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An invasive population of Xenopus laevis in Italy

Herpetozoa

January 2005

Authors:

Francesco Lillo

No istitution

Federico Marrone

Università degli Studi di Palermo

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Xenopus laevis (DAUDIN, 1802) in Italy Several papers indicate that introduc-tions of allochthonous species are a major threat for autochthonous biota and natural zoogeographical status of regions (e.g., IUCN 2000; MACK et al. 2000). Up to now, the allochthonous amphibians known from Italy are: American Bullfrog Rana cates-beiana SHAW, 1802, Balkan Frog Rana kurt-muelleri GAYDA, 1940, and Marsh Frog Rana ridibunda PALLAS, 1771 (SCALERA 2003). This note reports the occurrence in Italy of a new allochthonous anuran, the African Clawed Frog Xenopus laevis (DAUDIN, 1802). In numerous subspecies Xenopus laevis occurs throughout the Afro-tropical region (TINSLEY et al. 1996). Among these, only the nominate race seems to constitute feral pop-ulations outside the original distribution area; populations are known to occur in the USA, Chile, Ascension Islands, Wales, Germany, the Netherlands (TINSLEY & MCCOID 1996) and France (ACEMAV et al. 2003). Although a recent study proved this taxon to successfully colonize temperate cli-mate regions (FOUQUET & MEASEY, submit-ted), the African Clawed Frog seems to have established its most abundant and invasive populations in those areas with a Mediter-ranean climate, like central Chile (LOBOS & MEASEY 2002) and the southwestern USA (CRAYON, in press). The ease with which it breeds, the short time needed for attaining sexual matu-rity, its resistance to diseases and infections, along with its adaptability to extreme condi-tions, explain its worldwide diffusion as a pet and a laboratory animal and the possi-bility of accidental or deliberate releases in the wild (GURDON 1996). Moreover, this species usually feeds on invertebrates (MEASEY 1998) but can also actively prey on vertebrates, as was observed in California on an endemic goby (LAFFERTY & PAGE 1997) and on Bufo, Rana and Hyla tadpoles and juveniles (CRAYON, in press). Xenopus laevis is also known to be highly cannibalistic (MEASEY 1998). Although it is considered a potential threat for native fresh-water fauna (BEEBEE 1996), no exhaustive studies have been carried out in order to quantify the real impact of the African clawed frog on the autochthonous biota. Except for two specimens of X. laevis stored in the "Museo Regionale di Storia Naturale e Mostra permanente del Carretto siciliano" (Terrasini, Palermo district, Sicily) labelled "Diga Iato 5 Settembre 1999", no data about the actual presence of a viable Italian population of this taxon are available. In June 2004 individuals of the African Clawed Frog were for the first time observed in the drainage area of the "Fiume Iato", a river originating in the "Monti di Palermo" area (Sicily, southern Italy) and, after flowing 25 km through an agricultural landscape, drains into the Tyrrhenian Sea. In the 1960's, the "Lago Poma" reservoir was built by damming Iato River to supply irrigation and drinking water. The reservoir lies at 197 m a.s.l., its volume is about 78 * 10 6 m 3 , the mean and maximum depths being 12.9 m and 46.8 m, respectively (CALVO et al. 1993). The uppermost part of the river is characterized by a variable water flow, which reaches its higher values during late autumn and early winter thanks to precipita-tion, and the lower ones at the beginning of autumn because of summer drought. Beyond the dam, the river discharge is high-ly reduced. The depth of the upper part of the river ranges from a few centimetres to more than 1.5 m and the river bed is 1.5 to 4 m wide. The river banks are covered with riparian vegetation and the most common aquatic macrophytes are filamentous algae. A high number of agricultural ponds is present in the catchment area of the reser-voir and their average surface is 1200 m 2 . They are located 30 -2000 m from the river, with their altitudes differing from that of the river by up to 250 m. The environmental features of these ponds are extremely varied concerning size, turbidity and presence of macrophytes. All the surrounding land is extensively farmed with vineyards and olive-groves. No "ecological corridors" such as irrigation ditches, channels, hedges or uncultivated fields are present. From June to October 2004 field sur-veys were carried out in Fiume Iato, in the "Lago Poma" reservoir and in thirteen agri-cultural ponds in the reservoir watershed. In each site, the presence of X. laevis was SHORT NOTE HERPETOZOA 18 (1/2) Wien, 30. Juni 2005 SHORT NOTE 63

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An invasive population of Xenopus

laevis (DAUDIN, 1802) in Italy

Several papers indicate that introduc-

tions of allochthonous species are a major

threat for autochthonous biota and natural

zoogeographical status of regions (e.g.,

IUCN 2000; MACK et al.2000). Up to now,

the allochthonous amphibians known from

Italy are: American Bullfrog Rana cates-

beiana SHAW, 1802, Balkan Frog Rana kurt-

muelleri GAYDA, 1940, and Marsh Frog Rana

ridibunda PALLAS, 1771 (SCALERA 2003).

This note reports the occurrence in Italy of a

new allochthonous anuran, the African

Clawed Frog Xenopus laevis (DAUDIN,

1802).

In numerous subspecies Xenopus laevis

occurs throughout the Afro-tropical region

(TINSLEY et al. 1996). Among these, only the

nominate race seems to constitute feral pop-

ulations outside the original distribution area;

populations are known to occur in the USA,

Chile, Ascension Islands, Wales, Germany,

the Netherlands (TINSLEY & MCCOID 1996)

and France (ACEMAV et al.2003).

Although a recent study proved this

taxon to successfully colonize temperate cli-

mate regions (FOUQUET & MEASEY, submit-

ted), the African Clawed Frog seems to have

established its most abundant and invasive

populations in those areas with a Mediter-

ranean climate, like central Chile (LOBOS &

MEASEY 2002) and the southwestern USA

(CRAYON, in press).

The ease with which it breeds, the

short time needed for attaining sexual matu-

rity, its resistance to diseases and infections,

along with its adaptability to extreme condi-

tions, explain its worldwide diffusion as a

pet and a laboratory animal and the possi-

bility of accidental or deliberate releases in

the wild (GURDON 1996).

Moreover, this species usually feeds on

invertebrates (MEASEY 1998) but can also

actively prey on vertebrates, as was observed

in California on an endemic goby (LAFFERTY

& PAGE 1997) and on Bufo,Rana and Hyla

tadpoles and juveniles (CRAYON, in press).

Xenopus laevis is also known to be highly

cannibalistic (MEASEY 1998). Although it is

considered a potential threat for native fresh-

water fauna (BEEBEE 1996), no exhaustive

studies have been carried out in order to

quantify the real impact of the African

clawed frog on the autochthonous biota.

Except for two specimens of X. laevis

stored in the “Museo Regionale di Storia

Naturale e Mostra permanente del Carretto

siciliano” (Terrasini, Palermo district, Sicily)

labelled “Diga Iato 5 Settembre 1999”, no

data about the actual presence of a viable

Italian population of this taxon are available.

In June 2004 individuals of the African

Clawed Frog were for the first time observed

in the drainage area of the “Fiume Iato”, a

river originating in the “Monti di Palermo”

area (Sicily, southern Italy) and, after flowing

25 km through an agricultural landscape,

drains into the Tyrrhenian Sea. In the

1960’s, the “Lago Poma” reservoir was built

by damming Iato River to supply irrigation

and drinking water. The reservoir lies at 197

m a.s.l., its volume is about 78 *106m3, the

mean and maximum depths being 12.9 m

and 46.8 m, respectively (CALVO et al.

1993). The uppermost part of the river is

characterized by a variable water flow,

which reaches its higher values during late

autumn and early winter thanks to precipita-

tion, and the lower ones at the beginning of

autumn because of summer drought.

Beyond the dam, the river discharge is high-

ly reduced. The depth of the upper part of

the river ranges from a few centimetres to

more than 1.5 m and the river bed is 1.5 to 4

m wide. The river banks are covered with

riparian vegetation and the most common

aquatic macrophytes are filamentous algae.

A high number of agricultural ponds is

present in the catchment area of the reser-

voir and their average surface is 1200 m2.

They are located 30 - 2000 m from the river,

with their altitudes differing from that of the

river by up to 250 m. The environmental

features of these ponds are extremely varied

concerning size, turbidity and presence of

macrophytes. All the surrounding land is

extensively farmed with vineyards and

olive-groves. No “ecological corridors”

such as irrigation ditches, channels, hedges

or uncultivated fields are present.

From June to October 2004 field sur-

veys were carried out in Fiume Iato, in the

“Lago Poma” reservoir and in thirteen agri-

cultural ponds in the reservoir watershed.

In each site, the presence of X. laevis was

SHORT NOTE HERPETOZOA 18 (1/2) Wien, 30. Juni 2005 SHORT NOTE 63

All_Short_Notes18_1_2.qxd 10.08.2005 12:46 Seite 3

verified on different dates by visual survey

of surfacing frogs and catching tadpoles,

juveniles and adult specimens by means of

dip nets. On the whole, observations have

been performed in 29 sites: 10 along the

river above the reservoir, five below the

reservoir, 13 in agricultural ponds, and one

in the reservoir, near the inlet of the river.

Several adult specimens of different

size, juveniles and tadpoles were found in

the river above the reservoir (eight sites out

of 10, covering seven km of the river basin),

in the reservoir itself and in most of the sur-

veyed agricultural ponds (nine sites out of

13). The maximum distance between the

riverbed and a colonized pond was about

1000 m; the large number of ponds likely

constitutes a stepping-stone web for migrat-

ing animals as already observed in France

(FOUQUET & MEASEY, submitted). It is note-

worthy that X. laevis was not observed in

any site between the dam of the reservoir

and the mouth of Fiume Iato.

The occurrence of a viable population

of X. laevis in Sicily is confirmed by the

capture of a large number of individuals

belonging to different size-classes, adults,

tadpoles and juveniles. Although no attempt

was performed to evaluate the number of

individuals occurring in the Fiume Iato

drainage area, in some of the study sites sev-

eral dozens of individuals and large swarms

of tadpoles were observed.

The presence of two individuals stored

in the “Museo di Terrasini” suggests that the

invasion should date back at least to 1999.

Further studies are needed in order to get a

better understanding of the real status and

diffusion of this species in Sicily and to

evaluate the potential threat to the autoch-

thonous freshwater fauna. Such a study is

of immediate importance as the African

Clawed Frog has been shown to be capable

of rapidly establishing very large popula-

tions in regions characterized by a Mediter-

ranean climate (MCCOID & FRITTS 1995;

LOBOS & JAKSIC 2005).

ACKNOWLEDGEMENTS: We are especially

grateful to John MEASEY (Laboratoire d’Ecologie des

Sols Tropicaux, Bondy Cedex, France), Luigi NASELLI-

FLORES (University of Palermo, Italy) and Antonio

ROMANO (University of Rome “Tor Vergata”, Italy) for

their useful contribution to the draft of this note.

REFERENCES: ACEMAV coll. & DUGET, R. &

MELKI, F. (eds.) (2003): Les amphibiens de France,

Belgique et Luxembourg; Collection Parthénope, édi-

tions Biotope, Mèze (France), 480 pp. BEEBEE, T. J. C.

(1996): Ecology and conservation of amphibians;

London, (Chapman & Hall), VIII + 214 pp. CALVO, S.

& BARONE, R. & NASELLI-FLORES, L. & FRADÀ ORE-

STANO, C. & DONGARRÀ G. & LUGARO, A. & GENCHI, G.

(1993): Limnological studies on lakes and reservoirs of

Sicily; Naturalista siciliano, Palermo; (Ser. 4) 17

(Suppl.): 1-292. CRAYON, J. J. (in press): Species

account: Xenopus laevis; In: LANNOO M. J. (ed.): Status

and conservation of U.S. amphibians; University of

California Press (Berkeley). FOUQUET, A. & MEASEY, G.

J. (submitted): Plotting the course of a African clawed

frog invasion in Western France. GURDON, J. B. (1996):

Introductory comments: Xenopus as a laboratory ani-

mal; pp. 3-6. In: TINSLEY, R. C. & KOBEL, H. R. (eds.):

The biology of Xenopus. Oxford (Oxford Univ. Press),

440 pp. IUCN (2000): IUCN Guidelines for the pre-

vention of biodiversity loss caused by alien invasive

species - Approved by the 51st meeting of the IUCN

council; Gland (Switzerland). LAFFERTY, K. D. & PAGE,

C. J. (1997): Predation on the endangered Tidewater

Goby, Eucyclogobius newberryi, by the introduced

African Clawed Frog, Xenopus laevis, with notes on the

frog’s parasites.- Copeia, Washington, D.C.; 1997 (3):

589-592. LOBOS, G. & JAKSIC, F. M. (2005): The ongo-

ing invasion of the African clawed frog (Xenopus laevis)

in Chile: causes of concern.- Biodiversity and

Conservation, Dordrecht; 14: 429-439. LOBOS, G. &

MEASEY, G. J. (2002): Invasive population of Xenopus

laevis (DAUDIN) in Chile.- Herpetological Journal,

London; 12: 163-168. MACK, R. & SIMBERLOFF, D. &

LONSDALE, M. & VANS, H. & CLOUT, M. & BAZZAZ, F.

(2000): Biotic invasions: causes, epidemiology, global

consequences and control.- Ecological Applications,

Tempe, New York; 10: 689-710. MCCOID, M. J. &

FRITTS, T. H. (1995): Female reproductive potential and

winter growth of African Clawed frogs (Pipidae:

Xenopus laevis) in California.- California fish and game,

Sacramento; 81: 39-42. MEASEY, G. J. (1998): Diet of

feral Xenopus laevis (DAUDIN) in South Wales, U.K;

Journal of Zoology, London; 246: 287-298. SCALERA,

R. (2003): Anfibi e rettili italiani. Elementi di tutela e

conservazione; Ministero Agricoltura e Foreste,Roma,

Collana Verde (104), 231 pp. TINSLEY, R. C. & LOU-

MONT, C. & KOBEL, H. R. (1996): Geographical distri-

bution and ecology; pp 35-59. In: TINSLEY, R. C. &

KOBEL, H. R. (eds.): The biology of Xenopus; Oxford

(Oxford Univ. Press), 440 pp. TINSLEY, R. C. &

MCCOID, M. J. (1996): Feral population of Xenopus out-

side Africa; pp. 81-94. In: TINSLEY, R. C. & KOBEL, H.

R. (eds.): The biology of Xenopus; Oxford (Oxford

Univ. Press), 440 pp.

KEYWORDS: Amphibia: Anura: Pipidae:

Xenopus laevis, feral population, invasive species,

allochthonous species, Sicily, Italy, Fiume Iato

SUBMITTED: November 18, 2004

AUTHORS: Francesco LILLO, Wilderness Studi

Ambientali, Via Cruillas 34, I-90100 Palermo; Federi-

co MARRONE, Dipartimento di Scienze Botaniche, Uni-

versità di Palermo, Via Archirafi 38, I-90123 Palermo,

Italy < federico.marrone@neomedia.it >; Alessandra

SICILIA, Wilderness Studi Ambientali, Via Cruillas 34,

I-90100 Palermo; Giuseppe CASTELLI, Dipartimento di

Scienze Botaniche, Università di Palermo, Via

Archirafi 38, I-90123 Palermo, Italy; Bruno ZAVA,

Wilderness Studi Ambientali, Via Cruillas 34, I-90100

Palermo, Italy.

64 SHORT NOTE HERPETOZOA 18 (1/2) Wien, 30. Juni 2005 SHORT NOTE

All_Short_Notes18_1_2.qxd 10.08.2005 12:46 Seite 4

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In the Grinnellian niche concept, the realized niche and potential distribution is characterized as an interplay among the fundamental niche, biotic interactions and geographic accessibility. Climate is one of the main drivers for this concept and is essential to predict a taxon’s distribution. Mechanistic approaches can be useful tools, which use fitness-related aspects like locomotor performance and critical thermal limits to predict the potential distribution of an organism. These mechanistic approaches allow the inclusion key ecological processes like local adaptation and can account for thermal performance traits of different life-history stages. The African Clawed Frog, Xenopus laevis, is a highly invasive species occurring on five continents. The French population is of special interest due to an ongoing expansion for 40 years and a broad base of knowledge. We hypothesize that (1) the French population exhibits increased activity time in the invasive European range that could be devoted to fitness-relevant activity and (2) tadpoles may have less activity time available than adult frogs from the same range. We investigate how thermal performance traits translate into activity time budgets and how local adaptation and differences in the thermal responses of life-history stages may boost the European Xenopus invasion. We use a mechanistic approach based on generalized additive mixed models, where thermal performance curves were used to predict the hours of activity and to compare the potential activity time budgets for two life-history stages of native and invasive populations. Our results show that adult French frogs have more activity time available in Europe compared to South African frogs, which might be an advantage in searching for prey or escaping from predators. However, French tadpoles do not have more activity time in Europe compared to the native South African populations suggesting that tadpoles do not suffer the same strong selective pressure as adult frogs.

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Because of the current global biodiversity decline, understanding the consequences of each threat on biodiversity is crucial for conservation biology. Invasive species are among the main threats at the global scale, and can locally imply harmful damages on ecosystems. Studying the phenomena driving the effects and potential for expansion of these species appears as a crucial element to assess their long terms impacts. In this study, we focused our efforts on an invasive population of the African clawed frog, Xenopus laevis, in France, to bring insight about the interactions of this population with its environment and to study the changes in resource allocation to the life history traits, related to reproduction, survival and dispersal probabilities, during the range expansion of the population. We studied the diet in the French invasive population and in other invasive and native populations, and found that this species can expand by predating a narrow, as well as a broad, range of prey categories. We also detected an impact of X. laevis on the native amphibian community in France. In the second section of the thesis, we reported a decrease in reproductive investment, and an increased dispersal allocation of resources at the range edge. We finally studied population dynamics and detected a lower survival probability and density at the range core. All these results combined suggest that the potential for long term impacts is important in France for X. laevis as well as in other areas where the species has been, or will be, introduced.

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There are two populations of Xenopus laevis in Portugal, living in two streams, Laje and Barcarena, located in Oeiras, Portugal. Previous studies have found differences in the size of individuals of both populations. The present work intends to analyze this size difference through the analysis of the age structure, longevity and the growth of these animals, using skeletochronology. Laje’s is characterized by an aged population with higher values of individual length, age and longevity. Barcarena’s depicted a younger age structure with lower values of individual length, age and longevity. These results suggest that Barcarena may have better conditions for reproduction, but worse conditions for adult survival, while the opposite may happen in Laje. The environmental differences could explain these results, but the aged population of Laje may also be a result of the eradication program. We suggest different approaches for the continuation of the eradication program.

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Nov 2017

African clawed frog is a sub-saharan native anuran that has been introduced in various states of the old and the new world. The only Italian population of this species is located in western sicily, and it is known as the european clawed frog population with wider distribution area. This paper describes a new sicilian population of this species, and sets out to verify the effective isolation from the currently known distribution. The new site is a disused swimming pool, located near the mouth of the Belice river (province of Trapani), 31 km away from the nearest edge of the african clawed frog distribution area. To test whether this new population is the result of natural expansion of its range have been checked 21 control sites, arranged in a suitable area near the new site and along the basin of the Belice river, whose upper course is included in the sicilian range of this species. The surveys in the control sites did not reveal the presence of clawed frogs, therefore, it seems doubtful the hypothesis of natural expansion along the Belice river basin and plausible the occurrence of a man-mediated introduction event.

Ecology and Conservation of Amphibians

Article

Oct 1996

(in press): Species account: Xenopus laevis Status and conservation of U.S. amphibians

1-292

J J Crayon

(Suppl.): 1-292. CRAYON, J. J. (in press): Species account: Xenopus laevis; In: LANNOO M. J. (ed.): Status and conservation of U.S. amphibians; University of California Press (Berkeley). FOUQUET, A. & MEASEY, G.

An invasive population of Xenopus laevis in Italy

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