MARINE MAMMAL SCIENCE, 20( 1): 134-144 (January 2004) 0 2004 by the Society for Marine Mammalogy

FEEDING ECOLOGY OF THE MARINE OTTER (LUTRA FELINA) IN A ROCKY SEASHORE

OF THE SOUTH OF CHILE GONZALO MEDINA-VOGEL

Instituto de Ecologia y Evolucibn, Universidad Austral de Chile, Casilla 567, Valdivia, Chile E-mail: gmedina@uach.cl

CLAUDIO DELGADO RODR~GUEZ ComitC Nacional Pro Defensa de la Fauna y Flora (CODEFF)

Filial Valdivia Carlos Anwandter 624, C4, Valdivia, Chile

RICARDO E. ALVAREZ P. JOSE LUIS BARTHELD V.

Instituto de Ecologia y Evolucih, Universidad Austral de Chile, Casilla 567, Valdivia, Chile

ABSTRACT

The marine otter (Lutrafelina) lives exclusively along exposed rocky shorelines on the South American Pacific coast from Peru (6'9, to Cape Horn, Chile (56'S), and Isla de 10s Estados, Argentina. L. felina diet and its relationship to prey availability and energy content was assessed by spraint and prey remains analysis, direct observation, and the use of crab pots and fish traps, at four sites on the Valdivian coast in the south of Chile, between June 1999 and June 2000. Based on spraints analysis, the diet was composed of 25 species; 52% (13/25) of the species identified were crustaceans, 40% (10/25) were fish, and 8% (2/25) were mollusks. Crustaceans were found in 78% of 475 spraints, 100% of 929 prey remains, and 90.8% of prey determined by direct observation, fish in 20% of spraints and 9.0% of prey determined by direct observation, and mollusks in 2% of spraints and 0.2% of prey determined by direct observation. Observed seasonal variation in prey availability was reflected in the otter diet. Fourteen prey species were trapped; 43% (6114) were crustaceans and 57% (8/14) fish, crustaceans were 93% of 566 trapped individuals, fish 7%. L. felina showed opportunistic feeding behavior, selecting prey seasonally according to their availability rather than to their energy input.

Key words: marine otter, Ltltru felina, feeding ecology, seasonal variations, opportunistic predator.

134

MEDINA-VOGEL ETAL.: MARINE OTTER 135

Studies of the diet of L. felina are based on direct observation and spraint analysis (Castilla and Bahamondes 1979, Ostfeld et al. 1989, Sielfeld 1990, Medina 1995a). Previous diet studies indicated that fish are the main prey of L. filina in southern Chile, particularly species of the families Bovichthyidae, Nototheniidae, Branchios- tegidae, Scorpaenidae, Harpagiferidae, Blenniidae, Cheilodactylidae, Gobiesocidae, and Pomacentridae (Sielfeld 1990). In comparison, the diet of L. felina is composed mainly of macroinvertebrates (crabs) and mollusks north of 48"s (Castilla and Bahamondes 1979, Ostfeld et al. 1989, Medina 1995a), suggesting a latitudinal variation along its distribution from southern Peru (6"s) to Cape Horn (56"s). However, little is known about seasonal variation in the otter diet or prey selection and how diet is affected by variation in prey availability and energy content. In other otter species (Lutra perspicillata, Lutra ltltra) diets are related to prey availability and to the size or speed of fish prey (Erlinge 1967, Wise et al. 1981, Kruuk 1995, Houssain and Choudhury 1998). In areas where both fish and crabs were abundant, L. htra prefered fish, and in years with unusually low fish availability, otters consumed lower quality prey such as crabs (Kruuk and Moorhouse 1990, Kruuk 1995). The present paper examines seasonal variation in the diet of L. felina in relation to prey availability, and discusses the results with respect to differences in the net energy gain by marine otters from different prey.

METHODS

The study area consisted of four sites in Valdivia province between Punta Bonifacio (39"41'30"S, 73"W) and Punta Chungungo (39"39'3O''S, 73"W) (Fig. 1). Each site was approximately 1 km long and 1.5 km away from the other sites. The seashore of the study area had a tidal range of 0.6-3.0 m and was dominated by brown algae (Duwillaeu antartica, Macrocysits pyrifera, Lessonia nigrescens). The study sites were selected according to their accessibility, the abundance of otters, and the ease of observing otters.

The sites were patrolled each month for otter spraints and food remains from June 1999 to June 2000. Food remains refers to prey brought ashore but not completely consumed. Thereafter, monthly surveys were made in each site along the seashore and all spraints and food remains were collected for analysis from June 1999 to June 2000. Spraints were washed and dried at 75OC for 24-48 h and stored in paper bags (Bagenal 1978, Medina 1995a, 1998). Prey remains in spraints were identified with taxonomic keys and reference material (Viviani 1969). Prey size was determined by direct observation by comparing it with the size of the otter's head or paw using 10 X 50 binoculars (Ostfeld et al. 1989), whereby prey smaller than the width of the otter's paw are small, those larger than the paw, but smaller than the width of the head, are medium, and the others are large. To compare the three size categories of crabs and fish identified in spraints and food remains with those determined by direct observation, five otters were live-trapped using Victor 1.5 Soft Catch traps and the size of the heads and paws of the trapped otters measures. Finally we compared the measured results with the determined size of crabs and fish found in the spraints and food remains. The size of fish eaten by otters was estimated from the relation- ship between the length of caudal vertebrae and the length of previously measured fish (Sokal and Rolf 1981, Freund and Simon 1992, Kloskowski et al. 2000). Observations were made by three observers at three different points in each study site. Each observer scanned his entire section for 2 min every 8 min, for an 8-h period, one

136 MARINE MAMMAL SCIENCE, VOL. 20. NO. 1. 2004

.39"40' Study Area ,

Pacific

-39"42'

Figure I. Geographic location of the study area and four sites. Scale 1:60,000 at 0"

day per month for one year, for a total of 320 h of observation, recording the feeding events and prey characteristics of otters spotted only inside his section.

To examine the opportunistic feeding behavior of L. felina, we assessed the relationship between otter diet, prey quality, and availability by trapping macro- crustaceans and fish. Macrocrustaceans were trapped with a line of 10 crab pots, each crab pot had two opposite entrances 15 cm in diameter with a 0.5 cm wide bar placed across the middle allowing large crabs to enter, but preventing otters from entering the traps. Ten fish traps with a single 10 cm diameter entrance were used to assess fish availability in each site (Kruuk 1995). The fish traps consisted of two tandem compartments with serial entrances that passed fish through funnel-shaped throats to reduce the chance of fish escaping the trap. Both trap types were seated on the sea bed 30 rn from shore at each site for one day each month. Each macrocrustacean and fish captured was identified, measured, and used as a reference for spraint analysis. The energy content of each prey was obtained by analyzing captured samples with a calorimetric pump and from previous studies (Duarte et al. 1980). Prey availability was expressed as the number of trapped individualdhour (Houssain and Choudhury 1998). Jacobs Index of Preference [(D = Y - p ) / ( ~ + p - 2rp)l was used to assess prey preferences, where r is the relative proportion of prey identified in the diet, p the relative proportion of the same species trapped in the sea, and D varies from -1 to 0 when there is a negative preference, from 0 to 1 when there is a positive preference, and 0 when there is no preference (Jacobs 1974, Geideizs 1996).

Data were grouped and stratified by seasons. Our data were non-normal and variances differed significantly after transformation by Log,, according to the Kolmogorov-Simirnov test for normal distribution and the Bartlett test for equal variances (Sokal and Rolf 1981, Zar 1996). Thus, Friedman two-way ANOVA by ranks was used to examine the effect of season on diet (Zar 1996). Variation in diet composition was determined through a multiple-comparison procedure (among seasons and among species) using a chi-squared test of homogeneity (Siege1 1956,

MEDINA-VOGEL ETAL.: MARINE OTTER 137

Neu et al. 1974, Krebs 1989). Data were expressed as frequency of occurrence (num- ber of spraints in which a species occurred divided by the total number of spraints collected), and percentage of relative frequency (number of spraints in which a species occurred divided by the total occurrence of all species tested) (Erlinge 1967; Rowe- Rowe 1977; Krebs 1989; Medina 1997, 1998). Prey diversity in the diet was assessed using the Shannon-Wiener diversity index, while seasonal differences were tested using Hurcheson’s t-test (Magurran 1988). Significance was set at 5% for all tests.

RESULTS

Diet Composition

Thirteen crab species were the most frequent (78.4%) prey in the 475 spraints collected, followed by ten species of fish (20.2%) and two species of mollusks (1.4%). Tuliepzls dentatas (22%) and Petrolistbes desmarestii (1 3.6%) were the most frequent prey (Table 1). A seasonal difference in the diet (F3,37 = 12.7, P = 0.005) due to an increase in the frequency of C. edwardsi between spring and winter (& = 256.7, P= 0.000) was found. Also, there was a seasonal difference among fish remains in the determined diet (F3,28 = 10.9, P = 0.014).

The lowest diversity of prey species in the diet (Shannon-Wiener H’ = 0.81) was found in autumn and the highest in spring (H’ = 0.98), but no significant statistical difference (t120,2 = 1.6, P = 0.116) was found.

Eight crustacean species were identified in food remains. Cancer edwardsi (25.8%), Homulapsis plana (22.1%) and T, dentatas (20.1%) where the most frequent prey species. E. maclovinus (3.3%), C. genigzlttatzls (2.3%) and B. chilensis (2.2%) were the most frequently eaten fish species (Table 1). Direct observation indicated that crustaceans were the most important prey consumed (90.1%), followed by fish (9%).

Prey Size

Of the ten fish species identified in the otter spraints, the size of 100 individuals was determined. Fish of the species B. chilensis, E. muclovinw, C. genigzlttatzls, and l? microps were mainly large (83%) and medium-sized (17%).

Most food remains varied from medium-sized (55.5%), to large (23.2%), and small (21.3%) crabs. From spring to autumn, otter prey were mostly medium-sized crabs (3.8-7.6 cm carapace width) corresponding to 33.4% of the identified food remains. During winter, small crabs (up to 3.8 cm) were the most frequent prey.

Direct observation of 330 feeding events indicated that 33.4% were medium and 29.6% large crabs, 3% were medium and 5.4% large fish prey species, the rest (27.7%) were mostly small crabs.

Prey Avuilability

A total of 566 fish and crustaceans, including six species of crustaceans and eight species of fish were trapped. Crustaceans represented 93.3% of the sample (Table 2). Just as 1: dentutzls and C. edwardsi were the most abundant components of otter spraints and food remains, they were also the species most frequently trapped (Table 1, 2). Furthermore, as was recorded in the spraint analysis, there were significant seasonal (F3,16 = 13.9, P = 0.001) differences among trapped crustaceans species, with the

138 MARINE MAMMAL SCIENCE, VOL. 20, NO. 1, 2004

Table I . Occurrence and relative frequency (%) of prey species or family in 475 Lontra felina spraints and 929 prey remains collected.

Spraints Food remains

Prey species Relative Relative or family Occurrence frequency Occurrence frequency

Crustaceans Homalaspis plana Cancer setosus Cancer edwardsi Cancer coronatus Taliepus dentatus Ovalipes punctatus Paraxanthus barbiger Petrolisthes tuberculosus Petrolisthes violaceous Petrolisthes desmarestii Allopetrolisthes perlatus Allopetrolisthes punctatus Pisoides edwarsi Unidentified Total

Fish Gobiesocidae” Bovichthus chilensis Eleginops maclovinus Mugiloides chilensis Prolatilus jugularis Genyprerus chilensis Odonthestes regia Myxodes viridis Calliclinus geniguttatus Paralichthys microps Unidentified Total

Mollusks Octopus vulgaris Fisurella sp. Unidentified Total

12.8 1.8

33.0 3.0

58.0 3.8

14.3 4.8

12.3 36.0 0.8 7.5 0.5

18.8 207.0

4.5 5.8 8.8 1.3 2.5 1.3 0.3 0.5 6.0 0.5

22.0 53.25

2.0 1.5 0.5 3.75

4.8 0.7

12.5 1.1

22.0 1.4 5.4 1.8 4.6

13.6 0.3 2.8 0.2 7.1

78.4

1.7 2.2 3.3 0.5 1 .0 0.5 0.1 0.2 2.3 0.2 8.3

20.2

0.8 0.6 0.2 1.4

12.8 4.7

15.0 2.0

11.7 1.1

10.7

58.0

22.1 8.1

25.8 3.4

20.1 1.8

18.4

99.7

a From Duarte et al (1980).

2 major difference between spring and autumn (xs =96,387, P = O O O l ) , due to the high catch frequency of C. edwarsi. Also, as in the otter diets, the most frequently trapped fish species were E. maclovinus and C. geniguttatus followed by l? jugularis and B. chilensis, but there were no seasonal differences in fish catches (F3, ,9 = 1.3, P = 0.722) (Table 2). Additionally, as in the determined otter diet, most captured crustaceans and fish were medium (60.6%) and large-sized (35.2%), without seasonal variations (F3, , = 4.2, P = 0.24). During autumn T. dentatus was the only small crustacean trapped, while Mugiloides chilensis was the only small fish.

MEDINA-VOGEL ET AL.: MARINE OTTER 139

Table 2. Seasonal relative frequency (%) of crustaceans and fish species trapped during one year at the study site.

Seasons Prey species Summer Autumn Winter Spring

Crustaceans Homalaspis plana 10.8 12.0 16.0 19.0 Cancer setosus 6.3 8.4 3.9 2.5 Cancer edwardsi 29.7 15.0 2.0 43.8 Cancer coronatus 12.6 7.8 0.0 1.3

Oualipes punctatus 1.4 0.0 2.4 0.7 Total 94.8 95.2 90.3 92.7

Bovichthus chilensis 0.7 0.0 0.9 1.8 Eleginops marlwinus 1.6 1.2 1.2 2.7 Mugiloides chilensis 0.0 0.0 0.0 0.1 Prolatilus jugularis 0.7 0.6 0.0 1.7 Genypterus chilensis 0.0 0.6 2.1 0.0 Callicinus geniguttatus 1.6 1.8 3.3 0.5 Polistotrema polytrema 0.0 0.0 2.1 0.0

9.7 7.3 Total

Taliepus dentatus 33.9 52.1 66.0 25.5

Fish

~ ~. 4.8

~~

5.2 ~~

Prey Quality and Selection

There were only weak preferences for Oualipespunctatus during summer (J = 0.25) and spring (J = O . j l ) , for C. edwardsi in winter (J = 0.24), and for C. coronatus in spring (J = 0.25). There was no correlation between the frequency of consumed crustaceans and the energy content (J/g) of prey species. Furthermore, frequently consumed species like T dentatus had low energy content (10.9 J/g) (Table 3). Other species with higher or similar energy content such as 0. punctatus (20.5 J/g), C. setosus (13.8 J/g), and P. barbiger (13.4 J/g) were not important in the diet (Table 1, 3). However, there was a positive correlation (r = 0.82) between the fish species most frequently recorded in the diet and their energy content (Table 3), with E. muchinus (24.3 J/g) and C. geniguttatus (21.8 J/g) as the most frequent fish consumed.

DISCUSSION

Previous studies of L. felina elsewhere in Chile done by direct observation and spraints analysis recorded latitudinal variations in the diet, feeding periods, and dive time (Castilla and Bahamondes 1979, Ostfeld et al. 1989, Sielfeld 1990, Medina 1995a). We found that L. felina fed mostly on crustacean species, and the more frequently trapped species by our trap transects were also eaten in greater frequency. However, there were differences between the number of prey species trapped and those found in the spraints. Species of Gobiesocidae are mostly found in the intertidal zone (Moreno and Castilla 1976) and because of the continuous sea waves breaking strongly in the intertidal zone, the traps were located in the subtidal zone. Similarly, Odentbestes regia, M . uiridis, Paralicbtbys microps, P. tuberculosus, P. uiolaceous, l?

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Table 3. Relative frequency (%), energy, mean size and weight, and gross energy contribution to diet of crustaceans and fish species identified in the Lutra felinu diet.

Gross energy Relative Energy Mean size and content in diet

Prey species frequency (J/g dry mass) mass (g) (J dry mass) Crustaceans

Homalaspis plana 4.8 Cancer setosusa 0.7 Cancer edwardsi" 12.5

Ovalipes puncatus 1.4

Petrolisthes violaceous 1.8 Petrolisthes desmarestii 13.6

Taliepus dentatus' 22.0

Paraxanthus barbiger" 5.4

Fish Eleginops maclovinus 3.3

Prolatilus jugularis 1 .o

Odonthestes regia 0.1

Mugiloides chilensis 0.5

Genypterus chilensis 0.5

Calliclinus geniguttatus 2.3

a From Duarte et al (1980).

7.9 13.8 10.5 10.9 20.5 13.4 10.5 9.6

24.3 21.8 21.8 22.2 20.5 21.8

Large (225.6) Medium (180.1)

Large (228.2) Small (92.1) Large (204.8)

Medium (180.0) Small (22.4) Small (19.3)

Large (176.0) Large (I 2 5 .O)

Medium ( 107.8) Large (183.3)

Medium (85.0) Small (79.0)

8,555 1,740

29,95 1 22,086 5,878

13,025 423

2,520

14,113 1,363 2,350 2,035

174 3,961

desmarestii, and l? edwardsi are also associated with the intertidal zone (Moreno and Castilla 1976). Also there are factors that might affect the number of prey species trapped such as the size of the trap entrance, the area covered, type of bait, and the trap efficiency for different species. There was presumably a variation in the "trapability" among prey species, therefore our conclusions about relative prey preferences are tentative (Kruuk 1995). We tried to avoid biases from not considering prey without hard parts in the case of food remains, or whose hard parts were not ingested in case of spraints, and by supporting our research with direct observation (Castilla and Bahamondes 1979; Medina 1995a, 6; Kruuk 1995). Although the assessment of diet from spraints analysis, percentages of occurrence, and relative frequency tend to overrepresent minor items and underrepresent major ones (Wise et al. 1981), these methods are useful indicators of the most important prey categories and their relationship with variation in prey availability (Ruiz-Olmo et al. 1989; Kruuk 1995; Medina 1995a, 1997).

Otters appear to fall into two groups according to their diet: those that feed mostly on invertebrates (Enhydra lutris, Aonyx capensis, A. cinerea), and those that feed mainly on fish (Lontra canadensis, L. longuicaudis, Pteronura brasiliensis, and species of the genus Lutra) (Rowe-Rowe 1977, Estes et al. 1982, Chanin 1985, Mason and Macdonald 1986, Estes 1989, Gittleman 1989, Perrin and Carugati 2000). Although, crustaceans have been described as a lower quality (in terms of energy) food for otters than fish (Kruuk 1995 and this study), our results confirm previous studies that L. felina consume mainly invertebrates (Ostfeld et al. 1989, Medina 1995a), and that it is an opportunistic predator, feeding mainly on the most abundant subtidal prey species, responding to seasonal variations in prey availability. This behavior has also been described in Lutra lutra which eats bottom-dwelling fish during most of the year, but changes to other fish species during winter (Kruuk

MEDINA-VOGEL ET AL.: MARINE OTTER 141

and Moorhouse 1990, Kruuk 1995). Similarly, L. provocax eats mainly two type of crustaceans in freshwater habitats, one more abundant in the diet described in lakes, and the other in the outlet rivers (Medina 1998). In Belarus, L. lutra varies its diet in response to an increase in fish availability during spawning (Sidorovich 2000). In South Africa, A. capensis and L. maculicollis eat fewer crustaceans during winter, when crustaceans are less available (Perrin and Carugati 2000). These variations in otter diet have been attributed mostly to differences in prey availability (Kruuk 1995, Hussain and Choudhury 1998).

So why should an opportunistic behavior be of benefit to an aquatic carnivore like L. felina? Aquatic mammals may deal with heat loss imposed by their cold environ- ment in three ways: by increased insulation, increased metabolic heat production, and decreased surface-to-volume ratios (Scholander et al. 1950). However, there are exceptions that cast doubt on the invariability of the relationship of greater size and aquatic life style. This is the case of L. felina, which as the smallest of its congeners, inhabits the cold temperate marine environment of Chile and Peru. Therefore, L. felina might compensate for heat loss imposed by their cold environment by increasing heat production and spending time mostly feeding, thereby reducing search and pursuit times for prey and increasing net energy gain. This supports the view that food is an important limiting resource to otters. For example, the time spent by sea otters (Enhydra lutris) foraging, is correlated with population status and food availability (Estes et al. 1982, 1986). L.felina spent less than 30% of its daily activity feeding, and dive times varied throughout its distribution, being markedly shorter in the southern study areas than in more northern areas (Ostfeld et al. 1989, Medina 19956). But another factor that may influence the diet of L. felina is its feeding behavior (Gittleman 1989). Crustacean-eating otters, like Aonyx cinerea and E . lutris, use their digits to find prey, so vision is less important in hunting than it is for fish- eating otters like Lutra and Pteronwa (Estes 1989). In our study area underwater visibility is poor during most of the year, so L. felina, like E. lutris, may be required to use its digits and whiskers to search for prey on the seabed, rock surfaces, or in seaweed (Estes 1989). Thus, the diets we observed contained mostly seabed-dwelling species. Other factors contributing to prey selection and the variation in the net rate of energy gain by the marine otter include a long search, pursuit times, and high handling costs. These factors can cause what might seem to be highly valuable prey to actually being very costly to the consumer (Estes 1989). L. felina almost always take medium and large prey ashore but eat small prey at sea, and its large prey are associated with longer dive times (Ostfeld et al. 1989, Medina 1995a). Therefore, it appears that the high availability, ease of capture, and low handling time, make T. dentatus, a small prey, the most frequent prey for L. felina. Thus, as in other species of otters, L. felina hunting success is influenced by prey availability, water depth, and the size ofprey (Bainbridge 1958, Mason and Macdonald 1986, Kruuk 1995). The estimated gross energy contribution of a rather low quality prey, such as T. dentatus, was higher than that provided by the most commonly consumed large fish (E . maclovinus), that is transported to shore before eating. Therefore, highly available, easy to capture small crabs which can be eaten at the surface might be better prey in terms of the net energy gain for L. felina than a large fish.

The results of this study support the conclusion that the most common prey of L. felina is the one most available in the subtidal environment. Further, that the net energy gain of L. felina depends more on prey that are easy to capture, transport, and consume, rather than on high energy density. Therefore, it is possible that human predation of intertidal and subtidal invertebrates (e.g., Castilla and Durin 1985,

142 MARINE MAMMAL SCIENCE, VOL. 20, NO. 1, 2004

Moreno 2001) could decrease the availability for otters of more accessible prey species such as those with commercial interest (e.g., C. edwursi, H, pluna), causing otters to seek for less available prey or those more difficult to catch and eat (Ostfeld etul. 1989).

ACKNOWLEDGMENTS

We thank the Frankfurt Zoological Society, the Comiti Nacional Pro Defensa de la Fauna y la Flora, and the International Otter Survival Fund for financial and equipment support; Dr. Carlos Jara for help in species identification, Dr. Kristin L. Laidre for early revisions and comments, Mr. Fernando Jara for help in statistical analyses, and Drs. Jim Estes, J. Bodkin, and Milton Gallardo for reviewing the manuscript and important contributions. We also wish to thank Mr. Re& Monsalve for his help during the field work and the Earthwatch Institute volunteers for proofreading the English text.

LITERATURE CITED

BAGENAL, T. 1978. Methods for assessment of fish production in freshwater. Handbook No. 3. International Biological Program. Third edition. Blackwell Scientific Publications Ltd., Oxford, UK.

BAINBRIDGE, R. 1958. The speed of swimming of fish as related to size and the frequency and amplitude of the tail beat. Experimental Biology 35:109-133.

CASTILLA, J. C., AND I. BAHAMONDES. 1979. Observaciones conductuales y ecol6gicas sobre Lutra felina. (Molina) 1782 (Carnivora: Mustelidae) en las zonas central y centro-norte de Chile. Archivos de Biologia. y Medicina Experimentales 12:119-132.

CASTILLA, J. C., AND L. R. DURAN. 1985. Human exclusion from rocky intertidal zone of central Chile: The effects on Concholepas concholepus (Gastropoda). Oikos 45:391-399.

CHANIN, P. 1985. The natural history of otters. Facts On File, Inc., New York, NY. DUARTE, W. E., F. JARA AND C. A. MORENO. 1980. Contenido energitico del algunos

invertebrados bent6nicos de la costa de Chile y fluctuaci6n anual en Mytiha chilensis Hupe 1854. Boletin. Instituto Oceanogrhfico de Chile 29157-162.

ESTES, J. A. 1989. Adaptations for aquatic living by carnivores. Pages 242-282 in L. L. Gittleman, ed. Carnivore behavior, ecology, and evolution. Cornell University Press, New York, N Y

ESTES, J. A,, R. J. JAMESON AND E. B. RHODE. 1982. Activity and prey selection in the sea otter: Influence in population status on community structure. American. Naturalist 120:242-258.

ESTES, J. A., K. E. UNDERWOOD AND M. J. KARMA". 1986. Activity-time budget of sea otters in California. Journal of Wildlife Management 50:626-637.

ERLINGE, S. 1967. Food habits of the otter (Lutra lutva) and the mink (Mwtelu vison) in a trout water in southern Sweden. Oikos 2O:l-7.

FREUND, E. F., AND G. A. SIMON. 1992. Estadistica elemental. Octava edici6n. Prentice Hall, Mexico.

GEIDEIZS, L. 1996. Food availability versus food utilization by otters (Lutra lutva L.) in the Oberlausitz pondland in Saxony, Eastern Germany. IUCN Otter Specialist Group Bulletin 13:58-70.

GITTLEMAN, J. L. 1989. Carnivore behaviour ecology, and evolution. Cornell University Press, New York, NY.

HOUSSAIN, S. A,, AND B. C. CHOUDHURY. 1998. Feeding ecology of the smooth-coated otter Liitra perspicillata in the National Chambal Sanctuary, India. Pages 229-249 in N. Dunstone and M. Gorman, eds. Behaviour and ecology of riparian mammals. Cambridge University Press, Cambridge, UK.

JACOBS, J. 1974. Quantitative measurement of food selection. A modification of the forage ratio and Ivlev's electivity index. Oecologia 14:413-417.

MEDINA-VOGEL ET AL. : MARINE OTTER 143

KLOSKOWSKI, J., A. GRENDEL AND M. WRONKA. 2000. The use of fish bones of three farm fish species in the diet of the Eurasian otters, Lutra lutra. Folia Zoologica 49:184-190.

KREBS, C. J. 1989. Ecological methodology. Harpers Collins Publishers, Inc., New York, Ny.

KRUUK, H. 1995. Wild otters-predation and populations. Oxford University Press, Oxford, UK.

KRUUK, H., AND A. MOORHOUSE. 1990 Seasonal and spatial differences in food selection by otters (Lutra lutra) in Shetland. Journal of Zoology, London 221:621-637.

MAGURRAN, A. E. 1988. Ecological diversity and its measurement. Croom Helm, London, UK.

MASON, C. F., AND S. M. MACDONALD. 1986. Otters: Ecology and conservation. Cambridge University Press, Cambridge, UK.

MEDINA, G. 1995a. Feeding habits of marine otter (Lutra felina) in southern Chile. Pages 65-68 in C. Reuther and C. D. Rowe-Rowe eds. Proceedings of the VI International Otter Colloquium, Pietermaritzburg, Hankensbiittel. Habitat 1 1.

MEDINA, G. 19956. Activity budget and social behavior of marine otter (Lutra feiina) in southern Chile. Pages 62-64 in C. Reuther and C. D. Rowe-Rowe, eds. Proceedings of the VI International Otter Colloquium, Pietermaritzburg, Hankensbuttel. Habitat 11.

MEDINA, G. 1997. A comparison of the diet and distribution of southern river otter (Lutra provocax) and mink (Mustela vison) in Southern Chile. Journal of Zoology, London 242:291-297.

MEDINA, G. 1998. Seasonal variations and changes in the diet of southern river otter in different freshwater habitats in Chile. Acta Theriologica 43:285-292.

MORENO, C. 2001. Community patterns generated by human harvesting on Chilean shores: A review. Aquatic Conservation: Marine and Freshwater Ecosystems 11: 19-30.

MORENO, C., AND J. C. CASTILLA. 1976. Guia para el reconocimiento y observaci6n de 10s peces de Chile. Serie Expedici6n a Chile, Editora Nacional Gabriela Mistral, Santiago, Chile.

NEU, c. W., C. R. BVERS AND J. M. PEEK. 1974. A technique for analysis of utilization- availability data. Journal of Wildlife Management 38:541-545.

OSTFELD, R. S., L. EBENSPERGER, L. KLOSTERMAND AND J. C. CASTILLA. 1989. Foraging, activity budget, and social behavior of the South American marine otter Lutra felzna (Molina 1782). National Geographic Research 5:422438.

PERRIN, M. R., AND C. CARUGATI. 2000. Food habits of coexisting Cape clawless otter and spotted-necked otter in the KwaZulu-Natal, Drakensberg, South Africa. South African Journal of Wildlife Resources 30:85-92.

ROWE-ROWE, D. T. 1977. Food ecology of otters in Natal, South Africa. Oikos 28:210-219. RUE-OLMO, J., G. JORDAN AND J. GONZALBEZ. 1989. Alimentaci6n de la nutria (Lgtru htru

L., 1758) en el Nordeste de la Peninsula Ibirica. Doiiana Acta Vertebrata 16(2):

SCHOLANDER, P. F., R. HOCK, V. WALTERS AND L. IRVING. 1950. Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biological Bulletin 99259-27 1.

SIEGEL, S. 1956. Non-parametric statistic for the behavioural sciences. Hill Brook, Inc., New York, NY.

SIELFELD, W. K. 1990. Dieta del Chungungo (Ltltra felina, Molina, 1782) (Mustelidae, Carnivora) en Chile Austral. Investigaciones Cientificas y Ticnicas, Serie Ciencias de Mar 1:23-29.

SIDOROVICH, V. E. 2000. Seasonal variation in feeding habits of riparian mustelids in river valleys of NE Belarus. Acta Theriologica 45:233-242.

SOUL, R. R., AND F. J. ROLF. 1981. Biometry. W. H. Freeman, New York, NY. VIVIANI, C. A. 1969. Los porcellanidae (Crustacea Anomura) chilenos. Sonderdruck aus

227-237.

Beitrage zur Neotropischen Fauna, Band VI, Heft 1:40-56.

144 MARINE MAMMAL SCIENCE, VOL. 20, NO. 1, 2004

WISE, M. H., I. J. LINN AND C. R. KENNEDY. 1981. A comparison of the feeding biology of mink Mustela uison and otter Lutra lutra. Journal Zoology, London 192:25-31.

ZAR, J. 1996. Biostatistical analyses. Third Edition. Prentice Hall, Upper Saddle River, NJ.

Received: 14 June 2002 Accepted: 25 April 2003