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Large mammals generate both top-down effects and extended trophic cascades on floral-visitor assemblages

Published online by Cambridge University Press:  11 June 2019

Allison Louthan ,
Emily Valencia ,
Dino J. Martins ,
Travis Guy ,
Jacob Goheen ,
Todd Palmer  and
Daniel Doak
Allison Louthan*
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Department of Biology, Duke University, Durham, NC 27708, USA Environmental Studies Program, University of Colorado, Boulder, CO 80309, USA
Emily Valencia
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Environmental Studies Program, University of Colorado, Boulder, CO 80309, USA
Dino J. Martins
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya
Travis Guy
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Department of Biology, University of Florida, Gainesville, FL 32611, USA
Jacob Goheen
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Department of Zoology & Physiology, University of Wyoming, Laramie, WY 82071, USA
Todd Palmer
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Department of Biology, University of Florida, Gainesville, FL 32611, USA
Daniel Doak
Affiliation:
Mpala Research Centre, P.O. Box 555, Nanyuki, Kenya Environmental Studies Program, University of Colorado, Boulder, CO 80309, USA
*
*Email: allisonmlouthan@gmail.com
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Abstract

Cascading effects of high trophic levels onto lower trophic levels have been documented in many ecosystems. Some studies also show evidence of extended trophic cascades, in which guilds dependent on lower trophic levels, but uninvolved in the trophic cascade themselves, are affected by the trophic cascade due to their dependence on lower trophic levels. Top-down effects of large mammals on plants could lead to a variety of extended trophic cascades on the many guilds dependent on plants, such as pollinators. In this study, floral-visitor and floral abundances and assemblages were quantified within a series of 1-ha manipulations of large-mammalian herbivore density in an African savanna. Top-down effects of large mammals on the composition of flowers available for floral visitors are first shown, using regressions of herbivore activity on metrics of floral and floral-visitor assemblages. An extended trophic cascade is also shown: the floral assemblage further altered the assemblage of floral visitors, according to a variety of approaches, including a structural equation modelling approach (model with an extended trophic cascade was supported over a model without, AICc weight = 0.984). Our study provides support for extended trophic cascades affecting floral visitors, suggesting that trophic cascades can have impacts throughout entire communities.

Keywords

Extended trophic cascadefloral visitorflowerslarge mammalspollinatorstrophic cascadetop-down effectstrophic ricochet
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 4 , July 2019 , pp. 185 - 198
Copyright
© Cambridge University Press 2019 

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References

Literature cited

Augustine, DJ and McNaughton, SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. Journal of Wildlife Management 62, 1165–1183.10.2307/3801981CrossRefGoogle Scholar
Baines, D, Sage, RB and Baines, MM (1994) The implications of red deer grazing to ground vegetation and invertebrate communities of Scottish native pinewoods. Journal of Applied Ecology 31, 776–783.10.2307/2404167CrossRefGoogle Scholar
Biesmeijer, JC, Roberts, SPM, Reemer, M, Ohlemüller, R, Edwards, M, Peeters, T, Schaffers, AP, Potts, SG, Kleukers, R, Thomas, CD, Settele, J and Kunin, WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354.10.1126/science.1127863CrossRefGoogle ScholarPubMed
Byrnes, JE, Reed, DC, Cardinale, BJ, Cavanaugh, KC, Holbrooks, SJ and Schmitts, RJ (2011) Climate-driven increases in storm frequency simplify kelp forest food webs. Global Change Biology 17, 2513–2524.10.1111/j.1365-2486.2011.02409.xCrossRefGoogle Scholar
Carvell, C (2002) Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes . Biological Conservation 103, 33–49.10.1016/S0006-3207(01)00114-8CrossRefGoogle Scholar
Côté, SD, Rooney, TP, Tremblay, JP, Dussault, C and Waller, DM (2004) Ecological impacts of deer overabundance. Annual Review of Ecology, Evolution, and Systematics 35, 113–147.10.1146/annurev.ecolsys.35.021103.105725CrossRefGoogle Scholar
Diaz, S, Lavorel, S, Mcintyre, S, Falczuk, V, Casanoves, F, Milchunas, DG, Skarpe, C, Rusch, G, Sternberg, M, Noy-Meir, I, Landsberg, J, Zhang, W, Clark, H and Campbell, BD (2007) Plant trait responses to grazing– a global synthesis. Global Change Biology 13, 313–341.10.1111/j.1365-2486.2006.01288.xCrossRefGoogle Scholar
Donihue, CM, Porensky, L, Foufopoulos, J, Riginos, C and Pringle, RM (2013) Glade cascades: indirect legacy effects of pastoralism enhance the abundance and spatial structuring of arboreal fauna. Ecology 94, 827–837.10.1890/12-0856.1CrossRefGoogle Scholar
Estes, JA, Tinker, MT, Williams, TM and Doak, DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476.10.1126/science.282.5388.473CrossRefGoogle ScholarPubMed
Estes, JA, Peterson, CH and Steneck, R (2010) Some effects of apex predators in higher-latitude coastal oceans. In Terborgh, J and Estes, JA (eds), Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Washington, DC: Island Press, pp. 37–54.Google Scholar
Fahimipour, AK, Anderson, KE and Williams, RJ (2017) Compensation masks trophic cascades in complex food webs. Theoretical Ecology 10, 245–253.10.1007/s12080-016-0326-8CrossRefGoogle Scholar
Ford, AT and Goheen, JR (2015) Trophic cascades by large carnivores: a case for strong inference and mechanism. Trends in Ecology and Evolution 30, 725–735.10.1016/j.tree.2015.09.012CrossRefGoogle ScholarPubMed
Ford, AT, Goheen, JR, Otieno, TO, Bidner, L, Isbell, LA, Palmer, TM, Ward, D, Woodroffe, R and Pringle, RM (2014) Large carnivores make savanna tree communities less thorny. Science 346, 346–349.10.1126/science.1252753CrossRefGoogle ScholarPubMed
Goheen, JR, Young, TP, Keesing, F and Palmer, TM (2007) Consequences of herbivory by native ungulates for the reproduction of a savanna tree. Journal of Ecology 95, 129–138.10.1111/j.1365-2745.2006.01196.xCrossRefGoogle Scholar
Goheen, JR, Palmer, TM, Charles, GK, Helgen, KM, Kinyua, SN, Maclean, JE, Turner, BL, Young, HS and Pringle, RM (2013) Piecewise disassembly of a large-herbivore community across a rainfall gradient: the UHURU experiment. PLoS ONE 8, e55192.10.1371/journal.pone.0055192CrossRefGoogle ScholarPubMed
Goheen, JR, Augustine, DJ, Veblen, KE, Kimuyu, DM, Palmer, TM, Porensky, LM, Pringle, RM, Ratnam, J, Riginos, C, Sankaran, M, Ford, AT, Hassan, AA, Jakopak, R, Kartzinel, TR, Kurukura, S, Louthan, AM, Odadi, WO, Otieno, TO, Wambua, AM, Young, HS and Young, TP (2018) Conservation lessons from large-mammal manipulations in East African savannas: the KLEE, UHURU, and GLADE experiments. Annals of the New York Academy of Sciences 1429, 31–49.10.1111/nyas.13848CrossRefGoogle ScholarPubMed
Goulson, D, Nicholls, E, Botías, C and Rotheray, EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.10.1126/science.1255957CrossRefGoogle ScholarPubMed
Holdo, RM, Sinclair, ARE, Dobson, AP, Metzger, KL, Bolker, BM, Ritchie, ME and Holt, RD (2009) A disease-mediated trophic cascade in the Serengeti and its implications for ecosystem C. PLoS Biology 7, e1000210.10.1371/journal.pbio.1000210CrossRefGoogle ScholarPubMed
Jacobs, SM and Naiman, RJ (2008) Large African herbivores decrease herbaceous plant biomass while increasing plant species richness in a semi-arid savanna toposequence. Journal of Arid Environments 72, 91–903.10.1016/j.jaridenv.2007.11.015CrossRefGoogle Scholar
Kaiser-Bunbury, CN, Vásquez, DP, Stang, M and Ghazoul, J (2014) Determinants of the microstructure of plant-pollinator networks. Ecology 95, 3314–3324.10.1890/14-0024.1CrossRefGoogle Scholar
Koptur, S, Smith, CL and Lawton, JH (1996) Effects of artificial defoliation on reproductive allocation in the common vetch, Vicia sativa (Fabaceae: Papilionoideae). American Journal of Botany 83, 886–889.10.1002/j.1537-2197.1996.tb12780.xCrossRefGoogle Scholar
Louthan, AM, Doak, DF, Goheen, JR, Palmer, TM and Pringle, RM (2014) Mechanisms of plant-plant interactions: concealment from herbivores is more important than abiotic-stress mediation in an African savannah. Proceedings of the Royal Society B 281, 20132647.10.1098/rspb.2013.2647CrossRefGoogle Scholar
Louthan, AM,Pringle, RM, Goheen, JR, Palmer, TM, Morris, WF and Doak, DF (2018) Aridity weakens population-level effects of multiple species interactions on Hibiscus meyeri. Proceedings of the National Academy of Sciences USA 115, 543–548.10.1073/pnas.1708436115CrossRefGoogle ScholarPubMed
Martins, DJ (2004) Foraging patterns of managed honeybees and wild bee species in an arid African environment: ecology, biodiversity and competition. International Journal of Tropical Insect Science 24, 105–115.10.1079/IJT200411CrossRefGoogle Scholar
Martins, DJ and Johnson, SD (2013) Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context. Biological Journal of the Linnean Society 110, 199–213.10.1111/bij.12107CrossRefGoogle Scholar
Mayer, C (2004) Pollination services under different grazing intensities. International Journal of Tropical Insect Science 24, 95–103.10.1079/IJT20047CrossRefGoogle Scholar
McCauley, DJ, Keesing, F, Young, TP, Allan, BF and Pringle, RM (2006) Indirect effects of large herbivores on snakes in an African savanna. Ecology 87, 2657–2663.10.1890/0012-9658(2006)87[2657:IEOLHO]2.0.CO;2CrossRefGoogle Scholar
McCauley, DJ, Keesing, F, Young, TP and Dittmar, K (2008) Effects of the removal of large herbivores on fleas of small mammals. Journal of Vector Ecology 33, 263–268.10.3376/1081-1710-33.2.263CrossRefGoogle ScholarPubMed
Memmott, J, Craze, PG, Waser, NM and Price, MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecology Letters 10, 710–717.10.1111/j.1461-0248.2007.01061.xCrossRefGoogle ScholarPubMed
Moeller, DA (2005) Pollinator community structure and sources of spatial variation in plant–pollinator interactions in Clarkia xantiana ssp. Xantiana. Oecologia 142, 28–37.10.1007/s00442-004-1693-1CrossRefGoogle ScholarPubMed
Morris, T and Letnic, M (2016) Removal of an apex predator initiates a trophic cascade that extends from herbivores to vegetation and the soil nutrient pool. Proceedings of the Royal Society of London B 284, 1854.Google Scholar
Niesenbaum, RA (1996) Linking herbivory and pollination: defoliation and selective fruit abortion in Lindera benzoin. Ecology 77, 2324–2331.10.2307/2265734CrossRefGoogle Scholar
Nuttle, T, Yerger, EH, Stoleson, SH and Ristau, TE (2011) Legacy of top-down herbivore pressure ricochets back up multiple trophic levels in forest canopies over 30 years. Ecosphere 2, 1–11.10.1890/ES10-00108.1CrossRefGoogle Scholar
Pace, ML, Cole, JJ, Carpenter, SR and Kitchell, JF (1999) Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution 14, 483–488.10.1016/S0169-5347(99)01723-1CrossRefGoogle ScholarPubMed
Potts, SG, Vulliamy, B, Dafni, A, Ne’eman, G and Willmer, P (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84, 2628–2642.10.1890/02-0136CrossRefGoogle Scholar
Pringle, RM, Young, TP, Rubenstein, DI and McCauley, DJ (2007) Herbivore-initiated interaction cascades and their modulation by productivity in an African savanna. Proceedings of the National Academy of Sciences USA 104, 193–197.10.1073/pnas.0609840104CrossRefGoogle Scholar
Pringle, RM, Palmer, TM, Goheen, JR, McCauley, DJ and Keesing, F (2011) Ecological importance of large herbivores in the Ewaso ecosystem. Smithsonian Contributions to Zoology 632, 43–54.10.5479/si.00810282.632.43CrossRefGoogle Scholar
Pringle, RM, Prior, KM, Palmer, TM, Young, TP and Goheen, JR (2016) Large herbivores promote habitat specialization and beta diversity of African savanna trees. Ecology 97, 2640–2657.10.1002/ecy.1522CrossRefGoogle ScholarPubMed
Ripple, WJ and Beschta, RL (2006) Linking a cougar decline, trophic cascade, and catastrophic regime shift in Zion National Park. Biological Conservation 133, 397–408.10.1016/j.biocon.2006.07.002CrossRefGoogle Scholar
Ripple, WJ, Estes, JA, Beschta, RL, Wilmers, CC, Ritchie, EG, Hebblewhite, M, Berger, J, Elmhagen, B, Letnic, M, Nelson, MP, Schmitz, OJ, Smith, DW, Wallach, AD and Wirsing, AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343, 1241484.10.1126/science.1241484CrossRefGoogle ScholarPubMed
Roberson, EJ, Chips, MJ, Carson, WP and Rooney, TP (2016) Deer herbivory reduced web-building spider abundance by simplifying forest vegetation structure. PeerJ 4, e2538.10.7717/peerj.2538CrossRefGoogle Scholar
Schermelleh-Engel, K and Moosbrugger, H (2003) Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Methods of Psychological Research Online 8, 23–74.Google Scholar
Shurin, JB, Borer, ET, Seabloom, EW, Anderson, K, Blanchette, CA, Broitman, B, Cooper, SD and Halpern, B.S (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters 5, 785–791.10.1046/j.1461-0248.2002.00381.xCrossRefGoogle Scholar
Strauss, SY (1997) Floral characters link herbivores, pollinators, and plant fitness. Ecology 78, 1640–1645.10.1890/0012-9658(1997)078[1640:FCLHPA]2.0.CO;2CrossRefGoogle Scholar
Terborgh, J and Feeley, K (2010) Propagation of trophic cascades via multiple pathways in tropical forests. In Terborgh, J, and Estes, JA (eds), Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Washington, DC: Island Press, pp. 125–140.Google Scholar
Titcomb, G, Allan, BF, Ainsworth, T, Henson, L, Hedlund, T, Pringle, RM, Njoroge, L, Campana, MG, Fleischer, RC, Mantas, JN and Young, HS (2017) Interacting effects of wildlife loss and climate on ticks and tick-borne disease. Proceedings of the Royal Society B 284, 20160124.10.1098/rspb.2017.0475CrossRefGoogle ScholarPubMed
Van Klink, R, Van Der Plas, F, Van Noordwijk, CG, Wallisdevries, MF and Olff, H (2015) Effects of large herbivores on grassland arthropod diversity. Biological Reviews of the Cambridge Philosophical Society 90, 347–366.10.1111/brv.12113CrossRefGoogle ScholarPubMed
Vasquez, DP and Simberloff, D (2004) Indirect effects of an introduced ungulate on pollination and plant reproduction. Ecological Monographs 74, 281–308.10.1890/02-4055CrossRefGoogle Scholar
Wardle, DA and Bardgett, RD (2004) Human-induced changes in large herbivorous mammal density: the consequences. Frontiers in Ecology and the Environment 2, 145–153.10.1890/1540-9295(2004)002[0145:HCILHM]2.0.CO;2CrossRefGoogle Scholar
Warren, MS (1993) A review of butterfly conservation in central southern Britain: II. Site management and habitat selection of key species. Biological Conservation 64, 37–49.10.1016/0006-3207(93)90381-ACrossRefGoogle Scholar
Weiner, CN, Werner, M, Linsenmair, KE and Blüthgen, N (2014) Land-use impacts on plant–pollinator networks: interaction strength and specialization predict pollinator declines. Ecology 95, 466–474.10.1890/13-0436.1CrossRefGoogle ScholarPubMed
Weinstein, S, Titcomb, G, Agwanda, B, Riginos, C and Young, H (2017) Parasite responses to large mammal loss in an African savanna. Ecology 98, 1839–1848.10.1002/ecy.1858CrossRefGoogle Scholar
Westphal, C, Bommarco, R, Carré, G, Lamborn, E, Morison, N, Petanidou, T, Potts, SG, Roberts, SPM, Szentgyörgyi, H, Tscheulin, T, Vaissière, BE, Woyciechowski, M, Biesmeijer, JC, Kunin, WE, Settele, J and Steffan-Dewenter, I (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecological Monographs 78, 653–671.10.1890/07-1292.1CrossRefGoogle Scholar
Wilkerson, ML, Roche, LM and Young, TP (2013) Indirect effects of domestic and wild herbivores on butterflies in an African savanna. Ecology and Evolution 11, 3672–3683.10.1002/ece3.744CrossRefGoogle Scholar
Yoshihara, Y, Chimeddorj, B, Buuveibaatar, B, Lhagvasuren, B and Takatsuki, S (2008) Effects of livestock grazing on pollination on a steppe in eastern Mongolia. Biological Conservation 141, 2376–2386.10.1016/j.biocon.2008.07.004CrossRefGoogle Scholar
Young, HS, McCauley, DJ, Dirzo, R, Goheen, JR, Agwanda, B, Brook, CE, Otarola-Castillo, E, Ferguson, AW, Kinyua, D, McDonough, MM, Palmer, TM, Pringle, RM, Young, TP and Helgen, KM (2015) Context-dependent effects of large-wildlife declines on small-mammal communities in central Kenya. Ecological Applications 25, 348–360.10.1890/14-0995.1CrossRefGoogle ScholarPubMed
Young, TP and Augustine, DJ (2007) Interspecific variation in the reproductive response of acacia species to protection from large mammalian herbivores. Biotropica 39, 559–561.10.1111/j.1744-7429.2007.00281.xCrossRefGoogle Scholar