The Influence of Landscape Heterogeneity and Dispersal on Survival of

Neonate Insular Iguanas

Charles R. Knapp1, Silvia Alvarez-Clare2, and Caro Perez-Heydrich3

The relationship between dispersal and predator–prey interactions in heterogeneous landscapes is an underappreciatedfactor influencing species persistence. This relationship, however, is critical for understanding population dynamics andfor implementing management strategies for species. We investigated the influence of habitat heterogeneity anddispersal patterns on neonate survival for the iguana Cyclura cychlura cychlura inhabiting Andros Island in the Bahamas.Contrary to our hypothesis, there was a clear survival advantage for neonates that spent more time in open mangrovehabitat than relatively more closed-canopy habitats, most likely because of fewer primary predators in mangrovesrelative to other habitats. Snake predation was the most significant cause of mortality for neonates dispersing awayfrom nest sites and was highest during the first week after release. The probability of survival to 28 days ranged from16.7 to 28.4%. Most neonates displayed rapid, nearly linear movements away from nests for a minimum of 14 to 21 days.Mean straight-line distance away from nest sites for surviving neonates was 601 m. There was a significant positiverelationship between mean daily movement rates away from nests and days survived. We suspect that the initial andrapid movements away from nests reduce relative predation by dispersing neonates from a zone where predators learnto exploit them. Our results have implications for translocation programs targeting endangered insular iguanasthroughout the Neotropics because historically only the presence of non-native mammalian predators was used as ametric to evaluate potential translocation sites.

THE relationship between dispersal and predator–preyinteractions in heterogeneous landscapes is anunderappreciated factor influencing species persis-

tence. Theory suggests that native predator–prey interac-tions persist over the long term because of variation inpredation rates caused by landscape heterogeneity (Kareivaand Wennegren, 1995; Ellner et al., 2001). In turn, dispersalof prey through heterogeneous landscapes can appreciablyaffect predator–prey interactions by providing refugia forprey, thereby reducing predation pressure (Lewis and Eby,2002; Kauffman et al., 2007; Hakkarainen et al., 2008).Hypotheses concerning the effects of landscape complexityand predator–prey relations, however, are difficult to test inthe field because of variation in predator efficiency (Baberand Babbitt, 2004), prey behavior (Schwarzkopf and Shine,1992; Downes and Shine, 2001), predator learning, andpredator foraging strategy (Downes and Shine, 1998; Toddand Waters, 2007). Still, discerning predator–prey interac-tions and movements in heterogeneous landscapes is criticalfor understanding population dynamics, and for manage-ment and conservation of species.

Studies on survivorship in heterogeneous landscapes arerare for squamates, and have often provided inconsistentresults. For example, Bahamian lizards of the genus Anolissurvived better in forested areas, where encounters withavian predators were less than in non-forested areas(Schoener and Schoener, 1982). In contrast, adult lizardsof the genus Leiocephalus inhabiting a heterogeneouslandscape on the island of Hispaniola experienced uniformpredator pressure between forested and non-forested habi-tats (Gifford et al., 2008). Both studies, however, investigat-ed only survival of subadults and adults in heterogeneouslandscapes. Squamate neonates generally disperse widelyand experience greater selection relative to other age classes(Morafka et al., 2000). Thus, neonatal dispersal, especiallythrough heterogeneous landscapes, offers the opportunity

to study multiple selection pressures (Morafka et al., 2000;Aragon et al., 2007). Despite this opportunity, dispersal andsurvival of free-ranging squamates immediately post-emer-gence or parturition remain among the least studied aspectsof their biology (but see Christian and Tracy, 1981;Drummond and Burghardt, 1982; Jellen and Kowalski,2007; Warner and Shine, 2008).

Members of the genus Cyclura (nine species) inhabitislands throughout the West Indies, are among the mostendangered lizards in the world, and are the focus ofnumerous conservation management programs based onstudies of adults (Alberts, 2000; Hudson and Alberts, 2004;Knapp and Hudson, 2004). Until recently, no detailedinvestigations pertaining to neonate dispersal and survivalhad been conducted for any iguana in the genus. The onlytwo recent neonatal studies on West Indian iguanasdescribed extremely different rates of survival. Usingtelemetry, Perez-Buitrago and Sabat (2007) reported lowsurvival (22.0%) for dispersing neonates (Cyclura cornutastejnegeri) inhabiting Mona Island. Using long-term recap-ture data restricted to post-six-month-old juveniles, Iverson(2007) estimated extremely high annual neonate survival(95.3%) for C. cychlura inornata inhabiting the Bahamianarchipelago. This long-term study (Iverson et al., 2004),however, was conducted on small cays in the Exuma Islands,which presumably restrict juvenile dispersal opportunities.The cays also lack landscape heterogeneity and non-avianpredators, and therefore may not represent a realistic modelfor iguana species inhabiting large islands with complexlandscapes and predator assemblages.

The two reports of extreme survival rates for neonatesinhabiting a large island (57 km2; 22.0%) with a heteroge-neous landscape and a suite of predators (Perez-Buitrago andSabat, 2007), and two small cays in the Bahamas (# 4.5 ha;95.3%) without such attributes (Iverson, 2007), suggest thatmore research is required to test hypotheses pertaining to

1 Conservation Department, John G. Shedd Aquarium, 1200 South Lake Shore Drive, Chicago, Illinois 60605; and San Diego Zoo’s Institutefor Conservation Research, Escondido, California 92027; E-mail: cknapp@ufl.edu. Send reprint requests to this address.

2 School of Natural Resources and the Environment, University of Florida, Gainesville, Florida 32611; E-mail: silviacr@ufl.edu.3 Department of Infectious Diseases and Pathology, University of Florida, Gainesville, Florida 32611; E-mail: caroph@ufl.edu.Submitted: 16 January 2009. Accepted: 1 October 2009. Associate Editor: G. Haenel.F 2010 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-09-014

Copeia 2010, No. 1, 62–70

survival of insular neonatal iguanas. The objectives of thisstudy were to model the influence of habitat heterogeneity,and analyze the effects of dispersal patterns on neonatesurvival of the Andros Iguana (C. cychlura cychlura), whichinhabits the largest island in the Bahamian archipelago.Traditionally, natal dispersal is defined as the movementsmade by an immature animal from its birthplace to theplace of its first reproduction (Howard, 1960). Thus, weanalyzed initial dispersal patterns because our study timeframe most likely did not capture the entire individualdispersal phase.

Predation intensity should be greater in open habitatsthan closed habitats because of the protection offered bydense vegetation (Gifford et al., 2008). Consequently, wepredicted lower survival for neonates in open habitats (i.e.,mangrove , dry evergreen shrubland , pine woodland), asdefined by percent canopy cover and vegetation height.Moreover, lower survival rates on large islands comparedwith small islands have been recorded for other squamatesbecause of the complex predator assemblage associated withlarger islands (Schoener and Schoener, 1982). Therefore, wepredicted lower survival rates for the Andros Iguanacompared to conspecifics from the Exuma Cays becauseAndros is almost four orders of magnitude larger than thecays in the Exumas, and includes several species of predatorysnakes and birds that are absent from the smaller Exumacays.

MATERIALS AND METHODS

Study area.—Andros is the largest island in the Bahamianarchipelago, encompassing an approximate area of6,000 km2. This subtropical island is a composite of threemain islands (North Andros, Mangrove Cay, and SouthAndros), along with dozens of associated cays separated bysaline tidal channels. The substrate consists of oolitic andbioclastic limestone, subject to severe solution weathering.Fieldwork was conducted in a southerly cross-island zone onAndros Island between Mangrove Cay (24u109150N) andSandy Cay (24u059180N). The landscape is characterized by amosaic of three major habitat types (including percentage ofaggregate): pine woodland (42%), dry evergreen shrubland(33%), and mangrove (25%). The signature woody plant ofthe pine woodland is Pinus caribaea var. bahamensis, with avariable understory of species in the genera Bumelia,Cassytha, Exostema, Metopium, Pithecellobium, Savia, andThrinax. Canopy cover ranges between 50 and 60%, with amaximum canopy height of 20 m. Shrubland communitiesare represented primarily by species in the genera Bucida,Byrsonima, Coccothrinax, Erithalis, Jacquinia, Manilkara, Rha-chicallis, and Strumfia. Canopy cover ranges between zeroand 60%, with a maximum canopy height of 4 m. Plants inthe mangrove communities are generally short (, 1.5 m),with canopy cover between zero and 20%, and include thegenera Avicennia, Conocarpus, Laguncularia, and Rhizophora(Sullivan-Sealey et al., 2002). The geology of Andros Island isresponsible for a patchiness of habitat types based on slightfluctuations in elevation. Pine woodland is represented inhigher elevation sites (maximum elevation in study area is2 m), while shrubland is the predominant habitat in lowerelevation sites. Mangroves are not restricted to shorelinesbecause vast low-elevation inland areas become tidallyflooded. Depending on the season, these areas of open karstlimestone contain low-density mangrove species with rootsanchored in submerged solution holes.

Study animals.—The Andros Iguana (C. c. cychlura) is a largelizard (to 10 kg body mass) endemic to Andros Island, andthe only iguana (of three species) in the Bahamas that is notconfined presently to small cays. The lizards face uniqueanthropogenic pressures relative to lizards on other islandsin the archipelago, such as habitat loss, illegal hunting, andimpacts from historic large-scale logging practices. Thesedeleterious effects are compounded by predation by feralanimals (e.g., cats, dogs, and hogs). Consequently, theAndros Iguana is listed as Endangered according to IUCN,the International Union for the Conservation of Nature, RedList criteria.

Neonates (36 in 2003 and 30 in 2004) were collecteddirectly prior to nest emergence or from incubated eggs(Knapp et al., 2006). Mean snout–vent length (SVL) andbody mass (BM) were 97.0 6 0.4 mm (range 84 to 106 mm)and 44.0 6 5.6 g (range 31 to 57 g), respectively. We did notdetermine the sex (i.e., a potential covariate accounting fordifferences in spatial ecology) of individuals for fear ofpotentially endangering neonates via probing for hemi-penes.

Telemetry techniques.—We affixed a BD-2 or PD-2 modeltransmitter (Holohil Systems Ltd., Ontario, Canada) to theinguinal region as described by Knapp and Owens (2005a).Transmitters represented 6.0 6 0.7% of hatchling bodymass. Neonates were released from 12 August to 8 September2003 and from 7 to 27 August 2004 after they had emergedfrom eggs and their umbilical openings had closed. SinceAndros Iguanas are the only iguanas reported to deposittheir eggs within termitaria (Knapp and Owens, 2008), weused a release–relocation method that enabled us to recordthe exact initial position of dispersal. In 2003, neonates werepositioned directly on the dorsal surface of their natal nesttermitarium. A conditioning period (Pollock et al., 1989) ofone day was incorporated into the 2003 data set to minimizethe potential of short-term negative survival biases oftagging and releasing directly on the nest. In 2004, theconditioning period consisted of reburying neonates in theirnests and allowing them to emerge on their own (up to24 hours post-release). The different release protocols didnot result in significant survival differences between years(see below). Termitaria where iguanas were released oc-curred in pine woodland (63%, n 5 12 termite mounds) andevergreen shrubland (26%, n 5 5 termite mounds). Tworelease sites (11%) were from nests discovered in sandy areasat the interface of mangrove and evergreen shrublandhabitats. The potential effects of release location anddistance to habitat types were minimized because all threehabitat types were within one standard deviation of themean daily dispersal distance of neonates. Therefore,neonates theoretically could disperse to any habitat withinone day of emergence.

Iguanas were located with telemetry during the day andearly evening (0830 to 1900 h) at a mean interval of 1.3 6

0.5 days (range 1 to 3). After locating an iguana, we recordedlocation using a GarminH GPS receiver, time, activity, andhabitat association. Neonate locations were confirmed byvisual observation to ensure that we were recordinghatchling movements and not predators with ingestedtransmitters (Knapp and Owens, 2004).

Survival estimation.—Neonates were released over a period ofup to 27 days; therefore, individuals released later were in

Knapp et al.—Dispersal and survival of iguanas 63

the field over a shorter time period than individuals releasedearlier in the season. We therefore truncated survivalestimates at day 28 post-release for each individual becausethis was the shortest time interval spent in the field by atelemetered neonate surviving at the end of the study.Surviving individuals, however, were radio-tracked longerthan the truncated analysis period (mean 5 34.4 days, range28–55). All surviving neonates at the end of the study werefrom different clutches, suggesting that survival probabilitywas evenly distributed among clutches. Thus, we treatedindividual hatchlings as our unit of analysis for the survivaldata.

Temporal patterns of survival were analyzed using non-parametric Kaplan-Meier survival distribution functions,which examine time-to-event models in the presence ofcensored cases (Kaplan and Meier, 1958). The death of aneonate was our ‘‘event,’’ while censored cases wereinstances when an event was not recorded either becausethe individual survived greater than 28 days or because fateswere unknown. The Kaplan-Meier model is based onestimating conditional probabilities at each time pointwhen an event occurs and taking the product limit of thoseprobabilities to estimate the survival rate at each point intime. In 2003 and 2004, the fates of nine and six lizards,respectively, were unknown and thus considered censored.Unknown fates were the result of signal loss or the inabilityto confirm mortality because of stationary transmittersignals emanating from underneath the fragmented lime-stone surface. Estimation bounds of the Kaplan-Meiersurvival curves were thus generated to allow interpretationof extreme rates (Pollock et al., 1989). A pessimistic estimatewas obtained by assuming that every censored observationof unknown fate was a death, and an optimistic estimate byassuming that every censored observation was not a deathand that the hatchling survived to the end of the study. Thelog rank test was used to compare survival distributionfunctions between years (Collett, 2003). The probability ofsurvival using both the pessimistic and optimistic estimatesdid not differ by year (pessimistic: log rank test x2 5 3.34, P5 0.07; optimistic: log rank test x2 5 0.09, P 5 0.77), so the2003 and 2004 data were combined for each survivalestimate.

Effect of habitat use on neonate survival.—To address theimpact of habitat use on neonate survival, we incorporatedthe proportional time spent in individual habitats (pinewoodland, shrubland, and mangrove) as separate covariateswithin univariate parametric survival models. The relativefits of several commonly used parametric survival models(exponential, weibull, logistic, and log-logistic) were assess-ed via Akaiki’s Information Criterion (AIC). According toAIC values, the parametric model that best fits the data wasthen used to address the impact of habitat use on neonatesurvival. Three separate univariate regressions, each corre-sponding to a specific habitat type, were run using this best-fit parametric model. From each of the three fitted modelswe were then able to determine how habitat use affectedsurvival of neonates through our estimates of habitat-specific hazard ratios, which describe the effect of habitatuse on mortality risk. We calculated hazard ratios forintervals of 10% increases in proportional habitat use, asthey were expected to be more informative than those basedon a single percentage unit increase. Ninety-five percentconfidence intervals for hazard ratios and median survival

times were calculated using the delta method (Bolker, 2008).Survival regressions were performed through the survivalpackage in R (Therneau and Lumley, 2008; R DevelopmentCore Team, Vienna, Austria; http://www.r-project.org).

Initial dispersal movements.—We calculated three initialdispersal movement indices using ArcView GIS 3.2a software(Environmental Systems Research Institute, Redlands, CA).Initial dispersal distance was calculated as the straight-linedistance from nest to the last recorded location of a livinghatchling. Although the use of straight-line distance may beinappropriate in certain investigations of dispersal (Massotet al., 2003), Andros Iguana neonates in this studydemonstrated near-linear movement patterns away fromnest sites without establishing apparent home ranges.Additionally, despite the patchiness of habitat types, allwere suitable for neonates in our study time frame. Iguanas(both in this study and non-telemetered) have beenobserved regularly in all habitats over a larger three-yearstudy period in the area. Total distance was calculated bysumming the linear distances between fixed locations. Meandaily dispersal distance was calculated by dividing the totaldistance moved by the number of days individual hatchlingswere tracked.

We tested each animal for non-random movementpatterns using the site fidelity test, with 100 randomsimulations, in the Animal Movement Analysis Extension(Hooge et al., 1999) of ArcView. If animals deviated from anull random walk model, we tested patterns of pathmovement (linearity) using tortuousity analysis (Nams andBourgeois, 2004). Using the computer program Fractal(Nams, 2004), we measured tortuosity by analyzing thefractal dimension (D) of the total distance data, whosevalues range between one when the line is straight and amaximum of two when a line is so tortuous as to cover aplane completely.

Our analyses of dispersal focused on 50 neonates (notincluding the 16 with unknown fates) from 20 clutches. Insome instances, we recorded data from two or more siblingsand thus used two methods to account for non-indepen-dence of data. In the first method, analyses were based onmean trait values for each clutch to avoid pseudo-replication(Warner and Shine, 2008). To ensure independence of datain the second method, a single individual was randomlyselected per clutch. Analyses were then performed using oneindividual per clutch, and subsequently repeated using adifferent combination of randomly selected individuals.These analyses were reiterated 20 times, and the distributionof P-values was used to evaluate effects (Massot et al., 1994).Results from both of our approaches were similar and agreedwith results from analyses that treated siblings as indepen-dent data points (Fig. 1). The statistical results reported inthe text are from analyses that included all the individualsrecaptured.

We used linear regression to compare hatchling morpho-metrics (BM and SVL) and date of release with number ofdays survived and straight-line distance. Because iguanastraveled in a near linear direction, we used linear regressionto compare mean daily dispersal distance with number ofdays survived to evaluate the effect of mean dispersal speedon survival. We used mean daily dispersal distances fromtwo to 28 days because iguanas moved most rapidly duringthis period. Additionally, using mean daily dispersal dis-tance for longer periods would artificially deflate mean daily

64 Copeia 2010, No. 1

distances for surviving neonates because an asymptote forstraight-line dispersal distance was reached after 28 days.Dispersal distances and days survived were log transformedto meet statistical assumptions. Means are presented with 6

one standard deviation except where noted.

RESULTS

Neonate mortality was highest during the first week afterrelease (33 of 66 iguanas). Probability of survival to 28 daysusing the pessimistic estimate (n 5 11 survivors; unknownfates considered dead) was 16.7% (SE 5 0.046), and 28.4%

(SE 5 0.066) using the optimistic estimate (n 5 26 survivors;unknown fates considered alive; Fig. 2). Neonate mortalityduring the first week was significantly the result of

predation by the colubrid snake, Cubophis vudii (sensuHedges et al., 2009) followed by the boid, Epicrates striatus(x2 5 12.08, P 5 0.002; Fig. 3).

Among the four candidate survival models assessedinitially, the log-logistic survival probability distributionbest fit the censored survival data (logLikelihood 5 2192.0),and was therefore used to address the impact of habitat useon hatchling survival. The log-logistic survival regressionrevealed that mangrove habitat was more favorable toneonate survival than either pine woodland or shrublandhabitats. The mortality risk of neonates decreased byroughly 35% with 10% increases in proportional time spentin mangrove habitat. Conversely, mortality risk increased by12 and 10%, with 10% increases in proportional time spentin pine woodland and shrubland habitats, respectively(Table 1). Additionally, the estimated median survival timesof neonates increased significantly with proportional timespent in mangrove habitat, but decreased slightly withproportional time spent in pine woodland and shrublandhabitats (Fig. 4).

There were no between-year differences in SVL, BM, log-transformed days survived, log-transformed maximumstraight-line distance from nest, or in log- transformedmean daily movements rates (all t # 20.058, df 5 48, all P $

0.07), so data were combined for regression analyses. Date ofrelease was not correlated with days of survival (r2 5 0.014, P5 0.40) or maximum straight-line distance from nest (r2 5

0.018, P 5 0.20). Neither SVL (r2 5 0.002, P 5 0.73) nor BM(r2 5 0.016, P 5 0.30) were correlated with number of dayssurvived. Additionally, neither SVL (r2 5 0.002, P 5 0.70)nor BM (r2 5 0.005, P 5 0.57) were correlated withmaximum straight-line dispersal distance from nests. Therewas, however, a significant positive relationship betweenmean daily movement rates and days of survival (r2 5 0.375,P , 0.01). Predation events occurred at a mean distance of192 6 242 m (range 5–1090 m) from natal termitaria.Dispersal statistics are presented in Table 2.

Of neonates that survived a minimum of 14 days, 83% (n5 15) were classified as dispersers based on their non-random (all P , 0.05), over-dispersed movements away fromnests. Neonates moved principally in a straight, unidirec-tional fashion with little movement over previously occu-pied areas. Fractal analysis indicated that these movementpaths were directed linearly (mean D 5 1.06 6 0.02) awayfrom nest sites (Fig. 5).

Fig. 1. Example of P-value distributions from 20 iterations, each usingdifferent combinations of randomly selected siblings from singleclutches. See Massot et al. (1994) for details. The distributions arefrom the regression analysis of mean daily dispersal distance versusnumber of days survived. The vertical dashed line represents the cut-offpoint for statistical significance (P # 0.05). The solid arrow representsthe P-values from analyses that treated each sibling independently. Thedashed arrow represents the P-values averaged across all 20 iterations,which ensured independence of data points.

Fig. 2. Kaplan-Meier survival curves with 95% confidence intervals forAndros Iguana hatchlings using combined 2003 and 2004 data. Solidlines represent the pessimistic estimate where all censored hatchlingswere assumed dead. Hatched lines represent the optimistic estimatewhere every censored observation was assumed not a death and thatthe hatchlings survived to the end of the study.

Fig. 3. Weekly fates of Andros Iguana hatchlings with number ofhatchlings confirmed killed per week by snake genera (see text forspecies) and unknown avian species.

Knapp et al.—Dispersal and survival of iguanas 65

DISCUSSION

Our study demonstrated a striking degree of spatialvariability in survival at the landscape level. Contrary toour hypothesis, mangrove was the safest habitat forneonates among those assessed. An estimated hazard ratio, 1.0 indicated a protective effect of mangrove habitats onneonate survival, whereas pine woodland and shrublandhabitats both contributed to increasing the risk of mortalityamong neonates with hazard ratios . 1.0. Additionally, anincrease in proportional time spent in mangrove habitatswas associated with increases in median survival times,while the effects of pine woodland and shrubland habitatswere slightly negative.

Our habitat-specific survival results underscore the im-portance of landscape heterogeneity in influencing preda-tor–prey interactions on Andros Island. Although themechanisms for landscape influences on survival of AndrosIguana neonates remain unclear, spatially heterogeneousrates of survival may be a general feature of native predator–prey interactions on the island. We postulate increasedsurvival for neonate iguanas inhabiting mangroves becauseof a reduced presence of primary predators in that habitat(Knapp and Owens, 2004; pers. obs.). Further, we suspect

that nest site selection of adult iguanas influences predatorabundance during emergence periods. Iguana neonatesemerge predictably every year from conspicuous andconsistent nest sites (i.e., termitaria) within a one-monthtime frame (Knapp et al., 2006; Knapp and Owens, 2008).We hypothesize that snakes converge on these sites toexploit a temporal food source. There are numerousexamples of avian and snake predators exploiting newlyemerging, or recently emerged, iguana neonates frommainland and island locales (Christian and Tracy, 1981;Drummond and Burghardt, 1982; Werner, 1983; Rivas et al.,1998; Henderson and Powell, 2004), and thus snakes onAndros Island may be targeting habitats with nests (i.e., pinewoodland and shrubland) and not mangrove habitat.

This study demonstrates that snake predation was themost significant cause of mortality in neonate iguanasdispersing away from nest sites on an island lacking nativemammalian predators. The pessimistic and optimisticsurvival estimates of 16.7% and 28.4% are among the lowestreported for an insular iguana species. Neonate survival ratesof other insular iguana species range from 22.0% (MonaIsland; Perez-Buitrago and Sabat, 2007) and 46.9% (Galapa-gos Islands; Laurie and Brown, 1990) to 95.3% (ExumaIslands, Bahamas; Iverson, 2007). The latter two studies usedrecapture methods, which have noted limitations (Koenig etal., 1996). Additionally, the Exuma Island study wasconducted on small, snake-free islands with iguanas markedat six or more months of age, and hence is not directlycomparable. Survival estimates from our study, and those ofPerez-Buitrago and Sabat (2007; 22% 140-day survivalestimate), are more consistent with mainland iguana speciesin the genera Iguana (15% 180-day survival estimate; Harris,1982) and Ctenosaura (25–30% 360-day survival estimate;Van Devender, 1982) and contradict predicted life historytheory (i.e., lower fecundity, growth rates, and age to sexualmaturity, but increased survival for insular species relative tomainland species). The lower-than-expected neonate sur-vival rates are likely mitigated by high adult annual survivalon islands lacking non-native mammalian predators (Iver-son et al., 2006) and a longevity of 50 years or more (Iverson,2007). More survival studies of dispersing neonates areneeded, however, to provide additional survival estimatesfor insular iguanas.

The extreme survival reported from post-six-month-oldneonate iguanas inhabiting small Bahamian cays (# 4.5 ha)in the Exuma island chain (Iverson, 2007) could be a featureof that population (see Pike et al. [2008] for discussion onpotentially inflated mortality rates of reptiles). However,

Table 1. Summary of Survival Model Parameter Estimates and Inferences. Habitat-specific hazard ratios were calculated using maximum likelihoodparameter estimates (b0, b1, and l) of fitted univariate log-logistic survival models. The parameters b0 and b1 represent the intercept and slopecoefficients from the survival regression, and the parameter l represents the scale of the survival probability distribution. Standard errors forparameter estimates are listed in parentheses.

Habitat type b0a (SE) b1

a (SE) la (SE) logL Hazard ratio (95% CI)b

Pine woodland 2.507 (0.406) 20.00854 (0.005) 0.785 (0.087) 2190.5 1.115 (1.105–1.124)Shrubland 1.972 (0.194) 20.00779 (0.006) 0.794 (0.087) 2191.2 1.103 (1.09–1.116)Mangrove 1.498 (0.172) 0.03053 (0.007) 0.702 (0.077) 2182.4 0.647 (0.638–0.657)

a The maximum likelihood parameters b0, b1, and l were obtained by fitting the log-logistic survival function S(t)~1

1zatc, where

a~e{P

b0zb1x

l , and c~1

l, to censored survival data.

b Hazard ratios were calculated as e{b1

l

� �10, and represent the risk associated with a 10% increase in proportional time spent in a given

habitat type.

Fig. 4. Median survival time as a function of proportional time spent ineach of three habitats. Shown are the fitted curves from each habitat-specific regression model (solid line: pine woodland; dashed line:shrubland; dotted line: mangrove). See Table 1 for parameter values.

66 Copeia 2010, No. 1

more probable explanations include unrecorded mortalityduring the first six months, which would artificially inflatesurvival estimates. In our study no neonate mortality wasrecorded for individuals surviving a minimum of 28 days,suggesting that neonates are most susceptible to predationsoon after emergence. High neonate survival on smallBahamian cays versus Andros Island may also be attributedto a lower diversity of avian and non-avian predatorsincluding snakes. Indeed, lizard species inhabiting largerislands in the Bahamas (Andros and Abaco), which support agreater diversity of predators, have lower survival than thesame species inhabiting the smaller island of Bimini(Schoener and Schoener, 1982). Conversely, the low survivalrates of neonates on Andros could be an artifact ofunmeasured negative handicapping caused by transmittersthat reduced the ability to escape predation. Althoughpossible, we believe this not to be the case, as neonatesexhibited normal locomotor behavior in all habitats, andtransmitter burdening of up to 7.5% transmitter-to-bodymass ratios have been demonstrated not to significantlyaffect locomotor performance in other iguana species(Knapp and Abarca, 2009).

Dispersal is a complex phenomenon affected by multiplefactors (Clobert et al., 1994; Perrin and Goudet, 2001),including predation (Weisser, 2001). Mathematical modelspredict that high predation rates and risk of local populationextinction should correlate with increased dispersal (Johnsonand Gaines, 1990). Straight-line distance from nests in ourstudy reached an asymptote after 28 days, but the duration ofthis study precludes us from drawing conclusions onmovement patterns beyond this time frame. However, theactive initial dispersal of iguana neonates in this study rapidlyincreased their presence from concentrated emergence pointsto widespread areas. We suspect that the initial and rapidmovements away from nests reduce relative predation bydispersing neonates from a zone where predators learn toexploit them (Morafka et al., 2000). Indeed, there was asignificant positive relationship between mean daily move-ment rates away from nests and days survived. Althoughmultiple, often synergistic factors likely influence dispersal(Ronce et al., 2001), the likelihood of predation in the vicinityof nest sites appears to be an important selective forcefavoring vigorous and immediate dispersal (Drummond andBurghardt, 1982). Since relative snake predation of iguana

Fig. 5. Mean straight-line distance (m) 6 1 S.E. from nests for Andros Iguana hatchlings surviving a minimum of 14 days (n 5 18).

Table 2. Dispersal Statistics for Andros Iguana Neonates Tracked up to 28 Days Post Release from Natal Sites. Means are presented with 6 1standard deviation and ranges in parentheses.

Straight-line distance (m) Total distance (m) Mean daily distance (m)

All neonates (n 5 50) 261 6 371 (5–2300) 411 6 514 (13–2975) 21 6 14 (6–67)Neonates surviving $ 14 days (n 5 18) 532 6 281 (156–1090) 801 6 467 (210–1987) 25 6 12 (10–54)Surviving neonates (n 5 11) 603 6 233 (329–1033) 891 6 539 (463–1987) 26 6 11 (14–54)

Knapp et al.—Dispersal and survival of iguanas 67

neonates appeared to taper after two weeks and with distancefrom nest, investigations are needed to determine theunderlying physiological mechanisms responsible for theability of snakes to detect and presumably trail newlyemerged neonates. Studies of neonate dispersal should alsobe extended to determine factors that influence the end ofdispersal and initiation of home-range establishment.

Conservation implications.—Conservation programs basedexclusively on data from adult age classes may misrepresentthe population dynamics of a species and lead to spuriousmanagement initiatives (Kareiva and Wennegren, 1995).Our results must be incorporated with those from adultAndros Iguanas in order to understand the ecologicalrequirements of this species. Variation in survival probabil-ities over a heterogeneous landscape is particularly critical inapplied contexts, for example, in demarcating protectedareas (Cabeza, 2003). Knapp and Owens (2005b, 2008)demonstrated the importance of protecting pine woodlandsfor adult iguanas and their nest sites. Results from this studyunderscore the importance of further protecting mangrovehabitat for dispersing neonates.

Our results have implications for conservation efforts(e.g., translocation) targeting endangered insular iguanasthroughout the Neotropics. Typically, iguanas are translo-cated to islands free of non-native mammalian predators.Here, we demonstrated the potential for underestimatingthe impacts of native predators, such as snakes, on incipientiguana populations. The presence of these native predatorsshould offer an additional metric when evaluating the mostappropriate site for translocating iguana populations. Anyreduction in recruitment could hinder the success of theprogram, especially for a small, slowly reproducing popula-tion adjusting to a translocation. Therefore, both non-nativeand native predators should be evaluated prior to translo-cating or relocating endangered insular iguana species.

ACKNOWLEDGMENTS

This research was supported by the John G. SheddAquarium, the Association of Zoos and Aquariums Conser-vation Endowment Fund, and the Disney Wildlife Conser-vation Fund. We thank the Bahamas Department ofAgriculture for permission to conduct the study. TiamoResorts of South Andros provided crucial logistical support.We thank A. Owens and C. Sheehy, III for assistance in thefield, and B. Bolker for assistance with data analyses.Constructive comments on the original manuscript wereprovided by C. K. Dodd, Jr. and J. Iverson.

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