Animal decisions and conservation: the recolonization of a
severely polluted river by the Eurasian otter
M. Delibes1, S. Cabezas1,2, B. Jimé nez3 & M. J. González3
1 Doñana Biological Station, Department of Conservation Biology, CSIC, Sevilla, Spain
2 Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada
3 Instituto de Quı́mica Orgánica General, CSIC, Madrid, Spain
Keywords
bad decision; Eurasian otter; indicator; Lutra
lutra; Guadiamar River; toxic spill.
Correspondence
Miguel Delibes, Doñana Biological Station,
Department of Conservation Biology, CSIC,
Avenida de Marı́a Luisa s/n, 41013 Sevilla,
Spain. Tel: +34 954 232340; Fax: +34 954
621125
Email: mdelibes@ebd.csic.es
Abstract
Animals make decisions relying on environmental cues associated to high survival
or breeding success along their evolutionary history. However, because of rapid
anthropogenic changes in the environment, they may lack useful cues, making bad
decisions with potential consequences for individuals and populations. Contaminants are difficult or impossible to detect for animals, so polluted habitats could be
used in spite of their dangerous effects. The Eurasian otter Lutra lutra reoccupied
the Guadiamar River (SW Spain) o1 year after a toxic spill that killed the fauna
living in it. The levels of heavy metals and arsenic (As) in the river trophic web at
that moment were probably harmful for otters. To investigate this, we determined
the amount of several heavy metals including copper, cadmium, zinc (Zn) and lead
(Pb) and metalloids such as As in otter faeces and estimated the exposure of otters
to these elements as average ingestion. Concentrations of Zn, Pb and As were
statistically higher in faeces collected along the Guadiamar River than in those
collected along the Guadalete River (reference area). An ‘average otter’ in the
Guadiamar River would consume 3–4 mg of Pb and more than 5 mg of As daily.
Such doses must be hazardous for the species and challenge the usual assertion
that otter presence is a good indicator of river quality.
Introduction
The influence of individual decisions by animals on their
population dynamics and community ecology is an increasingly important study topic (e.g. Pulliam & Danielson, 1991;
Sutherland, 1996; Binckley & Resetarits Jr., 2005). Usually
it is assumed that animals are adapted to their environment
in such a way that they make decisions in order to maximize
their lifetime reproductive output. In the case of habitat
choice this implies that animals are able to judge quality
accurately and move to better habitats when available.
However, evaluating habitat quality is a difficult task,
especially for long-lived animals which must use the available
information when selecting habitat to forecast conditions in
the future. Instead of deciding on the basis of blind forecasting,
animals usually rely on environmental cues associated with
high survival and breeding success along their evolutionary
history. Nevertheless, persistent useful cues can be inefficient
or negative (i.e. no longer correlated with the expected habitat
quality) as a result of unusual changes in the environment. This
is especially true in our rapidly changing world due to human
influences. For instance, some grassland birds can select cereal
fields for breeding, because these landscapes include the
structural cues of natural grasslands; however, mechanical
grain harvesting will decrease the expected breeding performance by producing high nestling mortality (Best, 1986).
The study of behavioral decisions by individual animals is
an important topic in conservation biology, as wrong decisions influence conservation at least in two ways. On the one
hand, erroneous decisions can generate the so-called ‘ecological traps’ or ‘attractive sinks’ (e.g. Delibes, Ferreras & Gaona,
2001a; Schlaepfer, Runge & Sherman, 2002; Battin, 2004). On
the other hand, animals making bad decisions when using a
particular resource transmit misleading signals to managers
about the quality of this resource, in the same way as high
abundance of a species can be a less reliable indicator of a
high-quality habitat (e.g. Van Horne, 1983).
Contamination favors bad decisions because animals are
usually unable to identify cues about the presence of contaminants, though many of these products can reduce the
animals’ breeding success and increase their mortality. The
ingestion of lead (Pb) shot pellets as grit by birds is a classical
example (Scheuhammer & Norris, 1996). In this paper, we
analyze whether the recolonization of the highly polluted
Guadiamar River (SW Spain) by the Eurasian otter Lutra
lutra was an erroneous decision.
The Guadiamar River was highly polluted because of an
accident that occurred on 25 April 1998. The dam of a mine
tailing pond located in Aznalcollar, Seville, (c. 37131 0 N,
7143 0 W) was broken, releasing about 4 million m3 of acidic
water and 2 million m3 of toxic mud near the mouth of the
Agrio River, a small tributary of the Guadiamar River. The
M
toxic mud consisted mainly of iron (34–37%) and sulfur
(35–40%), but included significant amounts of zinc (Zn,
0.8%), lead (0.8%), arsenic (As, 0.5%) and copper (Cu,
0.2%), and minor quantities of antimony, cadmium (Cd),
cobalt, thallium, etc. (Grimalt, Ferrer & Macpherson, 1999).
As a result, aquatic life was eradicated from over 60 km of
the river. Restoration activities began 3 months after the
toxic spill and, within 1 year, the mud covering the riparian
zone was removed. About 6 months after the accident we
discovered the first signs of otters in the affected reaches.
The Eurasian otter, a mammal of the Order Carnivora
weighing about 7.5 kg in Spain (Ruiz-Olmo, Delibes &
Zapata, 1998), obtains all its food practically from the aquatic
environment. Its place in the aquatic trophic chain and its high
metabolic requirements (a daily food intake of 15% of body
mass is a conservative estimate; Mason & Macdonald, 1986a;
Kruuk, 1995) make it a highly sensitive species to pollution.
Because of this, otter presence is used frequently as an
indicator of healthy riverine systems (e.g. Chanin, 2003).
However, otters probably do not recognize pollutants as a
danger, evaluating river quality through cues associated to the
structure of the habitat and the abundance of prey. Hence,
otters in the Guadiamar River could be (1) compromising their survival and reproduction by unnoticeably ingesting
high quantities of heavy metals and metalloids and (2)
indicating the river ecosystem is recovered from the toxic spill
before it really does it. In a similar way, unnoticed poisoning
of Canadian otters Lontra canadensis eating fish with large
concentrations of Hg has been suggested (Wren, 1985), while
several authors have reported on both Eurasian and Canadian
river otters using in a regular way potentially hazardous
contaminated environments (e.g. Kruuk & Conroy, 1996;
Elliott, Guertin & Balke, 2008).
The objectives of this study are to: (1) evaluate the level of
reoccupation of the polluted river by otters about 1 year
after the spill; (2) determine the amount of several heavy
metals (Cu, Cd, Zn and Pb) and As in otter faeces during the
same period, comparing them with reference samples obtained from the unpolluted upper stretch of the Guadalete
River (Cadiz), about 200 km away; (3) estimate (from the
faeces and from the diet) the average daily ingestion by
otters of these elements; (4) discuss whether this exposure
poses health risks for otters, in which case the decision of
recolonize the river would be wrong and therefore the otter
presence a bad indicator of river quality.
chronic pollution. A few km downstream from the upper
reaches a toxic spill entered the Guadiamar River from a
small tributary, the Agrio River (see Fig. 1). The central
37 km of the Guadiamar River (‘medium reaches’) crosses
an agricultural matrix. In most of the last 41 km (‘lower
reaches’) the river has been canalized, running through a
marshy area flooded during the rainy periods and partially
corresponding to Donana National Park, an important
protected area in Europe. The 1-km-wide channel floods
into the Guadalquivir close to the Atlantic Ocean.
Climate in the area is Mediterranean with Atlantic influence. Summers are hot and dry and winters mild and rainy. In
the village of Aznalcazar, at the middle of the catchment, the
average annual temperature is 18 1C and the mean annual
rainfall is 667 mm. However, the main characteristic of the
rainfall regime is the intra- and inter-annual irregularity.
Consequently, the Guadiamar River has a torrential regime,
with peaks above 1000 m3 s—1 some winter days and only
temporal ponds during most of the summer. Also, annual
water transport averaged 209 hm3, but reached 724 hm3 in
1962/1963 and only 20 hm3 in 1982/1983 (Borja et al., 2001).
As a clean area for comparison, we selected the upper
reaches of the Guadalete River (Fig. 1), near the village of
Grazalema, Cadiz (c. 36148 0 N, 5119 0 W). Here, the river runs
through a rather high (about 370 m a.s.l.) agricultural area
just upstream the reservoir of Zahara-El Gastor. The
Guadalete River flows directly to the Atlantic Ocean and
no metal pollution was suspected in its high reaches.
Materials and methods
Analytical procedure for heavy metals and
As levels in faeces
Study area
The Guadiamar River is the lowest tributary of the Guadalquivir River (in south-western Spain; Fig. 1). It flows c.
107 km from north to south in the provinces of Huelva and
Seville, draining a catchment of about 1880 km2 and running from more than 500 m to 4 m above sea level. In the
upper 29 km (the ‘upper reaches’) it runs through a mountainous area with a forested matrix. The mining of pyrites
has occurred in this zone for a long time, producing some
Otter distribution
Standardized field surveys, based on searching for signs of
otter presence, are used extensively to assess the distribution
of the species (Reuther et al., 2000). The most commonly
used otter signs are spraints (the specific term for otter
faeces), which have an unmistakable aspect and odor and
are often deposited in conspicuous and predictable sites or
latrines. We searched for otter spraints in the Guadiamar
River during the month of June 1999, c. 13 months after the
toxic spill. We divided the whole river into 107 stretches of
1 km (29, 37 and 41 stretches in the upper, medium and
lower reaches, respectively) and searched each of them.
Otter occurrence within a stretch (site) was considered
positive, and the search concluded, when the first spraint
was found. It was negative if no spraints appeared in 600 m.
Thirty otter faeces collected in the medium reaches of the
Guadiamar River, the area most affected by the spill, were
grouped into 15 samples (each containing two spraints) to
be analyzed for the presence of trace elements (Cu, Cd, Zn,
Pb and As). The same procedures were adopted for 30
spraints (15 samples) collected at the upper reaches of the
Guadalete River in July 1999.
Each sample was dried to ambient temperature, pounded
and blended. For element determination, 0.25 g of blend was
c 2009 The Authors. Journal compilation Q
c 2009 The Zoological Society of London
Animal Conservation 12 (2009) 400–407 Q
401
Spain
Guadiamar
River
Guadalete
River
Upper reaches
(29 km: 100% positives)
Mine of Frailes
Aznalcollar Town
Agrio River
Guadalquivir River
Seville
Guadiamar River
Medium reaches
(37 km: 97% positives)
Doñana National
Park
Lower reaches
(41 km: 39% positives)
Atlantic Ocean
0
10
20 km
placed in hermetic Teflon digester vessels (DuPont, Wilmington, DE, USA). Digestion was performed in an acid
medium with 1.5 mL of HNO3 and eight drops of H2O2. The
sample was maintained in the furnace at 100 1C during 5 h.
Once the digestion was completed, the solution was dissolved to 25 mL with Milli-Q water (Millipore, Billerica,
MA, USA). Analyses of Cu, Cd, Zn and Pb were performed
using a flame Atomic Absorption Spectrometer (AAS)
(Spectra A-100, Varian, Palo Alto, CA, USA). Arsenic was
measured using a Perkin Elmer (PE) longitudinal AC Zeeman (AAnalyst 600) AAS equipped with a transversely
heated graphite atomizer and a built-in fully computer-controlled AS-800 autosampler (Perkin Elmer Hispania, Madrid,
Spain). PE pyrolitic graphite-coated tubes with an L’vov
platform were used. Concentrations are expressed in parts per
million (p.p.m.), i.e. mg g—1 (or mg kg—1) on a dry weight basis.
The detection limits of the methodology (LOD) were as
follows: Cu (0.3 mg g—1); Cd (0.01 mg g—1); Zn (0.1 mg g—1); Pb
Figure 1 Map of the study area in southwestern Spain, with details of the affected
Guadiamar River, the Doñ ana National Park
and the sampled reaches (number of kilometers = monitored stretches and per cent of them
with positive results for the presence of otters).
(0.03 mg g—1); As (0.012 mg g—1). All samples were analyzed in
batches, with method blanks, known standards, and reference
material, DORM-2 (dogfish liver Squalus acanthias) from
NRCC and Mussel from NCS. Accepted recoveries of reference material ranged from 88 to 110%. Relative standard
deviation in replicates and reference material analysis was
below 10%. In the case of undetected levels, we assigned the
value of the limit of detection.
Model of exposure of otters to heavy metals
and As
We assumed that diet was the main route of exposure of
otters to heavy metals and As. In order to obtain the most
reliable results, we estimated the daily amount of metals and
As ingested by the otters by two different ways: (1) from the
content of these elements in the faeces; (2) from the content
of these elements in the consumed prey.
M
Model of exposure from the amount of trace
elements in faeces
A European otter produces c. 70 g of dry faeces per day
(Mason & Macdonald, 1986b). Thus, we can estimate the
daily quantity (in mg) of As and heavy metals excreted through
the faeces by multiplying the geometric mean (expressed as
p.p.m., i.e. mg of trace element per dry kg of faeces) obtained
in our analyses by 0.07. In adult humans, the rate of absorption of Cd and Pb in the intestine barely reaches 10% (Mason
& Macdonald, 1986b; International Programme on Chemical
Safety, 1995). Consequently, we have assumed conservatively
that Cd and Pb were ingested in the same quantities as they are
excreted through the faeces (i.e. no absorption). Contrarily, in
humans substantial amounts of Cu (20–60%) and Zn (10–
40%), which are essential elements in living organisms, are
absorbed through the gastrointestinal tract (International
Programme on Chemical Safety, 1998, 2001a). Therefore, in
these cases we have assumed that the quantities of Cu and Zn
excreted represent 50% of the quantities ingested. The bioavailability of ingested As varies with the dose, the arsenical
compounds, the presence of nutrients in the gastrointestinal
tract, etc. Nevertheless, most of the ingested total As (on the
average 435%) is excreted through the urine and smaller
proportions through the skin, hair, etc.; another proportion is
absorbed and accumulated in the bones and some other body
parts (International Programme on Chemical Safety, 2001b).
Therefore, we estimated conservatively that 30% of the
ingested total As was excreted through the faeces.
Model of exposure from the amount of trace
elements in otter prey
To estimate the ingestion of metals throughout the prey we
estimated the diet of otters by analyzing 48 spraints collected in
the same area and temporal period. Spraint analysis followed
standard procedures and prey remains were identified using
published keys (e.g. Conroy et al., 1993) and our own collection for comparison. Each identified prey class in a spraint was
considered an ‘occurrence,’ and the general diet was expressed
as frequency of occurrence (number of occurrences of a certain
prey type divided by number of spraints analyzed). Fish
(mainly Barbus sclateri and Cyprinus carpio) and red swamp
crayfish Procambarus clarkii were the commonest prey, while
birds, amphibians and insects occurred with small frequencies.
Fish and crayfish occurred in an approximate proportion
of 65:35, thus to simplify we have ignored the rarer prey and
considered that 65% of the otter food was fish and 35% was
crayfish. Conservatively, we have estimated that individual
otters in the Guadiamar River consumed daily 1000 g of
fresh food (i.e. 650 g of fish and 350 g of crayfish). Data
on the amounts of metals in whole fish and crayfish collected
in the medium reaches in April 1999 were obtained from
Moreno-Rojas et al. (2002) and Otero et al. (2002), respectively. We have no data for the contents of As in fish and
crayfish in 1999. Also, we lack information about the content
of trace elements in the otter prey of the Guadalete River, so
this approach was not used for the reference population.
Statistical procedures
Because of their great dispersion, we have log-transformed
the data, expressing the averages as geometric means.
Differences between the results of the Guadiamar and the
Guadalete Rivers were tested statistically using t-tests for
Cu, Cd and Zn, which presented a normal type error
distribution (Kolmogorov–Smirnov test to Cu: KS = 0.113,
P = 0.200; Cd: KS = 0.109, P = 0.200; Zn: KS = 0.116,
P = 0.200), and Mann–Whitney U-test for Pb and As,
because they did not present a normal type error distribution (Pb: KS = 0.292, Po0.001; As: KS = 0.282, Po0.001).
Results
Otter distribution
The occasional presence of otters in the heavily polluted
stretch of the Guadiamar River was apparent at least since
November 1998. In June 1999, otter signs were detected in
75.7% of the 107 sites investigated. All the 29 stretches in the
upper reaches and 36 of the 37 stretches in the medium
reaches gave positive results. In the lower reaches, otter
signs were detected in 16 (39%) of the 41 stretches investigated, most of the negative results (92%) corresponding to
the lowest sites. This means that 1 year after the toxic spill all
the Guadiamar River, perhaps with the exception of the
salted and canalized areas closest to the sea, was occupied by
the otter.
Content of trace elements in faeces
There was considerable variation in metal levels among the
samples (Table 1). In the Guadiamar River, the variation
found among samples for Pb and As reached several orders
Table 1 Concentrations (expressed as p.p.m. dry weight) of heavy
metals and arsenic in otter spraints (n = 15 samples of two faeces in
each) collected in June 1999 in the polluted medium reaches of the
Guadiamar River and the upper reaches of the Guadalete River, used
as reference, south-western Spain
Copper Cadmium Zinc
(Cu)
(Cd)
(Zn)
Lead
(Pb)
Arsenic
(As)
Guadiamar River
Geometric mean
68.1
3.47
836.44 41.79 22.51
Minimum
12.96 1.28
532.1
2.28
1.53
Maximum
188.1
6.82
1411
159.8 142.6
Guadalete River
Geometric mean
37.21 3.93
354.32
1.3
0.02
Minimum
6.25 1.49
111.8
0.4
0.01
Maximum
136
8.25
841.1
3.82
0.64
Statistical test results Guadiamar versus Guadalete
t- or Mann–Whitney 1.906 —0.547
4.306
—4.500 —4.785
U-test
P values
0.670 0.589
o0.001 o0.001 o 0.001
Differences were tested statistically using t-tests for Cu, Cd and Zn
(with normal distributions) and Mann–Whitney U-tests for Pb and As.
c 2009 The Authors. Journal compilation Q
c 2009 The Zoological Society of London
Animal Conservation 12 (2009) 400–407 Q
403
of magnitude. The highest concentration was found for Zn,
and lowest for Cd (Table 1). In the Guadalete River the
range was also very wide, but not for Pb and As, which had
the lowest concentrations. When comparing both localities,
statistically significant differences in levels between rivers
were found for Zn, Pb and As, but not for Cu and Cd.
Level of exposure estimated from faeces
Considering the daily production of otter spraints and the
rates of excretion of metals through the faeces indicated in
‘Materials and methods,’ it is possible to estimate the amount
of metals and As ingested daily. Assuming an average weight
of 7 kg for an Iberian otter, the daily rate of ingestion can be
expressed as mg per kg of body weight. Accordingly, in June
1999 an ‘average otter’ in the medium reaches of the Guadiamar River consumed almost 10 mg of Cu, 0.25 mg of Cd,
117 mg of Zn, almost 3 mg of Pb and more than 5 mg of As
daily (Table 2). Estimated values for otters living in the
Guadalete River were much lower, except for Cd (Table 2).
Level of exposure estimated from diet
As noted previously, we simplified the method of estimating
ingestion of trace elements by otters from levels in their prey
by assuming that each otter ate 350 g of crayfish and 650 g of
fish daily. From the literature we knew the average content of
metals (except As) in crayfish and fish in the spring 1999 in
the medium reaches of the Guadiamar River, so we estimated
the amount of trace elements ingested with the food. The
results (Table 2) agreed moderately well with those obtained
by the previous approach, especially for Cd and Pb. In the
case of Cu, the rate of ingestion estimated from the diet was
higher than that estimated from the faeces, but in the same
order of magnitude. The contrary occurred with Zn.
Discussion
It could be argued that otter signs found in the polluted
stretch of the Guadiamar River belonged to transient individuals. In such a case, a recolonization would not be proved.
Although otters can move over large distances (lineal home
ranges of 30 km and daily travels close to 10–20 km are
common; Kruuk, 1995; Jimenez, Ruiz-Olmo & Pascual,
1998), usually high percentages of positive sites in otter
surveys are associated to settled individuals. By combining
the search for spraints with radio-tracking data and knowledge of the real number of otters in a reintroduction area,
Ruiz-Olmo, Saavedra & Jimenez (2001) found that signs of
four released otters were detected at 40% of the surveyed sites
in the reintroduction basin, along 80 km of river and 940 ha of
wetlands. When the search was made inside its home range, a
single resident otter can be detected in 71% of the monitored
sites, while the percentage increased to 96.9% where two or
more otters are established. Given that in the medium reaches
of the Guadiamar River 97.3% (n = 37) of the surveyed sites
were positive, it should be possible to say that, 1 year after the
toxic spill, otters have reoccupied the area.
The lack of otter spraints in much of the lower stretches
of the Guadiamar River might be due to a low number of
otters, but also explained by the difficulties of sampling in
this habitat (clay marshes with heliophytic vegetation and
lack of outstanding places to be marked by otters). As the
otter remained in the unaffected upper reaches after the
toxic spill (authors, unpubl. data), a rapid recolonization of
the severely polluted downstream reaches was possible.
There was extreme variability of the content of Pb and As
in the samples of the Guadiamar River. A part of this
variation can be explained by the mobility of otters and fish;
for instance, an otter can capture its prey out of the polluted
reaches but defecate inside; alternatively, fish can move from
Table 2 Estimated (from faeces and from food) amounts of heavy metals and arsenic ingested by otters in the polluted reaches of the Guadiamar
River and the Guadalete River (reference; only from faeces), in south-western Spain
Copper
Based on trace elements in faeces
Guadiamar River (Guadalete River)
Amount eliminated through faeces (mg day—1)
Estimated amount ingested (mg day—1)
Estimated rate of ingestion (mg kg—1 bw day—1)
Based on trace elements in food
Guadiamar River
Average content crayfish (mg kg—1 wet weight)a
Average content whole fish (mg kg—1 wet weight)b
Estimated content in diet (mg day—1)
Estimated rate of ingestion (mg kg—1 bw day—1)
LOAEL for Lontra canadensis (mg kg—1 bw day—1)c
PTDI for humans (mg kg—1 bw day—1)d
a
4.77 (2.61)
9.53 (5.21)
1.36 (0.74)
45.48
2.90
17.81
2.54
10.10
0.500
Cadmium
Zinc
0.24 (0.28)
0.24 (0.28)
0.04 (0.04)
58.55 (24.80)
117.10 (24.80)
16.73 (7.09)
0.67
0.03
0.25
0.04
0.40
0.001
61.19
27.00
38.97
5.57
132.00
1.000
Lead
2.93 (0.09)
2.93 (0.09)
0.42 (0.01)
10.95
0.75
4.31
0.62
0.30
0.004
Arsenic
1.58 (0.00)
5.26 (0.01)
0.75 (0.00)
–
–
–
–
0.52
0.002
Otero et al. (2002).
Moreno-Rojas et al. (2002).
c
Duwamish River and Elliot Bay Water Quality Assessment Team (1999).
d
European Environment and Health Information System (2007) (weekly intake converted to daily intake by dividing by 7).
The daily rate of ingestion is expressed as mg per kg of body weight (bw). Published ‘lowest observed adverse effect levels’ (LOAEL) for Lontra
canadensis and ‘provisional tolerable daily intake’ (PTDI) for humans are given for comparison.
b
M
clean reaches to the polluted one, and vice versa. Besides,
local (e.g. places where the removing of toxic mud was
inefficient), prey (e.g. some individual prey are more polluted than others) and host factors (e.g. age or physical
condition of the otters) could add variability to the samples.
Indeed, a high variation in metal concentrations is typical of
analyses of otter faeces (e.g. Josef et al., 2008).
We realize the difficulty of interpreting our results, mainly
because of the scarcity of reference values and the poor
knowledge about the relation of metal concentrations in
faeces with those in blood, kidney, liver or other tissues,
where they are usually measured and for which effects are
reported (e.g. Beyer, Heinz & Redmon-Norwood, 1996).
However, the use of faeces allows collecting a large number
of samples with a minimal disturbance for the animals.
Because of this, for instance, guano is analyzed frequently
for assessing pollution in bat colonies (e.g. O’Shea, Everette
& Ellison, 2001). Similarly, faeces from several species of
otters have been analyzed, mainly for organic compounds
(e.g. in Lu. lutra: Mason et al., 1992; Mason & Macdonald,
1994; van den Brink & Jansman, 2006; Lemarchand et al.,
2007; in Lo. canadensis: Elliott et al., 2008), but also for
some metals, such as Hg (e.g. in Pteronura brasiliensis:
Gutleb, Schenck & Staib, 1997; in Lontra longicaudis: Josef
et al., 2008). In our knowledge, only four studies are useful
for comparisons, having analyzed the same metals as ours in
otter spraints. All corresponded to not especially polluted
locations, in Great Britain, Greece, Slovenia and South
Korea (Mason & Macdonald, 1986b; C. F. Mason & S. M.
Macdonald, unpubl. data, quoted in Mason, 1989; Gutleb,
1994; Han et al., 2002).
In general, metal concentrations are higher in the Guadiamar River than in the Guadalete River and the other places
previously referenced. Nevertheless, average levels of Cd were
rather similar in faeces collected in the Guadiamar River, the
Guadalete River and the British and Greek localities (they
were lower in Slovenia and South Korea). This result was
expected, as Cd was not an important component of the toxic
spill. Values of Cu and Zn in the samples of Guadiamar were
twice those of Guadalete (although the difference for Cu was
not significant), while in the remaining localities are among
one order of magnitude and three times lower. Values of Pb
were 30 times greater and values of As three orders of
magnitude higher in the Guadiamar River (Table 1). Values
of Pb in the Guadiamar samples are around two times higher
than in Britain and Greece, two orders of magnitude higher
than in Slovenia and one order of magnitude higher than in
South Korea.
Except for the Guadalete River, where concentrations for
As are three orders of magnitude lower (Table 1), there are no
data from otter spraints to compare with those of the
Guadiamar River. However, O’Shea et al. (2001) analyzed
As in bat Eptesicus fuscus guano from four roosts in Colorado. Near a polluted area, they obtained values ranging
between 0.42 and 2.9 p.p.m., between one and two orders of
magnitude lower than those of the Guadiamar otter spraints.
Despite several assumptions
and simplifications
(regarding the diet, the type and size of particular prey, the
defecation pattern, the ingested and excreted biomass,
the rate of metal absorption, etc.), there was a relatively
good agreement between our two approaches to estimate the
level of exposure to metals through food by the Guadiamar
otters (Table 2). The effects of metals seem to be rather
consistent across mammalian carnivores (Mason & Wren,
2001). By scaling toxicity data based on body size of test
animals (rat, mouse and mink), the Duwamish River and
Elliot Bay Water Quality Assessment Team (1999) estimated
the toxicity reference values at the population level for
the American river otter Lo. canadensis, a similar species to
Lu. lutra. The lowest observed adverse effect levels
(LOAEL) on reproductive parameters were higher than the
ingested amounts by the Guadiamar otters for Cu, Cd and
Zn, but lower (between one-half and two-thirds) for Pb and
As (Table 2).
Experimenting with otters poses obvious ethical questions, so there are no experimental studies about the effects
of different exposures to As and heavy metals on the species.
Thus, we have used effects on humans and different laboratory mammals described in the literature as surrogates. To
compare with reference values for humans, we used the
Provisional Tolerable Weekly Intake (PTWI) proposed by
the Joint FAO/WHO Expert Committee on Food Additives
(European Environment and Health Information System,
2007), converted to daily intake by dividing by 7. Except for
Cu and Zn, the daily intake of the Guadiamar otters is
between one and two orders of magnitude above the tolerable daily intake to humans (Table 2). Probably this is
enough to overlook the possible overestimation of pollutants bioavailability suggested by Josef et al. (2008) when
hard materials (scales, bones, etc.) are not removed from the
spraints before the analyses.
There are a number of studies on the effects of high
exposure to Pb and As on laboratory and domestic mammals
and on humans. Pb doses as low as 0.1 mg kg—1 bw day—1
produced sublethal effects in monkeys, and chronic oral doses
of 0.3 mg kg—1 bw day—1 reduced survival in dogs (Eisler,
1988). In humans, accidental exposure to two young adults
who ingested between 5 and 10 mg of Pb daily during 1 month
produced symptoms of acute intoxication (Kehoe, 1961,
quoted in Mahaffey, 1977). Regarding As, its toxicity varies
with the chemical form (species) in which it exists; inorganic
arsenite and arsenate are highly toxic, whereas arsenobetaine,
the predominant species in most seafood, is less toxic (Agency
for Toxic Substances and Disease Registry, 2005). Although
we have not differentiated the species of As in the otter’s food,
most of it seems correspond to inorganic As (Devesa et al.,
2002). Besides cancer, studies in humans indicate that skin
lesions typically begin to manifest at oral exposure levels of
inorganic As of about 0.002–0.02 mg kg—1 bw day—1, whereas
LOAEL for short- and intermediate-term chronic ingestion
was fixed at 0.05 mg kg—1 bw day—1 (Agency for Toxic Substances and Disease Registry, 2005). It is likely that chronic
exposure above 1 mg of total As per kg bw day—1 was hazardous for the otter. Moreover, we cannot ignore the potential
synergistic and additive effects of simultaneous high exposure
to different metals and metalloids (Walker et al., 2001).
c 2009 The Authors. Journal compilation Q
c 2009 The Zoological Society of London
Animal Conservation 12 (2009) 400–407 Q
405
To conclude, our results confirm the initial hypothesis
about a bad decision by the otters when they reoccupied the
polluted stretch of the Guadiamar River. Although habitat
conditions (mainly refuge and food availability) could seem
favorable, the exposure to (at least) Pb and As was well
above the lowest proven levels with adverse effects on many
mammals. The inability to evaluate habitat quality at the
individual level can have demographic (population level)
consequences, as suggested by theoretical models (Doak,
1995; Delibes, Gaona & Ferreras, 2001b) and proved
experimentally (Gundersen et al., 2001). In this sense, the
toxic spill could have affected otter population at a regional
level over the reoccupation of the affected area. Thus, the
recolonization by the otter of the Guadiamar River, which
looked like a good news regarding the recovery of the river,
could actually be a conservation problem.
Our results seem to challenge the usual assertion that
otter presence is a good indicator of river quality. This is
depending of the pollutants (for instance, see Kruuk &
Conroy, 1996), but also a question of scale. Severe pollution
at the regional level will prevent the presence of otters
even at clean, local points. On the contrary, in clean regions
otters will be found in severely polluted punctual areas, like
our study stretch, because they can disperse there from other
places within the region. The fact that the Eurasian otter is
able to survive, at least locally and temporally, at a certain
level of pollution, opens the possibility to use it for monitoring the river ecosystem health, simply through the analysis
of contaminants in the easily collected spraints.
Acknowledgements
J.C. Rivilla and S. Alıs helped with fieldwork; A. Duenas
helped with literature; R. Baos, M.C. Blazquez, M. DelibesMateos, J. Swenson and two anonymous referees improved
the paper with their comments and suggestions. S. Zdunich
kindly revised the English. The work was financed by the
‘Consejerıa de Medio Ambiente, Junta de Andalucıa’
throughout the PICOVER program. S. Cabezas was
partially supported by the Gypaetus Foundation (Spain).
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