Journal of Mammalogy, 97(2):405–423, 2016
DOI:10.1093/jmammal/gyv185
Published online February 26, 2016
Systematic revision of the pocket gopher genus Orthogeomys
Theresa A. Spradling,* James W. Demastes, David J. Hafner, Paige L. Milbach, Fernando A. Cervantes,
and Mark S. Hafner
Department of Biology, University of Northern Iowa, Cedar Falls, IA 50614-0421, USA (TAS, JWD, PLM)
Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131, USA (DJH)
Colección Nacional de Mamíferos, Instituto de Biología, Universidad Nacional Autónoma de México, A.p. 70–153, 04510 México
Distrito Federal, México (FAC)
Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
(MSH)
* Correspondent: [email protected]
Pocket gophers of the genus Orthogeomys show unusually high morphological and ecological diversity compared
to other genera in the family Geomyidae. Whereas this diverse group once was divided into 3 genera (Merriam
1895), a revision by Russell (1968) recognized only Orthogeomys, with Merriam’s original genera relegated to
subgeneric status as Heterogeomys, Macrogeomys, and Orthogeomys. Recent studies have called into question
the monophyly of Orthogeomys, as well as the validity of 4 currently recognized Orthogeomys species. To date,
the taxonomic validity of only 1 of these species has been verified (Hafner et al. 2014). In this analysis, the first
to include all 11 recognized species of the genus, we examine 3 mitochondrial and 2 nuclear gene sequences
(4,352 base pairs) and analyze cranial morphology to explore relationships within the genus. Our data support
a taxonomic revision that restricts the genus Orthogeomys to a single species (O. grandis) and combines the
subgenera Heterogeomys and Macrogeomys into the resurrected genus, Heterogeomys (7 species). In addition,
3 currently recognized species of Orthogeomys are synonymized as follows: O. cuniculus with O. grandis;
H. thaeleri with H. dariensis; and H. matagalpae with H. cherriei. A synonymy and a key to the species of the
genera Orthogeomys and Heterogeomys are provided.
Las tuzas del género Orthogeomys muestran una diversidad morfológica y ecológica inusual en comparación con
otros géneros de la familia Geomyidae. Aunque este diverso grupo fue alguna vez dividido en 3 géneros (Merriam
1895), la revisión de Russell (1968) reconoció solo a Orthogeomys, mientras que los géneros originales de Merriam
fueron relegados a estatus subgenérico como Heterogeomys, Macrogeomys y Orthogeomys. Estudios recientes
han cuestionado la monofilia de Orthogeomys, así como la validez de 4 de las especies actualmente reconocidas.
A la fecha, la validez taxonómica de sólo una de estas especies ha sido verificada. En este análisis, el primero en
incluir las 11 especies reconocidas en el género, examinamos secuencias de 3 genes mitocondriales y 2 nucleares
y analizamos la morfología craneal para explorar las relaciones dentro del género. Nuestras 4,352 pares de bases
de secuencias de ADN apoyan una revisión taxonómica que retiene al género Orthogeomys (incluyendo sólo a
O. grandis) y combina los subgéneros Heterogeomys y Macrogeomys en un género recuperado, Heterogeomys
(7 especies). Además, 3 especies de Orthogeomys actualmente reconocidas son sinonimizadas de la siguiente
forma: O. cuniculus con O. grandis; H. thaeleri con H. dariensis; y H. matagalpae con H. cherriei. Se incluye
sinonimia y una clave para las especies de los géneros Orthogeomys y Heterogeomys.
Key words: Heterogeomys, Macrogeomys, mitochondrial DNA, morphology, nuclear DNA, taxonomic revision
© 2016 American Society of Mammalogists, www.mammalogy.org
The pocket gopher genus Orthogeomys (Rodentia: Geomyidae)
is notable for its morphological and ecological diversity. Size
variation is impressive, with up to a 6-fold difference in mass
among species, ranging from 150 to 950 g even within a single subgenus (Macrogeomys—Hafner 1991). In 1 Oaxacan
subspecies of O. grandis (O. g. carbo), populations living in
forests at 3,000 m elevation are large (approximately 850 g
adult body mass) and have long, dense pelage; in contrast,
populations of the same subspecies living in arid lowlands
along the Pacific coast (Morro Mazatán) are smaller as adults
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JOURNAL OF MAMMALOGY
(approximately 550 g) and have extremely sparse hair. Whereas
nearly all pocket gopher species are unicolored dorsally and
show a high degree of background (soil color) matching, 4
Orthogeomys species have conspicuous white patches in the
form of a full or partial lumbar belt (nearly fixed in O. underwoodi of the subgenus Macrogeomys and occasionally present
in O. hispidus of the subgenus Heterogeomys) or in the form
of a triangular head spot (fixed in O. cherriei and O. matagalpae of the subgenus Macrogeomys—Hafner and Hafner 1987;
Hafner 1991). Species of Orthogeomys can be found in humid
lowlands, arid lowlands, agricultural fields, rainforests, and
montane forests, at elevations ranging from sea level to 3,000
m (Nowak 1999).
In 1895, C. Hart Merriam published the 1st comprehensive
systematic study of pocket gophers exclusive of Thomomys.
Although his sample sizes were low (e.g., only 5 specimens
of Macrogeomys), Merriam (1895) recognized multiple genera of pocket gophers, including Orthogeomys of southwestern
Mexico (including the currently recognized species O. grandis
and O. cuniculus), Heterogeomys of northeastern Mexico south
to Honduras (currently including O. hispidus and O. lanius), and
Macrogeomys of Honduras, Nicaragua, Costa Rica, Panama,
and Colombia (currently including O. cavator, O. cherriei,
O. dariensis, O. heterodus, O. matagalpae, O. thaeleri, and
O. underwoodi; Fig. 1). Although Merriam (1895:24) made
few direct statements about interrelationships among genera
of pocket gophers, his conceptual tree depicted Orthogeomys,
Heterogeomys, and Macrogeomys as stemming from a common
ancestor not shared by other pocket gopher genera.
Much of the variation in body size, pelage coloration, and
ecological diversity in the genus Orthogeomys lies within
the subgenus Macrogeomys (Hafner 1991), yet cranial characters described by Russell (1968) show species of the subgenus Orthogeomys, particularly O. grandis, to be the most
distinct morphologically among the 3 subgenera. O. grandis
shows notable differences from all other Orthogeomys species
in width of the frontal bone, absence of an interorbital constriction, absence of an enamel plate on the posterior wall of
P4, and more medial placement of the anterior groove of the
upper incisor (Russell 1968). Despite his awareness of these
cranial differences, Russell (1968) nevertheless relegated
Merriam’s (1895) 3 genera (Orthogeomys, Heterogeomys, and
Macrogeomys) to subgeneric status within the single genus,
Orthogeomys. Russell’s assertion that “Merriam’s genera
Orthogeomys, Heterogeomys, and Macrogeomys are closely
related” (Russell 1968:510) was supported primarily on the
basis of shared dolichocephaly (elongated skulls) and adaptations to tropical environments (Russell 1968:569).
There have been several subsequent studies of relationships
among Orthogeomys species (e.g., Hafner 1982, 1991; Sudman
and Hafner 1992; Spradling et al. 2004), but these studies were
hampered by incomplete sampling of taxa. Adding to the taxonomic uncertainty surrounding this group of pocket gophers,
recent authors have used nuclear and mitochondrial sequence
data to suggest that the genus Orthogeomys, as it is currently
defined, is not monophyletic (Spradling et al. 2004). In addition,
the taxonomic validity of 4 species of Orthogeomys (O. cuniculus, O. lanius, O. matagalpae, and O. thaeleri), all originally
described on the basis of body size or pelage coloration, has
been questioned (Hall 1981; Hafner 1991, 2015; Sudman and
Hafner 1992; Villa-Cornejo and Espinoza-Medinilla 2014).
Both body size and pelage coloration are known to vary extensively within species of pocket gophers, thus providing little
evidence of phylogeny on their own (Patton and Brylski 1987;
Wilkins and Swearingen 1990; Krupa and Geluso 2000; Rios
and Álvarez-Castañeda 2007; Hafner et al. 2008, 2009).
Orthogeomys cuniculus (subgenus Orthogeomys) was originally described from 2 specimens (only 1 adult) that showed
Fig. 1.—Map of Central America with portions of Mexico and South America. Collecting localities (Appendix I) are shown with symbols and
numbers that correspond with the phylogenetic tree (Fig. 2) and localities of Appendix I. Map courtesy of NASA/JPL-Caltech.
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS407
subtle morphological differences from the few specimens of
Orthogeomys known at that time (Elliot 1905). Recently, the
taxonomic validity of O. cuniculus was questioned (VillaCornejo and Espinoza-Medinilla 2014) because the morphology of the 2 known specimens appears to fit well within the
range of morphological variation now known to exist in the
widespread sister species, O. grandis.
Orthogeomys matagalpae (subgenus Macrogeomys) was
described based on its smaller size, narrower rostrum, and
darker coloration as compared to O. cherriei (Allen 1910).
Both share a striking white head spot (Hafner and Hafner
1987) that is unique among geomyids. Hafner (1991) suggested
O. matagalpae may be conspecific with O. cherriei and called
for genetic analysis once tissue samples became available.
Orthogeomys thaeleri (subgenus Macrogeomys) was
described based on subtle external differences from its presumed sister species, O. dariensis (Alberico 1990), but Sudman
and Hafner (1992) questioned the validity of O. thaeleri because
of the low level of mitochondrial DNA sequence differentiation
(0.3%) measured between O. thaeleri and O. dariensis. This
level of divergence was considered comparable to that of many
conspecific populations of pocket gophers (Hafner 2015).
The taxonomic status of a 4th species of Orthogeomys,
O. lanius (subgenus Heterogeomys), was only recently validated following the fortuitous rediscovery of this species in the
mountains of Veracruz, Mexico (Hafner et al. 2014). O. lanius
was described from 2 adult specimens that were larger, darker,
and woollier than individuals of the presumed sister species,
O. hispidus (Elliot 1905). Hall (1981:512) suggested that
O. lanius might instead represent only a subspecies of O. hispidus, but Hafner et al. (2014) reported on molecular, morphological, and chromosomal analyses of the 2 new specimens of
O. lanius and confirmed its species status within the subgenus
Heterogeomys.
In this study, we examine 3 mitochondrial and 2 nuclear
gene sequences and analyze cranial morphology to resolve
these lingering questions regarding monophyly of the genus
Orthogeomys and validity of O. cuniculus, O. matagalpae, and
O. thaeleri. Our taxonomic sampling of the genus is by far the
most complete to date, representing all 11 currently named species in the genus (Patton 2005), with most species being represented by multiple individuals from multiple localities.
Methods
Thirty pocket gophers representing the 11 named species
of the genus Orthogeomys and 5 specimens representing the
other 5 genera of pocket gophers were included in the DNA
analyses (Appendix I). New specimens were collected under
authority of Mexican Scientific Collecting Permit number
FAUT-0002 issued to F. A. Cervantes using trapping methods
approved by the American Society of Mammalogists (Sikes
et al. 2011). These specimens are housed at the Colección
Nacional de Mamíferos, Instituto de Biología, Universidad
Nacional Autótoma de México (CNMA) or the Louisiana State
University Museum of Natural Science (LSUMZ). Tissues
from other specimens were provided by the Carnegie Museum
of Natural History and the Field Museum of Natural History.
Polymerase chain reaction (PCR) amplification for all gene
regions was performed using Promega Hot Start Master Mix
(Promega, Madison, Wisconsin). Two nuclear gene targets
were amplified and sequenced. Amplification of intron 7 of
the nuclear β-fibrinogen (Bfib) gene for some specimens was
performed using primers FIB-B17L and B3R as described in
Spradling et al. 2004. Most reactions were performed using
primers FIB-B17L and R2 (primers in Spradling et al. 2004).
Thermal cycles for these reactions were as follows: 95°C for
2 min, followed by 30–40 cycles of 95°C for 45 s, 50°C or 60°C
for 45 s, 72°C for 45 s, ending with a final extension at 72°C for
10 min. A portion of exon 1 of the interphotoreceptor retinoidbinding protein (IRBP) gene was amplified using primers 119A
and 1297D from Jansa and Voss (2000). Thermal cycles for
IRBP reactions were as follows: 95°C for 2 min, then 30–40
cycles of 95°C for 45 s, 52°C or 60°C for 45 s, 72°C for 45 s,
ending with a final extension at 72°C for 10 min.
Three mitochondrial gene targets were amplified and
sequenced. PCR amplification of the cytochrome c oxidase
subunit I (COI) gene was accomplished with a combination of
primers and reaction conditions reported in Spradling et al. 2004.
The cytochrome-b (Cytb) gene was amplified using a combination of primers and reaction conditions of Spradling et al. 2001.
DNA extracted from the museum skin of the O. cuniculus paratype was amplified before we collected our fresh specimen of
O. cuniculus, thus precluding potential laboratory contamination. Double-stranded PCR amplifications were performed on
DNA extracted from the O. cuniculus paratype using primers
L14724 with H14926 and L14945 with H15154 following the
reaction conditions specified by Demastes et al. (2003). Finally,
a 488 base pair (bp) fragment of the mitochondrial NADH
dehydrogenase 2 (ND2) gene was amplified for all specimens
using the primers H6305 and L5758 (adapted from Sorenson
et al. 1999) using 35 temperature cycles of 94°C for 1 min,
58°C for 1 min, and 72°C for 1 min.
PCR products were prepared for sequencing using Exosap-IT
(USB, Cleveland, Ohio), and sequencing reactions were performed using each of their respective amplification primers at the Iowa State University DNA Facility on an Applied
Biosystems 3730xl DNA Analyzer. DNA sequences were
edited and aligned using Geneious 6.0.3 (Kearse et al. 2012).
Heterozygous sites in nuclear sequences were evaluated by eye
and treated as ambiguous character states. All DNA sequences
used in this study are deposited in GenBank (Benson et al.
2013; accession numbers in Appendix I).
Phylogenetic analyses.—Past molecular analyses of members of the Geomyidae using heteromyid rodent outgroups
indicate monophyly of the geomyid tribe Geomyini relative
to members of the geomyid tribe Thomomyini (Hafner 1982;
Spradling et al. 2004). Thus, all phylogenetic analyses performed here were rooted using a thomomyine species, T. bulbivorus, as the outgroup taxon.
Partition Finder (Lanfear et al. 2012) was used to test for
concordance among the 5 genes analyzed. Models of molecular
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substitution for downstream analyses of each of the data partitions designated by Partition Finder were estimated using
jModelTest (Posada 2008) and chosen using the Bayesian
Information Criterion (BIC). Partitioned analyses of concatenated data were performed using a maximum likelihood
framework (Garli 2.0—Zwickl 2006) and using Bayesian inference (MrBayes 3.2—Ronquist et al. 2012) run on the CIPRES
Science Gateway (Miller et al. 2010). Models and substitution
parameters from jModelTest results were applied to each partition of the concatenated data. Likelihood analysis included 600
bootstrap pseudo-replicates. Default settings for priors were
implemented in MrBayes using random starting trees and 4
Markov chains (temperature 0.2) sampled every 2,000 generations for each of 2 independent analyses of 40 × 106 generations
with a 10% burn-in on each. Tracer (version 1.6.0—Rambaut
et al. 2014) was used to evaluate stationarity of the Markov
chain and to assure that effective sample size (ESS) values were
well above 300. TREE Annotator (version 2.13—Drummond
et al. 2012) was used to summarize information from the sample of trees after a 10% burn-in was removed.
To confirm that phylogenetic signal was evident in both mitochondrial sequences and nuclear sequences, Bayesian analysis
was performed for each type of genomic data independently.
Data were not partitioned by gene within these analyses, and
the substitution model indicated by jModelTest (Posada 2008)
was applied to each data set. Bayesian analysis was performed
using MrBayes via the CIPRES Science Gateway (Miller et al.
2010) as described above for 2 runs each with 20 × 106 generations for each data set, and results were evaluated as above.
An uncalibrated, ultrametric species tree was built using
Bayesian inference of the multilocus data (Heled and
Drummond 2010) via the *BEAST method (BEAST version
1.8—Drummond et al. 2012) run on the CIPRES Science
Gateway (Miller et al. 2010). Individuals were assigned to species according to current taxonomy. The 3 mitochondrial genes
were constrained to a single, linked tree, and the 2 nuclear
genes were treated each as separate loci, resulting in a total of
3 independent trees being estimated in the analysis. A relaxed,
log-normal clock was used for each of the 3 trees. The analysis was run for 300 × 106 generations sampled every 30,000
generations. Tracer (version 1.6.0—Rambaut et al. 2014) was
used to assess stationarity and to ensure satisfactory mixing of
the Markov chains as determined by values greater than 300
for the likelihood ESS, posterior ESS, and prior ESS. TREE
Annotator (version 2.13—Drummond et al. 2012) was used to
summarize information from the sample of trees after a 10%
burn-in was removed. Trees and molecular data sets are available at TreeBase (Sanderson et al. 1994) and Dryad (Spradling
et al. 2015).
Morphometric analyses.—Twelve cranial characters (following Hafner et al. 2005) were measured on 550 specimens
of Orthogeomys (181 males, 341 females, and 28 unrecorded
sex) representing all recognized species and 41 specimens of
Zygogeomys trichopus (20 males, 20 females, and 1 unrecorded
sex; Appendix I). Characters were measured to the nearest
0.05 mm using handheld digital calipers: occipital–nasal length
(ONL), occipital–incisor length (OIL), nasal length (NL), rostral width (RW), width of interorbital constriction (IOC), zygomatic breadth (ZB), cranial width (CW), mastoid breadth (MB),
diastema length (DIA), length of maxillary toothrow (MTR),
occlusal length of upper molars 1 and 2 (LM12), and occlusal length of upper molar 3 (LM3). Specimens were judged to
be adult based on fusion of the exoccipital–supraoccipital and
basioccipital–basisphenoid sutures (Daly and Patton 1986).
Mensural data for the same 12 cranial characters for 294 specimens of Cratogeomys (all adult females) were included for
genus-level comparison (specimens listed in Hafner et al. 2004,
2008). Only adult female specimens (361 Orthogeomys, 20
Zygogeomys, and 294 Cratogeomys) were used in the parametric analyses because of the extreme secondary sexual dimorphism in pocket gophers and a female-biased sex ratio (Daly
and Patton 1986; Patton and Brylski 1987; Smith and Patton
1988; Patton and Smith 1990; Hafner et al. 2004). For example, all cranial variables for O. hispidus (n = 217) except IOC,
MB, and dental characters (MTR, LM12, and LM3) showed
significant secondary sexual dimorphism (P < 0.05) based on
unpaired t-tests, and the sex ratio for our sample of O. hispidus
was 2:1 (female:male).
Statistical analyses of the morphometric data were conducted
using SYSTAT 7.0 (SPSS, Inc. 1998). Data were assessed for
normality and examined for extreme outliers, which were
removed from further analyses. Data were transformed ( X = 0,
SD = 1) and a multivariate analysis of variance (MANOVA)
was used to test the null hypothesis of no significant difference
between a priori groups. A post hoc analysis of the MANOVA
was assessed with Tukey’s honestly significant difference
(HSD) test. Principal component analyses (PCAs) were performed to reduce the 12 variables and explore the dimensionality of the data. Discriminant function analyses (DFAs) were
performed to predict group membership and evaluate if individuals could be correctly assigned to their a priori groups.
Significant factors in both analyses were determined by eigenvalues (≥ 1.0) and Cattell’s Scree Test (Cattell 1966), which in
1 analysis allowed a factor with eigenvalue < 1.0.
Results
Phylogenetic analyses.—Trimmed, aligned sequences for
the 5 genes yielded a total sequence length of 4,352 bp for 35
pocket gophers, with the 3 mitochondrial genes, Cytb, COI,
and ND2 contributing 1,140, 1,460, and 488 bp, respectively,
and the 2 nuclear genes, Bfib and IRBP, contributing 429 and
835 bp, respectively. Partition Finder indicated 3 partitions for
the data: Cytb + COI (partition 1), ND2 (partition 2), and Bfib
+ IRBP (partition 3). Molecular substitution models suggested
by jModelTest were GTR + I + G for partitions 1 and 2 and
K80 + I for partition 3. These models were used in partitioned
analyses of concatenated data using both maximum likelihood
and Bayesian inference.
Maximum likelihood tree structure (Fig. 2) supported monophyly of each of the 3 subgenera recognized by Russell (1968)
with 100% bootstrap support for each subgenus. However,
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS409
Fig. 2.—Maximum likelihood tree based on concatenated data, with best models applied to each of 3 data partitions (bootstrap support values
shown below branches). The tree based on Bayesian inference (MrBayes) showed identical branch structure (posterior probabilities are the
top numbers above branches). The species-tree analysis (*BEAST; see Supporting Information S1) showed the same branch structure except
for placement of Orthogeomys underwoodi (posterior probabilities are shown directly above branches as a middle number where appropriate).
Numbers following species names correspond with localities of Figure 1 and Appendix I. Symbols following numbers refer to the map (Fig. 1).
this analysis provided no support for monophyly of the genus
Orthogeomys, placing the subgenus Orthogeomys in a virtual
trichotomy with a clade consisting of all other Orthogeomys
species (the subgenera Macrogeomys and Heterogeomys) and
a clade containing C. planiceps and Pappogeomys bulleri. The
maximum likelihood analysis showed a possible sister relationship between the subgenus Orthogeomys and the Cratogeomys–
Pappogeomys clade, but bootstrap support for this relationship
was less than 50%. Bayesian analysis of concatenated data indicated the same set of relationships with a similar pattern of support (posterior probabilities in Fig. 2). Again the possible sister
relationship between the subgenus Orthogeomys and members
of the genera Pappogeomys and Cratogeomys was weakly supported (posterior probability [PP] < 0.50). Bayesian analysis
of the nuclear data alone was entirely concordant with these
relationships but yielded slightly higher support (PP = 0.76) for
the relationship between the subgenus Orthogeomys and the
Cratogeomys–Pappogeomys clade. Bayesian analysis of the
mtDNA data alone also was concordant with the larger analysis, but again, O. grandis was placed in a trichotomy (PP <
0.50) with a clade consisting of all other Orthogeomys species
and a clade containing C. planiceps and P. bulleri.
Species-tree analysis.—Simpler models of base substitution were used in the *BEAST analysis so that stationarity in the Markov chain could be reached within 300 million
generations. The HKY + I + G model was used for ND2, the
HKY model for Bfib and IRBP, and the GTR + I + G model
for COI and Cytb. The species tree generated in the *BEAST
analysis was entirely concordant with the maximum likelihood
and Bayesian trees built from partitioned, concatenated data,
with the exception of placement of O. underwoodi. Whereas
all phylogenetic analyses (Fig. 2) place O. underwoodi well
within the subgenus Macrogeomys with high support, the species tree placed O. underwoodi just outside a group containing
all other Macrogeomys species (see Supporting Information
S1). Support for this larger clade (O. underwoodi plus all other
Macrogeomys species) was strong in the species-tree analysis
(PP = 1.0), but support for monophyly of the Macrogeomys
species exclusive of O. underwoodi was weak (PP = 0.45),
indicating uncertainty in relationships among all Macrogeomys
species, including O. underwoodi. Similar uncertainty as to
placement of O. underwoodi within Macrogeomys was evident
in the phylogenetic analyses (PP = 0.69; Fig. 2).
Relationships of subgenera.—The subgenera Macrogeomys
and Heterogeomys formed reciprocally monophyletic sister lineages in the maximum likelihood, Bayesian, and species-tree
analyses (Fig. 2 and see Supporting Information S1). The relative genetic divergence between these 2 lineages, as estimated
from branch lengths of trees based on 3 mitochondrial and 2
nuclear genes, was lower than divergence observed between
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other geomyine genera. Uncorrected sequence divergence measured between these 2 subgenera averaged 10.7% for Cytb. This
value was lower than the divergence values measured between
each of these subgenera and the subgenus Orthogeomys, which
averaged 17.5% and 17.2%, respectively, and it was lower
than divergence values measured between these subgenera
and the other geomyine genera, Cratogeomys, Pappogeomys,
Zygogeomys, and Geomys, which ranged from 15.1% to 19.2%.
Relationships of problematic species.—A 355-bp fragment
of the Cytb gene from the skin of the paratype of O. cuniculus (FMNH 14051) collected in Zanatepec, Oaxaca, Mexico,
in 1904 was identical in nucleotide sequence to the Cytb gene
sequenced from a fresh specimen of Orthogeomys (LSUMZ
36765; Fig. 2) collected in 2010 from 2 km north of Zanatepec.
From this evidence, we conclude that LSUMZ 36765 represents the taxon originally described as O. cuniculus by Elliot
in 1905. Phylogenetic analyses of the full sequence data set
(4,352 bp) for LSUMZ 36765 place this specimen (and by
inference, O. cuniculus) well within the O. grandis clade with
strong branch support (PP = 1.0; Fig. 2). Uncorrected Cytb
sequence divergence within the clade represented by O. grandis and O. cuniculus specimens ranged from 1.2% to 7.5%
(average 4.9%), with O. cuniculus differing from 3 O. grandis
individuals by as little as 3.8%.
Specimens of O. matagalpae and O. cherriei collected from
disparate localities in Costa Rica, Honduras, and Nicaragua
(Appendix I) are genetically very similar (maximum Cytb
uncorrected p distance 1.2%) and the 2 species do not form
reciprocally monophyletic lineages (Fig. 2). Similarly, specimens of O. thaeleri from Colombia and O. dariensis from
Panama cluster together with high branch support (PP = 1.0)
and have almost identical Cytb sequences (uncorrected p distance 0.4%; Fig. 2).
Morphometric analyses.—One variable (OIL) was removed
from analyses so that we could include our single specimen of
O. matagalpae (UNAH 942) that was missing this character but
was otherwise intact. A PCA of transformed data for individuals
of Orthogeomys resulted in 2 principal components (PCs) with
eigenvalues ≥ 1.0. The 1st PC accounted for 72.0% of the variation in the data set, and all characters were strongly and positively loaded on this factor, indicating a strong overall influence
of size (Table 1). A scatterplot of PC 1 versus PC 2 (Figs. 3A
and 3B) indicated overlap of species among and between
Macrogeomys and Heterogeomys and separation of the subgenus Orthogeomys. The single specimen of O. cuniculus plotted near the 75% confidence ellipse of O. grandis, the single
specimen of O. thaeleri plotted within the confidence ellipse of
O. dariensis, and the single specimen of O. matagalpae plotted within the ellipse of O. cherriei. A one-way MANOVA
performed on the untransformed morphometric data for the
11 species of Orthogeomys indicated significant variation
among species (Wilks’ λ = 0.0057, F110,2056 = 17.464; Pillai’s
Trace = 2.79, F110,2820 = 9.94; Hotelling’s Trace = 12.819,
Table 1.—Component loadings for 11 morphometric variables,
eigenvalues, and proportion of variance explained for principal components (PCs) of principal component analyses employed to investigate morphological variation among the 11 species of Orthogeomys
(Fig. 3A) and the 3 subgenera of Orthogeomys (Fig. 3B).
Variables
PC 1
PC 2
Occipital–nasal length (ONL)
Nasal length (NL)
Rostral width (RW)
Width of interorbital constriction (IOC)
Zygomatic breadth (ZB)
Cranial width (CW)
Mastoid breadth (MB)
Diastema length (DIA)
Length of maxillary toothrow (MTR)
Occlusal length of upper molars 1 and 2 (LM12)
Occlusal length of upper molar 3 (LM3)
Eigenvalue
Proportion of variance explained
0.974
0.920
0.891
0.557
0.911
0.760
0.923
0.902
0.917
0.827
0.649
7.919
0.720
0.064
0.049
0.139
0.782
−0.133
−0.336
0.088
−0.097
0.054
0.094
−0.632
1.197
0.109
Fig. 3.—Distribution of principal component (PC) scores for 293 specimens of the 11 species of Orthogeomys on the first 2 PCs (PC 1 and PC 2) of a principal component analysis based on 11 cranial measurements; P = 0.75 confidence ellipses are shown for species with n > 10. Specimens
of Orthogeomys cuniculus (diamond), O. lanius (circles), O. matagalpae (square), and O. thaeleri (star) are shown in larger symbols. A) Species
confidence ellipses: dark-shaded ellipse and circles = subgenus Heterogeomys; light-shaded ellipse and diamond = subgenus Orthogeomys; open
ellipse, square, and star = subgenus Macrogeomys. B) Subgenus confidence ellipses, species with sample sizes < 10 are indicated as in A).
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS411
F110,2712 = 31.61; P < 0.0001 for all 3 tests) and between subgenera (Wilks’ λ = 0.057, F22,562 = 81.34; Pillai’s Trace = 1.39,
F22,564 = 58.35; Hotelling’s Trace = 8.69, F22,560 = 110.57; P <
0.0001 for all 3 tests).
A DFA of transformed data for the 293 specimens representing the 11 species of Orthogeomys generated 3 canonical
discriminant functions (DFs) with eigenvalues ≥ 1.0 together
explaining 92.7% of the total variance (Table 2). IOC, ONL,
and MB had strong positive loadings and ZB and CW had strong
negative loadings on DF 1; CW had a strong positive loading
and DIA had a strong negative loading on DF 2. Examination
of a scatterplot of DF 1 versus DF 2 (Fig. 4A) was similar to
the PCA (Fig. 3A), with overlap among and between species
of Macrogeomys and Heterogeomys and separation of the subgenus Orthogeomys (O. grandis and O. cuniculus). The single
specimen of O. cuniculus, when entered as “unknown” (i.e.,
unassigned as to species), is assigned a posteriori to O. grandis with a Mahalanobis PP = 1.00. Overall, 92% of individuals
were classified correctly into their a priori species: 100% of
individuals of species with small sample sizes (O. matagalpae,
O. thaeleri, and O. cuniculus, n = 1; and O. lanius, n = 3) were
classified correctly. Of the remaining species, all individuals
of O. dariensis (n = 11) were classified correctly, while 96%
of O. grandis (n = 80) and O. heterodus (n = 23), 93% of
O. underwoodi (n = 14), 90% of O. hispidus (n = 119), 86%
of O. cavator (n = 28), and 85% of O. cherriei (n = 13) were
classified correctly.
A DFA of transformed data for the 3 subgenera of
Orthogeomys generated 2 DFs with eigenvalues ≥ 1.0
together explaining 100% of the total variance (Table 2).
IOC and ONL had strong positive loadings and ZB and CW
had strong negative loadings on DF 1; ONL, ZB, and CW
had strong positive loadings and DIA, RW, and MTR had
strong negative loadings on DF 2. Examination of a scatterplot of DF 1 versus DF 2 showed clear separation of the subgenus Orthogeomys from Heterogeomys and Macrogeomys,
with some overlap between the latter 2 subgenera (Fig. 4B).
Overall, 93% of the individuals were classified correctly into
their a priori groups; 99% of individuals of Orthogeomys,
91% of Macrogeomys, and 91% of Heterogeomys were classified correctly.
A PCA of transformed data for the 7 species of the subgenus
Macrogeomys generated a single PC with eigenvalue = 9.179
explaining 83.5% of the total variance (see Supporting
Information S2). All characters were highly and positively
loaded on PC 1, indicating a strong overall influence of size.
Three size groups were arrayed along PC 1 (Tukey’s HSD,
P < 0.02): small (O. cherriei, O. matagalpae, and O. underwoodi), medium (O. heterodus, O. dariensis, and O. thaeleri),
and large (O. cavator) species. A PCA of transformed data
for the “small-sized” species generated 2 PCs with eigenvalues ≥ 1.0, explaining a combined 76.1% of the total variance
(see Supporting Information S3). A scatterplot of PC 1 versus PC 2 indicated extensive overlap between the 75% confidence ellipses of O. cherriei and O. underwoodi; the single
specimen of O. matagalpae was within the ellipse of O. cherriei but outside of the ellipse for O. underwoodi. A DFA of
transformed data for O. cherriei and O. underwoodi indicated
clear separation with 100% correct assignment between the 2
species (Wilks’ λ = 0.1611, F11,1,25 = 7.10; P = 0.0004). The
single specimen of O. matagalpae, entered as “unknown,” was
assigned to O. cherriei with a Mahalanobis PP = 1.00. A PCA
of transformed data for the “medium-sized” species generated
3 PCs with eigenvalues ≥ 1.0, explaining a combined 77.8% of
the total variance (see Supporting Information S4). A scatterplot of PC 1 versus PC 2 clearly indicated no overlap between
O. heterodus and O. dariensis (75% confidence ellipses), with
the single specimen of O. thaeleri equidistant between them.
A DFA of transformed data for O. heterodus and O. dariensis indicated clear separation with 100% correct assignment
between the 2 species (Wilks’ λ = 0.0973, F11,1,32 = 18.5529;
P < 0.0001). The single specimen of O. thaeleri, entered as
“unknown,” was assigned to O. dariensis with a Mahalanobis
PP = 0.98.
Table 2.—Component loading for 11 morphometric variables, eigenvalues, proportion of variance explained, and canonical correlations for discriminant functions of discriminant function analyses employed to investigate morphological variation A) among the 11 species of Orthogeomys
(Fig. 4A), B) among the 3 subgenera of Orthogeomys (Fig. 4B), and C) among selected genera of the subfamily Geomyinae (Fig. 5).
Variables
Occipital–nasal length (ONL)
Nasal length (NL)
Rostral width (RW)
Width of interorbital constriction (IOC)
Zygomatic breadth (ZB)
Cranial width (CW)
Mastoid breadth (MB)
Diastema length (DIA)
Length of maxillary toothrow (MTR)
Occlusal length of upper molars 1 and 2 (LM12)
Occlusal length of upper molar 3 (LM3)
Eigenvalue
Proportion of variance explained
Canonical correlation
A
B
C
DF 1
DF 2
DF 3
DF 1
DF 2
DF 1
DF 2
DF 3
0.998
−0.157
−0.154
1.017
−0.722
−0.662
0.480
−0.218
0.034
0.193
−0.462
8.794
0.686
0.948
0.281
0.362
0.253
0.095
0.003
1.241
0.338
−1.516
−0.490
−0.088
−0.041
1.777
0.139
0.800
0.138
0.451
−0.813
0.250
1.251
−0.162
−0.286
−0.847
−0.397
−0.173
−0.256
1.316
0.102
0.754
0.961
−0.014
−0.201
1.165
−0.876
−0.788
0.562
−0.297
0.006
0.277
−0.539
7.668
0.883
0.941
1.181
0.338
−0.887
0.247
1.039
0.872
−0.082
−1.805
−0.829
−0.187
−0.183
1.020
0.117
0.711
2.430
−0.248
−0.556
1.082
−0.502
−0.464
−0.818
−0.936
0.226
0.333
−0.125
13.803
0.791
0.966
1.985
−0.042
−0.595
−0.684
0.559
1.412
−2.935
−0.663
0.182
0.206
0.704
2.742
0.157
0.856
0.460
1.431
−1.431
0.090
1.043
1.014
−0.038
−1.523
−0.603
−0.066
−0.627
0.606
0.035
0.614
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JOURNAL OF MAMMALOGY
Fig. 4.—A) Distribution of discriminant function (DF) scores for 293 specimens of the 11 species of Orthogeomys on the first 2 DFs (DF 1 and
DF 2) of a discriminant function analysis (DFA) based on 11 cranial measurements; P = 0.75 confidence ellipses are shown for species with
n > 10. Specimens of O. cuniculus (diamond), O. lanius (circles), O. matagalpae (square), and O. thaeleri (star) are shown in larger symbols;
dark-shaded confidence ellipse and circles = subgenus Heterogeomys; light-shaded ellipse and diamond = subgenus Orthogeomys; open ellipse,
square, and star = subgenus Macrogeomys. B) Distribution of DF scores for 293 specimens of the 3 subgenera of Orthogeomys on the first 2
DFs (DF 1 and DF 2) of a DFA based on 11 cranial measurements (P = 0.75 confidence ellipses are shown). Species with sample sizes < 10 are
indicated as in (A).
Fig. 5.—Distribution of discriminant function (DF) scores for 605 specimens representing the geomyine genera Orthogeomys, Cratogeomys,
and Zygogeomys on A) DF 1 versus DF 2 and B) DF 3 versus DF 2 of a discriminant function analysis (DFA) based on 11 cranial measurements
(P = 0.75 confidence ellipses are shown). Sample sizes: 293 specimens representing the 3 subgenera of Orthogeomys (Orthogeomys, n = 80;
Heterogeomys, n = 122; and Macrogeomys, n = 91), 294 specimens representing 4 species of Cratogeomys (C. castanops, n = 105; C. fumosus,
n = 59; C. goldmani, n = 125; and C. planiceps, n = 5), and 18 specimens representing Zygogeomys (Z. trichopus).
A PCA of transformed data for 605 specimens representing
the 3 subgenera of Orthogeomys, the genus Zygogeomys, and
representative species of the genus Cratogeomys (C. castanops,
C. goldmani, C. fumosus, and C. planiceps) generated only a
single PC with eigenvalue ≥ 1.0, was strongly influenced by
size, and resulted in extensive overlap among the groups (plot
not shown). A DFA of transformed data for the same groups
generated 2 DFs with eigenvalues ≥ 1.0, explaining a combined
94.8% of the total variance (Table 2). A 3rd DF with eigenvalue = 0.6 explained an additional 3.5% of the total variance.
Although this DF had an eigenvalue < 1.0, it is included based
on Cattell’s Scree Test (Cattell 1966). ONL and IOC had strong
positive loadings and DIA and MB had strong negative loadings
on DF 1; ONL and CW had strong positive loadings and MB
had strong negative loadings on DF 2; NL had a strong positive
loading and DIA and RW had strong negative loadings on DF
3. A scatterplot of DF 1 versus DF 2 (Fig. 5A) showed clear separation of Cratogeomys and Orthogeomys, with overlap between
Zygogeomys and Macrogeomys and between Macrogeomys and
Heterogeomys. A scatterplot of DF 3 versus DF 2 (Fig. 5B)
separated Zygogeomys from Macrogeomys, leaving overlap
between Macrogeomys and Heterogeomys. Overall, 97% of the
individuals were classified correctly into their a priori groups;
100% of individuals of Cratogeomys and Zygogeomys, 99% of
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS413
individuals of Orthogeomys, 91% of Macrogeomys, and 90% of
Heterogeomys were classified correctly.
Discussion
Of the 4 taxa of Orthogeomys whose species status has been
challenged (O. lanius, O. cuniculus, O. matagalpae, and
O. thaeleri), only O. lanius has been investigated previously
using molecular, chromosomal, and morphological evidence
and shown to be specifically distinct from, yet closely related
to, O. hispidus of the subgenus Heterogeomys (Hafner et al.
2014). Data from the present analysis, with nearly twice as
much sequence data and greater geographic sampling, corroborate that conclusion given both the monophyly of O. hispidus
relative to O. lanius and the relatively large genetic divergence
between these species collected at nearby localities as compared
to smaller genetic divergence among geographically much
more widespread samples of O. hispidus (Fig. 1). This pattern
is suggested both by branch lengths of phylogenetic trees based
on multiple genes (Fig. 2 and see Supporting Information S1)
and by uncorrected sequence divergence values for Cytb, which
range from 6.9 to 8.3% between O. lanius and O. hispidus, but
average only 1.9% among all O. hispidus sampled. Moreover,
data from the present analysis help clarify the taxonomic status
of the remaining 3 problematic taxa, O. cuniculus, O. matagalpae, and O. thaeleri.
Orthogeomys cuniculus (the Oaxacan pocket gopher) is
known only from its type locality in Oaxaca, Mexico. Levels of
sequence divergence between specimens of O. cuniculus and
O. grandis are low (as little as 3.8% uncorrected p distance for
Cytb), which is similar to levels of divergence measured between
conspecific individuals of C. fulvescens (3.9%—Hafner et al.
2005), and within-species Cytb divergence among all O. grandis
and O. cuniculus examined here (1.2–7.5%) was comparable to
divergence among specimens of P. bulleri (3.5–7.8%—Hafner
et al. 2009). Therefore, we conclude that the degree of genetic
divergence observed between O. cuniculus and O. grandis is
not uncommon for conspecific populations of pocket gophers.
Given that O. cuniculus is nested phylogenetically within specimens of O. grandis (Fig. 2), fits within the range of morphological variation observed in O. grandis (Figs. 3A and 3B), and
was assigned to O. grandis with a Mahalanobis PP = 1.0 in the
DFA, we hereby synonymize O. cuniculus under O. grandis and
recognize it as a population of O. g. scalops, within which it is
also nested geographically. Orthogeomys cuniculus is listed as
“threatened” by the Mexican government (Semarnat 2010) but
“data deficient” by the IUCN (IUCN 2012). In January 2010,
we found abundant pocket gopher activity in the vicinity of the
type locality of O. cuniculus (Zanatepec, Oaxaca; MSH and
DJH, pers. obs.). Therefore, this population of O. g. scalops
formerly recognized as O. cuniculus is neither threatened nor
endangered and should be delisted.
Phylogenetic analyses (Fig. 2) strongly support the conclusion that O. matagalpae and O. cherriei are not reciprocally
monophyletic lineages that warrant recognition at the species
level. Levels of sequence divergence between individuals of the
2 taxa are low (1.2% uncorrected p distances for Cytb) and both
show similar external morphologies and share the white head
spot found in no other geomyid species (Hafner and Hafner
1987). O. matagalpae was originally described as distinct from
O. cherriei on the basis of what we now know to be phylogenetically dubious characters (body size, width of rostrum, and
pelage coloration—Allen 1910), and although we were able to
include only 1 specimen of O. matagalpae in our morphometric analysis, that specimen fell clearly within the 75% confidence ellipse for O. cherriei in the PCAs, and was assigned
to O. cherriei with a Mahalanobis PP = 1.0 in the DFA. In
addition, O. cherriei and O. matagalpae host the same species
of chewing louse (Geomydoecus cherriei—Price et al. 1985),
which is rare for different species of pocket gophers (Hafner
et al. 2003) and supports our argument for conspecificity of
O. cherriei and O. matagalpae. The combined evidence leads
us to synonymize O. matagalpae (Allen 1910) under O. cherriei (Allen 1893), and recognize it as a geographically isolated
subspecies, O. c. matagalpae.
We found no sequence differences between O. dariensis
and O. thaeleri in the 1,264 bp of nuclear sequence data examined in this study. Previous studies using even shorter (434–
1,049 bp) nuclear sequences reported sequence variation within
individual species of pocket gophers (e.g., Hafner et al. 2005,
2008, 2009), indicating that O. thaeleri and O. dariensis are
particularly closely related. Likewise, differences between the
2 taxa in mitochondrial DNA sequences were exceptionally
small (0.4% uncorrected p distance for Cytb) and consistent
with the findings of Sudman and Hafner (1992; 0.3% divergent
based on 929 bp of mitochondrial DNA sequences). A recent
examination of museum specimens by Hafner (2015) showed
that cranial characters previously thought to be diagnostic
for O. thaeleri (Alberico 1990) failed when a larger sample
of O. dariensis specimens were included in the analysis. Our
single specimen of O. thaeleri fell clearly within the 75% confidence ellipse for O. dariensis in the PCAs and was assigned
to O. dariensis with a Mahalanobis PP = 0.98 in the DFA of
medium-sized species. The combined evidence leads us to
synonymize O. thaeleri (Alberico 1990) under O. dariensis
(Goldman 1912), and recognize it as a geographically isolated
subspecies, O. dariensis thaeleri.
Analyses of the genetic data provide strong support for
monophyly of each of the 3 currently recognized subgenera
of Orthogeomys (all PP = 1.0) and strong support for a sister relationship between the subgenera Heterogeomys and
Macrogeomys (PP = 1.0). These relationships also are reflected
in the morphological analyses, which show clear separation of
Orthogeomys from the other 2 subgenera and considerable morphological overlap between Heterogeomys and Macrogeomys
(Figs. 3B, 4B, and 5).
Analyses of the genetic data show no support for monophyly of
the genus Orthogeomys as it is currently defined (comprising the
subgenera Orthogeomys, Heterogeomys, and Macrogeomys—
Russell 1968). Instead, the subgenus Orthogeomys forms
a virtual trichotomy with the Cratogeomys–Pappogeomys
and the Heterogeomys–Macrogeomys lineages (Fig. 2).
414
JOURNAL OF MAMMALOGY
Spradling et al. (2004), who included a greater representation of
taxa outside the genus Orthogeomys, reported similar findings,
showing a polytomy of 4 lineages including a Cratogeomys lineage, Pappogeomys lineage, O. grandis (subgenus Orthogeomys)
lineage, and a lineage containing the subgenera Macrogeomys
and Heterogeomys. As suggested by Spradling et al. (2004), the
phylogenetic uncertainty at the base of this large clade may result
from a rapid radiation that left few molecular clues as to the actual
branching sequence within the lineage. Regardless of the cause
of the polytomy, both this study and that of Spradling et al. (2004)
find no genetic support for Russell’s (1968) grouping of the genera Orthogeomys, Macrogeomys, and Heterogeomys (Merriam
1895) into a single genus, Orthogeomys. If anything, members
of the subgenus Orthogeomys show a weak sister relationship
to the Cratogeomys–Pappogeomys clade (albeit bootstrap support < 50%) rather than the Macrogeomys–Heterogeomys clade.
Morphologically, members of the subgenus Orthogeomys
(O. grandis) are at least as divergent from species of the subgenera Macrogeomys and Heterogeomys as are members of the
genera Zygogeomys and Cratogeomys (Fig. 5).
Genetic and morphological evidences presented here and
by Spradling et al. (2004) support division of the current
genus Orthogeomys into 2 genera, one containing the former
subgenus Orthogeomys (now restricted to O. grandis) and
the other containing the sister subgenera Heterogeomys and
Macrogeomys (the name Heterogeomys has page priority—
Merriam 1895:179). Because genetic divergence between the
subgenera Heterogeomys and Macrogeomys is not as great as
divergence between other geomyine genera (Fig. 2 and see
Supporting Information S1) and because Heterogeomys and
Macrogeomys show considerable overlap in all analyses of cranial dimensions (Figs. 3B, 4B, and 5), there is no compelling
justification for recognizing these reciprocally monophyletic
sister lineages as separate genera.
Nomenclatural statement.—A life science identifier (LSID)
number was obtained for this publication: [urn:lsid:zoobank.
org:pub:B4FB990A-6FAE-4BF1-8147-B1D706DCB645].
Synonymy of the genera Orthogeomys and
Heterogeomys
Genus Orthogeomys Merriam, 1895
Orthogeomys Merriam, 1895:172. Type species Geomys scalops Thomas, 1894, by original designation.
Before this study, the genus Orthogeomys included 11 species
divided among 3 subgenera, Orthogeomys, Heterogeomys, and
Macrogeomys (Russell 1968). This study restricts the genus
Orthogeomys to include a single species, O. grandis, with
O. cuniculus as a junior synonym.
Orthogeomys grandis (Thomas, 1893)
Giant Pocket Gopher
Geomys grandis Thomas, 1893:270. Type locality “Dueñas,
Guatemala.” Type specimen adult skin and skull, British
Museum number 65.5.18.65, collected in 1865 by O. Salvin.
Geomys scalops Thomas, 1894:437. Type locality “Tehuantepec,
Mexico.”
Orthogeomys grandis: Merriam, 1895:175. 1st use of current
name combination.
Orthogeomys nelsoni Merriam, 1895:176. Type locality “Mt.
Zempoaltepec, Oaxaca, Mexico. Altitude 8,000 feet.”
Orthogeomys latifrons Merriam, 1895:178. Type locality
“Guatemala” (exact locality unknown, but probably lowlands
of southern Guatemala).
Orthogeomys cuniculus Elliot, 1905:234. Type locality
“Yautepec [corrected by Elliot (1907) to “Zanatepec”], Oaxaca,
Mexico.” Considered indistinguishable from O. g. scalops (this
study).
Orthogeomys pygacanthus Dickey, 1928:9. Type locality “Cacaguatique, 3500 ft. Department of San Miguel, El
Salvador.”
Included subspecies.—Sixteen subspecies are currently recognized. All of these subspecies were named primarily on
the basis of body size or pelage coloration, features that have
been shown repeatedly to be of dubious taxonomic value in the
Geomyidae (Patton and Brylski 1987; Wilkins and Swearingen
1990; Krupa and Geluso 2000; Rios and Álvarez-Castañeda
2007; Hafner et al. 2008, 2009). Assessment of the taxonomic
validity of the subspecies of O. grandis was not within the
scope of this study, but it is likely that a rigorous analysis of
their validity using modern tools for systematic investigation
would reduce the number of subspecies considerably.
O. g. alleni Nelson and Goldman, 1930:156. Type locality
“near Acapulco, Guerrero, Mexico (altitude 2,000 feet).”
O. g. alvarezi Schaldach, 1966:292. Type locality “from ridge
above Lachao (pass above Kilometer 183), on road from
Oaxaca City to Puerto Escondido, approximately 40 kms.
N. San Gabriel Mixtepec, Municipio de Juquila, Oaxaca,
Mexico, altitude approximately 1700 m.”
O. g. annexus Nelson and Goldman, 1933:157. Type locality
“Cerro San Felipe, 10 miles north of Oaxaca, Oaxaca, Mexico
(altitude 10,000 feet).”
O. g. carbo Goodwin, 1956:5. Type locality “Escurano, 2500 ft.,
Cerro de San Pedro, 20 km W Mixtequilla, Oaxaca [Mexico].”
O. g. engelhardi Felten, 1957:151. Type locality: “Finca
El Carmen (1319 m), Volcán de San Vicente, [San Vicente
Department] El Salvador.”
O. g. felipensis Nelson and Goldman, 1930:157. Type locality
“Cerro San Felipe, 10 miles north of Oaxaca, Oaxaca, Mexico
(altitude 10,000 feet).”
O. g. grandis (Thomas, 1893:270); see above.
O. g. guerrerensis Nelson and Goldman, 1930:158. Type locality “El Limon, in the valley of the Rio de las Balsas about 20
miles northwest of La Union, Guerrero [Mexico].”
O. g. huixtlae Villa, 1944:319. Type locality “Finca Lubeca, 12
km NE Huixtla, 850 m, Chiapas [Mexico].”
O. g. latifrons Merriam, 1895:178; see above.
O. g. nelsoni Merriam, 1895:176; see above.
O. g. pluto Lawrence, 1933:66. Type locality “Cerro Cantoral,
north of Tegucigalpa, Honduras.”
O. g. pygacanthus Dickey, 1928:9; see above.
O. g. scalops (Thomas, 1894: 437); see above.
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS415
O. g. soconuscensis Villa, 1949:267. Type locality “Finca
Esperanza, 710 m, 45 km (by road) NW Huixtla, Chiapas
[Mexico].”
O. g. vulcani Nelson and Goldman, 1931:105. Type locality “Volcan Santa Maria, Quezaltenango, Guatemala (altitude
9,000 feet).”
Geographic range.—Patchily distributed along the Pacific coast
of Mexico from Colima City, Colima and Jilotlán de Dolores,
Jalisco, southward into Guatemala, El Salvador, and southwestern Honduras. The range of O. grandis also extends eastward
from the Pacific coast of Guerrero, Mexico, into southwestern
Puebla, then southeasterly to the mountains east of Oaxaca City
(Hall 1981). Elevational range from near sea level to at least
2,700 m.
Description.—Some individuals of O. grandis are among
the largest of geomyids (> 800 g body mass), whereas others, particularly individuals living in dry, lowland habitats,
are smaller (< 600 g). Specimens from higher elevations (>
1,000 m) have dense, woolly fur that is dark brown to almost
black in color. At lower elevations, the fur is extremely
sparse over the entire body, often giving the appearance of
nakedness. In all specimens, the tail is naked and the feet
nearly so.
Genus Heterogeomys Merriam, 1895
Heterogeomys Merriam, 1895:179. Type species G[eomys]. hispidus Le Conte, 1852, by original designation. Heterogeomys
was regarded as a subgenus of Orthogeomys by Russell (1968)
and Patton (2005), but is returned to full generic status in
this study.
Macrogeomys Merriam, 1895:185. Type species Geomys heterodus Peters, 1865, by original designation. Macrogeomys
was regarded as a subgenus of Orthogeomys by Russell (1968)
and Patton (2005), but is treated as a subgenus of the newly
resurrected genus Heterogeomys in this study.
Before this study, the subgenera Heterogeomys and
Macrogeomys contained 2 and 7 species, respectively. In this
study, we revise the genus Heterogeomys to include 7 of the
former 9 species. H. (formerly O.) matagalpae is synonymized under H. cherriei, and H. (formerly O.) thaeleri under
H. dariensis.
Subgenus Heterogeomys Merriam, 1895
Heterogeomys Merriam, 1895:179. Type species G[eomys].
hispidus Le Conte, 1852, by original designation. See key
to distinguish between the subgenera Heterogeomys and
Macrogeomys. Two species are currently recognized in the subgenus Heterogeomys.
Heterogeomys hispidus (Le Conte, 1852)
Hispid Pocket Gopher
G[eomys]. hispidus Le Conte, 1852:158. Type locality
“between Vera Cruz and the City of Mexico (restricted to near
Jalapa, Veracruz, Mexico by Merriam [1895]).” Type specimen
body mount, skull in skin, Academy of Natural Sciences of
Philadelphia number 133, collected in 1847 by W. H. Pease.
Orthogeomys hispidus: Merriam, 1895:181. 1st use of current
name combination.
Heterogeomys hondurensis Davis, 1966:175. Type locality “8
miles west of Tela, Province of Atlántida, Honduras, elevation
10 feet.”
Included subspecies.—Twelve subspecies are currently recognized. For the same reasons discussed in the O. grandis
synonymy, the taxonomic validity of these subspecies is in
need of rigorous analysis using modern tools for systematic
investigation.
H. h. cayoensis Burt, 1937:1. Type locality “Mountain Pine
Ridge, 12 mi. S El Cayo, British Honduras [Belize].”
H. h. chiapensis Nelson and Goldman, 1929:151. Type locality “Tenejapa, 16 miles northeast of San Cristobal, Chiapas,
Mexico.”
H. h. concavus Nelson and Goldman, 1929:148. Type locality
“Pinal de Amoles, Querétaro, Mexico.”
H. h. hispidus (Le Conte, 1852:158); see above.
H. h. hondurensis Davis, 1966:175; see above
H. h. isthmicus Nelson and Goldman, 1929:149. Type locality
“Jaltipan, Veracruz, Mexico.”
H. h. latirostris Hall and Álvarez, 1961:121. Type locality
“Hacienda Tamiahua, Cabo Rojo, Veracruz [Mexico].”
H. h. negatus Goodwin, 1953:1. Type locality “Gómez Feras [=
Farías], 1300 feet, about 45 miles south of Ciudad Victoria and
10 miles west of the Pan American Highway, on the west side
of a foothill of the Sierra Madre de Occidental, Tamaulipas,
Mexico.”
H. h. teapensis Goldman, 1939:176. Type locality “Teapa,
Tabasco, Mexico.”
H. h. tehuantepecus Goldman, 1939:174. Type locality “mountains 12 miles northwest of Santo Domingo and about 60 miles
north of Tehuantepec City, Oaxaca, Mexico (altitude 1,600
feet).”
H. h. torridus Merriam, 1895:183. Type locality “Chichicaxtle,
Veracruz [Mexico].”
H. h. yucatanensis Nelson and Goldman, 1929:150. Type locality Campeche, Campeche, Mexico.”
Geographic range.—Patchily distributed along the Gulf of
Mexico from southern Tamaulipas, Mexico southward through
the Yucatan Peninsula, Belize, Guatemala, and northwestern
Honduras. Generally found at lower elevations (< 1,000 m),
but occurs at higher elevations in the mountains of eastern
Querétaro and central Chiapas, Mexico. Elevational range from
near sea level to 2,500 m.
Description.—H. hispidus is a moderately large pocket
gopher (adult body mass 400–650 g), but is usually smaller
than O. grandis. Most specimens have coarse, short, and
extremely sparse pelage, but they never approach the appearance of nakedness seen in lowland populations of O. grandis. At higher elevations, the fur is somewhat denser, but it
is still coarse and short and never approaches the woolly fur
of H. lanius and O. grandis specimens collected at higher
elevations. The tail of H. hispidus is naked and the feet only
sparsely furred.
416
JOURNAL OF MAMMALOGY
Heterogeomys lanius Elliot, 1905
Heterogeomys cherriei (J. A. Allen, 1893)
Big Pocket Gopher
Heterogeomys lanius Elliot, 1905:235. Type locality “Xuchil,
Veracruz, Mexico” (restricted to El Xuchitl [18.886° N, 97.238°
W] in west-central Veracruz by Hafner et al. [2014]). Type
specimen adult male skin and skull, Field Museum of Natural
History number 14062, collected in June 1904 by E. Heller.
Included subspecies.—This species is monotypic.
Geographic range.—Known from only 2 localities in the
mountains southeast of Pico de Orizaba in Veracruz, Mexico
(Hafner et al. 2014). Elevational range 2,442–3,010 m.
Description.—H. lanius is a large pocket gopher (adults
approaching 900 g) that is easily distinguished from its sister species, H. hispidus, by presence of dense, woolly pelage
that is almost black in color. The tail is blackish in color and
almost naked.
Cherrie’s Pocket Gopher
Geomys cherriei J. A. Allen, 1893:337. Type locality “Santa
Clara, Costa Rica.” Type specimen adult skin and skull, National
Museum of Costa Rica number 664, collected October 1892 by
G. K. Cherrie.
Macrogeomys costaricensis Merriam, 1895:192. Type locality
“Pacuare, Costa Rica.”
Macrogeomys matagalpae J. A. Allen, 1910:97. Type locality
“Pena [Peña] Blanca, Matagalpa, Nicaragua.”
Heterogeomys cherriei: (this study). 1st use of current name
combination.
Included subspecies.—Four subspecies are currently recognized. For the same reasons discussed in the O. grandis
synonymy, the taxonomic validity of these subspecies is in
need of rigorous analysis using modern tools for systematic
investigation.
H. c. carlosensis (Goodwin, 1934:3). Type locality “Cataratas,
San Carlos, Province Alajuela, Costa Rica, about 400 feet
elevation.”
H. c. cherriei (J. A. Allen, 1893:337); see above.
H. c. costaricensis (Merriam, 1895:192); see above.
H. c. matagalpae (J. A. Allen, 1910:97); see above.
Geographic range.—Central Honduras through the lowlands
(< 1,000 m) of Nicaragua and northern Costa Rica, extending
southward to the Río Grande de Tárcoles on the Pacific coast
and almost to Panama along the Gulf coast. Elevational range
near sea level to approximately 1,000 m.
Description.—H. cherriei is a smaller member of the genus
(adults usually < 400 g) that is easily distinguished from all
other species of pocket gopher by presence of a conspicuous, white spot on the forehead, occupying most of the area
bounded by the eyes and ears. Otherwise, the fur dorsally
is dark brown to black and much lighter, almost white,
ventrally.
Subgenus Macrogeomys Merriam, 1895
Macrogeomys Merriam, 1895:185. Type species Geomys heterodus Peters, 1865, by original designation. See key to distinguish between the subgenera Macrogeomys and Heterogeomys.
Five species are currently recognized in the subgenus
Macrogeomys.
Heterogeomys cavator (Bangs, 1902)
Chiriquí Pocket Gopher
Macrogeomys cavator Bangs, 1902:42. Type locality “Boquete
[Chiriqui Province, Panama] 4,000 to 7,000 feet.” Type specimen
adult male, skin and skull, Museum of Comparative Zoology
number 10381, collected 9 March 1901 by W. W. Brown.
Macrogeomys pansa Bangs, 1902:44. Type locality “Bogaba
[Bugaba], Chiriqui Province, Panama.”
Heterogeomys cavator: (this study). 1st use of current name
combination.
Included subspecies.—Three subspecies are currently recognized. For the same reasons discussed in the O. grandis
synonymy, the taxonomic validity of these subspecies is in
need of rigorous analysis using modern tools for systematic
investigation.
H. c. cavator (Bangs, 1902:42); see above.
H. c. nigrescens (Goodwin, 1934:3). Type locality “El Muñeco
(Rio Navarro), 10 miles south of Cartago, Province Cartago,
Costa Rica, altitude 4,000 feet.”
H. c. pansa (Bangs, 1902:44); see above.
Geographic range.—Higher elevations in the Cordillera de
Talamanca of southern Costa Rica and extensions of this range
into western Panama at least as far as Veraguas Province.
Subspecies pansa found at lower elevations from extreme
western Panama (and adjacent Costa Rica) eastward at least to
Bahía Honda. Elevational range near sea level to 3,200 m.
Description.—H. cavator is a large pocket gopher (adult
mass 400–800 g) with dark brown, almost black, pelage that
is slightly grizzled and sparse, especially where the species
occurs at lower elevations.
Heterogeomys dariensis (Goldman, 1912)
Darién Pocket Gopher
Macrogeomys dariensis Goldman, 1912:8. Type locality “Cana
(altitude 2,000 feet) in the mountains of eastern Panama.” Type
specimen adult male skin and skull, United States National
Museum number 179587, collected 31 May 1912 by E. A.
Goldman.
Orthogeomys thaeleri Alberico, 1990:104. Type locality “ca. 7
km S Bahía Solano, Municipio Bahía Solano, Departamento
del Chocó, Colombia, ca. 100 m.”
Heterogeomys dariensis: (this study). 1st use of current name
combination.
Included subspecies.—Two subspecies are currently recognized. For the same reasons discussed in the O. grandis
synonymy, the taxonomic validity of these subspecies is in
need of rigorous analysis using modern tools for systematic
investigation.
H. d. dariensis (Goldman, 1912:8); see above.
H. d. thaeleri (Alberico, 1990:104); see above.
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS417
Geographic range.—Extreme eastern Panama southward into
coastal habitats of Chocó Department, Colombia. Elevational
range near sea level to at least 1,200 m.
Description.—H. dariensis is similar in size to H. cavator
(adult mass 400–800 g). The pelage is short, dull brown or
black, and sparse, especially in lowland individuals.
Heterogeomys heterodus (Peters, 1865)
Variable Pocket Gopher
Geomys heterodus (Peters, 1865:177). Type locality “Costa
Rica” (exact locality unknown). Type specimen adult (sex
unknown), skin and skull, Berlin Museum number 2864.
Macrogeomys dolichocephalus Merriam, 1895:189. Type
locality “San Jose, Costa Rica.”
Heterogeomys heterodus: (this study). 1st use of current name
combination.
Included subspecies.—Three subspecies are currently recognized. For the same reasons discussed in the O. grandis
synonymy, the taxonomic validity of these subspecies is in
need of rigorous analysis using modern tools for systematic
investigation.
H. h. dolichocephalus (Merriam, 1895:189); see above.
H. h. cartagoensis (Goodwin, 1934:2). Type locality “Paso
Ancho, Province Cartago, Costa Rica.”
H. h. heterodus (Peters, 1865:177); see above.
Geographic range.–Central highlands of Costa Rica
(Alajuela, San Jose, and Cartago Provinces). Elevational range
1,000–2,500 m.
Description.—H. heterodus is among the largest species of
pocket gophers (adult mass 500–950 g). The pelage is long,
moderately coarse, and dark brown to almost black. The
large nasal pad is almost naked. The tail is naked and feet are
nearly so.
Heterogeomys underwoodi (Osgood, 1931)
Underwood’s Pocket Gopher
Macrogeomys underwoodi Osgood, 1931:143. Type locality
“Alto de Jabillo Pirris, between San Geronimo and Pozo Azul,
western Costa Rica.” Type specimen adult female skin and
skull, Field Museum of Natural History number 35175, collected 23 April 1931 by C. F. Underwood.
Heterogeomys underwoodi: (this study). 1st use of current
name combination.
Included subspecies.—This species is monotypic.
Geographic range.—Coastal plain and lower foothills of western Costa Rica from just north of the Río Grande de Tárcoles,
southward almost to the border with Panama. Elevational range
near sea level to approximately 500 m.
Description.—H. underwoodi is among the smaller species in
the genus (adult mass 250–350 g) and is easily distinguished
from all other pocket gophers by presence of a conspicuous
white lumbar belt (rarely absent). The belt contrasts sharply
with the dark brown, almost black, dorsal pelage, which is short
and somewhat sparse.
Key to the species of Orthogeomys and
Heterogeomys
In this key, the reliability of a character (e.g., “97% reliable”) refers to the percentage of specimens of known identity
assigned to the correct taxon based on that character alone. For
example, 97% of all O. grandis specimens examined in this
study have an interorbital constriction > 11.9 mm.
1 Interorbital constriction > 11.9 mm (97% reliable) or, if
less, then CW > 28.2 mm; postorbital process inconspicuous to nearly absent; enamel plate on posterior wall of
upper P4 usually absent (Russell, 1968); diploid number
(2n) = 58; fundamental number (FN) = 110; not occurring
south of Honduras Orthogeomys grandis
1′Interorbital constriction < 11.9 mm (97% reliable); or if
greater, CW < 28.2 mm; postorbital process well developed; enamel plate on posterior wall of upper P4 always
present; 2n = 44–54, FN = 78–98; occurring from
northeastern Mexico, to northwestern Colombia genus
Heterogeomys 2
2Tail length (in flesh) < 91 mm (76% reliable); ratio
between width of interorbital constriction and occipitalnasal length > 0.165 (79% reliable); anterior margin of
mesopterygoid fossa even with plane of posterior wall of
M3; postorbital bar weakly developed; occurring from
southern Tamaulipas, Mexico, to northwestern Honduras
(Tela Department); 2n = 44–54, FN = 78–98 subgenus
Heterogeomys 3
2′Tail length (in flesh) > 91 mm (77% reliable); ratio
between width of interorbital constriction and occipitalnasal length < 0.165 (79% reliable); anterior margin of
mesopterygoid fossa decidedly behind plane of posterior
wall of M3; postorbital bar strongly developed; occurring from central Honduras (Olancho Department) to
northwestern Colombia (Chocó Department); 2n = 44,
FN = 78–82 subgenus Macrogeomys 4
3IOC ≥ 13 mm; size large for subgenus; thick, woolly
pelage; dark, almost black dorsal coloration; 2n = 44,
FN = 84; restricted to mountains near Pico de Orizaba in
Veracruz, Mexico above 2,400 m H. lanius
3′IOC < 13 mm; coarse, generally short and sparse pelage;
2n = 52–54, FN = 78–98; broad distribution along Gulf
coast of Mexico from southern Tamaulipas, spreading
throughout most of Chiapas and the Yucatán Peninsula
across Belize and Guatemala and into northwestern
Honduras, rarely above 2,400 m H. hispidus
4 Size small for subgenus (total length generally < 320 mm,
ONL generally < 60 mm) 5
4′Size large (total length generally > 320 mm, ONL generally > 60 mm) 6
5 Total length generally < 300 mm, ONL < 59 mm); pelage
dark brown or black with white dorsal lumbar belt (rarely
lacking); occurring from Pacific coastal lowlands just
north of the Río Grande de Tárcoles, Puntarenas Province,
Costa Rica south to the Costa Rica-Panama border region
H. underwoodi
418
JOURNAL OF MAMMALOGY
5′Total length 250–350 mm, ONL 48–64 mm; pelage dark
brown or black with white, triangular head spot; occurring
in lowlands of central Honduras (Olancho Department),
central Nicaragua, and northern Costa Rica H. cherriei
6 Skull relatively narrow (generally CW < 27 mm, RW <
13.5 mm, MB < 35 mm), pelage sparse; occurring from
southern Darien Province of eastern Panama to Chocó
Department of northwestern Colombia H. dariensis
6′Skull broad (generally CW > 27 mm, RW > 13.5 mm, MB
> 35 mm), pelage dense 7
7 Total length generally > 350 mm, LM12 usually > 4 mm;
restricted to the Cordillera de Talamanca of Costa Rica
and western Panama H. cavator
7′Total length generally < 350 mm, LM12 usually < 4 mm;
restricted to the central highlands of Costa Rica (Alajuela,
San José, and Cartago Provinces) H. heterodus
Acknowledgments
We are grateful to the late T. J. McCarthy (Carnegie Museum)
for providing specimens from Central America critical to this
study. H. B. McPherson (Centenary College) kindly provided
tissue samples from important localities in Costa Rica and
Nicaragua. Our thanks to the late M. S. Alberico (Universidad
del Valle, Colombia) for providing us with tissues and a museum
specimen of O. thaeleri (now H. dariensis) for our study. For
assistance in the laboratory, we thank S. Harper, K. Peiffer,
A. Popinga, F. Silva, and A. Smith of the University of Northern
Iowa (UNI). We are grateful to M. Aquina, L. J. Barkley, J. R.
Demboski, M. Esteva, E. González, J. C. Hafner, J. E. Light,
V. L. Mathis, and P. Vargas for helping us collect specimens
of Orthogeomys and Heterogeomys in the field. Special thanks
to the staff and students of the mammal section at Instituto de
Biología, Universidad Nacional Autónoma de México, especially Y. Hortelano-Moncada, for their kind support of all of our
fieldwork in Mexico. We thank the curators and collection managers at the American Museum of Natural History; Academy of
Natural Sciences of Philadelphia; Carnegie Museum of Natural
History; Field Museum of Natural History; Harvard University
Museum of Comparative Zoology; University of Kansas
Museum of Natural History; University of Michigan Museum
of Zoology; University of California, Berkeley, Museum of
Vertebrate Zoology; Universidad Nacional Autónoma de
Honduras; and the United States National Museum for allowing
us to examine and measure specimens in their care. This research
was funded by the University of Northern Iowa Intercollegiate
Academic Fund and undergraduate research (SOAR) awards.
Supporting Information
The Supporting Information documents are linked to this
manuscript and are available at Journal of Mammalogy online
(jmammal.oxfordjournals.org). The materials consist of data
provided by the author that are published to benefit the reader.
The posted materials are not copyedited. The contents of all
supporting data are the sole responsibility of the authors.
Questions or messages regarding errors should be addressed
to the author.
Supporting
Information
S1.—Species-tree
analysis
(*BEAST) with posterior probabilities.
Supporting Information S2.—Results of a principal component analysis of 91 specimens representing the 7 species of the
subgenus Macrogeomys.
Supporting Information S3.—Results of a principal component analysis and a discriminant function analysis of 28 specimens representing the 3 small-sized species of the subgenus
Macrogeomys (O. cherriei, O. matagalpae, and O. underwoodi).
Supporting Information S4.—Results of a principal component analysis and a discriminant function analysis of 35 specimens representing the 3 medium-sized species of the subgenus
Macrogeomys (O. dariensis, O. heterodus, and O. thaeleri).
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Associate Editor was Sharon A. Jansa.
Appendix I
Specimens Examined
Specimens used in this study are housed in the American
Museum of Natural History (AMNH); the Academy of Natural
Sciences of Philadelphia (ANSP); Carnegie Museum of
Natural History (CM); the Colección Nacional de Mamíferos,
Instituto de Biología, Universidad Nacional Autónoma de
México (CNMA); the Field Museum (FMNH); the University
of Kansas Natural History Museum (KU); the Collection of
Mammals, Louisiana State University Museum of Natural
Science (LSUMZ); the Museum of Comparative Zoology,
Harvard University (MCZ); the Museum of Vertebrate Zoology,
University of California, Berkeley (MVZ); the Museum of
Zoology, University of Michigan (UMMZ); Universidad
Nacional Autónoma de Honduras (UNAH); and the United
States National Museum of Natural History (USNM).
Specimens of Cratogeomys (n = 294) included in the morphological analysis are listed in Hafner et al. (2004, 2008): C. castanops (n = 105), C. fumosus (n = 59), C. goldmani (n = 125),
and C. planiceps (n = 5). Specimens used in the molecular analyses are mapped in Fig. 1, and numbers preceding localities
for the molecular analyses correspond with Fig. 2. GenBank
numbers for β-fibrinogen (Bfib) intron 7, interphotoreceptor
retinoid-binding protein (IRBP) exon 1, cytochrome-b (Cytb),
cytochrome c oxidase subunit I (COI) sequences, and NADH
dehydrogenase subunit 2 (ND2) gene (in that order) are listed
for specimens used in the molecular analyses. Sample sizes for
each type of analysis are indicated following the taxon names.
Molecular Analyses
Orthogeomys grandis (n = 7).—1) GUATEMALA: Zacapa;
2.55 km S, 1.55 km E La Unión, Finca El Chorro, 1,510 m,
CM 112150 (KC680008, KC680066, KC680045, KC680026,
KC680088). 2) MEXICO: Oaxaca; 1 km NE La Cumbre,
LSUMZ 36583 (KC680007, KC680065, KC680044,
KC680025, KC680087). 3) 3 km SE Morro Mazatán, LSUMZ
36582 (KC680006, KC680064, KC680043, KC680024,
KC680086). 4) ca. 2 km N Zanatepec, LSUMZ 36765
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS421
(KR259280, KR259288, KC692845, KR259297, KC692858).
5) Zanatepec, FMNH 14051 (study skin; Cytb in 2 fragments
KR349917, KR349918). 6) Michoacán; 3.5 km (by road) N
Arteaga, LSUMZ 34392 (AY331247, KC680051, KC680040,
AY331083, KC680083). 7) Puebla; 6 km N Tilapa, LSUMZ
36308 (AY331248, KR259285, KC692847, AY331082,
KR259299).
Heterogeomys (Heterogeomys) hispidus (n = 9).—8)
BELIZE: Cayo; 3 km W Belmopan, LSUMZ 29232
(AY331246, KR259283, KR259291, AY331081, KC692867).
9) HONDURAS: Atlántida; La Masica, Fundación Hondureña
de Investigación Agrícola, ca. 3.8 km N (by road) Tela-Ceiba
Hwy, 10 m, CM 112140 (KC680009, KC680067, KC680046,
KC680027, KC680089). 10) Olancho; El Plan de los Janos,
Pulpería Henner, 1,060 m, CM 112145 (KR259282, KR259290,
KC692852, KC692839, KC692865). 11) MEXICO:
Campeche; ca. 15 km NE Sabancuy, LSUMZ 36762
(KR259278, KR259286, KR259292, KR259295, KC692863).
12) Chiapas; 12 km by old Hwy 63 NW Ocuilapa, LSUMZ 36763
(KR259279, KR259287, KC692851, KR259296, KC692864).
13) Querétaro; Pinal de Amoles, LSUMZ 36090 (KC680004,
KC680052, KC680041, KC680022, KC680084). 14) Veracruz;
ca. 4 km NE Minatitlán, LSUMZ 36761 (KJ476893, KJ476897,
KC692850, KR259294, KC692862). 15) 36 km SE La Tinaja,
43 m, CNMA 41025 (KC680005, KC680063, KC680042,
KC680023, KC680085). 16) Tamaulipas; 19 km S, 9 km W
Llera de Canales, LSUMZ 36767 (KJ476892, KJ476896,
KJ476891, KR259293, KR259300).
Heterogeomys (Heterogeomys) lanius (n = 1).—17)
MEXICO: Veracruz; 2 km S El Xuchitl, 2,442 m CNMA 46463
(KJ476894, KJ476898, KJ476900, KR259298, KR259301).
Heterogeomys (Macrogeomys) cavator (n = 2).—18) COSTA
RICA: San José; 3 km SW División, 2,200 m, LSUMZ 29490
(KC680003, KC680060, KC680039, KC680021, KC680082).
19) PANAMÁ: Chiriquí; Santa Clarita, 32.5 km (by road)
W Volcán, 3,000 ft., LSUMZ 25431 (KC679997, KC680054,
KC680033, KC680015, KC680076).
Heterogeomys (Macrogeomys) cherriei (n = 6).—20)
COSTA RICA: Alajuela; 7 km (by road) NE Quesada, 700
m, LSUMZ 26345 (KC680000, KC680057, KC680036,
KC680018, KC680079). 21) Puntarenas; 5 km S, 6 km W
Esparza, 50 m, LSUMZ 28371 (KC680001, KC680058,
KC680037, KC680019, KC680080). 22) Limón; 4 km S, 5
km W Liverpool, LSUMZ 29494 (KR259277, KR259284,
KC692846, KC692836, KC692859). 23) HONDURAS:
Olancho; 2.8 km (along Trujillo Highway) NW Santa María El
Carbón (jct. Río Wampu Rd.), 500 m, CM 118617 (KR259281,
KR259289, KC692849, KC692838, KC692861). 24)
NICARAGUA: Granada; Reserva Natural Volcán Mombacho,
Finca Santa Ana, 650 m, CM 112148 (KR270732, KR270733,
KC692857, KC692844, KC692871). 25) Matagalpa; Finca
Heroes de Tawa (= La Laguna), 1 km S San Ramon, Lote
el Bosque, 908 m, CM 112149 (KC680011, KC680069,
KC680048, KC680029, KC680091).
Heterogeomys (Macrogeomys) dariensis (n = 2).—26)
COLOMBIA: Chocó; Municipio de Bahía Solano, Parque
Nacional Natural Utría, Ensenada de Utría, ca. 10 m, LSUMZ
30057 (KC679996, KC680053, KC680032, KC680014,
KC680075). 27) PANAMÁ: Darién; 6 km SW Cana, E
slope Cerro Pirre, ca. 1,200 m, LSUMZ 25434 (KC679998,
KC680055, KC680034, KC680016, KC680077).
Heterogeomys (Macrogeomys) heterodus (n = 1).—28)
COSTA RICA: Cartago; 2 km W Santa Rosa, 2,300
m, LSUMZ 29261 (KC680002, KC680059, KC680038,
KC680020, KC680081).
Heterogeomys (Macrogeomys) underwoodi (n = 2).—29)
COSTA RICA: Alajuela; 3 km S Orotina, LSUMZ 29537
(AY331245, KC679995, KC680052, AY331080, KC680098).
30) Puntarenas; 5 km N, 13 km W Palmar Norte, LSUMZ28365
(KC680013, KC679994, KC680051, KC680031, KC680097).
Zygogeomys trichopus (n = 1).—MEXICO: Michoacán; 6
km N, 2 km W Tancítaro, LSUMZ 34340 for COI and MVZ
154081 for other genes (KC680012, KC680073, KC680050,
KC680030, KC680095).
Cratogeomys planiceps (n = 1).—MEXICO: Mexico; 10 km
S, 16 km W Toluca, LSUMZ 36121 (AY506570, KC680070,
AF302183, AY506564, KC680092).
Pappogeomys bulleri (n = 1).—MEXICO: Jalisco; Cerro
Tequila, 7 mi. S, 2 mi. W Tequila, LSUMZ 36082 (AY331249,
KC680074, AF302177, AY331084, KC680096).
Geomys breviceps (n = 1).—USA: Louisiana; Vernon
Parish; 0.5 km N Ranger Station, LSUMZ 29336 (AY331250,
KC680071, KC680049, AY331085, KC680093).
Thomomys bulbivorus (n = 1).—USA: Oregon; Benton Co.;
4 mi. N Corvallis, Benton Co. Courthouse LSUMZ 31308
(AY331255, KC680072, AF155867, AY331090, KC680094).
Morphometric Analyses
Orthogeomys grandis (n = 148).—EL SALVADOR:
Chalatenanga; Los Esesmiles MVZ 1; Los Esesmiles, 6,400
ft., MVZ 1; Los Esesmiles, 7,000 ft., MVZ 4; E slope Los
Esesmiles, 7,200 ft., MVZ 2; N slope Los Esesmiles, 7,100
ft., MVZ 2; Morazán; N slope Mt. Cacaguatique, 3,700
ft., MVZ 1; N slope Mt. Cacaguatique, 3,800 ft., MVZ 1; N
slope Mt. Cacaguatique, 4,700 ft., MVZ 1; San Miguel; Mt.
Cacaguatique, 3,500 ft., MVZ 3; Santa Ana; 1 mi. ENE Cerro
de los Naranjos, 5,800 ft., MVZ 2; Sonsonate; Hacienda Chilata
MVZ 1; Hacienda Chilata, Finca las Tablas, 2,800 ft., MVZ 3;
Volcán Santa Ana, UMMZ 2; Volcán de Santa Ana, 4,500 ft.,
MVZ 1. GUATEMALA: Chimaltenango; Mpo. de Yepocapa,
Finca El Rosario, FMNH 1; Sta. Emilia, near Pochuta, MCZ
1; Sierra Santa Elena, 9,500 ft., FMNH 1; Tecpam [Tecpán],
FMNH 2; Escuintla; 11 mi. SW of Escuintla, Finca San Victor,
700 ft., FMNH 3; Río Guacalate, 1 mi. W Masagua 400 ft.,
USNM 1; Tiguisate, USNM 2; Huehuetenango; Nenton, 3,000
ft., USNM 1; Quezaltenango; 1 mi. NW San Juan Ostuncalco,
USNM 1; 2 mi. N Ostuncalco, USNM 1; 2.5 mi. N Ostuncalco,
USNM 3; Volcán Santa Maria, 9,000 ft., USNM 5; Quirigua;
Quinche Farm, ANSP 2; San Marcos; Volcán Tajamulca, S
slope, 11,000 ft. approx., FMNH 1; Sololá; San Lucas, AMNH
4. HONDURAS: Francisco Morazán; Cantoral, AMNH 1;
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JOURNAL OF MAMMALOGY
Alto Cantoral. AMNH 3; Cerro Cantoral, N of Tegucigalpa,
MCZ 3. MEXICO: Chiapas; 1 mi. SE Puerto Madero, KU 1; 7
mi. ENE Tapachula, KU 1; Tuxtla Gutiérrez, KU 1; Chicharros,
3,400 ft., USNM 1; Huehuetán, 300 ft., USNM 1; Tonalá, 500
ft., USNM 5; Tuxtla; 2,600 ft., USNM 1; Guerrero; 5.5 km N
Agua del Obispo, 3,400 ft., KU 1; Sihuatanejo Bay, UMMZ
1; Acapulco, 2,000 ft., USNM 2; Acapulco, near sea level,
USNM 1; El Limón, USNM 2; Tlalixtaquilla; 4,200 ft., USNM
1; Jalisco; 8 mi. E Jilotlán de los Dolores, 2,000 ft., KU 1;
Michoacán; 3.6 km (by road) N Arteaga, MVZ 3; 1/2 mi. E La
Mira, 300 ft., KU 1; Oaxaca; Mpo. Juchitán; Unión Hidalgo,
AMNH 1; Santo Domingo Ingenio (30 km W Zanatepec),
AMNH 1; Santo Domingo, 900 ft., USNM 1; Chahuites,
AMNH 1; Zanatepec, AMNH 1; Zanatepec, FMNH 1; ca. 2 km
N Zanatepec, 75 m, LSUMZ 1; Mpo. Oaxaca; San Felipe del
Agua, AMNH 1; San Felipe del Agua, Lower slopes of Cerro,
AMNH 1; Mpo. Tehuantepec; Guigoveo, AMNH 1; Limón,
AMNH 3; Morro Mazatán, AMNH 8; 3 km SE Morro Mazatán,
20 m, LSUMZ 1; Sta. Lucia, AMNH 1; Coatlán, AMNH 1;
Mpo. Yautepec; Zapotitlán, AMNH 1; Mpo. not recorded;
Mt. Zempoaltepec, 8,000 ft., USNM 2; (Mt. Zempoaltepec),
near Totontepec, 3,700 ft., USNM 1; near Totontepec, 3,700
ft., USNM 1; Distrito de Tehuantepec Escurano, Cerro de
San Pedro, 20 km W of Mixtequilla, 2,500 ft., AMNH 1; San
Gerónimo, KU 1, MCZ 1; San Gerónimo, 300 ft., USNM 9; 1
km NE La Cumbre, 2,673 m, LSUMZ 1; 1 mi. NNW Soledad,
4,700 ft., KU 1; Cerro San Felipe, 10,000 ft., USNM 8; Cerro
San Felipe, 8,500 ft., USNM 1; Comaltepec, 3,500 ft., USNM
1; 15 mi. W Oaxaca, 8,800–9,400 ft., USNM 1; 15 mi. W
Oaxaca, 8,900–9,200 ft., USNM 2; Pinotepa, 700 ft., USNM
1; Puerto Angel, 100–200 ft., USNM 2; Puebla; 1 mi. SSW
Tilapa, 3,700 ft., KU 3; 2 km N Tilapa, 1,300 m, LSUMZ 1.
Heterogeomys (Heterogeomys) hispidus (n = 217).—
BELIZE: Cayo; 12 mi. S Cayo UMMZ 2; Cayo UMMZ 6;
Orange Walk; Hill Bank, 50 ft., LSUMZ 6. GUATEMALA:
Alta Verapaz; Chipoc AMNH 8; Escuintla; Finca San Victor,
615 ft., FMNH 1; Petén, Uaxactun UMMZ 1. MEXICO:
Campeche; Campeche USNM 5; Conception [Concepción], 73
km SE Escárcega KU 2; Dzibalchen KU 2; 7 km N and 51 km
E Escárcega KU 1; 103 km SE Escárcega KU 3; ca. 15 km NE
Sabancuy, 2 m, LSUMZ 1; Chiapas; 2 mi. E El Real, 1,700 ft.,
KU 1; Ocuilapa; 3,500 ft., USNM 1; 12 km by old Hwy. 63
NW Ocuilapa, 960 m, LSUMZ 2; Pueblo Nuevo Solistahuacán,
AMNH 2; Pueblo Nuevo Solistahuacán, 6,500 ft., AMNH 1;
7.5 mi. (by road) NW Pueblo Nuevo, 6,000 ft., KU 4; Tenejapa;
7,800 ft., USNM 4; Mahosik [Majosík], Tenejapa, 18 mi. NE
San Cristobal, 4,900 ft., MVZ 1; Oaxaca: Mpo. Juchitán, La
Gloria, 1,500 ft., AMNH 1; Mtns. near Santo Domingo, 1,600
ft., USNM 6; 2 mi. S Tollocito [= Tolloso], 150 ft., KU 2; Mpo.
Súchil, Jesus Carranza, AMNH 1; Puebla; Huanchinango,
5,000 ft., USNM 3; Metlaltoyuca, 800 ft., USNM 4; 1 km SW
Ocomantla, 6 km E Villa Juárez, KU 1; 1 km NW Zihuateutla
KU 1; Querétaro; Pinal de Amoles, 5,500 ft., USNM 7; Pinal
de Amoles, 6,000 ft., USNM 1; Pinal de Amoles, 8,000 ft.,
LSUMZ 1; Quintana Roo; 60 km N and 16 km E Chetumal, KU
1; San Luis Potosí; 3 mi. NW Pujal, LSUMZ 1; San Antonio,
2 mi. SW Tilitla, 2,500 ft., MVZ 2; Valles, 400 ft., USNM 1;
Xilitla Region, LSUMZ 7; Tabasco; Montecristo, USNM 1;
Teapa, USNM 3; 1 mi. E Teapa LSUMZ 6; 17 mi. N Teapa,
LSUMZ 1; Tamaulipas; Gómez Farías AMNH 13; Ejido Santa
Isabel, 2 km W Pan American Highway, approx. 2,000 ft., KU
1; 19 km S, 9 km W Llera de Canales, 177 m, LSUMZ 1; 70
km S Cd. Victoria, 2 km W of village of El Carrizo, KU 1;
Veracruz; Achotal, FMNH 4; Catemaco, 100 ft., USNM 1; 20
mi. N of Catemaco, AMNH 1; Chichicaxtle, USNM 1; 14 km
SW Coatzacoalcos, 100 ft., KU 1; Coscomatepec, 2,000 ft.,
AMNH 1; 4 km WNW Fortín, 3,200 ft., KU 2; Jalapa AMNH
5; Jáltipan; 100 ft., USNM 13; Jico, 4,800 ft., USNM 2; 1/2
mi. NE Las Minas, USNM 1; 5 mi. SE Lerdo de Tejada, KU
4; ca. 4 km NE Minatitlán, 10 m, LSUMZ 1; Motzorongo KU
1; Motzorongo, 800 ft., USNM 15; 2 km N Motzorongo, 1,500
ft., KU 1; Papantla; 600 ft., USNM 2; 20 km WNW Piedras
Negras, Río Blanco, KU 1; Potrero AMNH 1; Potrero Viejo, 5
km W Potrero, KU 1; Potrero Viejo, 7 km W Potrero, 1,700 ft.,
KU 1; 3 km N Presidio, 1,500 ft., KU 1; Hacienda Tamiahua,
Cabo Rojo, KU 1 (holotype); 4 km W Tlapacoyan, 1,700 ft., KU
2; 3 km E San Andres Tuxtla, 1,000 ft. KU 5; 5 km N Talapa,
4,500 ft., KU 1; 12.5 mi. N Tihuatlán KU 8; 4 km N Tuxpan,
KU 1; Yucatán; Buenavista, FMNH 1; Chichen Itza AMNH 2,
UMMZ 1, USNM 1; 55 km SSW Mérida, Calcehtok, UMMZ
1; 6 km N Tizimin, KU 1; Yaxcach, USNM 10.
Heterogeomys (Heterogeomys) lanius (n = 4).—MEXICO:
Veracruz; 0.5 km E San José Pilancón, 3,010 m, CNMA 1; 2
km S El Xuchitl, 2442, CNMA 1; Xuchil, FMNH 2.
Heterogeomys (Macrogeomys) cavator (n = 49).—COSTA
RICA: Cartago; 4 km NE Copey, UMMZ 1; El Muñeco,
UMMZ 1; El Muñeco, 10 mi. S Cartago, 4,000 ft., AMNM 1;
San José; ca. 3 km E Canaan, LSUMZ 1; Fila la Máquina, ca.
7.5 km E Canaan, LSUMZ 1; División, 2,300 m, LSUMZ 1; 3
km SW División, 2,200 m, LSUMZ 2; 0.5 km (by road) N El
Empalme, 2,208 m, LSUMZ 1; La Piedra, ca. 4 km SW Cerro
Chirripó, 10,400 ft., LSUMZ 1. PANAMA: Bocas del Toro;
19 km NNW El Volcán, E of Cerro Pando, 2,200–2,400 ft.,
USNM 1; Chiriquí; Bogaba, 600 ft., FMNH 2, MCZ 2, USNM
1; Boquete UMMZ 2, USNM 1; Boquete, 4,000 ft., FMNH 3;
Boquete, 4,000–4,800 ft., MCZ 13; Boquete, 4,500 ft., FMNH
1; Boquete, 5,000 ft., AMNM 2; 1.6 km (by road) N Cerro
Punta, 7,000 ft., LSUMZ 1; Cerro Punta, ANSP 2; Cerro Punta,
Boquete trail, 7,750 ft., USNM 1; Siola, 4,100–4,300 ft., ANSP
3; 14.5 km NW El Volcán, Finca Santa Clara, USNM 1; 32.5
km (by road) W Volcán, 3,000 ft., LSUMZ 2.
Heterogeomys (Macrogeomys) cherriei (n = 33).—COSTA
RICA: Alajuela; Cataratos, AMNM 1; Villa Quesada, 2,000
ft., FMNH 2; Villa Quesada, 2,200 ft., Caribbean watershed,
FMNH 1; 7 km (by road) NE Quesada, 700 m, LSUMZ 2;
Cartago; Santa Teresa Peralta, AMNM 3; Guanacaste; Las
Juntas, LSUMZ 2; 2 km N, 8 km W Juntas, 90 m, LSUMZ
1; Limón; near Bataan, USNM 1; Cariari, LSUMZ 1; 3 km
S Cariari LSUMZ 3; Jiménez (Santa Clara Jiménez), AMNM
3, FMNH 1; Pacuare, USNM 1; Pacuarito, 80 m, LSUMZ
2; 1.5 km N, 1 km E Pacuarito, LSUMZ 1; Siquirres, MCZ
1; Puntarenas; 5 km S, 6 km W Esparza, 50 m, LSUMZ
SPRADLING ET AL.—SYSTEMATIC REVISION OF ORTHOGEOMYS423
2. HONDURAS: Olancho; Santa Maria del Carbón, UNAH
1. NICARAGUA: Matagalpa; Matagalpa, AMNM 4.
Heterogeomys (Macrogeomys) dariensis (n = 24).—
COLOMBIA: Chocó; Municipio de Bahía Solano, Parque
Nacional Natural Utría, Ensenada de Utría, ca. 10 m,
LSUMZ 1. PANAMÁ: Darién; Cana, 500 ft., LSUMZ 1;
Cana, 1,800–2,000 ft., USNM 8; 6 km SW Cana, E slope
Cerro Pirre, ca. 1,200 m, LSUMZ 1; Boca de Cupe, 250 ft.,
USNM 4; Jaque, USNM 1; Paya Camp, USNM 1; Río Paya
(mouth), USNM 1; Tapalisa, 400 ft., AMNM 1; Tarcarcuna,
2,650 ft., AMNM 5.
Heterogeomys (Macrogeomys) heterodus (n = 54).—
COSTA RICA: Alajuela; La Palmita, 1,700 m, LSUMZ 5;
Lajas Villa Quesada, 8 mi. off main rd. San Carlos, AMNM
2; Palmira de Zarcero, 7,000 ft., FMNH 3, UMMZ 3; San
Ramón de Tres Ríos, FMNH 3; Tapesco, AMNM 3; Cartago;
Cervantes, USNM 1; El Sauce Peralta, USNM 1; Paso Ancho,
AMNM 14, UMMZ 1; 2 km W Santa Rosa, 2,300 m, LSUMZ
10; San José; Escazú, 3,200 ft., AMNM 1; Escazú Heights,
4,000 ft., AMNM 1; 1 km (by road) SW Poás, 1,500 m, LSUMZ
3; Rancho Redondo, Volcán Irazú, KU 2; San José USNM 1.
Heterogeomys (Macrogeomys) underwoodi (n = 21).—
COSTA RICA: Puntarenas; 1 km N, 5 km W Palmar Norte,
10 m, LSUMZ 2; 5 mi. E Palmar Norte, LSUMZ 1; Parrita,
LSUMZ 1; Península de Osa, Playa Blanca MVZ 1; 6 km N,
11 km E Quepos, 200 m, LSUMZ 1; 1.5 km NE Tárcoles, 16
km S, 9 km W Orotina, 25 m, LSUMZ 3; 4.5 km N, 1.5 km
E Tárcoles, 30 m, LSUMZ 1; San José; alto de Jabillo Pirrís,
FMNH 6; 14 km (by road) S La Gloria, 200 m, LSUMZ 2; San
Gerónimo Pirrís, AMNM 4.
Zygogeomys trichopus (n = 41).—MEXICO: Michoacán; 2
mi. N Apo, UMMZ 1; Nahuatzin [Nahuatzén], 8,500 ft. USNM
6; Cerro Patamban, NW slopes, ca. 9,000 ft., LSUMZ 1; Sierra
Patamban, 9,100 ft., KU 2; Patamban, 11,000 ft., USNM 3;
Patamban, 11,800 ft., USNM 2; Pátzcuaro, 8,000 ft., USNM 1;
10 km E Pátzcuaro, Cerro del Burro, ca. 3,000 m, LSUMZ 1;
Mt. Tancítaro, USNM 1; Mt. Tancítaro, 6,000 ft., FMNH 2; Mt.
Tancítaro, 7,800 ft., FMNH 1; Mt. Tancítaro, 9,500 ft., USNM
1; Mt. Tancítaro, 10,500 ft., FMNH 1; Mt. Tancítaro, 11,000 ft.,
USNM 2; Mt. Tancítaro, 11,500 ft., USNM 7; 6 km N, 2 km W
Tancítaro, 2,000 m, MVZ 5; 6 km N, 12 km W Tancítaro, 2,000 m,
LSUMZ 4.