Abstract
Giving-up densities (GUDs) are a frequently used technique that ascertains the value of a forager’s patch use by measuring foraging harvest rate. However, it is not always feasible to measure GUDs due to issues such as non-target species accessing the food items and experimental designs not meeting all of the assumptions of GUDs. Under such circumstances, measuring activity densities can be a valuable alternative approach that can still address many of the same ecological questions as GUDs. Our objective was to design a feeder that enables the accurate measurement of ungulate habitat preference and space use by measuring activity densities and excluding non-target species from data collection. We conducted two experiments to measure the efficacy of our feeder design. The first measured the activity densities of white-tailed deer (Odocoileus virginianus) in three habitat types (forest, old-field, and ecotone). We then used trail cameras to monitor the frequency at which non-target species accessed our modified feeder design compared to a traditional feeding bin used in GUD experiments. We found that our feeders were able to discern habitat preference, and that white-tailed deer preferred to use the old-field habitat over the forest. From the camera-trap experiment, we found that non-target species foraged 173 times from feeding trays and zero times from our feeder design during asynchronous 5-day sampling periods. Additionally, our feeder design can be tailored to other ungulate species and provides a method that can quantify resource use and preference via measuring activity densities, while removing non-target species from data collection.
Significance statement
Giving-up densities (GUDs) are a powerful behavioral indicator of foraging preference. Studies that measure GUDs frequently address the foraging behavior of individuals relative to habitat preference, predation risk, and other costs that can influence the fitness of a forager. However, many studies that measure GUDs deal with the issue of non-target species gaining access to the food source which can alter the results of a study and, in some cases, make results impossible to attain. The feeder design that we use for this experiment is suitable for measuring activity densities in place of GUDs for ungulate species and restricts access to non-target species that could alter the results of an experiment. Our approach provides a method for research that is related to foraging behavior and landscape use, and enables activity densities to be collected in circumstances where GUDs cannot.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data that support this study are made available as supplementary information.
References
Abramsky Z, Pinshow B (1989) Changes in foraging effort in two gerbil species correlate with habitat type and intra- and interspecific activity. Oikos 56:43–53. https://doi.org/10.2307/3566086
Abramsky Z, Rosenzweig ML, Subach A (2002) The costs of apprehensive foraging. Ecology 83:1330–1340. https://doi.org/10.1890/0012-9658(2002)083[1330:TCOAF]2.0.CO;2
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bedoya-Perez MA, Carthey AJR, Mella VSA, McArthur C, Banks PB (2013) A practical guide to avoid giving up on giving-up densities. Behav Ecol Sociobiol 67:1541–1553. https://doi.org/10.1007/s00265-013-1609-3
Bedoya-Pérez MA, Isler I, Banks PB, McArthur C (2014) Roles of the volatile terpene, 1,8-cineole, in plant–herbivore interactions: a foraging odor cue as well as a toxin? Oecologia 174:827–837. https://doi.org/10.1007/s00442-013-2801-x
Bernal-Páez C, Sánchez F (2018) Harvest rates and foraging strategy of Carollia perspicillata (Chiroptera: Phyllostomidae) in an artificial food patch. Behav Process 157:396–401. https://doi.org/10.1016/j.beproc.2018.07.010
Blackwood CB, Smemo KA, Kershner MW, Feinstein LM, Valverde-Barrantes OJ (2013) Decay of ecosystem differences and decoupling of tree community–soil environment relationships at ecotones. Ecol Monogr 83:403–417. https://doi.org/10.1890/12-1513.1
Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47. https://doi.org/10.1007/BF00395696
Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1:49–71
Brown JS, Mitchell WA (1989) Diet selection on depletable resources. Oikos 54:33–43. https://doi.org/10.2307/3565894
Carthey AJR, Banks PB (2015) Foraging in groups affects giving-up densities: solo foragers quit sooner. Oecologia 178:707–713. https://doi.org/10.1007/s00442-015-3274-x
Cunningham CX, Johnson CN, Hollings T, Kreger K, Jones ME (2019) Trophic rewilding establishes a landscape of fear: Tasmanian devil introduction increases risk-sensitive foraging in a key prey species. Ecography 42:2053–2059. https://doi.org/10.1111/ecog.04635
Druce DJ, Brown JS, Kerley GIH, Kotler BP, MacKey RL, Slotow R (2009) Spatial and temporal scaling in habitat utilization by klipspringers (Oreotragus oreotragus) determined using giving-up densities. Austral Ecol 34:577–587. https://doi.org/10.1111/j.1442-9993.2009.01963.x
Embar K, Raveh A, Hoffman I, Kotler BP (2014) Predator facilitation or interference: a game of vipers and owls. Oecologia 174:1301–1309. https://doi.org/10.1007/s00442-013-2760-2
Esparza-Carlos JP, Laundré JW, Hernández L, Íñiguez-Dávalos LI (2016) Apprehension affecting foraging patterns and landscape use of mule deer in arid environments. Mamm Biol 81:543–550. https://doi.org/10.1016/j.mambio.2016.07.006
Gawlik DE (2002) The effects of prey availability on the numerical response of wading birds. Ecol Monogr 72:329–346. https://doi.org/10.1890/00129615(2002)072[0329:TEOPAO]2.0.CO;2
Goetsch C, Wigg J, Royo AA, Ristau T, Carson WP (2011) Chronic over browsing and biodiversity collapse in a forest understory in Pennsylvania: results from a 60 year-old deer exclusion plot. J Torrey Bot Soc 138:220–224. https://doi.org/10.3159/TORREY-D-11-00013.1
Hope ACA (1968) A simplified Monte Carlo significance test procedure. J Roy Stat Soc B Met 30:582–598. https://doi.org/10.1111/j.2517-6161.1968.tb00759.x
Hubbard T, Cove MV, Green AM, Iannarilli F, Allen ML, LaRose SH, Nagy C, Compton JA, Lafferty DJR (2022) Human presence drives bobcat interactions among the U.S. carnivore guild. Biodivers Conserv 31:2607262418. https://doi.org/10.1007/s10531-022-02445-2
Kotler BP, Brown JS (1990) Harvest rates of two species of gerbilline rodents. J Mammal 71:591–596. https://doi.org/10.2307/1381798
Kotler BP, Brown JS (1999) Mechanisms of coexistence of optimal foragers as determinants of local abundances and distributions of desert granivores. J Mammal 80:361–374. https://doi.org/10.2307/1383285
Kotler BP, Gross JE, Mitchell WA (1994) Applying patch use to assess aspects of foraging behavior in Nubian ibex. J Wildlife Manage 58:299–307. https://doi.org/10.2307/3809395
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Lenth RV (2021) emmeans: estimated marginal means, aka least-squares means. R package version 1.6.2–1, https://CRAN.R-project.org/package=emmeans. Accessed 12 Aug 2022
Makin D, Chamaillé-Jammes S, Shrader AM (2018) Changes in feeding behavior and patch use by herbivores in response to the introduction of a new predator. J Mammal 99:341–350. https://doi.org/10.1093/jmammal/gyx177
Mella VSA, Banks PB, McArthur C (2014) Negotiating multiple cues of predation risk in a landscape of fear: what scares free-ranging brushtail possums? J Zool 294:22–30. https://doi.org/10.1111/jzo.12146
Mitchell WA, Abramsky Z, Kotler BP, Pinshow B, Brown JS (1990) The effect of competition on foraging activity in desert rodents: theory and experiments. Ecology 71:844–854. https://doi.org/10.2307/1937356
Newman J (2018) Contemporary debates on opportunity cost theory and pedagogy. In: McCaffrey M (ed) The Economic Theory of Costs: Foundations and New Directions. Routledge, Abingdon, pp 11–26
Olsson O, Holmgren NMA (1999) Gaining ecological information about Bayesian foragers through their behaviour. I Models with predictions. Oikos 87:251–263. https://doi.org/10.2307/3546740
Olsson O, Molokwu MG (2007) On the missed opportunity cost, GUD, and estimating environmental quality. Isr J Ecol Evol 53:263–278. https://doi.org/10.1560/IJEE.53.3.263
Ovadia O, Abramsky Z (1995) Density-dependent habitat selection: evaluation of the isodar method. Oikos 73:86–94. https://doi.org/10.2307/3545729
Perrin MR, Kotler BP (2005) A test of five mechanisms of species coexistence between rodents in a southern African savanna. Afr Zool 40:55–61. https://doi.org/10.1080/15627020.2005.11407309
Pickett KN, Hik DS, Newsome AE, Pech RP (2005) The influence of predation risk on foraging behaviour of brushtail possums in Australian woodlands. Wildlife Res 32:121–130. https://doi.org/10.1071/WR03098
Pocock MJO, Bell SC (2011) Hair tubes for estimating site occupancy and activity-density of Sorex minutus. Mamm Biol 76:445–450. https://doi.org/10.1016/j.mambio.2011.02.002
R Core Team (2020) R: a language and environment for statistical computing, version 4.0.2. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/. Accessed 12 Aug 2022
Rieucau G, Vickery WL, Doucet GJ (2009) A patch use model to separate effects of foraging costs on giving-up densities: an experiment with white-tailed deer (Odocoileus virginianus). Behav Ecol Sociobiol 63:891–897. https://doi.org/10.1007/s00265-009-0732-7
Rooney TP, Waller DM (2003) Direct and indirect effects of white-tailed deer in forest ecosystems. Forest Ecol Manag 181:165–176. https://doi.org/10.1016/S0378-1127(03)00130-0
Russell RR, Wilkinson M (1979) Microeconomics: a synthesis of modern and neoclassical theory. Wiley, New York
Sánchez F (2006) Harvest rates and patch-use strategy of Egyptian fruit bats in artificial food patches. J Mammal 87:1140–1144. https://doi.org/10.1644/05-MAMM-A-415R2.1
Schmidt KA, Schauber EM (2007) Behavioral indicators of predator space use: studying species interactions through the behavior of predators. Isr J Ecol Evol 53:389–406. https://doi.org/10.1560/IJEE.53.3.389
Stears K, Shrader AM (2015) Increases in food availability can tempt oribi antelope into taking greater risks at both large and small spatial scales. Anim Behav 108:155–164. https://doi.org/10.1016/j.anbehav.2015.07.012
Tadesse SA, Kotler BP (2010) Habitat choices of Nubian ibex (Capra nubiana) evaluated with a habitat suitability modeling and isodar analysis. Isr J Ecol Evol 56:55–74. https://doi.org/10.1560/IJEE.56.1.55
Tadesse SA, Kotler BP (2013) Habitat use by mountain nyala Tragelaphus buxtoni determined using stem bite diameters at point of browse, bite rates, and time budgets in the Bale Mountains National Park, Ethiopia. Curr Zool 59:707–717. https://doi.org/10.1093/czoolo/59.6.707
Wheeler HC, Hik DS (2014) Giving-up densities and foraging behaviour indicate possible effects of shrub encroachment on arctic ground squirrels. Anim Behav 95:1–8. https://doi.org/10.1016/j.anbehav.2014.06.005
Ziv Y, Abramsky Z, Kotler BP, Subach A (1993) Interference competition and temporal and habitat partitioning in two gerbil species. Oikos 66:237–246. https://doi.org/10.2307/3544810
Ziv Y, Kotler BP (2003) Giving-up densities of foraging gerbils: the effect of interspecific competition on patch use. Evol Ecol 17:333–347. https://doi.org/10.1023/A:1027385100393
Acknowledgements
We thank our reviewers and the editor for their constructive comments through the revision process of this manuscript. We thank M. Kershner for granting us access to the trail cameras that we used in this experiment. We thank C. Combs for coordinating the acquisition of materials and assisting in collecting data. We are grateful for the insights on GUDs provided by Dr. Burt Kotler, Blaustein Institutes for Desert Research, Sede Boqer, Israel. We also extend our gratitude to A. Eagar and T. Michael for their helpful comments on early drafts of this manuscript. Last, we thank A. Wuensch for assistance in feeder design and construction, as well as in creating figures.
Funding
Funding was provided by the Herrick Trust, Kent State University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
A formal, ethical review of this experiment was not required because camera trapping and measuring activity densities are non-invasive techniques. The use of animals adhered to the guidelines set forth by the Animal Behavior Society/Association for the Study of Animal Behavior.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by C. Soulsbury
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wuensch, M.A., Pratt, A.M. & Ward, D. Using activity densities as an alternative approach to measuring ungulate giving-up densities in the presence of non-target species. Behav Ecol Sociobiol 77, 9 (2023). https://doi.org/10.1007/s00265-022-03283-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-022-03283-6