The influence of resource seasonality on thebreeding patterns of the Eurasian otter (Lutralutra) in Mediterranean habitats
Jordi Ruiz-Olmo, Josep Maria Olmo-Vidal, Sisco Mañas, and Antoni Batet
Abstract: Litters of small Eurasian otter (Lutra lutra) cubs ranged from one to four, with those of one and two ac-counting for 95%. Significant variations were found between locations and according to the main diet (average rangingbetween 1.1 and 2.4 cubs/female). We found a seasonal pattern in otter breeding in some areas, being different in each.In the Prepyrenees, most births took place between March and June (85%). In Mediterranean rivers of the Ebro basin,most births occurred between December and February (57%). In both, the small cubs were found outside the dens just2–3 months after the time of birth. Fish and crayfish exhibited a seasonal fluctuation, with a maximum density of bio-mass between the end of spring and the end of summer and minimum densities in winter. Water was always flowing inthe Pyrenees and Prepyrenees rivers; however, in Mediterranean rivers, important periods of drought were observed,concentrated especially in summer and some winters. Timing of birds corresponded to variation in abundance of food(energy needs) and water resources in space and time. The presence of adequate prey species for the cubs (Ebro’s bar-bel (Barbus graellsii and Barbus haasi) and American crayfish (Procambarus clarkii) in our study area) plays an im-portant role. Interannual variations in food can affect the otter’s reproductive cycle and breeding success.
Résumé : Au cours de cette étude, les portées de jeunes loutres (Lutra lutra) comptaient de un à quatre individus,mais 95 % des portées n’en comprenaient qu’un ou deux. Nous avons trouvé des variations significatives de ce nombreselon l’endroit et selon le régime alimentaire principal (en moyenne de 1,1 à 2,4 petits/femelle). Nous avons constatél’existence de patterns saisonniers de reproduction dans certaines régions, mais différents selon l’endroit. Dans les Pré-pyrénées, la plupart des naissances ont eu lieu entre mars et juin (85 %) et dans les rivières méditerranéennes du bas-sin de l’Èbre, de décembre à février (57 %). Aux deux endroits, les jeunes loutres ont été trouvées en dehors du terrier2–3 mois seulement après leur naissance. Les poissons et les écrevisses ont subi des fluctuations saisonnières et la den-sité maximale de leur biomasse a été enregistrée entre la fin du printemps et la fin de l’été et la densité minimale, enhiver. Il y avait toujours de l’eau dans les rivières des Prépyrénées et des Pyrénées mais, dans les rivières méditerra-néennes, il s’est produit d importantes périodes de sécheresse, concentrées surtout en été et pendant certains hivers. Laprésence des oiseaux suivait les variations de l’abondance de nourriture (besoins énergétiques) et des réserves d’eaudans l’espace et dans le temps. La présence d’espèces appropriées de proies pour les jeunes loutres (barbeau de l’Èbre(Barbus graellsii et Barbus haasi) et écrevisse (Procambarus clarkii) dans notre zone d’étude) joue un rôle important.Les variations annuelles de l’abondance de nourriture peuvent affecter le cycle de la reproduction et on succès chez lesloutres.
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Ruiz-Olmo et al.Introduction
The Eurasian otter (Lutra lutra) has a wide distributionthat covers most of the Palearctic region and part of southernAsia. Otters live in a wide variety of freshwater and marinehabitats and are well adapted to semiaquatic life (Polechla1991; Reuther 1991). The relationship that they have withtheir surroundings is clearly apparent in their diet, which ismainly aquatic and semiaquatic species (Mason and Mac-donald 1986; Kruuk 1995), especially in Mediterranean hab-itats (Ruiz-Olmo and Palazón 1997; Ruiz-Olmo 2001). Here,
the diet consists of species living in or near the water, withfish, crayfish, and amphibians being the most common preyand the most important part of the biomass ingested, al-though the otter also consumes water snakes, insects, birds,and small mammals (Adrián and Delibes 1987; Ruiz-Olmo1995a; Ruiz-Olmo and Palazón 1997; Bartolomé 2000).
The otter decreased in its area of distribution, especiallyin Europe (Foster-Turley et al. 1990; Macdonald and Mason1994), and measures to conserve and manage otter popula-tions, usually by preventing or mitigating the factors leadingto their reduction, have been necessary. General detrimentalfactors include, among others, fluctuations in food availabil-ity (also see Mason 1989; Kruuk 1995). Other specific fac-tors leading to otter decline occur in Mediterranean habitatsof the otter, such as decreasing hydrological resources (Jiménezand Lacomba 1991; Ruiz-Olmo and Delibes 1998; Ruiz-Olmo 2001).
The abovementioned factors can affect the balance be-tween successful breeding (population recruitment) and mor-
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tality (Kruuk et al. 1987, 1991; Kruuk 1995). If the deathrate in an animal population exceeds the birth rate, or if thesuccess rate in breeding diminishes, there will be a decreasein density and the population may end up disappearing(Margalef 1974). It is therefore fundamental in the manage-ment of any species to establish what its breeding patternsare, together with the factors that give rise to these. Bothgood management and a good progression of the breedingparameters that check and reverse the decline must be basedon increases in the reproduction rate and recruitment.
The otter is a polyoestrous species that generally has lit-ters of one to four young and is capable of reproducingthroughout the year (Chanin 1985; Mason and Macdonald1986; Heggberget 1988; Jorga et al. 1989; Röbin 1989; Stubbe1989; Wlodek et al. 1980; De Silva 1991; Sidorovich 1991;Ruiz-Olmo 1994; Sidorovich and Tumanov 1994; Kruuk 1995;Heggberget and Christensen 1996; Ansorge et al. 1997; Dülferand Roche 1998; Elmeros and Madsen 1999). On the IberianPeninsula, litters have been encountered throughout the entireannual cycle (Ruiz-Olmo 1994; Beja 1996). Nevertheless,seasonal variations in breeding chronology do exist in differ-ent European countries. Kruuk et al. (1987) and Heggbergetand Christensen (1996) reported predominant births in springand summer in marine environments in northern Europe (witha peak around December), while Beja (1996) reported morebirths in winter and spring in southwestern Europe. Variousstudies have also found a seasonality in the freshwater breed-ing cycle, with a higher frequency of litters normally occur-ring between the end of spring and autumn (Erlinge 1967;Stubbe 1969; Wijngaarden and Peppel 1970; Reuther 1980;Mason and Macdonald 1986; Jorga et al. 1989; Röbin 1989;Sidorovich 1991; Ruiz-Olmo 1994; Beja 1996; Elmeros andMadsen 1999). Some studies have also found that otters canbreed at least occasionally throughout the year even in veryharsh winter conditions (Stephens 1957; Sidorovich andTumanov 1994).
Much less work has been done on the relationship be-tween different types of breeding strategies and resource dis-tribution over time. Research has dealt almost exclusivelywith marine environments (Kruuk et al. 1991; Heggbergetand Christensen 1996; Kruuk 1995), and very little researchhas been done in fresh water to demonstrate the relationshipbetween the abundance or availability of food and otter breed-ing. It has recently been shown that there is a correlation be-tween the abundance of food (mainly fish) and the numberof breeding females and cubs living along a stretch of river(Ruiz-Olmo et al. 2001). This concurs with the fact thatL. lutra is a food-limited species (Kruuk and Carss 1996).Elmeros and Madsen (1999) have also produced indirectdata indicating that the female mating cycle occurs at thetime of highest fish density. Very few empirical data, how-ever, corroborate the fact that the seasonality of inland re-production depends on resource availability. No study hasbeen done on any resources other than food.
Our objective was to study the patterns of otter breedingin different environmental conditions on the northeastern Ibe-rian Peninsula. We assessed breeding patterns of otters withdifferent diets, as well as of otters with similar diets but dif-ferent degrees of water stress. The object was to determinewhether breeding patterns corresponded to food abundanceand the availability of water in the environment, which is a
very typical limiting factor in Mediterranean ecosystems(Jiménez and Lacomba 1991; Ruiz-Olmo and Delibes 1998).We also seek to know if certain prey species were more im-portant in structuring the otter breeding cycle.
Materials and methods
Study areasThe current study was carried out in the following river
basins situated on the northeastern Iberian Peninsula (Catalonia,the province of Castelló, and eastern Aragón): Medium Cinca,Isábena, Ésera, Noguera Ribagorçana, Noguera Pallaresa, Segre,Bergantes, Matarranya, Algars, Muga, and Fluvià togetherwith small streams and channels on the Alt Empordà plain(Fig. 1). These are grouped into four main areas (the Pyre-nees, the Prepyrenees, the Mediterranean rivers of the Ebrobasin, and the Mediterranean lowland rivers) according tothe diet of L. lutra and the rainfall regime. All of these areasare highly conditioned by precipitation (rain- and snow-fall),with minimum flow rates occurring in summer and maxi-mum rates during spring and autumn.
Riverbeds are often composed of stones, rocks, and gravelin the Pyrenees and Prepyrenees (the rivers Cinca, Ésera,Isábena, Noguera Ribagorçana, Noguera Pallaresa, and Segre).Vegetation on the banks varies with elevation, with the lowerstretches being dominated by Salix pupurea and Populusnigra interspersed with reeds (Typho-Schoenoplectetum glauci) andwhite poplar (Populus alba, with P. nigra, Fraxinus angustifolia,Ulmus minor, and Salix purpurea) with stretches of reedcommunities (T.-S. glauci and Phragmition australis). River-banks along stretches at higher elevations are composed ofrock, and vegetation is scarce, with Alnus glutinosa, P. nigra,and S. purpurea and occasionally grass and small shrubs.
The Mediterranean rivers of the Ebro basin includes severalrivers (the Bergantes, Matarranya, and Algars) whose riverbedsare also composed of stones, rocks, and gravel. Riverbankvegetation consists of hoary willow, willow (S. purpurea andSalix eleagnos among others), and black poplar (P. nigra) invarying phases of growth, with F. angustifolia and P. alba.Helophytic vegetation (Typha sp. and Phragmites sp.) blendstogether with riverside woodland and is dense in certain areas.
In coastal Mediterranean river basins (the Muga and Fluviàrivers), riverine woodland dominates with F. angustifolia andP. alba, although this has been replaced along many stretches
by plantations of P. nigra × canadensis and Platanus orientalis.The Empordà marshes are situated between the estuaries ofthe two rivers and the dominant habitats are freshwater chan-nels and lagoons where reeds (Phragmites sp.) and bulrushes(Typha sp.) grow extensively.
In the river systems under study in the Ebro basin (Prepy-renean and Mediterranean), below 800 m, the primary foodin the otter’s diet is barbel (mainly Barbus graellsii and alsoBarbus haasi), Iberian nase (Chondrostoma miegii), and morerecently the American crayfish (Procambarus clarkii) (Ruiz-Olmo 1995a, 1998; Ruiz-Olmo and Palazón 1997). Above800 m, these are replaced by trout (Salmo trutta) and, inspringtime, amphibians (Bufo bufo, Rana perezi, and Ranatemporaria). Other species that can be important in the dietof some stretches are chub (Squalius cephalus), Iberian roach(Chondrostoma arcasii), carp (Cyprinus carpio), gudgeon(Gobio gobio), bleak (Alburnus alburnus), and the viperinesnake (Natrix maura).
The main species in the Fluvià and Muga river basins arethe American crayfish, eel (Anguilla anguilla), Catalan bar-bel (Barbus meridionalis), roach (Rutilus lemmingi), carp,chub, other euryhaline fish species (mainly Mugilidae), am-phibians, and water snakes.
Studies of fish populations have been concentrated in onerepresentative area of the Prepyrenees (the Noguera RibagorçanaRiver) between 490 and 600 m in altitude and along anotherrepresentative section of the Mediterranean stretch of theEbro (Algars) between 200 and 460 m.
DefinitionsIn this study, “small cubs” are individuals between 2 and
6 months old, which is the period that covers the time whenthey begin to come out of the holt (Mason and Macdonald1986; Kruuk 1995; Durbin 1996) and the age when it is difficultto distinguish them from adult otters (mainly the mother) asthey reach 90% of their total length (TL) in the study area(Table 1). “Big cubs” are cubs over 6 months old, up untilthe time of dispersal (which often occurs between 8 and16 months; Watt 1993; Kruuk 1995).
Otter breedingThis study was set up to detect as many small and big cub
litters as possible, establish the minimum number of young
in each litter, and estimate the date of birth. Data were com-piled from several studies (Ruiz-Olmo 1995a, 1998, 2001;López-Martín et al. 1998; Ruiz-Olmo and Palazón 1997;Ruiz-Olmo and Delibes 1998; Ruiz-Olmo et al. 2001; J.Ruiz-Olmo and S. Mañas, unpublished data). The followingdata were considered.
A female and her cubs observed during visual censusesTo calculate the date of birth, the TL of the cubs was used
in relation to that of the mother to determine whether or notthey were small cubs (Table 1) using data obtained by Ruiz-Olmo et al. (1998) for Iberian otters. These are slightlysmaller than otters found in central and northern Europe(around 2–12% shorter in length, according to the popula-tion; Ruiz-Olmo et al. 1998), although in the case of veryyoung otters, the difference in length is small and is ab-sorbed by the variation and confidence interval. Apparentmass was not used due to various factors including the im-precision of visual calculation, the fact that allometry isclearly apparent with an exponential increase that is greaterthan TL, it is affected more by food and physical condition(Kruuk and Conroy 1991), and because larger differencesoccur between different studies (Stephens 1957; Renaud 1994,1999). The cubs’ date of birth could be estimated on the ba-sis of the observed size of the individuals in intervals of10 cm (Table 1), representing an error, according to TL, of±1 month.
Carcasses of cubs and dead pregnant females and livecubs taken into wildlife centres or caught for radio-tracking studies
The TL and mass were measured to an accuracy of ±0.5 cmand ±10 g, respectively. The ranges given in Table 1 werealso used. In the case of pregnant females, the number ofembryos was established and they were measured and weighed(to an accuracy of ±1 mm and ±1 g); the expected date ofbirth of the embryos was calculated on the basis that gesta-tion lasts approximately 2 months (Reuther 1991; De Silva1991). Accuracy was the same as in the previous case.
Clearly defined footprints or tracks of small cubsencountered
This method has also been used by Erlinge (1967, 1968),Macdonald and Mason (1987), Sidorovich (1991), Dülfer
Age (months)
Sourcea Sex 2 3 4 5 6 7 8
M (kg) 1 Male 2.00 3.00 3.5 3.8 4.5 4.8 5.8Female 1.33 1.67 2.5 3.0 3.5 3.67 4.3
2 Both 1.45–2.10 2.45–2.80 — — — — —3 Both 1.40–1.70 2.00–2.50 2.2–3.0 — — — —4 Both 1.3–2.1 2.00–2.80 2.2–3.0 3.5–3.8 3.8–4.5 4.0–4.8 4.5–6.0
TL (cm) 2 Both 55–62 72–75 — — — — —3 Both 55–58 66–69 73–77 — — — —4 Both 55–60 67–73 73–77 80 85–90 — —
a1, Stephens (1957); 2, Renaud (1994); 3, Reuther (1999); 4, data used in the current study recalculated according to Ruiz-Olmo (1995a) and authorsconsulted above; 5, this study.
Table 1. Estimated age of otter cubs according to mass (M), total length (TL), and measurement of the footprints (FFTLc, total lengthof the front footprint including the claw; RFTLc, total length of the rear footprint including the claw).
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and Roche (1998), and Ruiz-Olmo et al. (2001). To deter-mine the footprint size of small cubs, measurements weretaken from 34 different specimens (live and carcasses) ofIberian otter of known size (TL) and mass. Ten differentmeasurements were taken of the soles of the footprints, fiveof each (back and front): eight lengthwise ones were taken(TL, TL including the claw, TL excluding the heel, TL with-out the heel but including the claw and length of paw pad)and two were taken of the width (width of the paw mark andwidth of the paw pad). The size measurements of the sole ofotter paws and those of paw marks found in the wild weremeasured to an accuracy of ±1 mm. Regression function cal-culations were made between all of these parameters forpaws, TL, and mass to find the most appropriate sole dimen-sions for establishing the length and mass of the otters fromtheir paw marks. Finally, it was decided to use more accu-rate measurements by taking the TL of the front and rearpaws including the claw, FFTLc and RFTLc, respectively.These refer to the maximum distance between the tip of theclaw on the middle toe and the point on the outermost partof the heel. Only footprints on flat ground and where thesubstrate was sufficiently solid to prevent the footprint fromlosing its shape were considered. In this case again, the esti-mation error for age and date of birth is calculated accordingto footprint measurements as ±1 month. In the case of foot-prints, the minimum number of cubs in the litter was esti-mated through the monitoring of tracks along long stretchesof river.
We collected data on 129 litters, of which 12.4% were ot-ters that could be weighed and measured (carcasses, recov-ered and captured cubs, and pregnant females), 28.7% weresightings of wild otters, and 58.9% were tracks (footprints).In the case of establishing the date of birth (n = 61), thesevalues were 23, 20, and 57%, respectively. The elevation atwhich the litters were detected was established for all cases.
Otter dietRecent studies carried out in the rivers of the Ebro basin
included in the study area showed that L. lutra has feedinghabits that fit well-defined patterns (Ruiz-Olmo 1998, 2001;Ruiz-Olmo and Palazón 1997). The otter’s dominant prey isS. trutta above 800 m, B. graellsii and C. miegii below thiselevation, and the introduced American crayfish, either inconjunction with the two previous species or alone.
Results by Ruiz-Olmo and Palazón (1997) referring to 28locations (4015 scats collected between 1984 and 1996, con-taining a minimum of 7773 prey items) were used to deter-mine the otter’s diet in the different rivers in the Ebro basinstudy and to establish what the main prey items are. Despitethe fact that no studies have been published on the otter’sdiet in the Muga and Fluvià river basins and the channelsand marshes of the Alt Empordà plain, data from this rela-tively small area are clustered together for various reasons:elevation is no higher than 200 m, the watercourses are nearthe sea and there are no dams to block the movement of fish,and the availability of prey focuses on the American cray-fish, eel, carp, and various catadromous fish (Ruiz-Olmo2001; D. Saavedra, personal communication). The same studieswere used, together with those by Beja (1995), to establishthe seasonality of the presence of barbel, nase, and crayfishin the diet of L. lutra and in general.
In the Prepyrenees and Mediterranean rivers of the Ebrobasin (where sufficient data on breeding were obtained), weanalysed the effect of the most highly consumed species(B. graellsii and C. miegii; Ruiz-Olmo et al. 2001) on otterreproduction. In the Noguera Ribagorçana, the size of thefish consumed was studied. We collected 396 otter scats be-tween November 1989 and October 1990, which were usedto establish the fork length (FL) of fish. Regression functionswere used to correlate length with three different lengths ofpharyngeal teeth and two sizes of cephalic vertebrae in accor-dance with the functions encountered by Ruiz-Olmo (1995a)(the fit was statistically significant in all cases, while thevariance ranged between 0.81 and 1.00). Special attentionwas paid to the presence of large specimens of B. graellsiiwith a FL greater than 25 cm and C. miegii greater than14 cm, which in the study area are the sizes at which thesefish migrate and contribute to a greater biomass in the river(our unpublished data).
The percentage of occurrences (the percentage of scatswhere there were remains) has been used as an index of fooduse in the case of migratory barbel in the diet.
Fish and crayfish populationsAs the otter’s diet is similar for rivers from each of the
four defined areas (Pyrenees, Prepyrenees, the Mediterraneanrivers of the Ebro basin, and the Mediterranean lowlandrivers; Ruíz-Olmo and Palazón 1997), the fish populationswere studied in places that are representative of the generalpatterns. In the case of trout, studies show that this speciesbehaves mainly in a sedentary way in these rivers (Sostoa etal. 1995), so it was considered less necessary to carry outany studies on variations in this food resource over time inplaces where it is the main source of prey (above 800 m;Ruiz-Olmo 1998).
In areas where cyprinids (B. graellsii and C. miegii) arethe main sources of prey, previous studies on similar speciesin other Mediterranean settings on the Iberian Peninsula(Rodríguez-Ruiz and Granado-Lorencio 1992) have deter-mined that studies should be made of the temporal dynamicsof populations of these species. In the Noguera Ribagorçana(Prepyrenees area) and Algars (Mediterranean rivers of theEbro basin) rivers, fish populations were studied to establishpatterns in fluctuations in abundance. Five stretches, each100 m long, were chosen along the Noguera RibagorzanaRiver between the Canelles and Sopeira dams, which werefished during 1999–2001, while six other stretches were cho-sen along the Algars River between the village of Arnes andthe 200-m altitude level. They were electrofished during 2000and 2001 by means of successive catches per unit of effort(Zippin 1958). All caught fish were measured and their bio-mass retrocalculated in accordance with functions obtainedfor the area (our unpublished data). Estimated populationfigures for each species were obtained, which in turn wereused to calculate the biomass by way of a linear relationship:Ct/N = B/Be, where Ct is the total number of fish caught, N isthe estimated number based on catchability, B is the mass ofcaught fish obtained from the length with length–mass func-tions, and Be is the estimated biomass.
These data were calculated for all of the species presentand all together. Special emphasis was also put on determin-ing the length (FL) of migrating barbel and nase that are not
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present in the area during winter. It was thus also possible tocalculate the density of migratory individuals. The age ofthese individuals was established according to the lines ofgrowth on scales extracted from between the dorsal fin andthe lateral line.
In the case of the American crayfish, the results of themonthly variations in abundance and biomass obtained byBeja (1995) in southern Portugal were used, as the pattern ofpredation by L. lutra is identical there to the one in ourstudy area (Ruiz-Olmo and Palazón 1997).
Water availabilityIn all visits to the different sites or stretches of river that
were carried out during the period of data compilation, thepresence of water was determined according to whether itwas running water (there was water flowing along the wholestretch of river), whether the water was concentrated in poolsand puddles (with an absence of water flowing between
them), or if the stretch of river was dry (no water anywhereor with water in pools of less than 2 m maximum width andless than 10 cm deep, as long as these did not exceed 1% ofthe length of the stretch of river in question).
StatisticsThe monthly distribution of the number of cubs was tested
using χ2.
Results
Calculating the age of ottersTable 1 gives the data obtained on otter age according to
mass and TL, as well as those calculated for the Iberian Pen-insula, together with the criteria used to establish whether acub was small. The regression functions between FFTLc andRFTLc and TL for the Iberian otters were obtained (Fig. 2).
Fig. 2. Regression functions found between footprint measurements (total length of forefoot, claw included (FFTLc), and total lengthof rear foot, claw included (RFTLc)), and total length (TL) for the Iberian otters (Lutra lutra). Arrows indicate the threshold for smallcubs.
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These threshold values are the ones used to establish the ageof otters according to footprint size.
Otter breeding parametersThe litters of small cubs encountered varied from one to
four cubs, and those with one and two cubs accounted for95.2% of the total (n = 84). Significant variations werefound among locations and according to the main diet (Ta-ble 2), with mean values varying between 1.1 and 2.4 cubsper female. Minimum values occurred in mountainous areasin the Pyrenees. Maximum values occurred in the rivers inthe Prepyrenees sector colonized by American river crayfish(also with an abundant presence of fish). No significant dif-ferences were found in the Mediterranean rivers of the EbroRiver basin between places with a diet made up predomi-nantly of barbel and nase and habitats where the Americancrayfish is predominant.
ElevationThe maximum elevation where a litter was detected was
1050 m, although litters were scarce above 900 m (7.5%, n =40 places with litters). Average litter size does not correlatewith elevation (p = 0.505).
Seasonality in otter breedingAll together, it was possible to estimate the date of birth
of 56 litters, which were distributed throughout all monthsof the year.
In the Prepyrenees, there was a seasonal pattern in otterreproduction (χ2 = 20.865, df = 11, p = 0.035) (Fig. 3). Inthe Prepyrenees, the great majority of estimated and knownbirths (n = 33) took place between March (the month duringwhich 33.4% occurred) and June, with 84.8% all told occur-ring during these four months. There was no report of anybirth between October and December. These data are inkeeping with data on the sighting of small cubs outside thedens, which also followed a seasonal pattern (Fig. 4) thatwas significant in the Prepyrenees area (χ2 = 22.669, df =11, p = 0.020). The peak time for the appearance of cubswas June (22.2% of the data in this month, n = 54), just 2–3 months after the time of birth; the proportion diminishedas cubs grew in size and could not be distinguished from themother.
In tributaries of the Mediterranean rivers of the Ebro ba-sin, it was only possible to estimate the date of birth of 14litters (Fig. 3). Births occurred during most of the year, but57% occurred between December and February, althoughmonthly distribution was not significant (χ2 = 8.790, df = 11,p = 0.641). However, this was clearly different from litter
Area No. Area Main dieta n Mean SDRivers withavailable datab
Procambarus clarkii 5 2.40 1.14 CI 1, 2a, 3a, 3b, 43a, 3b Mediterranean rivers of the
Ebro basin*Barbus graellsii,
Chondrostoma miegii13 1.85 0.56 BE, MA, AL 1, 2b
Procambarus clarkii 5 1.60 0.55 BE, MA, AL 1, 2b4 Mediterranean lowland rivers
(<200 m altitude)dProcambarus clarkii and (or)
fish of different species4 1.50 0.58 MU, FL, AE 2b
Note: Areas marked with an asterisk are included in the Ebro basin.aAcording to Ruiz-Olmo and Palazón (1997) and our unpublished data.bRivers: Cinca (CI), Ésera (ES), Isábena (IS), Noguera Ribagorçana (NR), Noguera Pallaresa (NP), Segre (SE), Bergantes (BE), Matarranya (MA),
Algars (AL), Muga (MU), Fluvià (FL), Alt Empordà plain (AE).cStudent’s t test (p < 0.05) with regard to area number.dThese areas have recently been recolonized by the otter.
Table 2. Average number of 2- to 6-month-old otter cubs in five different areas according to the main type of food.
Fig. 3. Comparison of monthly percentage of estimated births inotters from the rivers of the Prepyrenean area and in the Medi-terranean rivers of the Ebro basin.
Fig. 4. Comparison of monthly of percentage of sightings ofsmall cubs in the rivers of the Prepyrenean area and in the Med-iterranean rivers of the Ebro basin.
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distribution in the Prepyrenees area (χ2 = 25.336, df = 9, p =0.003). In the Algars River, the detection of small cubs (Fig. 4)did not vary significantly between months (χ2 = 9.668, df =11, p = 0.5605); this could be due to the small sample size.However, the peak started in April (again around 2–3 monthsafter the peak in the number of births) and reached its maxi-mum in May (78.9% of small cubs were detected betweenApril and August, n = 19). This distribution was statisticallyno different from that in the Prepyrenees (χ2 = 10.570, df =11, p = 0.384), which may also be due to the small samplebecause the percentages for between March and May in theMediterranean rivers of the Ebro basin are twice those in thePrepyrenees area.
In the High Pyrenees (the most mountainous area), whereS. trutta predominates in the diet, there was an insufficientnumber of litters (eight) to study the intra-annual variationaccurately. Reported births occurred in January (two litters),April (two), June (two), August (one), and September (one).In coastal river basins on the Alt Empordà plain, the monthof birth could only be established for two litters, as the pop-ulation has only recently been reintroduced.
Seasonality in otter dietPrevious research in our study area (Table 3) noted that
the occurrence of B. graellsii in the diet of L. lutra inPrepyrenees rivers was more frequent in summer and insome years during autumn as well. There were importantinterannual variations in the case of nase, with minimumvalues occurring during summertime.
In the tributaries of the Mediterranean rivers of the Ebrobasin, no maximum values for the consumption of barbelwere found in summer, with high values occurring in winterand autumn. Nase showed little variance in seasonal avail-ability.
Migratory barbel (FL > 25 cm) occur more frequently inthe otter’s diet in the Noguera Ribagorçana between spring(March) and autumn (November) than in winter (Decemberto February) (χ2 = 36.796, df = 11, p = 0.001), which weremonths when no remains of these large fish were found (n =117 scats for these three months) (Fig. 5). In August andSeptember, large barbel play a much more important part inthe diet (occurring in more than 30% of the samples). Cray-fish are eaten more in summertime (Table 3), with some ex-ceptions occurring in the spring of various years.
Seasonality in fish abundance and biomass
Noguera Ribagorçana River (Prepyrenees area)Average total fish biomass varied between months, with
maximum densities occurring between the end of spring and
the end of summer and minimum densities in winter (Fig. 6).The average maximum values in summer were 30.7 g/m2 in1999, 11.5–12.0 g/m2 in 2000, and 12.4 g/m2 in 2001, whereasbarely 1–3 g/m2 was found between October and March overthe 3-year period.
Barbel accounted for more biomass in this seasonality,reaching on average 11–28 g/m2 in June and July in the 3years and less than 0.6 g/m2 between October and March.The values for nase reached a maximum in April (3.9 g/m2)and September (3.7 g/m2) in 1999, and the values were verylow for the remaining months during the 3 years. Averagevalues during winter were less than 1 g/m2.
Most of the biomass contained in the river throughout thestudy was due to B. graellsii and C. miegii, which repre-sented on average between 72 and 100% of the fish biomassbetween April and September over the 3 years studied. Thesevalues descend to a minimum in January when approxi-mately half of the biomass is made up of both species in1999 and 2000 (47.7% in 1999 and 47.3% in 2000) and upto 82.8% in 2001 (probably due to the low population num-bers of other fish species). These percentages contributedvery little during this month because biomass also reached aminimum, with mean values of total biomass lower than2.0 g/m2 in 2000 and 2001. The remaining species found inthe river were S. trutta, Oncorhynchus mykiss (very lownumbers), A. alburnus, S. cephalus, C. carpio, Micropterussalmoides (very low numbers), and Barbatula barbatula. Barbusgraellsii represented from 91 to 94% of the biomass in theriver between May and July over the 3 years (48–90% inApril and 54–61% in September). Between October and Jan-uary, it is no more than 14% of the total biomass.
The seasonality in the migration of barbel in the NogueraRibagorçana River was also studied, with only large migra-tory specimens being considered because these are absent
Mediterranean rivers of the Ebro basin (n = 3) Barbus spp. 49.0±18.0 63.6±21.1 63.7±25.4 63.5±25.7Chondrostoma miegii 53.0±35.4 28.8±19.5 31.0±25.2 24.9±16.9
aIn the case of B. graellsii and C. miegii, the locations are different from those of P. clarkii.
Table 3. Seasonal variation (mean values and range of the relative frequencies in relation to the fish total and, in the case of crayfish,prey total) in different prey items in the diet of L. lutra in the Prepyrenees (Noguera Ribagorçana, Isábena, Segre, and Cinca) and theMediterranean rivers of the Ebro basin (Bergantes, Matarranya, Algars and Montsant) (calulated from Ruiz-Olmo and Palazón 1997).
Fig. 5. Monthly variation in occurrence of remains of large barbel(Barbus graellsii) in the river Noguera Ribagorçana (Prepyreneanarea).
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from the study area during the winter months (Fig. 7). Largemigrating barbel (FL > 25 cm) that come to breed from wa-ter bodies farther downstream appeared in the stretches un-der study in April and reached maximum average densityvalues between May and July, the age of these individualsbeing 4–6 years or older. Average densities of around 0.10
specimen/m2 (with specific maximum values in stretches of100 m in length of 0.50 specimen/m2) were observed in 1999,whereas in 2000, these values were only 0.025 specimen/m2
(maximum values of 0.20 specimen/m2) and in 2001 were0.02 specimen/m2 (maximum values of 0.045 specimen/m2).Migrated barbel begin to return to the water bodies where
Fig. 6. Variation in average total fish biomass along the five stretches of the Noguera Ribagorçana River, Prepyrenean area (top panel),between 1999 and 2001 and the Algars River (bottom panel) between 2000 and 2001.
Fig. 7. Migration of big barbel (FL > 25 cm) in the Noguera Ribagorçana River (Prepyrenean area) between 1999 and 2001 estimatedas the average density of individuals caught monthly in the five stretches studied.
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they spend the winter in August. There were no large speci-mens of barbel in the river between October and March(Fig. 7). Interannual differences were important.
Algars River (Mediterranean rivers of the Ebro basin)The data refer to quantities of fish during all four seasons
of the year in 2000 and 2001. A similar pattern appears inwhich there are maximum values of total fish biomass be-tween April and the end of summer (Fig. 6). Nevertheless,the mean values were clearly lower than for the NogueraRibagorçana; in spring, they only reached 2.4–5.3 g/m2 andin summer 1.5–5.9 g/m2.
Barbel and nase in the Algars River were alternately thedominant elements in the community and all together reachedan average of 44.3–97.8% of the fish biomass in the riverthroughout 2000 and 2001: 22.7–66.7% B. graellsii and 21.6–31.1% C. miegii. These again represented minimum percent-ages of total fish biomass during the winter months. Otherspecies were caught in the river, although in a much lowerproportion, including Scardinius erythrophtalmus.
In the Algars River, barbel began to appear in May andleave around September. Migrating barbel densities were al-ways much lower. Unlike the Noguera Ribagorçana River,populations of the American crayfish were detected in theAlgars River at two of the sites that were fished (n = 6).
Seasonality of water availabilityWater was flowing in the river in 100% of the visits to
sites in areas regularly occupied by otters in the Pyreneesand Prepyrenees areas. In the Mediterranean rivers of theEbro basin, however, important periods of drought were ob-served, concentrated especially in summer (at 60% of thestations sampled in August throughout the years of study, ei-ther the stretch of river was dry or water was restricted toisolated ponds, n = 9) and winter (Fig. 8). This was also thecase in the Mediterranean lowland rivers area, although to alesser degree.
Discussion
Size of small cub littersThe mean values for the number of cubs found (1.1–2.4)
was within the range described within the species’ range(Chanin 1985; Mason and Macdonald 1986; Heggberget 1988;Jorga et al. 1989; Röbin 1989; Stubbe 1989; Wlodek et al.1980; De Silva 1991; Sidorovich 1991; Ruiz-Olmo 1994;Sidorovich and Tumanov 1994; Kruuk 1995; Beja 1996;Ansorge et al. 1997; Dulfer and Roche 1998; Elmeros andMadsen 1999). Breeding was connected to prey quality andabundance. The highest values were found in areas wherefood consisted of fish and crayfish, which could ensure ahigher food intake, less affected by environmental factors.The smallest litters were found in places where the diet wasalmost monospecific (brown trout) and food availability waslower due to elevation (Ruiz-Olmo 1998). In areas of theMediterranean rivers of the Ebro basin where the otter’s dietis based on fish and crayfish (which at certain times arehighly abundant), litters were smaller than in other areaswhere the diet is the same. The effect of drought appears tobe the most important factor in explaining this, with theavailability (and biomass) of the main sources of prey being
affected just at the time when they should be most abundant(Beja 1995).
Reproductive cycle and food resourcesBirth distribution patterns of otters in the study area corre-
sponded to variations in abundance of food resources inspace and time. Similar patterns have been found in otherplaces (Kruuk et al. 1987; Heggberget 1993; Heggberget andChristensen 1996; Kruuk 1995; Elmeros and Madsen 1999).The care of cubs is undertaken exclusively by the female(Kruuk 1995).
We found a relationship between the peaks of both births andthe presence of cubs outside the dens and peaks of biomassin the environment. Availability of food resources when thecubs are 2 months old seems to be particularly important fortheir survival, as was also suggested by Heggberget (1993).At about this age, the females suckle the cubs, which beginto venture out of the dens to take solid food and to increasetheir energy needs through movement and as they learn toswim and acquire other skills (Mason and Macdonald 1986;Heggberget 1993; Kruuk 1995; Durbin 1996), finding themaximum needs several weeks after the beginning of lacta-tion (Gittleman and Oftedal 1987; Oftedal and Gittleman1989; Nolet and Kruuk 1994). This takes on a special meaningfor the otter, which has a higher metabolism than nonmustelidterrestrial species (Iversen 1972; McNaab 1989). Given theirsmall body size and inability to store fat, L. lutra has higherenergy limitations than other species of terrestrial carnivores;thus, timing breeding to coincide with times of higher foodavailability in the environment becomes even more important.
Lutra lutra is a species capable of breeding all through theyear but, locally, breeding seasonally. Heggberget (1993)suggested a mechanism based on the polyoestrous pattern ofotter breeding. The ability of the otter to be ready to breedthroughout the whole year, but synchronizing births withmaximum food availability is a good strategy for reducingthe risk of mistaking the time of greatest energy need andlosing the litter in a highly unpredictable setting (Negus andBerger 1987; Philippi and Seger 1989; Heggberget 1993).
Role of large barbel and crayfishIn our Prepyrenees study area, the greater availability of
food during summer is due mainly to the migration of largereproducing barbel (over 256 g) that appear in streams andrivers in April through to October from reservoirs and large
Fig. 8. Monthly variation in the percentage of surveyed stretchesfound dry or with water restricted to pools in rivers of thePrepyrenean area and the Mediterranean rivers of the Ebro basin.
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rivers. During the time when the cubs are in the den, the ot-ter preys more frequently on these large barbel. In otherplaces on the Iberian Peninsula, other similar species of bar-bel can play a similar role, given their similarities in sizeand ecology (Rodriguez-Ruiz and Granado-Lorencio 1992).The higher consumption of these large fish could well be ageneral mechanism for increased reproductive success in thistype of habitat, along the lines of that affirmed by Ruiz-Olmo and Palazón (1997) and Ruiz-Olmo et al. (2001). Inthe Mediterranean rivers of the Ebro basin, the role of largebarbel must be equally important to that in the Prepyrenees,although drought may mainly affect the larger fish owing totheir increased need for water and oxygen and lower toleranceto eutrophication. This is why the food abundance pattern isdifferent here from the one in the Prepyrenees, despite thefact that the prey community is similar. As the water beginsto disappear, large fish like barbel must emigrate to other ar-eas or simply die in the shallow ponds that remain. Smallerfish then follow suit. In such conditions, the otter cubs donot encounter adequate conditions to survive and grow. How-ever, during wet years, otters could breed more easily.
In our study area, nase and other fish seem to be less im-portant in regulating otter breeding, although they do com-plement the effect of barbel. Furthermore, in certain yearswith a high abundance of nase occurring and consequentlyan abundant diet (Ruiz-Olmo 1995a), they could help in thisrole.
Crayfish, especially P. clarkii at the present time, have aseasonality similar to that of barbel (Beja 1995; this study).With their dependence on temperature, the highest abun-dance occurs in summer, which is the time when crayfishappear more often in the otter’s diet, especially betweenMay and September (Beja 1995; Ruiz-Olmo and Palazón1997). Crayfish are also larger in size between the end ofspring and the end of summer (Beja 1995). The Americancrayfish is a smaller prey, with individuals weighing be-tween 5 and 30 g (up to a maximum of around 70 g; Beja1995; our unpublished data). As a source of prey, crayfishare much smaller than reproductive barbel and have a lowdigestibility coefficient, and an important part of each individ-ual is left without being consumed (Konencny 1987; Ruiz-Olmo et al. 1998). Nevertheless, the calorific content of theingested parts is similar (Cummins and Wuycheck 1971;J. Ruiz-Olmo, J. Blasco, S. Santilari, and J.M. López-Martín,in preparation), and crayfish can be found in abundance innumerous patches, with biomass densities that even exceedthose of fish. In such conditions, crayfish become a very ap-propriate prey for L. lutra cubs.
In other areas, with other types of prey communities, theeffect that each one has on breeding may differ because oflocal ecological, ethological, or other determining factors.
Our results show that the presence of adequate prey spe-cies for the cubs (high energy input, easy to catch, handle,and consume, and lower transportation costs for the females)plays an important role in the Eurasian otter breeding cycle.Kruuk (1995) also reported that marine crabs in the ShetlandIslands are a suitable prey for cubs, while Heggberget (1993)in Norway and Kruuk et al. (1987), also in the Shetlands,noted that cubs and their mother consumed larger fish thanfemales without cubs. In our study area otters selected stretcheswith an abundance of fish and crayfish to bring up their cubs
(J. Ruiz-Almo, A. Batet, J. Jiménez, and D. Martínez, inpreparation), and Ruiz-Olmo et al. (2001) reported that thereis a correlation between food abundance, especially barbel,and the number of females that reproduce and the number ofcubs accompanying the females.
In summary, the otter’s breeding cycle was seasonal inboth studied areas. However, patterns varied according tofood and water availability, Ebro’s barbel and the Americancrayfish being the main species affecting the otter’s breedingcycle.
Acknowledgements
This study was carried out with the help of various people.Special thanks to José María López-Martín, Diego Martínez,Santiago Palazón, Javier Pérez-Tous, Ignasi Rodríguez, MariaJosep Vargas, the rangers (Miquel Arilla, Kim Bada, J. Bardina,Josep Manel Bolado, Leocadio Cruz, Josep Gelabert, XavierMaurín, Miquel Palacín, Jaume Perelada, and Just Sorando),and the wildlife reserve wardens (Xavier Agut, Juanjo Cruz,Francesc Julve, and Lluis Tafalla) from the Department ofthe Environment of the Autonomous Government of Catalonia.
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