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Large carnivore foraging contributes to heterogeneity in nutrient cycling

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Abstract

Context

Carnivores influence the spatial heterogeneity of biogeochemical processes in ecological communities through predation and the deposition of animal carcasses, and these processes may lead to positive feedback loops that influence large-scale patterns of nutrient cycling.

Objectives

We assessed whether ambush predator foraging impacted soil chemistry and plant forage quality, and then scaled these effects to the landscape to assess whether carnivores contribute to heterogeneity in resource distributions.

Methods

We measured total nitrogen (N) and N stable isotope composition (δ15N) of soils and plants at 172 ungulate carcasses killed by mountain lions in the Yellowstone Ecosystem, USA. We measured kill rates and estimated the probability of a mountain lion foraging in any location to scale their carrion contributions to the landscape.

Results

Carcasses altered total nitrogen N and δ15N of soils and plants, and changes in δ15N suggested that plants absorbed significant N from carcasses. On average, plant δ15N at kill sites increased by 2.3 milles (‰), which is large compared to the 6.3 ‰ range of variation in local plants across xeric and mesic systems. We conservatively estimated that resident mountain lions in our study area annually contributed the carrion mass of a blue whale, or 44.1 kg of carrion and 1.4 kg of N per km2. We also determined that mountain lion foraging was concentrated in just 4% of our study system.

Conclusions

Ambush carnivore foraging may contribute to landscape-scale heterogeneity in nutrient distributions, and set the stage for positive feedback loops between carnivores and prey that drive biogeochemical processes.

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Data availability

The data are archived in the following archive: https://figshare.com/s/eb800917542576038c1d.

References

  • Allen ML, Elbroch LM, Wilmers CC, Wittmer HU (2015) The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am Nat 185:822–833

    Article  PubMed  Google Scholar 

  • Augustine DJ, McNaughton SJ, Frank DA (2003) Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem. Ecol Appl 13:1325–1337

    Article  Google Scholar 

  • Barry JM, Elbroch LM, Aiello-Lammens ME, Sarno RJ, Seelye L, Kusler A, Quigley HB, Grigione MM (2019) Pumas as ecosystem engineers: ungulate carcasses support beetle assemblages in the Greater Yellowstone Ecosystem. Oecologia 189:577–586

    Article  PubMed  Google Scholar 

  • Barton PS, Bump JK (2019) Carcass decomposition. In: Olea PP, Mateo-Tomás P, Sánchez-Zapata JA (eds) Carcass ecology and management. Springer, Cham., pp 101–124

    Google Scholar 

  • Barton PS, Cunningham SA, Lindenmayer DB, Manning AD (2013) The role of carcass in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171:761–772

    Article  PubMed  Google Scholar 

  • Barton PS, Evans MJ, Foster CN, Pechal JL, Bump JK, Quaggiotto MM, Benbow ME (2019) Towards quantifying carcass biomass in ecosystems. Trends Ecol Evol 34(10):950–961

    Article  PubMed  Google Scholar 

  • Benninger LA, Carter DO, Forbes SL (2008) The biochemical alteration of soil beneath a decomposing carcass. Forensic Sci Int 180:70–75

    Article  CAS  PubMed  Google Scholar 

  • Boyce MS, Vernier PR, Nielsen SE, Schmiegelow FK (2002) Evaluating resource selection functions. Ecol Model 157:281–300

  • Brenna JT, Corso TN, Tobias HJ, Caimi RJ (1997) High-precision continuous-flow isotope ratio mass spectrometry. Mass Spectrometry Rev 16:227–258

    Article  CAS  Google Scholar 

  • Brodie JF, Redford KH, Doak DF (2018) Ecological function analysis: incorporating species roles into conservation. Trends Ecol Evol 33:840–850

    Article  PubMed  Google Scholar 

  • Bump JK, Peterson RO, Vucetich JA (2009a) Wolves modulate soil nutrient heterogeneity and foliar nitrogen by configuring the distribution of ungulate carcasses. Ecology 90:3159–3167

    Article  PubMed  Google Scholar 

  • Bump JK, Webster CR, Vucetich JA, Peterson RO, Shields JM, Powers MD (2009b) Ungulate carcasses perforate ecological filters and create biogeochemical hotspots in forest herbaceous layers allowing trees a competitive advantage. Ecosystems 12:996–1007

    Article  Google Scholar 

  • Buxton DR, Marten GC (1989) Forage quality of plant parts of perennial grasses and relationship to phenology. Crop Sci 29:429–435

    Article  Google Scholar 

  • Cook RC, Shipley LA, Cook JG, Camp MJ, Monzingo DS, Robatcek SL, Berry SL, Hull IT, Myers WL, Denryter KA, Long RA (2022) Sequential detergent fiber assay results used for nutritional ecology research: Evidence of bias since 2012. Wildlife Society Bulletin 46(4):e1348

  • Cristescu B, Bose S, Elbroch LM, Allen ML, Wittmer HU (2019) Habitat selection when killing primary versus alternative prey species supports prey specialization in an apex predator. J Zool 309:259–268

    Article  Google Scholar 

  • Danell K, Berteaux D, Bråthen KA (2002) Effect of muskox carcasses on nitrogen concentration in tundra vegetation. Arctic 55:389–392

    Article  Google Scholar 

  • Day TA, Detling JK (1990) Grassland patch dynamics and herbivore grazing preference following urine deposition. Ecology 71:180–188

    Article  Google Scholar 

  • DeVault TL, Rhodes OE Jr, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234

    Article  Google Scholar 

  • Dostaler S, Ouellet JP, Therrien JF, Côté SD (2011) Are feeding preferences of white-tailed deer related to plant constituents? J Wildl Manage 75:913–918

    Article  Google Scholar 

  • Elbroch LM, Allen ML, Lowrey BH, Wittmer HU (2014) The difference between killing and eating: Ecological shortcomings of puma energetic models. Ecosphere 5:1–16

    Article  Google Scholar 

  • Elbroch LM, O’Malley C, Peziol M, Quigley HB (2017) Vertebrate diversity benefiting from carcass provided by pumas and other subordinate, apex felids. Biol Conserv 215:123–131

    Article  Google Scholar 

  • Elbroch LM, Marescot L, Quigley H, Craighead D, Wittmer HU (2018) Multiple anthropogenic interventions drive puma survival following wolf recovery in the Greater Yellowstone Ecosystem. Ecol Evol 8:7236–7245

    Article  PubMed  PubMed Central  Google Scholar 

  • Evans RD (2007) Soil Nitrogen isotopic composition. Stable Isotopes Ecol Environ Sci 2:83–98

    Article  Google Scholar 

  • Frank DA, Evans RD (1997) Effects of Native Grazers on Grassland N Cycling in Yellowstone National Park. Ecology 78:2238–2248

  • Goering HK, Van Soest PJ (1970) Forage fiber analyses (apparatus, reagents, prcedures, and some applications). USDA Agr Handb

  • Griffin JM, Turner MG, Simard M (2011) Nitrogen cycling following mountain pine beetle disturbance in lodgepole pine forests of Greater Yellowstone. For Ecol Manag 261:1077–1089

    Article  Google Scholar 

  • Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36

  • Hanley TA, Robbins CT, Hagerman AE, McArthur C (1992) Predicting digestible protein and digestible dry matter in tannin-containing forages consumed by ruminants. Ecology 73:537–541

    Article  CAS  Google Scholar 

  • Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556–562

    Article  PubMed  Google Scholar 

  • Hilderbrand GV, Hanley TA, Robbins CT, Schwartz CC (1999) Role of brown bears in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121:546–550

    Article  CAS  PubMed  Google Scholar 

  • Holmes BR, Laundré JW (2006) Use of open, edge and forest areas by pumas Puma concolor in winter: are pumas foraging optimally? Wildl Biol 12:201–209

    Article  Google Scholar 

  • Keenan SW, Schaeffer SM, Jin VL, DeBruyn JM (2018) Mortality hotspots: nitrogen cycling in forest soils during vertebrate decomposition. Soil Biol Biochem 121:165–176

    Article  CAS  Google Scholar 

  • Knopff KH, Knopff AA, Kortello A, Boyce MS (2010) Cougar kill rate and prey composition in a multiprey system. J Wildl Manage 74:1435–1447

    Article  Google Scholar 

  • Leghari SJ, Wahocho NA, Laghari GM, HafeezLaghari A, MustafaBhabhan G, HussainTalpur K et al (2016) Role of nitrogen for plant growth and development: A review. Adv Environ Biol 10:209–219

    Google Scholar 

  • Lendrum PE, Elbroch LM, Quigley H, Thompson DL, Jimenez M, Craighead D (2014) Home Range characteristics of a subordinate predator; selection for refugia or hunt opportunity? J Zool 294:58–66

  • Manly BFL, McDonald L, Thomas DL, McDonald TL, Erickson WP (2007) Resource selection by animals: Statistical design and analysis for field studies. Springer Science & Business Media, Dordrecht

  • McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM et al (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312

    Article  CAS  Google Scholar 

  • Melis C, Selva N, Teurlings I, Skarpe C, Linnell JD, Andersen R (2007) Soil and vegetation nutrient response to bison carcasses in Białowieża Primeval Forest, Poland. Ecol Res 22:807–813

    Article  CAS  Google Scholar 

  • Monk JD, Schmitz OJ (2022) Landscapes shaped from the top down: predicting cascading predator effects on spatial biogeochemistry. Oikos 2022:e08554

    Article  Google Scholar 

  • Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48

    Article  PubMed  Google Scholar 

  • Oro D, Genovart M, Tavecchia G, Fowler MS, Martínez-Abraín A (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514

    Article  PubMed  Google Scholar 

  • Parmenter RR, MacMahon JA (2009) Carcass decomposition and nutrient cycling in a semiarid shrub–steppe ecosystem. Ecol Monogr 79:637–661

    Article  Google Scholar 

  • Pojar TM, Bowden DC (2004) Neonatal mule deer fawn survival in west-central Colorado. J Wildl Manage 68:550–560

    Article  Google Scholar 

  • Qi XM, Zhang LD, Du XL, Song ZJ, Zhang Y, Xu SY (2003) Quantitative analysis using NIR by building PLS-BP model. Spectrosc Spectral Anal 23:870–872

    CAS  Google Scholar 

  • Robbins C (2012) Wildlife feeding and nutrition. Elsevier

    Google Scholar 

  • Robbins CT, Moen AN, Reid JT (1974) Body composition of white-tailed deer. J Anim Sci 38:871–876

    Article  CAS  PubMed  Google Scholar 

  • Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107

    Article  CAS  Google Scholar 

  • Robbins CT, Spalinger DE, van Hoven W (1995) Adaptation of ruminants to browse and grass diets: are anatomical-based browser-grazer interpretations valid? Oecologia 103:208–213

    Article  PubMed  Google Scholar 

  • Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162

    Article  CAS  PubMed  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Sebastián-González E, Morales-Reyes Z, Botella F, Naves-Alegre L, Pérez-García JM et al (2020) Network structure of vertebrate scavenger assemblages at the global scale: drivers and ecosystem functioning implications. Ecography 43:1143–1155

    Article  Google Scholar 

  • Schmitz OJ, Hawlena D, Trussell GC (2010) Predator control of ecosystem nutrient dynamics. Ecol Lett 13:1199–1209

  • Seidensticker JC, Hornocker MG, Wiles WV, Messick JP (1973) Mountain lion social organization in the Idaho Primitive Area. Wildl Monogr 35:3–60

    Google Scholar 

  • Smith JA, Donadio E, Bidder OR, Pauli JN, Sheriff MJ, Perrig PL, Middleton AD (2020) Where and when to hunt? Decomposing predation success of an ambush carnivore. Ecology 101:e03172

    Article  PubMed  Google Scholar 

  • Towne EG (2000) Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122:232–239

    Article  CAS  PubMed  Google Scholar 

  • Wikenros C, Sand H, Ahlqvist P, Liberg O (2013) Biomass flow and scavengers use of carcasses after re-colonization of an apex predator. PLoS ONE 8:e77373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilmers CC, Stahler DR, Crabtree RL, Smith DW, Getz WM (2003) Resource dispersion and consumer dominance: scavenging at wolf-and hunter-killed carcasses in Greater Yellowstone, USA. Ecol Lett 6:996–1003

    Article  Google Scholar 

  • Wilmshurst JF, Fryxell JM (1995) Patch selection by red deer in relation to energy and protein intake: a re-evaluation of Langvatn and Hanley’s (1993) results. Oecologia 104:297–300

    Article  PubMed  Google Scholar 

  • Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carcass structure communities. Trends Ecol Evol 26:129–135

    Article  PubMed  Google Scholar 

  • Yang LH (2004) Periodical cicadas as resource pluses in North American forests. Science 306:1565–1567

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the numerous field technicians and private individuals who contributed to this work. Research was supported by the Summerlee Foundation, Kaplan Graduate Award, Gerry and Meriam Scully, the National Geographic Society (grant no. C236–13), the Community Foundation of Jackson Hole and the Harold Nyberg Endowed Scholarship and in part by the USDA National Institute of Food and Agriculture, McIntire-Stennis Project 1018967.

Funding

Summerlee Foundation, National Geographic Society, C236–13.

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Authors and Affiliations

  1. School of Environment, Washington State University, 642812, Pullman, WA, 99164‐2812, USA

    Michelle Peziol, Lisa A. Shipley & Daniel H. Thornton

  2. Panthera, 8 West 40Th Street, New York, NY, 10018, USA

    Michelle Peziol & L. Mark Elbroch

  3. School of Biological Sciences and WSU Stable Isotope Core Facility, Washington State University, 644236, Pullman, WA, 99164-4236, USA

    R. Dave Evans

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  1. Michelle Peziol
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Contributions

MP and LME conceptualized the project and conducted the fieldwork. LME funded and managed the field project. LAS and RDE provided lab resources, mentoring in lab methods and interpreting results. DHT was primary responsible for graduate student support and guidance, including internal funding. MP, LME and DHT drafted the manuscript and all authors provied feedback and approved the final version.

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Correspondence to L. Mark Elbroch.

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Peziol, M., Elbroch, L.M., Shipley, L.A. et al. Large carnivore foraging contributes to heterogeneity in nutrient cycling. Landsc Ecol 38, 1497–1509 (2023). https://doi.org/10.1007/s10980-023-01630-0

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