Social behavior and ecosystem processes: river otter latrines and nutrient dynamics of terrestrial vegetation.
River otters (Lutra canadensis Schreber) inhabiting coastal environments forage in the intertidal and subtidal zones for marine fish and invertebrates (Larsen 1984, Stenson et al. 1984, Bowyer et al. 1994). These mustelids frequently occur and forage in social groups (Rock et al. 1994) that occupy large home ranges (20-40 km) along the shoreline (Bowyer et al. 1995). As part of their social behavior, river otters mark specific locations along the coast, known as latrine sites (Testa et al. 1994, Bowyer et al. 1995, Kruuk 1996). In these sites, which can be 5-20 m in radius and are typically 25-300 m apart ([approximately]160 latrines/100 km of shoreline), river otters deposit feces and urine, as well as excretions from their anal glands. Although the social function of these latrine sites is not clearly understood (i.e., marking to establish social dominance, marking of feeding sites, etc.; Kruuk 1996), direct observations and removal of feces suggest that the visitation rate to latrine sites is high (Testa et al. 1994, Bowyer et al. 1995; M. Ben-David, personal observation). The distribution of latrine sites along the coast is dependent on several habitat variables. Otters show preference for sites that have shallow, tidal slopes with large rocks and shallow, vegetated slopes with high overstory cover (Bowyer et al. 1995).
In this study, we investigated the effects of marking behavior by river otters on terrestrial vegetation in the marine-terrestrial interface. Because species of intertidal fish and invertebrates have high stable nitrogen ([Delta]15N) values (Kline et al. 1993, Ben-David et al. 1997a, b), we hypothesized that plants growing in latrine sites of river otters would have enriched values of stable nitrogen isotope compared with plants growing elsewhere, reflecting the incorporation of marine-derived nutrients from otter excretions. We further hypothesized that fertilization by river otters would affect community composition of plants as well as nitrogen content of plant tissues.
Two study areas were selected in south-central Alaska, United States: Knight Island (60 [degrees] 30[minutes] N, 147 [degrees] 0[minutes] W) in Prince William Sound and Kachemack Bay (59 [degrees] 40[minutes] N, 151 [degrees] 20 [minutes] W) on the Kenai Peninsula, Both areas have a maritime climate; summers are cool and wet and winters are characterized by deep snow (2200 mm annual precipitation). The snow-free period extends from early May to early November at lower elevations. Vegetation at higher elevations is typically alpine tundra. At lower elevations, there is coastal, old-growth forest of Sitka spruce (Picea sitchensis) and western hemlock (Tsuga heterophylla), with a well-developed understory (mainly Oplopanax horridus, Vaccinium spp., Menziesia ferruginea, and Rubus spp.). Alder (Alnus spp.) tends to occur on disturbed sites and near the boundary of terrestrial vegetation and the intertidal zone.
We obtained samples of otter fur from 12 individuals that were live-trapped in a companion study by G. M. Blundell (Alaska Cooperative Fish and Wildlife Research Unit, University of Alaska Fairbanks). In addition, we collected otter feces (n = 18), vegetation samples from latrine sites (n = 12), and vegetation samples from random sites (n = 9) along the coast. Vegetation samples from random sites were collected only from those sites that had no indication of otter activity (e.g., nonlatrine sites). Vegetation samples were collected within a 10-m radius from the latrine entrance, or the random point for nonlatrine sites, at the beginning of the growing season (early May) in 1994 and 1996. These samples included: spruce needles (Picea sitchensis); leaf buds of red elderberry (Sambucus racemosa); leaf buds of alder (Alnus crispa ssp. sinuata); leaf buds of blueberries (Vaccinium sp.); leaf buds of salmon berries (Rubus spectabilis); leaf buds of devil's club (Oplopanax horridus); blades of grasses (Poaceae); newly emerging fiddleheads of shield fern (Dryopteris expansa); and fronds of goose-necked moss (Rhytidiadelphus triquetrus). When possible, samples were collected from more than one individual plant within the 10-m radius, thereby representing the site rather than an individual plant. Samples were stored in plastic bags and kept frozen until processing.
Analysis of stable isotope ratios
Samples of vegetation, fur, and feces were dried at 60 [degrees]-70 [degrees] C for 48 h and then ground to fine powder using a Wig-L-Bug grinder (Cresent Dental Company, Chicago, Illinois, USA). Subsequently, a subsample (11.5 mg for feces and fur, and 8-10 mg for plant tissues) was weighed into a miniature tin cup (4 X 6 mm) for combustion. We used a Europa C/N continuous-flow isotope ratio mass-spectrometer (CFIRMS, Europa, Crewe, UK) to obtain the stable isotope ratios as well as values of percentage of carbon (C) and nitrogen (N). Each sample was analyzed in duplicate and results were accepted only if the variance between the duplicates did not exceed that of the peptone standard (CV = 0.1).
Values of stable isotopes of possible prey of river otters were adapted from Ben-David et al. (1997a). These values were obtained using methodology identical to that described here (for a detailed species list, see Ben-David et al. 1997a). We used a dual-isotope, multiple-source mixing model to estimate the relative contribution of each prey to the diet of individual otters (Kline et al. 1993, Ben-David et al. 1997a, b), with fractionation values of 1[per thousand] for carbon and 3[per thousand] for nitrogen (Ben-David et al. 1997a, b).
We employed the K nearest neighbor randomization test (Rosing et al. 1998) to investigate whether stable isotope ratios of possible prey were significantly different from each other as required for the use of the mixing model (Rosing et al. 1998). We used a Mann-Whitney test (Zar 1984; SPSS for Windows) to investigate whether stable nitrogen ratios of each species of plant differed significantly between latrines and nonlatrines, as well as the differences in percentage of nitrogen and C:N ratios in plant tissues. We used a one-tailed variance-ratio test to determine if variation in [[Delta].sup.15]N values of plants from latrine sites was higher than that of plants from nonlatrine sites (Zar 1984).
Stable isotope ratios of intertidal and subtidal fish, salmon, freshwater fish, and intertidal crabs differed significantly from each other (K nearest neighbor randomization test; P [less than] 0.05). Stable isotope ratios of otter feces were similar to those of intertidal fish and salmon [ILLUSTRATION FOR FIGURE 1 OMITTED]. Results from the dual-isotope multiple-source mixing model on otter fur indicated that the relative contribution of intertidal and subtidal fish to the diet of otters was 45 [+ or -] 3% (mean [+ or -] 1 SE); salmon composed 32 [+ or -] 3%; intertidal crabs 14 [+ or -] 1%; and freshwater fish only 8 [+ or -] 0.5% of the diet of otters.
Vegetation samples collected on latrine sites were highly enriched with [[Delta].sup.15]N compared with nonlatrine sites (Mann-Whitney for each pairwise comparison, P [less than] 0.05; [ILLUSTRATION FOR FIGURE 2A-C OMITTED]), except for alder (P = 0.46; [ILLUSTRATION FOR FIGURE 2A OMITTED]). Values of [Delta]15N in elderberry were higher than those of otter fur or feces [ILLUSTRATION FOR FIGURES 1 AND 2A OMITTED]. Values of [Delta]15N in moss from latrine sites were significantly higher than those of moss from nonlatrine sites (P = 0.01; [ILLUSTRATION FOR FIGURE 2C OMITTED]), but were within the range of other plant species from nonlatrine sites [ILLUSTRATION FOR FIGURE 2C OMITTED]). Values of [Delta]15N in samples of salmon berry buds, spruce needles, grass blades, and moss fronds from latrine sites showed higher variability than those of plants collected from nonlatrine sites (one-tailed variance ratio test; P [less than] 0.05 for each pairwise comparisons). In addition, the differences in values of [Delta]15N between species within latrine sites were higher than those between species from nonlatrine sites [ILLUSTRATION FOR FIGURE 2A-C OMITTED].
Levels of N in grass and moss from latrine sites were significantly higher than those of the same plants from nonlatrine sites (Table 1). Similarly, C:N ratios in plant tissues were lower in grass and moss from latrines, but no significant difference between sites was detected in either N content or C:N ratio for any of the other plants (Table 1).
Stable isotope ratios of otter feces were similar to those of intertidal and subtidal fish and salmon. These results, along with the stable isotope ratios of otter fur and the results of the mixing model, suggest that river otters in our study areas relied on intertidal fish as the main component of their diet. This is in agreement with results from several studies on the feeding ecology of coastal river otters (Larsen 1984, Stenson et al. 1984, Bowyer et al. 1994).
All plant species collected from latrine sites, except for alder, had significantly higher values of [Delta]15N than did plants collected from nonlatrine sites, reflecting the incorporation of marine-derived nitrogen (N) from otter excretions. Because alder derives most of its nitrogen from the atmosphere via N fixation (Bormann and Gordon 1984), we expected that the fertilization by otters would have no effect on the [Delta]15N in that species. The [TABULAR DATA FOR TABLE 1 OMITTED] overall low values of [Delta]15N in the nonvascular moss in both types of sites are suggestive of absorption of dissolved ammonia (N[H.sub.3]), probably volatilized from urea (Mizutani et al. 1985, Nadelhoffer and Fry 1994, McFarlane et al. 1995), whereas the other plants probably assimilate differing amounts of inorganic ammonium and nitrates (Nadelhoffer and Fry 1988, 1994).
The samples of elderberry from latrine sites had exceptionally high values of [[Delta].sup.15]N compared with other species in the latrines, as well as with values previously reported in the literature (Nadelhoffer and Fry 1994). A plausible explanation for the high values in elderberry is that this species may be assimilating amino acids from otter feces or anal gland secretions. Several studies recently have demonstrated that alpine and arctic plants can absorb free amino acids from the soil (Kielland 1994, 1997, Raab et al. 1996).
Values of [Delta]15N in samples of salmon berries, spruce, moss, and grass from latrine sites showed higher variability than those of the same plants collected from nonlatrine sites. This variation could be due to the patchy nature of fecal deposition and distribution of roots within the latrines. Also, different latrines experience different rates of visitation and fecal deposition, resulting in high variability between sites, and the use of latrine sites by otters may differ through time, resulting in difference in the latrine age.
The differences in values of [Delta]15N between species within latrine sites were higher than those between species from nonlatrine sites. Different N sources and forms of N taken up by plants can cause variation in [Delta]15N values (Schulze et al. 1994, Nadelhoffer et al. 1996). That plants collected from nonlatrine sites showed less difference in [Delta]15N values than those of the same species collected on latrine sites may reflect a more uniform source of N, and suggests higher competition for N in those sites. Whether increased differences in [Delta]15N values with increasing N sources is a result of species-specific uptake of different nitrogenous compounds merits further investigation.
The general lack of difference in plant tissue N concentration between latrines and nonlatrines may result from our sampling procedures. For all plants except moss and grass, we collected newly emerging buds, needles, and fiddleheads (sampling period in early May). Bryant (1987) noted that fertilization had an inconsistent effect on total nitrogen content of shoots, suggesting that the high growth rate of fertilized plants can reduce the N concentration in those tissues. It is possible that fertilization by otters increases productivity and growth rate, rather than elevating N concentration in the newly growing buds. In grasses and mosses, we collected both old and new shoots and no distinction was made between them in the lab analysis. The higher N concentration in latrine specimens from these two species probably represents a higher proportion of new blades and fronds in specimens collected from latrine sites.
Our results indicate that the scent-marking behavior of river otters fertilized the terrestrial vegetation along the shoreline in south-central Alaska. Latrine sites of these carnivores provide an unique system in which such fertilization, uncoupled from herbivory, can be studied, especially in cases in which latrines are found on islands lacking herbivores.
We thank G. M. Blundell for providing samples of otter fur. J. B. Faro, H. Golden, and P. Berry assisted in collecting vegetation samples. N. Haubenstock and B. Barnette performed the analysis of stable isotope ratios. R. Boone, A. Doyle, J. M. Gulledge, K. Kielland, R. W. Ruess, J. Schimel, and two anonymous reviewers provided helpful comments on earlier versions of the manuscript. All procedures were approved by an independent animal care and use committee at the University of Alaska Fairbanks. Funding for the project was provided by the Institute of Arctic Biology, Coastal Marine Institute and Mineral Management Services, and the Trustees Council for the Exxon Valdez Oil Spill.
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|Author:||Ben-David, M.; Bowyer, R.T.; Duffy, L.K.; Roby, D.D.; Schell, D.M.|
|Date:||Oct 1, 1998|
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