus and
Sciurus squirrels (Fig. D2). Litter size was not associated with body mass ( R2 = 0.013,
2 F1, 14 = 0.18, P = 0.675), precipitation ( R = 0.335, F1, 16 = 8.06, P = 0.012), length of
2 2 head and body ( R = 0.008, F1, 13 = 0.11, P = 0.747), number of plant species eaten ( R = 174
2 0.076, F1, 10 = 0.82, P = 0.386), and female home range size ( R = 0.22, F1, 8 = 2.26, P =
0.171; Fig. D2).
Survival .―Number of days alive post collaring for males (134.1 days ± 37.3) and
2 females (80.8 days ± 64.4) did not differ in 2006 (Kaplan Meier, χ 1 = 2.19, P = 0.139); survival for males was 90% (9 out of 10) and for females 75% (6 out of 8). In 2007, number of days alive for males (97.2 days ± 58.2) and females (114.4 days ± 52.1) also
2 was similar (Kaplan Meier, χ 1 = 0.59, P = 0.444); survival for males decreased to 80%
(12 out of 15) and to 58.3% (7 out of 12) for females. During both years, number of days alive for males (195.0 days ± 165.2) and females (135.8 days ± 125.8) also was similar
2 (Kaplan Meier, χ 1 = 1.94, P = 0.163); however, survival for males was 80% (16 out of
20) and for females 61.1% (11 out of 18; Fig. D3). One male and one female were found
alive in May 2008, during a last visit to the study area, increasing the longevity of adult
males to a minimum of 703 days (1.9 years); but not of adult females (1.2 years).
2 Survival was influenced by sex and its interaction with body mass (χ 7 = 19.19, P =
0.008; Table D2). In total, 11 adults (4 males, 7 females) were killed by predators, whereas 27 (16 males, 11 females) were censored (Fig. D3). Potential predators observed in the study area included great horned owls (Bubo virginianus ), red tailed hawks (Buteo jamaicensis ), bobcats ( Lynx rufus ), coyotes ( Canis latrans ), and gray foxes ( Urocyon
cinereoargenteus). Number of days alive for the cohort of juvenile males (439.5 days ±
2 71.0) and females (418.3 days ± 35.2) was similar (Kaplan Meier, χ 1 = 0.12, P = 0.730);
survival during the two years of study was 50% (2 out of 4) for males and 50% (2 out of
4) for females. 175
Body mass .—Adult body mass differed between years ( F1, 74 = 5.24, P = 0.025) but
not sexes ( F1, 74 = 1.09, P = 0.299), with an interaction between years and sexes ( F1, 74 =
7.46, P = 0.008); males were on average 2.6 g heavier in 2007, whereas females were
28.9 g heavier in 2006 (Fig. D4). During both years, mean body mass of males was
271.6 g (± 18.1; range: 220 300; n = 39) and females 271.7 g (± 31.1; range: 220 360; n
= 39); however, a lactating female on 21 May 2006 weighed 360 g. Juvenile body mass of females (206.7 g ± 35.2; n = 29) was greater than that of males (189.8 g ± 30.7; n = 38; t65 = 2.089, P = 0.041). Mean body mass of juveniles (<1 year old) was ≥140 g when
started to explore the forest floor and ≥240 g at sexual maturity.
Nesting behavior .―During the two years of telemetric monitoring, Mearns’s
squirrels nested primarily in tree cavities with only one male nesting occasionally
underground (Ramos Lara et al. 2012). Number of cavity nests used by squirrels did not
differ between sexes ( F1, 39 = 0.01, P = 0.759), years ( F1, 39 = 1.24, P = 0.272), or their interaction ( F1, 39 = 2.28, P = 0.139). During the two years, males used on average 3.40 nests (± 1.79; n = 20) and females 3.59 nests (± 1.58; n = 17). Similarly, maximum number of days a cavity nest was used by an individual did not differ between sexes ( F1,
39 = 0.04, P = 0.840), years ( F1, 39 = 2.01, P = 0.164), or their interaction ( F1, 39 = 0.08, P
= 0.776). During the two years, males used on average the same tree cavity for 56.40 days (± 71.18; n = 20) and females 47.59 days (± 67.74; n = 17).
We observed four instances of squirrels finding their tree cavities occupied by other
squirrels when retreating before dusk, and two instances of males evicting females from
their nocturnal nests. In all cases, squirrels avoided confrontation and moved to another 176
cavity either in the same or nearby tree; however, we found the squirrels nesting in their
original cavities on subsequent days. On 10 August 2007, we saw an adult male digging
a tree cavity in a Jeffrey pine snag. We observed five instances of squirrels carrying
materials for nest bedding during 9 13 August 2005 (3 adult females), 11 August 2006 (1
adult male), and 7 9 June 2007 (1 adult female). Materials included shredded bark and
wood from Jeffrey pines, cotton from a discarded mattress, and furniture foam.
Feeding behavior .—We did not find the middens that are commonly used by other
congeners. In contrast, Mearns’s squirrels cached food items in the branches of trees. On
24 June 2007, a male was feeding on lodgepole pine cones (ca. 20 30) cached underneath
a log but this behavior was not observed again. Mearns’s squirrels fed on pine ( Pinus )
and fir ( Abies ) seeds, pollen from pine strobili, twigs from fir and pine trees, conifer branch tips, pine needles, bones, deer antlers, salt from rocks, and three types of fungi;
including veiled polypore ( Cryptoporus volvatus ). We did not observe squirrels feeding on seeds of canyon live oaks ( Quercus chrysolepis ) that are abundant in the study area.
Squirrels fed on fresh pine cones from April October and fir seeds from May August; however, squirrels fed on seeds from dry and open pine cones from June August and
October April. Pollen was eaten in June and July. Conifer branch tips and twigs were consumed from April November. We only observed adult females feeding on bones and salt from May October. Fungi were consumed from May November. During the summer rains, squirrels drank water from temporary creeks and stagnant water on boulders. We were unable to determine whether a juvenile female (12 June 2006) and an 177
adult female (6 July 2006) fed on nestlings or eggs after attacking the tree cavity nests of
western bluebirds ( Sialia mexicana ).
During 2006, in 158 telemetric observations (males, n = 81; females, n = 77),
squirrels spent more time feeding on Jeffrey pine seeds, lodgepole pine seeds, and fungi
compared to other food types (Fig. D5). Together, tree seeds accounted for 79.0% of the
diet of squirrels, tree parts 7.6%, and other food types 13.4%, with no difference between
2 sexes (χ 2 = 5.06, P = 0.086; Fig. D5). During 2007, in 320 telemetric observations
(males, n = 179; females, n = 141), squirrels spent more time feeding on Jeffrey pine
seeds, branch tips, lodgepole pine seeds, and pollen compared to other food types (Fig.
D5). Together, tree seeds accounted for 66.3% of the diet of squirrels, tree parts 30.5%,
2 and other food types 3.2%, with no difference between sexes (χ 2 = 1.53, P = 0.466; Fig.
D5). Between years, males spent 3.4 times more feeding on tree parts (98% CI = 0.00
0.17), and 3.4 times less on other food types (98% CI = 0.00 0.15) during 2007 compared
2 to 2006 (χ 2 = 15.88, P = 0.0004), with no difference in tree seeds (98% CI = 0.73 0.95;
Fig 5). Similarly, females spent 4.9 times more feeding on tree parts (98% CI = 0.00
0.14), and 4.6 times less on other food types (98% CI = 0.07 0.32) during 2007 compared
2 to 2006 (χ 2 = 26.78, P < 0.0001); with no difference in tree seeds (98% CI = 0.60 0.88;
Fig 5). During the two years, males and females spent similar times feeding on tree seeds
2 (70.5%), tree parts (22.8%), and other food types (6.7%; χ 2 = 6.74, P = 0.035).
Time budgets .―During 2006, in 506 telemetric observations (males, n = 268; females, n = 238), squirrels spent more time feeding, searching for food, in their cavities, and resting compared to other behaviors (Fig. D6). Together, foraging behaviors 178
accounted for 50.9%, idle 34.1%, and movement 15.0%, with no difference between
2 sexes (χ 2 = 4.44, P = 0.109; Fig. D6). During 2007, in 916 telemetric observations
(males, n = 509; females, n = 407), squirrels spent more time feeding, searching for food, resting, and running compared to other behaviors (Fig. D6). Together, foraging behaviors accounted for 63.6%, idle 19.8%, and movement 16.6%, with no difference
2 between sexes (χ 2 = 0.04, P = 0.981; Fig. D6). Between years, males spent 1.5 times
2 more in idle behaviors (98% CI = 0.22 0.38) during 2006 compared to 2007 (χ 2 = 9.43,
P = 0.009), with no differences in foraging (98% CI = 0.47 0.64) and movement behaviors (98% CI = 0.09 0.21; Fig. D6). In contrast, females spent 1.4 times more in
foraging behaviors (98% CI = 0.38 0.56) and 1.9 times less in idle behaviors (98% CI =
2 0.30 0.47) during 2007 compared to 2006 (χ 2 = 27.48, P < 0.0001); with no difference in movement behaviors (98% CI = 0.09 0.22; Fig. D6). During the two years, males and females spent similar times in foraging (59.0%), idle (25.0%), and movement behaviors
2 (16.0%; χ 2 = 1.88, P = 0.390).
DISCUSSION
Life history tactics of Mearns’s squirrels .—Overall, reproduction of Mearns’s
squirrels appears to follow the pattern observed in other Tamiasciurus located at higher
latitudes (Table D3). We did not monitor Mearns’s squirrels during winter, but backdating from the emergence of litters suggests that mating season starts in February or
March similar to other congeners (Koford 1982; Layne 1954). Mearns’s squirrels had
smaller litter sizes compared to other congeners (Table D3). However, it is still unknown
if the species can produce larger litter sizes during years of abundant food supply. 179
Weather and amount and quality of food are known to regulate reproduction in tree
squirrels (Lair 1985). Our results revealed that interyear variation may strongly affect
reproduction in Mearns’s squirrels. The two peaks in precipitation recorded in 2006 were
consistent with the two litters produced by females in spring and summer (Fig. D1).
Similarly, the only peak in precipitation recorded during 2007 also was consistent with
the only litter produced by females until summer (Fig. D1). Douglas’s and red squirrels
have two litters (Steele 1998, 1999) when winters are not so severe and there is enough
food supply (Gurnell 1987). However, red squirrels inhabiting cold boreal forests at
higher latitudes in North America generally have one litter (Kemp and Keith 1970;
Gurnell 1987; Boutin and Larsen 1993). Milder weather (Millar 1970), longer growing
season for plants (Smith 1981), and high quality food available at the time of conception
(Sullivan 1990) may facilitate multiple litters in Tamiasciurus at lower latitudes such as
Mearns’s squirrels that occur in the southernmost portion of the genus’s range.
Interestingly, despite occupying a warmer and drier habitat, with less presence of snow per year, Mearns’s squirrels show mean litter sizes larger than those of other species of
tree squirrels located at higher latitudes in cold and mesic forests with more presence of
snow per year (Fig. D2: A D). Tree squirrel populations in the midlatitudes have more
litters than those at higher latitudes (Heaney 1984), which also may be the case of
Mearns’s squirrels, as they seem to maintain high reproductive demands similar to
Sciurus squirrels with larger body sizes (Gurnell 1987).
Survival of adults and juveniles differs among all Tamiasciurus with no specific pattern in the genus (Table D3). In Mearns’s squirrels, lower survival rates of adults in 180
2007 possibly was due to the decline in precipitation and food supply recorded during
this year, suggesting a trade off between survival and reproduction, similar to other
species of tree squirrels (Gurnell 1987). The positive interaction between survival and body mass seems to support this idea, in particular for adult females, which had lower
survival rates than males. Lower survival rates in female tree squirrels are associated
with the stress of raising a litter (Rusch and Reeder 1978; Halvorson and Engeman 1983;
Conner 2001). Douglas’s and red squirrels populations also have been suggested to be
strongly influenced by food supply, rather than by just territorial behavior independent of
food (Rusch and Reeder 1978; Sullivan and Sullivan 1982).
The Mearns’s squirrel is the heaviest of the three species in the genus Tamiasciurus
(Table D3), with morphological and genetic evidence indicating that the species evolved
from Douglas’s squirrels (Lindsay 1981; Arbogast et al. 2001). However, Mearns’s
squirrels appear to have increased in body mass during the 12,000 years of isolation in
the SSPM Mountains (Yensen and Valdés Alarcón 1999). Mearns’s squirrels averaged
the largest in 6 of 17 cranial characters when compared with the nearest populations of
Douglas’s and red squirrels (Lindsay 1981), suggesting also larger body size.
Nonetheless, despite greater body mass and size, Mearns’s squirrels show smaller mean
litter sizes than other Tamiasciurus , but similar to Sciurus squirrels (Fig. D2: E F). Tree
squirrels show evolutionary interactions with the trees they use for food sources (Smith
1981; Steele 2008). In Tamiasciurus , the stronger jaw musculature of red squirrels
allows greater efficiency than Douglas’s squirrels in biting open hard foods and in
carrying heavy foods (Smith 1981). As a result, Douglas’s squirrels are smaller in size 181
and have weaker jaw muscles (Steele 2008). In contrast, Mearns’s squirrels have adapted
to feed on the large cones of Jeffrey and sugar pines and contrary to Douglas’s squirrels,
are able to carry whole pine cones from one branch to another, suggesting stronger jaw
muscles like those of red squirrels.
In sexually dimorphic species, larger size in males is commonly associated with a
strong intra sexual competition for resources (Schulte Hostedde et al. 2002). Contrary to
other congeners, female Mearns’s squirrels tend to be heavier than males (Table D3).
Although not considered dimorphic (Brown 1984; Gurnell 1987; Ralls 1976), larger or
heavier females also have been documented in Sciurus squirrels (e.g., Best 1995; Best
and Riedel 1995; Nitikman 1985). A possible selective pressure resulting in larger
females would arise if females compete more intensely for some resource, such as food,
than do the males (Ralls 1976). In chipmunks, female biased sexual size dimorphism is
more pronounced in severe environments (Schulte Hostedde et al. 2002). Given the open
and xeric conditions of the SSPM Mountains (Koprowski et al. 2006), and the interyear
variation in precipitation and food supply, heavier females may survive better the stress
of raising a litter in this environment compared to other Tamiasciurus located at higher
latitudes in mesic forests.
Behavioral tactics of Mearns’s squirrels .—Contrary to other Tamiasciurus ,
Mearns’s squirrels rely primarily on tree cavities for nesting; one adult male nested underground, but this behavior apparently is rare (Table D3). Douglas’s and red squirrels prefer natural tree cavities for nesting, but where suitable cavities are lacking, they construct dreys and occasionally underground burrows (Table D3). It still remains 182
unclear why Mearns’s squirrels rely strongly on tree cavities for nesting. Mearns’s
squirrels also nest communally with other conspecifics (Ramos Lara and Koprowski
2012). However, communal nesting behavior has not been reported in Douglas’s
squirrels and only rarely in red squirrels (Table D3), suggesting that this variation in the behavior of Mearns’s squirrels may be important for their persistence in SSPM.
Communal nesting behavior is common in nonterritorial Sciurus squirrels (Koprowski
1996).
Mearns’s squirrels do not construct the middens that are characteristic of the genus
Tamiasciurus (Table D3). Middens provide a cool and moist environment for the cones
which remain closed almost indefinitely, providing an important source of food during
the winter months (Gurnell 1987). In SSPM, however, the open and xeric forests do not
seem to provide suitable conditions for the construction of middens (Koprowski et al.
2006). As a result, Mearns’s squirrels scatterhoard food items as do other Tamiasciurus and Sciurus squirrels (Greer and Koprowski 2009; Harestad 1982; Table D3).
Nonetheless, tree squirrels that only store food in this way, like those in the genus
Sciurus , are unable to defend caches and are nonterritorial (Gurnell 1987).
Because of their restricted distribution and the xeric conditions of their habitat,
Mearns’s squirrels appear to feed on a little varied diet of tree seeds and other food types compared to other congeners (see Smith 1968; Ferron et al. 1986). Despite their limited dietary diversity, Mearns’s squirrels maintain mean litter sizes larger than those of other species of tree squirrels with more diverse diets (Fig. D2: G). Mearns’s squirrels spent most of their time in 2006 feeding on pine and fir seeds and fungi. However, because of 183
the delay in pine cone production, squirrels in 2007 spent more time feeding on conifer branch tips and pollen. Other Tamiasciurus are known to feed on conifer branch tips in winter or early spring when food supply is scarce, but provide less energy than seeds
(Rusch and Reeder 1978; Steele 1998; Verts and Carraway 1998).
Mearns’s squirrels spent most of their time feeding, searching for food, and resting similar to other species of tree squirrels (Ferron et al. 1986; Greer and Koprowski 2009;
Gurnell 1987; Shaw and Flick 2002). Time spent in tree cavities was consistent with reproductive events, fluctuations in precipitation, and food supply. In 2006, when food supply was abundant and reproductive output high, lactating females spent more time in their tree cavities than adult males. In contrast, when food supply was scarce and reproductive output low in 2007, males and females considerably decreased the time spent in their tree cavities and spent more time feeding and searching for food. Male and female red squirrels also spend a large proportion of their time in their nests (Greer and
Koprowski 2009). Because of the open forests in the SSPM Mountains, Mearns’s squirrels spend a lot of time running from tree to tree searching for food or exploring potential new tree cavities. As a result, resting becomes important, especially during the warmest months of the year similar to other species of tree squirrels (Ferron et al. 1986;
Gurnell 1987). Despite having smaller home range sizes, Mearns’s squirrels maintain mean litter sizes larger than those of other species of tree squirrels with larger home ranges (Fig. D2: H). Surprisingly, Mearns’s squirrels seem to spend less time caching food items compared to other Tamiasciurus (Dempsey and Keppie 1993; Shaw and Flick
2002; Greer and Koprowski 2009). 184
Conclusion .—Mearns’s squirrels maintain life history and behavioral tactics similar to other Tamiasciurus located at higher latitudes. However, the species also appears to have adopted unique strategies to persist in the open and xeric forests of SSPM. Without middens to store and protect pines cones, Mearns’s squirrels seem to have adopted tactics similar to tree squirrels in the genus Sciurus such as nonterritorial behavior, scatterhoarding, and communally nesting with other conspecific individuals (Edelman and Koprowski 2007; Gurnell 1987; Koprowski 1996). Northeastern populations of red squirrels build and protect small and scattered caches instead of the midden structures used by other populations throughout most of their range (Hamilton 1939; Layne 1954;
Dempsey and Keppie 1993; Steele 1998), suggesting that larderhoarding was important in the evolution of territoriality in the genus Tamiasciurus . Increased body mass and a strong reliance on tree cavities for nesting also are important variations found in
Mearns’s squirrels compared to other congeners. Similarly, interyear variation in weather and food supply may strongly influence fitness related traits and behavior of the species. The lack of dreys and middens seems to be associated with tactics adopted by
Mearns’s squirrels that are similar to those found in Sciurus squirrels, suggesting
important adaptive implications.
RESUMEN
Análisis comparativos de variación en las historia de vida y comportamiento han proporcionado conocimiento en la adaptación entre taxa. En mamíferos, las ardillas rojas
(Tamiasciurus hudsonicus ) y las ardillas de Douglas ( T. douglasii ) a menudo son usadas como modelos para examinar variación de historia de vida. Por el contrario, el miembro 185
más sureño del género, la ardilla de Mearns ( T. mearnsi ), ha permanecido pobremente
estudiada. Sin embargo, la especie muestra desviaciones importantes de
comportamientos comunes observados en otros congéneres tales como la falta de basurales y nidos de hoja. Utilizando monitoreo por telemetría, examinamos si la
ausencia de estas estructuras puede estar asociada con diferencias observadas en las
tácticas de historia de vida y comportamiento entre las ardillas de Mearns y otros
congéneres. También examinamos si la variación interanual en el clima y la abundancia
de alimento influye fuertemente rasgos relacionados con la adecuación y el
comportamiento de la especie. En general, la reproducción y sobrevivencia de las
ardillas de Mearns son similares a otros congéneres. Sin embargo, a pesar de ocupar un
hábitat más cálido y seco, el tamaño promedio de la camada de las ardillas de Mearns es
similar a otras ardillas arborícolas localizadas en bosques fríos y mesófilos en latitudes
más altas. La sobrevivencia de las ardillas adultas estuvo influenciada por el sexo y la
masa corporal. Las ardillas de Mearns son más pesadas y aparentemente también más
grandes que otros congéneres, posiblemente en parte como una adaptación a alimentarse
de conos de pino ( Pinus ) grandes. La variación interanual en el clima y la abundancia de
alimento influenciaron fuertemente rasgos relacionados con la adecuación y el
comportamiento de las ardillas de Mearns. La falta de basurales y nidos de hoja parece
estar asociada con las tácticas adoptadas por las ardillas de Mearns que son similares a las
encontradas en las ardillas Sciurus tales como esparcir alimento, comportamiento de
anidación comunal y pérdida de territorialidad, sugiriendo importantes implicaciones
adaptativas. 186
ACKNOWLEDGMENTS
We thank the Desert Southwest Cooperative Ecosystem Studies Unit, the
Intermountain Region International Conservation Office of the National Park Service, the
Arizona Agricultural Experiment Station, and T&E, Inc. for funding. The Consejo
Nacional de Ciencia y Tecnología and the Wallace Research Foundation provided financial support to N. Ramos Lara. L. Norris, D. Swann, and N. Kline of the National
Park Service and W. Zúñiga, Á. López, and M. Valles of the Sierra de San Pedro Mártir
National Park supported the concept of the project. J. Franco, P. Strittmatter, B. Powell,
J. Sasian, J. Bohigas, D. Hiriart, D. Carrasco, A. García, I. González, and E. Valdés facilitated housing logistics at Observatorio Astronómico Nacional. The Servicio
Meteorológico Nacional provided temperature and precipitation data of the region. W.
Shaw, R. W. Mannan, B. Pasch, M. Merrick, N. Tautfest, C. Schvarcz, C. Zugmeyer, and
G. Palmer assisted with fieldwork. L. Bojórquez, S. Stephens, R. Minnich, J. Vargas, C.
Porras, E. Meling, E. Mellink, E. Salgado, B. Mackintosh, and G. Mackintosh graciously shared their knowledge of the Sierra de San Pedro Mártir. J. Bronstein, R. W. Mannan, and W. Shaw provided valuable comments that improved the manuscript.
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TABLE D1.—Behaviors of adult Mearns’s squirrels ( Tamiasciurus mearnsi ) recorded during radio telemetric observations in the Sierra de San Pedro Mártir, Baja
California, Mexico, from May 2006 November 2007.
Behaviors Description
Foraging
Feeding eating any food item (e.g., seeds, fungi, pollen, twigs, bones)
Searching searching for food in trees
Caching placing food items in branches of trees
Idle
In tree cavity squirrel known to be in tree cavity during the day
Resting resting, sleeping, or basking in tree
Vigilant sitting in tree alert of humans or any other animals
Grooming licking fur in tree
Movement
Running moving through the forest floor, including from tree to tree
Breeding mating chases with one or several squirrels, copulations
Chasing chasing away other animals or squirrels from the area
Defense escaping or hiding from potential predators
Nest searching for tree cavities, working on tree cavities, carrying
maintenance materials for nest bedding
200
TABLE D2.—Results of the multivariate Cox proportional hazards model to explore relationship between survival of adult male and female Mearns’s squirrels ( Tamiasciurus mearnsi ) with predictor variables, in the Sierra de San Pedro Mártir,
Baja California, Mexico, using radio telemetry from May 2006 November 2007. Significance (P < 0.05) is marked with an asterisk.
Variables Coefficient SE χ2 df P Odds ratio
Body mass (g) 0.029 0.024 1.527 1 0.217 0.971
NCU a 0.286 0.255 1.261 1 0.261 0.751
MND b 0.004 0.006 0.394 1 0.530 0.984
Sex 38.107 18.774 4.120 1 0.042* 0.0001
Sex x body mass (g) 0.140 0.065 4.597 1 0.032* 1.151
Sex x NCU a 0.184 0.590 0.097 1 0.755 1.202
Sex x MND b 0.062 0.034 3.260 1 0.071 0.940
a Number of cavity nests used by an individual squirrel
b Maximum number of days a cavity nest was used by an individual squirrel
201
TABLE D3.―Comparison of life history and behavioral traits among Mearns’s squirrels ( Tamiasciurus mearnsi ),
Douglas’s squirrels ( T. douglasii ), and red squirrels ( T. hudsonicus ).
Characteristics Mearns’s squirrels Douglas’s squirrels Red squirrels
Reproduction
Scrotal males April August 23, 33† March August 1, 9 January December 2, 17, 21, 22
Lactating females May September 33 May September 1 March October 2, 12, 16, 17, 21, 22
Litter sizes 2 5 young/litter 33 4 8 young/litter 3, 11 1 8 young/litter2, 4, 27
Reproductive events 1 2 per year 33 1 2 per year 3 1 2 per year 5
Age at sexual maturity 10 12 months 33 10 12 months 3 10 12 months 6, 16
Adult sex ratio (♂:♀) 1.25:1 33 1.08:1 to 1.33:1 5
Survival
Adults ♂: 15 22% higher 33 ♀: 15 20% higher 1 ♂: 8% higher 7; ♀: higher 5§, 18§
Juveniles ♂: 50%; ♀: 50% 33 ♀: 17 71% higher 1 ♂ and ♀ similar 7§, 15§
Body mass
Adults 220 360 g 33 161 203 g 8, 10, 11 126 282.2 g 2, 5, 11, 17 202
At sexual maturity ≥240 g 33 ≥150 g 1, 8 ≥180 g 12, 19, 20, 28
Dimorphism ♀: up to 60 g heavier 33 ♂: heavier 3§ ♂: larger 5§ ; ♂: 4 30 g heavier 2, 15, 28
Nesting behavior
Type of nests Tree cavities, 23, 31 Dreys, tree cavities, Dreys, tree cavities,
underground holes 33‡ underground holes 14, 29 underground holes 2, 5, 17, 29, 30
Communal nesting Yes 31, 33 No 3, 14 Yes 32‡
Feeding behavior
Larderhoarding No 23, 31, 33 Yes 3, 11, 26 Yes 5, 11, 24, 25
Scatterhoarding Yes 31, 33 Yes 29 Yes 2, 24, 25, 29
Data sources: 1Sullivan and Sullivan 1982, 2Layne 1954, 3Steele 1999, 4Kemp and Keith 1970, 5Steele 1998, 6Flyger and
Gates 1982, 7Rusch and Reeder 1978, 8Ransome and Sullivan 2004, 9Koford 1982, 10 Carey 1995, 11 Smith 1981, 12 Dolbeer
1973, 13 Larsen et al. 1997, 14 Verts and Carraway 1998, 15 Boutin and Larsen 1993, 16 Lair 1985, 17 Hamilton 1939,
18 Halvorson and Engeman 1983, 19 Wheatley et al. 2002, 20 Sullivan 1990, 21 Millar 1970, 22 Koprowski 2005, 23 Koprowski et
al. 2006, 24 Hurly and Lourie 1997, 25 Greer and Koprowski 2009, 26 Shaw and Flick 2002, 27 McDam et al. 2007, 28 Klenner
and Krebs 1991, 29 Harestad 1982, 30 Edelman et al. 2009, 31 Ramos Lara and Koprowski 2012, 32 Munroe et al. 2009,
33 Herein. 203
† No observations conducted during December March.
‡ This behavior is rare.
§ No exact data provided by the authors.
204
FIGURE LEGENDS
FIG . D1.―Mean monthly temperature (A) and precipitation (B) recorded by
Servicio Meteorológico Nacional during 2005 2007 at ejido San Matías, located ca. 25 km north of the Sierra de San Pedro Mártir, Baja California, Mexico. Dark bars show reproductive events recorded for radio collared female Mearns’s squirrels ( Tamiasciurus mearnsi ).
FIG D2.―Latitude (A), precipitation (B), temperature (C), body mass (D), length of
head and body (E), number of plant species eaten (F), percentage of year frost free (G),
and female home range size (H) versus litter size illustrating life history trends in
Tamiasciurus and Sciurus squirrels. Acronyms and data sources: Sab (S. aberti —
Edelman and Koprowski 2006; Hayssen 2008; Heaney 1984), Sal (S. alleni —Hayssen
2008; Heaney 1984), Sar (S. arizonensis —Cudworth and Koprowski 2010; Hayssen
2008; Heaney 1984; Pasch and Koprowski 2005), Sau (S. aureogaster —Hayssen 2008;
Heaney 1984), Sca (S. carolinensis —Hayssen 2008; Heaney 1984), Sco (S. colliaei —
Hayssen 2008; Heaney 1984), Sde (S. deppei —Hayssen 2008; Heaney 1984), Sgn (S. granatensis —Hayssen 2008; Heaney 1984), Sgr (S. griseus —Hayssen 2008; Heaney
1984; Linders et al. 2004), Sna (S. nayaritensis —Hayssen 2008; Heaney 1984; Pasch and
Koprowski 2005; Pasch and Koprowski 2006), Sni (S. niger —Hayssen 2008; Heaney
1984), Sri (S. richmondi —Hayssen 2008; Heaney 1984), Svu (S. vulgaris —Hayssen
2008; Lurz et al. 2000), Syu (S. yucatanensis —Hayssen 2008; Heaney 1984), Thu 205
(Tamiasciurus hudsonicus —Hayssen 2008; Heaney 1984; Humphries and Boutin 2000;
Leonard and Koprowski 2009; Zugmeyer and Koprowski 2009), Tdo (T. douglasii —
Hayssen 2008; Heaney 1984; Smith 1981; Steele 1999), Tme (T. mearnsi —Heaney 1984;
Herein).
FIG . D3.―Survival curves for adult male ( n = 20) and female ( n = 18) Mearns’s squirrels ( Tamiasciurus mearnsi ) in the Sierra de San Pedro Mártir, Baja California,
Mexico, using radio telemetry from May 2006 November 2007.
FIG . D4.—Mean (± SD ) body mass of adult male ( n = 20) and female ( n = 18)
Mearns’s squirrels ( Tamiasciurus mearnsi ) captured in the Sierra de San Pedro Mártir,
Baja California, Mexico, from May 2006 November 2007.
FIG . D5.―Percentage (± SD ) of time spent by adult Mearns’s squirrels
(Tamiasciurus mearnsi ) feeding on different types of food in the Sierra de San Pedro
Mártir, Baja California, Mexico from May November 2006 (A) and 2007 (B). Dotted lines indicate the three categories used in the analysis: tree seeds (TS), tree parts (TP), and other food types (O).
206
FIG . D6.—Percentage (± SD ) of time spent by adult Mearns’s squirrels
(Tamiasciurus mearnsi ) in different behaviors in the Sierra de San Pedro Mártir, Baja
California, Mexico during 2006 (A) and 2007 (B). Dotted lines indicate the three categories used in the analysis: foraging (F), idle (I), and movement (M). FIG . D1 207
A)
B)
208 F IG . D2
A)
B)
209 FIG . D2 Continued
C)
D)
210 F IG . D2 Continued
E)
F)
211 F IG . D2 Continued
G)
H)
212 FIG . D3
213 FIG . D4
FIG . D5 214
A)
B)
215 F IG . D6
A)
B)
216
APPENDIX E
DISTRIBUTION OF ACTUAL AND RANDOM HOME RANGES OF ADULT MALE
AND FEMALE MEARNS’S SQUIRRELS ( TAMIASCIURUS MEARNSI ) IN THE
NORTHERN PART OF THE SIERRA DE SAN PEDRO MÁRTIR
217
Brown 1984
La Corona
Vallecitos
La Tasajera
218
APPENDIX F
DETECTED PRESENCE OF MEARNS’S SQUIRRELS ( TAMIASCIURUS MEARNSI )
DURING THE STUDY IN DIFFERENT AREAS OF THE SIERRA DE
SAN PEDRO MÁRTIR
219
Arroyo San Rafael
Punta San Pedro
La Corona
Vallecitos Brown 1984
La Tasajera
La Zanja La Encantada La Grulla