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HTTPS://JOURNALS.KU.EDU/REPTILESANDAMPHIBIANSTABLE OF CONTENTS IRCF & AMPHIBIANSREPTILES • VOL &15, AMPHIBIANS NO 4 • DEC 2008 • 27(3):382–389189 • DEC 2020

IRCF REPTILES & AMPHIBIANS CONSERVATION AND NATURAL HISTORY

TABLE OF CONTENTS

MitesFEATURE ARTICLES (Geckobia hemidactyli, Actinedida: . Chasing Bullsnakes (Pituophis catenifer sayi) in Wisconsin: Pterygosomatidae)On the Road to Understanding the Ecology and Conservation in Tropicalof the Midwest’s Giant Serpent ...... House Joshua M. Kapfer 190 . The Shared History of Treeboas (Corallus grenadensis) and Humans on Grenada: A Hypothetical( Excursion ...... mabouia) in RobertCuba: W. Henderson 198 RESEARCH ARTICLES A .ReviewThe Texas Horned inwith Central and Western New Texas ...... Distribution Emily Henry, Jason Brewer, Krista Mougey, and Records Gad Perry 204 . The Knight Anole (Anolis equestris) in Florida ...... Brian J. Camposano, Kenneth L. Krysko, Kevin M. Enge, Ellen M. Donlan, and Michael Granatosky 212 Rafael Borroto-Páez1, Carlos C. Martínez-Rivera2, and Denise Reyes Pérez1 CONSERVATION ALERT 1Instituto de Geografía Tropical, Calle F entre 13 y 15, , La Habana, ([email protected], [email protected]) . World’s Mammals in Crisis ...... 2The Philadelphia Zoo, Philadelphia, Pennsylvania 19104, USA ...... 220 . More Than Mammals ...... 223 . The “Dow Jones Index” of ...... 225

HUSBANDRY he Tropical .HouseCaptive Care of the Central (Hemidactylus Netted Dragon ...... mabouia) is across Cuba and its satellite Shannon islands Plummer and 226 is particularly abun- Tthe most abundant of Cuba’s four introduced in dant in urban and rural areas (Borroto-Páez et al. 2015). It is the HemidactylusPROFILE. Hemidactylus mabouia is distributed considered invasive throughout the and in most . Kraig Adler: A Lifetime Promoting Herpetology ...... Michael L. Treglia 234

COMMENTARY . The Turtles Have Been Watching Me ...... Eric Gangloff 238

BOOK REVIEW . Threatened Amphibians of the World edited by S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R. Berridge, P. Ramani, and B.E. Young ...... Robert Powell 243

 CONSERVATION RESEARCH REPORTS: Summaries of Published Conservation Research Reports ...... 245  NATURAL HISTORY RESEARCH REPORTS: Summaries of Published Reports on Natural History ...... 247  NEWBRIEFS ...... 248  EDITORIAL INFORMATION ...... 251  FOCUS ON CONSERVATION: A Project You Can Support ...... 252

Front Cover. Shannon Plummer. Back Cover. Michael Kern Totat et velleseque audant mo Totat et velleseque audant mo estibus inveliquo velique rerchil estibus inveliquo velique rerchil erspienimus, quos accullabo. Ilibus erspienimus, quos accullabo. Ilibus aut dolor apicto invere pe dolum aut dolor apicto invere pe dolum fugiatis maionsequat eumque fugiatis maionsequat eumque moditia erere nonsedis ma sectiatur moditia erere nonsedis ma sectia- ma derrovitae voluptam, as quos tur ma derrovitae voluptam, as accullabo.

Fig. 1. Tropical House Geckos (Hemidactylus mabouia) infected with parasitic mites (Geckobia hemidactyli) collected in three localities in northern Cuba. (A) A gecko photographed on 10 June 2019 on a building in Víbora, Municipality of , (No. 2 on the map in Fig. 2) with a number of mites on its flank. (B and C) A gecko collected in January 2020 in an apartment in Corralillo, (No. 4 on the map) with mites in front of its eye, on its shoulder, and on its venter. (D) A gecko collected on 20 February 2020 in a house on Playa Rincón de Guanabo, (No. 3 on the map) with mites on the shoulder and forelimb. (E) A mite (Geckobia hemidactyli) embedded beneath a ventral scale of the gecko from Rincón de Guanabo. (F) A mite detached from the same host photographed through a microscope. Photographs by Rafael Borroto-Páez.

Copyright is held by the authors. Articles in R&A are made available under a 382 Reptiles & Amphibians ISSN 1098-6324 Creative Commons Attribution-NonCommercial 4.0 International license. BORROTO-PÁEZ ET AL. REPTILES & AMPHIBIANS • 27(3):382–389 • DEC 2020 of the tropical and subtropical climates it has colonized out- 2013) and in some turtles (Bauer et al. 1990). Twelve species side of its natural African range (Powell et al. 1998, 2011; of Geckobia have been recorded in the Americas. Of these, Weterings and Vetter 2018). three are considered exotic hitchhikers that arrived with inva- These invasive geckos can exert numerous direct and sive lizard hosts: Geckobia bataviensis (Vitzthum 1926) and indirect effects in the habitats they colonize through preda- G. keegani (Lawrence 1953) with Hemidactylus frenatus (Díaz tion and interference competition with native species (Rivero et al. 2020) and G. hemidactyli (Lawrence 1936) with H. 1978; Powell 2004; Meshaka 2001; Iturriaga and Marrero mabouia (Martínez Rivera et al. 2003). 2013; Borroto-Páez and Reyes Pérez 2019). In some cases, Geckobia hemidactyli is a common ectoparasite of they can be considered a nuisance by having a negative effect Hemidactylus mabouia and has been recorded from several on the human economy (Borroto-Páez and Reyes Pérez 2020) localities in the Western Hemisphere, suggesting that its entry and potentially by playing a role in the spread of dengue fever occurred with the introduction of its host. To date, the presence by preying on that act as a natural biological control of G. hemidactyli in the Americas has been found only on H. of Aedes mosquitoes (Weterrings et al. 2019). The establish- mabouia, and no other pterygosomatid mites have been iden- ment of invasives also can affect native species by spreading tified from live hosts (Martínez Rivera et al. 2003). Although non-native parasites and diseases (Murphy and Myers 1993; Martínez Rivera et al. (2003) reported finding Geckobia mites in Goldberg et al. 1998; Goldberg and Bursey 2000; Kraus museum specimens of H. frenatus, those mites were never keyed 2009; Dunn et al. 2012; Dunn and Hatcher 2015; Jiménez to species and the geckos came from areas where H. mabouia Quirós 2014; Weterings et al. 2019). is not present, and as such they should be treated as Geckobia Mites and ticks are vectors of several infectious diseases (e.g., sp. A first report confirmed the presence of these mites in the dermatitis and anemia) and can have a direct impact on the health Americas by visual inspection of live H. mabouia from Puerto of their native hosts (Fajfer, 2012) as well as serve as intermedi- Rico and by studying preserved specimens of H. mabouia from ary hosts to internal parasites (Norval et al. 2014). However, the several American localities deposited in the herpetology collec- effects that introduced ectoparasites hitchhiking on invasive spe- tion at the Natural History Museum of the University of Kansas cies could have on new native hosts has not been assessed effec- by one of the authors (Martínez-Rivera). In that study, mites tively in any of the areas invaded by their hosts (Kraus 2009). were found on H. mabouia collected from Puerto Rico (live More importantly, parasites often are key players in the invasion and museum specimens) and from museum specimens from process of their hosts; they can mediate the outcome and impact Antigua, Cuba (Guantanamo only), Culebra (Puerto Rico), of invasions or might themselves be invasive species (Dunn 2009; Dominica, Grenada, Guadeloupe, Isla de Mona (Puerto Rico), Tompkins et al. 2011), thus identifying their presence along with St. Eustatius, St. Lucia, Tortola (British Virgin Islands), Vieques the invasive host species is of utmost importance. (Puerto Rico), the U.S. Virgin Islands (St. Croix, St. John, St. Pterygosomatid mites, such as Geckobia spp., are ubiquitous Thomas, and other localities), Colombia, and northern Brazil in some populations of geckos in the genus Hemidactylus but are (Martínez Rivera et al. 2003). A second study confirmed its rarely reported when new localities of these invasive geckos are presence in the mainland United States (Corn et al. 2011). identified. At least two species of Geckobia have been reported As noted above, the only reports of Geckobia hemidactyli on Cuban but have not been widely or systematically in the Cuban Archipelago came from mites in a collection jar studied. The first record of Geckobia in Cuba was the descrip- of 20 Hemidactylus mabouia that had been collected at the U.S. tion of a new species (G. tarentolae) parasitizing the native Naval Base at Guantanamo Bay in southeastern Cuba between gecko Tarentola americana by de la Cruz (1973). The second 1965 and 1969 and deposited in a U.S. herpetological col- report documented the presence of G. hemidactyli on twenty lection (Martínez Rivera et al. 2003). Reports of G. hemidac- Tropical House Geckos collected at the U.S. Naval Station at tyli from live specimens of H. mabouia collected elsewhere in Guantanamo Bay (Martínez Rivera et al. 2003). Five species of Cuba or from specimens deposited in Cuban museums were pterygosomatid mites have been reported from Cuba (Paredes- absent until recently and are listed chronologically. León et al. 2013), but the most recent list of Cuban mites Our first observation of orange mites on a live H. mabouia (Torres and Cuervos 2019) did not include records in either de from Cuba was in June 2019 in a small yard in front of the la Cruz (1973) or Martínez Rivera et al. (2003). senior author’s (RBP) home in Víbora, La Habana Province. Within the family Pterygosomatidae, the genus Geckobia RBP took photographs of the gecko and only later noticed the Mégnin 1878 exhibits the widest geographic distribution presence of numerous groups of orange ectoparasites in the (Machado et al. 2019). It comprises 73 species that parasit- lateral view of the while curating the images (Fig. 1A). ize lizards of different families (, Phyllodactylidae, After this initial observation, we began paying attention to Carphodactylidae, , and Eublepharidae) in all house geckos detected in the region and reviewed the lim- the infraorder (Fajfer 2012; 2018) but also in liz- ited literature and anecdotal information available on ectopic ards in the family Liolaemidae (Fajfer and González Acuna mites reported on Cuban herpetofauna. A few days later, we

383 BORROTO-PÁEZ ET AL. REPTILES & AMPHIBIANS • 27(3):382–389 • DEC 2020

Fig. 2. Map of Cuba showing localities where mites (Geckobia hemidactyli) are known to infect Tropical House Geckos (Hemidactylus mabouia) or where geckos were free of mites. (1) Mites are known to infect geckos at the U.S. Naval Base at Guantanamo Bay (Martínez Rivera et al. 2003), which is marked by a blue dot. Red dots mark four new localities where we found mites infecting geckos: (2) Víbora, Municipality of Diez de Octubre, La Habana Province (23°05'19"N, 82°22'40"W); (3) Playa Rincón de Guanabo, Mayabeque Province (23°10'20.62"N, 82°05'48.29"W); (4) Corralillo region (family apart- ment and Elguear Hotel) of Villa Clara Province (22°58'48"N, 80°36'05"W); (5) Güines, Mayabeque Province. Yellow dots mark localities where geckos were free of mites: (6) Guanacahabibes Peninsula National Park, Pinar del Río Province; (7), Topes de Collantes National Park, Sancti Spiritus Province. observed another adult H. mabouia at the same locality with We randomly searched for geckos with mites in additional similar groups of orange ectoparasites. localities along the northern coast of Cuba and inspected any Subsequently, RBP reviewed his private collection and lizard with orange mites. We collected two adult male geckos selected all photographs of H. mabouia taken at multiple with Geckobia hemidactyli from two different localities, one locations since 2006. Geckos with G. hemidactyli were found in the town of Corralillo, in Villa Clara Province (January in four previous years and at one new locality, the town of 2020), a rural area located about 340 km east of Habana Corralillo. Mites were found in 2016 in Corralillo in the axilla (Figs. 1B–C), and one from Playa Rincón de Guanabo, in and on the sides of hosts, in 2017 at home (RBP) in the axillae, Mayabeque Province (February 2020) about 25 km east of in 2018 in the yard at home (RBP) on the shoulder of a gecko Habana (Fig. 1D). More recently, in May 2020, we collected shown in Borroto-Páez and Reyes Pérez (2019) but from an and released two H. mabouia in the apartment of RBP, a unpublished photograph, and in 2019 in Güines, Mayabeque female with six mites on the abdomen and legs, and a mite- Province, south of La Habana in a photograph taken at a free juvenile. All sampled locations are illustrated in Fig. 2. friend’s house. Photographs from 2006 and 2011–2015 do not In August 2020, we collected H. mabouia in the family show Geckobia mites in RBP’s home or at the Corralillo locali- apartment and in the Elguear Hotel, 7 km to the north, both ties, nor do photographs from 2018 from Guanahacabibes, in the Corralillo region of Villa Clara Province. In the family Pinar del Rio Province, in the extreme west of Cuba, and Topes apartment, 23 of 24 geckos had mites (prevalence 95.8%), de Collantes in Sancti Spiritus Province in central and southern with only one juvenile (SVL 33.2 mm) free of mites. In the Cuba. Given that most of the photographs depict dorsal views Elguear Hotel, where geckos were abundant, only three of 14 of geckos, sometimes showing a bit of the sides, a complete individuals collected (21.4%) had mites, but intensities were count of all mites present was not possible, especially as the very low (1, 2, and 2 mites). The distribution and abundance mites tend to preferentially congregate on the venter. Thus, the of mites on the bodies of the 26 infected geckos are provided photographic review is very likely flawed. in Table 1. Relationships (simple linear regression) between

Table 1. Distribution and abundance of pterygosomatid mites (Geckobia hemidactyli) on the bodies of 26 Tropical House Geckos (Hemidactylus mabouia) from the Corralillo region of Villa Clara Province, Cuba; (mean SVL ± SE [range] = 56.9 ± 1.4 mm [33.2–66.7 mm]; mean weight ± SE [range] = 4.5 ± 0.3 [0.7–7.9]).

Venter Forelimbs Hindlimbs Axillae Groin Flanks Tail Neck n (%) 18 (69.2) 4 (15.4) 18 (69.2) 20 (76.9) 13 (50.0) 21 (80.7) 9 (34.6) 10 (38.4) Total (range) 151 (1–26) 11 (1–21) 100 (1–15) 131 (1–21) 56 (1–6) 202 (1–38) 18 (1–4) 30 (1–11) Mean ± SD 4.4 ± 7.6 2.4 ± 2.2 3.3 ± 3.5 3.7 ± 2.7 2.4 ± 1.5 6.1 ± 8.7 2.0 ± 1.3 3.0 ± 3.1

384 BORROTO-PÁEZ ET AL. REPTILES & AMPHIBIANS • 27(3):382–389 • DEC 2020 intensity and body size (SVL) and weight were not significant identification (Figs. 1E–F) using the taxonomic key to Cuban (SVL: r = 0.356, t = 1.9, P = 0.06; weight: r = 0.244, t = 1.23, species of pterygosomatids in Paredes León et al. (2013). P = 0.22). Geckobia hemidactyli was identified under the microscope Mites initially observed and photographed on live hosts by its inconspicuous dorsal shield and dorsum covered with were quickly identified by the second author (CCMR) as many short hairs (setae) and by the lateral position of the pterygosomatids, possibly of the genus Geckobia. Geckobia inconspicuous eyes located on the prodorsal shield. spp. are mostly parthenogenic and sexually dimorphic, with males being rare and considered neotenic deutonymphs Intra- and interspecific transmission of (second-stage larvae). The sexes exhibit distinct behaviors Geckobia hemidactyli mites and congregate at different levels of maturity at various loca- To test for possible intra- and interspecific transmission of tions on the bodies of hosts (Bauer et al. 1990). Mobility is Geckobia mites, we confined 13 adult male Tropical House reduced in various life cycles; protonymphs (first-stage larvae), Geckos infected with mites (intensities of 2–41) for 5–15 tritonymphs (third-stage larvae), and adults are calyptostasic days with adult conspecifics (n = 5), West African House (quiescent stage), whereas deutonymphs (second-stage larvae) Geckos (H. angulatus; n = 3; Fig. 3A), and Ashy Geckolets are active (Girot 1969). Mites in the genus are characterized ( elegans; n = 2; Fig. 3B) that were free of mites by orange color and the rounded and flat morphology of the (Table 2) in ten 2–3-liter containers with corrugated paper as idiosoma (= body; average size 200–250 µm). They posi- substrate and refugia to facilitate contact between individuals tion themselves in predictable fashion embedded or attached and promote mite transmission. beneath the ventral scales of the host’s body. The mites are Geckos were fed daily with small flies and lepidopterans quite small and are most easily observed in high infestations. and held at ambient humidity (70–80%) and temperature Mites prefer to congregate in the axillae, but also on and near (25–28°C) in a shaded location. Observations confirmed the bases of tails, groins, necks, ventral scales, lamellae of the that geckos in each container were in direct contact with each fingers (especially in gekkotans), and between folds of skin, other on multiple occasions each day. After the observation which matches our observations of the mites occurring on period, all geckos were checked for ectoparasites, some were Cuban geckos. These characteristics are generally enough released (some H. mabouia and S. elegans); others killed, pre- to identify mites in the family Pterygosomatidae and tenta- served in 95% alcohol, and stored in the private collection of tively assign them to the genus Geckobia based on host species the senior author (RBP); and some remain in captivity. and locality. Of the three species of mites known to colonize After the tests, showed no signs of suffering Hemidactylus geckos in the Americas, G. hemidactyli is the or stress attributable to the restricted environment or the only one reported from live H. mabouia and on any host in presence of the other individuals. Neither interspecific test the Caribbean region (Martínez Rivera et al. 2003). resulted in the transmission of mites; the Tropical House However, further examination of mites was necessary Geckos still had Geckobia mites, but both the West African to confirm the identity to genus and species. We used an House Geckos and the Ashy Geckolets remained free of Embedded System NSZ-800LCD Microscope to observe mites. All but one of the intraspecific tests also were negative; additional morphological characteristics and assure proper we found only one mite that had moved to a previously unin-

Fig. 3. Tests of interspecific transmission of mites (Geckobia hemidactyli) by contact in confinement with infected Tropical House Geckos (Hemidactylus mabouia) over a period of 10 days: (A) A West African House Gecko () (darker gecko) and (B) an Ashy Geckolet (Sphaerodactylus elegans) (small gecko). Note that the in B was collected with dorsal skin lesions and a loss of scales not related to the mite infection. Photographs by Rafael Borroto-Páez.

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Table 2. Results of ten tests for intra- and interspecific transmission of pterygosomatid mites (Geckobia hemidactyli) from infected hosts (Tropical House Geckos, Hemidactylus mabouia) to non-infected conspecifics (n = 5), West African House Geckos (H. angulatus; n = 3), and Ashy Geckolets (Sphaerodactylus elegans; n = 2). Abbreviations for species: Hm = H. mabouia, Ha = H. angulatus, Se = S. elegans; sex: m = male, f = female; localities: C = Corralillo (Villa Clara Province), EH = Hotel Elguear (Villa Clara Province), RG = Rincon de Guanabo (Mayabeque Province); VT = Vibora, La Habana (La Habana Province).

Non-infected sp., Infected host (all Hm) Days in Test locality, sex locality, sex, intensity contact Results 1 Ha, C, f C, f, 41 10 — 2 Ha, EH, m C, m, 23 15 — 3 Ha, EH, m C, m, 21 15 — 4 Se, EH, m C, f, 11 7 — 5 Se, VT, f RG, f, 12 10 — 6 Hm, EH, m C, f, 7 9 — 7 Hm, EH, m C, m, 11 9 +* 8 Hm, EH, m C, m, 11 9 — 9 Hm, EH, f EH, f, 2 12 — EH, f, 2 10 Hm, EH, f C, m, 23 5 — EH, f, 2 EH, f, 2 *one mite on different parts of the body on days 7 and 9 with no means of determining if it was the same individual. fected host (test 7 in Table 2). On days 7 and 9 , a single mite Differential arrival times of house geckos was on a different part of the gecko’s body with no means of and mites to Cuba determining if it was the same mite or not. The transmission As noted above, Martínez Rivera et al. (2003) searched for of Geckobia hemidactyli mites is evidently not an easy event. mites only on preserved specimens of Hemidactylus mabouia Successful transmission might require specific microhabitat collected at the U.S. Naval Base at Guantanamo Bay that had conditions, the presence of specific developmental stages, or been deposited in a U.S. museum. While specimens from more prolonged contact with infected hosts. multiple localities in a number of other countries were in We understand that the sample sizes in our preliminary the collection sampled, the only specimens from the Cuban tests were small and that the tests lacked negative controls, but Archipelago originated in U.S. territory on the island. This the observations tentatively support the lack of empirical evi- was not due to under-sampling, but rather a response to the dence of any transmission of pterygosomatid mites from inva- historically limited access to and exchange of information sive geckos to different species or to native geckos (Bertrand and museum specimens between Cuba and the rest of the et al. 2008; Barnett et al. 2018). Martínez Rivera et al. (2003) world. However, an extensive record of herpetological studies noted a similar absence of interspecific transmission when he carried out on the island by local Cuban herpetologists and collected three H. angulatus free of mites although they had the international community is available. This information been syntopic with H. mabouia. Hanley et al. (1995) found is summarized in many sources (e.g., Barbour and Ramsden no evidence of mite transfer between geckos ( 1919; Garrido and Jaume 1984; Estrada and Ruibal 1999; spp.) after keeping them together for 48 h. However, anec- Rodríguez-Schettino 2003; Estrada 2012; Rodríguez Schettino dotal evidence and the morphology of the mites suggest that et al. 2013; Borroto-Páez et al. 2015). From 1965 to 1980, Geckobia sp. spend their entire lives on geckos and are trans- many parasitologists from former socialist countries, especially mitted only as eggs, in immature stages, or adults during close Czechoslovakia, worked extensively in Cuba. Nevertheless, and prolonged intraspecific contact, such as mating, sharing despite the available information, no records of G. hemidactyli refuges, and fighting (Bauer et al. 1990; Martínez Rivera et from the rest of the island have appeared until now. al. 2003). To date no evidence suggests any effect these mites Acarologist Jorge de la Cruz worked intensively in Cuba could have on the body condition of hosts or in wild popula- and described two species of native pterygosomatid mites: tions (Hanley et al. 1995). Geckobia tarentolae (de la Cruz 1973) from a native American

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Wall Gecko (Tarentola americana) and Cyclurobia javieri (de la hikers that were carried so far north by their human dispersers; Cruz 1984), now Geckobiella javieri, from the endemic Cuban nevertheless, they highlight the dispersal ability of these geckos. Iguana (Cyclura nubila). Moreover, he found other species Introduced populations are common in ports and warehouses of mites, such as Bertrandiella otophila, on T. americana (de and quickly adapt and spread to urban settings and coastal la Cruz 1984). The available material on the mites and other towns. Females lay eggs in communal nests in rotten logs and arachnids of the island fails to show records of any pterygoso- other natural cavities (Sousa and Freire 2010; Meshaka 2011; matid mites on geckos of the genus Hemidactylus, even though and references therein), but also in any available cavity in, for Paredes León et al. (2013) did a thorough study of the available example, cinder blocks, plant pots, electrical boxes, and timber acarology collections when describing pterygosomatid mites in buildings (Rivero 1978; CCMR and RBP, independent per- from Cuban lizards. In that study, they identified three known sonal observations), which further aids their successful disper- pterygosomatid mites and described a new species that para- sal. Recently, a preliminary study of sitizes native Cuban lizards: Geckobia tarentolae, Bertrandiella (Hemidactylus frenatus) populations in their native Taiwan sug- otophila, and B. griseldae from Tarentola americana and gests that eggs are capable of withstanding submersion in seawa- Geckobiella javieri from Cyclura nubila. Paredes León et al. ter and considerable desiccation (Hsu et al., submitted). Some (2013) were aware that H. mabouia was a reported host of G. researchers (e.g., Punzo 2005; Kratochvíl and Frynta 2006) hemidactyli in Cuba and that both species are naturalized on the have suggested that the round hard-shelled eggs of these geckos island, but did not include G. hemidactyli in their key of Cuban facilitate the retention of moisture and allow females to be less mites, most likely because none were available in the collec- selective of nesting sites. tions they sampled. The team instead used G. hemidactyli from We must consider the possibility that Hemidactylus mabouia Brazil. This suggests that G. hemidactyli is absent from acaro- continues to arrive in Cuba (or any place where it is considered logical collections with extensive Cuban specimens and poses invasive) at multiple ports of entry and on multiple occasions the questions of how G. hemidactyli is distributed in Cuba and in separate incidents of dispersal (Weterings and Vetter 2018). if multiple introductions of H. mabouia and its mites occurred Some suggestions involve natural transatlantic dispersal on at different ports of entry. Moreover, several published studies currents of several species of Hemidactylus from the west- from the past 20 years on several aspects of the natural his- ern coast of to various localities in the Americas (Kluge tory and morphology of Hemidactylus geckos from throughout 1969; Rivero 1978) or with human mediation via ships trans- Cuba (Rodríguez-Schettino 2003; Rodriguez-Schettino et al. porting slaves and other goods from Africa to tropical America 2013; Iturriaga and Marrero 2013; Paredes León et al. 2013; (Vanzolini 1978). Such possibilities would explain the presence Díaz 2014; Borroto-Páez et al. 2015; Velasco and Neyra 2016) of Hemidactylus spp. native to the Americas and the presence have involved extensive handling, measuring, and observations of H. mabouia in Brazil and other Neotropical regions prior to of live animals as well as museum specimens. globalization (Weterings and Vetter 2018). The Tropical House However, even with a history of published work on Gecko is ubiquitous in the Greater Caribbean, and together pterygosomatid mites and on the ecology and natural history with three native Cuban species, the Cuban Treefrog (Osteopilus of Hemidactylus geckos, no one has reported the presence of septentrionalis), the Cuban Flat-headed Frog (Eleutherodactylus Geckobia hemidactyli on geckos outside of the U.S. Naval Base planirostris), and the Cuban Brown Anole (Anolis sagrei), is at Guantanamo Bay. Consequently, one has to ask why has among the most frequent herpetofaunal invaders in the region this ubiquitous mite from such a ubiquitous gecko not been (Powell et al. 2011). Those four species have become invasive documented? We propose that G. hemidactyli was absent from generalists in multiple localities during the past century by dis- most of Cuba except for the U.S. Naval Base at Guantanamo persing as hitchhikers in various cargos. In the case of Cuba, Bay until as recently as 2016. we propose that H. mabouia and its ectoparasite, G. hemidac- House geckos of the genus Hemidactylus are classic hitchhik- tyli, arrived separately at the U.S. Naval Base at Guantanamo ers that commonly travel from place to place in cargo on boats, Bay prior to its arrival elsewhere in the archipelago. Geopolitical airplanes, and various terrestrial vehicles (Heath and Whitaker realities effectively isolate the U.S. base from the rest of the 2015). Several species of Hemidactylus regularly show up in new island while connecting it indirectly to the U.S. mainland, localities and are established introduced species in many tropi- especially Florida, and Puerto Rico, where the gecko is ubiqui- cal and subtropical regions around the world. Weterings and tous. This same route (Guantanamo to Florida to Puerto Rico Vetter (2018) compiled all the locality data known for some of and beyond) has been proposed for the dispersal of Osteopilus the most cosmopolitan species of Hemidactylus, including H. septentrionalis and Anolis sagrei (e.g., Eales and Thorpe 2009). mabouia, and listed isolated records of individuals as far north as Consequently, we presume that the population of H. mabouia the northern coast of France and the Great Lakes Region in the at the U.S. Naval Base at Guantanamo Bay arrived indepen- USA. Such individuals most likely do not represent viable pop- dently of other Cuban populations that most likely entered the ulations but instead are merely chance encounters with hitch- country through different ports of entry.

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For many years, Hemidactylus mabouia was considered to (2011) reported G. hemidactyli in the U.S. in 2005. However, be very localized and limited to human settlements in Cuba the specimens from the U.S. Naval Base at Guantanamo Bay (Barbour and Ramsden 1919; Barbour 1937). More recently, dating to 1965–1969 actually constitute the earliest records it still was considered relatively abundant only in eastern Cuba in the region (CCMR, unpublished data). Our initial discov- (Schwartz and Henderson 1991). Today, however, the species ery in 2016 of G. hemidactyli elsewhere in Cuba (Fig. 4) fur- is quite abundant and has an extensive nation-wide distribu- ther reinforces the conclusion that the populations described tion. The discovery of G. hemidactyli on house geckos at four herein originated independently of that at the naval base. different localities geographically distant from Guantanamo Bay (Fig. 2), all of them relatively close to the main ports Acknowledgements and tourist areas of Habana and Varadero, suggests that these We thank Yamilka Rodríguez from the Faculty of Biology populations correspond to multiple separate introductions of of the University of Habana who facilitated the use of the H. mabouia into Cuba distinct from that at the U.S. Naval Embedded System LCD Microscopy to photograph the mites Base at Guantanamo Bay. Although Hemidactylus geckos reg- and a student who helped. Boris A. Fabres, Environmental ularly show up in new localities far from any known popula- Protection in the Caribbean (EPIC), helped with English and tions, Short and Petren (2011) demonstrated that once geckos made useful suggestions that improved this manuscript. arrived at a particular area in Florida, dispersal was minimal and that, in order for them to become established, multiple Literature Cited human-assisted translocations to the same region and to dif- Barbour, T. 1937. Third list of Antillean reptiles and amphibians. Bulletin of the ferent areas within that region is likely a necessity. Short and Museum of Comparative Zoology 82: 77–166. Barbour, T. and C.T. Ramsden. 1919. The herpetology of Cuba. Memoirs of the Petren (2011) also found no detectable genetic structure on Museum of Comparative Zoology 47: 1–213. a statewide scale; in other words, populations from one met- Barnett, L.K., B.L. Phillips, A.C. Heath, A. Coates, and C.J. Hoskin. 2018. The impact of ropolitan area are more genetically similar to each other than parasites during range expansion of an invasive gecko. Parasitology 145: 1400–1409. to those from other metropolitan areas, as would be expected Bauer, A.M., A.P. Russell, and N.R. Dollahon. 1990. Skin folds in the gekkonid lizard genus Rhacodactylus: A natural test of the damage limitation hypothesis for urban species with limited migration abilities. Evidence of of mite pocket function. Canadian Journal of Zoology 68: 1196–1201. genetic differentiation between Florida and other areas where Bertrand, M., N. Cole, and D. Moodry. 2008. Adaptation in parasitic mites: H. mabouia occurs was evident. Spread by the host or stay with the host?, pp. 137–146. In: M. Bertrand, S. Kreiter, K.D. McCoy, A. Migeon, M. Navajas, M.‐S. Tixier, and L. Vial Hitchhiking geckos presumably arrived at the various (eds.), Integrative Acarology. Proceedings of the Sixth Congress of the European Cuban sites from multiple locations like Florida or other Association of Acarolgists. European Association of Acarolgists, Creative Caribbean islands with a relative high exchange of passen- Commons, Mountain View, California. Borroto-Páez, R. and D. Reyes Pérez. 2019. Competitive interference between the gers and baggage. Based on published photographs taken endemic Cuban Green Anole (Anolis porcatus) and invasive Tropical House in Puerto Rico (Rivero 1978) and Anguilla (Malhotra and Geckos (Hemidactylus mabouia). Reptiles & Amphibians 26: 43–46. Thorpe 1999), the earliest unreported records of Geckobia Borroto-Páez R. and D. Reyes Pérez. 2020. Damage to televisions and other electrical appliances by invasive and native geckos in Cuba. Reptiles & Amphibians 27: 50–53. hemidactyli in the Caribbean date to 1972, and Corn et al. Borroto-Páez, R., R. Alonso Bosch, B.A. Fabres, and O. Alvarez García. 2015. Introduced amphibians and reptiles in the Cuban Archipelago. Herpetological Conservation and Biology 10: 985–1012. Corn, J.L., J.W. Mertins, B. Hanson, and S. Snow. 2011. First reports of ectopara- sites collected from wild-caught exotic reptiles in Florida. Journal of Medical Entomology 48: 94–100. de la Cruz, J. 1973. Nueva especie de ácaro del género Geckobia Megnin, 1878 (Acarina; Pterygosomidae) parásito de la Tarentola americana (Gray) de Cuba. Poeyana 102: 1–6. de la Cruz, J. 1984. Sistemática de la familia Pterygosomidae (Acarina: Prostigmata), con la descripción de un nuevo género y especie. Poeyana 278:1–22. Díaz, L.M. 2014. A new locality record for the Common House Gecko Hemidactylus frenatus Schlegel (: Gekkonidae) in Cuba, with com- ments on the other colonizing species of the genus in the island. Reptiles & Amphibians 21: 30–34. Díaz, J.A., R. Torres, L. Paternina, D. Santana, and R. Miranda. 2020. Traveling with an invader: Ectoparasitic mites of Hemidactylus frenatus (Squamata: Gekkonidae) in Colombia. Cuadernos de Herpetología 34: 1–4. Dunn, A.M. 2009. Parasites and biological invasions. Advances in Parasitology 68: 161–184. Dunn A.M. and M.J. Hatcher 2015. Parasites and biological invasions: Parallels, interactions, and control. Trends in Parasitology 31: 189–199. Fig. 4. The earliest record of a Cuban Tropical House Gecko (Hemidactylus mabouia) with pterygosomatid mites (Geckobia hemidactyli) photographed Dunn A.M., M.E. Torchin, M.J. Hatcher, P.M. Kotanen, D.M. Blumenthal, in 2016 in a family apartment in Corralillo, Villa Clara Province. Note the J.E. Byers, C.A.C. Coon, V.M. Frankel, R.D. Holt, R.A. Hufbauer, A.R. Kanarek, K.A. Schierenbeck, L.M. Wolfe, and S.E. Perkins. 2012. Indirect orange mites on the shoulder and in the axilla. effects of parasites in invasions. Functional Ecology 26: 1262–1274.

388 BORROTO-PÁEZ ET AL. REPTILES & AMPHIBIANS • 27(3):382–389 • DEC 2020

Eales, J. and R. Thorpe. 2010. Revealing the geographic origin of an invasive lizard: Powell, R. 2004. Species profile. Asian House Gecko (Hemidactylus frenatus). The problem of native population genetic diversity. Biological Invasions 12: Iguana 11: 20. 77–86. Powell, R., R.I. Crombie, and H.E.A. Boos. 1998. Hemidactylus mabouia. Catalogue Estrada, A.R. 2012. The Cuban Archipelago, pp. 113–125. In: R. Powell and R.W. of American Amphibians and Reptiles 674: 1–11. Henderson (eds.), Island lists of West Indian amphibians and reptiles. Bulletin Powell, R., R.W. Henderson, M.C. Farmer, M. Breuil, A.C. Echternacht, G. van of the Florida Museum of Natural History 51: 85–166. Buurt, C.M. Romagosa, and G. Perry. 2011. Introduced amphibians and Estrada, A.R. and R. Ruibal. 1999. A review of Cuban herpetology, pp. 31–62. In: reptiles in the Greater Caribbean: Patterns and conservation implications, pp. B.I. Crother (ed.), Caribbean Amphibians and Reptiles. Academic Press, San 63–143. In: A. Hailey, B.S. Wilson, and J.A. Horrocks (eds.), Conservation of Diego, California. Caribbean Island Herpetofaunas. Volume 1: Conservation Biology and the Wider Fajfer, M. 2012. Acari (Chelicerata)–parasites of reptiles. Acarina 20: 108–129. Caribbean. Brill, Leiden, The Netherlands. Fajfer, M. 2018. New species and records of scale mites (Acariformes: Punzo, F. 2005. The introduction of hemidactyline geckos in Florida: Colonization Pterygosomatidae) from geckos (Squamata: Gekkonidae and and impact on native fauna, pp. 231–237. In: W.E. Meshaka, Jr. and K.J. Carphodactylidae). BioMed Research International 2018: 1–8. Babbitt (eds.), Amphibians and Reptiles: Status and Conservation in Florida. Krieger Publishing Company, Malabar, Florida. Fajfer, M. and D. González-Acuña. 2013. Pterygosomatid mites of a new species group ligare (Acariformes: Pterygosomatidae: Pterygosoma) parasitizing tree Rivero, J.A. 1978. Los Anfibios y Reptiles de Puerto Rico. The Amphibians and Reptiles iguanas (Squamata: Liolaemidae: Liolaemus). Zootaxa. 3693: 301–319. of Puerto Rico. Universidad de Puerto Rico, Río Piedras, Puerto Rico. Garrido, O.H. and M.L. Jaume. 1984. Catálogo descriptivo de los anfibios y rep- Rodríguez-Schettino, L. (ed.). 2003. Anfibios y Reptiles de Cuba. UPC Print, Vaasa, tiles de Cuba. Doñana, Acta Vertebrata 11: 5–128. Finland. Girot, B. 1969. Étude du cycle de Geckobia latastei et Geckobia loricata, Acariens Rodríguez Schettino, L., C.A. Mancina, and V. Rivalta. 2013. Reptiles of parasites du Gecko Tarentola mauritanica. Vie et Milieu 19: 63–141. Cuba: Checklist and geographic distributions. Smithsonian Herpetological Information Service 144: 1–96. Hanley K.A., R.N. Fisher, and T.J. Case 1995. Lower mite infestations in an asex- ual gecko compared with its sexual ancestors. Evolution 49: 418–426. Schwartz, A. and R.W. Henderson. 1991. Amphibians and Reptiles of the West Indies. Descriptions, Distributions, and Natural History. University of Florida Heath, A.C. and A.H. Whitaker. 2015. Mites (Acari: Pterygosomatidae, Press, Gainesville, Florida, USA. Macronyssidae) taken from lizards intercepted at the New Zealand border. Systematic and Applied Acarology 20: 739–757. Short, K.H. and K. Petren. 2011. Multimodal dispersal during the range expansion of the tropical house gecko Hemidactylus mabouia. Ecology and Evolution 1: 181–190. Hsu, M.-H., J.-W. Lin, C.-P. Liao, J.-Y Hsu, and W.-S Huang. Submitted. Over- ocean dispersal inferred from the saltwater tolerance of lizards from Taiwan. Sousa, P.G. de. and E.M.X. Freire. 2010. Communal nests of Hemidactylus DOI 10.21203/rs.3rs-20111/v1. mabouia (Moreau de Jonnès, 1818) (Squamata: Gekkonidae) in a remnant of Atlantic Forest in northeastern Brazil. Biotemas 23: 231–234. Iturriaga, M. and R. Marrero. 2013. Feeding ecology of the Tropical House Gecko Hemidactylus mabouia (Sauria: Gekkonidae) during the dry season in , Tompkins, D.M., A.M. Dunn, M.J. Smith, and S. Telfer. 2011 Wildlife diseases – Cuba. Herpetology Notes 6: 11–17. from individuals to ecosystems. Journal of Animal Ecology 80: 19–38. Jiménez Quirós, R. 2014. Riesgo potencial para la salud humana por Salmonella Torre Santana, P.E. de la and N. Cuervo Pineda. 2019. Actualización de la lista de proveniente del geco casero introducido (Hemidactylus frenatus) en dos regio- ácaros (Arachnida: Acari) de Cuba. Revista Ibérica de Aracnología 34: 102–118. nes de Costa Rica. Unpublished Tesis de Magister Scientiae, Universidad Vanzolini, P.E. 1978. On South American Hemidactylus (Sauria, Gekkonidae). Nacional, Heredia, Costa Rica. Papéis Avulsos de Zoologia 31: 307–343. Kluge, A.G. 1969. The evolution and geographical origin of the New World Velazco, K. and B. Neyra, B. 2016. Sexual dimorphism in Hemidactylus mabouia Hemidactylus mabouia-brooki complex (Gekkonidae, Sauria). University of (Sauria: Gekkonidae) in relation to the size of the head. Poeyana 502: 55–59. Michigan Museum of Zoology Miscellaneous Publication 138: 1–78. Weterings, R. and K. Vetter. 2018. Invasive house geckos (Hemidactylus spp.): Their Kratochvíl, L. and D. Frynta. 2005. Egg shape and size allometry in geckos current, potential and future distribution. Current Zoology 64: 559–573. (Squamata: Gekkota), lizards with contrasting eggshell structure: Why lay spherical eggs? Journal of Zoolgical Sciences 44: 217–222. Note added in proof.—On 16 November 2020, Ariel Kraus, F. 2009. Alien Reptiles and Amphibians: A Scientific Compendium and Analysis. Invading Nature: Springer Series in Invasion Biology 4. Springer, Espinosa Lima from Morón in northern Ciego de Avila Dordrecht, The Netherlands. Province, Cuba (22°06'56.26"N, 78°37'14.86"W), observed Machado, I., G. Gazêta, J. Pérez, R. Cunha, and A. Giupponi. 2019. Two new a Tropical House Gecko (Hemidactylus mabouia) infected species of the genus Geckobia Mégnin, 1878 (Acariformes, Prostigmata, Pterygosomatidae) from Peru. Zootaxa 4657: 333–351. with mites (Geckobia hemidactyli). The gecko was not col- Malhotra, A. and R.S. Thorpe. 1999. Reptiles and Amphibians of the Eastern lected but the broken tail bore more than ten oranges mites. Caribbean. McMillan Education Ltd., London and Oxford, England. This extends the known distribution of these mites over 150 Martínez Rivera, C.C., A.G. Negrón, M. Bertrand, and J. Acosta. 2003. Hemidactylus mabouia (Sauria: Gekkonidae), host of Geckobia hemidac- km northeast of the nearest previously documented locality. tyli (Actinedida: Pterygosomatidae), throughout the Caribbean and . Caribbean Journal of Science 39: 321–326. Meshaka, W.E. 2000. Colonization dynamics of two exotic geckos (Hemidactylus garnotii and H. mabouia) in Everglades National Park. Journal of Herpetology 34: 163–168. Meshaka, W.E. 2011. A runaway train in the making: The exotic amphibians, reptiles, turtles, and crocodilians of Florida. Monograph 1. Herpetological Conservation and Biology 6: 1–101. Murphy, T.J. and A.A. Myers. 1993. A review of Salmonella infections in reptiles with particular reference to Gekkonidae. Amphibia-Reptilia 14: 357–371. Norval, G., S.R. Goldberg, C.R. Bursey, J. Mao, and K. Slater. 2014. Internal parasites of lizards from Taiwan. Herpetological Conservation and Biology 9: 484–494. Paredes-León R., N. Cuervo-Pineda, and T. M. Pérez. 2013. Pterygosomatid mites from Cuba, with the description of a new species of Bertrandiella (Acari: Prostigmata: Pterygosomatidae). Revista Mexicana de Biodiversidad 84: 1142–1152.

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