Isotopic and Gross Fecal Analysis of American Black Bear Scats

Isotopic and gross fecal analysis of American black bear scats

K.A. Hatch1,7, B.L. Roeder2, R.S. Buckman2, B.H. Gale2, S.T. Bunnell3, D.L. Eggett4, J. Auger3, L.A. Felicetti5, and G.V. Hilderbrand6

1Department of Biology, C.W. Post Campus, Long Island University, Brookville, NY 11548-1327, USA 2Department of Biology, Brigham Young University, Provo, UT 84602-5255, USA 3Department of Plant & Wildlife Sciences, Brigham Young University, Provo, UT 84602-5255, USA 4Department of Statistics, Brigham Young University, Provo, UT 84602-5255, USA 5Department of Natural Resources, Washington State University, Pullman, WA 99164, USA 6National Park Service–Alaska Region, Anchorage, AK 99501, USA

Abstract: Previous studies have demonstrated the potential of carbon and nitrogen stable isotope analysis (SIA) of feces for use in understanding dietary components and sources. These studies suggest that SIA is useful because it is noninvasive and provides more recent dietary information integrated over a shorter time period than SIA of tissues. We sought to determine whether SIA could be employed in the analysis of feces of American black bears (Ursus americanus) in Utah. Using archived feces, we compared SIA with gross fecal analyses (GFA) to determine if a relationship existed. The percent volume of grass and pine nuts were the only significant indicators of the d13C of feces. The amount of animal matter was the sole significant indicator of the d15N value of feces. Although these measures were only weakly indicative (R2 , 0.21), it is interesting that even in an environment that is isotopically homogenous, d15N and d13C provided information on the contribution of dietary components. The comparatively tight distribution of fecal d13C values, essentially ranging 224 to 228%, clearly indicated a diet of C3 plants. However, this study did not examine the effect of differential digestibility or intestinal slough on d13C and d15N values of feces. This needs to be examined. We also encourage additional studies on the usefulness of SIA of feces of omnivores and carnivores. Very few studies exist for these species, and since many of these species are particularly difficult to handle, SIA of feces may provide crucial knowledge of their short-term dietary habits.

Key words: American black bears, diet, feces, gross fecal analysis, stable isotopes, Ursus americanus

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Dietary analysis of animals has traditionally been West et al. 2004, Mizukami et al. 2005, Podlesak limited to gross fecal analysis, stomach content et al. 2005, Cerling et al. 2006) and measuring the analysis, and foraging observations. In the past incorporated dietary components (Hilderbrand et al. 20 years, however, researchers have made great 1996, 1999; Mowat and Heard 2006). strides in understanding the relationships between American black bears (Ursus americanus) are oppor- stable isotope composition of an animal’s diet and tunistic, generalist omnivores (Benson and Chamberlain the isotopic composition of the animal and its 2006, Fortin et al. 2007) whose foraging behavior can be tissues. Stable isotope analysis (SIA) to understand affected by season, gender, reproductive status, and composition of an animal’s diet commonly uses predation risk to offspring (Jacoby et al. 1999, Fortin animal tissues such as bone collagen, muscle, blood, et al. 2007). Although they are morphologically and feathers, and hair. These tissues offer the advantages taxonomically ranked with carnivores, they have a of measuring changes in stable isotope ratios at broad dietary niche with varying degrees of insectivory, different times scales (Hilderbrand et al. 1996, piscivory, frugivory, and herbivory depending on Dalerum and Angerbjorn 2005), acting as recorders available resources (Bull et al. 2001, Iverson et al. of changes in stable isotope ratios (Knoff et al. 2002, 2001, Belant et al. 2006, Fortin et al. 2007). Researchers have developed a strong understand- [email protected] ing of the relationship between the isotopic signatures

133 134 ISOTOPIC AND GROSS FECAL ANALYSIS OF SCATS N Hatch et al. of mammal (including bear) tissues and their diet small mammal species exhibited a greater difference (Tieszen et al. 1983, Hilderbrand et al. 1996, Roth and and variability between fecal and diet d13C(23.5%) Hobson 2000, Ayliffe et al. 2004, De Smet et al. 2004), than exhibited by large herbivorous mammals but working with bears can be expensive and (Hwang et al. 2007). As a result the d13C of the dangerous. Therefore, we are interested in exploring feces of these small mammals was not particularly whether the SIA of feces can be used to predict a indicative of the d13C of their diet. The variance of bear’s diet. fecal d15N values appears to be much greater than If SIA of feces can be used to identify diet, it could that of d13C for all species. Foregut fermenters have advantages over the analysis of tissues. It can appear to have more enriched feces relative to their provide a measure of dietary turnover on a short time diet than some (but not all) hindgut fermenters scale (Sponheimer et al. 2003a, Botha and Stock 2005, (Sponheimer et al. 2003b, but see Sare et al. 2005). Codron and Codron 2009). It does not require Thus, despite the drawbacks, for herbivores at mathematical corrections for differences in growth rate least, SIA of feces can be a useful alternative to or attenuation time (Ayliffe et al. 2004). It is noninvasive GFA. For example, SIA of feces has been used to (Codron and Codron 2009); the animal does need to be determine the degree of dietary niche separation or killed or, in most cases, captured or handled. In many overlap (Botha and Stock 2005; Codron et al. 2007a, cases it is easier to find scats and safer to work with scats 2009), the degree to which animals either graze or than to find and work with the animal itself. It may also browse (Botha and Stock 2005; Codron et al. 2005a, provide a shortcut for gross fecal analysis (GFA), which 2005b, 2007a, 2009), and how much C3 and C4 is time- and labor-intensive. components contribute to the diet (Botha and Stock Isotopic analysis of feces has the obvious draw- 2005; Codron et al. 2005b, 2007a, 2009). SIA has back that feces contain the undigested material from also proven useful in determining seasonal changes the diet as well as intestinal slough and gut flora. in diet (Botha and Stock 2005) and changes in the Thus an isotopic analysis of the feces does not diets of frugivorous birds (Podlesak et al. 2005). provide information on what has been assimilated SIA of the feces of carnivores also appears from the diet. This fact is particularly problematic promising. SIA of the feces of brown hyenas (Hyaena where the dietary components vary in digestibility. brunnea) in the Waterberg region of South Africa In such cases easily digestible components are not as suggests that they feed primarily on grazers. Hyena readily detected, while poorly digested components feces also exhibited clear evidence of trophic enrich- have a disproportionately large effect on the isotopic ment compared to herbivores (Codron et al. 2005b). signature (Jones et al. 1979). That said, a number of Where prey differ isotopically, stable isotope analysis controlled feeding studies have demonstrated that of feces can prove useful in determining the relative for herbivores the d13C signature of feces is similar to contribution of different prey to the diet, as has been that of their diet (Steele and Daniel 1978, Jones et al. shown for the insectivorous spotted bat (Euderma 1979, Coates et al. 1991, Garcia et al. 2000, Sare maculatum) (Painter et al. 2009). The feces of et al. 2005, Codron et al. 2007a, Varo and Amat insectivorous birds have also been analyzed to find 2008), is a strong indicator of dietary components evidence of nutrient flow through food webs (Christie (Garcia et al. 2000), and is generally depleted by et al. 2008). Crows (Corvus macrorhynchos and C. .1% relative to diet (Jones et al. 1979, Sponheimer corone), like black bears, are omnivorous and SIA of et al. 2003a, Codron et al. 2005a, Norman et al. their feces has been used to determine nutrient flow 2009, Wittmer et al. 2010, but see Jones et al. 1979). from urban landscapes to forest fragments. Changes Evidence to date suggests that among grazers, diet to a more insectivorous diet were inferred, in part, selection and differential digestibility have little based on SIA of feces, although no attempt was made effect on feces or diet fractionation factors (Wittmer to correct for the differential digestion of plant and et al. 2010). In addition, feces collected in the field animal matter (Fujita and Koike 2007). from a wide variety of taxa closely track even Our objectives were to determine if stable isotope relatively subtle shifts or differences in the d13C signatures of carbon (d13C) and nitrogen (d15N) in dried of their diet (Codron et al. 2005b, 2007a, 2007b; homogenized, archived black bear scats were in Codron and Codron 2009). concordance with predominant diet as previously However, one cannot assume this consistency to categorized by GFA (Bunnell 2000), and if fecal-centric be universal. In a controlled feeding study, several analysis by light isotope ratio mass spectrometry

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Table 1. Components in the stepwise multiple regression model correlating d15N and d13C with dietary components of American black bears from the East Tavaputs Plateau, Utah, USA. Std. Coeff. Model Component Coefficient (slope) SE (normalized slope) F-to-remove d15N intercept 1.806 0.593 1.806 9.286 combined animal matter 3.012 0.943 0.460 10.191 d13C intercept 225.241 0.197 225.241 16,354 volume grass 20.780 0.381 20.316 4.182 volume pine nuts 28.642 5.208 20.256 2.754

(IRMS) could provide an accurate estimate of resource for carbon and nitrogen are reported in per mil (%) use. notation relative to Pee Dee Belemnite (PDB, Craig 1957) and atmospheric nitrogen (Mariotti 1983), respectively. Methods We sought to determine which fecal components We used archived scats from a previous study correlated most strongly with d13C and d15N of the (Bunnell 2000) to determine whether stable isotope feces. Because multiple fecal samples were col- analysis of black bear scats might be useful to lected from some bears, but not others, we used characterize diet. We subsampled (n 5 40) black only the first fecal sample collected from each bear bear scats collected in the East Tavaputs Plateau, in our analysis. We conducted forward stepwise commonly referred to as the ‘‘Book Cliffs’’, during multiple linear regression with the percent volume the spring and summer of 1991–97. The study area of the above 6 categories plus a category combin- was roughly 20.5 miles east to west and 12.5 miles ing vertebrates and ants (referred to as animal north to south, with the corners of the resulting matter) as independent variables and d15N or d13C parallelogram as follows: NE: 39u 359 51.40–109u 39 7.20; as the dependent variable. The d13Coftwo SE: 39u 249 54.00–109u 319 12.00;NW:39u 329 54.20–109u samples were anomalous and outliers. We had 259 44.40; and SW: 39u 219 48.20–109u 269 16.80. We used reason to believe that this was due to a problem the following categories in our GFA classification: with sample preparation and therefore we did not vertebrates (mammal and bird), ants, dicots (i.e. hard include these values in any of the d13C analyses. mast, soft mast, dicotyledonous species), grasses, pine Because simple linear regression showed that the nuts, and debris (indigestible items, e.g. rocks and combined category of vertebrates-and-ants pro- sticks). Quadrant tray categorization was used to duced a significant relationship with d15N, we also determine GFA (Bunnell 2000). included this category in our stepwise multiple We prepared the scats for isotopic analysis by regression. We used 1.3 as the t-to-remove value oven-drying them, then grinding and homogenizing (i.e. the variable remains in the model if P , 0.2 them using a TS 3383-L10 Wiley Mill (Thomas but is removed from the model if P . 0.2; Draper Scientific, Swedesboro, New Jersey, USA). The scats and Smith 1981). The software (StatView 5.0.1; were then stored in sealed plastic bags at room SAS Institute Inc., Cary, North Carolina, USA ) temperature. The dried, homogenized scats were required that these values be converted to F- combusted using an elemental analyzer (Costech, statistics. Therefore F-to-enter was 1.713 and F-to- Valencia, California, USA) coupled to a Delta V remove 1.7. Predictor variables were entered Advantage mass spectrometer (Finnigan, Bremen, sequentially. If their partial F-values exceeded Germany) for analysis of stable isotopes of carbon the F-to-enter, they were included in the model. (d13C) and nitrogen (d15N). All stable isotope ratios However, if upon inclusion of additional variables of the samples are reported as delta values: dsample 5 their F-to-remove was below the above-stated [(Rsample/Rstandard) 21] x 1000, where the dsample is value, the variable was removed from the model. the isotope ratio of the sample relative to the This allowed inclusion of all variables likely to be standard, and Rsample and Rstandard are the fractions predictive, while excluding those that did not add of heavy to light isotopes (13C/12C and 15N/14N) in to the model. Both the slope and the slope based the sample and standard, respectively. Delta values on normalized data are given for components

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of the feces (F 5 10.2; 1, 38 df; P , 0.003), but much of the variance remained unexplained (R2 5 0.21, Fig. 1). Forward stepwise multiple linear regression produced the same result. Animal matter was the only significant contributor to the model (F 5 10.191; 1, 38 df; P 5 0.003, R2 5 0.21; Table 1). We found no significant relationship between d13C and animal matter (F 5 2.213; 1, 36 df; P 5 0.15; Fig. 1). However, forward stepwise multiple linear regression indicated that the percent volume of grass and pine nuts contributed significantly to the d13C value of homogenized feces (F 5 3.476; 2, 35 df; P 5 0.042; R2 5 0.17), but here again, much of the variance remained unexplained. Other variables were considered for the model (Table 1, 2). Histograms of the distribution of fecal d13C and d15N values show a normal and relatively tight distribution (Fig. 2). Overall, grass and animal matter formed the greatest portion of the feces (Fig. 3). However, when considered individually, each fecal sample differed in the percent volume of animal matter, plant matter, and pine nuts (considered separately from plant matter; Fig. 4).

Fig. 1. The percent of the fecal volume that was animal matter was positively related to the mean d15N Discussion of the feces (A, n = 40), but was not predictive of the SIA of feces is most useful when dietary compo- d13C of the feces (B, n = 38) of American black bears from the East Tavaputs Plateau, Utah, USA. nents exhibit relatively large isotopic differences, such as when a major protein source is marine in origin while the rest of the diet is terrestrial included in the model (coefficient and standard- (Darimont and Reimchen 2002), when the diet has ized coefficient respectively, Table 1). both C3 and C4 plant components (Botha and Stock 2005), or when the composition of the diet is relatively simple (e.g. Bryan et al. 2006). Under such Results conditions, fecal SIA can reveal dietary information Although neither percent volume of vertebrate covering a shorter period of time than the SIA of animal matter nor ants alone were significant most tissues (Sponheimer et al. 2003a, Botha and predictors of d15N, when combined, the total volume Stock 2005, Codron and Codron 2009). However, of animal matter was significantly related to d15N when the diet is complex, consisting of many

Table 2. Components excluded from the stepwise multiple regression models correlating d15N and d13C with dietary items of American black bears from the East Tavaputs Plateau, Utah, USA.

d15N d13C Item Partial correlation F-to-enter Partial correlation F-to-enter volume vertebrate 0.060 0.135 20.052 0.929 volume grass 0.195 1.468 volume ants 20.0003 0.000003 0.118 0.480 volume dicots 20.010 0.004 volume pine nuts 0.006 0.001 volume debris 20.177 1.192 0.043 0.063 combined animal matter 0.013 0.006 20.106 0.384

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Fig. 2. Histograms showing the distribution of the d13C (A, n = 38) and d15N (B, n = 40) values of feces collected from black bears on the East Tavaputs Plateau, Utah, USA. different components, and when those dietary feces may prove useful in measuring the contribution components do not exhibit clear isotopic differences, of these components to the diet. This may prove inferences become more difficult. especially true if some of the components are Two important facts stand out regarding SIA of difficult to identify through GFA. bear feces in this study: first, we found significant However, this study also suggests that different relationships between the volume of certain fecal mixes of plants using the same carbon pathway do components and the d13C and d15N of the feces. not have much effect on the d13C values of the feces. Second, these relationships were of low predictive The tight distribution of d13C values of the feces value. At first glance this may suggest that SIA of (Fig. 2) further supports the robustness of SIA of bear feces is not a very promising method for dietary feces for assessing isotopically different categories of analysis. However, (1) the study area was within a food, such as the C3 versus C4 components of a diet. system consisting entirely of C3 plants, (2) the Although animal matter was the only significant isotopic signature of the feces clearly indicated this contributor to the d15N of feces, we did not address (Fig. 2), and (3) there were significant relationships differential digestibility of dietary components. between components of the feces and fecal d15N and Animal matter is much more digestible than plant d13C. This demonstrates the robustness of SIA of matter. As a result, GFA underestimates the amount feces and suggests a certain sensitivity in SIA of of animal matter in the diet of bears by a factor of 2 feces. It is particularly interesting that pine nuts, an (Hewitt and Robbins 1996). It is likely that SIA of uncommon dietary component (Figs. 3, 4), had a fecal d15N would suffer the same problem. The measurable effect on d13C. This suggests that even in contribution of intestinal slough to the d15N of the situations where dietary components differ from or feces is also unknown. The presence of slough in the contribute slightly to fecal d13C, analysis of bear feces may provide some memory effect as an animal

Fig. 3. Contribution of each dietary category as mean percent of volume of the feces of American black bears from the East Tavaputs Plateau, Utah, USA.

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compared to plant matter, as well as the possible effect of intestinal slough on the stable isotope ratios of feces. Because the bears in our study live in a rather isotopically homogenous region dominated by C3 plants, it is not surprising that differences in diets were hard to discern based on SIA of the feces. Despite this, several dietary components were observed to influence the d15N of feces. This suggests that SIA of bear feces might be useful in providing short-term dietary information under circumstances where dietary components differ significantly. For example, SIA of feces might be useful in understanding day-to-day changes in diet where bears have access to salmon (Oncorhynchus spp.) or to human food. Both of these food sources can provide a strong d13C signal that should be evident in the feces. Nevertheless, any fecal analysis is an analysis of the components of the diet not used by the animal, not of the components of the diet assimilated by the animal. Therefore, the degree to which SIA of feces in omnivores and carnivores is representative of the diet as a whole needs to be more fully established. We encourage further studies in this direction.

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