Society for Conservation Biology

Species Translocation Menaces Iberian Waterfrogs

Author(s): Begona Arano, Gustavo Llorente, Mario Garcia-Paris and Pilar Herrero
Source: Conservation Biology, Vol. 9, No. 1 (Feb., 1995), pp. 196-198
Published by: Wiley for Society for Conservation Biology
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Notes

Species

Translocation Menaces

Iberian

Waterfrogs

BEGONA ARANO,* GUSTAVO LLORENTE,t MARIO GARCIA-PARIS,t AND

PILAR HERRERO?
*Departmentof Biodiversity and EvolutionaryBiology, Museo Nacional de Ciencias Naturales, 28006 Madrid,Spain
tDepartment of Animal Biology (Vertebrates), Universidad de Barcelona, 08028 Barcelona, Spain
tMuseum of Vertebrate Zoology, University of California at Berkeley, Berkeley, CA, U.S.A.
?Department of Biology, Universidad Autonoma de Madrid, 28049 Madrid, Spain

The numerous reports on declining amphibian populations throughout the world led to the creation in December 1990 of the Declining Amphibian Populations
Task Force (DAPTF), activated by the Species Survival
Commission of the International Union for the Conservation of Nature and Natural Resources, one of whose
main goals is "the identification of target populations,
species, and regions which merit immediate attention."
We want to highlight one such target region, the Iberian
peninsula, and a particular species, Rana perezi.
Despite major efforts on behalf of the Spanish conservation authorities to preserve local and endemic species
and the fact that the Iberian peninsula is considered one
of the redoubts of biodiversity in Europe, locally
adapted populations are menaced by the potentially fatal effects of events such as species translocations (Dodd
& Seigel 1991; Reinert 1991). If a unique reproductive
mode such as hybridogenesis is added to the problem of
species translocation, the difficulties of preserving local
species increase. Hybridogenesis is widely prevalent in
European water frogs, having originated in the Rana
esculenta complex, which includes seven species, and a
series of hybridogenetic lineages stemming from interspecific hybridizations. Several systems, consisting of a
host species (or parental species) and a hybridogenetic
lineage in each, are found throughout Europe (Graf &
Polls-Pelaz 1989).
During gametogenesis in such systems the hybrid premeiotically excludes one of its parental genomes by producing only gametes containing the other parental genome. This remaining genome is transmitted clonally
because premeiotic exclusion implies prevention of recombination through crossing over. In most cases the
genome of one of the species, generally R ridibunda, is
clonally transmitted, whereas the other parental genome is excluded. In general, the lost genome correPaper submitted February 28, 1994; revised manuscript accepted
June 2, 1994.

sponds to that of the species living in sympatry with the

hybrid.
Because of its special way of reproduction, hybridogenesis may present new problems for the conservation of natural populations. The voluntary or fortuitous introduction of samples from other species of
Rana capable of provoking hybridogenesis can cause
alterations that can modify the genetic structure of local
parental populations. The hybrids may act as transmitters of allelic variants that could profoundly modify the
gene frequencies in the original populations.
A highly successful hybrid is expected because survival of hybrids has been demonstrated to be superior to
that of parentals in experimental nonhybridogenetic hybrid populations of other animal species (Howard et al.
1993). Hybrid individuals also tend to have other advantages, such as higher growth rates, lower metabolic
demand, and resistance to diseases. In addition, their
developmental periods are often faster and more stable
(Mitton & Grant 1984; Mitton et al 1986; Allendorf &
Leary 1986; Ledig 1986). Nevertheless, due to sterility,
these hybrids would present a reduced fitness compared with hybridogenetic populations.
One of these hybridogenetic systems corresponds to
the hybridization between R perezi and R ridibunda,
found in southern France and northeastern Spain. The
distribution of hybrid populations in strictly delimited,
and, in recent studies on the genetic variability of the
parental syntopical species R perezi (262 individuals,
29 populations), we found significant differences in the
rate of polymorphism between those populations where
hybridization occurs and the remaining ones in central
and western Spain where hybridogenetic hybrids were
not originally found (Mann-Whitney U-test, U = 0.014,
p < 0.02).
During the course of our study, an introduction of the
bullfrog (Rana catesbeiana) and of water frogs from
northern Italy occurred in the Sierra de Gata (western
Spain) from a nearby, unsuccessful frog farm (Garcia-

196
Conservation Biology, Pages 196-198
Volume 9, No. 1, February 1995

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IberianFrog Translocations

Aranoet al.

Paris 1991). Using genetic markers, we were able to

detect the presence at the same place of some European
water frogs not native to Spain, including the widely
extended hybridogenetic hybrid Rana esculenta and its
two parental species R lessonae and R. ridibunda,
which could have been introduced either accidentally
with Rana catesbeiana or in unknown previous importations.
A two-year follow-up study of this population disclosed the presence of hybridogenetic hybrids between
R ridibunda and R perezi that originated from recent
crosses (Fig. 1). Such hybrids may seriously endanger
local water-frog populations, which can be expected to
be less successful in their coexistence with hybrids
(Howard et al. 1993). Considering the lower heterozygosity values found in the Sierra de Gata local populations, the introduction of individuals capable of inducing hybridogenesis and increasing heterozygosity levels
are expected to affect the local populations negatively.
In addition, the second system there, R kl. esculenta,

100 Km

197

may prove equally harmful for local populations. Because both parentals are present, the probability of new
R kl. esculenta hybrids arising is very high, and the
continuity of such a population is assured. R kl. esculenta, along with the genome of R ridibunda, has been
extremely successful in central Europe, where its range
has expanded. Under harsh conditions, the advantage of
R kl. esculenta over the parentals has been widely documented (Semlitsch & Reyer 1992), in some cases provoking the complete extinction of the parental species
and yielding all-hybrid populations (Berger 1988). Although most interhybrid crosses result in nonviable R
rididunda, due to possible degeneration of the R ridibunda genome after many generations of clonal replication, there are some cases where crosses between
hybrids have yielded viable R ridibunda (Hotz et al.
1992).
Consequently, we have identified three potential dangers menacingR perezi in the Iberian Peninsula: ( 1) the
introduction of the extraneous species R catesbeiana,

|t2

Figure 1. Distribution of the R. perezi-R. ridibunda system in the Iberian peninsula The asterisk indicates the
introduced population at Villasbuenas de Gata (Caceres) referred to in the text Black dots show the locations
of the other three introduced populations.

Conservation Biology
Volume 9, No. 1, February 1995

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198

IberianFrog Translocations

with negative effects expected at ecological levels based

on other sites where it has been introduced (Moyle
1973); (2) the introduction of R ridibundag R lessonae, and the highly successful hybrid R kl. esculenta,
(3) the initiation of hybridogenetic populations R ridibunda-R. perezi in competition with local lowpolymorphic R perezi Moreover, in recent months we
have noticed three other introductions of R kl. esculenta; two of which have been confirmed, and individuals have been checked for their respective markers.
These introductions took place in areas where hybridogenesis has not formerly occurred. Independent of
these events, Spanish water frogs may be suffering the
consequences of habitat fragmentation, which in itself
can reduce drastically the population sizes, decrease the
rates of immigration and recolonization, and drive populations to extinction. Other issues, such as changes in
population densities and changes in the trophic chainsince the water frog is a key prey-should also be taken
into consideration in this case of translocation.
Given the relatively restricted distribution of R
perezi and the strong competition it already faces in
several regions, it is important that strict measures be
taken to control the consequences of irresponsible species translocation. Such measures should include (1)
legal protection of the autoctonous species, (2) stronger regulation of imports through adequate laws and, in
cases of importation, strict controls on importers to
avoid irresponsible management of foreign species,
which could lead to fortuitous releases affecting local
populations. If these measures are not enacted soon, R
perezi, a species of reduced distribution, may face a
serious decline in its populations.

Acknowledgments
We would like to thank D. Wake, T. R. Halliday, P. Alberch, J. W. Arntzen, and K Dunlap for valuable comments on the manuscript. This work was supported by

Aranoet al.

research grants DGICYT-PB 91-0115-C02

CYT-PB92-0091.

and DGI-

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Conservation Biology
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