Biological Conservation 105 (2002) 75–80
www.elsevier.com/locate/biocon
Ecology of the native and introduced crayfishes Austropotamobius
pallipes and Procambarus clarkii in southern Spain and implications
for conservation of the native species
José M. Gil-Sánchez, Javier Alba-Tercedor*
Departamento de Biologı´a Animal y Ecologpei´a, Facultad de Ciencias, Universidad de Granada, 18071-Granada, Spain
Received 6 February 2001; received in revised form 9 August 2001; accepted 27 August 2001
Abstract
The former and present distribution of white clawed crayfish (Austropotamobius pallipes) in the province of Granada (southern
Spain) is studied. Before 1980 it was widely distributed but at present only 16 populations exist. The decline is related to the
presence of the freshwater red-swamp crayfish (Procambarus clarkii), an American species, vector of the aphanomycosis disease,
introduced to the Iberian Peninsula in 1974 and now widely distributed in the watercourses and marshes of southern Spain. To
establish an appropriate conservation policy for A. pallipes at its southernmost distribution limit, we studied watercourses from
two river basins, Genil and Guadiana Menor, (tributaries of the Guadalquivir River). P. clarkii inhabits the medium to lower
reaches of these two river basins (with its upper limit at 820 m a.s.l.). The distribution of this species was best explained by the
effect of three of the 12 analyzed variables: altitude, water-current and minimum winter temperatures. From our results, the
repopulation of the native crayfish is almost impossible in those reaches inhabited by P. clarkii. However, based on the habitat
selection study, it is clear that upper reaches are unsuitable for the red-swamp crayfish, where the native white-clawed crayfish may
have greater survival possibilities, and these sites can be used for future restocking projects. # 2002 Elsevier Science Ltd. All rights
reserved.
Keywords: Austrapotamobius pallipes; Conservation; Ecological factors; Procambarus clarkii; Southern Europe; Spain
1. Introduction
Austropotamobius pallipes is the only native European
freshwater crayfish distributed in the Iberian Peninsula,
southern Spain (province of Granada) being its southernmost limit (Holdich and Lowery, 1988). In Europe it
is considered a vulnerable species (IUCN, 1996), and is
at high risk of extinction in southern Spain (Gil-Sánchez
and Alba-Tercedor, 1998). Recently, Santucci et al.
(1997), in a genetic study, have compared different
European populations, concluding that those from
Granada have an exclusive genetic identity, though closely linked to the Italian subspecies Austropotamobius
pallipes italicus, considered by many authors to be a
separate species, Austropotamobius italicus. The taxonomic status of the freshwater crayfish in the province
* Corresponding author. Tel.: +34-958-244015; fax: +34-958243238.
E-mail address: [email protected] (J. Alba-Tercedor).
of Granada is far from clear; in fact, in addition to the
genetic idiosyncrasies shown by some populations, they
differ slightly morphologically (particularly in having a
shorter rostrum) and ecologically (Gil-Sánchez, 1999).
Santucci et al. (1997) suggested that this species
could represent a glacial relict, and thus its extinction
would represent a loss of an animal of significant scientific interest.
The red-swamp crayfish (Procambarus clarkii) (family
Cambaridae), a species endemic to southeastern North
America (Huner, 1988), was introduced into the marshes of the Guadalquivir River in southwestern Spain in
1973 for commercial reasons (Habsburgo-Lorena,
1979). The selling of live specimens spread the species
throughout the Iberian Peninsula and, this crayfish is
now quite common and especially abundant in the
southern half of the peninsula (Gutiérrez-Yurrita et al.,
1999). Between 1988 and 1990 the species was recorded
in nine different sites from two different river basins in
Granada (Zamora-Muñoz, 1992; Picazo-Muñoz, 1995;
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(01)00205-1
76
J.M. Gil-Sánchez, J. Alba-Tercedor / Biological Conservation 105 (2002) 75–80
Zamora-Muñoz and Alba-Tercedor, 1996). This species
is well known as a vector of the aphanomycosis, disease
caused by the fungus Aphanomyces astaci (DiéguezUribeondo and Söderhäl, 1993; Diéguez-Uribeondo et
al., 1995), which is lethal to the European species of
freshwater crayfish (Astacidae), decimating entire
populations (Alderman and Polglasse, 1988; Gherardi
and Holdich, 1999).
In this paper we present the results of studies of the
distribution of Austropotamobius pallipes and P. clarkii
in the province of Granada. Moreover, in an effort to
establish conservation measures for the native species,
possible consequences of the expansion and habitat
selection of P. clarkii are analyzed.
2. Study area
The province of Granada (Fig. 1) occupies 12,351
km2 of mountainous country with elevations ranging
from sea level (Mediterranean coast) to 3492 m a.s.l.
(Sierra Nevada mountains). Geologically, there are both
calcareous and siliceous zones. The general climate is
Mediterranean, with variations from a typical or subarid Mediterranean to cold high mountains ‘‘crioroMediterranean’’.
Most watercourses belong to the Guadalquivir River
basin, and some drain the Sierra Nevada Mountains
(Pulido-Bosch, 1980; Zamora-Muñoz, 1992; PicazoMuñoz, 1995). In general, water quality is very good at
the headwaters but deteriorates downstream as a result
of urban sewage. The high seasonality and extensive
water extraction for agriculture drastically diminishes
flow, sometimes even resulting in dry watercourses
(Zamora-Muñoz, 1992; Picazo-Muñoz, 1995; ZamoraMuñoz and Alba-Tercedor, 1996).
3. Material and methods
Using bibliographical data (Pardo, 1941; Torre and
Rodrı́guez, 1964) and a questionnaire sent to all the
municipalities and river authorities, we attempted to
determine the historical distribution of Austropotamobius pallipes. This information, in combination with the area of potential distribution (estimated
according to limestone geological composition), was
used to establish a network of sampling stations.
To establish the actual distributions of the native and
introduced species, we conducted six sampling campaigns during 1991, 1996, 1997, 1998, 1999 and 2000 in
153 sites throughout the Province. For this purpose,
hand sampling and/or baited fish traps were used following the normal sampling procedures used to study
freshwater crayfish populations (Brown and Bowler,
1977; Arrignon, 1983; Holdich and Domaniewski, 1995;
Fig. 1. Historical and actual distribution of Austrapotamobius pallipes in Granada.
J.M. Gil-Sánchez, J. Alba-Tercedor / Biological Conservation 105 (2002) 75–80
Reynolds and Mathews, 1993; Lappalainen and Pursiainen, 1995; Gherardi et al., 1996). Cylindrical fish
traps of 5020 cm, were made using plastic netting of
11 cm mesh size. These had two free opposite openings to permit entry (Fjälling, 1995) and another
blocked central opening to permit extraction. In summer (July and August), three traps (baited with frozen
squid) were set during the evenings (between 1700 and
2100 h) at each sampling site and collected the following
day (between 0800 and 1200 h).
The habitat selected by P. clarkii was investigated by
characterizing each sampling station using 12 variables
(Table 1). To identify the factors responsible for the
distribution of the species, two statistical analyses were
done, as follows. First, using a forward stepwise discriminant analysis variables were related to the presence/absence of the species at each sampling site. A
multiple regression analysis was then conducted to
relate each independent variable to the standardized
abundance of P. clarkii (expressed as number of captures/trap) as has been done by other authors (Eversole
and Foltz, 1993; Foster, 1995). Results from a total of
16 positive and 48 negative sampling sites (corresponding to the sampling of 1996 and 1998) were used for
statistical analyses.
4. Results
Data from the questionnaire and bibliography
revealed that the native species was formerly distributed
in the calcareous water courses studied, but not distributed in the larger rivers (Genil and Guadiana
Menor) or siliceous zones of the Sierra Nevada mountains. A total of 427 km of water courses were occupied
by Austropotamobius pallipes (Fig. 1). However, a drastic decline in populations occurred after 1980, and now
there are only 16 populations, of which two are the
result of successful artificial reintroductions during 1997
77
and 1998 (Figs. 1 and 2). The present populations are
located in headwater streams and small springs up to
1450 m a.s.l., generally with very limited occupation of
territory (4–7875 m). Since they are clearly isolated from
other sites they can be considered as marginal and relict
populations. It is interesting to point out that in every
case these populated sites are isolated from each other
by dry stretches, anti-erosion dams or water falls.
The abundance in 1998–2000 was quite variable; in
some sites it was possible to catch only one specimen
after an extensive sampling effort by hand, whereas in
other sites up to 47 specimens were caught in a baited
fish-trap overnight.
Currently, P. clarkii is found throughout the Province, inhabiting three different river basins (Fig. 3). It is
distributed in the middle and lower reaches of watercourses up to 840 m a.s.l. and occupies 30% of the historical distribution area of Austropotamobius pallipes
(Figs. 1 and 3).
Values of variables used in the habitat selection analysis of P. clarkii are shown in Table 2. From the discriminant analysis of 12 variables eight could be
ranked in order of importance: 8, 4, 7, 12, 10, 9, 3 and
5. These explain 80.85% of the total sampling sites;
64.28% of positive sites (presence) and 87.87% of
negative ones (absence). With the number of variables
reduced to three first-order variables (8: altitude, 4:
current velocity and 7: winter temperature), the model
explains 75% of total sampling sites, 56.25% of positive sites and 81.25% of negative ones. According to the
discriminant function, the following equations were
thus formulated:
P ¼ 0:034A 5:70V þ 5:83T 42:79
N ¼ 0:040A 1:02V þ 5:32T 42:23
where P=positive site (with P. clarkii), N=negative site
(without P. clarkii); A=altitude, V=current velocity,
T=minimum winter temperature.
Table 1
Variables used to characterise sampling sites
Variables
Description
1
2
3
4
5
6
7
8
9
Mean of width (cm)
Maximum depth (cm)
Mean of depth (cm)
Mean of current velocity (m/sec)
Flow (litre/sec)
Minimum summer temperature ( C; measured between 0800 and 1100 h)
Minimum winter temperature ( C; measured as variable 6, during the coldest month—February)
Altitude above sea level (m)
Biological water quality class (ranging from 1: very good conditions, to 5: extremely polluted, according with the Spanish
BMWP score system, by Alba-Tercedor and Sánchez-Ortega, 1988; and Alba-Tercedor, 1996)
% of soft substrate area suitable to burrower species (a visual estimation)
% of soft riverbanks suitable to burrower species (in general muddy substrate or muddy and silt substrates fixed by roots of the
river banks vegetation)
% area occupied by macrophytes
10
11
12
78
J.M. Gil-Sánchez, J. Alba-Tercedor / Biological Conservation 105 (2002) 75–80
Fig. 2. Decline of number of populations during the last two decades.
Fig. 3. Present distribution of Austrapotamobius pallipes and Procambarus clarkii.
The analysis of abundance by multiple regression did
not give significant results; the three first selected variables explained only 31.9% of the variance and was
without statistical significance (R2=0.319, F=2.031,
P=0.159).
5. Discussion
A recent paper (Gutiérrez-Yurrita et al., 1999), considered Austropotamobius pallipes to be virtually absent
in the province of Granada. However, this is not correct, since we found 16 populations. This point is extremely important when preparing conservation strategies
to preserve this native species at its southernmost limit
in southern Europe.
The arrival of P. clarkii coincided with the first
observations of local extinction of the indigenous species Austropotamobius pallipes in Granada. Aphanomycosis disease in Austropotamobius pallipes has been
detected in Granada (Gil Sánchez, 1999). As there are
now no sympatric populations of the two species in the
whole area, it appears highly likely that the introduced
species caused (at least in the past) the regression of the
native species, and it is now blocking the recovery of
Austropotamobius pallipes. Probably other factors
(drought, water extraction, and pollution) have a
synergic effect, but these are minor if one considers the
wide colonization and distribution area of P. clarkii.
The reduction in distribution of Austropotamobius
pallipes, seems now to have stabilized (Fig. 2). This can
be explained by considering the inability of P. clarkii to
colonize mountainous headwater streams.
The model computed for the habitat selection of P.
clarkii explains quite well its current distribution in the
province of Granada, with altitude being identified as
the most important single variable. Studies carried out
in other Spanish regions, such as Aragon and Navarra,
concluded that this species is distributed only along the
lower stretches of the watercourses of these regions
(Bolea Berné, 1995; Diéguez-Irubeondo et al., 1997).
Altitude may explain other variables selected by the
discriminant analysis; that is, in upper reaches the current velocity is higher, and thereafter substrate is coarser, more compacted (and more difficult to excavate)
and thus not suitable for the introduced red-swamp
crayfish. Thus, although the species shows a great plasticity, it is a typical burrowing inhabitant of permanent
and temporary marshes with calm waters (see revision
by Huner, 1988). Therefore, in Spain the highest densities and commercial production are restricted to the
Guadalquivir river marshes (Gallego and Ocete, 1985).
Water temperature closely follows altitude, and P. clarkii in its original area is a typical inhabitant of warm
waters (Huner, 1988). However, in Europe it sometimes
appears to inhabit cold areas (Gherardi et al., 1999),
and in northern Germany Dehus et al. (1999) recorded a
population tolerating an ice cover of several weeks
duration. The role of temperature as an isolated factor
is not clear, and probably it acts synergically with some
of the other variables selected by the computed model.
As a typical member of the family Cambaridae
(Payne, 1997), P. clarkii exhibits fast development
(Huner, 1988) and requires productive water systems.
This fits with the lower reaches of the watercourses in
Granada province, which are strongly affected by cultural eutrophication (Zamora-Muñoz, 1992; PicazoMuñoz, 1995; Zamora-Muñoz and Alba-Tercedor,
1996), and hence the variables related to the biological
water quality were selected by the discriminant analysis.
The poor results obtained from applying the multipleregression analysis may be due to the low number of
captures of P. clarkii in each positive site, an overall
average of 1.58 specimens per trap (n=52 traps, maximum capture=8 specimens/trap) compared with an
overall average of 8.52 Austropotamobius pallipes per trap
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J.M. Gil-Sánchez, J. Alba-Tercedor / Biological Conservation 105 (2002) 75–80
Table 2
Habitat selection of Procambarus clarkii with meanstandard deviation of variables and significant differences
Variablesa
Occupied sites
Unoccupied sites
tb
1 Width
2 Max. depth
3 Mean depth
4 Velocity
5 Flow
6 Min. summer temperature
7 Min. winter temperature
8 Altitude
9 Biological water quality
10 % of suitable substrate
11 % of suitable river bank
12 % area of macrophytes
7.560.66
123.1259.0
56.7510.18
0.1370.21
786.56856.52
16.931.49
10.641.74
636.25105.94
2.4690.99
68.7533.24
78.1240.69
2.183.63
4.773.32
92.5641.69
52,.321.20
0.1950.36
673.451108.56
15.083.06
9.561.57
828.75243.72
1.8020.90
36.8740.23
64.8940.16
6.3514.61
1.61 n.s.
1.91 n.s.
1.08 n.s.
1.2 n.s.
0.42 n.s.
U=239.5*
2.20*
U=165.5***
2.39*
U=196.5**
1.30 n.s.
16.2 n.s.
a
See Table 1.
t, Student’s; U, Mann–Whitney; n.s., non significant.
* P <0.05.
** P <0.01.
*** P <0.001.
b
(n=92 traps, maximum capture=47 specimens/trap).
This difference in captures of the two species is highly
significant (U=1137.0, Z=5.28, P=0.00001), suggesting that P. clarkii is not well adapted to the ecological conditions of the water courses in the province of
Granada.
In other regions of the Iberian Peninsula within the
area of distribution of Austropotamobius pallipes, no
detailed studies are available on the factors limiting P.
clarkii. In northeast Spain, however, Diéguez-Irubeondo et al. (1997) suggested that low temperatures
and oligotrophic conditions were probably the factors
limiting P. clarkii in the region of Navarra. Not far
away, in the region of Aragon, Bolea-Berné (1995)
expressed a similar idea, adding the negative effect of
the presence of very compacted substrates.
In conclusion, the introduction of the freshwater redswamp crayfish (P. clarkii) appears to have caused
regression in the native species (Austropotamobius pallipes), and currently constitutes a major risk factor for
the survival of this species, as well as a limitation for its
rehabilitation. However, according to our data on the
distribution and limiting factors of P. clarkii, we conclude that a great part of potentially suitable watercourses for Austropotamobius pallipes in the province of
Granada remain unthreatened. Such areas can be used
to develop future rehabilitation projects by restocking
with the native species as proposed by Diéguez-Irubeondo et al. (1997), Holdich and Rogers (1997) and
Gherardi and Holdich, (1999).
Acknowledgements
We thank the Consejerı́a de Medio Ambiente, Junta
de Andalucı́a, for permitting our field works in Natural
Parks and for the initial financial support. To José
Antonio Simón, Manuel Chirosa, and Carlos Norman,
for their interest and encouragement. Dr. John Flannagan improved the English version, and Pablo Jáimez,
Julio Luzón and Miguel Ballesta gave information on
additional populations. This study was benefited by the
project HID98-0323-C05-05 (Dirección General de
Enseñanza Superior e Investigación Cientı́fica, Subdirección General de Proyectos de Investigación Cientı́fica y Técnica. Madrid).
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