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BREEDING OF OTTERS (LUTRA LUTRA L.) IN THE WILD IN THE MEDITERRANEAN AREA Jordi RUIZ-OLMO, Francesc MAÑAS AND Antoni BATET Departament de Medi Ambient i Habitatge, Generalitat de Catalunya, Dr. Roux 80, 08017 – Barcelona, Spain. email: [email protected]

Abstract. We update our knowledge on otter breeding in the Iberian Mediterranean habitats: detailing size of litters (embryos, small and large cubs), seasonal breeding patterns, habitat for rearing cubs and pre-dispersal findings. We show the effect of temporal variation of the resources (both food and water availability), providing information about some suspected key species for otter breeding (barbels, eel, corkwing and American crayfish). Key words: Eurasian otter, Lutra lutra, otter, cubs, breeding, Mediterranean habitats, prey

1 INTRODUCTION Otters (Lutra lutra) are a semi-aquatic species, whose life is closely related to water. This is especially true in the case of diet, which is largely made up of aquatic and semi-aquatic species (CHANIN, 1985; MASON AND MACDONALD, 1986; KRUUK, 1995; RUIZ-OLMO AND PALAZÓN, 1997). Fish, crayfish, and amphibians are the most common prey, although, in Mediterranean habitats, water snakes, insects, birds and small mammals are also common items in the diet (ADRIAN AND DELIBES, 1987; RUIZ-OLMO, 1995; RUIZ-OLMO AND PALAZÓN, 1997; BARTOLOMÉ, 2000; CLAVERO ET AL., 2003). Studies of otter breeding behaviour have been carried out mainly in wet, colder and even snowy habitats, such as Britain, Scandinavia, and central and north eastern Europe (STEPHENS, 1957; ERLINGE, 1967; STUBBE, 1969, 1989; WIJNGAARDEN AND PEPPEL, 1970; REUTHER, 1980; CHANIN, 1985; MASON AND MACDONALD, 1986; KRUUK, CONROY AND MOORHOUSE ET AL., 1987; HEGGBERGET, 1988; JORGA, STUBBE AND ZINKE, 1989; RÖBIN, 1989; DE SILVA, 1991; SIDOROVICH, 1991, 1997; SIDOROVICH AND TUMANOV, 1994; KRUUK, 1995; HEGGBERGET, 1993; HEGGBERGET AND CHRISTENSEN, 1996; ANSORGE, ZINKE AND ZINKE, 1997; DÜLFER AND ROCHE, 1998; ELMEROS AND MADSEN, 1999; HAUER, ANSORGE AND ZINKE , 2002; CONROY AND BACON, 2005). Following these studies, the Eurasian otter (Lutra lutra) is confirmed as a polyoestrous species, with litters of 1-5 cubs (more often 1-3). Otters normally breed between spring and early autumn, but some studies have reported otters breeding throughout the year often with seasonal variations, while others have shown breeding to be predominately during the winter months (CONROY AND BACON, 2005) Mediterranean habitats are a special situation for semi-aquatic species such as the otter, because, in these regions, there are large fluctuations and shortages in water and feeding resources, affecting deeply the ecology and behaviour of the species (JIMÉNEZ AND LACOMBA, 1991; RUIZ-OLMO AND PALAZÓN, 1997; RUIZ-OLMO AND DELIBES, 1998; RUIZ-OLMO, LÓPEZMARTÍN AND PALAZÓN 2001b; RUIZ-OLMO ET AL., 2001a, 2002; PRENDA ET AL., 2001; CLAVERO ET AL, 2003; RUIZ-OLMO, 2001, 2004; JIMÉNEZ AND RUIZ-OLMO, in press). Otters are food-limited species (KRUUK AND CARSS, 1996; RUIZ-OLMO, LÓPEZ-MARTÍN AND PALAZÓN, 2001b), because of their high metabolic needs, breeding patterns, heat losses and lifestyle (IVERSEN, 1972; GITTLEMAN AND OFTEDAL, 1987; OFTEDAL AND GITTLEMAN, 1989; MCNAAB, 1989; NOLET AND KRUUK, 1994; KRUUK, 1995), so large fluctuations in resources may be a handicap during breeding time, otters being pressed to adapt to a more efficient way of life (HEGGBERGET, 1993; KRUUK, 1995).

However, most of these studies deal with the biology of the species, and very few with the recruitment, pre-dispersal and dispersal stages, or the habitat selection for breeding or cub rearing (JENKINS, 1980; HARPER, 1981; KRUUK, CONROY AND MOORHOUSE, 1991; KRUUK, 1995; SIDOROVICH, 1997). The only published works on otter breeding in the Mediterranean habitats were carried out in the Iberian Peninsula (RUIZ-OLMO, 1994, 1998; BEJA, 1995, 1996; RUIZ-OLMO ET AL., 2001b, 2002, in press a & b). It is of interest to study the different prey species of otters living in such habitats, with low water availability. This paper updates the information from these studies, in view of the importance of such resource changes, and identifies future research needs.

2 DEFINITIONS To understand more fully the results discussed below, the following definitions are used (RUIZ-OLMO ET AL., 2002, in press b): • •

• •

Cubs in den. Cubs between birth and when they begin to leave their dens. Small cubs. Individuals, approximately 2-3 to six months old (the period at which they begin to leave the den, to when it is difficult to distinguish them from adult otters (mainly the mother) [when they reach 90% of their total length (TL) in the Iberian Peninsula]. Large cubs. Over about six months old up to the time of dispersal (which often occurs between eight and 16 months). Similar size to mothers, with higher walking, escaping and foraging capacities. Rearing cubs’ sector. Is a special stretch or patch selected by females with litters in which they find a quality habitat, to ensure low cub mortality and easier dispersal of young?

3 SIZE OF LITTERS AND FEEDING HABITS RUIZ-OLMO (1994) found an average of 2.0 embryos/female (SD = 0), from a very small sample of Spanish otters (n=5). However, unpublished new data (J. RUIZ-OLMO AND F. MAÑAS, unpublished data) shows an average of 2.06 embryos for 18 Spanish females (SD = 0.54; range 1 – 3), 72% of litters being of two embryos. This is a smaller litter size compared with other studies carried out in Europe in other freshwater habitats (HAUER, ANSORGE AND ZINKE, 2002; CONROY AND BACON, 2005), ranging from 2.3 to 2.9, but similar to coastal Atlantic otters (ranging from 1.7 to 2.2). Explanations for this may vary, but the smaller size of Iberian otters (RUIZ-OLMO, DELIBES AND ZAPATA, 1998), the relative proportion of young and old females in population, proved to have smaller litters (HAUER, ANSORGE AND ZINKE, 2002), and the wide fluctuations and unpredictability in water and food availability (RUIZOLMO ET AL., 2002) could contribute to this smaller litter size. Mean small cubs litter sizes for the different Iberian otter populations range from 1.1 to 2.9 (Table 1) and are within the range described in other countries (Table 1) (CHANIN, 1985; MASON AND MACDONALD, 1986; DE SILVA, 1991; SIDOROVICH, 1991; KRUUK, 1995; ANSORGE, ZINKE AND ZINKE, 1997; DÜLFER AND ROCHE, 1998; ELMEROS AND MADSEN, 1999; HAUER, ANSORGE AND ZINKE, 2002).

Table 1: Breeding patterns of otters (litters of small cubs outside dens) in some Iberian Mediterranean habitats, in relation to variations in food resources. Area

South west Portugala

North east Spain. Ebro basinb, c

Type

Habitat

Mean altitude (m)

Coast

Marine

0

Number of prey species over 5 % in diet 5

Inland

Lowland Mediterranean rivers and streams Altitude oligotrophic streams

0 – 100

5

700 - 1100

Mountain Mediterranean rivers Mountain Mediterranean rivers

Inland. High Pyrenees

Inland. Prepyrenean rivers. Eating fish Inland. Prepyrenean rivers. Eating fish and crayfish Inland. Mediterranean rivers. Eating fish Inland. Mediterranean rivers. Eating fish and crayfish Inland. Mediterranean lowland rivers and wetlands (a)

Average cubs/litter (n)

Breeding pattern

Main births time

Main estimated time to live in den

Maximal food abundance time

Main species in habitat and otter diet

1.73 (11) 2.86 (7)

Seasonal

X – XII

XII – III

XII – III

Seasonal

I – III

III – VI

III - VII

corkwing wrasse (Symphodus melops) eel (Anguilla anguilla)

1

1.12 (8)

All around year (Small sample)

brown trout (Salmo trutta)

2–3

1.57 (49)

All around year (Small sample) V - IX

-

350 – 700

Non seasonal (Small sample) Seasonal

V – IX

Ebro’s barbel (Barbus graellsii)

200 – 400

3–6

2.40 (5)

V – IX

Mediterranean rivers

200 – 600

2–4

1.85 (13)

American crayfish (Procambarus clarckii) and cyprinids Ebro’s Barbel and ase (Chondrostoma miegii)

Mediterranean rivers

200 – 500

3–5

1.60 (5)

>5

1.50 (4)

Lowland Mediterranean rivers, streams and wetlands

0 – 100

Seasonal

III – VI

XII – II for dry years

III - XII

XII – IX for normal years

Small sample

Small sample

Small sample

BEJA (1995, 1996); (b) RUIZ-OLMO AND PALAZÓN (1997), RUIZ-OLMO ET AL. (2001, 2002); (c) Catalonia, eastern Aragón and northern Castelló.

Spring Summer

V – IX

American crayfish and Cyprinids

Small sample

American crayfish, eel and cyprinids

Breeding success (small cub litter size) was connected to prey quality and abundance (Figure 1 and RUIZ-OLMO ET AL., 2002), and for this reason with altitude (Figure 2), because of a decline in fish availability (biomass and numbers) and prey community diversity (RUIZOLMO, 1998). The highest values were found in areas where food diversity was higher (consisting of several fish species and crayfish (Table 1). In comparison, the smallest litters were found in areas where the diet was almost monospecific (brown trout) and food availability lower due to altitude (RUIZ-OLMO, 1998). However, it is also true that in some areas of the Mediterranean, e.g., the rivers of the Ebro basin, where the otter’s diet diversity was high (based on fish and crayfish, which at certain times can be highly abundant), litters were smaller than in other areas with similar diet. In such cases, the effect of drought appears to be the most important factor in explaining this. The availability (and biomass) of the main sources of prey is affected by the lack of water, just at the time when they, the prey species, should be most abundant (BEJA, 1995; RUIZ-OLMO ET AL., 2002, in press c).

Main prey species (> 5%)

6 5 4 3 2 y = 1,9511x - 0,5169 R = 0,77; P = 0.016

1 0 1

1,5

2

2,5

3

Litter size (small cubs / female)

Figure. 1: Relationship between the size of small cub litters and the variety of the otter diet (number of main species in diet, over 5%) in the Iberian peninsula (freshwater and marine habitats), including only localities with sufficient sample size. 1000 900 800

y = -354,29x + 1064,8 R = 0,85; P = 0.015

Altitude (m)

700 600 500 400 300 200 100 0 0,8

1,3

1,8

2,3

2,8

Litter size (small cubs / female)

Figure 2: Relationship between the size of small cub litters and altitude for freshwater habitats of the Iberian Peninsula (including only localities with sufficient sample size).

4 SEASONAL BREEDING PATTERNS AND RESOURCES From a general view, L. lutra was capable of breeding throughout the year in the Iberian Peninsula but, locally, breeding was seasonal (Table 1). Birth distribution patterns of otters corresponded also to variations in abundance of food resources in space and time (Table 1), as previously reported in northern Europe (KRUUK, CONROY AND MOORHOUSE, 1987; HEGGBERGET, 1993; HEGGBERGET AND CHRISTENSEN, 1994; KRUUK, 1995; ELMEROS AND MADSEN, 1999; CONROY AND BACON, 2005). The emergence of cubs outside the dens, at 2-3 months old, coincided with peaks of biomass of main species in the environment. Even if the regulating-species were different in each case (Table 2) and the temporal pattern changed in these different areas, the availability of food resources when the cubs were 2-3 months old, seemed to be particularly important for their survival and breeding patterns, as suggested by HEGGBERGET, (1993) in Norway and KRUUK (1995) in Shetland. At about this age, cubs begin to venture out of the dens, start to take solid food, and increase their energy needs through movement (MASON AND MACDONALD, 1986; HEGGBERGET, 1993; DURBIN 1996; KRUUK, 1995). HEGGBERGET, (1993) suggests a mechanism based on the polyoestrous pattern of otter breeding. The ability of the otter to be ready to breed throughout the whole year, but synchronising births with maximum food availability, is a good strategy for reducing the risk of mistaking the time of greatest energy need and losing the litter in a highly unpredictable setting (NEGUS AND BERGER 1987; PHILIPPI AND SEGER 1989; HEGGBERGET, 1993).

5 HABITAT FOR REARING CUBS AS A LIMITING FACTOR RUIZ-OLMO ET AL (2001b) showed, a narrow relationship between the number of litters using a stretch of water and the fish abundance in such areas for a number of rivers in north east Spain. This relationship was also true for the number of cubs present at each stretch. In both cases, an asymptotic value was found of 3-5 cubs or two litters per 10-12 kilometres stretch of water. So, again otters seemed to be food-limited (KRUUK AND CARSS, 1996), but other complimentary causes may also affect the use of resources. Behavioural avoidance seems to be the complimentary suitable explanation for this. So ‘good habitat’ for rearing litters appears to be an important ‘property’, excluding other litters for competition for feeding or other resources. Some studies have been carried out in north eastern Spain to describe and study such kinds of ‘good habitats’. RUIZ-OLMO ET AL. (in press a) have shown how females rearing small cubs selected special stretches of water: the deepest, with more pools and calm waters, a greater abundance of food and a greater availability of potential and complex dens. So, during this period of breeding, females have selected patches with abundant food (decreasing the foraging time needs and probably the home range size), shelter and cover (to reduce danger of predation), water abundance (to avoid effects of droughts and it is easier for them to learn to swim) and with less danger of cubs dying because floods. In other words, trying to ensure the cubs’ survival and declining the mortality rate. RUIZ-OLMO ET AL. (in press b) demonstrated a low mortality rate during this time, when using rich small patches, both for small and large cubs. But patches to rear small cubs (and also large cubs) can be a limiting factor (RUIZOLMO ET AL., in press a), so females must actively look for such habitat.

Table 2: Characteristics of the key species controlling otter breeding in some areas of the Iberian Peninsula. Area

South west Portugal a

North east Spain. Ebro basinb, c

Habitat

Key species controlling breeding

Abundance in diet (%) during peaks

Average weight in studied areas (g)

Maximum weight in study areas (g)

Calorific value (kJ/g wet weight) d

Coastal

Corkwing wrasse (Symphodus melops) a Eel (Anguilla anguilla) a

57 (biomass) 40 – 50 (energetic value) 10 – 20 (prey –items) 67.2 – 100 (prey-items) 53.7 – 76 (prey-items) 37.5 – 58. 7 (prey-items)

51.0

?

?

20.5

2.500 (up to 10.000)

5.06 – 6.08

50-150

2.000

5.82 – 6.02

98 - 100 %

53 – 259

2.500

5.38 +- 1.08

5 – 30

70

3.99 –4.1

54 - 99 % (biomass) ?

Lowland Mediterranean rivers and streams High Pyrenees Prepyrenean and Mediterranean rivers.

Brown trout (Salmo trutta) b, c Ebro’s barbel (Barbus graellsii) b, c American crayfish (Procambarus clarckii) a,

% of the key species in the fish community (except for crayfish) at 2 month old cubs time 81.2 % (angled) 27.5 % (biomass)

Abundance in patches at 2 moth old cubs period 20 – 25 catch.hour-1.day1

3 – 5 g.m-2

>15 catch.hour-1.day-1

b, c

(a) BEJA (1995, 1996); (b) RUIZ-OLMO AND PALAZÓN (1997), (c ) RUIZ-OLMO ET AL. (2001, 2002) , (d) NORMAN (1963), ELLIOT (1976), CUMMING AND WUYCHECK (1979), NELSON AND& KRUUK (1997), BEJA (1995), RUIZ-OLMO, SANTIPALLI AND BLASCO (Unpublished data)

6 AREAS FOR PRE-DISPERSAL CUBS: REDUCING MORTALITY Recently RUIZ-OLMO ET AL. (in press b) found that females with large cubs from the Spanish Pyrenees, were also selecting special rich patches for food and shelter and largely reducing the home range size. As a result of this, mortality rate during the pre-dispersal time was especially low. Large cub litters from rivers Noguera Ribagorçana and Noguera Pallaresa (Lleida) were found more often than expected at the heads of reservoirs (very rich in prey during fish migrations and spawning), river complex sections (meanders and islands), wider stretches, rough waters, areas with caves and rocky holt systems. Small cub litters were detected more often at narrow stretches and calm (less than 0.5 m3/sec) waters. The ability of females to find and select such patches could be of significant importance in our understanding of otter breeding in different habitats. Part of our current research is focusing on these areas because this is not an unusual situation. From a total of 27 north eastern Spain large cub litters detected in recent years, 33.3 % were found at the heads of a reservoir, despite this being a very rare habitat (RUIZ-OLMO ET AL., in press b). Considering only large litters from the Pyrenees (n=17), this percentage rises to 47.1 %, all the remaining litters being observed at rivers. Such results confirm the general importance of these types of areas. However, large cub litters could select other attributes in other conditions, for example natural rivers or streams, lakes, marshes or marine habitats. Description, location and conservation of such patches are essential tasks. Presently, RAFAEL ROMERO (personal communication) is carrying out his PhD on coastal otters of Galicia (north west Spain), where large litters also seem to use a similar kind area in coastal lagoons for pre-dispersal large cubs.

7 KEY PREY SPECIES FOR BREEDING As with seasonal breeding, RUIZ-OLMO ET AL. (2002) has shown the importance of certain prey species in the regulation of breeding success, habitat use and selection, and otter abundance. Large Iberian barbels (genus Barbus) [in north east Spain, mainly Barbus graellsii], particularly migrating reproductive fish appear to be the main factor regulating otter breeding in most of the stable rivers of the Iberian Peninsula (Tables 1 and 2). These are medium-sized fish (average body mass of reproductive B. graellsii ranging for example from 53 to 259 grams but often reaching more than two kilogrammes; being very abundant at the time of otter breeding, when they are also easy to catch (Table 2). So the abundance and availability of the species could possibly be responsible, at least in part, for controlling otter breeding. However, this is a fish which is badly affected by droughts and this may also be responsible for the problems that otters have in breeding during the droughts of spring and summer (RUIZ-OLMO ET AL., 2001b, 2002). The Iberian Peninsula is a large and diverse region, so we can find other key prey species with a similar role (Table 2). The most widespread is the American crayfish (Procambarus clarckii), sharing habitat with the precedent fish. This is a smaller prey species, but with a very high availability in many patches (BEJA, 1995, RUIZ-OLMO ET AL., 2002). It is a new invasive species which is probably occupying the niche of the native nowendangered crayfish species (Austrapotamobius pallipes), which was formerly a main species in otter diet (CALLEJO, 1998; RUIZ-OLMO AND PALAZÓN, 1997). Perhaps this was also the case of the eel (Anguilla anguilla), now restricted to low altitude rivers and streams, downstream of dams. This was the controlling species in streams of south west Portugal, and seems also to be one of the main factors controlling the breeding of otters in the lowlands of other parts of Portugal, south west Andalusia, Galicia, Asturias, and Cantabria, according also

to its importance in the otter diet in such regions (CALLEJO, 1994; GOMES, 1998; CLAVERO ET 2003; MÓNICA RODRÍGUEZ, personal communication). The dramatic decline of salmon and sea trout has also had a significant influence on this. Finally, BEJA (1995, 1996) identified the importance of the corkwing wrasse (Symphodus melops) for breeding of coastal Atlantic otters, as KRUUK (1995) demonstrated with eelpout (Zoarces viviparus) and rocklings (Ciliata) in Shetland. Such small fish (BEJA, 1995) seemed to be the more favoured in these habitats, being again the most common and abundant, with the exception of the different eel species. However, very little is known about temporal changes and substitute species during shortages of the controlling species. AL.,

8 FUTURE LINES OF RESEARCH The pattern of otter breeding in the Mediterranean countries follows a similar pattern to elsewhere in Europe, with food availability being a main factor regulating this. However, the main differences are related to water limitation, and the shortages originating from this. More research is needed in order to define accurately the actual mechanisms and energetic balance of breeding. Also the role of fluctuations and inter-annual changes should be studied. Finally, the study of natal and cub rearing areas must be undertaken because of its importance in the design of conservation areas.

9 ACKNOWLEDGEMENTS We are grateful for the help of Victòria Asensio, Juan Jiménez, José María López-Martín, Diego Martínez, Antoni Margalida, Josep Maria Olmo-Vidal and Santiago Palazón. Jim Conroy helped to make the manuscript more understandable.

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