Corresponding author: Robert Murphy ( email@example.com )
Academic editor: Johannes Penner
© 2016 Taylor Edwards, Alice Karl, Mercy Vaughn, Philip Rosen, Christina Meléndez Torres, Robert Murphy.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Edwards T, Karl AE, Vaughn M, Rosen PC, Torres CM, Murphy RW (2016) The desert tortoise trichotomy: Mexico hosts a third, new sister-species of tortoise in the Gopherus morafkai–G. agassizii group. ZooKeys 562: 131-158. doi: 10.3897/zookeys.562.6124
Desert tortoises (Testudines; Testudinidae; Gopherus agassizii group) have an extensive distribution throughout the Mojave, Colorado, and Sonoran desert regions. Not surprisingly, they exhibit a tremendous amount of ecological, behavioral, morphological and genetic variation. Gopherus agassizii was considered a single species for almost 150 years but recently the species was split into the nominate form and Morafka’s desert tortoise, G. morafkai, the latter occurring south and east of the Colorado River. Whereas a large body of literature focuses on tortoises in the United States, a dearth of investigations exists for Mexican animals. Notwithstanding, Mexican populations of desert tortoises in the southern part of the range of G. morafkai are distinct, particularly where the tortoises occur in tropical thornscrub and tropical deciduous forest. Recent studies have shed light on the ecology, morphology and genetics of these southern ‘desert’ tortoises. All evidence warrants recognition of this clade as a distinctive taxon and herein we describe it as Gopherus evgoodei sp. n. The description of the new species significantly reduces and limits the distribution of G. morafkai to desertscrub habitat only. By contrast, G. evgoodei sp. n. occurs in thornscrub and tropical deciduous forests only and this leaves it with the smallest range of the three sister species. We present conservation implications for the newly described Gopherus evgoodei, which already faces impending threats.
Gopherus agassizii, Gopherus morafkai, Sinaloa, Sonora, Testudinidae, Xerobates
Desert tortoises (genus Gopherus: G. agassizii group) occupy a large geographic range throughout the Mojave and Colorado deserts and in the Sonoran desert region of the United States and mainland Mexico (
Conservative estimate of the distribution of G. evgoodei in Mexico indicated by diagonal lines. Desert tortoise range limit, modified based on our field sampling, from
Ecological and morphological characteristics distinguish the northern “Sonoran” and southern “Sinaloan” lineages of tortoises found in thornscrub and tropical deciduous forest of southern Sonora and northern Sinaloa from those occurring further north in Sonoran Desertscrub (
Herein, to assist direct comparison with previous data, we add mtDNA divergence estimates for cytochrome b (Cytb) as well as the standard barcoding locus cytochrome oxidase subunit I (COI) for species discrimination within the Cold Code project (
Measurements were taken on most tortoises that we encountered during field trips in Sonora and northern Sinaloa from 2006 through 2012. These animals served as the genetic resources for
A comprehensive analysis of morphological characters for these desert tortoises does not exist. Thus, our taxonomic evaluation was based on a statistical analysis of the following variables that appeared to us to consistently diagnose the species by exhibiting little intraspecific variation: shell color; integument color; tail length; depth of male plastron concavity; presence of a spur at the radial-humeral joint; and roundness of carapace (e.g. dome-shape vs. flat) based on the ratio of the height at the 3rd vertebral scute to carapace length, while accounting for depth of plastron concavity in males. Shell and integument highlights and hues were coded based on the following wavelengths of colors (
We estimated the area of occurrence for the Sinaloan lineage by using the web-based tool GEOCAT (http://geocat.kew.org/what). Due to having few data points and a hybrid zone, we did not calculate the area of occupancy. Estimated values for G. morafkai and G. agassizii were taken from
Edwards et al. (2016) presented a species-tree reconstructed using a multi-locus Bayesian species delimitation analysis reconstructed from mtDNA and four nDNA loci. The tree depicted Sonoran and Sinaloan tortoises as sister lineages and together they formed the sister to G. agassizii. Nodes of the tree had overlapping standard deviations. This tree topology was consistent with that of an independent analysis of 15 nuclear loci performed by Spinks et al. (P. Spinks,
We generated a 761 bp sequence of mtDNA that encodes part of the gene encoding COI and identified seven unique haplotypes in our sample set (GenBank accession numbers; KR610436–KR610442). Divergence at COI between G. agassizii and Sonoran G. morafkai was 4.1%, between Sinaloan lineage tortoises and G. agassizii 3.6%, and between Sinaloan lineage tortoises and Sonoran G. morafkai 3.4%. Divergence between all three species/lineages of desert tortoise with G. berlandieri averaged 6.1%. For Cytb, we generated 1140 bp sequences and identified six haplotypes (GenBank Accession No. KT956833–KT956838). We included GenBank sequences from G. agassizii (Accession No. AY434562.1) in our alignment and analyses. Divergence at Cytb between G. agassizii and Sonoran G. morafkai was 4.5%, between Sinaloan lineage tortoises and G. agassizii 3.7%, and between Sinaloan lineage tortoises and Sonoran G. morafkai 4.2%. Divergence between all three species/lineages of desert tortoise with G. berlandieri averaged 5.9%.
All species of Gopherus shared the following morphological characteristics with other members of the family Testudinidae (
The flat shell profile/shape of carapace generally distinguishes G. evgoodei from other species of desert tortoises. Live, wild-caught individuals from (i–iv) Rancho Las Cabras and (v–vi) Rancho La Sierrita near Alamos, Sonora, Mexico (in Tropical Deciduous Forest).
The rounded ventral surface of the rear feet (i–ii) and multiple enlarged, raised scales present on surface of forelegs generally (iii–iv) diagnose G. evgoodei in relation to other species of desert tortoises. i–ii same individual in Figure
While male Gopherus have longer tails than females in all species, Sinaloan lineage tortoises differed highly significantly from the other desert tortoises in having a very short tail in both sexes (F5,153 = 56.044; p<0.0005) (Fig.
Gopherus evgoodei differs from other species of desert tortoises in having a very short tail. i Rancho El Chupadero east of Guaymas (in thornscrub habitat); ii Rancho Las Cabras; and iii–i Rancho La Sierrita near Alamos, Sonora, Mexico (in Tropical Deciduous Forest).
Subdued shell mottling and spotting differed highly significantly in Sinaloan lineage tortoises (orange hues) versus G. agassizii and Sonoran G. morafkai (F5,162 = 49.118; p<0.0005) (Fig.
Gopherus evgoodei differs from other species of desert tortoises in often having yellow/orange integument (skin) and shell. i Rancho El Divisadero ii–iii Rancho Las Cabras; and iv–v Rancho La Sierrita near Alamos, Sonora, Mexico (in Tropical Deciduous Forest).
The concavity on the plastron of male Sinaloan lineage tortoises was similar to that of G. morafkai yet highly significantly shallower than that of G. agassizii (F5,77 = 17.885; p<0.0005). Several other morphological characters appeared to consistently diagnose the Sinaloan lineage tortoises. Sinaloan lineage tortoises typically displayed rounded pads on the rear feet (Fig.
Analyses using GeoCAT suggested that the distribution of the Sinaloan lineage encompassed roughly 24,000 km2. We could not calculate the area of occupancy owing to the limited number of data points.
To varying degrees, some of these morphological differences have been recognized in other studies (
Xerobates agassizii Cooper, 1861 (partim)
(Cooper, 1861) (partim). Generic reassignment by
Gopherus morafkai Murphy, Berry, Edwards, Leviton, Lathrop & Riedle, 2011 (partim)
Ventral view of the holotype of Gopherus evgoodei,
Molecular data can readily diagnose all species of Gopherus and their hybrids (
Least-square means (LSM) and sample size (N) for ANOVA for five morphometric characters that are highly descriptive for G. evgoodei and frequency percentages for one character. Mixed samples from localities in the Sinaloan thornscrub-Sonoran desertscrub ecotone with the occurrence of both G. evgoodei and G. morafkai genotypes and/or hybrids. Carapace shape measures ‘roundness’ of carapace.
|Lineage (Location)||Shell Color||Integument color||Tail length||Male plastron concavity||Carapace shape||Humeral spurs|
|LSM||N||LSM||N||LSM||N||LSM||N||LSM||N||% with spurs||N|
|G. evgoodei (Mexico)||601.686||35||593.543||35||0.61||33||10.185||17||0.419||36||100.0||37|
|Mixed G. evgoodei / G. morafkai (Mexico)||574.8||10||560.667||9||0.778||9||13.8||4||0.447||10||62.5||8|
|G. morafkai (Mexico)||548.25||16||541.563||16||0.833||12||11.35||8||0.454||16||25.0||16|
|G. agassizii (Imperial County, California)||562.706||17||546.882||17||0.947||19||25.312||10||0.449||18||15.8||19|
|G. agassizii (San Bernardino County, California)||549.654||26||552.882||17||0.96||25||19.786||8||0.461||25||73.9||23|
|G. agassizii (Kern County, California)||563.219||64||543.578||64||0.934||61||22.844||36||0.454||63||74.6||63|
(parallels that of G. morafkai by
Gopherus evgoodei may exhibit orange or yellow mottling or spotting on the shell and integument. Because color constitutes a diagnostic feature, these data are given above.
As with all species of Gopherus, substantial variability exists among individuals for most morphological features (
The distribution of G. evgoodei (Fig.
, G. morafkai and G. evgoodei appear to have diverged roughly 5.7–5.9 Ma from a common ancestor that was potentially widespread throughout what is now the Mojave, Colorado and Sonoran desert regions (Edwards et al. 2016). Gopherus agassizii likely diverged first via allopatric speciation when the Bouse embayment extended northward between 8–4 Ma (
Ecologically, G. evgoodei occupies hills and low mountains with at least some large boulders or rock outcrops in the TDF, and the TDF–STS ecotone. Its distribution differs from G. morafkai by its strong association with TDF and STS, as well as its absence from SDS. Similar to G. morafkai, G. evgoodei often associates with slopes where rock outcrops and boulders are common. In TDF, the tortoise generally excavates burrows under already existing boulders or enters and modifies existing rock cavities. In flatter areas where boulders are not be available, it digs burrows in soil, although possibly not as extensively as its congeners. During 2012–2013 surveys in Sonora, only 9 of 44 tortoise burrows (20%) in TDF were in soil. In comparison, 56 of 87 burrows (64%) occurred in soil in STS and SDS. Local variation was not surprising. In northern Sinaloa, Vargas V (1994) reported G. evgoodei used packrat middens, dry cacti and even burrows dug by other animals (e.g. nine-banded armadillo, Dasypus novemcinctus). Our observations of G. evgoodei, as part of an ongoing radio-telemetry study near Alamos, Sonora, suggested that Goode’s Thornscrub Tortoise uses several burrows a year and exhibits strong site-tenacity, returning to familiar dens year after year (unpublished data), just like its sister-species.
Presumably, tortoise activity corresponds with monsoonal rains and vegetation growth (
Little is known about daily activity patterns, reproduction, movements or forage of G. evgoodei. Like other species of Gopherus, their activity relates to forage availability and ambient temperatures.
The new species is a patronym, a noun in the genitive case, in recognition of Eric V. Goode, a conservationist, naturalist, and founder of the Turtle Conservancy. He has contributed generously to the conservation of this species via the preservation of land in Mexico, and he actively pursues the conservation of turtles and tortoises on a global scale. Eric sets an important precedent by complementing this taxonomic description with a tangible action that contributes to the conservation of the new species in its native habitat.
We designate paratypes conservatively to exclude the possibility of hybrid individuals that could confound the identity of G. evgoodei (
Because of the high level of variability within all species of Gopherus, descriptions based on only a few individuals or individuals from few populations should be viewed cautiously. For instance,
Our divergence estimates for COI are consistent with species-level divergence in other chelonians (Cytb, 2.8–18.3%;
Desert tortoises command a strong interest in their conservation. A distinct population segment (DPS) of G. agassizii was federally listed in 1990 as threatened under the U.S. Endangered Species Act based on its status (
Additional field work is necessary to assess the conservation status of G. evgoodei, as the above summary is primarily based on observations during field work by
Fortunately, successional forces can restore habitat quality for G. evgoodei in some buffelgrass pastures in thornscrub and especially in TDF. Upon cessation of slashing and burning, secondary growth of native, woody species can quickly replace buffelgrass, and there is some evidence for this in thornscrub as well. Many local people are aware that tortoises enjoy protection and are part of nature. Their occurrence benefits society by providing employment in ecotourism and natural resource conservation. A positive trend involves the establishment and partial re-purposing of private ranches as hunting and conservation reserves throughout much of the tortoise’s distribution in Mexico. Part of the distribution of Gopherus evgoodei includes natural protected areas in Mexico, including Área de Protección de Flora y Fauna Sierra de Álamos-Río Cuchujaqui and certificaded área for conservation Reserva Monte Mojino in Sonora, both relatively recent institutions. If these current trends continue, environmental concerns are likely to tip the balance between pasture and native habitats somewhat in favor of tortoises, particularly if the threats to biodiversity are widely understood. However, these and other impacts on the species, such as the fragmentation of habitat, some mining activities and collection, necessitate further research that can better inform conservation and management efforts.
The recognition of G. evgoodei reduces the area of occurrence for G. morafkai by about 14% from roughly 171 km2 (
For decades, herpetologists have noted the distinctiveness of Mexican populations of desert tortoises in the southern part of the range of G. morafkai, particularly where they occur in STS and TDF. Our review of recent studies sheds light on the ecology, morphology and genetics of these southern populations, which warrant species recognition of this southernmost group. Divergence estimates for COI and Cytb are consistent with species-level differences in other chelonians. Gopherus evgoodei primarily occurs in the state of Sonora, Mexico, extending southward into the northerly extensions of TDF in southern Sonora, northern Sinaloa, and extreme southwestern Chihuahua. The new species occurs only in STS and TDF, leaving it the smallest distribution of the three species of desert tortoises. It is important to define accurately the limits of its distribution, especially because it may occur further south in Mexico. Molecular analyses can easily diagnose all species of Gopherus and their hybrids (Edwards et al. 2016). Further, morphologically, G. evgoodei is easily distinguished from G. morafkai and G. agassizii by several characters, among the most obvious of which is the coloration of both the shell and integument. Gopherus evgoodei is a dark tan to medium-brownish tortoise with a distinctly orange cast. To assess the conservation status of G. evgoodei, additional field work is necessary as very little research on this newly described species exists and a comprehensive understanding of its ecology and behavior must be determined to inform conservation and management initiatives.
We obtained Mexican samples through a multinational, collaborative effort including Comisión de Ecología y Desarrollo Sustentable del Estado de Sonora (CEDES) and F.R. Méndez de la Cruz,