population biology and behaviour of the alien species ... · biology of introduced iguana iguana in...

Introduction

Continental biotas that had been isolated for millions of years were drastically opened to outside influence at the beginning of the Exploration Age (Mooney and Cleland, 2001). Among other human-induced changes to these newly exposed ecosystems, the introduction of exotic species can damage ecosystems by altering the normal evolutionary course through processes such as competitive exclusion, niche displacement, and hybridization; all of which may lead to extinction of native species (Mooney and Cleland, 2001).

The introduction of exotic species is cited as one of the most important causes of biodiversity loss by Vié, Hilton-Taylor and Stuart (2009). The same authors

affirm that there is a lack of information about the issue of invasive species, resulting on an underestimate of the effects of species introductions and on a lack of adequate prevention and mitigation measures. As exotic species often do not have many natural predators, their populations can grow unbounded, thereby increasing the impacts of the introduction on landscapes and native populations (Global Invasive Species Database, 2008).

The species Iguana iguana (Linnaeus, 1758) is a lizard that can reach up to 1.8 metres in length. It has

Herpetology Notes, volume 4: 445-451 (2011) (published online on 15 December 2011)

Population biology and behaviour of the alien species Iguana iguana (Linnaeus, 1758) on a restored wetland

in Puerto Rico

Caio A. Figueiredo-de-Andrade1*, Ruby A. Montoya-Ospina2, Júlio Cesar Voltolini3 and Carlos R. Ruiz-Miranda4

1 Departamento de Zoologia, Instituto de Biologia, Univer-sidade Federal do Rio de Janeiro. CEP 21944-970. Rio de Janeiro, RJ, Brazil.

2 Escuela de Ciencias y Tecnología, Universidad Metropolitana. PO BOX 21150, ZIP CODE 00928-1150, San Juan, Puerto Rico.

3 Departamento de Biologia, Universidade de Taubaté. CEP 12030-010.Taubaté, SP, Brazil.

4 Laboratório de CiênciasAmbientais, Centro de Biociências e Biotecnologia, UniversidadeEstadual do NorteFluminense Darcy Ribeiro. CEP 28013-602.Campos dos Goytacazes, RJ, Brazil.

*Corresponding author: [email protected]

Abstract. Population biology and behaviour of Iguana iguana were analysed on a restored freshwater wetland. The research was conducted throughout March and April of 2008, on an area measuring approximately 40,000m2 (4ha), where a habitat restoration project (using wetland and mangrove plant species) has been running since 2002. Research included an estimation of I. iguana population density in this area and behavioural observations at restored areas. A very high population density was encountered within the study area (ca. 32 animals/ha; 109 animals/km), although animals were not observed in the restored areas much of the time. Observed activities of I. iguana on in the restored areas comprised basking (the most common observation), foraging, locomotion and displaying behaviours. Plant species consumed during foraging activities were not the same as those used in the restoration process; however, we recommend a constant monitoring of this population throughout other periods of the year to determine whether population control measures are required.

Keywords. Animal behaviour, population density, species introduction, habitat restoration.

Figure 1. Research area and observation points. S1, S2, S3, S4, S5 and S6 show observation points used for population density estimates; B1 and B2 show observation points used for behavioural study. Red line delineates extent of the research area. White lines delineate the restoration areas.

Caio A. Figueiredo-de-Andrade et al. 446

long spines on its back and tail, a large globular plate under the tympanums, and a double chin skirted with small spines on the front border. The body colour may range from green to reddish or dark grey, sometimes with dark vertical bands distributed along the body and tail. These lizards can be encountered on trees as well as on the ground, and can swim with great agility (Rivero, 1998).

Iguana iguana, or the Green Iguana, as it is known around the world, displays accentuated sexual dimorphism as an adult, and has a diurnal activity period. These animals are generalist herbivores, foraging on leaves, shoots, flowers and fruits (Distel and Veasey, 1982; FAO/PNUMA, 1993; Gusmán-Ramirez, 2007). Although primarily vegetarian, the species may also forage on animal matter (Rivero, 1998; Lara-López and González-Romero, 2002).

Iguana guana is native to tropical and subtropical regions of the Americas, including Mexico, Brazil and Paraguay (Burghardt and Rand, 1982). The species also occurs naturally on some islands near to the American continent (e.g. Cozumel, Utila, Roatán, Guanaja, Corn, Providencia, San Andres and Aruba) and has been introduced to some Caribbean islands (Burghardt and Rand, 1982; FAO/PNUMA, 1993). Green Iguanas are restricted to regions of low altitude, occurring no higher than 1,000 metres above sea level (FAO/PNUMA, 1993).

In Puerto Rico, the species has appeared at numerous sites during recent years. According to Rivero (1998),

the first animals were probably escaped pets, since a large number of young animals are frequently imported for this purpose. Currently the species is well distributed across the island group, with large colonies on Culebra Island, the coastal regions of mainland Puerto Rico (particularly in ‘Las Cabezas de San Juan’), and in the zoo in Mayagüez (Rivero, 2006). According to the Global Invasive Species Database (2008), the Green Iguana is considered an exotic pest in both Puerto Rico and Florida. In the latter, the species is known to use the burrows of the owl Athene cunicularia floridana, to disperse seeds of alien vegetal species, and is cited as a source of human salmonellosis. Furthermore, the species is cited as an airport runway hazard to some airport operations in Puerto Rico (Engeman, Smith and Constantin, 2005).

A few studies have focused on the ecology of the Green Iguana and the environmental impacts of its introduction in Puerto Rico. Such work has focused on control strategies of I. iguana populations (Días-Maldonado, 2002), the role of these animals as runway hazards in airport operations (Engeman, Smith and Constantin, 2005), and the species’ impact in a wildlife refuge (Gusmán-Ramirez, 2007).

The present work aimed to analyse population and behavioural characteristics of I. iguana on a restored freshwater wetland in Puerto Rico, evaluate population density in the study area, and determine whether the animals are eating the plant species used in the restoration project.

Adult males

Animals possessing large spines and large double chin; mandible muscles well developed; reddish body colouration on all or part of the body.Adult females

Animals possessing small spines and small double chin; mandible muscles not well developed; grey or greenish body colouration.Sub-adults

Animals possessing small spines and small double chin; mandible muscles not developed, green body colouration; estimated total length lesser than 1 metre.

Table 1. Criteria used in the classification of sampled Iguana iguana individuals into different size classes.

Table 2. Description of Iguana iguana behaviour categories used for classification.

Active behaviours Locomotion: Walking or running a distance more than 0.5m. Displaying: Exhibitions when there is not any other iguana within close sight. Foraging: Acquiring and consuming leaves, including locomotion and rest periods shorter than 15 seconds.

Inactive behaviours Basking: Any inactivity stance, with more than 75% of the body under sunlight.

Biology of introduced Iguana iguana in Puerto Rico 447

Figure 2. Mean density of each Iguana iguana size category at each of the six observation points.

Figure 3. Total population density and population density of each size class across the whole study area.


Figure 4. Observed behaviours of Iguana iguana across both of the sampled restoration areas.

Treatment Mean SE

Males (S1) 2.83 0.54

Males (S2) 0.67 0.21

Males (S3) 1.50 0.50

Males (S4) 1.17 0.31

Males (S5) 1.67 0.49

Males (S6) 4.17 0.95

Females (S1) 5.17 1.19

Females (S2) 1.17 0.40

Females (S3) 2.50 0.43

Females (S4) 1.83 0.70

Females (S5) 1.00 0.26

Females (S6) 3.00 0.86

Sub-adults (S1) 3.83 0.91






Table 3. Iguana iguana density records (mean number of animals and Standard Error) by size class and site, during 6 sampling days (9 hours of observation).

Material and Methods

Study areaFieldwork was conducted throughout the months of March and April 2008, in an area measuring ca. 40,000 m2 (4 ha) that was previously donated to the Universidad Metropolitana (UMET). This area is part of a larger wetland complex known as ‘Ciénaga Las Cucharillas’ (18º26’40”N and 66º9’17”W), which belongs to the townships of Bayamón, Cataño, Guaynabo and Toa Baja, since it is a part of the San Juan’s Bay (Fig. 1). This region is characterised by a vegetation community composed of mangrove and freshwater swamp species. It supports high biological and ecological diversity, and is located on the past watercourse of the Bayamón’s River (Morales-Agrinzoni, pers. comm.).A habitat restoration process using mangrove and wetland plant species (Pterocarpus officinallis, Annona glabara and Laguncu-laria racemosa) was being conducted in a part of the study area. This process was being conducted in two different areas since 2002 as a payment of a fine by two local companies (Morales-Agrinzoni, pers. comm.).

Sampling methodsOur research was composed of two parts: an evaluation of I. igu-ana population density in the study area and behavioural observa-tions of the species in the restoration areas.To evaluate population density, we applied an adapted point sam-pling method, selecting six observation points (each one ca. 50 m in length) in the study area (Fig. 1 – S1, S2, S3, S4, S5 and S6). There were no observable differences in habitat composition between the observation points that could potentially influence density estimates. The observations were made between 08:00h and 11:00h (the period of the day that animals bask in the sun, and the density count work becomes more effective). Each obser-vation point was checked vertically (only the vegetation’s cano-py was observed) for 15 minutes, and the number of animals at each point was counted. The lizards moved slowly on the trees, assuring that the same animals were not counted more than once in any given sample. Counted animals were grouped into three size classes (adult males, adult females and sub-adults), as shown in Table 1. The total period of sampling was 6 days (with an in-terval of 7 days between each sample day), totalling 9 hours of observation.To make the behavioural observations, a central observation point was chosen within each restoration area (Fig. 1 – B1 and B2), and observations made between 08:00h and 16:00h. Area B1 was ca. 1,000 m2 (0.1 ha), while area B2 was ca. 2,700 m2 (0.27 ha). Ob-servation periods were at intervals of 20 minutes, checking half of each restoration area for ten minutes and then the other half (for another ten minutes) within each time interval. Disruption of nor-mal iguana behaviour was avoided by using a barrier made of tree branches. Whenever an animal was detected in the sampling are-as, its behaviour was classified as either inactive (basking beha-viour) or active (locomotion, foraging or displaying behaviours). Behaviour category descriptions are given in Table 2. The total period of sampling was 4 days (with an interval of 7 days between each sample day), totalling 32 hours of observation.The plant species observed being consumed during foraging were collected and stored in paper bags for later identification in the

laboratory. The equipment used during field sampling included field tables, 10x50 binoculars and a stopwatch.

Data analysisWe calculated mean iguana density for each observation point using combined data from the six observation days. The same process was applied to obtain densities of males, females and sub-adults for each observation point.A two-way ANOVA (Zar, 1998) was used to identify significant differences in iguana distribution and point density of males, females and sub-adults between the six observation points. Tukey tests (Zar, 1998) were performed, using 95% confidence levels, to compare iguana densities by size class and site.Population density (number of animals/ha) was calculated by dividing the total estimated density of animals by the overall size of the study area (4 ha). To obtain the population density in animals/km, the total density of the species was divided by total length of the observation points (0.294 km).Proportions of animals’ presences for each restoration area were obtained by dividing the number of hours where the animals were present on the restoration areas by total observation hours. This parameter was calculated for both restoration areas individually, and com-bined. Proportions of observed behaviours were calculated by dividing the total hours of each behaviour class by the number of hours during which the animals were present in the sampling areas.Plant species consumed by animals during foraging were identified to family level.

Results

The density of iguanas recorded differed among size classes (F2, 107= 10.83; P< 0.001) and among sites (F5, 107= 12.69; P< 0.001) (see also Table 3). We also detected an interaction between both variables (F7,

107= 3.03; P< 0.001) (Fig. 2). Results of Tukey tests (comparing iguana densities by size class and site) are given in Table 4.

The distribution of the three animal size classes also differed between observation points. The density of adult males was higher at S6, whereas the densities of adult females and sub-adults were higher at S1 (Tables 3 and 4). No sub-adults were observed at observation points S4 and S6 (Fig. 2).

We observed a mean population density of 32.33 animals/ha, of which 12 were adult males, 14.66 were adult females and 5.66 were sub-adults (Fig. 3). We found 32 animals along 0.294 km (total length of observation points), giving a population density of ca. 109 animals/km (approximately one animal every ten metres).

Green Iguanas were not observed in the restoration areas much of the time (absent during ca. 74% of total observation hours). Area B1 had a higher percentage presence of I. iguana (present during ca. 41% of total observation hours) than area B2 (present during ca.


11% of total observation hours). Basking, foraging, locomotion and displaying behaviours were observed at B1, while only basking and locomotory behaviours were observed at B2.

Observed behaviours at both areas combined predominantly comprised basking, followed by foraging, locomotion and displaying behaviours (Fig. 4).

The plant species observed being consumed during foraging behaviour were identified as members of the families Cyperaceae, Gramineae and Leguminosae. Apart from these plants, iguanas were also observed consuming leaves from three aquatic plants that could not be identified.

Discussion

The higher population density observed at point S1 can be explained by the occurrence of a high number of sub-adults at this specific point compared with other observation points.

During our study, no differences in habitat between observation points that could influence animals’ distribution were observed. However, adult Green Iguana males are known to defend their home ranges, and permit only adult females within their territory (Dugan, 1982). The larger males were located at observation points S4 and S6, providing a probable reason for the absence of sub-adults at these points. The sub-adults appear to have been displaced to areas located to the north of the

study area (away from territories of the larger males), increasing the density at observation point S1.

The population density found in this study is very high when compared with research data from Brazil (Campos, 2003) and Colombia (Muñoz, Ortega and Bock, 2003), where the Green Iguana is a native species. These works reported density values of 5.5 animals/km (Campos, 2003) and 1.5-13.7 animals/ha (Muñoz, Ortega and Bock, 2003). Data comparison shows a population density in our study area almost 20 times larger than the values reported for Brazil and from 2.3 up to 21.5 times larger than the values reported for Colombia. A comparison of our data with those collected in Florida (Smith, Golden and MeshakaJr, 2007), where there are introduced populations of the Green Iguana, suggested a population density in our study area almost five times larger than that observed in Florida.

Green Iguanas spend ca. 96% of the day inactive and only 1% of the day foraging (Dugan, 1982). This tendency is supported by the respective percentages of observed behaviours within our study site, where a large proportion of inactive behaviour was observed.

Basking, locomotion, foraging and displaying behaviours were all observed at area B1. Foraging and displaying behaviours were not observed at area B2, possibly because this area was more flooded than B1, providing less vegetation on the ground, which was used by the animals for foraging in area B1. Since foraging was not possible in B2, it is possible that animals


S (S1) S (S2) S (S3)

S (S4)

S (S5) S (S6) M

(S1)M

(S2)M

(S3)M

(S4)M

(S5) M (S6) F (S1)

F (S2)

F (S3)

F (S4) F (S5) F

(S6)

S (S1) -

S (S2) 0.07 -

S (S3) 0.00 1.00 -

S (S4) 0.00 1.00 1.00 -

S (S5) 0.02 1.00 1.00 1.00 -

S (S6) 0.00 1.00 1.00 1.00 1.00 -

M (S1) 1.00 0.71 0.11 0.07 0.42 0.07 -

M (S2) 0.02 1.00 1.00 1.00 1.00 1.00 0.42 -

M (S3) 0.29 1.00 0.97 0.92 1.00 0.92 0.97 1.00 -

M (S4) 0.11 1.00 1.00 0.99 1.00 0.99 0.83 1.00 1.00 -

M (S5) 0.42 1.00 0.92 0.83 1.00 0.83 0.99 1.00 1.00 1.00 -

M (S6) 1.00 0.02 0.00 0.00 0.01 0.00 0.97 0.01 0.11 0.04 0.19 -

F (S1) 0.97 0.00 0.00 0.00 0.00 0.00 0.29 0.00 0.00 0.00 0.01 1.00 -

F (S2) 0.11 1.00 1.00 0.99 1.00 0.99 0.83 1.00 1.00 1.00 1.00 0.04 0.00 -

F (S3) 0.97 0.92 0.29 0.19 0.71 0.19 1.00 0.71 1.00 0.97 1.00 0.83 0.11 0.97 -

F (S4) 0.56 1.00 0.83 0.71 0.99 0.71 1.00 0.99 1.00 1.00 1.00 0.29 0.01 1.00 1.00 -

F (S5) 0.07 1.00 1.00 1.00 1.00 1.00 0.71 1.00 1.00 1.00 1.00 0.02 0.00 1.00 0.92 1.00 -

F (S6) 1.00 0.56 0.07 0.04 0.29 0.04 1.00 0.29 0.92 0.71 0.97 0.99 0.42 0.71 1.00 0.99 0.56 -

Table 4. Results of Tukey tests (P-values) comparing Iguana iguana records by size class and site. M= Males; F= Females; S= Sub-adults. P-values in bold are < 0.05.

would not defend this area, nor perform displaying behaviours.

The foraging preference of iguanas on those plant types observed, is probably associated with the lower levels of lignin and other defence components in their leaves (Lara-López and González-Romero, 2002), compared with other available groups. Although this hypothesis is suggested by Lara-López and González-Romero (2002), we did not confirm that the plant species eaten by iguanas in the present study had less lignin than the species used in the restoration process.

Gusmán-Ramirez (2007) reported feeding of I. iguana on P. officinallis, A. glabara and L. racemosa (plants used in the restoration process). However, these plant species were not observed being consumed by iguanas in this study, suggesting that the species was not interfering with the restoration process. It should be borne in mind, however, that our data were collected during the egg-laying period, which occurs between February and March (Dugan, 1982). During this phase, an appetite decrease in both male and female I. iguana individuals is thought to occur; while females often show a period of anorexia during gestation, males spend a greater proportion of time displaying and defending territories (López-Briones, 1993).

We recommend a constant monitoring effort of this population throughout other periods of the year, and the formation of a careful, pre-emptive management plan to control this population, should such actions be required. We would also like to suggest that the prohibition of the free commerce of exotic species as pets (such as I. iguana) is a good solution to avoid the problems caused by species introductions to natural ecosystems.

Acknowledgements.We thank Angel A. García, Juan P. Alvarez, Mariana C. Leon-Perez and Shakira Osorio for helping on transport and data collection on fieldworks. Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES) by financing the research, Universidad Metropolitana (UMET) and Bacardi Co. by all legal permissions obtained to the research’s execution. The manuscript was greatly improved due to comments of Jamie Carr and an anonymous reviewer.

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