2015 Final Report Ctenosaura oaxacana
The effects of habitat fragmentation and hunting on the genetic diversity of the threatened Oaxacan Spiny-tailed Iguana

Report submitted by Gabriela Díaz-Juárez and Víctor Hugo Reynoso

Photos by Gabriela Díaz-Juárez unless otherwise noted.

Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM).

 

Ctenosaura_oaxacana_Diaz3Abstract. Support was requested from the IIF to cover fieldwork expenses for the project: “Effects of habitat fragmentation and hunting on the genetic diversity of endangered Oaxacan Spiny-tailed Iguana.” We cover two survey periods, the first in February 2015 and the second in April-May 2015. We captured 370 iguanas from 24 localities, from Puerto Escondido to the border of Chiapas, in the Isthmus of Tehuantepec, Oaxaca. We obtained 30 samples from nine sites where C. oaxacana suffers either habitat fragmentation and/or hunting, and 10 samples from 10 localities throughout the distributional range of the species to understand its overall genetic variability. During this survey, we also obtained basic natural history parameters of the species throughout the species range, photographed 370 iguanas to document the morphological variation of the species, evaluated the habitat and microhabitat where iguanas were found, conducted an evaluation of local people’s perception towards the conservation of the iguana, and verified presence of iguanas in areas where they were reported previously. Sampling for genetic studies was the main aim of the project overall – to attempt to establish the effect of habitat fragmentation and hunting on the overall genetic diversity and structure of the species, and to establish the effective population size of all populations and the species’ population trends. The results from this project will provide information to create management plans and/or conservation strategies to preserve the Oaxacan Spiny-tailed Iguana.

 

Introduction. The constant increase in human activities such as changing land use for logging, agriculture, livestock, and urbanization have led to an increase in habitat fragmentation, causing a heterogeneous distribution of populations. Fragmentation of iguana populations will produce numerous habitat patches smaller than the original continuous forest, forcing the animals to move, and in the short term to reduce their populations (Gerber and Templeton, 1996). Habitat fragmentation also creates barriers that isolate populations (Hitchings and Beebe, 1997; Gerlach and Musolf, 2000). Fragmentation and loss of habitat combined with extensive hunting are serious problems facing most ctenosaur iguana populations. Habitat fragmentation and hunting has increased with human population growth and unemployment. Despite protection by Mexican law NOM 059 (SEMARNAT, 2010), iguanas are considered for traditional use and hunting by native people is tolerated. VHR’s team has studied the impact of hunting on some iguana species (e.g., Ctenosaura pectinata: Medina-Mantecón and Reynoso, in preparation; Aguirre et al., in preparation). It is known that iguanas are more vulnerable during nesting season because both females and eggs are removed from the system, thus, preventing the recruitment of new individuals.

 

The Oaxacan Spiny-tailed Iguana, C. oaxacana, is endemic to the Mexican state of Oaxaca and restricted to very small areas (526 km2) of tropical dry forest in the lowlands of the southeastern Oaxaca. The IUCN Red List of Threatened Species assesses it as Critically Endangered, with a decreasing population trend, and being one of the most vulnerable species of Ctenosaura (Köhler, 2004). Their populations have suffered significant reductions due to hunting and land use change for agriculture, livestock, and logging that has changed their natural environment (Rioja et al., 2012). A recent study about demography and life history revealed that populations not hunted in conserved forest areas remain stable (Díaz-Juárez, 2014), but to date the conservation status of populations in areas with a high degree of habitat fragmentation and intensive hunting is unknown. Martinez (2015) showed a very low genetic variation in a very small fragment with these iguanas. The only published study on the ecology of this species was about habitat preference (Rioja et al., 2012), and Díaz-Juárez and Reynoso (submitted) now provide a detailed and comprehensive analysis of the life history traits and demography of the species.

 

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Laboratory analysis of blood samples for genetic markers. Photo by Canek Rivera Arroyo.

The study of the structure and genetic diversity of populations of the Oaxacan Spiny-tailed Iguana, combining mitochondrial DNA, nuclear DNA, and microsatellite markers, will provide a short cut to understanding the conservation status of the iguana throughout its distribution, with good accuracy and is an alternative to extensive monitoring. These methods are especially useful for species with large populations or that live in complicated areas (e.g., topography) where detailed monitoring is impossible. At the end of this study we aimed to achieve two main goals: a) determine the genetic diversity and structure of the species as a whole and establish the effect of habitat fragmentation and hunting by comparing three populations in undisturbed continuous forest, three in continuous forest with high hunting rates, and three in fragmented forest without hunting; and b) establish the effective population size of every population, and its predicted population trend for the future.

 

METHODS and RESULTS

Habitat and Microhabitat. Spiny-tailed Iguanas, C. oaxacana, were exhaustively searched for within tree hollows along the whole distributional area of the species in the tropical dry forest along the southern coast of Oaxaca and the Tehuantepec Isthmus, in southern México. From February 2nd to 26th, 2015, nine populations were selected in the Tehuantepec Isthmus according to the following experimental design: three sites with continuous forest where iguanas are not hunted, three sites with continuous forest and high hunting rate, and three fragmented areas where iguanas are not hunted. Each site was searched for 2-3 days. In each site we evaluated environmental factors, topography, and vegetation.

 

From April 11th to May 15th, we sampled 15 randomly-selected sites throughout the southern coast of Oaxaca and the Isthmus of Tehuantepec to understand the morphological and genetic geographic variation of the species. During this second survey we also recorded the species of tree where iguanas were captured, the diameter of the cavity occupied by the iguana, the trunk diameter where the cavity was, environmental temperature and humidity, and the temperature inside the hole.

 

Oaxacan Spiny-tailed Iguanas were captured only in tree species that produce holes. These tree species are: Lysiloma microphyllum, Genipa americana, Byrsonima crassifolia, Mimosa eurycarpa, M. tenuiflora, Acacia coulteri, Cordia elaegnoides, Comocladia engleriana, Crescentia alata, C. cujete, Haematoxyllum brasiletto, and Havardia campylacantha. The hollows that iguanas inhabit ranged from 4 to 80 cm diameter (average 34.32 ± 14.78 cm), the tree diameter ranged from 12 to 250 cm (average 130.9 ± 44.71 cm). The environmental temperature ranged from 24 to 40° C (average 36.67 ± 2.08° C) while the temperature in the refuge ranged from 24 to 36° C (average 35.09 ± 1.68° C), one degree less in average than environmental temperature. Environmental humidity ranged from 47 to 75% RH (average 57.17 ± 10.96% RH).

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Collecting morphometric data. Photo by Adrian Guerra Galvan.

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Morphological Data. From all iguanas we recorded their snout-vent length (SVL), head length (HL), head width (HW), tail length (T), tibia length (Tib), mass, and sex. We generated a high-quality photographic record of each iguana with full body pictures (dorsal, lateral, and ventral views) to understand the geographical variation and to produce a morphological variation catalogue for the species.

 

We captured 370 iguanas from two field sampling sessions, where 34% were females, 43% males, 13% juveniles (sexually immature individuals), and 10% hatchlings. The length for females ranged from 12 to 13.5 cm (average 12.7 ± 0.58 cm), males ranged from 13.5 to 18 cm (average 14.9 ± 1.02 cm), juveniles ranged from 10.5 to 11.75 cm (average 11.2 ± 0.55 cm), and hatchlings ranged from 4 to 10 (average 8.7 ± 0.18 cm). The female’s mass ranged from 26 to 108 g (average 67.5 ± 16.9 g), males from 60 to 200 g (average 114.2 ± 27.5 g), juveniles from 26 to 64 g (average 47.5 ± 1.4 g), and hatchlings from 10 to 42 g (average 26 ± 1.3 g). Morphometric information recorded in this randomly sampled survey will be useful to understand the demography of the species and to establish morphometric relationships with other species of Ctenosaura.

 

Community Interviews. We interviewed one hundred people from different localities along the coast of Oaxaca and the Tehuantepec Isthmus to gather information about the use and practices towards iguanas within their communities, and to evaluate people’s perception towards the benefit of protecting the Oaxacan Spiny-tailed Iguana. The interview was conducted through an open discussion based on a questionnaire that was intended to make people feel comfortable.

 

Based on these conversations, we can establish that generically “iguanas” have been an important part of the culture and development of Mexican society as the subjects of consumption and trade. However, the increase of human activities and loss of habitat has altered the populations of iguanas and many other wild species.

 

The people we spoke to asserted that hunting iguanas increases during the egg-laying season (February-March). However, catches are also made occasionally throughout the year, mainly by people working in the fields and by those that survey trees or fences that divide land ownership. Iguanas are captured primarily for meat consumption, because it is a free available resource and is mostly very tasty. However, there are people who capture them to sell their meat, as pets, or just for fun. In regions with some degree of urban development, people have stopped working in fields, so hunting iguanas has become an occasional activity. Moreover, they know that iguanas are prohibited for trade, that their populations have decreased by the action of hunting, habitat destruction, and the introduction of exotic species (cattle, poultry, dogs, and cats). Unfortunately, they believe that iguanas are used as a resource due to lack of government support for agriculture, fisheries, and the lack of paying jobs. People living in interviewed communities expressed willingness to participate in conservation, together with government and private institutions as long as their rights and their natural, social, and economic resources are respected, and that they are provided with short-term results to benefit their communities.

 

In the absence of sufficient information about the use and conservation of iguanas, it is essential to start with educational programs to raise awareness on the conservation and sustainable use of species that are in some category of protection, and especially for the iguanas.

 

Genetics Laboratory Work. From each of the 370 captured iguanas, we withdrew 0.5 ml of blood from the caudal vein and preserved it in 96% alcohol. The DNA was extracted using the salt extraction method of Aljanabí and Martinez (1997). We have successfully conducted PCR reactions on five fluorescent microsatellite markers (Pec-01, Pec-03, Pec-16, Pec-20, and Pec-25) and collected allelic data for all populations. Genetic analysis with four markers for mitochondrial and nuclear DNA is still preliminary.

 

DISCUSSION

Populations of Oaxacan Spiny-tailed Iguanas are mostly in small fragments or patches as a result of the development of human activities. Vegetation structure indicates that generally this iguana is mainly distributed in dry forests throughout its range as reported by Rioja et al. (2012) and in Nizanda by Díaz-Juárez and Reynoso (submitted). Ctenosaura oaxacana prefers trees with small holes in proportion to their body size, where they can fit tightly. The distribution of iguanas is limited to the presence of tree species with holes, but can also live in fences made with this same kind of tree. Díaz-Juárez (2014) observed that the trees mainly used as refuges are Mimosa eurycarpa (Gui’chi bateede, 93%), Mimosa tenuiflora (Gui’chi bu, 4%), and only occasionally (1.1%) iguanas were captured in the trunk of Chloroleucon manguense (Gui’chi dxita) and Caesalpinia platyloba (Tepeguaje). In our fieldwork, we observed that the topographical composition changes between each locality in the Isthmus of Tehuantepec and the coasts of Oaxaca.  These areas are dominated by tropical deciduous and semi-deciduous forest. We identified new species of trees that are used as shelters by Oaxacan Spiny-tailed Iguana: Lysiloma microphyllum, Genipa americana, Byrsonima crassifolia, Acacia coulteri, Cordia elaeagnoides, Comocladia engleriana, Crescentia alata, C. cujete, Haematoxyllum brasiletto, and Havardia campylacantha. Unfortunately, habitat loss and land use change for agriculture or livestock is a common aspect of the landscape in the whole distribution area of this iguana.

 

Morphometric data indicate that the average length of females and males (12.6 ± 1.15 cm), coincide well with those reported by Díaz-Juárez and Reynoso (submitted), as well as for body mass (67.6 ± 21.02 g). Topographic composition also appears to influence dispersal, morphology, and perhaps social structure. Morphometric data revealed that populations in the Isthmus of Tehuantepec have similar proportions to those reported by Díaz-Juárez and Reynoso (submitted), except in La Venta where the largest iguanas were captured at 18 cm SVL and 200 g body mass. Along the coast of Oaxaca, the smallest sizes were found in the northern coast with a maximum length of 16.5 cm and weight of 145 g. Contrasting, the southern coast of Oaxaca reported the larger sizes of 17 cm SVL and 180 g body mass.

 

The skin color of Oaxacan Spiny-tailed Iguana changes slightly throughout its distribution, mainly in males. Iguanas along the Oaxacan coast were observed with small white spots on the back and pigmentation from yellow to orange on the belly. In contrast, in the Isthmus Tehuantepec they have small white dots and dark bands and the ventral region is beige.

 

Overall, we observed that the sex ratio does not differ from an even 1:1 (χ2 = 14.7, P = 0.54) and compares to that estimated by Díaz-Juárez and Reynoso (submitted) in Nizanda where the proportion was also 1:1 (χ2= 0.338, P=0.56). We observed that this species increases its vagility during the egg-laying season (February-March), hatching season (June-August), and breeding season (December-January). However, hunting and fragmentation also might be influencing these results (Díaz-Juárez and Reynoso, submitted).

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Presentations on iguana conservation were held for local communities. Photo by Ricardo Colin.

 

The Isthmus of Tehuantepec and the coast of Oaxaca have marked fragmentation, which has caused a considerable reduction among the populations of iguanas. According to the commentaries of people, it is becoming less common to find these iguanas in the fields, and even some young people are unaware this species exists.

 

People believed that legislation or season closures on the use of ctenosaurs and other wildlife species should be established. In some localities, people are willing to organize and work to ensure that there is no looting and misuse of Oaxacan Spiny-tailed Iguana, and some want to build small iguana programs where they can establish a method of partial-incubation of eggs with the aim to increase recruitment of individuals to populations.

 

Survival for the Oaxaca Spiny-tailed Iguana is possibly related to protecting the microhabitat that contains trees preferred as refuges. Therefore, it is important to expand the ecological and demographic studies at sites that were sampled to determine the temporal and environmental variability characterizing this species, and provide basic information such as population density, life history, home range, population structure, and behavior.

 

CONCLUSIONS

Knowledge of the natural history of the Oaxaca Spiny-tailed Iguana is essential to provide information to people and create awareness about the conservation of wild populations of C. oaxacana and other iguana species, habitat conservation, and their sustainable use. Here we show that with a relatively small number of individuals captured along the distribution range of a species with a complex distribution pattern, it is possible to obtain a great variety of relevant information at a low cost and in a short time frame. Information on aspects of habitat, environment, natural history, morphometry, and demography were obtained. Furthermore, information generated from the genetic analysis will determine the viability and genetic variation of populations. Therefore, it is advisable to carry out such studies with species that are in some category of risk, are economically important, or endemic, such as the Oaxacan Spiny-tailed Iguana.

 

REFERENCES

Aguirre-Hidalgo, V., C.S. Venegas-Barrera, R. Clark-Tapia, and V.H. Reynoso. Patterns of reproductive trait allocation: relative clutch mass and hatchling variation in the mexican spiny-tailed iguanas Ctenosaura pectinata. Submitted to Journal of Herpetology.

Aljanabi, S.M., and I. Martinez. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25:22–32.

Díaz-Juárez, G. 2014. Demografía e historia de la iguana nguio (Ctenosaura oaxacana: Iguanidae) para su conservación y manejo en la región de Nizanda, Oaxaca. Masters Thesis, Instituto de Biología, UNAM, México D.F. 118 pp.

Díaz-Juárez, G., and V.H. Reynoso. Life history of the Oaxacan Spiny-tailed Iguana Ctenosaura oaxacana. Submitted to Herpetological Conservation and Biology.

Gerber, A.S., and A.R. Templeton. 1996. Population sizes and within-deme movement of Trimerotropis saxatilis (Acrididae), a grasshopper with a fragmented distribution. Oecologia 105:343–350.

Gerlach, G., and K. Musolf. 2000. Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology 14(4):1066–1074.

Hitchings, S.P., and T.J. Beebee. 1997. Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (Common Frog) populations: implications for biodiversity conservation. Heredity 79:117–127.

Köhler, G. 2004. Ctenosaura oaxacana. The IUCN Red List of Threatened Species 20042004. Available from http://www.iucnredlist.org/details/44190/0.

Martinez, G.C. 2015. Diversidad y estructura genética de la iguana Nguio (Ctenosaura oaxacana: Iguanidae) en un bosque continuo y uno fragmentado del istmo de Tehuantepec, Oaxaca, México. Bachelors thesis, Facultad de Ciencias, UNAM, México D.F. 78 pp.

Medina Mantecón and Reynoso, submitted

SEMARNAT, NOM 059. 2010. Norma Oficial Mexicana 2010 Modificada. Protección Ambiental-Especies Nativas de México de Flora y Fauna Silvestre. Diario Oficial de la Federación, 5 de Septiembre de 2015.

Rioja, T., A. Carrillo-Reyes, E. Espinoza-Medinilla, and S. López-Mendoza. 2012. Basic ecology of the Oaxacan Spiny–tailed Iguana Ctenosaura oaxacana (Squamata: Iguanidae), in Oaxaca, México. Revista de Biología Tropical 60(4):1613–1619.