Download Literature review on the American bullfrog

Literature review on the
American bullfrog
Rana catesbeiana (Shaw, 1802)
REPTIELEN AMFIBIEËN VISSEN ONDERZOEK NEDERLAND
Literature review on the American bullfrog Rana
catesbeiana (Shaw, 1802)
A report by RAVON
Invasive Alien Species Team (TIE); Ministry of Agriculture, Nature and Food Quality
A. M. Spitzen – van der Sluijs & R. Zollinger
March 2010
STICHTING RAVON
POSTBUS 1413
6501 BK NIJMEGEN
www.ravon.nl
Literature review R. catesbeiana
Stichting RAVON
Colofon
© 2010 Stichting RAVON, Nijmegen
Report nr: 2009-31.
Cover: A. van Rijsewijk & A. M. Spitzen – van der Sluijs
Text: Annemarieke Spitzen – van der Sluijs & Ronald Zollinger
For: Team Invasive Exotic Species; Ministry of Agriculture, Nature and Food Quality
Cite as: Spitzen – van der Sluijs, A. M. & R. Zollinger, 2010. Literature review on the American
bullfrog Rana catesbeiana (Shaw, 1802). Stichting RAVON, Nijmegen, the Netherlands.
Literature review R. catesbeiana
Stichting RAVON
INHOUD
SAMENVATTING ......................................................................................................................................................... 1
SUMMARY ...................................................................................................................................................................... 3
1. INTRODUCTION..................................................................................................................................................... 5
2. METHODS ................................................................................................................................................................. 7
3. THE AMERICAN BULLFROG ............................................................................................................................. 9
3.1 Origin........................................................................................................................................................9
3.2 Morphology............................................................................................................................................9
3.3 Habitat ...................................................................................................................................................10
3.4 Ecology .................................................................................................................................................10
3.4.1 Reproduction ...........................................................................................................................10
3.4.2 Density .......................................................................................................................................11
3.4.3 Diet .............................................................................................................................................11
3.4.4 Temperature.............................................................................................................................11
3.4.5 Dispersal ....................................................................................................................................12
3.4.6 Competition ..............................................................................................................................12
3.5 Alien Invasive Species and chytridiomycosis..............................................................................12
3.6 Global dispersal ..................................................................................................................................13
3.6.1 Belgium ......................................................................................................................................13
3.6.2 the Netherlands ......................................................................................................................14
4. RISKS ..........................................................................................................................................................................17
4.1 Effects on a naive ecosystem..........................................................................................................17
4.2 Risk of invasion ....................................................................................................................................17
4.2.1 Risk of settlement.....................................................................................................................18
5. MANAGEMENT ....................................................................................................................................................21
5.1 Theory ...................................................................................................................................................21
5.2 Cases ......................................................................................................................................................22
6. CONCLUSION .......................................................................................................................................................25
REFERENCES................................................................................................................................................................27
Stichting RAVON
SAMENVATTING
De Amerikaanse brulkikker (Rana catesbeiana or Lithobates catesbeianus) is een invasieve exoot en zijn
aanwezigheid kan een zeer negatieve invloed hebben op inheemse soorten door competitie om
bronnen en door predatie. De soort komt oorspronkelijk uit oostelijk Noord Amerika en is
gedurende de afgelopen eeuw in meer dan 40 landen (over 4 continenten) geïntroduceerd. In
Europa zijn in ieder geval 25 onafhankelijk introducties bekend in 8 verschillende landen.
In de jaren ’80 en ’90 waren enkele tientallen brulkikkers aanwezig in Nederland en ook nu nog
leeft er in ieder geval 1 populatie in een ommuurde tuin. In 2009 werd een brulkikker gedood in
Sint-Oedenrode (Noord-Brabant). In België lijkt de soort een sterke basis te hebben in zowel
Vlaanderen als in Wallonië.
Het is waarschijnlijk en aannemelijk dat de brulkikker Nederland binnen zal komen, zeer
waarschijnlijk via de aangrenzende populaties in Vlaanderen. De eerste kolonisaties worden dan
ook verwacht in Noord-Brabant, gevolgd door Zeeland en Limburg.
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SUMMARY
The American bullfrog (Rana catesbeiana or Lithobates catesbeianus) is an alien invasive species and its
presence can have negative impacts on native amphibian species by competition for resources and
by predation. It is native of eastern North America and has been introduced in over 40 countries
and four continents over the last century (Ficetola et al., 2007a). In Europe, at least 25
independent introductions of the bullfrog occurred in eight countries (Lanza and Ferri, 1997;
Ficetola et al., 2007b). The American bullfrog is listed on the list of ‘100 of the world’s worst
invasive alien species’
In the eighties and nineties several dozens bullfrogs were present in the Netherlands (Veenvliet,
1996) and until recently, a population of bullfrogs was known to inhabit a fenced garden pond in
the Netherlands. This year, a bullfrog sighting was reported from Sint-Oedenrode (province of
Noord-Brabant), this animal was killed. In Belgium the bullfrog seems to have gained a firm
foothold both in Flanders and in Walloon regions (Jooris, 2002a).
It is likely that the bullfrog will invade the Netherlands, most likely from the neighbouring
populations in Flanders. First colonizations might be expected especially in the province of
Noord-Brabant, followed by the provinces of Zeeland and Limburg.
The best way to control invasive species is to prevent their introduction or establishment in a new
regions, and two management options are feasible being either direct removal or habitat
manipulation.
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1.
INTRODUCTION
Human alterations to the landscape influence the habitat of many species. One far reaching
human impact is the introduction of non-native species and this threat affects virtually all
ecosystems (Vitousek et al., 1997) and is even suggested to be a leading cause of animal extinctions
world-wide (Clavero and Garcia-Berthou, 2005). The American bullfrog (Rana catesbeiana or
Lithobates catesbeianus) is an alien invasive species and its presence can have negative impacts on
native amphibian species by competition for resources and by predation. Not only amphibians are
affected by its presence, but due to an alteration of the ecosystem dynamics, its presence
influences other trophic levels as well.
Bullfrogs are representative of a large suite of non-indigenous species that are characterized by 1)
a broad invasion that is well established in some areas; 2) a lack of obvious economic impacts
compared to some other invasive species; and 3) a lack of reasonably feasible control methods
(Adams and Pearl, 2007). Biological invasions can have long time lags from introduction and
establishment to successful invasion.
In the eighties and nineties several dozens bullfrogs were present in the Netherlands (Veenvliet,
1996). Fortunately, the sale of the frogs in garden centers was quickly forbidden (EU-directive
338/97/EC) and bullfrogs were brought to shelters or killed. Until recently, a population of
bullfrogs was known to inhabit a fenced garden pond in the Netherlands. Unfortunately, the
location is kept a secret. This year, a bullfrog sighting was reported from Sint-Oedenrode
(province of Noord-Brabant). Unfortunately the specimen was not collected after being killed.
RAVON will monitor the location the coming years for the presence of more bullfrogs. Bullfrogs
have established themselves in Belgium and have approached the Dutch border quite closely. As
bullfrogs pose an enormous threat to native fauna, it is essential to have a detailed overview of its
current locations and its ecology.
Current literature study is a part of a larger risk assessment study on the presence of both the
chytrid fungus Batrachochytrium dendrobatidis and the American bullfrog in the Netherlands as alien
invasive species.
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2.
METHODS
Literature was searched using Scopus, accessed via Wageningen University. Scopus is the largest
online abstract and citation database, covering over 16,000 peer-reviewed journals. No limit in
publication year was added. Additionally the library of RAVON, accessed via ReferenceManager
was used, using similar (but in Dutch) keywords. Additionally, the references of relevant
manuscripts were searched for new articles or books.
Used keywords were: Rana catesbeiana; Lithobates catesbeianus; alien invasive species; invasive species;
wildlife trade; amphibian diseases
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3.
THE AMERICAN BULLFROG
3.1
Origin
The American bullfrog is native of eastern North America. The species has been introduced in
over 40 countries and four continents over the last century (Ficetola et al., 2007a). In Europe, at
least 25 independent introductions of the bullfrog occurred in eight countries (Lanza and Ferri,
1997; Ficetola et al., 2007b). Italy was the first country where successful introductions occurred
and this country suffers the largest number of introductions (Ficetola et al., 2007b). The IUCN
website (http://www.iucnredlist.org/details/58565) provides information on the current range of
the bullfrog and states that introduced populations are present in Belgium; Brazil; China;
Colombia; Cuba; Dominican Republic; Ecuador; France; Germany; Greece; Indonesia; Italy;
Jamaica; Japan; Malaysia; Netherlands; Peru; Philippines; Puerto Rico; Singapore; Spain; Taiwan,
Province of China; Thailand; United Kingdom; Venezuela and also in Western North America
(Santos-Barrera et al., 2009; e.g. Baxter and Stone, 1980). Free-ranging populations in Europe are
present in Belgium, France, Germany, Greece and Italy (Jooris, 2005; Lanza and Ferri, 1997;
Ficetola et al., 2007b)
3.2
Morphology
A detailed description of the morphology of the American bullfrog is given in several publications
as done by Mudde (1992) and Jooris (2005). It is a distinctive large frog (10 – 18 cm) with a large
tympanic membrane (the external ear). The frogs lack dorsolateral skin folds, but have a skin fold
from around the ear to the base of the forelegs (Stumpel and Strijbosch, 2006), which, in
combination with the very large ear-drum makes them easy to distinguish from European Rana.
The larvae become large, up till 167 mm and weigh maximally 47 grams. The mean snout-vent
length of juvenile Belgium bullfrogs measured 45.1 mm with an average weight of 12 grams
(Jooris, 2005).
Both males and females continue to grow when adult, females are larger than males. Males
become sexually mature at earlier ages and/or at smaller sizes than females (Howard, 1981). Males
mature one year after metamorphosis and females mature one or two years after metamorphosis
(Howard, 1978a).
In a natural American population, population densities of bullfrog larvae varied during the season
from 13.2 – 0.9 tadpoles per m2 pond. The mean survival rates for larvae for three populations of
bullfrog were 11.8%, 13.1% and 17.6% (Cecil and Just, 1979) which is extremely high for anurans.
For example, the survival rates from egg to metamorphosis for Rana arvalis (moorfrog) is between
0.06 – 3.45% (Lyapkov et al., 2001; Ishchenko, 1989). Van Gelder (1992) has calculated roughly
that it is only 6.4% of the ‘average frog eggs’ that survive and metamorphose and that it is 0.1%
of the ‘average frog eggs’ that survives up to adulthood.
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3.3
Habitat
The American bullfrog preferably lives in large, deep water which is densely vegetated. They
require permanent wetlands for breeding. The frog is mainly aquatic, but can spend considerable
time on land (Clarkson and Devos, 1986). It may disperse from water in wet weather. Eggs and
larvae develop in permanent slow or non-flowing water bodies (Santos-Barrera et al., 2008). In
most of the range, also in Belgium and in the Netherlands, the tadpoles of bullfrogs require more
than one year for metamorphosis, and overwinter in water (Ryan, 1953; Willis et al., 1956;
Govindarajulu et al., 2006).
Important factors for successful acclimatisation of bullfrogs in Europe appear to be presence of
several deep ponds or lakes at close distance to each other and nutrient-rich water with some
aquatic vegetation. It is also in these kinds of waters that bullfrogs can be found in Belgium.
These are mainly deep basins, intended for recreational fishing by private owners. These basins
are extremely rich in nutrients and have a well developed vegetation on the banks, but lack aquatic
vegetation. Contrary to most native amphibians, the presence of (alien) fish species does not seem
to have a negative impact on its presence (Veenvliet and Veenvliet, 2002). Ficetola et al. (2007a)
found that bullfrogs can take advantage from human modifications of land and from the increase
of permanent ponds created (Rubbo and Kiesecker, 2005; Maret et al., 2006).
3.4
Ecology
3.4.1
Reproduction
In our region most individuals start hibernation in October. During soft spells in winter,
hibernation can be interrupted. Late in spring (half April – early May) they arouse and sunbathe
on the vegetated banks. Males continuously call during summer, especially after dawn until early
morning. Calling activity strongly decreases in August and only occasionally calling males can be
heard in September. Population density is, compared to European anurans, relatively low. Males
are territorial and do not form choruses. They act aggressively towards other sexual active males
and only a few males (2 – 4) inhabit a water body (Jooris, 2005). Male parasitism occurs in
younger males, meaning that they intercept and mate with females attracted to older, larger males
instead of defending a territory and attracting their own mates (Howard, 1984).
The females produce up to 20,000 eggs in a layer of 1 egg thickness. This spawn can have a
surface of 1,000 – 2,000 cm2. After some time (approx. 20 minutes) the spawn sinks and the eggs
develop (Mudde, 1992). Larger, older, individuals produce more hatchlings than younger
individuals because of size-related advantages in competition for mates (males) or production of
large clutches (females; Howard, 1983). In Belgium the new generations appear from July –
September and is it common for the bullfrog to metamorphose after 2 years (Jooris, 2005), but
some metamorphose even later, in their 3rd or 4th year.
Older females can produce two clutches (in the USA) in one year, with the second clutches
containing fewer eggs than the 1st. It was the experience of Howard (1978b) that all females
deposited eggs within four days of each other. Their choice of oviposition sites was determined
by an a) avoidance of areas with high water temperatures (> 32°C) and b) preference for areas
that increase the developmental rate of the embryo’s and c) preference for areas that decrease the
efficiency of predation by the leech Macrobdella decora (Howard, 1978b).
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Jooris (2005) found that the juveniles migrate to suboptimal habitats after metamorphosis, small,
sometimes overshadowed pools with few or none adult bullfrogs. In Jooris’ study areas the
bullfrogs concentrated in ditches along paddocks, in the shore vegetation or in the more swampy
zones. When disturbed they jump away and call a distinctive ‘jiep’-sound. Subadult males mature
in their 4th calendar year. Also in Belgium the adults can become quite large; a male of 157 mm,
weighing 560 grams was found.
3.4.2
Density
Due to its territorial behaviour and cannibalism population densities remain low (Jooris, 2005). In
their original range of distribution the older females deposit eggs twice a year, but the second
clutch contains smaller and fewer eggs (Howard, 1978b). In contrast to the Belgium findings,
Schwalbe and Rosen (1988) mention (in Arizona, USA) high adult bullfrog densities at breeding
sites (>780 adults/ha).
3.4.3
Diet
Larvae of the bullfrog mainly forage near the banks of the pool, in the warm upper layer of the
water (Jooris, 2005). Young and subadult individuals mainly eat invertebrate prey, but adult
bullfrogs eat anything they can manage, from invertebrates and amphibians to fish, small rodents,
reptiles and birds (Corse and Metter, 1980; Albertini and Lanza, 1987; Beringer and Johnson,
1995). They also prey on their own eggs and larvae (Jooris, 2005). Preys on the banks are
approached from the water and pounced on. Larger preys are drowned before they are swallowed.
The main predator of the eggs of the bullfrog in America is the leech Macrobdella decora (Howard,
1978b), and possibly in Europe the leech Hirudo medicinalis does the same. The latter however is
extremely rare in The Netherlands . Currently this is investigated by RAVON.
3.4.4
Temperature
The American bullfrog is considered a ‘warm-adapted species’ (Bachmann, 1969), since below
15°C, adults are generally inactive, eggs will not hatch, and larvae will not develop (Viparina and
Just, 1975), although Mudde (1992) gives a broader thermal range for bullfrog activity: 8 – 37 °C.
High temperatures in summer (above 26°C) are preferred by the adults and are considered a key
determinant of suitability for bullfrogs (Lillywhite, 1970; Graves and Anderson, 1987). In the
north of their natural range (south-east Canada) American bullfrogs are reported to breed during
June and July, when air/water temperatures reach 27 °C/21 °C (Banks et al., 2000).
The adults try to maintain their body temperature between 26 – 33°C during daytime, having a
mean body temperature of approximately 30°C (Lillywhite, 1970). Despite the narrow and high
range within which bullfrogs tend to maintain body temperature, they are capable of activity over
a much broader thermal range.
Ficetola et al. (2007a) observed in their study on the development of a model to predict the risk of
invasion of the American bullfrog a bell-shaped relationship between minimum temperature and
bullfrog distribution, meaning bullfrogs are not present in areas with very cold winters (-20°C). In
January 1942 the lowest temperature in the Netherlands was measured: -24.8°C, it was then in
2005 that the temperature dropped below -20°C (-20.7°C; www.knmi.nl). The figures indicate
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these low temperatures are not common in the Netherlands, meaning winter survival is possible
for these frogs.
3.4.5
Dispersal
Post-metamorphic stages are capable of dispersing long distances and are adept at colonizing new
sites (>1200 m; Willis et al., 1956). In Smith and Green (2005) an overview is given of the
dispersal distances of many amphibian species, among which the bullfrog. Three studies are
quoted that give maximum distances recorded of 1600, 914 and 966 meter, tracked with markrecapture studies by adult individuals (Ingram and Raney, 1943; Raney,1940 and Willis et al.,
1956).
3.4.6
Competition
Bullfrogs can have negative impacts on native amphibian populations. The large tadpoles of this
species can outcompete the larvae of native species; moreover, adults are generalist predators and
also prey on other amphibians (Blaustein and Kiesecker, 2002; Kats and Ferrer, 2003). Complex
biotic interactions with native species are also possible. For example, when bullfrogs are present
the tadpoles of native frogs can alter their habitat use, therefore becoming more vulnerable to the
predation by fish (Blaustein and Kiesecker, 2002). Also, it is suspected that skin excretions of
bullfrog larvae cause reduced growth and even mortality in other amphibian species (Laufer and
Sandte, 2004).
Studies have shown that amphibian larvae grow less or metamorphose at smaller sizes when they
are raised with alien predators than when they are raised without them (Kats and Ferrer, 2003). It
is now generally accepted that alien predators can drive local populations of amphibians to
extinction (Bradford, 1991; Bradford et al., 1994; Gamradt and Kats, 1996; Matthews et al., 2001).
Surveys where alien predators and amphibians co-exist may reflect in part a more recent
colonization by the aliens (Kats and Ferrer, 2003). Hecnar and M’Closkey (1997) describe a
fourfold increase in the abundance of native green frogs (R. clamitans) upon eradication of the
invasive bullfrog.
The larvae of the bullfrog are highly competitive with native amphibian larvae, inhibiting their
growth and development (Jooris, 2005). An experimental set up testing the consumption of the
predatory fish pike (Esox lucius) and perch (Perca fluviatilis) showed that the single pike had
predated 75% of all small fish in the basin (original number: 100), 24% of the Rana ridibunda
larvae (original number: 50) and only 16% of the larvae of the bullfrog (original number: 25). The
2 perches were only kept with the bullfrog larvae and consumed 15% of the bullfrog larvae
(original number: 40), but regurgitated half of them (Jooris, 2005).
3.5
Alien Invasive Species and chytridiomycosis
The American bullfrog is listed on the list of ‘100 of the world’s worst invasive alien species’.
These species were selected using two criteria: their serious impact on biological diversity and/or
human activities, and their illustration of important issues of biological invasion (Lowe et al.,
2000).
It is not only by competition and predation that bullfrogs pose serious threats to native species,
but it is also their relative resistance to the disease chytridiomycosis, caused by the fungus
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Batrachochytrium dendrobatidis (Daszak et al., 2004). Chytridiomycosis is an emerging infectious
disease that is considered one of the main causes of global amphibian decline and extinctions
(Berger et al., 1998; Lips et al., 2006; Pounds et al., 2006) and bullfrogs are probably one of the
vectors of the expansion of this disease (Garner et al., 2006). For this reason, bullfrogs are
considered to be among the most harmful alien invasive species around the world (Lowe et al.,
2000). Plans to halt their expansion and/or new introductions are a priority for amphibian
conservation. In Great Britain, bullfrogs may have introduced chytridiomycosis into the country
(Cunningham et al., 2005).
Bullfrogs are traded in enormous amounts over the world for human consumption. The global
trade of farmed amphibians for human consumption has massively increased over the last two
decades (Daszak et al., 2006). Schloegel et al. (2009) found an overall infection prevalence of 62%
and 8.5% for B. dendrobatidis and ranaviruses in samples from freshly-imported market frogs in
three major American ports of entry (Los Angeles, San Francisco and New York). In Brazil,
bullfrog farms are likely to act as reservoirs, allowing for spread between captive and wild
populations (Schoegel et al. 2010). Similar results were found by Daszak et al. (2006). Live
amphibians imported from Asia to American cities proved to be (highly) infected with
Batrachochytrium dendrobatidis and with the ranaviral agent FV3. These studies underline the urge for
measures to be taken to prevent the spreading of diseases to native amphibians.
3.6
Global dispersal
The large native range of the bullfrog is indicative of the adaptability and success of the species
outside its normal range (Adams and Pearl, 2007). Bullfrogs have been intentionally distributed to
new habitats as a human food item (Moyle, 1973; Jennings and Hayes, 1985). The first
introductions occurred during the 1930s (Italy) and 1960s (France), but 60% of the introductions
occurred during the 1980s and 1990s. At least two introductions occurred in 1997, the year when
the introduction of the American bullfrog was forbidden in Europe (law of the European Council
2551/1997). Five introductions were performed as attempts at commercial farming. This study by
Ficetola et al. (2007b) shows an alarming increase of the presence of the American bullfrog in
Europe, probably caused by the combined effect of multiple introductions from North America,
secondary translocations within European countries and natural expansion. Despite the fact that
new introductions are forbidden by law, translocations by personal initiatives seem to be the main
cause of current introductions.
3.6.1
Belgium
In Belgium the bullfrog seems to have gained a firm foothold both in Flanders and in Walloon
regions (Jooris, 2002a). Especially in the valley of the river Grote Nete (Jooris, 2002b) the
presence of many ponds created for recreational fishing is appreciated by the bullfrogs. The larvae
can originally be imported accidentally with exotic fish or they can deliberately be released. Until
1977 the American bullfrog could be bought on a nearby market. Since the ban on the import of
these frogs (22 Dec. 1997- EC regulation 338/97) hardly any, or even no frogs were sold
anymore. The fish ponds provide a good habitat for the bullfrogs, as they provide a relative warm
and sheltered habitat with a suitable microclimate (Jooris, 2002a). During surveys hardly any
native frogs were found at bullfrog locations. This can be explained by the presence of the
bullfrogs, but also by the presence of many (and high concentrations of) (exotic) fish and maybe
the relatively unsuitable form of shores (very steep) and water quality (eutrophic). The possibility
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for the bullfrogs to expand in these areas (via the river and its contributories, ditches and ponds)
poses threats for more vulnerable areas with native amphibians.
Currently, the bullfrogs in Belgium are restricted to shallow, warm ponds on sandy soils and in
valleys, which are relatively eutrophic . Deep and cold water can limit the growth of the larvae
increasing the predation rate. This could have influenced the current distribution of the bullfrog
in Belgium, but this is very likely also highly influenced by human activities.
3.6.2
the Netherlands
The bullfrogs are very close to the Netherlands (figure 2), and it is very likely that they have
entered the Netherlands already. In 2008 a bullfrog was heard (bullfrogs make a distinctive sound
when entering the water upon disturbance (paragraph 3.4.1)) entering the water in the river Mark,
which enters The Netherlands south of Breda in the province of Noord-Brabant (Spitzen – van
der Sluijs, 2008 pers. obs.), close to the Dutch border (< 2km).
In the eighties and nineties of the previous century, American bullfrogs were for sale in the
Netherlands. Soon the sale was stopped and approximately 45 bullfrogs were brought to shelters.
Veenvliet (1996) notes that 7 adults and nearly 200 larvae were registered as ‘free-living’
individuals..
Figure 1. Newspaper article on the recent sighting of a bullfrog in Noord Brabant
From an Amsterdam garden pond a reliable sighting in 2002 of a single bullfrog exists. In 2009 it
was reported that in 2006 a bullfrog was captured in ‘het Wormdal’ in the province Limburg. In
the period 1971 – 1995 three times successful reproduction has been registered. At least up till
2003 reproducing animals were present in two open-air terrariums in the province Limburg. Even
though these are not free ranging specimens, it means that the bullfrog can survive in The
Netherlands (Veenvliet, 2009). This year (2009), a single adult bullfrog male was reported from
Sint-Oedenrode near the valley of the Belgian-Netherlands small river Dommel (province of
Noord-Brabant; figure 1). This animal was shot, but not collected. RAVON will monitor the
location the coming years for the presence of more bullfrogs. The origin of this specimen is
unknown.
In Veenvliet (2009) an overview is given on the sightings of bullfrogs in the Netherlands (figure 3;
from: Veenvliet, 2009). Several locations are not mentioned, such as historical sightings by Van
Diepenbeek (pers. comm.) in Veghel (eastern part province Noord-Brabant) in 1991 and by Van
Rijsewijk in June 1997 (pers. comm.) in the ‘Wilhelminapark’ in Tilburg, (figure 4; map from
www.telmee.nl; accessed 26March2010; see also Spitzen – van der Sluijs and Zollinger, 2010).
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Figure 2. The black dots resemble square kilometers where bullfrogs have been sighted in Flanders from 1995
till now. From: http://www.hylawerkgroep.be/index.php?id=94#verspreiding. Accessed 11 Jan. 2010
Figure 3. All sightings of American bullfrogs in the
Netherlands from: Veenvliet (2009).
■ 1971 - 1995
● 1996 - 2007
Figure 4. Additional validated sightings of the American
bullfrog in 1991 and in 1997 (green squares). From:
www.telmee.nl
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4.
RISKS
4.1
Effects on a naive ecosystem
The influence of an invasive species, not only influences amphibians, but impacts numerous fresh
water taxa. The natural predators of the amphibians are affected too, by a severe decrease in prey
items (Matthews et al., 2002). The presence of this frog can have a significant impact on other
amphibian species. In North America in particular, its introduction to new areas has, in
combination with habitat changes and the introduction of non-native fish, been linked with
declines in other amphibian species. In California, examples include declines of red-legged frog R.
aurora and yellow-legged frog R. boylii (Moyle, 1973). Bullfrog tadpoles reduced the percentage
survival and body mass at metamorphosis of both species (Kupferberg, 1997; Kiesecker and
Blaustein, 1997). Bullfrogs have also been linked with declines of the plains leopard frog R. blairi
and the northern leopard frog R. pipiens in Colorado, and the spotted frog R. pretiosa in the Pacific
north-west of America (Hammerson, 1982).
The invasiveness of American bullfrogs is enhanced by the presence of invasive fish species. This
indirect, faciliatory relationship between two non-native vertebrates was studied by Adams et al.
(2003). Combining efforts in the reduction of the distribution and numbers of bullfrogs and
exotic fish species such as sunfish(Lepomis gibbosus), will enhance the success rate.
It is known that bullfrogs are effective generalist predators and interspecific larval competitors,
and it is thought that through these mechanisms bullfrogs negatively affect local communities
(Kats and Ferrer, 2003). However, bullfrogs coexist with many species of amphibians while
preying on or competing with them (McAlpine and Dilworth, 1989; Hirai, 2004; Laufer and
Sandte, 2004). This suggests that predation and competition may not be the only explanations for
declines associated with bullfrog introductions.
Since bullfrogs are vectors for B. dendrobatidis (paragraph 3.5), disease, predation and competition
all influence native species after a bullfrog introduction. The latter two can be eliminated with the
successful removal of bullfrogs from an ecosystem, but the removal of B. dendrobatidis from the
environment has not yet been accomplished (Garner et al., 2006). Until now, no European
evidence is presented that, due to the presence of the American bullfrog, native amphibian
populations decrease in population size. However, the predation pressure on native species can
not be underestimated (Jooris, 2005).
4.2
Risk of invasion
Invasion depends on environmental characteristics that may predispose a habitat to invasion. A
model developed by Ficetola et al. (2007a) predicts a medium suitability for the largest part of the
Netherlands for the invasion of the American bullfrog (figure 5). Nonetheless, the southern parts
of the Netherlands (figure 5) are at higher risk. It is also clear that the ongoing climatic changes
alter the suitability of an area. The main focus for the Netherlands should be firstly aimed at the
southern provinces Zeeland, Noord-Brabant and Limburg, all adjacent to the Belgian border.
17
Literature review R. catesbeiana
Figure 5 (a) Worldwide projection for the environmental suitability for bullfrogs. (b) Projected
suitability in the areas of Europe where bullfrog introductions occurred. Squares: invasive
populations; circles: non-invasive populations. From: Ficetola, et al. (2007a)
Population invasiveness (Ficetola et al., 2007b) is positively related to the number of amphibian
species recorded in the community. This is contrary to what would be observed if the richest
communities were more resistant to invasion. As the American bullfrog is a vector for B.
dendrobatidis, the positive association of bullfrog invasions with areas of high richness of
amphibians is a cause of particular concern for the fate of native species (Ficetola et al., 2007b).
4.2.1
Risk of settlement
A study by D’Amore et al. (2010) showed that an invasive species is favoured over the native
species in sites with hydrological alteration, landscape-level habitat fragmentation and degradation
of the habitat. The bullfrog has the capability to invade an ecosystem from only a very small
number of founders (Ficetola et al., 2008a). Most non-native populations derive from less than six
females. Once bullfrogs colonize a habitat they are difficult to remove and their effects on aquatic
systems are long-lasting (Bury and Luckenbach, 1976; Todd, 2001).
Mudde (1992) does not think that the American bullfrog can settle permanently in The
Netherlands, due to the unpredictable winter temperatures (cold, warm, cold) and the warmth
needed for successful reproduction. Veenvliet (1996) agrees with this and poses the proposition
that a geographic form was introduced that was not resistant to our climate. These insights seem
to be out of date, as in Belgium just on the other side of the border, the bullfrog can maintain
itself extremely well. Our climate does not seem to be an inhibiting factor, which is confirmed by
Stumpel (1992) who describes the population at Breda as reproducing very well under our climatic
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conditions. In a large garden pond 5 larvae from Belgium were introduced in 1986 and in 1990
160 larvae in several life-stages were caught.
Summarizing, it is likely that the bullfrog will invade the Netherlands, most likely from the
neighbouring populations in Flanders. First colonizations might be expected especially in the
province of Noord-Brabant, followed by the provinces of Zeeland and Limburg. The provinces
of Noord-Brabant and Limburg are the most amphibian species rich of all Dutch provinces (Van
Delft, 2009) and the southern part of Zeeland adjacent to Belgium harbours important
populations of the Red List species Triturus cristatus and Hyla arborea (Arntzen and Smit, 2009;
Stumpel et al., 2009). Only a handful reproductive females and one or a few males, that could stay
unnoticed for several years, are sufficient to establish a population, which could be difficult to
eradicate.
19
Literature review R. catesbeiana
20
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5.
MANAGEMENT
5.1
Theory
Species with the ability to become invasive from only a small number of founder animals, should
be identified at an early stage of introduction and challenges usual management strategies. It is
generally accepted that establishment and invasion risk increases with large propagule pressure
(Colautti et al., 2006). This could lead to the assumption that the introduction of only a few
individuals will not pose a risk. Similar reasoning may occur during eradication programmes. For
example, if during bullfrog eradication, just a handful of adults remain, a new invasion is highly
probable in a few generations, rendering previous management action ineffective (Ficetola et al.,
2008a).
The best way to control invasive species is to prevent their introduction or establishment in new
regions. This is because it is often difficult to detect new invasions early and eradication is much
more realistic for species with a limited distribution (Simberloff et al., 2005). Ficetola et al. (2008b)
developed a new method for the detection of secretive species by a novel approach, based on the
limited persistence of DNA in the environment. When bullfrog presence is suspected in Dutch
waters, this analysis could quickly give a definitive answer.
Whatever the method, success seems to depend to a large extent on the size of the water body
involved (Nomi, 2001). Adams and Pearl (2007) suggest two management options: 1) direct
removal and 2) habitat manipulation.
Direct removal. The high fecundity, density dependence, and evasiveness of bullfrogs, along with
the complexity of invaded wetlands, often make direct removal difficult. Even in small and
relatively simple ponds, direct manual removal may need to be coupled with other activities to
eradicate or control a population (Banks et al., 2000; Doubledee et al., 2003). Still, such actions are
warranted in situations where bullfrogs are threatening an endangered species and in the early
stages of invasion. Direct removal will be more effective for small, isolated ponds where removal
can be complete and reinvasion by overland dispersal is less likely.
Habitat manipulation can be viewed as a technique to indirectly reduce or eliminate bullfrogs.
Protecting and maintaining ephemeral habitats, reduces the risk of bullfrog settlement. Bullfrogs
overwinter as larvae in many regions and they generally depend on permanent waters for larval
growth. In Italy, changed water management due to changing agricultural activities in the Po
Valley has successfully reduced or even eliminated bullfrog presence (Veenvliet and KusVeenvliet, 2002). How to use drying rotations to reduce bullfrogs without harming natives (also
among other taxonomic groups) in wetlands is poorly known (e.g. Maret et al., 2006). Care must
be taken to time draining such that there will not be selection for rapid development of larval
bullfrogs. This means draining the pond fast enough and early enough to prevent any rapidly
developing portion of the population from reaching metamorphosis. Whether there are habitat
features other than hydroperiod that can be manipulated to control bullfrog density is an open
question.
Depending on location and habitat, different management techniques are feasible. Draining
livestock grazing ponds is possible, but draining larger wetlands is often too detrimental for other
21
Literature review R. catesbeiana
organisms. Shooting is an option in those cases (Schwalbe and Rosen 1988; Rosen and Schwalbe
1995). In their model simulations Doubledee et al. (2003) calculated that the combined
management strategy of pond draining and the shooting of adults (once a year), will drive
populations extinct within 10 years. Combining these management techniques was much more
successful than either strategy independently. Even shooting at low effort, significantly decreased
adult bullfrog densities by 80%. Govindarajulu et al., (2005) state that killing metamorphs in fall is
the most effective method of decreasing bullfrog population growth. The partial removal of
tadpoles may lead to higher tadpole survival and development rates and higher postmetamorphic
survival due to decreased density-dependent competition. Removal of adults leads to higher
survival of early metamorphic stages through reduced cannibalism.
Bullfrogs often co-occur with sunfish. These fish have an effect on pond communities that
bullfrogs exploit: they reduce the size and abundance of macroinvertebrates that can be major
predators of bullfrog larvae (Werner and McPeek, 1994; Skelly, 1996). Research in America has
shown that invasive bluegill (Lepomis macrochirus) increase the survival of bullfrog tadpoles by
reducing the abundance of indigenous aeshnid dragonfly larvae (Adams et al., 2003). Survival of
bullfrog tadpoles was 0% in experimental enclosures that lacked bluegill but had aeshnids;
compared to 20% survival in enclosures with both bluegill and aeshnids. This suggests that
reducing or eliminating bluegill and perhaps other similar centrarchid fish could be a way to
reduce or eliminate bullfrog populations. Moreover, limiting the spread or intentional
introduction of such ‘‘facilitator’’ species may help limit the spread or abundance of bullfrogs.
5.2
Cases
Successful eradication was performed in at least three cases, while in 11 further cases bullfrogs
disappeared after the introduction (Ficetola et al., 2007b). Two of the successful eradications (UK
and Germany) coped killing individuals (adults and tadpoles) and complete drainage of ponds
where the population was breeding. In the third successful eradication (Germany) a complete
fencing of the breeding pond was performed in addition to the killing of individuals (Thiesmeier et
al., 1994). The three successful attempts have been performed at early stages of invasion and by
means of strenuous destruction or fencing of all breeding wetlands (Ficetola et al., 2007b).
The costs of bullfrog eradication will be limited when executed in an early stage, but will increase
later on. Nonetheless, the economic costs of the loss of native amphibians and/or restoring
damaged ecosystems are always
higher.
In Germany, five infested ponds were
pumped out twice, with the help of
20 volunteers and the local fire
department. Adults bullfrogs and
tadpoles were removed. In addition,
these ponds were electronically fished
Figure 6. Costs of eradication of the bullfrog, when starting
twice (Weizmann, 2002). Costs for
in the future, from: Reinhardt et al (2003).
these measures were: 20 volunteers,
working occasionally over the course of a year (roughly the equivalent of one full-time employee,
hence € 50,000,-). Costs to pump out and electrofish was € 500,- and € 1,200,- per day,
respectively. This predicts an annual cost of € 53,000,- per pond per year (Reinhardt et al., 2003).
22
Stichting RAVON
Reinhardt et al. (2003) calculated that eradicating bullfrogs in Germany would grow exponentially
(figure 6) with time. Starting control management early upon establishment, is most cost efficient.
Direct removal: Banks et al. (2000) installed fences around the main ponds to limit dispersal and
used lamps to collect adult frogs at dusk. They then drained the ponds and excavated the
sediment to remove remaining frogs and larvae. This effort apparently did not result in complete
eradication: limited breeding was detected the following summer, and post metamorphic bullfrogs
were found in the vicinity two years after management. Another direct removal effort that has
been partially documented in the literature is in ponds that are relatively isolated in a desert
landscape in Arizona, USA (Schwalbe and Rosen, 1988; Rosen and Schwalbe, 1995). They used
funnel traps, gigs, guns, and hand capture to remove bullfrogs annually. Reductions in bullfrog
densities were said to be small and short-lived.
Habitat management/manipulation: Maret et al. (2006) found that drying could be used to
eliminate bullfrogs in some livestock watering ponds. Pond drying was also effective for local
elimination of non-indigenous fish (Maret et al., 2006) as was also successfully done in a Dutch
moorland pool to eradicate sunfish (Bosman, 2004), which can interact with bullfrogs in ways
detrimental to indigenous amphibians(Kiesecker and Blaustein, 1998; Adams et al., 2003).
In Britain a large eradication project was undertaken in 1999 in an attempt to eradicate the
population of American bullfrogs that was still fairly localised. The ponds were surrounded by a 1
meter-high, plastic frog-proof fence and visited at dusk to capture bullfrogs. Captured individuals
were anaesthetised using Benzocaine and promptly dispatched. Terrestrial activity of froglets was
greatest on mild (> 10°C) damp evenings. They congregated around the inner perimeter of the
frog-proof fence and were easy capture by hand, with 477 animals caught in one night. Bottle
traps placed in the pond, and carpet sections placed on land as refugia however caught relatively
few frogs. The ponds were drained in December 1999 in order to eliminate the remaining
tadpoles and allow a significant number of the remaining frogs to be captured by hand in the
mud. The frogs did not accumulate in the central hollow, but remained in burrows in the mud
throughout the pond, among stands of emergent vegetation, under collapsed mats of green algae
and water plants lying over deep silt and litter. The bullfrogs were most frequent in deeper
‘mudslide’ areas of silt below steeper rocky banks. Finally, the ponds silt was excavated, buried
and covered in compacted soil. Small numbers of bullfrogs were found hibernating on land
around the margin of the enclosure fence. By the end of 1999, 4,744 tadpoles, 2,269 froglets and
an adult female bullfrog had been captured (Banks et al., 2000).
When breeding is suspected, ponds may need to be enclosed promptly in a frog-proof fence, the
ponds drained (preferably before the tadpoles are able to metamorphose) and any frogs or
tadpoles collected. This is most feasible on small water bodies. Should bullfrogs become
established in more extensive wetlands, control is likely to be very difficult (Banks et al., 2000).
23
Literature review R. catesbeiana
24
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6.
CONCLUSION







The persistence of American bullfrog populations is enhanced by alien fish species
Human alternated habitats that retain water year-round are specifically prone to bullfrog invasion
Bullfrogs negatively impact native species by competition, habitat modification and possibly by
introducing Batrachochytrium dendrobatidis to a site
Considering dispersal capacity, the closeness of Belgian populations and their possibility of
survival and reproduction, bullfrogs are likely to invade the Netherlands
Therefore we suggest the promotion of educational programs to reduce the risk of new
introductions and translocations from established populations.
Careful monitoring is necessary for the early detection and management of newly established
populations.
Eradication can especially be successful in small isolated ponds by direct elimination and habitat
management and especially in early stages of colonisation.
25
Literature review R. catesbeiana
26
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