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Bufo marinus Linnaeus, 1758
Marine Toad, Cane Toad Jean-Marc Hero1
Melody Stoneham2
1. Historical versus Current Distribution. Marine toads (Bufo marinus) are native from Sorona to Tamaulipas in Mexico in an area forming a continuous arc into the Orinoco and Amazon River Basins in South America (Tyler, 1975; Easteal, 1986); they are also native to extreme southern Texas (Easteal, 1986). They have been introduced to most tropical regions as a control for agricultural pests (Von Volkenberg, 1935; Oliver, 1949, 1955b; Mead, 1961; Krakauer, 1968; Easteal, 1981, 1986; Evans et al., 1996), including Jamaica and the Philippines in the late 1800s to control rats, and Puerto Rico, Fiji, New Guinea, America, and Australia in the early 1900s to control sugar cane pests (Freeland, 1985). In 1919, marine toads were introduced to Puerto Rico. By the early 1930s their numbers had grown and they were distributed both inland and on the coast (Grant, 1931). The demise of white-grub (Phyllophaga sp.) in Puerto Rico's cane fields was attributed to the introduction of marine toads in the 1920s (Freeland, 1985). However, it is unknown whether this decline was a result of toad predation or due to unusual weather conditions that prevented the emergence of Phyllophaga pupae (Freeland, 1985). It was the assumption that marine toads were a successful biological control for cane pests that led to their introduction throughout the Pacific Basin (Freeland, 1985). While native to extreme southern Texas, marine toads were introduced elsewhere in the United States (Florida and Hawaii) to control insect pests. In Florida, specimens from Puerto Rico were released in 1936 at Canal Point and Belle Glade, Palm Beach County, as a control for sugar cane pests (Lobdell, 1936; Krakauer, 1968). These introductions, as well as introductions into the Florida interior were unsuccessful (Reimer, 1958; Krakauer, 1968). Present populations in Florida were established from accidental releases at Miami International Airport, where they remained until the completion of a canal dug in 1958 that linked the airport rock pits to the extensive south Florida canal system (Krakauer, 1968). They are also sold as pets, and releases or escapes facilitate range expansion (Bartlett and Bartlett, 1999a). Altitudinal limits vary from sea level to 1,600 m (in Venezuela; Zug and Zug, 1979; see also Easteal, 1986). In 1935 in Australia, marine toads (known in Australia as cane toads) were introduced to Gordonvale, just south of Cairns on the east coast of Queensland, to control cane beetles (grey-backed [Dermolepida albohirtum] and Frenchi beetles [Lepidiota frenchi; Straughan, 1966; Freeland, 1985; Alford et al., 1995a,b]). Their failure to control cane beetles and their subsequent spread north, south, and west at rates of 25–30 km/yr quickly lead to their current status as a pest species (Grigg, 2000). By the 1950s, marine toads had spread throughout most of the eastern seaboard of Queensland and northern New South Wales; in 1986, they had reached Calvert Hills Station in the Northern Territory (Alford et al., 1995a). To date, marine toads have colonized 500,000–785,000 km2 of eastern Australia, including 50% of Queensland, and continue their northwesterly advance at 27–40 km/yr and their southerly advance at 1.07–5 km/yr (Beurden and Grigg, 1980; Sabath et al., 1981; Freeland and Martin, 1985; Sutherst et al., 1995; Caneris and Oliver, 1999). In northern Australia, marine toads reached Mataranka (40 km south of Darwin, Northern Territory) in 1999 (Caneris and Oliver, 1999) and entered Kakadu National Park (a World Heritage area) in the summer of 2000/2001. The potential geographical distribution of marine toads in Australia has been predicted based on climatic conditions around the country and tolerance limits of the toad (Sutherst et al., 1995). These workers predicted that marine toads have the potential to expand their range as far south as Bega, near the New South Wales and Victorian border, and across the top of Australia to Broome in Western Australia (Sutherst et al., 1995). Temperature and rainfall extremes are foreshadowed to prevent marine toad occupation of other regions (Sutherst et al., 1995). 2. Historical versus Current Abundance. Because marine toads have been introduced to parts of the United States, Australia, and throughout the Indo-Pacific region, they are more abundant now than they have been historically. In Oahu, Hawaii, the number of individuals increased from 148 to ≥ 100,000 in 2 yr (Oliver, 1949). In Australia, 101 adult marine toads were introduced in 1935 (Freeland, 1985, 1986). The number of toads currently in Australia is unknown, but populations have been observed to increase dramatically within a short period, and the density of adult toads in Australia is now greater than that in their native homeland, South America (Alford et al., 1995b). Long-term studies on toad populations in Townsville, Queensland, show that populations fluctuate greatly between seasons with males reaching higher densities in the early to mid wet season, females in early dry season, and juveniles late in the wet season (Alford et al., 1995a). Comparisons of old and newly established toad populations indicate that toads exhibit a "boom and bust" population growth pattern common to many pest species (Olding, 1994). For example, immediately after colonization the population increases exponentially (boom) until it reaches a peak, and then it declines (bust) and finds a "natural" level (Olding, 1994). Populations also contain a higher proportion of juveniles than adults and more males than females (Alford et al., 1995a); despite being introduced in relatively small numbers, the populations of marine toads in Australia and the United State have been shown to be genetically divergent (Easteal, 1985). 3. Life History Features. A. Breeding. Reproduction is aquatic. i. Breeding migrations. In Australia, male toads begin to move toward breeding sites from aestivation sites when the temperature begins to rise after winter—usually about August–September (Tyler, 1975). It is not known when the females arrive at the breeding sites, but they only appear at these sites when their oocytes have matured and they are ready to mate (Floyd and Bendow, 1984). ii. Breeding habitat. Includes brackish water: "…low concentrations of sea water constitute a favorable environment for the development of B. marinus larvae" (Ely, in Wright and Wright, 1949). Within their natural range in Venezuela, breeding habitat is determined by the transparency and pH of the water (with preferences for clearer water with a higher pH), the density of the vegetation surrounding the water body (with preferences for less dense vegetation), and permanence of the waterbody (with preferences for temporary, shallow, and warm water; Hero, 1992; Evans et al., 1996). The size and abundance of fish is apparently not important in breeding site choice (Hero, 1992; Evans et al., 1996). In central Amazonas, Brazil, marine toads breed in ephemeral ponds, permanent lakes, or large temporary ponds and can breed in sites with fish (Hero, 1990, 1992; Azevedo-Ramos, 1992). In the U.S., marine toads are associated and will breed in a variety of wetlnds sites, both natural and man made (Meshaka, 2003). The breeding season varies between seasons and geographic location. In Florida, females have mature eggs throughout the year and have been observed breeding all through the year within their natural range—with a tendency towards spring and summer (Krakauer, 1968). Chorusing is sporadic until late March, when it becomes nightly through early September (Krakauer, 1968). Choruses can occasionally be heard during the day, in bright sunshine. Wright and Wright (1949) note that there is controversy about whether a female can breed once or twice a year. In Australia, toads breed from September–March (peaking in January) in static or slow-flowing water (Tyler, 1975). Breeding sites are usually relatively free from dense ground vegetation, and while only large toads will crawl through dense ground vegetation to get to ponds, they generally avoid these habitats (Hero, 1994; Olding, 1994). Marine toads prefer sparse, patchy fringing vegetation (Dickman, 1991). Adult toads have also been shown to prefer breeding habitats where there are trees within 5 m of the pond for shelter (Hero, 1994; Olding, 1994). Other studies have noted that there are substantially more toads in areas cleared of ground vegetation and canopy cover (such as paddocks) than in naturally vegetated areas (Dickman, 1991). Their presence in natural areas is usually facilitated by tracks that cut into the vegetation (Dickman, 1991). B. Eggs. i. Egg Deposition Sites. Temporary to permanent, fresh to brackish waters (Wright and Wright, 1949). Evans et al. (1996) report that sites with high water transparency, high density of macrophytic vegetation, and neutral pHs are preferred. Females select a mate and may travel for days with him in amplexus before depositing eggs (Reed and Borowsky, 1967). One pair was recorded to have been in amplexus for 2 wk prior to breeding and several days after breeding (Reed and Borowsky, 1967). In Guyana, females (carrying males) have been observed constructing shallow nests filled with water, usually in sandy areas at the edges of pools (Reed and Borowsky, 1967). ii. Clutch size. Bartlett and Bartlett (1999a) state females can lay up to 20,000 eggs in long jelly strings, which are usually attached to submergent or emergent vegetation. Oliver (1949) gives a value of 10,000 eggs/female; Crump (1974) found a range between 4,240–12,700 eggs in Ecuador. Zug and Zug (1979) found a range between 6,050–23,000 eggs in Panama; Hearnden (1991) found a range between 6,970–36,100 eggs in northern Australia. The number of eggs/female increases with body size (Alford et al., 1995b). C. Larvae/Metamorphosis. Tadpoles emerge from the jelly surrounding the eggs approximately 48–72 hr after they are laid (Tyler, 1975). i. Length of larval stage. Tadpoles metamorphosed about 45 or 46 d following egg laying (Ruthven, 1919, in Wright and Wright, 1949), or 27 d post hatching (Wright and Wright, 1949). In Australia, marine toad cohorts were observed to take between 37–40 d to reach metamorphosis from eggs (Alford et al., 1995b). The length of the tadpole stage has been known to vary considerably, between 10 d (J.-M.H., unpublished data) and 6 mo (Tyler, 1975). This may reflect differences between climatic zones, environmental factors, competition, or a lack of food available to tadpoles, therefore delaying metamorphosis (Tyler, 1975). A correlation between density and growth rates exists, such that tadpoles at lower densities tend to metamorphose more quickly than tadpoles in higher densities (Alford et al., 1995a). In Australia, marine toad tadpoles have been observed at densities of between 15–61/m2 (Alford et al., 1995a). The pressure from competition may be higher in this species because of their tendency to travel in large aggregations. ii. Larval requirements. Descriptions of tadpoles and geographic variation in tadpole morphology, are given by Savage (1960a). Tadpoles will develop in brackish water at about 5% to < 10‰ sea water (similar concentrations are also given in Ely, 1944). In 1971, experiments were carried out on the resistance of B. marinus tadpoles to desiccation. These experiments determined that pre-metamorphic toad tadpoles can survive without water for 10 hr, provided the substrate is damp (Valerio, 1971). This indicates a limited ability to survive through pond drying or drought. Marine toads can tolerate temperatures between 16.8 ˚C and 42 ˚C (Krakauer, 1970). Although in the lab tadpoles recovered after 24 hr at 0.4 ˚C, below 16.8 ˚C they became movement impaired and would not survive prolonged periods in this state due to the cessation of feeding (Krakauer, 1970). Tadpoles have highest survival rates at temperatures around 29 ˚C (Floyd, 1983), and larger tadpoles tend to be more tolerant of changes in temperature (Floyd, 1984). Earlier studies recorded tadpoles surviving prolonged periods in temperatures between 8 ˚C and 43.7 ˚C (Heatwole et al., 1968). The turbidity of the water also appears to influence the distribution of toad tadpoles, with tadpole abundance decreasing as turbidity increases (Olding, 1994). a. Food. Toad tadpoles eat algae (Hinckley, 1962). The availability of food is known to affect the time required for tadpoles to become toadlets (Tyler, 1975). Competition for food becomes an issue at higher densities (Alford et al., 1995a). b. Cover. As they prefer warmer water and are adapted to high water temperatures, marine toad tadpoles are often exposed in pools with little to no vegetative cover beside or in the water body (Krakauer, 1970). Tadpoles remain active throughout their development and swim in large aggregations mid water column (Straughan, 1966). iii. Larval polymorphisms. Under natural conditions, studies have revealed that the main source of predation on hatchlings appeared to be marine toad tadpoles from earlier cohorts (Alford et al., 1995a). For example, hatchling survival in the presence of older tadpoles was reduced to 1.7% (from 88% without predators). Therefore, it would appear that cannibalistic behavior develops at mid to late tadpole stages. Interestingly, marine toad tadpoles do not prey heavily upon tadpoles of other species (Crossland, 1998a). iv. Features of metamorphosis. In the United States, metamorphosis takes place from late spring to mid summer, although time to metamorphosis is known to vary considerably (Tyler, 1975). This variation is due to factors such as differences between climatic zones, competition, tadpole food availability (Tyler, 1975), and tadpole density (Alford et al., 1995a). In northern Australia, tadpoles metamorphose in October to early April. The size at metamorphosis is relatively small (11 mm SVL) and toadlets are quite underdeveloped upon emergence (Cohen and Alford, 1993). Their weight represents only 0.01% of the eventual adult mass (Cohen and Alford, 1993). Emergence at such a small size is thought to reduce the risk of larval mortality through desiccation, however it may lead to high mortality of newly metamorphosed animals (Cohen and Alford, 1993). v. Post-metamorphic migrations. Newly metamorphosed marine toads require easy access to water to facilitate gas exchange and to prevent desiccation, therefore they often stay within 1–5 m of the water source (Straughan, 1966; Alford et al., 1995a). Within 3–4 d following metamorphosis, juveniles (< 30 mm) disperse from the banks of their breeding canals and lakes and do not return until they are about 90 mm (Alford et al., 1995a). As toads get older and larger they are found at greater distances from water (Alford et al., 1995a). Only 10–47% of metamorphosed toads will survive through their first dry season (Alford et al., 1995a). Studies have indicated that juvenile toads act as dispersalists and colonizers within the toad life cycle (Freeland and Martin, 1985). For example, surveys in northern Australia found two immature toads (< 90 mm) approximately 12 mo before the establishment of substantial populations, and similar occurrences have been recorded in western Queensland (Freeland and Martin, 1985). Other studies have suggested that as shelter positions are taken up by adults at the onset of the dry season, juvenile toads are forced to move away; when this happens at the edge of the toads distribution, new breeding sites are established (Straughan, 1966). D. Juvenile Habitat. Newly metamorphosed marine toads are primarily diurnal until they are about 3–4 d old, at which time they establish nocturnal activity patterns (Krakauer, 1968). Post-metamorphic toads (< 30 mm) generally do not travel far from a water source (remaining within 0–5 m of the water's edge) because their heart, lungs, and aerobic capacity are poorly developed and most gas exchange occurs across the skin (which must be moist for respiration to occur; Cohen and Alford, 1993). The necessity to be in such close proximity to a water source means that the density of newly metamorphosed toads in this area is high and detracts from survival and growth rates of toads (Cohen and Alford, 1993). As the toads develop they are generally able to move further away from the water source, but will return for the duration of the wet season (Cohen and Alford, 1993). Juveniles (30–70 mm) have different habitat preferences and activity patterns than do newly metamorphosed animals and adults (Krakauer, 1968). Juveniles are found in lawns or associated with buildings, where they emerge at dusk and are active at night—they are frequently found under lights, feeding on the insects attracted to the light (Krakauer, 1968). E. Adult Habitat. Adults are tolerant of humans and found in gardens, around houses, and in water tanks (Wright and Wright, 1949). Krakauer (1968, 1970) notes that marine toads are frequently found in disturbed areas and rarely encountered in undisturbed habitats. Marine toads are nocturnal and attracted to house and patio lights that also attract the insects on which toads feed (Wright and Wright, 1949). Toads are only active 1 out of every 3, 4, or 5 nights (Brattstrom, 1962a; Zug and Zug, 1979; Floyd and Benbow, 1984), and their activity tends to be correlated with rain (Floyd and Benbow, 1984). During the day, the toads are secretive, hiding under rocks and boards, in burrows (Wright and Wright, 1949), and under long grass clumps out of direct sunlight (Cohen and Williams, 1992). As their name suggests, marine toads are generally found along rivers and coasts in association with fresh and/or brackish water, including mangrove swamps. In a study by Krakauer (1970), adult toads were found to survive in 10‰ sea water, but quickly died in 15‰ sea water. Johnson (1972) found that marine toads also have a broad temperature tolerance and could survive at temperatures from 5–41.8 ˚C. These temperature tolerance limits influence the altitudes and latitudes where the toad is found (Brattstrom, 1968). The immediate response of a toad to heat stress is to escape; failing this, they are often found floating in water with their lungs inflated and their heart rates raised (Stuart, 1951; Novotney, 1976; Sherman, 1980). As temperatures reach the lower limits of tolerance levels, marine toads become less active and lose reflexes (Stuart, 1951; Novotney, 1976; Sherman, 1980). Temperature also has an influence on the respiration of marine toads. Experiments reveal that toads generally rely on pulmonary (lung) respiration (as opposed to cutaneous respiration) more than co-occurring tropical frogs (Hutchison et al., 1968). However, as the temperature increases, marine toads rely increasingly on cutaneous respiration for gas exchange (Hutchison et al., 1968). F. Home Range Size. Variable, dependent to an extent on the size of their water bodies and feeding sites (Brattstrom, 1962a; Carpenter and Gillingham, 1987). Displaced animals will home (return to their capture site), with local landscape and visual cues providing the key inputs for orientation (Brattstrom, 1962a). In Queensland, Australia, mark-recapture studies were done using several toads over a period of ten nights. The average minimum home range was calculated at 340 m2 (Pearse, 1979). A similar study by Zug and Zug (1979) found that at least some toads were familiar to an area of 2,812 m2. Spooling studies on marine toads have shown that they rarely move > 25 m away from the water's edge, but some adult toads were spooled a distance of 200 m (Cohen and Williams, 1992). The greater distance traveled by adult marine toads may be related to their ability to jump further than juveniles. For example, as the body size of marine toads increases, the distance they can jump also increases by an equivalent amount, such that a toad twice as large as another can jump twice as far (Rand and Rand, 1966). G. Territories. Marine toads do not establish defended territories during the reproductive season at the breeding site or in the terrestrial foraging zone (Sabath, 1980). Adult toads display some fidelity to shelter sites and prefer shelters with high soil moisture (they often increase soil moisture by urinating on the soil; Alford et al., 1995a). Adult toads seem to establish long-term foraging territory associations, and therefore it is more likely that newly metamorphosed and juvenile toads act as the dispersalists in the life cycle of the toad (Sabath et al., 1981). Juvenile toads are often excluded from breeding sites at the onset of the dry season, as all appropriate shelter sites are taken up by adult toads (Straughan, 1966). The juveniles then move away to establish new breeding colonies (Straughan, 1966). H. Aestivation/Avoiding Dessication. Marine toads aestivate during the dry season under boulders along rivers, under leaf litter, in old burrows of other animals, under long grass, and in hollow logs (Straughan, 1966). Captive specimens from Guyana kept in aquarium conditions were observed to dig nests in moist soil and bury themselves so only the eyes and top of the head were visible (Reed and Borowsky, 1967). Marine toads can lose 52.5% of body water before desiccation and will store water in their bladder. They therefore have the ability to survive for long periods without water (Krakauer, 1970). I. Seasonal Migrations. The only migrations made by marine toads are to and from breeding sites at the onset and the closure of the wet/breeding season. J. Torpor (Hibernation). Marine toads are intolerant of freezing conditions, and low temperatures appear to be restricting their spread northward and inland in Florida (Krakauer, 1968). Juveniles living near buildings and suburban lawns become inactive for long periods during cold weather. K. Interspecific Associations/Exclusions. In their natural habitat in Venezuela, toads are known to co-occur with 21 other species, but usually occur by themselves or with one other species at any one time or location (Hero, 1992). This suggests that marine toads select waterbodies at times or locations when other species are absent, or that other species are avoiding marine toads (Hero, 1992). In 12% of cases, marine toads co-occur with a South American treefrog species (Hyla crepitans), whose larvae are known to consume anuran eggs and therefore may be a potential predator of marine toads (Hero, 1992). In the United States, marine toads occur in regions with southern toads (B. terrestris), but unlike marine toads, southern toads are found in drier pine lands and on drier ground within the Everglades. L. Age/Size at Reproductive Maturity. Toads are able to reproduce from 66–220 mm, with males averaging about 13 mm shorter than females (Wright and Wright, 1949; Easteal, 1986). Bartlett and Bartlett (1999a) note that animals in northern populations are smaller and speculate that cooler winter temperatures may inhibit growth. It takes 1 yr for toads to reach reproductive maturity in tropical regions and 2 yr in temperate zones (Easteal, 1982). In northern Australia, toads must be from 65–90 mm and usually in their second wet season before they are capable of reproduction (Cohen and Alford, 1993). Rapid growth follows emergence and lasts through the wet season but slows at the approach of the dry season, probably reflecting food availability (Zug and Zug, 1979). Once the toads reach adult size, little growth is experienced (Zug and Zug, 1979). M. Longevity. The lifespan of toads under natural conditions is not known (Tyler, 1975). An age of 40 yr has been attributed to a similar species of Bufo in captivity (Tyler, 1975). There are two records of captive marine toads surviving beyond 15 yr (Tyler, 1975). A female marine toad held in captivity to determine longevity lived for 15 yr, 10 mo, and 13 d (Pemberton, 1949). N. Feeding Behavior. Marine toads feed on a wide variety of prey, especially terrestrial arthropods, including tenebrionid and carabid beetles (Taylor and Wright, in Wright and Wright, 1949; Krakauer, 1968), crabs, spiders, centipedes, millipedes, scorpions (Easteal, 1982), and cockroaches (Easteal, 1986; see list in Krakauer, 1968; see also Rabor, 1952 [Phillipines] and Strüssmann et al., 1984 [Brazil]). In one study, the most popular prey items in the stomach contents of 100 toads were ants, bees, caterpillars, millipedes, beetles, snails, bugs, slugs, and leafhoppers (in that order; Hinckley, 1962). The proportions of prey consumed largely reflect the availability of the prey at that time (Hinckley, 1962). A study on stomach contents in northern Australia showed ants and beetles to be the most popular prey items (Cohen and Williams, 1992). Krakauer (1968) noted a low percentage of empty stomachs. Marine toads are considered to be non-specific and aggressive predators and will occasionally consume native frogs and toads, even dog food and feces (Alexander, 1964; Tyler, 1975; Rossi, 1983; Bartlett and Bartlett, 1999a). Other prey include snakes (Rabor, 1952), birds (Krakauer, 1968), and mammals (Oliver, 1949). Alexander (1964) notes that individuals ingest plant material and repeats Oliver's (1955b) observation of toads being killed by strychnine after ingesting fallen blossoms of the strychnine trees. A study by Ingle and McKinley (1978) on the effects of stimulus on prey-catching behavior found that striking behavior in marine toads was more commonly elicited by dark objects rather than lightly colored objects and that the toads struck at the leading edge of moving objects representing prey. While many bufonids appear to rely on visual cues to detect and capture prey, marine toads differ in also using strictly olfactory cues (Tyler, 1975; Rossi, 1983). The prey that a toad will eat is largely limited by the gape of its jaws and the distention of its stomach (Tyler, 1975). O. Predators. Due to the presence of noxious chemicals in all stages of the toad’s life cycle, marine toads have few predators. At the tadpole stage, Australian studies have revealed that several species of native dragonfly naiads will readily consume marine toad tadpoles and eggs, as will dytiscid beetles, water scorpions (Lethocerus sp.), notonectids (Anisops sp.), leeches, tortoises, Macrobrachium spp., and crayfish (Cherax quadricarinatus; Crossland, 1992, 1993; Alford et al., 1995a). Native fishes have been found to ignore or taste and reject toad tadpoles unharmed (Alford et al., 1995a; Lawler and Hero, 1997). The most frequent predators of toad eggs and tadpoles, however, are older cohorts of marine toad tadpoles (Alford et al., 1995b). Toads may be most vulnerable to predation immediately following metamorphosis, whilst the development of terrestrial skin glands is occurring (Cohen and Alford, 1993). Although there are no studies on predators of newly metamorphosed toads, several animals have been observed to eat them, including adult marine toads, ants, centipedes, wolf spiders, small mammals, and some birds (e.g., Ibis sp.; Cohen and Alford, 1993). Predators of adult toads include small mammals (Krakauer, 1968; Cintra, 1988; Garrett and Boyer, 1993), snakes, including common garter snakes (Thamnophis sirtalis; Licht and Low, 1968, and references therein), and birds (Krakauer, 1968). Automobiles are likely the major source of mortality in Florida (Krakauer, 1968). In Australia, several vertebrate species have been observed to eat juvenile and adult marine toads, including fork-tailed kites (Lavery, 1969; Mitchell et al., 1995), ibises (Goodacre, 1947), koels (Cassels, 1970), tawny frogmouth owls (Freeland, 1985), crows, common rats (Adams, 1967), and white-tailed water rats (St. Cloud, 1966). These animals have apparently learned to flip the toad on its back, slit its belly open and eat its insides, therefore avoiding the toxic skin (Freeland, 1985). In northern Australia, keelback snakes (Amphiesma mairii) are unaffected by marine toad poison (Freeland, 1985) and readily consume juvenile toads in preference to native frog species (J.-M.H., unpublished data). The mortality of juvenile and adult toads in South America (87%/yr) is much greater than that in Australia (30–70%/yr) due to the larger number of co-evolved aquatic and terrestrial predators (Alford et al., 1995a). P. Anti-Predator Mechanisms. Marine toads are highly poisonous and secrete a whitish, viscous compound from their parotoid glands (in Wright and Wright, 1949; Allen and Neill, 1956; Licht, 1967b; Easteal, 1986). The parotoid glands produce and store a mixture of bufotenine and epinephrine—steroid-like substances that are toxic to most animals (Chen and Osuch, 1969; Freeland, 1986). Bartlett and Bartlett (1999a) describe the head-down defensive position marine toads assume to present their parotoid glands to potential predators. These toads are known to approach potential predators and attempt to force contact with their parotoid glands. Toad-eating snakes have apparently evolved tolerances to bufonid parotoid gland venom (Licht and Low, 1968). Toad eggs and tadpoles are also known to be toxic, although there are ontogenic shifts in palatability and toxicity such that older tadpoles are less palatable and more noxious than younger ones (Azevedo-Ramos, 1992; Lawler and Hero, 1997; Crossland, 1998b). This shift in palatability coincides with the development of poison-producing glands in the skin (Crossland, 1998). Unpalatability offers marine toad tadpoles protection from most aquatic vertebrate predators, especially fish. The conspicuous dark color of toad tadpoles makes them easy to recognize, and it is thought that fish learn to avoid them (Lawler and Hero, 1997). Experiments on the effects of Bufo toxins on Australian and Brazilian tadpoles reveal that tadpoles native to Brazil (where marine toads are endemic) readily consume marine toad tadpoles without any ill effect (Crossland and Azevedo-Ramos, 1999). However, native Australian tadpoles were found to display varied behaviors towards marine toad tadpoles and consequently had varied mortality rates (Crossland and Azevedo-Ramos, 1999). For example, marine toad tadpoles were avoided by most Litoria alboguttata, Litoria gracilenta, and Litoria rubella tadpoles. These tadpoles had a high rate of survival in the presence of toxic toad tadpoles. Of the native Australian tadpoles that consumed marine toad tadpoles, Bufo toxins were only fatal to half the tadpoles of L. alboguttata and Cyclorana brevipes and always toxic to Limnodynastes ornatus and L. gracilenta. Crossland and Azevedo-Ramos (1999) suggested that the differences in the responses of Brazilian and Australian tadpoles to toxic marine toads may result from differences in their evolutionary histories of exposure to Bufo toxins. Tadpoles of native species that prey on the noxious toad eggs have been found to suffer high mortality rates, between 60% (Litoria nigrofrenata) and 100% (Litoria bicolor and Litoria infrafrenata) within a span of 24 hr (Crossland, 1992; Crossland and Azevedo-Ramos, 1999). Small tadpoles have higher survival rates than large tadpoles in the presence of marine toad eggs, as small tadpoles cannot effectively penetrate the jelly surrounding the egg strings to graze on the toxic eggs (Crossland, 1998c). There is also some suggestion that the toxins within toad eggs can leach out into the water body and poison potential predators, although this theory remains to be verified (Crossland, 1992). Experimentation on native Australian aquatic predators have found that toad eggs are always lethal to snails and fish, but that notonectids and leeches experienced differential mortality, and nepids, dytiscid larvae, belostomatids, and crustaceans were unaffected (Crossland and Alford, 1998). Some invertebrate species, including dytiscid beetles, dragonfly naiads, and crayfishes, also seem to be unaffected by the unpalatability and toxicity of toad tadpoles (Crossland, 1992, 1998; Alford et al., 1995a). These predators have piercing and sucking mouthparts, and either avoid the glands in the skin that produce the toxins or simply lack the ability to taste (Crossland, 1998). Q. Diseases. Speare (1990) lists the diseases that have been found in marine toads. A fatal disease of unknown etiology arose in a Philippine population (Alcala, 1957). This disease was also observed by Tyler (1975) in New Britain in 1967. The individuals suffering from this disease appeared emaciated and ultimately died (Tyler, 1975). Upon dissection they were found to have food in their stomachs, however the liver and some muscles were atrophied (Tyler, 1975). Some heritable diseases occur in toads that cause myotonia (Bretag et al., 1980). This disease affects muscle membranes and often results in muscle spasms and stiffness (Bretag et al., 1980). Animals in this condition suffer reduced movement and may starve to death. Research has also discovered six iridoviruses in toads from Venezuela (Hyatt et al., 1995). In experiments that involved bathing native Australian frog spawn and toad spawn in inoculum, substantial mortality was observed in toad spawn (Hyatt et al., 1995). The reason for the survival of the Australian frog spawn is unknown (Hyatt et al., 1995). Marine toads have been shown to act as a host for ranaviruses that infect native fish and amphibians (Hyatt et al., 1995). Marine toads are also known to be a disease vector in areas with poor hygiene standards, where some toads have been found to harbor Salmonella (Tyler, 1975). Chytrid fungus is also lethal to marine toads and is reported to have had an important role in the disappearance of many native frogs in the Australian Tropics and Panama (Hyatt et al., 1995). R. Parasites. Lehmann (1967; see also Easteal, 1986) found two blood parasites in marine toads. Kloss (1974, in Easteal, 1986) reported on the nematodes of marine toads, including the round worm Ascaris lumbricoides. Marinkelle and Willems (1964) commented on the toad's potential to act as a vector of the eggs of A. lumbricoides, which may then infect small mammals. In laboratory experiments, Rhabdias sphaerocephala, a parasitic worm found in the lungs of Bufo, was found to be both highly infectious and fatal to toads (Williams, 1960). Interestingly, further experimentation showed that treefrogs were more resistant to the worm (suffering smaller parasitic loads) and were not a natural host to R. sphaerocephala (Williams, 1960). Brooks (1976a) reported five species of platyhelminths from marine toads. The trematode Mesocoelium danforthi is believed to have reached the West Indies through its marine toad host (Tyler, 1975). Levels of endoparasite infection rates are greater in South America than in Australia (Alford et al., 1995b). Marine toads have also been shown to act as a host for endoparasites that infect native fish and amphibians (Barton, 1995). In 1995, a microsporidian was discovered in tadpoles and post-metamorphic toads. It was previously thought to be a hyperparasite (occurring in trematodes within toads; Paperna and Lainson, 1995). This parasite forms cysts within the gut walls, spleen, and kidney and is passed on via cannibalism of dead tadpoles (Paperna and Lainson, 1995). It is not known to be fatal, as infected tadpoles survive and successfully metamorphose and the infection soon disappears as the toad develops (Paperna and Lainson, 1995). In South America, the presence of debilitating ticks (Amblyomma dissimile and A. rotundatum) reduces survival and fecundity of adult marine toads, having a large impact on toad numbers (Lampo, 1995). 4. Conservation. In the United States, marine toads are apparently native to southern Texas but were introduced to Florida and Hawaii to control insect pests. They continue to be sold as pets, and releases and escapes facilitate range expansion. Outside of their native range, marine toad populations should be considered introduced or invasive, and attempts should be made to control them. Krakauer (1968) suggests that competition between marine toads and other anurans may be minimal. Krakauer (1968) also notes the rapid expansion of the Miami metropolitan area is destroying habitat for southern toads while creating habitat for marine toads. In Australia, marine toads are known to co-occur with several other species of anurans, and their effects on these native species is widely varied. For example, when raised with tadpoles of Limnodynastes ornatus, marine toad tadpoles suffer greatly reduced growth and fail to survive to metamorphosis (Alford et al., 1995a). However, when raised with Litoria rubella, Limnodynastes terrareginae, Limnodynastes tasmaniensis, and Notaden bennetti, this situation is reversed and the native tadpoles fail to reach metamorphosis (Alford et al., 1995a). Marine toad tadpoles have not been found to exert predation pressure on native populations, and experiments have shown them to eat very few native Australian frog eggs, hatchlings, or tadpoles in comparison to native species of anuran larvae (Crossland, 1998a). However, many species of native tadpoles are known to suffer high mortality via direct consumption of marine toad tadpoles and eggs and show varying ability to detect and avoid marine toad toxins (Crossland, 1992; Alford et al., 1995a; Crossland, 1995). Some frogs may avoid using breeding sites used by marine toads (Williamson, 1995). For example, pond experiments have found the presence of toad tadpoles significantly reduces populations of predatory Limnodynastes ornatus tadpoles (Crossland, 2000). This in turn has an effect on other species of native tadpoles that co-occur with L. ornatus, because it reduces the predation pressure they would normally suffer, and species such as L. rubella have been shown to have increased survivorship (Crossland, 2000). In northern Australia, native fish tend to learn to avoid marine toad eggs and tadpoles (Crossland, 1995; Lawler and Hero, 1997). There is no conclusive evidence to support the theory that in Audtralia adult marine toads have had a negative impact on native adult frog populations, although predation and competition for food, shelter, and breeding sites is a probable result of marine toad introductions (Freeland, 1985; Williamson, 1995; Grigg, 2000). Some frogs may avoid using breeding sites used by marine toads (Williamson, 1995). In the Northern Territory, Australia, research is currently underway to assess the impact of toads on native frog populations. This research involves monitoring breeding activity of native frogs before and after the arrival of marine toads (Grigg, 2000). Marine toads have also had an impact on a number of endemic Australian predators, including goannas/monitors (Varanus spp.), native ‘cats’ or quolls (Dasyurids), several snakes (brown snakes, death adders and tiger snakes; Covacevich and Archer, 1975; Burnett, 1996), and dingoes (Canis lupus dingo; Catling, 1995). As toads colonize new areas, these animals show a substantial drop in numbers, presumably a result of being poisoned after attempting to eat the toads (Burnett, 1996). Three quoll species and 8 of 20 monitor species are now considered to be at risk because they include amphibians in their diet and their distributions overlap with current and potential marine toad distributions (Burnett, 1996). Studies in the Northern Territory comparing the fauna at sites before and after toad invasion have also indicated the presence of a long-term effect on dingoes, coleopterans, and reptiles, particularly small reptiles (Catling et al., 1999). 1Jean-Marc Hero
School of Environmental and Applied Sciences
Griffith University
PMB50 Gold Coast Mail Centre
Queensland 9726, Australia
m.hero@mailbox.gu.edu.au 2Melody Stoneham
School of Environmental and Applied Sciences
Griffith University
PMB50 Gold Coast Mail Centre
Queensland 9726, Australia
Literature references for Amphibian Declines: The Conservation Status of United States Species, edited by Michael Lannoo, are here.
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