Size-selected Harvesting of a Common Iguana Species (Ctenosaura similis): Possible Impacts on Population Structure, Sexual Dimorphism, and Social Dynamics. Elizabeth C. Miller Size-selected harvesting, where hunters preferentially take large size classes of a population, is well documented in many exploited species. The effects of size-selected hunting pressure include: reduced growth rate, smaller size at sexual maturity, changes in social hierarchies, and decreased number and quality of offspring. This study evaluated the impacts that size-selected harvesting could have on Ctenosaura similis (ctenosaur) populations in the Guanacaste Province of Costa Rica. C. similis populations were compared in three sites protected from hunting with populations in three nearby unprotected sites. From the photographs of 95 individuals, I estimated snout-vent length, head length, and body height. Males in hunted areas that were identifiable by secondary sex characteristics were smaller across all three measurements taken, while females did not show changes in body or head size. Additionally, more juveniles showed territorial behavior in hunted areas, while juveniles in protected areas were likely displaced by large adults. These results suggest that hunting adults of this species impacts on social behavior and sexual dimorphism. 29 Introduction Size-selected harvesting occurs when larger size classes, which are the most desirable for meat or trophy hunting, are preferentially hunted over smaller individuals. 1 This differential selection pressure causes skewed size class distributions, reduced reproductive output in cases where individual fitness is positively correlated with body size, and behavioral changes in species with size-dependent social hierarchies. These effects have been seen in both wild and experimental populations of species hunted by humans. 2-6 Due to the negative impacts on individual fitness, there is potential for slowed population growth and reduction of population size. In order to maintain healthy iguana populations, it is important to evaluate the degree to which animal populations have experienced unnatural selection pressure caused by hunting. Large iguanid lizards (Iguana, Ctenosaura) have a long history of traditional use in Central America. These iguanas are exported for the fashion and pet trade in addition to local consumption of their eggs, meat, and fat. While iguana farming holds promise for relieving local populations from being hunted, wild iguanas are still heavily exploited. The ctenosaur, Ctenosaura similis, is common in the dry forests of Costa Rica. Juveniles are ubiquitous in yards and roadsides, but adults at their maximum size are rare in places where they are not protected from hunting. In addition to being economically and culturally important, large individuals are important for the health of dry forests because they eat more fruit than smaller individuals and act as seed dispersers. 8-9 Therefore, sizeselected harvesting of ctenosaurs may have a negative impact on dry forest plants; thus making it important to conserve them as part of a healthy ecosystem as well as to maintain the populations for human use. SALTMAN QUARTERLY VOL 10 The morphology of individuals, especially the head length, body mass, and body length, is sexually dimorphic, 15 with males being much larger and having longer heads than females. Secondary sex characteristics of male iguanids develop with increasing age. 24 Therefore, older males will show a greater degree of morphological difference from females than younger males. Male body and head size also influences social rank. 16 In females, clutch size is positively correlated with body size. 17 Mortality due to natural predation is highest in juveniles and decreases as individuals grow. 13 Due to these factors, reproductive success increases with body size in both sexes. Many studies have demonstrated that lizard sociality is more complex than was once believed 10. Like most iguanids, ctenosaurs are territorial and have sizedependent dominance hierarchies that are most pronounced among males. 11-13 Though small males may succeed in sneak-mating in a large male s territory, males may improve their reproductive success by postpone mating until they become large enough to defend a territory or become receptive to females. 14 Experiments show that growth rate and aggressive behavior, both of which are factors that influence social rank in male iguanas, are plastic depending on the social and environmental context. 18-20 Not much is known about the anthropogenic impacts on aspects of iguana biology besides the reduction of population size from exploitation. In this study I explored the possible effects of size-selected hunting on distribution of size classes, shifts in social behavior, and physical proportions of individuals by comparing individuals in areas protected for conservation with those in hunted areas. I predict that 1) in hunted areas, the majority of individuals will be smaller than those in protected areas; (2) small Figure 1. A photograph of a large adult male (taken at Junquillal Beach on 11 May 2011), with lines demonstrating the body measurements estimated using ImageJ software. individuals will show more head-bobbing displays in hunted areas than in protected areas; and (3) the difference in absolute head length between males and females will be lower in hunted areas than in protected areas. Methods Study Sites This study was conducted in seasonal dry forest and developed sites near the Pacific coast of the Guanacaste Province. Populations were observed from May 2nd until May 14th, 2011. During this time period, the rainy season had not yet started (May-November) and the breeding season for this species was already over (February to March). Six different sites were surveyed: three protected and three hunted. Protected sites were located in three different sectors of the Area de Conservación Guanacaste (ACG); Each sector sampled was within an area no larger than 1 km 2 and contained the main administration and camping area of the park. These included (1) Sector Murcielago (7 km west from the town of Cuajiniquil), (2) Sector Junquillal (4 km north of Cuajiniquil), and (3) Sector Santa Rosa (21 km southeast from Cuajiniquil). The hunted areas were the roads and communities surrounding the ACG which included (1) town of Cuajiniquil sq.ucsd.edu
Table 1. Numbers of each class of individuals seen in each site. In protected sites (P), many more adults were seen than juveniles, while in hunted sites (H) many more juveniles were seen than adults. More larger individuals display in protected sites, while in hunted sites smaller individuals displayed most often. * # Seen (# with size measurements taken from photograph). ** # Seen displaying (# smaller than 25cm SVL). (10 56'35.86"N, 85 41'9.10"W), (2) a 4 km road between the town of Cuajiniquil and the entrance of Sector Junquillal, and (3) a 7 km road between the town of Cuajiniquil and the administration building of Sector Murcielago, with a second 1.7 km road branching off from this and ending at Playa Cuajiniquil. Identification in the Field Ctenosaurs were found indiscriminately by walking along roads and surrounding areas, campgrounds, buildings, and trails. Observations were made as early as 0800h and as late as 1700h. Ctenosaurs were photographed as they were found. Individuals were placed into three categories based on their visible secondary sex characteristics: male (possessing hypertrophied jaw muscles and a long crest), female (not possessing a long crest but having a large body weight relative to juveniles), or juvenile (small and thin body). From photographs, individuals were distinguished from one another based on location, pattern, color, and tail regrowth. If a ctenosaur ran away before it could be photographed, it was still recorded as seen though no size data were taken. Each individual was recorded as seen only once even if it was seen multiple times. The presence or absence of head-bob displays during the observational period by the focal animal was also recorded, signaling a territorial claim or confrontation. Estimation of Size Measurements In areas where C. similis has been hunted, individuals are wary of humans and very secretive. For this reason, individuals were estimated from photographs instead of capturing them to measure directly. Using a tape measure, snout-vent length (SVL) measurements were taken from two live, captured individuals (eye and head length of live individuals were estimated from photographs based on known SVL for safety reasons). From these measurements, it was determined that the height of the eye, usually 0.5 cm, varied little between individuals. Using ImageJ software (National Institute of Health; http://rsb. info.nih.gov/ij/), the height of the eye was standardized at 0.5 cm and used as a scale to measure the head length (from jaw to end of ear opening), body depth (a substitute for mass, widest point of trunk from belly to beginning of crest) and SVL (estimated from jaw to end of pelvic girdle) of individuals photographed in the field (Figure 1). Data Analysis Due to low sample size, individuals from the six sites were pooled into two groups: hunted and protected. A Welch s t-test was used to statistically compare the differences in SVL, head length, and body depth between the two groups. An additional t-test was used to determine difference in SVL of only head-bobbing individuals between the two groups. An Analysis of Covariance (ANCOVA) was used to test for a difference in the proportional relationship of SVL and body depth across the two groups. Results Abundances A total of 155 individuals over 44.7 hours were observed. Size measurements were taken from the photographs of 95 individuals (64 in protected sites, 31 in hunted sites). This included two deceased individuals found on roads, a juvenile and a male, that were dissected and measured with a measuring tape. These two measurements are included in the data for the hunted site Cuajiniquil, which was the closest site to where the two individuals were found (though not included in data for displaying individuals). Within protected sites, size measurements were taken from 30 females, 21 males, and 13 juveniles. Within hunted sites, size measurements were taken from four males, five females, and 21 juveniles (Table 1). Size Class Distribution and Size Measurements In protected sites, the distribution of size within classes roughly follows a normal distribution. However, in hunted sites the size class distribution is right skewed (Figure 2). Males in hunted areas were shorter in SVL (t 3.85 =3.16, P= 0.036) and had smaller body depths (t 4.35 = 2.86, P = 0.042). Male head length tended to be shorter in hunted sites, though this relationship was not significant (t 5.52 = 2.36, P= 0.06). This suggests that males in hunted sites are smaller in size and have a smaller body mass as compared to males in protected sites, though there was no significant proportional difference (Figure 3). Females and juveniles did not show a difference in these measurements between protected and hunted sites. Sexual Dimorphism The difference in mean head length between males and females was 40% smaller in hunted sites (Figure 4). The ratio of male head length to female head length was 1.38 in protected sites and 1.14 in hunted sites. The ratio of male SVL to female SVL was 1.20 in protected sites, compared to 0.99 in hunted sites. The measurements of males in hunted sites are closer to those of females across two sexually dimorphic characteristics. Differences in Display Behavior In protected sites, twenty adults and two juveniles with size data head-bobbed during the observational period. In hunted sites, two adults and nine juveniles displayed. No juvenile in any site was observed headbobbing in view of an adult male; however, juveniles were observed head-bobbing near adult females. The mean SVL of individuals observed head-bobbing was smaller in hunted sites compared to protected sites (t 15.77 = 4.60, P= 0.0003). In hunted sites, 43% of individuals smaller than 25 cm SVL displayed, while 23% of individuals of the same size class in protected sites displayed. Discussion Though C. similis remains common in hunted areas, these populations are disproportionately comprised of juveniles. Juveniles are likely to have home ranges hidden from adults due to the risk of cannibalism, 21 which may explain why they are more visible in the absence of large adults. It is possible that fewer adults were sq.ucsd.edu VOL 10 SALTMAN QUARTERLY 30
31 Figure 2. A histogram of size classes in hunted sites (white bars) and protected sites (black bars). Data includes males, females, and juveniles. Figure 3. The relationship between SVL and body depth in males. White squares represent males from hunted sites, and black diamonds represent males from protected sites. There is not much overlap in size between the two groups. seen in hunted areas because of differences in predatory avoidance behavior. Adults in protected sites could be easily approached within 1 meter. In contrast, most adults seen in hunted sites did not let me approach them, and had to be observed from far away. This shows a marked difference in the recognition of humans as predators between the two groups. It is likely that there is selection for secretive behavior in hunted populations. In addition, individuals could be learning to avoid humans by accumulating negative experiences during their lifespan. The cautious nature of large individuals in hunted areas is one source of sampling SALTMAN QUARTERLY VOL 10 bias. This bias could contribute to the size differences observed in hunted and protected populations. There is a degree of error associated with the method of estimating size data from photographs. In some cases, individuals tried to escape before a profile shot could be taken. Size data had to be estimated from slightly tilted images of ctenosaurs in these cases. This could alter the measurements taken from the photograph. However, due to the difficulty of capturing ctenosaurs, this noninvasive technique was the best method available for this study. C. similis is considered to be the world s fastest sprinting lizard species, 22 and as mentioned above they are often wary of humans. Future studies with greater available resources could take advantage of trapping methods for more accurate measurements, though at the risk of causing stress to the ctenosaurs. Some small individuals in hunted sites (between 20 and 30 cm SVL) could be identified as male based on their secondary sex characteristics; though I did not observe males smaller than 30 cm SVL in protected areas. An entire size class of males was present where hunting occurred, and not observed in areas protected from hunting. One hypothesis for this observation is that smaller males become more visible in the absence of large dominant males, and the discrepancy is the result of sampling bias. If males identifiable by secondary sex characteristics smaller than 30 cm SVL exist in protected sites, they are displaced by larger dominant males and have territories in subpar locations. The removal of large dominant males by hunters opens up better territorial opportunities for smaller males; therefore they became more visible A second hypothesis to explain the presence of a smaller size class of males in hunted areas is that the removal of large dominant males acts as a social cue to turn on the development of the secondary sex characteristics. Many studies on various iguanid species show that dominance hierarchies affect the development of males. In many territorial iguanids, the presence of a large dominant male can elevate levels of corticosterone and depress levels of testosterone in subordinate males. 18 Even the visual cue of an adult male suppresses the growth rate of juvenile males in the green iguana. 23 In a study on Galapagos marine iguanas, the experimental injection of testosterone into subordinate males caused them to act more aggressively and display territorial behavior, showing that there is plasticity in reproductive phenotypes caused by hormone levels. 20 Therefore, in the case of C. similis, it is possible that the removal of large males by hunters removes this depressive pressure on the hormones of smaller males and they develop the secondary sex characteristics such as the elongated crest and swollen jaw muscles at a much smaller size. Thus, these individuals are recognizable males even though they are small relative to those in protected sites. To test this hypothesis, individuals in protected and hunted areas of the same size could be captured and sexed using cloacal analysis. 24 Males in hunted areas had size measurements of the head and body that resembled those of females in both hunted and protected sites. This decrease in sexual dimorphism can be explained again by the differences in social behavior of males and females. Secondary sex characteristics of male iguanids develop with increasing age. 24 Therefore, males that develop secondary sex characteristics at a younger age would not differ in head and body proportions from a female as much as in an older male. It remains yet to be determined if the reduced size of males in hunted areas leads to reduced offspring quality. The presence of head-bobbing displays was used in this study to signify the ownership of a territory. All individuals, including juveniles, are territorial 15 though juveniles may be displaced by large individuals. If a small male displays within the territory of a sq.ucsd.edu
Figure 4. The differences in head length between males (M) and females (F) in unprotected sites. Dimorphism of this trait was reduced in unprotected sites. larger male, the small male would probably be chased away by the large male. Therefore, if a juvenile displays, it can be safely assumed that it is not within the territory of a large male. The increased prevalence of small individuals displaying in areas affected by hunting could be explained by the decreased number of territories owned by large individuals. Smaller individuals are more easily able to acquire and defend territories in the absence of larger individuals that would otherwise displace them. These trends could be confirmed by increased monitoring and sampling of populations in these sites. It is also important to examine if there are changes in life history traits in these populations, including growth rate, size at sexual maturity, and reproductive success with age. A mark-recapture study would reveal any differences in growth rate and size at maturity between protected and hunted populations. The number and survival of these offspring would reveal differences in reproductive success caused by age and size differences of parents in hunted and protected populations. It is essential for the health of iguana populations to detect changes in life history traits as a result of hunting pressure that could compromise their reproductive success. Another future area of research is the role of protected areas as population sources for hunted areas. Are populations restricted to their home range, or does migration occur? Fitch and Henderson noted that individuals rarely travel more than 50 meters from their central refuge. 13 During observations, hatchling iguanas were found near the road outside of Sector Junquillal and hatchlings became more abundant closer to the park, with peak abundance within the park (Miller, pers. obs.). Molecular testing could confirm if hatchlings outside the park came from parents living in the park. It is important to understand the role of protected sites in preserving large populations of C. similis, as well as for promoting the health of populations outside of parks. Acknowledgements I thank Frank Joyce for general project guidance, help with data analysis, assistance in the field, facilitating transportation to my sites, and helpful comments on the manuscript. Robert Drewes and Erick McAdam also gave advice. Additional thanks to Maria Fernanda Carazo for help in the field sighting ctenosaurs. I am thankful to the Campos-Castro family for housing me for two weeks in the community of El Congrejal, Cuajiniquil while I conducted field work. Equipment such as binoculars and cameras were supplied by the University of California Education Abroad Program. Bob Drewes, Heather Henter, and the Saltman Quarterly team made helpful comments. This research was funded in part by the Friends of the International Center at the University of California, San Diego. References 1. Fenberg, P.B., and Roy, K. (2008). Ecological and Evolutionary Consequences of Size-selective Harvesting: How Much Do We Know? Molecular Ecology, 17(1), 209-20. 2. Platt, S.G., and Thorbjarnarson, J.B. (2000). Population Status and Conservation of Morelet's Crocodile, Crocodylus Moreletii, in Northern Belize. Biological Conservation, 96, 21-26. 3. Conover, D.O., and Munch, S.B. (2002). Sustaining Fisheries Yields Over Evolutionary Time Scales. Science, 297(5578), 94-96. 4. Jennings, S., and Blanchard, J.L. (2004). Fish Abundance with No Fishing: Predictions Based on Macroecological Theory. Journal of Animal Ecology, 73(4), 632-42. 5. Carver A.M., Wolcott, T.G., Wolcott, D.L., and Hines, A.H. (2005). Unnatural selection: effects of a malefocused size-selective fishery on reproductive potential of a blue crab population. 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Fox, S.F, McCoy, J.K., and Baird, T.A. Johns Hopkins University Press, 278-309. 17. King, R.B (2000). Analyzing the Relationship between Clutch Size and Female Body Size in Reptiles. Journal of Herpetology, 34(1), 148-50. 18. Phillips, J., Alberts, A., and Pratt, N. (1993). Differential Resource Use, Growth, and the Ontogeny of Social Relationships in the Green Iguana. Physiology & Behavior, 53(1), 81-88. 19. Baird, T.A, and Timanus, D.K. (1998). Social inhibition of territorial behavior in yearling male collard lizards, Crotaphytus collaris. Animal Behavior, 58, 989-994. 20. Wikelski, M., Steiger, S.S., Gall, B., and Nelson, K.N (2004). Sex, Drugs and Mating Role: Testosteroneinduced Phenotype-switching in Galapagos Marine Iguanas. Behavioral Ecology, 16(1), 260-68. 21. Mora-Benavies, J.M (1991). Cannibalism in the ctenosaur lizard, Ctenosaura similis, in Costa Rica. Bulletin of the Chicago Herpetological Society, 26(9), 197-198. 22. Garland, T.G. (1984). Physiological correlates of locomotory performance in a lizard: an allometric approach. American Journal of Physiology, 247(5), R806-815. 23. Alberts, A., Jackintell, L., and Phillips, J. (1994). Effects of Chemical and Visual Exposure to Adults on Growth, Hormones, and Behavior of Juvenile Green Iguanas. Physiology & Behavior, 55(6), 987-92. 24. Rivas, J.A. and Avila, T.M. (1996). Sex identification in juvenile green iguanas (Iguana iguana) by cloacal analysis. Copeia, 1996(1), 219 221. WRITTEN BY ELIZABETH MILLER. Elizabeth Miller is a Ecology, Behavior, and Evolution major from Marshall College. She graduated in 2012. sq.ucsd.edu VOL 10 SALTMAN QUARTERLY 32
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