Eleutherodactylus planirostris
(greenhouse frog)

E. planirostris is a frog native to Cuba, the Bahamas and the Cayman Islands. It has been introduced to countries worldwide and there are established populations in the Caribbean, North and Central America, Oceania and Asia. This species is commonly transported unintentionally as a hitchhiker in nursery plants and materials and can rapidly colonise new areas. E. planirostris thrives in human-altered landscapes and is well-adapted to a variety of disturbed and natural habitats. It may threaten native invertebrate communities and compete with native insectivore species. Due to its small size, inconspicuous call and habitat, initial infestations of this species are often overlooked until populations are already too large and widespread to control. E. planirostris is listed as invasive in Florida, Louisiana and Hawaii, USA.

E. planirostris is native to Cuba, the Cayman Islands and northern Bahamas (Barbour and Ramsden, 1919; Schwartz, 1974; Schwartz and Henderson, 1991; Estrada and Ruibal, 1999; Hedges, 1999; Echternacht et al., 2011; Powell and Henderson, 2012). Several early distribution records considered only the Cuban population as native (Goin, 1947; Schwartz and Henderson, 1991). Schwartz et al. (1975) stated that the Bahaman and Cayman populations originated in Cuba, but does not indicate if he believed they were introduced via natural or human-mediated dispersal. However, molecular studies and fossil records indicate that the Bahamas and Grand Cayman individuals arrived naturally and prior to human colonisation (Seidel and Franz, 1994; Heinicke et al., 2011). In Cuba, E. planirostris is one of the most widely distributed amphibians and is found throughout the island of Cuba, Isla de la Juventad and the smaller islands off the northern and southern coasts of Cuba (Powell and Henderson, 2012; González et al., 2014). In the Bahamas, their native range is limited to the northern islands of Great Bahama Bank and Little Bahama Bank and in the Cayman Islands, Grand Cayman and Cayman Brac islands (Powell and Henderson, 2012).

In the Caribbean, E. planirostris has been introduced into Great Inagua Bank in the south of the Bahamas (Schwartz, 1974, Schwartz and Henderson, 1991, Powell and Henderson, 2012). Schwartz (1974) speculated that populations found on Caicos (North Caicos) are native, but E. planirostris are now considered non-native in all of the Turks and Caicos (Lever, 2003; Reynolds and Niemiller, 2010; Reynolds, 2011; Reynolds, 2012; Powell and Henderson, 2012). Established populations are recorded on the islands of Providenciales, Grand Turk, North Caicos, Middle Caicos and Big Ambergris Key. E. planirostris is widespread throughout Jamaica, more commonly in open and disturbed habitats (Crombie, 1999; Hedges, 1999; Powell et al., 2011; Wilson, 2011). There are records for E. planirostris in Grenada (Kaiser, 1992; Hedges, 1999; Kraus et al., 1999) but some think that this is a mistake (Powell et al., 2011; Powell and Henderson, 2012). In Guadeloupe, there is a record of Eleutherodactylus cf planirostris but additional records are lacking and it is possible that it may have been a misidentification (Breuil, 2002; Lorvelec et al., 2007; Powell and Henderson, 2012). This species has also been recorded in Honduras, in San Pedro Sula in 2007, Isla de la Guanaja in 2012, La Ceiba in 2012 and Tegucigalpa in 2014 (McCranie et al., 2008; McCranie and Orellana, 2014; Solís et al., 2014a; Solís et al., 2014b) and in the neighbourhood of Cerro Ancón in Panama City, Panama in 2007. They have also been found in the neighbourhoods of Costa del Este, Dorado Lakes and Balboa, Altos del Chase and Fuentes del Fresno, Panama (Crawford et al., 2011). An abundant greenhouse population was recorded in the mangroves of Cayo Mayor, Cayos Miskitos in Nicaragua in 1992 (Villa, 2015). There is one record for an individual E. planirostris in a residential area of Paramaribo, Suriname (Ouboter and Jairam, 2012) but there is no further information. Records for E. planirostris in Mexico include the port of Veracruz and, more recently, from Yucatán peninsula, in Playa del Carmen, 2010 and Cancun, 2015 (Schwartz, 1974; Cedeño-Vázquez et al., 2014; García-Balderas et al., 2016).

On Guam, an established population was found at St. John’s School, Tumon in 2003 and later populations were found in Tamuning, Mangilao and Manengon and at the US Naval Computer and Telecommunications Station (Christy et al., 2007b, Mathies et al., 2012). This species is now found throughout the island (Olson et al., 2012b). In Asia, calling males were first detected in 2013 in a landscaped residential area of Davao City on the island of Mindanao, Philippines (Olson et al., 2014). Established populations have also been found on the islands of Cebu, Luzon and Negros (Sy et al., 2015a; Sy et al., 2015b; Sy and Salgo, 2015). In Hong Kong, sightings of E. planirostris have been reported since 2011 at the Lung Fu Shan Country Park and Campus University of Hong (HKBWS, 2013; iNaturalist, 2016; Po et al., 2016). A record from Singapore reports a single individual frog in the residential area of Sembawang in 2015 (Groenworld and Law, 2016). A photograph was taken, but no specimens were collected and there have been no additional individuals observed at the site.

A biodiversity study in southeastern Nigeria reported that several E. planirostris were found at a site in 2008 (Ukpong et al., 2012), but there is no indication whether they established, or if verification photographs or specimens were collected.

In the USA, the first record for E. planirostris is from 1863 in an unspecified location of southern Florida (Cope, 1863; Cope, 1875) and in 1889 in Key West, Monroe County (Cope, 1889). Populations were later recorded in Brevard and Miami-Dade (Dade) counties in southern Florida (Barbour, 1910). Krysko et al. (2011) determined that there are vouchered specimens from 47 Florida counties and unvouchered reports for two counties; Gadsden and Hernando. The distribution of E. planirostris is considered continuous in southern Florida and disjointed in the panhandle counties of Bay, Escambia, Franklin, Okaloosa, Leon, Gadsden and Wakulla, with most records from coastal areas (Krysko et al., 2011; Meshaka, 2011; US Geological Survey, 2016). There are also new records for De Soto County in southwest Florida, Gilchrist County in northern Florida and Gulf County in the panhandle (Thawley et al., 2012; Greene, 2014; Godwin, 2014). An individual was found alive at the Detroit Zoo in a bag of mulch shipped from Gilchrist County, Florida but it is not established in the area (Zippel, 2005). In Louisiana, E. planirostris was first documented in 1975 at the Audubon Park Zoo in New Orleans, Orleans Parish, over 500 km from the nearest population at the time (Plotkin and Atkinson, 1979). Its distribution now covers 10 parishes in residential and natural areas (Dundee et al., 1989; Dundee 1994; Williams and Wygoda, 1997; Boundy, 1998; Boundy, 2004; Elbers 2007; Liner 2007; Meshaka et al., 2009). In Alabama, the first record is for Fairhope, Baldwin County in 1982 (Carey, 1982), but there are no other records for the state until Alix et al. (2014) reported an expansion into natural areas of Baldwin County. In 2013, a population was recorded in Mobile County (McConnell et al., 2015). In Georgia, E. planirostris was found in flower pots in 1998 in Savannah, Chatham County (Winn et al., 1999) and by 2008 their distribution included areas of Camden, Chatham, Glynn, Lowndes and Thomas Counties (Jensen et al., 2008). E. planirostris is common on St. Simon Island and Brunswick, Glynn County. Records in Mississippi are for Gulfport, Harrison County from 2003, an undated record for Starkville and a record for Oktibbeha County and Ocean Springs, Jackson County from 2014 (Dinsmore, 2004; Lamb and Chatfield, 2014). In South Carolina, E. planirostris was found in two different areas of Mount Pleasant, Charleston County in 2016 (Dillman and Gibbons, 2016). This is the most northern distribution record for an established E. planirostris population. There are records of E. planirostris in Texas, Missouri, Oklahoma and Michigan (Zippel, 2005; Tipton et al., 2012; US Geological Survey, 2016). Both the Missouri and Oklahoma populations are restricted to indoors (US Geological Survey, 2016). E. planirostris was first introduced to the Pacific Basin in or before 1994 to Hawaii (Kraus and Campbell, 2002). First records were from three established populations on Hawaii Island in nurseries or nursery adjacent areas and one in a residential area of Maui (Kraus et al., 1999). E. planirostris is now found on five Hawaiian Islands: Hawaii, Kauai, Lanai, Maui, Oahu (Olson et al., 2012a; Ferreira et al., 2015).

E. planirostris is one of the most successful amphibian invaders (Bomford et al., 2009). Given that their primary mode of transport through the nursery trade is active and globally expanding, further introductions and establishment are likely. Establishment success in invaded habitats and dispersal risk of this species is high. Due to its inconspicuous nature and the habitats it occupies, initial infestations are often overlooked until populations are already too large and widespread to control (Kraus and Campbell, 2002; Olson et al., 2012b). Although most introductions will be restricted to tropical areas (Rödder and Lötters, 2010), long-term residence in the Florida Keys may have allowed E. planirostris to evolve adaptations to colder climates and populations from Florida may be able to spread into temperate zones (Heinicke et al., 2011). 

E. planirostris is a terrestrial or sub-fossorial species, and can occassionally be found up to 2 m off the ground (Duellman and Schwartz, 1958). They are often found under objects such as leaf litter, rocks, gravel, fallen branches, coconut husks, flower pots, human debris, or hidden inside low-growing bromeliads, caves, lava tubes, rock crevices, gopher tortoise burrows, irrigation boxes, burrowing into loose, moist soil and under loose bark (Goin 1947; Neill 1951; Stewart and Martin 1980; Lips 1991; Schwartz and Henderson, 1991; Díaz and Cádiz, 2008; Olson and Beard 2012; Villa, 2015).

In Cuba, E. planirostris is found in wet and dry forests, coastal and mountainous areas, riversides, streambeds, caves, rocky outcrops, gardens and houses (Garrido and Schwartz, 1968; Díaz and Cádiz, 2008).

In its introduced range, it is often found in gardens, urban and residential areas and disturbed habitats, but will also be found in a variety of natural and forested areas. For example, in Florida, it is found in agricultural areas, disturbed areas, urban parks and gardens, mangrove forests, tropical hardwood hammocks, oak-palm hammocks, mesic hammocks, rockland hammocks, pine rockland, pine flatwoods, xeric uplands, scrub habitats, wet and dry prairie, freshwater marshes and coastal scrub areas (Meshaka, 2011). In Jamaica, it is found in open grasslands, scrub, lawns, pastures, roadsides and other disturbed areas (Stewart and Martin, 1980). In Panama and Mexico, records of E. planirostris are from urban areas, associated with houses and gardens and in grassy and forested areas close to residential sites (Crawford et al., 2011; Cedeño-Vázquez et al., 2014). In Hawaii, they are found in disturbed sites such as nurseries, roadsides, residential gardens, orchards and areas with native shrublands and forests (Olson et al., 2012a). In Guam, they are found in residential areas and secondary scrub forests (Olson et al., 2012b). Records from the Philippines are from urban areas with landscaped plants (Olson et al., 2014; Sy et al., 2015a; Sy et al., 2015b; Sy and Salgo, 2015).

Genetics

Nucleotide sequencing of the mitochondrial cyt-b gene and nuclear rag-1 and pomc genes of E. planirostris indicates two separate lineages; an eastern and western lineage. The “eastern” lineage is found in eastern/central Cuba, the Bahamas and the Cayman Islands and has been introduced into Jamaica, Nicaragua (Miskito Cay) and North Caicos. The “western” lineage is found in western Cuba and has been introduced into Florida and Hawaii. Genetic variation is higher for eastern lineages and Cuba than for the introduced population from Florida (Heinicke et al., 2011). Genetic analyses of mitochondrial Cytochrome Oxidase Subunit I (COI) and a fragment of the ribosomal 16S gene confirmed species introductions to Panama City, Panama and Yucatán, Mexico (Crawford et al., 2011; Cedeño-Vázquez and others 2014). The Panama population are of the “western” lineage and may be a secondary introduction from Florida origin (Crawford et al., 2011).

Reproductive Biology

E. planirostris is a direct-development frog, which means there is no tadpole phase and complete metamorphosis takes place inside of the egg. Eggs are laid on the ground, or under fallen leaves, rocks, or other debris (Goin, 1947; Díaz and Cádiz, 2008). Clutch size ranges from 3-26 eggs, and eggs hatch 13-20 days after deposition (Goin, 1947). Hatchlings resemble adult frogs, with similar colour patterns and an egg-tooth and reduced tail that is absorbed (Goin, 1947). Snout-vent-length (SVL) ranges from 4.3-5.7 mm (Goin, 1947; Lazell, 1989).

In Cuba, vitellogenesis is bimodal with first occurrence from April to June and then again from September to October. Temperature is a vital environmental cue for onset. Spermatogenesis occurs from March to November peaking in June and July (Iturriaga et al., 2014). A description of the gonads is provided by Iturriaga et al. (2012).

E. planirostris breeds seasonally in Cuba from April through January (Meshaka and Layne, 2002) and April to September in Florida (Goin, 1947; Meshaka and Layne, 2002). In Louisiana, breeding is limited to June and July (Dundee and Rossman, 1989). Breeding is seasonal in Hawaii and mirror the breeding season of Florida (Ferreira et al., 2015). Breeding usually occurs at night in warm and humid conditions (Meshaka and Layne, 2002). Males will call on the ground or vegetation, under debris or rocks and from subterranean lava tubes (Díaz and Cádiz 2008; Olson et al., 2012b).

Frogs become reproductively active 6-8 months after hatching in south-central Florida (Meshaka and Layne, 2002) and after one year in north Florida (Goin, 1947). The mean survivorship in Florida is estimated to be 1.9 ± 2.3 months (range: 0.03-6.6) (Meshaka and Layne, 2002).

Activity Patterns

E. planirostris is active all year round in Cuba but in Florida, it may limit its activity during cooler temperatures (Goin, 1947). In the Everglades of southern Florida, E. planirostris was found hibernating under the bark of a wild tamarind tree (Harper, 1935). In native and introduced habitats, they are predominantly nocturnal, actively foraging at night and seeking daytime retreat sites in leaf litter or under debris (Goin, 1947; Stewart 1977; Díaz and Cádiz, 2008; Meshaka, 2011; Olson and Beard, 2012). Advertisement calls are heard at night with peak chorus just after sunset and before sunrise (Goin, 1947).

Population Size and Structure

Population density estimates are only available from introduced habitats. Densities estimated from mark-recapture studies of adults at three sites on the island of Hawaii were 4,564, 2,400 and 5,300 adults ha⁻¹ (Olson et al., 2012a; Olson et al., 2012b). Preadult to adult ratio was also determined at the first site as 1.7, thus the total population density was estimated to be 12,522 frogs ha^-1. In Jamaica, the density of E. planirostris and three other Eleutherodactylus species was estimated at 4,635 frogs ha^-1. The abundance of E. planirostris was found to be higher in the dry season, at coastal regions and sites without native species (Stewart and Martin, 1980). For the latter survey, it was the most abundant species found. In southeastern Florida, it was one of the most abundant species during a study using coverboards (Engeman et al., 2016), In southwestern Florida, it was the only anuran species, native or exotic, in which mean calling intensity increased over a ten year period (Everham et al., 2013).

Nutrition

Dietary studies indicate that E. planirostris is primarily an insectivore and predominantly consumes leaf litter invertebrates. They will eat a variety of available species, but may specialise on ants (Olson and Beard, 2012; Ferreira et al., 2015). In Cuba, the native range, ants comprised 100% of their diet (Goin, 1947). In its introduced habitats of Florida, Jamaica and Hawaii, ants were also the dominant prey (Goin, 1947; Stewart, 1977; Olson and Beard, 2012; Ferreira et al., 2012). Other invertebrates found in their diet include springtails, arachnids (spiders and mites), termites, beetles, collembola, amphipods, isopods, cockroaches, dermaptera, millipedes, centipedes, worms, flies (adults and larvae), hemiptera (true bugs), Lepidoptera larvae and snails.

Associations

In southeastern USA, E. planirostris is one of many species that are found commensal with the gopher tortoise (Gopherus polyphemus) using its burrows in mesic and xeric forests (Lips, 1991; Witz et al., 1991). One study in a long-leaf pine savannah habitat indicated that there is a slight correlation between E. planirostris abundance and number of gopher tortoise burrows (Catano and Stout, 2015).

Environmental Requirements

E. planirostris has a high tolerance for warm and dry conditions compared to other Jamaican Eleutherodactylus species, with a preferred temperature of 27.3 ± 0.66°C (Pough et al., 1977). The maximum temperature range for E. planirostris was found to be from 36.4 to 41.8°C and critical water loss at 34.9% ± 0.004 of initial body weight in 40-50% relative humidity (Pough et al., 1977). Most areas of introductions have similar mean annual and maximum warmest-month temperatures to Cuba (Rödder and Lötters, 2010). Temperature and rainfall will likely limit its spread in temperate climates; for example, populations found in Oklahoma City and Missouri are limited to indoor greenhouses and buildings (US Geological Survey, 2016). However, there is a record of one individual that survived one month in a frozen mulch bag in Michigan (Zippel et al., 2005) and given their long term residence in peninsular Florida, E. planirostris may have evolved adaptations to survive colder climates (Bomford et al., 2009; Heinicke et al., 2011). Species distribution models indicate that E. planirostris exhibits niche conservatism in its invaded habitats but this may be due to the environmental gradients available (Rödder and Lötters, 2010). It is believed that the distribution of E. planirostris is increasing northward as a result global warming.

E. planirostris seems to be restricted to low elevation areas. They are found from sea level up to 720 m in Cuba, 600 m in Jamaica and 500 m in the southeastern USA and Hawaii (Stewart and Marin, 1980; Díaz and Cádiz, 2008; Olson et al., 2012b).

Snakes are a predator of E. planirostris in its native and introduced range, including three species of native racers; Cubophis canterigerus in Cuba, C. caymanus on Grand Cayman and C. vudii in the Bahamas (Henderson and Powell, 2009). In Florida, the native ringneck snake, Diadophis punctatus, a small, fossorial species found in humid and moist habitats, is a predator of E. planirostris (Wilson and Porras, 1983; Lazell, 1989). In Guam the invasive brown tree snake, Boiga irregularis, has been documented consuming E. planirostris (Mathies et al., 2012).

Other species of frog are also predators of E. planirostris. On Grand Cayman, E. planirostris was found in stomach content analyses of the Cuban treefrog, Osteopilus septentrionalis (Meshaka, 1996). Other predators in its native and introduced range probably also include invertebrates, lizards, birds and mammals (Henderson and Powell, 1999).

Documented parasites in its native Cuba include the nematodes Batracholandros bassi and Oswaldocruzia lenteixeirai (Goldberg and Bursey, 1991; Henderson and Powell 2009). Intestinal fluke parasites from the Mesocoeliidae family, Mesocoelium meggitti and M. monodi were found in introduced E. planirostris from the southeastern USA (Dronen et al., 2012). E. planirostris has also tested positive for the chytrid fungus, Batrachochytrium dendrobatidis, in its introduced range in Florida and Jamaica (Rizkalla, 2010; Holmes et al., 2012).

Genetic analyses involving sequencing of mitochondrial DNA was conducted to confirm the introduction of E. planirostris into Panama City, Panama, Yucatán, Mexico and Isla de Guanaja, Honduras (Crawford et al, 2011; Cedeño-Vázquez et al., 2014; McCranie et al., 2014). The results from Panama were deposited at the Barcode of Life Data Systems (Ratnasingham and Hebert, 2007) under project code “BSINV” and from Mexico Caribbean, under project code “EMC.”

E. planirostris is fairly quiet and inconspicuous and may be difficult to detect until introduced populations are too large to manage (Olson et al., 2012a). In Hawaii, visual and aural inspections of plant shipments may occur but are somewhat ineffective due to the small size of the frogs and eggs and because inspections are conducted during the day, when males are not usually actively calling (Olson et al., 2012b). A number of keys and descriptions are provided to enable accurate identification (Conant and Collins, 1998; Díaz and Cádiz, 2008; Köhler, 2011). 

E. planirostris is similar in appearance to a number of species within the same genus. For example, in Cuba, both E. ricordii and E. goini are similar but are larger than E. planirostris (Schwartz 1965; Schwartz, 1974). E. casparii is also similar but has black bands on the sides of the body behind the front limbs and a greenish tint to the dorsal colouring. E. tonyi and E. simulans, are almost identical to E. planirostris but can be differentiated by advertisement calls (Díaz and Cádiz, 2008). These species however, have not been introduced into areas outside of their native range.

In the southeastern USA, its introduced range, Acris crepitans and A. gryllus, are distinguished by their warty skin and dark stripes on the inside of their thighs and black triangle under their eyes and spring peepers and Pseudacris crucifer, is distinguished by an "X" mark on its back (Bartlett and Bartlett, 1999). These species also have very different advertisement calls.

In Hawaii, the invasive and closely related species E. coqui is distinguished by its larger size and toe pads, wider snout and loud, two-note advertisement call (Olson et al., 2012b). In the Philippines, some terrestrial species of Platymantis superficially resemble E. planirostris, but their calls are distinctly different (Olson et al., 2014).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

Early Warning Systems/Rapid Response

The US Geological Society (USGS) has an online sighting report form where new locations of Nonindigenous Aquatic Species (NAS) can be reported for the country (US Geological Survey, 2016).

Public Awareness

Public awareness is required to prevent the spread of E. planirostris from nurseries and, where possible to help control local populations. A series of newspaper articles have been published detailing the threats of invasive E.coqui and E. planirostris in Hawaii (Thompson, 2000; Thompson, 2001; Honolulu Star-Bulletin, 2001; Fujimori, 2001; Chun et al., 2003; Raloff, 2003; CTAHR, 2016; HEAR, 2016). These were however produced too late to control these populations.

Control

Cultural Control and Sanitary Measures

Leaf litter and debris removal may reduce the abundance of E. planirostris in privately owned areas (Olson et al., 2012b; CTAHR, 2016).

Physical/Mechanical Control

Hand capture may not be an efficient control method for the cryptic and elusive E. planirostris because abundances may actually be quite large once an introduction is detected and the frog is too quick to capture (Olson et al., 2012b). Native habitat management of fire-adapted communities may be an effective means of control in the southeastern USA (Meshaka, 2011).

Movement Control

Traps and barriers that were developed in Hawaii for E. coqui may work on E. planirostris and could be placed at invasion fronts or to prevent spread to vulnerable biodiverse habitats or privately owned areas. Hot water spray and vapour treatments of plant shipments has been effective for controlling E. coqui and may be employed by plant nurseries, quarantines zones and residential areas to prevent the spread of E. planirostris (Olson et al., 2012b).

Chemical Control

In Hawaii, a variety of chemical substances has proved effective in reducing populations of Eleutherodactylus species. Most applications have however specifically targeted E. coqui. Citric acid is the only approved chemical for controlling species of Eleutherodactylus in Hawaii and has been shown to be effective on E. planirostris (Pitt and Sin, 2004; Olson et al., 2012b; CTAHR, 2016).

With new records indicating an expanding global population it is important that further studies on this species are undertaken (Rödder and Lötters, 2010). Such studies should focus on the biology of E. planirostris in both native and introduced habitats; conducting studies to determine minimum temperature tolerances are needed. This would help to understand the risk of E. planirostris spreading to temperate climates.

In most of its introduced range, it is unknown if E. planirostris is invasive and impacting native ecosystems. Comprehensive diet studies, including evidence of prey preference and demographic impacts on native species, should be conducted in invaded habitats outside of Hawaii (Olson and Beard, 2012; Ferreira et al., 2015). Although it may compete with native species in many of its introduced habitats, no specific studies have studied competition with native species. Large densities E. planirostris may be altering its prey (invertebrate) communities and impacts to ecosystem processes should be assessed. Studies should also examine the effect that large densities of E. planirostris have on both native and non-native predator populations (Mathies et al., 2012; Cassani et al., 2015). 

17/05/2016 Original text by:

Christina Olson, Utah State University, USA