Am. Midl. Nat. 161:243–250
Nutrient Encounter by a Generalist Herbivore in a Heterogeneous Landscape GUY N. CAMERON1 Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221
JERRY J. JOHNSTON Geospatial Information Officer, United States Environmental Protection Agency, 1200 Pennsylvania Avenue NW, Washington, DC 20460 AND
J. C. RANDOLPH School of Public and Environmental Affairs, Indiana University, Bloomington 47405 ABSTRACT.—Most landscapes are heterogeneous in vegetation composition and thus, in the distribution of nutrients required by herbivores for growth and reproduction. Hispid cotton rats (Sigmodon hispdus) inhabit Texas coastal prairies which are characterized by habitat patches dominated by dicots, monocots or both [mixed] plant types. Hispid cotton rats must obtain nutrients necessary for reproduction by ingesting both dicots and monocots, and reproductive females concentrate their activity in mixed patches. Mixed patches may be selected because they have high nutrient contents or because presence of both monocot and dicot food plants lowers cost of foraging movements. Because hispid cotton rats select a nutritionally complete diet and may detect protein by odor and taste cues, we hypothesized that nutrient concentrations may cue position of foraging paths. We used nutrient maps to measure amount of protein, P and Ca encountered during foraging from radiotracked individuals. We compared these values to those obtained from randomly generated foraging paths. Actual and random paths did not differ in amount of protein, P or Ca encountered. Differences in nutient accumulation between seasons were explained by seasonal differences in availability. We conclude that foraging paths do not respond to nutrient content of plants, but that reproductive females likely occupy mixed habitat patches because presence of both dicot and monocot food plants decreases time and energy spent foraging.
INTRODUCTION Understanding the impact of habitat heterogeneity upon natural populations is becomming more important as landscapes are increasingly fragmented (Hutchings et al., 2000; Turner et al., 2001). Resources, as well as habitats, have patchy distributions that may be likened to a cost-benefit surface comprised of patches of different quality (Pastor et al., 1997; Wiens, 2000; Fortin et al., 2002). Foraging paths through heterogeneous landscapes result from an interplay of foraging decisions with energetic and nutritional needs of the animal, dispersion of food plants and impact of abiotic disturbances (Pastor et al., 1997). Foraging paths, in turn, affect how an animal interacts with food, predators and mates (Bowne et al., 1999; McIntyre and Wiens, 1999; Brown, 2000). Some foraging models demonstrate that animals forage to maximize net energy content of foods (Belovsky, 1978, 1984; Pyke, 1984), while others predict that foraging maximizes the rate of gain of some nutrient or minimizes intake of a toxin (Westoby, 1974; Pulliam, 1975; Altmann and Wagner, 1978; Rapport, 1980). Generalist herbivores ingest plants that 1
Corresponding author:
[email protected]
243
244
THE AMERICAN MIDLAND NATURALIST
161(2)
differ markedly in nutrient content, digestibility, palatability and repellent compounds, and they forage to ensure quality of their diet. For example, generalist herbivores may exhibit partial preferences (e.g., mixing or balancing diet items) to obtain requisite nutrients (Breitwisch et al., 1984; Bjorndal, 1991; Willig and Lacher, 1991; Dearing and Schall, 1992). Hence, nutrient requirements affect habitat selection (McNaughton, 1988; Ben-Shahar and Coe, 1992; Grasman and Hellgren, 1993) and variation in nutrient content of food plants may in turn affect diet composition and population parameters of herbivores (Justice and Smith, 1992; Bergeron and Jodoin, 1994). We studied foraging movements of a generalist herbivore, the hispid cotton rat (Sigmodon hispidus), on the coastal prairie of Texas where the habitat is comprised of three types of habitat patches (Kincaid and Cameron, 1985). Monocot patches are dominated by little bluesterm grass (Schizachyrium scoparium) and the shrub sea myrtle (Baccharis halimifolia). Dicot patches are primarily goldenrod (Solidago spp.) and Chinese tallow trees (Sapium sebiferum). Mixed patches contain reduced amounts of these monocots and dicots along with peppervine (Ampelopsis arborea), mist-flower (Eupatorium coelestinum), Chinese privet (Ligustrum sinense), frogfruit (Phyla incisa), southern dewberry (Rubus trivialis), Gulf cordgrass (Spartina spartinae) and bushy beardgrass (Andropogon glomeratus). Sigmodon hispidus consumes both monocot and dicot plants to balance its diet (Kincaid and Cameron, 1985; Randolph et al., 1991); monocots provide carbohydrates and fiber while dicots provide protein, P and Ca necessary for growth and reproduction (Randolph et al., 1995; Cameron and Eshelman, 1996; Schetter et al., 1998; Randolph and Cameron, 2001). In this coastal prairie habitat, reproductive female cotton rats prefer mixed patches and avoid dicot patches (Kincaid and Cameron, 1985; Cameron and Spencer, 2008). Since there is no difference among patch types in overhead cover, preference for mixed patches could reflect a higher concentration of nutrients required for growth and reproduction. Alternatively, mixed patches may lower the cost of foraging because they contain both monocot and dicot food plants thereby reducing distance traveled during foraging. Dicot patches, on the other hand, contain more bare ground than monocot or mixed patches and likely are avoided because lower ground cover could increases predation risk (Cameron and Spencer, 2008). We evaluated the hypothesis that placement of foraging paths enables reproductive hispid cotton rats to encounter areas in the habitat rich in those nutrients necessary for reproduction, particularly in mixed patches. For example, dispersion of a critical limiting nutrient such as protein could cue placement of foraging paths through a heterogeneous landscape particularly during the reproductive season when nutrient availability is most critical. A nutrient cue is plausible because hispid cotton rats are able to select a nutritionally complete diet containing protein (Harriman, 1977) and laboratory rats discern protein by odor and taste (Brot et al., 1987; Heinrichs et al., 1990). We predicted that cotton rats would encounter higher levels of nutrients in their foraging paths compared to randomly placed foraging paths and that this selection of foraging paths would explain the higher occurrence of female hispid cotton rats in mixed habitat patches. An alternative hypothesis was that cost of foraging would be lower in mixed habitat patches because distance moved while foraging would be less since both monocot and dicot diet items occur in mixed patches. METHODS Our study was conducted at the University of Houston Coastal Center, 56 km southeast of Houston, Texas. Animals were collected monthly in a 2-ha field with Sherman live traps set
2009
CAMERON ET AL.: GENERALIST HERBIVORE
245
in a 9 by 10 grid at 15-m intervals during spring (Feb.–May) and autumn (Sept.–Jan.) 1981 and 1982. Live traps were baited with sliced apples, set in the evening and checked in the morning of the next 3 d. Data on body mass, sex and reproductive condition were collected from each captured animal. Traps were closed between trap days and were closed and left in the field between monthly sampling periods. Measurements are reported as mean 6 SE. Radio-transmitters (SM-1; AVM Instruments, Inc., Colfax, California, USA; mass ,4 g) were fitted on animals .85 g in body mass after they were lightly anesthetized with MetofaneH. Only animals in reproductive condition were used (e.g., males with descended testis and females with open vagina, lactating or obviously pregnant). Animals were released at their exact site of capture 30–40 min after the last one was anesthetized. Tracking commenced after animals equilibrated in the field for 24 h. Two null-peak (4-element Yagi) antenna systems mounted on 6-m masts and positioned along one side of the grid were used to triangulate on the signal from each animal. Pilot studies with fixed transmitters demonstrated an accuracy of 2.03 m 6 0.33 m (n 5 17) in this habitat. This error was small relative to average size of habitat patches (monocot 5 1405 6 823 m2; dicot 5 1101 6 932 m2; mixed 5 388 6 126 m2). Fixes were taken every 30 min on each animal during peak activity (2 h before until 2 h after sunset; Cameron et al., 1979) over 2–6 d. Animals were recaptured after tracking, their collars were removed and they were released at their capture site. Animal trapping and handling followed guidelines adopted by the American Society of Mammalogists (Gannon et al., 2007). Data on 28 individuals (13 males, 15 females) for whom we obtained $10 fixes were used for analyses. Data were aggregated by reproductive group (e.g., reproductive males, reproductive non-lactating females, lactating females) and by reproductive season (e.g., spring, Feb.–May; autumn, Sept.–Jan. for hispid cotton rats in coastal prairie). Both seasons had high cotton rat density, but differed in abundance of food plants and nutrient availability (Kincaid and Cameron, 1985; Randolph and Cameron, 2001). Plant biomass differed significantly among all three patch types, with biomass in monocot patches 2 to 3 times higher than in mixed patches during all seasons. Within a patch type, biomass of monocots was similar among seasons while biomass of dicots was more seasonally variable (Randolph and Cameron, 2001). Seasonal availability of food plants and nutrients was taken into account in the nutrient landscapes described below. Two observers recorded type of habitat patch encountered at 1-m intervals along and between adjacent traplines. We constructed paper maps that depicted location and size of each habitat patch and entered these maps into ArcInfoH Geographic Information System (GIS; Environmental Systems Research Institute, Inc., Redlands, California, USA) with a CalCompH Model 23600 large-format digitizer (GTCO CalComp, Columbia, Maryland, USA). We devised a simulation methodology using a combination of self-developed computer programs and ArcInfoH GIS. Four major steps were taken in performing the analyses: (1) creation of nutrient landscapes using field data on distribution and size of types of habitat patches; (2) computation of potential nutrient benefit gained by foraging paths of radiotracked individuals; (3) computation of potential nutrient benefit gathered along randomly placed foraging paths; and (4) comparison of results from actual and random foraging paths in hypothesis testing to determine whether foraging paths encountered similar nutrients, whether nutrients encountered differed seasonally, or whether nutrients encountered differed among reproductive groups. Randolph and Cameron (2001) identified four types of activities from observations and videotapes of cotton rats in enclosures: (1) inactive, apparently sleeping, (2) slow walking or
246
THE AMERICAN MIDLAND NATURALIST
161(2)
foraging (1.94 6 0.09 cm/s, n 5 129 observations) typically examining vegetation, (3) sitting and ingesting food and (4) infrequent rapid running, apparently a fright reaction. Foraging movements were in a relatively straight line, whereas fright elicited non-linear movements. Duration of foraging was 10.5 6 0.5 h/d (n 5 12), with inactivity occupying the remainder of the day. Based upon these results, we assumed that movements documented by telemetry were related to foraging and that foraging paths between fixes was relatively linear. CREATION OF NUTRIENT LANDSCAPES
We used average biomass, energy and nutrients of constituent plants in each patch type during spring and autumn when animals were radiotracked (Randolph and Cameron, 2001). Protein, Ca, and P were selected for our study because these nutrients are potentially limiting to hispid cotton rats (Randolph et al., 1995; Schetter et al., 1998; Randolph and Cameron, 2001). We computed mean density of each nutrient in each habitat patch as: Nj ~
n X
Bi : Cij
i~1
where Nj 5 mean density of each nutrient j (g/m2) Bi 5 mean dry mass density of plant species i (g/m2) Cij 5 concentration of nutrient j in plant species i (mg/g dry mass). COMPUTATION OF POTENTIAL NUTRIENT BENEFITS GAINED IN ACTUAL FORAGING PATHS
Radiotelemetry fixes were entered as points in a GIS coverage and vectors were used to portray actual movements of these individuals. To approximate positions in the field during an entire day, we assumed linear movements between known positions observed at 30 min intervals. The GIS was used to overlay the locomotion pattern of each animal on the nutrient landscapes during each season. Encounter of protein, Ca and P was computed by multiplying area over which an individual rat foraged by density of each nutrient present in each habitat patch encountered. Area foraged was estimated as linear distance traveled by each individual multiplied by the mean body width of adult cotton rats (45 mm; Randolph and Cameron, 2001). Potential nutrient benefits represent nutrients encountered along the foraging path rather than actual nutrient mass gained through foraging which cannot be observed directly. Results were summarized by reproductive status (i.e., reproductive males, reproductive, non-lactating females, lactating females) and season and were expressed as mean 6 95% CI. COMPUTATION OF POTENTIAL BENEFIT GAINED IN RANDOM FORAGING PATHS
A computer program was developed in ANSI C++ to produce random foraging paths over an area with the same proportions as the study field. At each simulated telemetry period, individual rats moved a random distance in one of eight cardinal directions. Both travel distance and direction were selected randomly for each step using a random number generator. Algorithms were included to constrain movements of simulated individuals to borders of the simulation grid. At each randomly generated step, the program checked whether coordinates of new locations were inside the sample grid, and, if they were not, a new random step was computed and tested for whether it was inside the study grid.
2009
CAMERON ET AL.: GENERALIST HERBIVORE
247
To simulate locomotion patterns of actual rats reliably, we measured mean total distance traveled for individuals in each reproductive group in each season. Using these mean travel distances, a random number generator was systematically adjusted until it produced total daily travel distances comparable to those observed for actual individuals in the field. This parameterization resulted in a travel distance of 95.2 6 1.49 m/d for 750 random runs (each representing 1 d of locomotion) which was not significantly different from the actual travel distance of 92.4 6 5.8 m/d for all radiotracked individuals. Subsequent comparison among actual and random foraging paths was slightly biased in favor of random paths because of longer average daily travel distance. Given that our goal was to determine whether actual populations gained more nutrients than would be expected at random, we concluded that this parameterization of the model was appropriate, particularly given high variability in travel distance for actual individuals. The simulation was run 750 times for each demographic group. Mean 6 95% CI was computed for potential nutrient benefits (e.g., Ca, P, protein) by rat reproductive status during both autumn and spring. This effort produced a distribution of expected values for potential nutrient benefits that would be garnered from daily randomly placed foraging paths. To estimate nutrients encountered over multiday periods, we randomly sampled 250 d of data from the set of 750 random d that were produced for random male and female populations. Sampling was designed to produce multiday periods averaging 4 d in length, to maintain consistency with telemetry data from the actual population. Number of days in each simulation ranged from 1 to 6, but results consisting of only 1 d of data were not used. Mean amount 6 95% CI for each nutrient encountered was computed for multiday time intervals. RESULTS AND DISCUSSION There was no significant difference between actual and random foraging paths in amount of Ca, P or protein encountered in autumn or spring (Table 1). Random foraging paths of males and lactating females encountered more Ca during spring than autumn; lactating females also encountered more protein during autumn. Increased encounter of Ca during spring and protein during autumn reflected increased availability of these nutrients in forage plants (Randolph and Cameron, 2001). Detection of seasonal availability of Ca and protein by lactating females may reflect their increased need for these nutrients during lactation (Randolph et al., 1995). Increased encounter of protein by reproductive males during spring, however, likely reflects their movement to patches containing reproductive females rather than reflecting nutrient requirements of males. P also is critical for successful reproduction and its availability also increased during spring (Randolph and Cameron, 2001). However, encounter of P by females did not differ between seasons. We conclude that hispid cotton rats do not use nutrients as a cue to position foraging paths, and that lactating females do not occupy mixed patches because foraging paths enable them to encounter higher concentrations of necessary nutrients than if foraging randomly. Rather than garnering more nutrients along foraging paths, reproductive female hispid cotton rats moved shorter distances in mixed patches (e.g., exhibited area-restricted search) and made more directed, linear forays (Cameron and Spencer, 2008). Hence, we accept our alternative hypothesis. The shorter distances moved in mixed patches are consistent with a patch size smaller than either monocot or dicot patches, and also are shorter than the distance across an average sized home range for hispid cotton rats (620 m2, Spencer et al., 1990). Traveling shorter distances to obtain necessary food plants would be advantageous for lactating females for several reasons. Shorter distances moved would allow
Actual paths rmale n rfemale n lfemale n Random paths rmale n rfemale n lfemale n
Group
35.59 6 3.88 207 22.04 6 3.18 218 22.04 6 3.18 218
18.69 6 14.59 6 23.41 6 5.41 3 16.82 6 6.24 6
Spring
Ca
16.28 6 2.33 205
22.98 6 2.70 206 na
18.49 6 4.57 6
19.62 6 5.70 7 na
Autumn
4.33 6 0.57 210 3.45 6 0.49 211 3.45 6 0.49 211
2.73 6 2.09 6 3.66 6 0.75 3 2.23 6 0.76 6
Spring
P
2.75 6 0.46 201
3.93 6 0.51 220 na
3.07 6 1.03 6
2.95 6 0.80 7 na
Autumn
200.42 6 25.52 200 144.76 6 20.95 208 144.76 6 20.95 208
122.83 6 94.99 6 154.70 6 36.85 3 110.94 6 40.55 6
Spring
Protein
191.07 6 30.4 203
278.59 6 36.38 205 na
227.65 6 54.35 6
248.55 6 77.09 7 na
Autumn
TABLE 1.—Amount of Ca, P and protein (mg, mean 6 95% CI) encountered along actual foraging paths of Sigmodon hispidus and along randomly generated foraging paths; rmale 5 reproductive male, rfemale 5 reproductive female, lfemale 5 lactating female, n 5 sample size; na 5 no reproductive females tracked in autumn
248 THE AMERICAN MIDLAND NATURALIST 161(2)
2009
CAMERON ET AL.: GENERALIST HERBIVORE
249
lactating females to partition less energy into movement and thus, more energy into nourishment for young. Additionally, females spending less time foraging would leave young in nests unattended for a shorter time and would limit exposure of young to risk from abiotic elements and predators. Hence, lowered foraging cost and improved foraging efficiency in mixed patches results from closer proximity of food plants, not nutrient-cued foraging paths, and explains higher occupancy by reproductive females in mixed patch types. A lower cost of foraging also is likely to enhance fitness of female hispid cotton rats. Acknowledgments.—We thank S. Spencer for collaborating in the field studies critical to this research. This study was supported by National Science Foundation grants DEB 79-21766 to JCR and DEB 7921496 to GNC, the University of Houston Coastal Center and the GIS Laboratory, School of Public and Environmental Affairs, Indiana University.
LITERATURE CITED ALTMANN, S. A. AND S. S. WAGNER. 1978. A general model of optimal diet. Rec. Adv. Primatology, 4:407–414. BELOVSKY, G. E. 1978. Diet optimization in a generalist herbivore: the moose. Theor. Pop. Biol., 14:105–134. ———. 1984. Herbivore optimal foraging: a comparative test of three models. Am. Nat., 124:97–115. BEN-SHAHAR, R. AND M. J. COE. 1992. The relationships between soil factors, grass nutrients and the foraging behaviour of wildebeest and zebra. Oecologia, 90:422–428. BERGERON, J.-M. AND L. JODOIN. 1994. Comparison of food habits and of nutrients in the stomach contents of summer- and winter-trapped voles (Microtus pennsylvanicus). Can., J. Zool., 72:183–187. BJORNDAL, K. A. 1991. Diet mixing: nonadditive interactions of diet items in an omnivorous freshwater turtle. Ecology, 72:1234–1241. BOWNE, D. R., J. D. PELES AND G. W. BARRETT. 1999. Effects of landscape spatial structure on movement patterns of the hispid cotton rat (Sigmodon hispidus). Landscape Ecol., 14:53–66. BREITWISCH, R., P. G. MERRITT AND G. H. WHITESIDES. 1984. Why do northern mockingbirds feed fruit to their nestlings? Condor, 86:281–287. BROT, M. D., D. J. BRAGET AND I. L. BERNSTEIN. 1987. Flavor, not postingestive, cues contribute to the salience of proteins as targets in aversion conditioning. Behav. Neuroscience, 101:683–689. BROWN, J. S. 2000. Foraging ecology of animals in response to heterogeneous environments, p. 181–214. In: M. J. Hutchings, E. A. John and A. J. A. Stewart (eds.). The ecological consequences of environmental heterogeneity. Blackwell Science, Ltd., Oxford. CAMERON, G. N. AND B. D. ESHELMAN. 1996. Growth and reproduction of hispid cotton rats (Sigmodon hispidus) in response to naturally occurring levels of dietary protein. J. Mammal., 77:220–231. ——— AND S. R. SPENCER. 2008. Mechanisms of habitat selection by the hispid cotton rat (Sigmodon hispidus). J. Mammal., 89:126–131. DEARING, M. D. AND J. J. SCHALL. 1992. Testing models of optimal diet assembly by the generalist herbivorous lizard Cnemidophorus murinus. Ecology, 73:845–858. FORTIN, D., J. M. FRYXELL AND R. PILOTE. 2002. The temporal scale of foraging decisions in bison. Ecology, 83:970–982. GANNON, W. L., R. S. SIKES AND THE ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2007. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal., 88:809–823. GRASMAN, B. T. AND E. C. HELLGREN. 1993. Phosphorus nutrition in white-tailed deer: nutrient balance, physiological responses, and antler growth. Ecology, 74:2279–2296. HARRIMAN, A. E. 1977. Self-selection of diet by hispid cotton rats (Sigmodon hispidus). Psyh. Reports, 41:343–346. HEINRICHS, S. C., J. A. DEUTSCH AND B. O. MOORE. 1990. Olfactory self-selection of protein-containing foods. Physiol. Behav., 47:409–413. HUTCHINGS, M. J., E. A. JOHN AND A. J. A. STEWART (eds.). 2000. The ecological consequences of environmental heterogeneity. Blackwell Science, Ltd., Oxford.
250
THE AMERICAN MIDLAND NATURALIST
161(2)
JUSTICE, K. E. AND F. A. SMITH. 1992. A model of dietary fiber utilization by small mammal herbivores, with empirical results for Neotoma. Am. Nat., 139:398–416. KINCAID, W. B. AND G. N. CAMERON. 1985. Interactions of cotton rats with a patchy environment: dietary responses and habitat selection. Ecology, 66:1769–1783. MCINTYRE, N. E. AND J. A. WIENS. 1999. Interactions between landscape structure and animal behavior: the roles of heterogeneously distributed resources and food deprivation on movement patterns. Landscape Ecol., 14:437–449. MCNAUGHTON, S. J. 1988. Mineral nutrition and spatial concentrations of African ungulates. Nature, 334:343–345. PASTOR, J., R. MOEN AND Y. COHEN. 1997. Spatial heterogeneities, carrying capacity, and feedbacks in animal-landscape interactions. J. Mammal., 78:1040–1052. PULLIAM, H. R. 1975. Diet optimization with nutrient constraints. Am. Nat., 109:765–768. PYKE, G. H. 1984. Optimal foraging theory: a critical review. Ann. Rev. Ecol. Syst., 15:523–575. RANDOLPH, J. C. AND G. N. CAMERON. 2001. Consequences of diet choice by a small generalist herbivore. Ecol. Monogr., 71:117–136. ———, ——— AND P. MCCLURE. 1995. Nutritional requirements for reproduction in the hispid cotton rat, Sigmodon hispidus. J. Mammal., 76:1113–1126. ———, ——— AND J. A. WRAZEN. 1991. Dietary choice of a generalist grassland herbivore, Sigmodon hispidus. J. Mammal., 72:300–313. RAPPORT, D. J. 1980. Optimal foraging for complementary resources. Am. Nat., 116:324–346. SCHETTER, T., R. J. LOCHMILLER, D. M. LESLIE, JR., D. M. ENGLE AND M. E. PAYTON. 1998. Examination of the nitrogen limitation hypothesis in non-cyclic populations of cotton rats (Sigmodon hispidus). J. Anim. Ecol., 67:705–721. SPENCER, S. R., G. N. CAMERON AND R. K. SWIHART. 1990. Operationally defining home range: temporal dependence exhibited by hispid cotton rats. Ecology, 71:1817–1822. TURNER, M. G., R. H. GARDNER AND R. V. O’NEILL. 2001. Landscape ecology in theory and practice. Pattern and process. Springer-Verlag, New York. WESTOBY, M. 1974. An analysis of diet selection by large generalist herbivores. Am. Nat., 108:290–304. WIENS, J. A. 2000. Ecological heterogeneity: an ontogeny of concepts and approaches, p. 9–31. In: M. J. Hutchings, E. A. John and A. J. A. Stewart (eds.). The ecological consequences of environmental heterogeneity. Blackwell Science Ltd., Oxford. WILLIG, M. R. AND T. E. LACHER, JR. 1991. Food selection of a tropical folivore in relation to leaf-nutrient content. J. Mammal., 72:314–321. SUBMITTED 1 OCTOBER 2007
ACCEPTED 25 AUGUST 2008
