Green Iguanas (Iguana iguana) in Puerto Rico: is it time for management?

Iguana iguana is native to Central and South America, and was introduced into Puerto Rico in the 1970s as a result of pet trade. The invasive biology of this reptile has not been studied in Puerto Rico, where its negative effects may threaten local biodiversity. The purposes of this study were to: (1) estimate population densities of I. iguana; (2) describe some aspects of its reproductive biology; and (3) assess its potential impacts. Visual-encounter surveys were performed at Parque Lineal in San Juan and Canal Blasina in Carolina, while nesting activity data were collected at Las Cabezas de San Juan in Fajardo. Densities of I. iguana in Puerto Rico reached a maximum of 223 individuals ha⁻¹, higher than in any known locality in its native range, and showed fluctuations related to seasonality. Our 2008–2009 observations at the nesting sites document that this population of I. iguana is a reproductively successful species, producing more than 100 egg clutches and 2,558 eggs with a 91.4% egg viability. The ability to proliferate in a low predation environment and the absence of good competitors are the major drivers of the population densities observed in Puerto Rico. We found evidence that I. iguana is threatening native biodiversity and impacting infrastructure, agriculture and human safety. Thus, a management program to control the species must soon be developed to prevent this invasive reptile from becoming more widespread and dominant in other localities around the island.     

Does mating behaviour affect connectivity in marine fishes? Comparative population genetics of two protogynous groupers (Family Serranidae)

Pelagic larval duration (PLD) has been hypothesized to be the primary predictor of connectivity in marine fishes; however, few studies have examined the effects that adult reproductive behaviour may have on realized dispersal. We assessed gene flow (connectivity) by documenting variation in microsatellites and mitochondrial DNA sequences in two protogynous species of groupers, the aggregate spawning red hind, Epinephelus guttatus, and the single‐male, harem‐spawning coney, Cephalopholis fulva, to ask whether reproductive strategy affects connectivity. Samples of both species were obtained from waters off three islands (Puerto Rico, St. Thomas and St. Croix) in the Caribbean Sea. Despite the notion that aggregate spawning of red hind may facilitate larval retention, stronger signals of population structure were detected in the harem‐spawning coney. Heterogeneity and/or inferred barriers, based on microsatellites, involved St. Croix (red hind and coney) and the west coast of Puerto Rico (coney). Heterogeneity and/or inferred barriers, based on mitochondrial DNA, involved St. Croix (coney only). Genetic divergence in both species was stronger for microsatellites than for mitochondrial DNA, suggesting sex‐biased dispersal in both species. Long‐term migration rates, based on microsatellites, indicated asymmetric gene flow for both species in the same direction as mean surface currents in the region. Red hind had higher levels of variation in microsatellites and lower levels of variation in mitochondrial DNA. Long‐term effective size and effective number of breeders were greater for red hind; estimates of θ_f, a proxy for long‐term effective female size, were the same in both species. Patterns of gene flow in both species appear to stem in part from shared aspects of larval and adult biology, local bathymetry and surface current patterns. Differences in connectivity and levels of genetic variation between the species, however, likely stem from differences in behaviour related to reproductive strategy.     

Origin of the green iguana (Iguana iguana) invasion in the greater Caribbean Region and Fiji

Invasive populations of green iguanas (Iguanidae: Iguana iguana) are widely established beyond their native Central, South American, and Lesser Antillean range in various islands of the Pacific, Florida USA, and in the Greater Caribbean Region. Although widespread, information about these invasions is scarce. Here we determine the origin of invasive populations of green iguanas in Puerto Rico, Fiji, The Caymans, Florida USA, The Dominican Republic, the US Virgin Islands (USVI) of St. Thomas and St. Croix, and a U.S.A pet store. We sampled 120 individuals from these locations and sequenced one mitochondrial (ND4) and two nuclear (PAC and NT3) loci. We also include a preliminary characterization of population structure throughout Puerto Rico using six microsatellite loci to genotype individuals across 10 sampling sites. Comparing the genealogical relationships of all our samples to published sequencing data from the native range, we found that sampled populations were largely a product of populations from Colombia and El Salvador; two countries with multiple, industrial-size pet iguana farming operations. Notably, we found that haplotypes detected exclusively in the USVI and Puerto Rico’s outlying island of Vieques are closely linked to green iguanas native to Saba and Montserrat (Lesser Antilles); a clade not reported in the pet trade. Our population genetic analyses did not reveal isolation among sampling sites in Puerto Rico, rather the evidence supported admixture across the island. This study highlights the roles of the pet trade and lack of regulation in the spread of green iguanas beyond their native range.

     

Genetic analysis of a novel invasion of Puerto Rico by an exotic constricting snake

The tropical island Puerto Rico is potentially vulnerable to invasion by some species of exotic snakes; however, until now no established populations had been reported. Here we report and genetically characterize the nascent invasion of Puerto Rico by an exotic constricting snake of the family Boidae (Boa constrictor) using mtDNA and microsatellite data. Over 150 individual B. constrictor have been removed from Mayagüez municipality since May 2011, and our results from the genetic analysis of 32 individuals suggest that this population was recently founded by individuals of one subspecies from a genetic lineage common to zoo and breeding collections, but that the potential propagule pool consists of two subspecies. We also suggest that anthropogenic long-distance dispersal within the island of Puerto Rico may be occurring from the established population, with implications for further establishment across the island. This study represents the first report of the naturalization of an invasive species of boid snake in Puerto Rico and will be important in determining mitigation strategies for this invasion as well as providing a basis for comparison to other on-going studies of invasive snakes.     

Conservation status assessment of the Sharp‐shinned Hawk,an endangered insular raptor in Puerto Rico

Sharp‐shinned Hawks (Accipiter striatus) are forest raptors that are widely distributed in the Americas. A subspecies endemic to Puerto Rico (A. s. venator) is listed as endangered and restricted to mature and old secondary montane forests and shade coffee plantations. However, recent information about the population status and distribution of Puerto Rican Sharp‐shinned Hawks is lacking. We developed a spatial geographic distribution model for Sharp‐shinned Hawks in Puerto Rico from 33 locations collected during four breeding seasons (2013–2016) using biologically relevant landscape variables (aspect, canopy closure, elevation, rainfall, slope, and terrain roughness). Elevation accounted for 89.8% of the model fit and predicted that the greatest probability of occurrence of Sharp‐shinned Hawks in Puerto Rico (> 60%) was at elevations above 900 m. Based on our model, an estimated 56.1 km² of habitat exists in Puerto Rico with a high probability of occurrence. This total represents ~0.6% of the island's area. Public lands included 43.8% of habitat with high probability of occurrence (24.6 km²), 96% of which was located within four protected areas. Our results suggest that Sharp‐shinned Hawks are rare in Puerto Rico and restricted to the higher elevations of the Cordillera Central. Additional research is needed to identify and address ecological limiting factors, and recovery actions are needed to avoid the extinction of this endemic island raptor.     

Oeceoclades maculata, an alien tropical orchid in a Caribbean rainforest

Background and Aims

Undisturbed forest habitat can be relatively impenetrable to invasive, non-native species. Orchids are not commonly regarded as invasive, but some species have become invasive and these generally depend on habitat disturbance. One of the most aggressive orchids is Oeceoclades maculata, a terrestrial species with remarkable ecological amplitude. Originally from tropical Africa, it is now widespread in the neotropics. By associating its local distribution with land-use history and habitat characteristics, it was determined whether O. maculata is dependent on habitat disturbance. It was also investigated whether this exotic orchid occupies the same habitat space as two sympatric native species.

Methods

Six 10 m × 500 m transects were censused in June 2007 on the 16-ha Luquillo Forest Dynamics Plot, located in the Luquillo Mountains, Puerto Rico. The plot had been mapped for historical land use, topography and soil type.

Key Results

Oeceoclades maculata was the most abundant of three orchid species surveyed and was found in all four historical cover classes. In cover class 3 (50–80 % forest cover in 1936), 192 of 343 plants were found at a density of 0·48 plants per 5 × 5 m subplot. Over 93 % of the 1200 subplots surveyed were composed of Zarzal or Cristal soil types, and O. maculata was nearly evenly distributed in both. The orchid was most common on relatively flat terrain. The distribution and abundance of two sympatric orchid species were negatively associated with that of the invasive species.

Conclusions

Oeceoclades maculata does penetrate ‘old growth’ forest but is most abundant in areas with moderate levels of past disturbance. Soil type makes little difference, but slope of terrain can be important. The negative association between O. maculata and native species may reflect differences in habitat requirements or a negative interaction perhaps at the mycorrhizal level.Key words: Oeceoclades maculata, Wullschlaegelia calcarata, Prescottia stachyodes, Orchidaceae, land-use history, tropical forest disturbance, terrestrial orchids, invasive species, Luquillo Experimental Forest, Puerto Rico, forest recovery, Caribbean     

Pollination biology in an endangered rocky mountain toadflax (Linaria cavanillesii)

Knowledge about the reproductive system of species inhabiting rocky habitats is scarce. The reproductive biology (floral biology, experimental pollination, insect visits, inbreeding depression, and seed predation) of the rupicolous Linaria cavanillesii was analyzed under field and experimental conditions. Self-compatibility was revealed by the high fruit set, seed set, and seed mass in the pollination experiment. Furthermore, results disclose that this species does not need insect visitors for seed production since fruit set after autonomous self-pollination was similar to that by hand cross-pollination. Self-offsprings were not affected by a strong degree of inbreeding depression in early life-cycle stages. Seed predation by Cucurlionidae is the main limiting factor of fruit and seed production in this species. Contrary to other perennial species of Linaria previously studied, L. cavanillesii represents the first clear report of self-fertility.     

Colonization history and genetic diversity: adaptive potential in early stage invasions

The introduction of Anolis cristatellus from the multiple species anole community of Puerto Rico in the Greater Antilles to the island of Dominica in the Lesser Antilles, with its solitary endemic anole, provides an example of a very recent, timed, single colonization. We investigate the geographic origin and adaptive potential of the Dominican population using a range of methods including mtDNA phylogeography, nuclear microsatellite variation and multiple paternity studies, as well as heritability estimates, common garden experiments and comparative geographic studies of quantitative scalation traits. Phylogeographic analysis of NADH2 and microsatellite studies suggests that the Dominican population arose from a set of individuals from the central west area of Puerto Rico within their endemic range. The multiple‐individual inoculation, together with sperm storage and evidence of multiple paternity indicate genetic variability and suggest the potential for adaptation by natural selection. Estimates of heritability, common garden experiments and broad sense Q_ST/F_ST ratios, linked to replicated comparisons along elevational transects go some way to suggesting that the invasive populations may be adapting by natural selection, in parallel with the endemic anole, in the brief period since their introduction.     

Morphological flexibility across an environmental gradient in the epiphytic orchid,Tolumnia variegata: complicating patterns of fitness

Deceit‐pollinated orchid species show substantial variation in floral traits, which may be maintained by genetic drift or various forms of selection, or may reflect phenotypic plasticity. We explored how much plasticity occurs in both vegetative and floral traits of Tolumnia variegata (Oncidiinae, Orchidaceae) across two different light environments in Puerto Rico using data from a reciprocal transplant experiment. We also examined how fruit set, a measure of reproductive success and a surrogate for fitness, is associated with this morphological variation, and whether it changes over time. Tolumnia variegata responded to environmental variables in multiple ways. Vegetative characters were more plastic than those associated with sexual reproduction. Transplant effects accounted for significant variation in flower length, lip length, number of inflorescences, peduncle length, leaf length and the total number of ramets, but responses were not always consistent among years. Phenotypic selection on morphological characters was dependent on plant location. The trends detected were complex, and often inconsistent across years, probably as a result of wetter and drier years than average. Overall fruit set was quite variable among plants, averaging 15%, with no significant differences among sun and shade plants. Although reproductive success was similar among sites, habitat heterogeneity and annual variation had an effect on morphological expression, which sometimes modified the trajectories of phenotypic selection. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163 , 431–446.     

Colonization history and population differentiation of the Honey Bees (Apis mellifera L.) in Puerto Rico

Honey bees (Apis mellifera L.) are the primary commercial pollinators across the world. The subspecies A. m. scutellata originated in Africa and was introduced to the Americas in 1956. For the last 60 years, it hybridized successfully with European subspecies, previous residents in the area. The result of this hybridization was called Africanized honey bee (AHB). AHB has spread since then, arriving to Puerto Rico (PR) in 1994. The honey bee population on the island acquired a mosaic of features from AHB or the European honey bee (EHB). AHB in Puerto Rico shows a major distinctive characteristic, docile behavior, and is called gentle Africanized honey bees (gAHB). We used 917 SNPs to examine the population structure, genetic differentiation, origin, and history of range expansion and colonization of gAHB in PR. We compared gAHB to populations that span the current distribution of A. mellifera worldwide. The gAHB population is shown to be a single population that differs genetically from the examined populations of AHB. Texas and PR groups are the closest genetically. Our results support the hypothesis that the Texas AHB population is the source of gAHB in Puerto Rico.     

Reproductive biology of Trichocentrum pumilum: an orchid pollinated by oil-collecting bees

The reproductive biology, reward production and pollination mechanism of Trichocentrum pumilum were studied in a gallery forest in the interior of the State of São Paulo, southeast Brazil. The floral visitors and pollination mechanism were recorded, and experimental pollinations were carried out in order to determine the breeding system of this species. Trichocentrum pumilum blooms in spring. Each paniculate inflorescence bears an average of 85 flowers that present a central yellow callus and finger‐like trichomes on the lateral lobes of the lip. A lipoidal substance is produced and stored among these trichomes. In the studied population, T. pumilum is exclusively visited and pollinated by two bee species (Tetrapedia diversipes and Lophopedia nigrispinis). Pollinaria are deposited on mouthparts of bees during collection of the lipoidal substance from the lateral lobes of the labellum. Trichocentrum pumilum is self‐incompatible and pollinator‐limited. Natural fruit set was low (9%, compared to 45% in experimentally cross‐pollinated flowers). Potentially viable seed exceed 97% in fruits obtained through cross‐pollination and in natural conditions (open pollination).     

The influence of spatial scale on the genetic structure of a widespread tropical wetland tree, Pterocarpus officinalis (Fabaceae)

Identifying factors that cause genetic differentiation in plant populations and the spatial scale at which genetic structuring can be detected will help to understand plant population dynamics and identify conservation units. In this study, we determined the genetic structure and diversity of Pterocarpus officinalis, a widespread tropical wetland tree, at three spatial scales: (1) drainage basin “watershed” (<10 km), (2) within Puerto Rico (<100 km), and (3) Caribbean-wide (>1000 km) using AFLP. At all three spatial scales, most of the genetic variation occurred within populations, but as the spatial scale increased from the watershed to the Caribbean region, there was an increase in the among population variation (Φ_ST=0.19 to Φ_ST=0.53). At the watershed scale, there was no significant differentiation (P=0.77) among populations in the different watersheds, although there was some evidence that montane and coastal populations differed (P<0.01). At the island scale, there was significant differentiation (P<0.001) among four populations in Puerto Rico. At the regional scale (>1000 km), we found significant differentiation (P<0.001) between island and continental populations in the Caribbean region, which we attributed to factors associated with the colonization history of P. officinalis in the Neotropics. Given that genetic structure can occur from local to regional spatial scales, it is critical that conservation recommendations be based on genetic information collected at the appropriate spatial scale.     

Reproductive biology of Lactoris fernandeziana (Lactoridaceae)

Lactoris fernandeziana, monotypic in its family, is endemic to the cloud forests of Robinson Crusoe Island. Although there has been considerable study of the relationships of Lactoris, as a rare species and as a putative primitive paleoherb, little is known of its reproductive biology. Knowledge of the latter is essential for effective conservation programs. The species is gynomonoecious. The overall proportion of flowers is ∼1 female:1 hermaphrodite. The inconspicuous semipendulous green flowers, usually in mixed-gender inflorescences, do not produce rewards. Hermaphrodite flowers are herkogamous and protogynous. Pollen grains are shed from the extrorse anthers in permanent dry tetrads. There is a mean of 12879 tetrads per hermaphrodite flower. Both flower types bear an average of ∼18 ovules. The P/O (pollen/ovule) ratios imply facultative or obligate xenogamy, but hand pollinations show that Lactoris is self-compatible. No floral visitors were ever observed, but stigmata of open-pollinated flowers bore tetrads, and 64% of such styles had pollen tubes. Flowers enclosed in large mesh (1 mm) bags bore similar numbers of tetrads and pollen tubes. Thus, we conclude that Lactoris is anemophilous, a syndrome perhaps reflected by the P/O ratio. Low genetic diversity (isozymes and DNA) supports selfing and implies limited distance wind pollen dispersal. The small size of the island, the ± 1000 extant Lactoris plants, coupled with anemophily, self-compatibility, and pendant flower position, have yielded a geitonogamous system with high seed set and low genetic diversity. If inbreeding depression is expressed, it is in seed germination and seedling vigor, for Lactoris is very difficult to cultivate. For this species, effective conservation practices need to focus on habitat preservation and promotion of outcrossing.     

Parasites of free-ranging Cayo Santiago macaques after 46 years of isolation

Three hundred and thirty seven Macaca mulatta from a population that had been isolated on a small island off the coast of Puerto Rico for 46 years were examined for parasites. Anatrichosoma cynamolgi (26%), Strongyloides fuelleborni (54%); Trichuris trichiura (23%); and Balantidium coli (2%) were detected. Toxoplasma antibodies were found in 10% of the sera examined. Milk was examined for Stronglyloides, and blood was examined for microfilariae and protozoa, but no parasites were found in these specimens. The animals in this colony harbored intestinal parasites but were in excellent physical condition, with a high reproductive rate and a low mortality rate. It is concluded that the presence of intestinal and tissue parasites has little measurable effect on the overall health of rhesus in this free-ranging environment.     

Reproductive success of Mariana Swiftlets (Aerodramus bartschi) on the Hawaiian island of O'ahu

Mariana Swiftlets (Aerodramus bartschi) are federally listed as endangered, with populations currently limited to just three islands in the Mariana Islands plus an introduced population on the Hawaiian island of O'ahu. Before efforts are made to reintroduce Mariana Swiftlets to other islands in the Mariana archipelago, additional information is needed concerning their breeding biology. Therefore, our objective was to examine the reproductive biology of Mariana Swiftlets over five annual cycles on the Hawaiian island of O'ahu. This introduced population used a human‐made tunnel for roosting and nesting, and was studied as a surrogate to negate interference with endangered populations in the Mariana Islands. Active nests (N = 478) were observed in every month of the year, with peak nesting activity between May and September. All clutches consisted of one egg. Mean duration of incubation and nestling periods were 23.9 d (range = 18–30 d, N = 233) and 55.0 d (range = 41–84 d, N = 228), respectively. Estimated nest success was 63%. Over half (52%) of nest failures were attributed to eggs found on the tunnel floor. Predation by rats (Rattus spp.) was also an important cause of nest failure and often resulted in the loss of most active nests. However, Mariana Swiftlets did re‐nest after these predation events. Our results suggest that rat predation of both nests and adults may limit growth of the Mariana Swiftlet population on O'ahu, and could also affect the chances for successful establishment of relocated populations in the Mariana Islands. Another limiting factor on O'ahu is that only one nesting site is apparently available on the island. Current goals for downlisting Mariana Swiftlets from endangered to threatened include establishing populations on Guam, Rota, Aguiguan, and Saipan. To meet these goals, the population of Mariana Swiftlets on O'ahu can be important for testing reintroduction techniques, learning more about the natural history of these swiftlets, and providing individuals for reintroduction efforts in the Mariana Islands.     

The effects of a rust infection on fitness components in a natural population of Tolumnia variegata (Orchidaceae)

The effects of a rust infection (Sphenosphora saphena, Basidiomycetes) on several fitness components of the orchid Tolumnia (Oncidium) variegata were quantified in a subtropical moist forest of Puerto Rico. Infected and uninfected plants of two size categories were observed and manipulated by increasing natural levels of fruit production to determine the effects of infection on short and long-term sexual reproduction, subsequent vegetative and reproductive growth, and mortality. Under artificially high levels of fruit production, infection had no effect on short or long-term reproduction through male or female function except for a modest decline in seed viability in small plants. Under natural levels of fruit production, infection was only related to a reduction in the number of leaves per shoot. At artificially high levels of fruit production, infection reduced leaf length, leaf width, and the number of live shoots. Survival was not associated with rust occurrence. The rust appears to have minor ecological impact on this orchid population.     

Breeding system and thrips (Thysanoptera) pollination in the endangered tree Ocotea porosa (Lauraceae): implications for conservation

Ocotea porosa has been extensively exploited over the past few decades because of the quality of its wood. Today, populations are reduced and the species is now included in the Red List of threatened species by the International Union for Nature Conservation. For conservation and management purposes, it is extremely important that we understand its reproductive ecology. Floral morphology was described based on field and scanning electron microscopic examination. The reproductive system was determined through experimentally controlled pollination along with observations of pollen tube growth. Pollinators were identified through field observations. Flowers of O. porosa are small, shallow, inconspicuous, asynchronous and grouped in inflorescences. This species presented self‐compatibility, but did not reproduce through apomixy and spontaneous self‐pollination was very rare (5%). Despite being monoclinal, flowers were protogynic, and the gynoecium was receptive after the first day of anthesis when the anthers were closed. Spontaneous self‐pollination was avoided by the extrorse position of the anthers of the internal stamens. Frankliniella gardeniae (Thysanoptera) was the only pollinating species observed and, after visiting several asynchronous flowers in the same inflorescence, favors geitonogamy. Together the small distance supposedly achieved by thrips in flight and the small population density of O. porosa can reduce the chances of cross‐pollination in this species. If so, conservation measures must include preservation of the current population and possibly planting to increase population density. This would reduce the distance between individuals and increase genetic variability. Thrips as pollinators must be included in conservation planning for O. porosa.     

Reproductive biology and conservation genetics of Goodyera procera (Orchidaceae)

Goodyera procera is an endangered terrestrial orchid in Hong Kong. Information on its reproductive biology and pattern of genetic variation is needed to develop efficient conservation strategies. Pollination experiments showed that the species is self-compatible, but dependent on pollinators for fruit set. Bagged plants produced no fruits. Artificial pollinations resulted in 92% fruit set through selfing, 94% with geitonogamous pollination, and 95% following xenogamous pollination. Fruit set in the open-pollinated control was 75% at the same sites. Allozyme electrophoresis and random amplified polymorphic DNA (RAPD) were used to evaluate genetic variation and structure of 15 populations of Goodyera procera. Despite its outbreeding system, allozyme data revealed low variation both at the population (P = 21.78%, A = 1.22, and H = 0.073) and species (P = 33%, A = 1.33, and H = 0.15) levels, in comparison with other animal-pollinated outbreeding plant species. However, RAPD variation was relatively high (P = 55.13% and H = 0.18 at the population level, and P = 97.03% and H = 0.29 at the species level). G_ST estimates indicated high levels of genetic differentiation among populations (G_ST = 0.52 and I = 0.909 ± 0.049 based on allozyme data, and G_ST = 0.39 and I = 0.859 ± 0.038 based on RAPD data), much above the average for outcrossing species, suggesting that gene flow was limited in this species. Based on these data, suitable strategies were developed for the genetic conservation and management of the species.     

Intestinal Parasites of the Free-Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatto)

Free-ranging rhesus macaques on the island of Cayo Santiago, Puerto Rico, were surveyed for intestinal parasites for the first time in over 40 years. Results were compared with the only previous study [10], and the relationships between the prevalence of Strongyloides and dominance rank, body weight, age, and matriline examined in the sampled population.     

Evaluation of the eradication program forAmblyomma variegatum (Acari: Ixodidae) on Puerto Rico

A cooperative effort between the United States Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, the Agricultural Research Service, and the Department of Agriculture, Commonwealth Government of Puerto Rico has been successful in eardicatingAmblyomma variegatum (Fabricius) from the islands of Puerto Rico and Vieques (an island municipality of Puerto Rico). Application of acaricides to livestock and dogs at 14-day intervals for an 18-month period eliminated foci of tick infestation on 188 farms in four different locations without additional aerial or ground treatment. Reasons for the success and some of the costs associated with the eradication program on Puerto Rico are presented.