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Seasonality influences ant-mediated nutrient acquisition (myrmecotrophy) by a Neotropical myrmecophyte

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Abstract

Tachia guianensis (Gentianaceae), a Neotropical understory myrmecophyte, shelters ant colonies in its hollow trunks and branches (domatia). In turn, it is protected from defoliators and obtains nutrients from ant-produced wastes (myrmecotrophy). Aiming to verify if seasonality influences nitrogen assimilation via ant wastes using the stable isotope nitrogen-15, we first studied Tachia’s phenology and its seasonal leaf production, and then the life cycle of its two more frequent guest ant species. We found that leaf production was much higher during the rainy than the dry season. Mature guest ant colonies produced sexuals regardless of the season and the net weight of the waste piles inside the domatia did not vary between seasons, so that the availability of nutrients to their host plant is steady year-long. By providing the two most frequent mutualistic guest ant species with food enriched with nitrogen-15, we showed that Tachia individuals assimilate more nitrogen from ant wastes during the rainy season, when the plant is physiologically active, compared to the dry season. Thus, one can deduce that the increase in nitrogen assimilation during the rainy season is determined by the increase in Tachia’s physiological activity during that season. Information gathered through a bibliographic compilation confirms that none of the 15 ant species known to be associated with myrmecophytes for which the life cycle was studied is characterized by seasonal reproduction (which would result in fluctuating waste production). The same is true for 49.7% of 167 tropical ant species (seasonal production for the remaining species). We concluded that, in contrast to the non-seasonal ant colony reproductive cycle, Tachia’s phenology determines the myrmecotrophic assimilation rate.

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References

  • Beattie AJ (1989) Myrmecotrophy: plants fed by ants. Trends Ecol Evol 4:172–176

    CAS  PubMed  Google Scholar 

  • Becker P, Castillo A (1990) Root architecture of shrubs and saplings in the understory of a tropical moist forest in lowland Panama. Biotropica 22:242–249

    Google Scholar 

  • Benson WW (1985) Amazon ant-plants. In: Prance GT, Lovejoy TE (eds) Amazonia. Pergamon Press, Oxford, pp 239–266

    Google Scholar 

  • Bonal D, Burban B, Stahl C, Wagner F, Hérault B (2016) The response of tropical rainforests to drought -lessons from recent research and future prospects. Ann For Sci 73:27–44

    PubMed  Google Scholar 

  • Chanam J, Sheshshayee MS, Kasinathan S, Jagdeesh A, Joshi KA, Borges RM (2014) Nutritional benefits from domatia inhabitants in an ant-plant interaction: interlopers do pay the rent. Funct Ecol 28:1107–1116

    Google Scholar 

  • Craine JM, Engelbrecht BMJ, Lusk CH, McDowell NG, Poorter H (2012) Resource limitation, tolerance, and the future of ecological plant classification. Front Plant Sci 3:246

    PubMed  PubMed Central  Google Scholar 

  • Dejean A, Orivel J, Rossi V, Roux O, Lauth J, Malé P-JG, Céréghino R, Leroy C (2013) Predation success by a plant-ant indirectly favours the growth and fitness of its host myrmecophyte. PLoS ONE 8:e59405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dejean A, Petitclerc F, Compin A, Azémar F, Corbara B, Delabie JHC, Leroy C (2017) Hollow internodes permit a Neotropical understory plant to shelter multiple mutualistic ant species, obtaining protection and nutrient provisioning (myrmecotrophy). Am Nat 190:E124–E131

    PubMed  Google Scholar 

  • Dejean A, Azémar F, Petitclerc F, Delabie JHC, Corbara B, Leroy C, Céréghino R, Compin A (2018) Highly modular pattern in ant-plant interactions involving specialized and non-specialized myrmecophytes. Sci Nat 105:43

    Google Scholar 

  • Enzmann BL, Gibbs AG, Nonacs P (2014) The cost of being queen: investment across Pogonomyrmex harvester ant gynes that differ in degree of claustrality. J Insect Physiol 70:134–142

    CAS  PubMed  Google Scholar 

  • Fernandes TT, Silva RR, Souza-Campana DR, Silva OGM, Morini MSC (2019) Winged ants (Hymenoptera: Formicidae) presence in twigs on the leaf litter of Atlantic Forest. Biota Neotrop 19:e20180694

    Google Scholar 

  • Fiala B, bin Hashim B, Dumpert K, Maschwitz U (2017) Nuptial flight of the Southeast Asian plant-ant Crematogaster captiosa (Forel, 1911) and the phenology of colony founding. Asian Myrmecol 9:e009013

    Google Scholar 

  • Frederickson ME (2006) The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites. Oecologia 149:418–427

    PubMed  Google Scholar 

  • González-Teuber M, Heil M (2015) Comparative anatomy and physiology of myrmecophytes: ecological and evolutionary perspectives. Res Rep Biodiv Stud 4:21–32

    Google Scholar 

  • Heil M (2015) Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu Rev Entomol 60:213–232

    CAS  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1994) Journey to the ants: a story of scientific exploration. Harvard University Press, Cambridge

    Google Scholar 

  • Janzen DH (1967) Interaction of the bull’s-horn acacia (Acacia cornigera L.) with an ant inhabitant (Pseudomyrmex ferruginea F. Smith) in eastern Mexico. Kansas Univ Sci bull 47:315–558

    Google Scholar 

  • Kaspari M, Pickering J, Longino JT, Windsor D (2001a) The phenology of a Neotropical ant assemblage: evidence for continuous and overlapping reproduction. Behav Ecol Sociobiol 50:382–390

    Google Scholar 

  • Kaspari M, Pickering J, Windsor D (2001b) The reproductive flight phenology of a Neotropical ant assemblage. Ecol Entomol 26:245–257

    Google Scholar 

  • Kenne M, Dejean A (1998) Nuptial flight in Myrmicaria opaciventris (Formicidae: Myrmicinae). Sociobiology 31:41–50

    Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell Environ 25:275–294

    CAS  Google Scholar 

  • Leroy C, Séjalon-Delmas N, Jauneau A, Ruiz-González M-X, Gryta H, Jargeat P, Corbara B, Dejean A, Orivel J (2011) Trophic mediation by a fungus in an ant-plant mutualism. J Ecol 99:583–590

    Google Scholar 

  • Longino JT (2003) Ants of Costa Rica. Crematogaster tenuicula Forel 1904. http://ants.biology.utah.edu/genera/Crematogaster/species/tenuicula/tenuicula_01.html

  • Nielsen MG, Peng RK, Offenberg J, Birkmose D (2016) Mating strategy of Oecophylla smaragdina (Hymenoptera: Formicidae) in northern Australia. Austral Entomol 55:261–267

    Google Scholar 

  • Orivel J, Lambs L, Malé P-JG, Leroy C, Grangier J, Otto T, Quilichini A, Dejean A (2011) Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants. Oecologia 165:369–376

    PubMed  Google Scholar 

  • Orivel J, Malé P-J, Lauth J, Roux O, Petitclerc F, Dejean A, Leroy C (2017) Trade-offs in mutualistic investment in a tripartite symbiosis. Proc R Soc London B 284:20161679

    Google Scholar 

  • Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci USA 107:17234–17239

    CAS  PubMed  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Google Scholar 

  • Pfeiffer M, Linsenmair KE (1997) Reproductive synchronization in the tropics: the circa-semiannual rhythm in the nuptial flight of the giant ant Camponotus gigas Latreille (Hym./Form.). Ecotropica 3:21–32

    Google Scholar 

  • Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282

    Google Scholar 

  • Pohlit AM, dos Santos EVM, da Silva TCM, de Morais SKR, Nunomura SM, Struwe L (2012) A rare secoiridoid monoterpene and a xanthone from Tachia grandiflora Maguire and Weaver. Biochem Syst Ecol 44:267–269

    CAS  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago

    Google Scholar 

  • Rowland L, Malhi Y, Silva-Espejo JE, Farfan-Amezquita F, Halladay K, Doughty CE, Meir P, Phillips OL (2014) The sensitivity of wood production to seasonal and interannual variations in climate in a lowland Amazonian rainforest. Oecologia 174:295–306

    PubMed  Google Scholar 

  • Stahl C, Hérault B, Rossi V, Burban B, Bréchet C, Bonal D (2013) Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter? Oecologia 173:1191–1201

    PubMed  Google Scholar 

  • Struwe L, Kinkade MP (2013) Revision of Tachia (Gentianaceae: Helieae). Syst Bot 38:1142–1159

    Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc London B 274:151–164

    Google Scholar 

  • Tobin M, Lopez OR, Kursar TA (1999) Response of tropical understory plants to a severe drought: tolerance and avoidance of water stress. Biotropica 31:570–578

    Google Scholar 

  • Torres JA, Snelling RR, Canals M (2001) Seasonal and nocturnal periodicities in ant nuptial flights in the tropics (Hymenoptera: Formicidae). Sociobiology 37:601–625

    Google Scholar 

  • Vasconcelos HL (1993) Ant colonization of Maieta guianensis seedlings, an Amazon ant-plant. Oecologia 95:439–443

    PubMed  Google Scholar 

  • Wagner F, Hérault B, Bonal D, Stahl C, Rossi V, Anderson LO et al (2016) Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests. Biogeosciences 13:2537–2562

    Google Scholar 

  • Woodcock P, Edwards DP, Newton RJ, Edwards FA, Khen CV, Bottrell SH, Hamer KC (2012) Assessing trophic position from nitrogen isotope ratios: effective calibration against spatially varying baselines. Naturwissenschaften 99:275–283

    CAS  PubMed  Google Scholar 

  • Wright SJ (1991) Seasonal drought and the phenology of understory shrubs in a tropical moist forest. Ecology 72:1643–1657

    Google Scholar 

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Acknowledgements

We are grateful to John T. Longino for providing information on the nuptial flight phenology of different plant-ant species, Eric Marcon for his advice concerning the presentation of the statistics, Andrea Yockey for proofreading the manuscript and the Laboratoire Environnement de Petit Saut for logistical assistance. Financial support was provided by the ‘Investissement d’Avenir’ grants managed by the French Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01).

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Authors and Affiliations

  1. Ecolab, Laboratoire écologie fonctionnelle et environnement, Université de Toulouse, CNRS, Toulouse, France

    Alain Dejean & Frédéric Azémar

  2. CNRS, UMR EcoFoG, AgroParisTech, CIRAD, INRAE, Université des Antilles, Université de Guyane, 97310, Kourou, France

    Alain Dejean & Frédéric Petitclerc

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  1. Alain Dejean
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  2. Frédéric Petitclerc
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  3. Frédéric Azémar
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Correspondence to Frédéric Azémar.

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Dejean, A., Petitclerc, F. & Azémar, F. Seasonality influences ant-mediated nutrient acquisition (myrmecotrophy) by a Neotropical myrmecophyte. Evol Ecol 34, 645–657 (2020). https://doi.org/10.1007/s10682-020-10056-y

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