The American bullfrog has been transported around the world primarily with the intention of cheaply cultivating its large and meaty hind legs for human consumption. It is also of commercial interest to biological supp...
The American bullfrog has been transported around the world primarily with the intention of cheaply cultivating its large and meaty hind legs for human consumption. It is also of commercial interest to biological supply houses, fish bait suppliers, the pet trade, and pond landscapers. In North America in the early 20th Century it was released outside of its natural range by wildlife agencies keen on introducing a new game species (Lannoo, 1996; Tangley, 2003). Once liberated it is extraordinarily prolific, prone to migration, and highly adaptable to new environments. It grows into a relatively large, voracious, and indiscriminate predator that can come to dominate the margins of lakes and ponds. It competes with native anurans. Larvae can have a significant impact upon benthic algae, and thus perturb aquatic community structure. Adults may be responsible for significant levels of predation on native anurans and other aquatic herpetofauna, such as snakes and turtles. The species also contributes to the spread of pathogens such as the chytrid fungus, Batrachochytrium dendrobatidis (Garner et al., 2006). R. catesbeiana has been identified by the World Conservation Union (IUCN) as one of the world’s 100 worst invasive alien species (ISSG, 2005).
The American bullfrog is a member of the nearly cosmopolitan family Ranidae. For most of the past 200 years this species has been unambiguously assigned to the genus Rana and the species R. catesbeiana, Shaw, 1802. Over the past 30 years, however, advances in biochemical systematics have led to both increased knowledge and increased contention concerning how new and ever-more refined data sets should be interpreted and taxonomically expressed. Thus, there are today numerous taxonomic synonyms for R. catesbeiana, e.g. Lithobates catesbeianus,Aquarana catesbeiana, and Novirana catesbeiana, that have received varying degrees of acceptance amongst herpetological systematists and the broader zoological community (Frost 2009).
An illustration of this is found in the Atlas of Amphibians of China by Fei, L. et al (1999), wherein the “Bull Frog” is identified taxonomically as Rana (Aquarana) catesbeiana Hillis 2007. In a paper by Frost et al (2006), it is proposed that the American bullfrog and its closest ranid relatives be moved from the genus Rana to the genus - formerly subgenus - Lithobates. This taxonomic reassignment may last or it may not, as the results from future investigations of the family Ranidae emerge. One of the co-authors in Frost et al (2006) recommends adopting the device of employing subgenera to accommodate Frost et al, e.g. Rana (Lithobates) catesbeiana (Green 2007). Currently, and at least for the time being, it appears that Lithobates catesbeianus (Shaw, 1802) will most likely supersede Rana catesbeiana and all other proposed or resurrected taxonomic synonyms as the preferred scientific name for the American bullfrog. However, anyone searching for literature references that predate Frost et al (2006) will need to be aware that virtually the entire historical database for this species is assigned, and in many cases continues to be assigned, to Rana catesbeiana.
Collins and Taggart (2009) in their influential list - Standard Common and Current Scientific Names for North American Amphibians, Turtles, Reptiles, and Crocodilians - have unilaterally declared ‘Lithobates catesbeianus’ to be the new scientific standard. However, Pauly et al (2009) - Taxonomic Freedom and the Role of Official Lists of Species Names - point out in a comprehensive and compelling way that ‘official’ lists of scientific names can have a confounding influence on objective taxonomic discussion, taxonomic stability, and the adoption, usage, and understanding of taxonomic names by non-taxonomists.
Consistency in biological nomenclature is not strictly a taxonomist’s concern. Today legislators, policy analysts, lawyers, customs agents and wildlife regulators all have a need to know exactly what taxon they are dealing with and how to unambiguously represent and recognize that taxon in writing. In this context common names can become as important as their scientific alternatives. For example, the common name ‘American bullfrog’ is almost completely unambiguous in which species it represents. However, in Collins and Taggart (2009) the common name for this species is listed simply as ‘bullfrog’. The problem here is that in global terms there are also - among others - an ‘African bullfrog’ (Pyxicephalus adspersus), an ‘edible bullfrog’ (Pyxicephalus edulis), an ‘Indian bullfrog (Hoplobatrachus tigerinus)’, an Australian ‘bullfrog’ (Limnodynastes dorsalis), and a ‘South American bullfrog’ (Leptodactylus pentadactylus). It is therefore reasonable to recommend that either ‘American bullfrog’ or ‘North American bullfrog’ be adopted as the international standard common name, as in Lannoo (2005), and used consistently to eliminate confusion.
R. catesbeiana is not the largest frog species in the world but it is one of the top ten (and the largest true frog in North America) with a maximum body length slightly in excess of 200 mm (typical length 90-152 mm) and body weight up to 0.5 kg. Like most frogs, it undergoes a drastic metamorphosis during its life cycle, passing from a young aquatic life phase with branchial respiration, predominantly plankton feeding, iliophagous or herbivorous, to reach adult life as an animal with pulmonary and skin respiration and a carnivorous feeding habit (Teixeira et al., 2001). Bullfrog tadpoles are also very large by frog standards (80-150 mm) and can take from 12 to 48 months to reach metamorphosis. A bullfrog tadpole’s body can be as large as a golf ball with a relatively long, high-finned and muscular tail. The colouration of the tadpole stage is brown to light olive with small black spots scattered across the head and upper body. At metamorphosis the tadpoles resorb their gills and finned tails while transforming into juvenile miniatures of adult bullfrogs but without secondary sexual characters. The colour of adults varies from olive, green or brownish on the dorsum with vague spots or blotches; the head is lighter green, and the legs blotched or banded; the eardrums are conspicuous. The hind feet are fully webbed. The skin is mostly smooth. There are no dorsolateral folds; a short fold extends from the eye over and past the eardrum to the forearm.
Bullfrogs become sexually dimorphic as they mature. Males develop yellow skin pigments on the chin and throat, and the ear covering (tympanic membrane) enlarges to several times the diameter of the eye. On the other hand, as females mature they tend to retain the superficial morphology and colouration of the juvenile stage, e.g. they lack yellow pigmentation on the chin and throat and the tympanic membrane remains about the same diameter as the eye.
Only adult male bullfrogs produce the advertisement call. They do this by trapping air between the lungs and the vocal pouches. The trapped air is forced back and forth over the larynx which generates the sound of the male’s call (Gans, 1974). The vocal pouches are located on either side of the throat, just below the jaw hinge, and were thought until recently to be the primary source of amplification and broadcast of sound. However, Purgue (1997) has shown that more sound is emitted by the male’s enlarged tympanic membrane than by the vocal pouches. A calling male has longitudinal folds of stretched throat skin that are aligned with the bones of the lower jaw beneath the angle of the mouth. The advertisement call of male bullfrogs communicates a variety of signals. It identifies the location of adult males in reproductive condition. It also attracts other males to form a lek, or calling aggregation (Emlen, 1976), and communicates territorial rights and neighbour-stranger discrimination (Boatright-Horowitz et al., 2000; Bee and Gerhardt, 2001; Bee, 2003).
The eggs of the American bullfrog are very small and appear black or dorsally black with a slightly lighter undersurface. Each egg is surrounded by a jelly capsule with additional jelly that creates a loose cohesion to the entire mass of eggs. A female bullfrog in her first year may produce a single egg mass of only a few hundred eggs, but as she increases in age her egg production increases as well. By her third year she will be capable of producing 20-30,000 (FAO, 2005). At least in some cases, there are two separate clutches produced at consecutive spawning events in a single season. A bullfrog egg mass can be anywhere from 20 cm to over 1 metre across and sits at the surface in order to facilitate oxygen diffusion. The eggs will hatch in 3 to 5 days (Bury and Whelan, 1984).
R. catesbeiana is native to eastern North America, ranging naturally from Nova Scotia, southern Quebec and Ontario in Canada, down through the eastern United States and Mississippi drainage, and southward along the east coast of Mexico. It has been introduced to Hawaii, parts of the western USA and Canada, Mexico and the Caribbean, South America, Europe and Asia (ISSG, 2005). In the central United States it is difficult to say for certain where natural populations end and alien populations begin, but there is no disputing the fact that all occurrences west of the Rocky Mountains are the result of translocation and release during the late 19th century and throughout the 20th. (It is known that bullfrogs were introduced to areas of California and Colorado in the early 1900s -- University of Michigan Museum of Zoology, 2005).
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Established in San Bernadino Wildlife Refuge and Leslie Canyon National Wildlife Refuge in Cochise county; also in Buenos Aires National Wildlife Refuge in Pima county
First released near Libourne then spread all over department of the Gironde, to Landes, Dordogne, Lot-et-Cher. Populations in southwest are expanding at an alarming rate
Historically the primary motive for moving bullfrogs from place to place has been to profitably cultivate them for human consumption, but there have also been many releases for less obvious reasons. There are currently websites offering to ship bullfrog tadpoles anywhere in the United States ostensibly to enliven backyard ponds. The development of irrigation networks, reservoirs, sewage settling ponds, golf course ponds, farm ponds, and man-made ponds in public parks will permit bullfrogs to take hold in many urban and semi-urban situations and this also facilitates their subsequent dispersal.
People continue to routinely transport bullfrogs from one place to another because they appear to be an easily cultivated and profitably marketable commodity for human consumption. Bullfrogs almost inevitably escape because they are, if not impossible, then certainly impractical to confine (see Liu and Lee (2009) for information on the effects of enclosure type and other factors on the risk of escape). However even in the face of wide recognition that it is not a good thing to do, some people persist in moving this ecologically damaging species from place to place for a complex of reasons that range from genuine ignorance to wilful mischief.
Bullfrogs are behaviourally and physiologically adaptable to a variety of habitats and temperature regimes. Thriving populations of thousands of individuals can arise within the first 12 months of colonization and after only a single successful spawning. Particularly in nutrient-poor (oligotrophic) ponds the algae-eating and rapidly growing bullfrog tadpoles can quite suddenly monopolize primary production (Pryor, 2003), though they are not strictly vegetarian but essentially opportunistic and adaptable omnivores that readily exploit abundant vegetation (Altig et al., 2007). At metamorphosis they convert from primarily vegetarian tadpoles to exceptionally unspecialized carnivores; prey selection above and below the water surface is determined largely by the size of potential prey and whether or not it can be swallowed. Bullfrogs also cannibalize their own tadpoles and juveniles.
Bullfrogs will colonize a wide variety of lakes, ponds, reservoir, irrigation ditches and marshes, but there are vital characteristics for supporting a population. Permanent water is necessary because bullfrog tadpoles generally take at least 12 months and as much as 48 months to reach metamorphosis; seasonal or intermittent pools, though useful as way stations for migrating bullfrogs, will probably not permit successful reproduction. Water temperature is also important because bullfrogs reproduce only in very warm water when summer temperatures exceed 25 degrees Celsius. For this reason, lakes and ponds that are not too deep < 6 m) and have good sun-exposure around the margins provide most favourable habitat for bullfrog reproduction. Riparian thickets and an abundance of aquatic and emergent vegetation are other factors that, while not vital, are often associated with thriving bullfrog populations because they provide cover and likely a more diverse prey base. However, golf course ponds with edges denuded of most riparian plants can also support healthy bullfrog populations. Acidification of waterways has been associated with bullfrog population declines in southern Ontario (Berrill et al., 1992), but the tolerance limits of bullfrogs to water chemistry extremes and various synthetic chemicals are still being explored.
Recent studies have looked at genetic markers to try to identify the geographical origin, number of founders, and number of introductions of alien, invasive bullfrog populations (Ficetola et al, 2008a; Austin et al., 2004). While this line of research has demonstrated success at achieving its scientific goal, it has not yet been applied to bullfrog management and eradication. These studies do highlight the fact that American bullfrogs are physiologically adaptable and behaviourally flexible when moved between environments that are markedly dissimilar, and that they can invade huge areas starting from only a small number of founder individuals.
Genetic evidence has also been used to investigate gender-biased dispersal in the bullfrog (Austin et al., 2003a), and to detect the presence or absence of bullfrogs by simply analysing a tablespoon of pond water for DNA emanating from mucus, faeces, urine, or decomposing bodies (Ficetola et al., 2008b).
Reproductive biology
Bullfrogs reach sexual maturity about 2 years after metamorphosis. Breeding size males attract females by advertising their location through vocalizations. To spawn, a male positions himself on the female’s back and grasps her with his forearms around the anterior thorax or axillary region. This positioning of the male relative to the female at spawning is called axillary amplexus, and is just one of many positions exhibited by frogs (Duellman and Trueb, 1986). The male has ‘nuptial pads’ of roughened skin on the outer edges of the thumbs to assist in holding on to slippery females. Once paired off they ‘spawn’ as fish do with a passive simultaneous release of eggs and sperm whereby fertilization is external. The eggs are very small, dark, and coated in proteins that immediately begin to bond with water molecules to form a protective jelly- and water-filled egg capsule. The egg mass can be anywhere from the size of a small watermelon to over 1 metre across. It is generally anchored in aquatic vegetation in shallow water and floats at the surface. The eggs usually hatch in 3 to 5 days (Bury and Whelan, 1984), but can hatch in as little as 48 hours at 26° Celsius or above (FAO, 2005).
Physiology and phenology
At higher latitudes bullfrogs mostly overwinter in the water, resting in a physiologically torpid state on the bottom of lakes and ponds where they remain until temperatures rise again in the spring. Bullfrogs are not freeze-tolerant but can withstand temperatures near to freezing. Adults become torpid in the autumn before the juveniles and at higher temperatures. Juveniles also emerge first in the spring and at lower temperatures than adults. Bullfrogs are capable of over-wintering in damp situations on land and should be able to survive quite well provided they can avoid freezing temperatures. In north temperate populations the active season for the adults can be as short as five months, but in the tropics and subtropics bullfrogs remain active year-round. In northerly populations there is a lag period after spring emergence before bullfrogs reproduce, which generally coincides with rising water temperatures to 25° Celsius and above. The spawning season is initiated by mature males finding a territory to defend and then announcing this with their vocalizations. Females then move towards the males to select mates, but not en masse (Ryan 1980). At higher latitudes, e.g. British Columbia, the spawning season lasts about 90 days and coincides with mid to late summer. Further south in the Mississippi drainage the reproductive season is three months in length, and in the tropical climates of Panama and Ecuador, bullfrogs commonly spawn year-round (FAO 2005).
Nutrition
Bullfrog tadpoles mostly graze on aquatic plants, or eat suspended matter, organic debris, algae, plant tissue, and small aquatic invertebrates. After metamorphosis, bullfrogs are carnivorous, and eat any animal (vertebrate or invertebrate) that can be captured and swallowed (including tadpoles and juveniles of their own species).
Associations
In western North America bullfrogs are often found in association with fish species with which they have co-evolved in the eastern United States. Sunfish, bass, and catfish are all non-native in the western states and western Canada but are now common throughout. The result of this fish/frog association is that the fish can indirectly facilitate bullfrog survival by, for example, depressing the densities of predatory dragonfly nymphs and diving beetle larvae that would otherwise be expected to consume large numbers of larval bullfrogs (Smith et al., 1999; Adams et al., 2003). Bahls (1992) estimates that 95% of western montane lakes and ponds formerly lacked fish, but now virtually all lakes and ponds are stocked with one or more species of non-native fish. Kiesecker and Blaustein (1998) found that when introduced bullfrogs live in association with non-native smallmouth bass (Micropterus dolomieui) they produce an amplified detrimental effect on the growth, development and survival of native red-legged frogs (Rana aurora). The mere presence of bullfrog tadpoles has also been shown to reduce survivorship in both California red-legged frog (R. draytonii, also known as R. aurora draytonii) tadpoles (Lawler et al., 1999) and Columbia spotted frog (Rana luteiventris) tadpoles (Monello et al., 2006). Murray et al. (2004) tested chemical cues from exotic bullfrogs on naive prey species and concluded that some but not all species of naive amphibian prey chemically perceive risk from bullfrog predators and have an avoidance behaviour response. Under laboratory conditions bullfrog tadpoles, in concert with the non-native red swamp crayfish (Procambarus clarkii), have also been shown to eat the eggs and larvae of the endangered razorback sucker (Xyrauchen texanus) in the western United States (Mueller et al., 2006).
At many locations in western North America, bullfrogs are found in association with populations of introduced green frogs, Rana (Lithobates) clamitans, which are also native to eastern North America. Werner et al., (1995) found that in Michigan these two species are able to co-exist even though the bullfrogs prey heavily on juvenile green frogs, because the bullfrogs are primarily aquatic foragers while adult green frogs tend to remain on land within a few metres of the water’s edge.
Beaver ponds have a beneficial effect on bullfrogs by providing new habitat (Cunningham et al., 2007), but beavers are not as widely distributed as they once were. Stock ponds in Tennessee with unrestricted access for cattle were found to support fewer bullfrog tadpoles, presumably due to various negative impacts on water quality by the cattle (Schmutzer et al., 2008).
Environmental requirements
Bullfrogs require permanent water to reproduce and over-winter, but can utilize seasonal water as way stations to facilitate migration to new lakes and ponds. Adult bullfrogs require a period of months when the water temperature remains above 17 degrees Celsius and a breeding period when water temperatures rise above 25 degrees Celsius. All age-classes of bullfrogs generally overwinter in the water and require dissolved oxygen concentrations sufficient to drive cutaneous diffusion and maintain aerobic metabolism; they have only a very limited ability to tolerate anoxic conditions (Stewart et al., 2004).
Bullfrog eggs are commonly attacked by fungi (Ruthig, 2009) and perhaps leeches (Licht 1969), while the tadpoles are preyed upon by aquatic invertebrates such as dragonfly larvae and predatory water beetles. Although fish sometimes predate bullfrog eggs, tadpoles and juveniles (Bury and Whelan, 1984; Casper and Hendricks, 2005), tadpoles avoid predation by being distasteful to many of the more widespread predatory fish, or use chemical-cued avoidance behaviour in their presence (Pearl et al., 2003). Chemical-cued avoidance behaviour is also used by bullfrog tadpoles in the presence of predatory dragonfly nymphs (Peacor, 2006). Larger aquatic-foraging garter snakes (Thamnophis spp.) might be effective predators of bullfrog tadpoles and juveniles, but garter snakes are commonly eaten by adult bullfrogs. Avian predators include herons and egrets (Ardeidae; Casper and Hendricks, 2005); various reptiles and mammals also eat bullfrogs.
Bullfrogs and their tadpoles have been implicated in the transmission of the pathogenic chytrid fungus Batrachochytrium dendrobatidis (Daszak et al., 2004; Blaustein et al., 2005; Hanselmann et al., 2004; Pearl et al., 2007; they are susceptible to infection, but appear to be immune to the lethal effects experienced by other frog species. Bullfrog tadpoles exposed to chytrid fungus appeared to behave normally (Blaustein et al., 2005). Other pathogens associated with American bullfrogs in recent studies include iridoviruses (Ranavirus), and the bacterium Mycobacterium marinum (Ferreira et al., 2006). Also of interest is the fact that when Kiesecker and Skelly (1999) infected bullfrog tadpoles with the debilitating pathogen Asterotremella humicola (Candida humicola), they found that healthy bullfrog tadpoles avoided infected conspecifics, presumably to reduce the risk of infection.
Limb malformations in frogs, including bullfrogs, have garnered considerable media attention largely due to the initial suspicion that they might be related to deteriorating water quality with potential human health implications (Souder, 2000; Lannoo, 2008). Subsequent research has shown that in many cases these malformations are the result of natural infections by the trematode Ribeiroia, though the incidence of these infections seems to have recently increased (Johnson et al.,2003). Chemical, nutrient and pesticide run-off into wetlands have also been implicated, and all evidence has been comprehensively reviewed by Lannoo (2008).
Bullfrog tadpoles will spread throughout the water bodies in which they have hatched, though they tend to seek out the warmest water. From here they can enter the inflow and outflow waterways that feed and drain lakes and ponds and therefore have a limited ability to migrate. However, because bullfrog larvae (tadpoles) are gill-breathing and entirely aquatic this life stage is unable to move out of the water on its own.
Near the end of each active season a new generation of bullfrog juveniles, recently transformed from tadpoles, aggregate around lake and pond margins waiting for warm, rainy nights. While the ground surface is wet and under the cover of darkness hundreds to thousands of these juveniles can be seen migrating en masse overland and away from the home lake. Through this risky collective impulse at least some of them will find their way to adjacent lakes and ponds to pioneer new populations. As this activity goes on throughout the late summer and autumn, juveniles seemingly run the risk of being trapped by early frosts.
Natural dispersal (non-biotic)
Deluge floods that create sudden or seasonal spillways to interlink otherwise disconnected lakes and ponds could facilitate the dispersal of bullfrog tadpoles and eggs.
Accidental introduction
Accidental introductions have occurred where bullfrogs that were meant to be confined as pets or as farm stock have escaped captivity.
It is difficult to quantify the economic impact of populations of aggressively invasive bullfrogs. They are known to threaten populations of rare vertebrates such as certain species of turtles, birds and frogs, but it is not clear how this can be translated into economic terms, for example what it is worth to people to save a population or species from extinction, or to save native aquatic ecosystems from an alien invasive that will quickly become one of the dominant species and top predators. Many people are disgusted by the very idea of large bullfrogs swallowing baby ducks or the loss of familiar spring choruses of native frogs, but it is not clear how much they are prepared to spend to have the problem fixed. The summer chorusing of dense aggregations of large male bullfrogs is sometimes identified as a source of noise pollution. However, if this is having a negative effect on real estate values or tourism the damage has yet to be quantified. Aggregations of large bullfrog tadpoles and juveniles at lake edge swimming areas are psychologically disturbing to some people, but it is not clear whether these people will lobby for the funds to have the problem fixed or they simply go swimming elsewhere. There is an interval during the initial stages of a bullfrog invasion when eradication is at its most practical but rapid response is seldom employed and so the cost of eradication becomes increasingly onerous from year to year.
Bullfrogs are prolific and aggressive competitors for space and voracious predators of a very wide variety of organisms, so displacement of native species is the primary problem that they create (Bury and Whelan, 1984; Lannoo, 2005; Santos-Barrera et al., 2009). They have a much higher critical thermal maximum than most other frogs, meaning that they are able to thrive in higher water temperature, and have a longer breeding season and a higher rate of pre-metamorphic survivorship, which also allows them to be more successful than other frogs. (They also do well with changes in the environment that have occurred due to human modification).
Consequently, their invasions are routinely identified as a principal cause of declining populations of native amphibians (Fisher and Shaffer, 1996; Hecnar and M’Closkey, 1997; Adams, 2000; Kats and Ferrer, 2003; Lannoo et al., 1994; Moyle, 1973; Hammerson, 1982), but questions have been raised about the certainty of some of these claims, as habitat modifications and the introduction of exotic predatory fish and crayfish (Mueller et al., 2006) were concurrent events which can make isolating the effects of invasive bullfrogs difficult to impossible (Hayes and Jennings, 1986). Lannoo et al. (1994) repeated an amphibian survey conducted in 1923 in Dickinson County, Iowa, USA, and concluded that the most immediate threat to the existing populations of native amphibians came from the impact of the introduced bullfrog. Bullfrogs may be a primary predator of several federally endangered waterfowl in Hawaii (Pitt et al., 2005).Schwalbe and Rosen (1988) concluded that bullfrogs negatively impact populations of native amphibians and reptiles, and at least two species of endangered fish in southeastern Arizona. The presence of bullfrog tadpoles has been shown to reduce survivorship in both California red-legged frog (Rana draytonii, also known as R. aurora draytonii) tadpoles (Lawler et al., 1999) and Columbia spotted frog tadpoles (Monello et al., 2006). Kiesecker and Blaustein (1998) found that the red-legged frog Rana aurora was negatively impacted by bullfrog larvae and adults. Hecnar and M'Closkey (1997) found that Rana clamitans populations increased greatly after bullfrog extirpation at a site in Ontario. Under laboratory conditions bullfrog tadpoles, in concert with the non-native red swamp crayfish (Procambarus clarkii), have also been shown to eat the eggs and larvae of the endangered razorback sucker (Xyrauchen texanus) in the western United States (Mueller et al., 2006).
The results of Kupferberg (1997) suggest that invasive bullfrog tadpoles can exert differential effects on native ranid and hylid frogs and perturb aquatic community structure, and Kiesecker et al. (2001) had similar findings when looking at interactions between non-native bullfrog tadpoles and tadpoles of a native ranid. However, Kiesecker et al.(2001) also suggested that human-induced habitat alteration was a key factor in properly interpreting the results. Pearl et al.(2004) confirmed differential effects of introduced bullfrogs on two species of native ranid frogs in the western United States. In Brazil there are no studies on the consequences of bullfrog introduction, although there is news that in several regions bullfrogs have been seen in the wild, near frog farms (Jim, 1995).
Further data on the negative impact of bullfrogs on other amphibians are reported by D'Amore et al. (2009 and 2010) (California) and Li et al. (2011) (China).
Bullfrogs are known to be asymptomatic carriers of the emerging pathogenic chytrid fungus Batrachochytrium dendrobatidis that has been implicated in numerous amphibian declines and extinctions (Mazzoni et al., 2003; Daszak et al., 2004; Garner et al., 2006; Adams et al., 2007; Sánchez et al., 2008; Schloegel et al., 2009). The fact that bullfrogs and bullfrog meat are transported internationally suggests that bullfrogs may be a primary vector of B. dendrobatidis (Mazzoni et al., 2003). Ranavirus is another pathogen associated with bullfrogs that has been implicated in > 90% mortality rates in free-ranging non-bullfrog amphibians (Daszak et al., 1999; Schloegel et al., 2009) and > 50% mortality amongst bullfrogs in an American ranaculture facility (Miller et al., 2007). A recent outbreak in one pond in western Japan (Une et al., 2009) involved a mass die-off of free-living bullfrog tadpoles, but no dead adult bullfrogs were found. Ranavirus now represents a serious threat to the many endemic amphibians of Japan (Une et al., 2009). There have been significant mortality events reported from bullfrog farming operations involving a variety of pathogenic bacteria (Pasteris et al., 2006). The bacterium Aeromonas hydrophila commonly infects bullfrogs in farms and in nature and the symptomatic syndrome is often called ‘red leg disease’ (Kong et al 1997).
Dense bullfrog populations can also become habitats themselves for many species of internal helminth parasites (McAlpine, 1997; McAlpine and Burt, 1998), and a haemogregarine parasite – Hepatozoon catesbianae – was recently described that appears to be transmitted directly between bullfrogs and mosquitoes (Desser et al., 1995). A trematode was taken from the large intestine of both the western garter snake (Thamnophis elegans) and the American bullfrog with leeches being the intermediate host (Nicol et al, 1985).
There have been cases of severe allergic reaction in some people who ingest the meat of bullfrogs (Hilger et al.,2002). Also, bullfrog tadpoles and metamorphs have been shown to be suitable hosts for the pathogenic bacterium Escherichia coli (Gray et al., 2007). In Japan it was found that 92% of the bullfrogs sampled were highly infected with Blastocystis, a single-celled parasite that infects the gastrointestinal tract of hosts including humans (Yoshikawa et al., 2004). The skinning of bullfrogs has been implicated in rare cases of nematode infection of humans (Quirks and Quarks, CBC Radio, Canadian Broadcasting Corporation). Studies are currently under way looking into whether bullfrogs could play a role in transmission of West Nile virus (WNV), because the virus has been isolated in many amphibian-feeding species of mosquitoes (Klenk and Komar, 2003; Danner & Phillips, 2008). An investigation of a cholera outbreak in Hunan, China, in 2006 concluded that aquatic products such as snapping turtles and bullfrogs constituted the major causes of cholera (Deng et al., 2008).
In many parts of the world where American bullfrogs are non-native, the adults are known to be hunted for food, e.g. in China. It is not known whether this utilization of bullfrogs provides an important dietary supplement or an important source of income, or is simply a recreational activity.
Economic value
Trade for human consumption and the pet trade are the two most important forms of trade in amphibians (Daszak et al., 2006). Commercial uses of bullfrogs include supplying frog meat for human consumption, biological supply house specimens for educational dissection, tadpoles and juveniles for pets, and tadpoles for fish bait. There is now a scientific basis for the oft-heard assertion that bullfrogs taste like chicken (Nóbrega et al., 2007), which partly explains why there is a persistent market demand for them. Bullfrog meat can be either consumed locally as a cheap source of protein or exported to places where it is used as a restaurant novelty or as a traditional menu item in countries like France, Belgium and Luxembourg (United Nations Statistics Division 2008) whose native frog populations are apparently no longer commercially viable. Commercial frog harvesting in France was banned in 1980 (Henley, 2009). Even the United States, where bullfrogs are native, now imports almost all its frogs’ legs (Henley, 2009) and is currently the world’s third top importer. Most are shipped into the United States alive, primarily from Taiwan, followed by Brazil, Ecuador, and China (Schloegel et al., 2009). Indonesia is also one of the world’s largest exporters of frog meat for human consumption, shipping out thousands of tons of native frogs’ legs annually. An experiment in farming American bullfrogs in Indonesia that was initiated in 1982 apparently petered out because of high maintenance costs and vulnerability of bullfrogs to disease (Kusrini and Alford, 2006). Though a number of countries have investigated the viability of commercial culturing of bullfrogs there has so far been little to show for it. Chronic problems that have yet to be solved include nutrition and disease management (Lutz and Avery, 1999). In addition, both semi-natural and artificial systems must deal with predation and cannibalism while rearing an aggressive but fragile amphibian through a complicated life cycle (Lutz and Avery, 1999). Taiwan seems to have been exceptionally successful at producing marketable bullfrogs through aquaculture after a slow start in the 1980s (FAO 2005).
Experiments are currently underway into the aquaculture of native European frogs. These involve the pool frog (Rana lessonae) and the marsh frog (R. ridibunda) as well as a hybrid of the two called the edible frog (R. esculenta [Pelophylax esculenta]). Of these, R. ridibunda has turned out to be the best candidate for farming because it fared best in captivity and reached the target weight of 30 grams. It is proposed that farmed marsh frogs could supply the domestic European market for frogs’ legs and also provide frogs for the re-establishment of populations where they have been extirpated (Barley, 2009; Neveu, 2009), and that a ready supply of domestic frogs’ legs would eliminate any future need for exotic species such as imported and disease-carrying bullfrogs. However, the taxonomic status of European “marsh frogs” is very complex (there is a complex of hybridizing species), and the introduction of these frogs for aquaculture results in hybridization and extinction of native taxa (Holsbeek et al., 2008). Critics also point out that the fish meal pellets that are fed to these captive frogs are an extravagant drain on declining fish populations (Barley, 2009).
As well as their use for food or as pets, bullfrogs are also important for medical research because their skeletal, muscle, digestive, and nervous systems are similar to those of other animals. They also help to control insect pests (University of Michigan Museum of Zoology, 2005).
Social benefit
There are no identified social benefits to populations of alien, invasive American bullfrogs. They are, however, an iconic species from their native Mississippi drainage and vicinity.
Environmental services
Marcogliese et al. (2009) use bullfrogs as their model to point out the importance of parasitism in ecotoxicological studies. Hothem et al. (2009) suggest that due to the bullfrog's widespread abundance in non-native habitats and varied aquatic diet, it should be the species of choice for all lethal biomonitoring of mercury.
The average person might find it difficult to distinguish between many species in the widely distributed and speciose family Ranidae (853 described species) because so many of them are green, brown and/or olive-coloured with black irregular patterns. In any case, colour and pattern are not the most reliable of bullfrog characteristics. Size narrows the possibilities where large adult specimens are concerned – a very big specimen is likely to be a bullfrog -- but juvenile bullfrogs can easily be mistaken for other species. The low, sonorous timbre of a male bullfrog’s advertisement call is distinctive compared to that of other frogs. It sounds more in the vocal range of a cow than a frog and amounts to multiple repetitions of “Rrrungh” that vary in volume and intensity depending upon the size of the frog and the temperature of the water in which it is sitting. Juvenile bullfrogs have a distinctive escape behaviour. They produce a characteristic “MEEP” alarm call as they propel themselves into the water when frightened. This action commonly involves skipping over the water surface by rapid multiple kicks of the hind legs before submerging and swimming away.
The Rana catesbeiana species group consists of seven species found across eastern North America (Austin et al., 2003b), six of which resemble one another to some degree and could therefore be confused with Rana catesbeiana. Unlike most European and North American ranids, such as leopard frogs (Rana (Lithobates) pipiens) and green frogs (Rana (Lithobates) clamitans), bullfrogs do not have a distinctive pair of dorso-lateral ridges. These are thin, straight-edged lines of raised glandular skin tissue that extend from directly behind the eye and above the ear covering (tympanum) and run longitudinally along both upper edges of the back, tapering out toward the upper groin. Bullfrogs do have a slightly protruding fold of skin that extends from just behind the eye and skirts the top and posterior edge of the tympanum.
Bullfrogs are transported by people from place to place, so virtually every means utilized by people to transport themselves and/or their possessions is a de facto means of dispersal for bullfrogs, e.g. aeroplanes, cars, boats, shipping crates, etc. Preventing a determined person from acquiring and transporting eggs, tadpoles, juveniles, or adult bullfrogs from place to place is as complicated as drug enforcement. Education is of some value in making bullfrog problems common knowledge, but this assumes that an informed public will voluntarily be a responsible public. Alternatively, enforced and meaningful penalties for introducing alien species should have some deterrent effect.
If bullfrogs are to be farmed, keeping them in secure enclosures at a distance from suitable habitat can reduce, but by no means eliminate, the risk of escape and establishment of feral polulations (Liu and Lee, 2009).
When bullfrogs are introduced they quickly make their presence known. The males make a distinctive call. The adults make a loud splash when they jump into the water. All age-classes crave warmth so they are conspicuously active during the day, basking in sunlight. After an initial spawning, thousands of large tadpoles, and later juveniles, crowd the sun-exposed shallows of lakes and ponds. If people can learn to identify bullfrogs by their call and by their appearance, and if they can then be motivated to report what they have seen or heard then a rapid response can be most effective. Responding rapidly is one thing and responding rapidly and effectively is another. Rapid response also requires in advance a plan of exactly what needs to be done and the resources at hand to carry out the plan without delay and on to its logical conclusion. Most jurisdictions currently have a limited budget and poor understanding of what to do. This situation can result in directing the limited money available towards actions such as studying the problem further, writing reports, and launching education campaigns -- none of which will directly address the real need of eradicating a species before it can take hold. The greater the delay in controlling the species, the more it expands.
Eradication
There is little encouragement to be gleaned from contemporary literature regarding the prospects for successfully eradicating populations of invasive bullfrogs (Adams and Pearl, 2007; Kraus, 2007 & 2009; Pitt et al 2005; Ficetola et al., 2007). Kraus (2009) subjectively rates ‘high rate of reproduction’ as the most constraining factor in controlling or eradicating bullfrogs followed by ‘crypsis’, ‘high density’, and ‘lack of control methods’. There are many examples of both successful (Nehring and Klingenstein, 2008) and unsuccessful eradication efforts (Kraus, 2009), but the successful ones generally seem to apply fairly primitive techniques, e.g. shooting, spearing, netting or fencing, with an extreme intensity of effort at relatively few sites. This approach can result in very expensive operations (Reinhart et al, 2003) that are clearly impractical on a broad regional scale involving multiple lakes and ponds and long-established populations of high density. Consequently, with few success stories to draw from, a conventional dogma has developed that bullfrog eradication is essentially impossible and could be made possible only through the spending of exorbitant and thus prohibitive amounts of money. This line of reasoning seems to discount the possibility of practical innovations coming to the rescue and therefore advises that what little money is available for bullfrog control should go into perpetual public awareness programs, monitoring, and interdiction efforts (Pitt et al., 2005). Unlike ‘eradication’ where there is an end point at which the problem is solved, choosing not to eradicate means that education, monitoring, and interdiction efforts will continue until the public becomes resigned to living with invasive bullfrogs and funding is removed.
Bomford and O’Brien (1995), speaking generally about vertebrate eradication programmes, list the following as criteria for a successful eradication: 1) proper planning; 2) socio-political commitment; 3) a removal rate exceeding replacement rate; 4) all individuals being placed at risk; and, 5) prevention of re-invasion. Clout and Veitch (2002) elaborated upon this list with two additional conditions: 1) support from local people; and 2) an ability to demonstrate the benefits of the eradication programme. Unfortunately it is not currently possible to place all individual bullfrogs at risk simultaneously – there is no easy way to round up the eggs and tadpoles in highly vegetated or otherwise obstructed habitats. Thus, the risk to bullfrog tadpoles is deferred until they metamorphose and can be readily located and captured at the surface.
A recent matrix model analysis by Govindarajulu et al. (2005) asserts that eradication programs that target adult bullfrogs will have the detrimental effect of increasing the survivorship of metamorphs by removing cannibalism as a control factor. They further recommend that targeting recent metamorphs in the autumn and egg masses in the spring would be the most profitable approach. Kraus (2009) points out that this notion has yet to be field tested. Schlaepfer et al.(2005) have proposed fast-tracking the evolution of native frog species by carefully exposing them to selective pressures that would drive an evolutionary change in their behaviour relative to the bullfrog predator, e.g. increased escape speed or increased predator detection ability. Their second management approach would then be to inoculate ‘naive’ native populations with individuals from ‘experienced’ populations.
Bullfrog invasions are not stemmed by half measures but there are modest actions that can be taken to improve the time efficiency of an eradication program. For example, keeping lake and pond margins free of debris and excessive vegetation that can impede manoeuvrability and visibility from the water will help to speed up the process of locating and capturing bullfrogs, and even when site eradication has been completed these measures will continue to assist the on-going process of monitoring and surveillance to prevent re-colonization.
Containment/zoning
When bullfrogs appeared in a pond in England in 1996, seven ponds were enclosed behind a barrier fence to prevent the post-metamorphic age-classes from escaping before they could be caught. Twelve thousand bullfrogs were ultimately removed, but at least some of the ponds were eventually filled in which hardly qualifies this as an entirely successful or eco-friendly eradication method (Banks et al.2000; Kraus 2009), as the hope is that a primary goal of bullfrog eradication is to save the habitat for returning native species. In any case, many lakes and ponds would be impossible to easily contain with a barrier fence because of uneven rocky terrain or thick vegetation - and without total containment the exercise is pointless. Containment also needs to take into account that this species can jump nine times its body length, so barriers must be more than a metre high.
Control
Although American bullfrogs are labelled as ‘invasive’ – which they are - the primary cause of almost every invasion is ‘translocation’ of bullfrogs by humans. Somehow the ecological problems created by bullfrog invasions and civic responsibilities in the face of bullfrog invasions need to be insinuated into the broader culture. Bullfrogs have a certain charisma and magnetic appeal to the mass media who generally do a more cost-effective job than government in reaching the general public and informing them about the bullfrog problem. Laws should be enacted and enforced that aim to prevent bullfrogs from being transported from place to place. The public needs to be aware of how to identify bullfrogs and where to report sightings; agencies should be prepared to act on these reports, or else the exercise is pointless and the public will feel simply manipulated. There is often community cohesion among people who live around the edges of lakes because of their common interest and investment in the environmental health of the lake. Tapping into these special interest groups can be enormously helpful for intelligence gathering prior to and during eradication and monitoring post-eradication to prevent future re-colonization by bullfrogs.
Physical/mechanical control
There are natural physical barriers to bullfrog dispersal such as thick forest, mountains, deserts, and salt water, and unnatural barriers such as busy highways. However, wherever forests have been cleared and seasonally warm freshwater is available, bullfrogs will invade and it would be very difficult to stop them by any means other than eradication. Mechanical control methods would need to be on the scale of Australia’s rabbit-proof fences, and the cost of such a barrier would far exceed the cost of manually eradicating bullfrog populations. Such barriers, on a small scale, might prevent a generation of juvenile bullfrogs from migrating out of a stock pond or golf course pond, but the barrier would also interfere with the activities of native species that seasonally migrate in and out of ponds and would be likely not to be tolerated by land owners.
Movement control
Bullfrogs are well-recognized internationally as an undesirable alien and appear on the lists of species prohibited for import or translocation. However, this fact has proven to be ineffective in controlling the translocation of bullfrogs by people once the bullfrogs are landed, released and thriving. The best way to prevent translocations thereafter would seem to be to eradicate established populations and put in place rapid response plans to prevent bullfrog populations from becoming re-established. As bullfrog numbers dwindle it can be hoped that the opportunities for and inclinations of people to move them around will also dwindle.
Biological control
Natural biological controls on bullfrog numbers range from fungi (Ruthig, 2009) and leeches that attack the egg stage, through dragonfly nymphs and predatory water beetles that prey on newly hatched bullfrog tadpoles, to piscivorous birds and small mammals that eat juvenile and young adult bullfrogs. Where the density of dragonfly nymphs is great they have been shown to be an effective predator of bullfrog tadpoles, but populations of introduced bullfrogs are commonly found in association with introduced predatory fish such as pumpkinseed sunfish (Lepomis sp.) which effectively suppress dragonfly nymph densities through predation. The lesson to be learned from the cases of bullfrogs and cane toads is that when an organism is released into the wild it can have unpredictable and often undesirable results, so the idea of developing or utilizing biological controls such as viruses, bacteria, fungi or predators has inherent dangers that must be approached with extreme caution.
Chemical control
Historically, fisheries agencies have removed so-called ‘non-game’ fish, often referred to as ‘trash fish’ or ‘coarse fish’, from lakes and ponds by poisoning the water with one of a variety of chemical formulations, e.g. toxaphene, antimycin, or activated rotenone. This technique has sometimes been referred to as ‘lake rehabilitation’. Since the larval stage of bullfrogs is entirely aquatic and takes anywhere from 12 to 48 months to reach metamorphosis, this technique would effectively kill one or more generations of tadpoles in a single treatment. It is unlikely that this form of chemical control would have much effect on adult or juvenile bullfrogs because they are able to leave the water and go somewhere else or return later. In any event, there are broad ecological consequences to this form of chemical control because it is also lethal to a host of non-target organisms. Thus, chemical control is not recommended except in the most dire circumstances or where bullfrogs are virtually the only species present during the application of the toxin.
Some chemicals released into the environment as fertilizers or pesticides could indirectly increase mortality of bullfrogs at any of their life stages. Conversely, some pesticides and contaminants are apparently harmless to bullfrog embryos and tadpoles (Pauli et al., 1999), and others can indirectly benefit bullfrogs by suppressing the densities of their predators (Boone and Semlitsch 2003) while not harming the bullfrogs. Malformations and decreased swimming performance have been noted in bullfrog tadpoles exposed to potentially toxic trace elements associated with coal combustion (Hopkins et al., 2000). The commonly available pesticide malathion may delay development of bullfrog tadpoles by decreasing thyroid function, but beyond this effect Fordham et al. (2001) found that it took unusually high concentrations to produce any other overt behavioural symptoms such as loss of equilibrium posture. When the popular pesticide Sevin was tested on bullfrog tadpoles in combination with cues from predators it was found to be 46 times more deadly than in tests excluding predator cues (Pelley, 2004).
Harvesting/hunting
It is often suggested that permitting and encouraging the harvesting of bullfrogs for human consumption would be an efficient way to control their numbers. However, there are many practical reasons why this approach will not work. For example, if a market demand for bullfrog meat or a recreational interest in hunting them is created, this becomes an argument for sustaining populations rather than eradicating them. Juvenile bullfrogs, the most abundant post metamorphic age-class, are of little interest to hunters because they have relatively little meat on them. Similarly, the egg and tadpole stages are of no interest to meat hunters.
Another prevalent notion is to control bullfrog numbers by offering a bounty on them, but this could have serious adverse consequences. For example, it introduces an untrained work force that may not be able to discriminate between invasive bullfrogs and native frogs and may do great damage to sensitive habitats; there are legal liability issues to consider if people are prompted to wander into treacherous habitats; and there is a mercenary incentive to catch bullfrogs elsewhere and bring them for profit to the region where the bounty is paid.
Monitoring and surveillance
It is essential at the planning stage of an eradication program to have up-to-date knowledge of the regional limits of bullfrog distribution. Various low-tech methods of surveying for the presence of bullfrogs are very effective, e.g. listening for calling males, searching pond margins, etc. (Heyer et al.,1994). Some high-tech methods such as sampling water for bullfrog DNA or remote-sensing listening stations have also been developed, but remain costly and therefore impractical for broad application. Monitoring and surveillance are also required after a population has been eradicated to prevent a subsequent re-colonization through bullfrog migration or capture and release by humans. However, on-going monitoring and surveillance programs that are not components of comprehensive eradication programs but are carried out for their own sake are difficult to justify. While the actual eradication of bullfrog populations is best left to professionals, post-eradication monitoring and surveillance can often be turned over to willing volunteers, particularly lakeside residents.
Ecosystem restoration
Once a lake or pond is cleared of all life-stages of bullfrogs, many native species that may have been extirpated by the presence of bullfrogs are likely to find their way back on their own if bullfrog-free habitats have persisted nearby. In the bullfrog’s own native range, Hecnar and M’Closkey (1997) reported a four-fold increase in green frog (Rana clamitans) numbers once the bullfrogs were gone. In California, D’Amore et al.(2009) reported a marked increase in the numbers of California red-legged frogs (Rana draytonii, also known as R. aurora draytonii) within the first year of bullfrog removal. There are various case studies where bullfrog removal has been carried out on a relatively small scale as part of a larger wildlife habitat restoration project (Morrison et al. 1994).
It is possible to manage areas designed for human recreation, e.g. golf course ponds, so that the survival of non-native bullfrogs and introduced predatory fish is reduced to the point where native amphibian assemblages can flourish (Boone et al. 2008). Intermittent draining of ponds is one way to accomplish this, and the results of Maret et al. (2006) suggest that manipulation or restoration of natural disturbance regimes may be a powerful tool in managing for native species threatened by biotic invasions.
There is a nearly universal agreement that American bullfrogs are one of the worst alien invasive species internationally. They are ecologically destructive and therefore eradication is acknowledged as the most desirable goal. However, there is also a collective sense of defeatism permeating all recent published discussions concerning bullfrog management (Adams and Pearl, 2007; Kraus, 2009). Adams and Pearl (2007) conclude that the “lack of obvious economic impacts” and a lack of reasonably feasible control methods inevitably translate into a lack of political will to supply the resources for large-scale management. Kraus (2009) lists some apparently successful eradication case studies that have been carried out in Europe, but then concludes that these may be exceptions to the general pattern of eradication failure. However, Kraus also observes that large-scale ecological problems are beyond the capabilities and outside the skill sets of the average volunteer organization or institutional research lab, though these are most often the people who are expected to take the initiative. In fact, eradication programs are more akin to military operations. The strategies, tactics and techniques for an effective eradication are to out-flank, out-pace, and ultimately to overwhelm your foe. Traditionally, biologists are trained to study a problem, collect data, and publish results but eradication is something quite different in the degree of dedication and improvisation required. It also needs sufficient long-term commitments from funding agencies as well as adequate support staff.
The largest gap then, with respect to knowledge/research needs, has been the lack of a reasonably feasible control method and case studies that unambiguously demonstrate success in applying the method. Beyond feasibility, practicality and affordability must be considered. It is currently difficult to quantify what it is worth to people to have populations of invasive bullfrogs controlled or eradicated. Bullfrog choruses may affect property values, or bullfrog predation may threaten the existence of native species in and around lakes and ponds, or aggregations of thousands of tadpoles and juvenile bullfrogs at swimming beaches may be intolerable to some swimmers. It is unclear, however, what is it worth to the people concerned to carry out a total eradication, and what the political profit is in championing the solving of an environmental problem before success is assured. Politicians are often more likely to fund a short-term project than a long-term one. Many conclusions on the prospects for eradication success have been based on subjective or statistical assumptions and deficient data.
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World: IUCN/SSC Global Amphibian Assessment, IUCN/SSC, International, http://www.issg.org
Italy: FAO (Food and Agriculture Organization of the United Nations), Viale delle Terme di Caracalla, 00100 Rome, http://www.fao.org/
Mexico: CONABIO - National Commission for Knowledge and Use of Biodiversity, Liga Periférico - Insurgentes Sur, Núm. 4903, Col. Parques del Pedregal, Delegación Tlalpan, 14010, http://www.conabio.gob.mx
USA: US Geological Survey - USGS, USGS National Center
12201 Sunrise Valley Drive, Reston, VA 20192, http://nas.er.usgs.gov
