A third case of amelia in Morelet´s crocodile from the Yucatan peninsula

DISEASES OF AQUATIC ORGANISMS Dis Aquat Org Vol. 109: 263–267, 2014 doi: 10.3354/dao02743 Published July 3 NOTE A third case of amelia in Morelet’s crocodile from the Yucatan Peninsula Pierre Charruau1,*, Carlos A. Niño-Torres2 1 Centro del Cambio Global y la Sustentabilidad en el Sureste, A.C., C.P. 86080, Villahermosa, Tabasco, Mexico 2 Universidad de Quintana Roo, C.P. 77019 Chetumal, Quintana Roo, Mexico ABSTRACT: Congenital defects in crocodilians have received little interest. In the context of global change and increasing threats to biodiversity, data on birth defects occurring in wildlife could be of importance for estimating the health of species populations and their ecosystems. Herein, we report the first case of amelia (i.e. absence of limbs) in Morelet’s crocodiles Crocodylus moreletii from Mexico and the third on the southern Yucatan Peninsula. The crocodile in question was a juvenile (41 cm total length) captured in July 2012 in the Río Hondo, the river that forms the border between Mexico and Belize south of the state of Quintana Roo. The prevalence of this malformation in the C. moreletii population of Río Hondo (0.35%) is similar to that reported in 2 previous cases in Belize. Several causes of birth defects in crocodilians have previously been cited in the literature. Although we do not have relevant information to elucidate this case, we discuss some plausible explanations for this birth defect. KEY WORDS: Congenital defect · Crocodiles · Crocodylus moreletii · Ectromelia · Mexico · Quintana Roo Resale or republication not permitted without written consent of the publisher INTRODUCTION Congenital defects in crocodilians have received little interest and have been more likely to be considered mere curiosities rather than of ecological importance. However, in the context of global change, with an increasing number and intensity of threats to biodiversity, data on birth defects occurring in wildlife could be of importance for evaluating the health of species populations and their ecosystems. In crocodilians, several cases of congenital abnormalities of limbs have been reported in different species (Ferguson 1985, Foggin 1987, Huchzermeyer 2003). Malformations include extra digits (polydactyly), absence of digits (ectrodactyly), reduced digits (microdactyly), fusion of digits (syndactyly), extra limbs (polymelia), absence of limbs (amelia) and reduced limbs (micromelia) (Table 1). However, most of these reports are from captive individuals, and few observations have *Corresponding author: charruau_pierre@yahoo.fr been recorded in the wild (Table 1). This is likely due to the early death of malformed embryos and neonates and to the low percentage of individuals affected, which reduce their encounter rate (Huchzermeyer 2003). Furthermore, loss of extremities is common in crocodilian populations, especially in dense populations (Seijas 2007), which can make the detection of birth defects difficult. Herein, we report the first case of amelia in crocodilians of Mexico and the third in Crocodylus moreletii in the southern Yucatan Peninsula. We also discuss possible causes of limb agenesis. CASE REPORT Crocodylus moreletii (Morelet’s crocodile) is a medium-sized freshwater species distributed in the Atlantic and Caribbean lowlands of Mexico, in Belize © Inter-Research 2014 · www.int-res.com Dis Aquat Org 109: 263–267, 2014 264 Table 1. List of limb and digit defects reported in crocodilians. W: wild; C: captive; (–) no information Type of malformation Species W/C References Polymelia Alligator mississippiensis Crocodylus niloticus Crocodylus sp. C C C Ferguson (1985, 1989) Huchzermeyer (2003) Youngprapakorn et al. (1994) Amelia Crocodylus moreletii Crocodylus sp. Caiman sp.a W C C Rainwater et al. (1999), this study Youngprapakorn et al. (1994) Troiano & Román (1996) Micromelia Crocodylus sp. C Youngprapakorn et al. (1994) Polydactyly Alligator mississippiensis Alligator mississippiensis Crocodylus porosus Crocodylus johnsoni Crocodylus niloticus Crocodylus sp. W C – – C C Giles (1948) Ferguson (1981, 1982)b Deraniyagala (1936, 1939)b Ferguson (1985) Huchzermeyer (2003) Youngprapakorn et al. (1994) Ectrodactyly Alligator mississippiensis Crocodylus niloticus Crocodylus acutus C W Ferguson (1982)b Ferguson (1985) Charruau (2010) Syndactyly Alligator mississippiensis Crocodylus sp. Crocodylus niloticus C C C Ferguson (1985) Youngprapakorn et al. (1994) Huchzermeyer (2003) Microdactyly Crocodylus acutus W Charruau (2010) Not specified Crocodylus niloticus C Foggin (1987) a C. latirostris or C. crocodylus yacare; bcited in Ferguson (1985) and in northern Guatemala (Platt et al. 2010). The species is currently listed as ‘Lower risk, conservation dependent’ by the International Union for the Conservation of Nature and Natural Resources (IUCN) and in Appendix II of the Convention on International Trade of Endangered Species of Flora and Fauna (CITES) for Mexico (Platt et al. 2010). In Mexico, C. moreletii is considered as a ‘species subject to special protection’ (Diario Oficial de la Federación 2010). Río Hondo is a relatively deep river (mean depth of about 8 m) that forms the border between Mexico and Belize. The river houses a relatively high number of C. moreletii, with individuals of all size classes and encounter rates that range from 1.72 to 4.70 crocodiles km−1 (Cedeño-Vázquez et al. 2006). During a crocodile survey in the Río Hondo, Quintana Roo, Mexico, on July 17, 2012, we captured a yearling individual (total length: 41 cm; snout−vent length: 20 cm; mass: 132 g) which was missing its left forelimb (Fig. 1). There was no evidence of scarring or other disfigurement to indicate that limb absence was caused by mutilation. Radiography revealed that the bones of the shoulder (coracoid and scapula) were also absent (Fig. 2). The crocodile was marked and released at the site of capture. Crocodiles with missing parts of extremities have been previously captured. In all these cases, evident Fig. 1. Malformed crocodile Crocodylus moreletii captured in Río Hondo, Quintana Roo, Mexico. Note the missing left forelimb. (A) Dorsal view; white arrow = 66 mm. (B) Side (lateral) view (photography by Pierre Charruau and Magdalena Hernández Chávez) scar marks resulting from mutilations during inter- or intra-specific interactions were easily observable. However, in the present case, the entire limb was missing, including the coracoid and scapula bones, and such mutilation would have left evident scars on the skin. These observations indicate that the absence of the limb is likely to be due to agenesis and Charruau & Niño-Torres: Amelia in Morelet’s crocodile Fig. 2. Radiograph plate of the malformed crocodile Crocodylus moreletii captured in Río Hondo, Quintana Roo, Mexico. Note the absence of the shoulder bones (i.e. coracoid and scapula). White arrow = 30.7 mm not mutilation. This case is the first report of forelimb agenesis in crocodilians in Mexico and the third case in C. moreletii in the southern Yucatan Peninsula after those reported in Belize by Rainwater et al. (1999). This is the first observation of such an abnormality among the 286 individuals of C. moreletii captured in Río Hondo to date (J. R. Cedeño-Vázquez pers. comm.). Our prevalence rate (0.35%) is similar to that reported by Rainwater et al. (1999) (0.31%). POSSIBLE CAUSES OF AGENESIS The different factors associated with congenital deformities in crocodilians have been discussed by Ferguson (1985, 1989) and include the age of reproductive females, malnutrition of breeding animals, 265 extremes in incubation temperatures, abnormalities in the hydric or gaseous incubation environment, variation in the orientation of eggs, and exposure to teratogens (such as organochlorine [OC] compounds). Furthermore, a genetic cause could also be considered (Huchzermeyer 2003). As we do not have relevant information to help us elucidate this case, we discuss some plausible explanations. A young/old mother. Ferguson (1985) reported that Alligator mississippiensis embryos produced by young (<15 yr) and old (> 30 yr) females exhibit a higher percentage of spontaneous malformations. Unfortunately, we do not know the age of the mother and we thus cannot conclude that this factor is responsible for the amelia case reported here. A poor diet. Ferguson (1989) reported that A. mississippiensis females fed on a diet rich in fish are more likely to produce malformed embryos than females fed a diet rich in red meat. Although the diet pattern of the mother of the malformed crocodile is unknown, we discard this possibility. Studies on the diet of Crocodylus moreletii from Northern Belize (relatively near to the capture zone) have shown that although fish are an important part of the diet of adult crocodiles, they principally consume gastropods and other prey items such as insects, crustaceans, reptiles, birds and mammals (Platt et al. 2006). Río Hondo presents all this prey diversity (Espinoza Ávalos et al. 2009). Anomaly in incubation conditions. It has been documented that anomalies in some incubation conditions (i.e. temperature, humidity, gas exchange, egg orientation) promote malformations in crocodilian embryos (Ferguson 1985, 1989, Webb & Manolis 1998). C. moreletii is a mound-nesting species that uses vegetation, soil and leaf litter to form a mound in which the female deposits the eggs (Platt et al. 2008). The nest type and nest-site choice generally provides a good and stable level of incubation conditions that buffer the effect of external factors (e.g. environmental temperature, rain, storms) (Magnusson 1979). Once again, in our case we do not know the thermal conditions during the incubation period that may have played a role in the development of the malformed yearling. However, the mean hatching date of C. moreletii in the study area is mid-September (Platt et al. 2008), and based on the total length of the yearling (i.e. 41 cm), it likely hatched in September 2011. Only 2 tropical storms occurred in the region in 2011, and they occurred after hatching or during the last stages of embryo development. Thus, tropical storms, causing sudden temperature fluctuations, are unlikely to be related to the amelia of the yearling, as 266 Dis Aquat Org 109: 263–267, 2014 this defect originates at a very early developmental CONCLUSION stage of the embryo. It is impossible to know the orientation of the egg of the malformed yearling during The absence of the entire left forelimb, including incubation. the shoulder bones, in the captured yearling crocodile Exposure to teratogenic compounds. Raynaud in Río Hondo, together with the absence of clear mu(1990) demonstrated that exposure of embryos to tilation marks, indicate a likely third case of amelia in some chemicals induce limb deformities in reptiles. Crocodylus moreletii in the southern Yucatan PeninFurthermore, higher rates of thyroid dysfunction, sula. Although several factors can induce amelia, it is hatching success, egg shell thinning, and gross birth very difficult to know which one is responsible for the deformities in numerous wildlife populations across present case of limb agenesis. The prevalence of malthe world have been related to habitat contamination formation is very low and does not represent a threat (Hamlin & Guillette 2010). In crocodilians, several to the wild population. Although these cases of birth birth defects related to endocrine system disruption defects are rare and generally considered to be a cuhave been observed in a wild population of A. missisriosity, it is important to report them as they could besippiensis inhabiting a contaminated lake (Guillette come more frequent in the future due to the increase & Milnes 2001, Sepúlveda et al. 2006). However, no in factors inducing these defects. We recommend direct relationships between the high level of concontinuing the monitoring of C. moreletii in the taminants and deformities have been proved. Crocoregion and studying the different factors that can indilians are a top predator, and due to their elevated duce birth defects in crocodiles, especially incubation position in the food web they bioaccumulate and bioconditions and contamination. magnify high concentrations of adverse chemicals (Guillette & Milnes 2001, Campbell 2003, GonzalezAcknowledgements. We thank A. Escobedo-Galván for his Jauregui et al. 2012). Organochlorine pesticides comments on an earlier draft of the manuscript and M. Hernández Chávez for help during the photographic pro(OCPs) are used in agriculture and disease vector cess. The Secretaría de Educación Pública provided support control in the region (Álvarez-Legorreta 2009). Furfor this project through PROMEP funds. P.C. was awarded a thermore, heavy metals and OCPs have been defellowship from the postdoctoral fellowship program of the tected in eggs and scutes of crocodilians near the Universidad Nacional Autónoma de México. All activities were conducted under Mexican law and regulations with a study area (Wu et al. 2000a,b, 2006, Rainwater et al. research permit issued by the Secretaría de Medio Ambi2002, 2007, Charruau et al. 2013). Therefore, conente y Recursos Naturales (SEMARNAT) of Mexico (Permit tamination could be a cause of amelia in the yearling numbers: SGPA/DGVS/03366/12, SGPA/DGVS/10636/11, C. moreletii. SGPA/DGVS/03386/12). Genetic cause. A last cause of amelia could be the presence of a mutated deleterious allele in parents LITERATURE CITED of the neonate (Huchzermeyer 2003). Deleterious alleles may be recessive and remain inapparent ➤ Al Riyami N, Ahmed A, Tanzeem S, Abdul-Latif M (2012) Fetal amelia: A case report. 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