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Spinescence and Total Phenolic Content Do Not Influence Diet Preference of a Critically Endangered Megaherbivore, but the Mix of Compounds Does

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Abstract

In contrast to understanding spinescence in savanna woody species, little is known about the functions of plant secondary metabolites (PSM). Negative effects of PSMs on individual animal performance potentially translate into negative effects on herbivore population growth. Hence, understanding PSM functions is important for the conservation of savanna megafauna. We tested the view that black rhinoceros (Diceros bicornis) diet preference is not affected by spinescence or total phenolic abundance. We hypothesized that the composition of phenolic mixtures, however, would affect preference. Furthermore, we tested our data from 71 woody species for a trade-off between structural and chemical defenses. Spinescence type, and spinescence generally, did not deter black rhino feeding. Using eco-metabolomic data, we found that total abundance of phenolics did not affect preference, but mixture composition did and that the probability of spinescence trading off against phenolics depended on the mixture. We note that our study was restricted to black rhino and that diet preferences of other mammal herbivores might be influenced by subtle differences in phenolic mixtures. However, our results did support a previous, more detailed study of phenolic profiles of six species showing the same patterns in relation to preference generalised across mammal herbivore species in savannas. Our results represent substantial advancement in the understanding of the roles of PSMs, especially flavonoid compounds, in the functioning of savanna ecosystems, and highlight the need to dig deeper into broad groups of traits such as spinescence or total phenolics to improve understanding of woody plant defenses in savannas.

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References

  • Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science 193:24–29

    Article  CAS  PubMed  Google Scholar 

  • Basha NAD, Scogings PF, Dziba LE, Nsahlai IV (2012) Diet selection of Nguni goats in relation to season, chemistry and physical properties of browse in sub-humid subtropical savanna. Small Ruminant Res 102:163–171

    Article  Google Scholar 

  • Basha NAD, Scogings PF, Nsahlai IV (2013) Effects of season, browse species and tannins on gas production kinetics of forages in the sub-humid subtropical savannah, South Africa. J Sci Food Agr 93:1338–1348

    Article  CAS  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bell AD (1991) Plant form. Oxford University Press, UK

  • Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Buk KG, Knight MH (2010) Seasonal diet preferences of black rhinoceros in three arid south African National Parks. Afr J Ecol 48:1064–1075

    Article  Google Scholar 

  • Charles-Dominique T, Davies TJ, Hempson GP, Bezeng BS, Daru BH, Kabongo RM, Maurin O, Muasya AM, van der Bank M, Bond WJ (2016) Spiny plants, mammal browsers, and the origin of African savannas. P Nat Acad Sci 113:E5572–E5579

    Article  CAS  Google Scholar 

  • Charles-Dominique T, Barczi J, Chamaillé-Jammes S (2020) Woody plant architecture and effects on browsing herbivores in savannas. In: Scogings PF, Sankaran M (eds) Savanna woody plants and large herbivores. John Wiley and Sons Ltd, Hoboken, pp 469–488

    Google Scholar 

  • Coates Palgrave M (2002) Trees of southern Africa, 3rd edn. Struik Publishers, South Africa

  • Codron D (2020) Evolution of large mammal herbivores in savannas. In: Scogings PF, Sankaran M (eds) Savanna woody plants and large herbivores. John Wiley and Sons Ltd, Hoboken, pp 213–243

    Google Scholar 

  • Coley P, Bryant J, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  CAS  PubMed  Google Scholar 

  • Cooper SM, Owen-Smith N (1985) Condensed tannins deter feeding by browsing ruminants in a south African savanna. Oecologia 67:142–146

    Article  CAS  PubMed  Google Scholar 

  • Cooper SM, Owen-Smith N (1986) Effects of plant spinescence on large mammalian herbivores. Oecologia 68:446–455

    Article  PubMed  Google Scholar 

  • Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189

    Article  Google Scholar 

  • DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, Wallis IR, Johnson CN, Foley WJ (2014) Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 123:298–308

    Article  Google Scholar 

  • Duthé V, Defossez E, van der Westhuizen R, Glauser G, Rasmann S (2020) Out of scale out of place: black rhino forage preference across the hierarchical organization of the savanna ecosystem. Conserv Sci Pract 2:e191

    Google Scholar 

  • Dziba LE, Scogings PF, Raats JG, Gordon IJ (2003) Effects of season and breed on browse species intake rates and diet selection by goats in the false Thornveld of the eastern cape, South Africa. Small Ruminant Res 47:39–52

    Article  Google Scholar 

  • Ferreira SM, Bissett C, Cowell CR, Gaylard A, Greaver C, Hayes J, Hofmeyr M, Moolman-van der Vyver L, Zimmermann D (2017) The status of rhinoceroses in south African National Parks. Koedoe 59(1):a1392

    Article  Google Scholar 

  • Fomum SW, Scogings PF, Dziba LE, Nsahlai IV (2015) Seasonal variations in diet selection of Nguni goats: effects of physical and chemical traits of browse. Afr J Range For Sci 32:193–201

    Article  Google Scholar 

  • Ganqa NM, Scogings PF, Raats JG (2005) Plant factors affecting diet selection by black rhino in the great fish river reserve, South Africa. S Afr J Wildl Res 35:77–83

    Google Scholar 

  • Gowda JH, Palo RT, Udén P (2019) Seasonal variation in the nutritional value of woody plants along a natural gradient in eastern Africa. Afr J Ecol 57:226–237

    Article  Google Scholar 

  • Gyöngyi K, Elmeros M (2017) Forage choice of the reintroduced black rhino and the availability of selected browse species at Majete wildlife reserve, Malawi. Pachyderm 58:40–50

    Google Scholar 

  • Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178

    Article  Google Scholar 

  • Hattas D, Hjältén J, Julkunen-Tiitto R, Scogings PF, Rooke T (2011) Differential phenolic profiles in six African savanna woody species in relation to antiherbivore defense. Phytochem 72:1796–1803

    Article  CAS  Google Scholar 

  • Hattas D, Scogings PF, Julkunen-Tiitto R (2017) Does the growth differentiation balance hypothesis explain allocation to carbon based secondary metabolites in Combretum apiculatum, an African savanna woody species? J Chem Ecol 43:153–163

    Article  CAS  PubMed  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hostetler GL, Ralston RA, Schwartz SJ (2017) Flavones: food sources, bioavailability, metabolism, and bioactivity. Adv Nutr 8:423–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Illius AW, Duncan P, Richard C, Mesochina P (2002) Mechanisms of functional response and resource exploitation in browsing roe deer. J Anim Ecol 71:723–734

    Article  Google Scholar 

  • Joubert, D.F., Stolter, C., Krewenka, K.M., Uunona, N., Amputu, V., Nghalipo, E., Thompson, S., Schütte, K., Kruspe, M., Throop, H., du Preez, P., Beytell, P., le Roux, M. & Aindongo, H. (2018) Impacts of fire history in a semi-arid woodland savanna. In: Revermann R, Krewenka KM, Schmiedel U, Olwoch JM, Helmschrot J, Jürgens N (eds) Climate change and adaptive land management in southern Africa – assessments, changes, challenges, and solutions. Klaus Hess Publishers, Göttingen, Germany, pp 207–218

  • Katjiua MLJ, Ward D (2006) Resistance and tolerance of Terminalia sericea trees to simulated herbivore damage under different soil nutrient and moisture conditions. J Chem Ecol 32:1431–1443

    Article  CAS  PubMed  Google Scholar 

  • Kingdon J, Happold D, Butynski T, Hoffmann M, Happold M, Kalina J (2013) Mammals of Africa. Bloomsbury, UK

  • Landman M, Schoeman DS, Kerley GIH (2013) Shift in black rhinoceros diet in the presence of elephant: evidence for competition? PLoS One 8:e69771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenth R (2019) Emmeans: estimated marginal means, aka least-squares means. R package version 1.3.3. R Foundation for Statistical Computing, Vienna, Austria

  • Marsh KJ, Wallis IR, Kulheim C, Clark R, Nicolle D, Foley WJ, Salminen J (2020) New approaches to tannin analysis of leaves can be used to explain in vitro biological activities associated with herbivore defence. New Phytol 225:488–498

    Article  CAS  PubMed  Google Scholar 

  • McArt SH, Spalinger DE, Collins WB, Schoen ER, Stevenson T, Bucho M (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-Central Alaska. Ecology 90:1400–1411

    Article  PubMed  Google Scholar 

  • McArthur C, Finnerty PB, Schmitt MH, Shuttleworth A, Shrader AM (2019) Plant volatiles are a salient cue for foraging mammals: elephants target preferred plants despite background plant odour. Anim Behav 155:199–216

    Article  Google Scholar 

  • Mengistu G, Karonen M, Salminen J, Hendriks WH, Pellikaan WF (2017) In vitro fermentation of browse species using goat rumen fluid in relation to browse polyphenol content and composition. Anim Feed Sci Tech 231:1–11

    Article  CAS  Google Scholar 

  • Midgley JJ, Ward D (1996) Tests for inducible thorn defences against herbivory must consider plant growth strategies. Afr J Range For Sci 13:75–77

    Article  Google Scholar 

  • Mkhize NR, Scogings PF, Nsahlai IV, Dziba LE (2014) Diet selection of goats depends on season: roles of plant physical and chemical traits. Afr J Range For Sci 31:209–214

    Article  Google Scholar 

  • Mkhize NR, Heitkӧnig IMA, Scogings PF, Dziba LE, Prins HHT, de Boer WF (2015) Condensed tannins reduce browsing and increase grazing time of free-ranging goats in semi-arid savannas. Appl Anim Behav Sci 169:33–37

    Article  Google Scholar 

  • Moles AT, Peco B, Wallis IR, Foley WJ, Poore AG, Seabloom EW et al (2013) Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytol 198:252–263

    Article  PubMed  Google Scholar 

  • Moreira X, Mooney KA, Rasmann S, Petry WK, Carrillo-Gavilán A, Zas R, Sampedro L (2014) Trade-offs between constitutive and induced defences drive geographical and climatic clines in pine chemical defences. Ecol Lett 17:537–546

    Article  PubMed  Google Scholar 

  • Mouradov A, Spangenberg G (2014) Flavonoids: a metabolic network mediating plants adaptation to their real estate. Front Plant Sci 5:Article 620

  • Mudge JF, Baker LF, Edge CB, Houlahan JE (2012) Setting an optimal α that minimizes errors in null hypothesis significance tests. PLoS ONE 7:e32734

  • Muya SM, Oguge NO (2000) Effects of browse availability and quality on black rhino (Diceros bicornis michaeli groves 1967) diet in Nairobi National Park, Kenya. Afr J Ecol 38:62–71

    Article  Google Scholar 

  • Nobler JD, Camp MJ, Crowell MM, Shipley LA, Dadabay C, Rachlow JL, James L, Forbey JS (2019) Preference of specialist and generalist mammalian herbivores for mixtures versus individual plant secondary metabolites. J Chem Ecol 45:74–85

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner E (2019) Vegan: community ecology package. R package version 2.5-5. R Foundation for statistical computing, Vienna, Austria

  • Owen-Smith N (2008) The comparative population dynamics of browsing and grazing ungulates. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing. Springer, Berlin, pp 149–177

    Chapter  Google Scholar 

  • Owen-Smith N, Chafota J (2012) Selective feeding by a megaherbivore, the African elephant (Loxodonta africana). J Mammal 93:698–705

    Article  Google Scholar 

  • Owen-Smith N, Page B, Teren G, Druce DJ (2020) Megabrowser impacts on woody vegetation in savannas. In: Scogings PF, Sankaran M (eds) Savanna woody plants and large herbivores. John Wiley and Sons Ltd, Hoboken, pp 585–611

    Google Scholar 

  • Peters K, Gorzolka K, Bruelheide H, Neumann S (2018) Seasonal variation of secondary metabolites in nine different bryophytes. Ecol Evol 8:9105–9117

    Article  PubMed  PubMed Central  Google Scholar 

  • Provenza FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J Range Manag 48:2–17

    Article  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Routaboul J, Dubos C, Beck G, Marquis C, Bidzinski P, Loudet O, Lepiniec L (2012) Metabolite profiling and quantitative genetics of natural variation for flavonoids in Arabidopsis. J Exp Bot 63:3749–3764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salminen J, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338

    Article  Google Scholar 

  • Sankaran M, Augustine DJ, Ratnam J (2013) Native ungulates of diverse body sizes collectively regulate long-term woody plant demography and structure of semi-arid savanna. J Ecol 101:1389–1399

    Article  Google Scholar 

  • Schmitt MH, Shuttleworth A, Ward D, Shrader AM (2018) African elephants use plant odours to make foraging decisions across multiple spatial scales. Anim Behav 141:17–27

    Article  Google Scholar 

  • Schmitt MH, Shuttleworth A, Shrader AM, Ward D (2020) The role of volatile plant secondary metabolites as pre-ingestive cues and potential toxins dictating diet selection by African elephants. Oikos 129:24–34

    Article  Google Scholar 

  • Scogings PF, Dziba LE, Gordon IJ (2004) Leaf chemistry of woody plants in relation to season, canopy retention and goat browsing in a semi-arid subtropical savanna. Austral Ecol 29:278–286

    Article  Google Scholar 

  • Scogings PF, Mamashela TC, Zobolo AM (2017) Growth, nitrogen and tannins of semi-arid savanna saplings in response to herbivory and water. J Arid Environ 137:21–29

    Article  Google Scholar 

  • Scogings PF, Sankaran M (2020) Woody plants and large herbivores in savannas: ancient past – uncertain future. In: Scogings PF, Sankaran M (eds) Savanna woody plants and large herbivores. John Wiley and Sons Ltd, Hoboken, pp 683–712

    Google Scholar 

  • Scogings PF, Siko S, Taylor RW (2014) Calibration of a hand-held instrument for measuring condensed tannin concentration based on UV- and red-excited fluorescence. Afr J Range For Sci 31:55–58

    Article  Google Scholar 

  • Skarpe C, Jansson I, Seljeli L, Bergström R, Røskaft E (2007) Browsing by goats on three spatial scales in a semi-arid savanna. J Arid Environ 68:480–491

    Article  Google Scholar 

  • Skarpe C, Bergström R, Danell K, Eriksson H, Kunz C (2012) Of goats and spines – a feeding experiment. Afr J Range For Sci 29:37–41

    Article  Google Scholar 

  • Steuer P, Südekum K, Tütken T, Müller DWH, Kaandorp J, Bucher M, Clauss M, Hummel J (2014) Does body mass convey a digestive advantage for large herbivores? Funct Ecol 28:1127–1134

    Article  Google Scholar 

  • Stolter C (2008) Intra-individual plant response to moose browsing: feedback loops and impacts on multiple consumers. Ecol Monogr 78:167–183

    Article  Google Scholar 

  • Stolter C, Ball JB, Julkunen-Tiitto R, Lieberei R, Ganzhorn JU (2005) Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response. Can J Zool 83:807–819

    Article  CAS  Google Scholar 

  • Tan Y, Chang SKC (2017) Digestive enzyme inhibition activity of the phenolic substances in selected fruits, vegetables and tea as compared to black legumes. J Funct Food 38:644–655

    Article  CAS  Google Scholar 

  • Tews J, Moloney K, Jeltsch F (2004) Modeling seed dispersal in a variable environment: a case study of the fleshy-fruited savanna shrub Grewia flava. Ecol Model 175:65–76

    Article  Google Scholar 

  • Tohge T, Perez de Souza L, Fernie AR (2017) Current understanding of the pathways of flavonoid biosynthesis in model and crop plants. J Exp Bot 68:4013–4028

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson KW, van Langevelde F, Ward D, Prins HHT, de Bie S, Vosman B, Sampaio EVSB, Sterk FJ (2016) Defence against vertebrate herbivores trades off into architectural and low nutrient strategies amongst savanna Fabaceae species. Oikos 125:126–136

    Article  CAS  Google Scholar 

  • van Lieverloo RJ, Schuiling BF, de Boer WF, Lent PC, de Jong CB, Brown D, Prins HHT (2009) A comparison of faecal analysis with backtracking to determine the diet composition and species preference of the black rhinoceros (Diceros bicornis minor). Eur J Wildl Res 55:505–515

    Article  Google Scholar 

  • Villalba JJ, Provenza FD, Catanese F, Distel RA (2015) Understanding and manipulating diet choice in grazing animals. Anim Prod Sci 55:261–271

    Article  CAS  Google Scholar 

  • Watson LR, Brown DR (2000) Browsing of Grewia occidentalis by domestic stock in a south African savanna: the influence of bush clumps. Afr J Range For Sci 17:60–63

    Article  Google Scholar 

  • Wigley BJ, Fritz H, Coetsee C (2018) Defence strategies in African savanna trees. Oecologia 187:797–809

    Article  PubMed  Google Scholar 

  • Wigley BJ, Coetsee C, Augustine DJ, Ratnam J, Hattas D, Sankaran M (2019) A thorny issue: Woody plant defence and growth in an east African savanna. J Ecol 107:1839–1851

    Article  Google Scholar 

  • Wilson SL, Kerley GIH (2003a) The effect of plant spinescence on the foraging efficiency of bushbuck and boergoats: browsers of similar body size. J Arid Environ 55:150–158

    Article  Google Scholar 

  • Wilson SL, Kerley GIH (2003b) Bite diameter selection by thicket browsers: the effect of body size and plant morphology on forage intake and quality. For Ecol Manag 181:51–65

    Article  Google Scholar 

  • Wood S, Scheipl F (2017) Gamm4: generalized additive mixed models using “mgcv” and “Lme4”. R Foundation for Statistical Computing, Vienna

    Book  Google Scholar 

  • Yonekura-Sakakibara K, Higashi Y, Nakabayashi R (2019) The origin and evolution of plant flavonoid metabolism. Front Plant Sci 10:Article 943

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Acknowledgments

We are grateful for the contributions of Keryn Adcock and colleagues at the African Rhino Specialist Group and Riitta Julkunen-Tiitto whose lab facilities at the University of Eastern Finland were used for the HPLC analyses.

Funding

DH was supported by Grant 48494 of the National Research Foundation’s (NRF) Sweden-South Africa Programme. Any opinions, findings and conclusions, or recommendations expressed in this material are those of the authors and therefore the NRF does not accept any liability in regard thereto.

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All authors contributed to conceptualization. DH collected the data. SD analyzed the data. PFS wrote the first draft. DH and SD contributed to all drafts.

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Correspondence to Peter F. Scogings.

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Scogings, P.F., Demmer, S. & Hattas, D. Spinescence and Total Phenolic Content Do Not Influence Diet Preference of a Critically Endangered Megaherbivore, but the Mix of Compounds Does. J Chem Ecol 47, 322–333 (2021). https://doi.org/10.1007/s10886-021-01258-x

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