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.
Citation: AmphibiaWeb: Information on
amphibian biology and conservation. [web application]. 2008. Berkeley, California:
AmphibiaWeb.
Available: http://amphibiaweb.org/.
(Accessed: Aug 20, 2008).
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