Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-18T18:43:17.284Z Has data issue: false hasContentIssue false
  • English
  • Français

Extrafloral nectar as a driver of ant community spatial structure along disturbance and rainfall gradients in Brazilian dry forest

Published online by Cambridge University Press:  11 October 2019

Carlos Henrique Félix da Silva Open the ORCID record for Carlos Henrique Félix da Silva [Opens in a new window] ,
Xavier Arnan ,
Alan N. Andersen  and
Inara R. Leal
Carlos Henrique Félix da Silva
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Professor Moraes Rego s/n, Cidade Universitária, CEP: 50670-901, Recife, PE, Brasil
Xavier Arnan
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Professor Moraes Rego s/n, Cidade Universitária, CEP: 50670-901, Recife, PE, Brasil CREAF, Cerdanyola del Vallès, Catalunya, Spain
Alan N. Andersen
Affiliation:
Research Institute for the Environment and Livelihoods, Charles Darwin University, Ellengowan Dr, Casuarina, Northern Territory, 0810, Australia
Inara R. Leal*
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Professor Moraes Rego s/n, Cidade Universitária, CEP: 50670-901, Recife, PE, Brasil
*
*Author for correspondence: Inara R. Leal, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Although extrafloral nectar (EFN) is a key food resource for arboreal ants, its role in structuring ground-nesting ant communities has received little attention, despite these ants also being frequent EFN-attendants. We investigated the role of EFN as a driver of the spatial structure of ground-nesting ant communities occurring in dry forest in north-eastern Brazil. We examined the effects on this relationship of two global drivers of biodiversity decline, chronic anthropogenic disturbance and climate change (through decreasing rainfall). We mapped EFN-producing plants and ant nests in 20 plots distributed along independent gradients of disturbance and rainfall. We categorized ant species into three types according to their dependence on EFN: heavy users, occasional users and non-users. We found a strong relationship between ant dependence on EFN and nest proximity to EFN-producing plants: heavy-users (mean distance 1.1 m) nested closer to EFN-producing plants than did occasional users (1.7 m), which in turn nested closer to EFN-producing plants than did non-users (2.3 m). Neither disturbance nor rainfall affected the proximity of heavy-user nests to EFN-producing plants. Our study shows for the first time that EFN is a key driver of the spatial structure of entire communities of ground-nesting ants.

Keywords

Aridityclimate changedry foresthuman disturbanceoptimal foraging
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 6 , November 2019 , pp. 280 - 287
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Andersen, AN (1992) Regulation of “momentary” diversity by dominant species in exceptionally rich ant communities of the Australian seasonal tropics. American Naturalist 140, 401–420.CrossRefGoogle ScholarPubMed
Andersen, AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. Journal of Biogeography 22, 15–29.CrossRefGoogle Scholar
Arnan, X, Leal, IR, Tabarelli, M, Andrade, JF, Barros, MF, Câmara, T, Jamelli, D, Knoechelmann, C, Menezes, TGC, Menezes, AGS, Oliveira, FMP, de Paula, AS, Pereira, SG, Rito, KF, Sfair, JC, Siqueira, FFS, Souza, DG, Specht, MJ, Vieira, LA, Arcoverde, GB and Andersen, A (2018) A framework for deriving measures of chronic anthropogenic disturbance: surrogate, direct, single and multi-metric indices in Brazilian Caatinga. Ecological Indicators 94, 274–282.CrossRefGoogle Scholar
Baccaro, FB, Feitosa, RM, Fernández, F, Fernandes, IO, Izzo, TJ, Souza, JLP and Solar, R (2015) Guia para os gêneros de formigas do Brasil. Editora INPA, Manaus.Google Scholar
Bennett, B and Breed, MD (1985) The nesting biology, mating behavior, and foraging ecology of Perdita opuntiae (Hymenoptera: Andrenidae). Journal of the Kansas Entomological Society 58, 185–194.Google Scholar
Bequaert, JC (1922) Ants in their diverse relations to the plant world. Bulletin of the American Museum of Natural History 45, 333–621.Google Scholar
Blois, JL, Williams, JW, Fitzpatrick, MC, Jackson, ST and Ferrier, S (2013) Space can substitute for time in predicting climate-change effects on biodiversity. Proceedings of the National Academy of Sciences USA 110, 374–9379.CrossRefGoogle ScholarPubMed
Blüthgen, N and Fiedler, K (2004) Competition for composition: lessons from nectar feeding ant communities. Ecology 85, 1479–1485.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. New York, NY: Springer-Verlag.Google Scholar
Byk, J and Del-Claro, K (2011) Ant–plant interaction in the neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Population Ecology 53, 327–332.CrossRefGoogle Scholar
Caddy-Retalic, S, Andersen, AN, Aspinwall, MJ, Breed, MF, Byrne, M, Christmas, MJ, Dong, N, Evans, BJ, Fordham, DA, Guerin, GR, Hoffmann, AA, Hughes, AC, van Leeuwen, SJ, McInerney, FA, Prober, SM, Rossetto, M, Rymer, PD, Steane, DA, Wardle, GM and Lowe, AJ (2017) Bioclimatic transect networks: powerful observatories of ecological change. Ecology and Evolution 7, 4607–4619.CrossRefGoogle ScholarPubMed
Câmara, T, Leal, IR, Blüthgen, N, Oliveira, FMP, De Queiroz, RT and Arnan, X (2018) Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant-plant mutualistic networks in the Caatinga, a Brazilian dry forest. Journal of Animal Ecology 87, 1022–1033.CrossRefGoogle ScholarPubMed
Cook, SC and Davidson, DW (2006) Nutritional and functional biology of exudate-feeding ants. Entomologia Experimentalis et Applicata 118, 1–10.CrossRefGoogle Scholar
Covich, AP (1976) Analyzing shapes of foraging areas: some ecological and economic theories. Annual Review of Ecology, Evolution, and Systematics 7, 235–257.CrossRefGoogle Scholar
Davidson, DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biological Journal of the Linnean Society 61, 153–181.CrossRefGoogle Scholar
Davidson, DW and Patrell-Kim, L (1996) Tropical arboreal ants: why so abundant? In Gibson, AC (ed.), Neotropical Biodiversity and Conservation. Berkeley, CA: University of California, pp. 127–140.Google Scholar
Davidson, DW, Cook, SC and Snelling, RR (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300, 969–972.CrossRefGoogle ScholarPubMed
Eisner, T (1957) A comparative morphological study of the proventriculus of ants (Hymenoptera: Formicidae). Bulletin of the Museum of Comparative Zoology 116, 429–490.Google Scholar
Grundel, R (1992) How the mountain chickadee procures more food in less time for its nestlings. Behavioral Ecology and Sociobiology 31, 291–300.CrossRefGoogle Scholar
Grundel, R, Jean, RP, Frohnapple, KJ, Glowacki, GA, Scott, PE and Noel, NB (2010) Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecological Applications 20, 1678–1692.CrossRefGoogle ScholarPubMed
Heil, M (2011) Nectar: generation, regulation and ecological functions. Trends in Plant Science 16, 191–200.CrossRefGoogle ScholarPubMed
Hijmans, RJ, Cameron, SE, Parra, JL, Jones, PG and Jarvis, A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.CrossRefGoogle Scholar
Hölldobler, B and Wilson, EO (1990) The Ants. Cambridge, MA: Belknap Press, Harvard University Press.CrossRefGoogle Scholar
Holway, DA and Case, TJ (2000) Mechanisms of dispersed central-place foraging in polydomous colonies of the Argentine ant. Animal Behaviour 59, 433–441.CrossRefGoogle ScholarPubMed
Jakobsen, H and Kristjánsson, K (1994) Influence of temperature and floret age on nectar secretion in Trifolium repens. L. Annals of Botany 74, 327–334.CrossRefGoogle Scholar
Janzen, DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249–275.CrossRefGoogle ScholarPubMed
Kacelnik, A, Houston, AI and Schmid-Hempel, P (1986) Central-place foraging in honey bees: the effect of travel time and nectar flow on crop filling. Behavioral Ecology and Sociobiology 19, 19–24.CrossRefGoogle Scholar
Kay, A (2002) Applying optimal foraging theory to assess nutrient availability ratios for ants. Ecology 83, 1935–1944.CrossRefGoogle Scholar
Keasar, T, Sadeh, A and Shmida, A (2008) Variability in nectar production and standing crop, and their relation to pollinator visits in a Mediterranean shrub. Arthropod–Plant Interactions 2, 117–123.CrossRefGoogle Scholar
Koptur, S (1992) Extrafloral nectary-mediated interactions between insects and plants. In Bernays, E. (ed.), Insect-Plant Interactions. Boca Raton, FL: CRC Press, pp. 81–129.Google Scholar
Lange, D, Dáttilo, W and Del-Claro, K (2013) Influence of extrafloral nectary phenology on ant-plant mutualistic networks in a neotropical savanna. Ecological Entomology 38, 463–469.CrossRefGoogle Scholar
Leal, LC, Andersen, AN and Leal, IR (2015) Disturbance winners or losers? Plants bearing extrafloral nectaries in Brazilian Caatinga. Biotropica 47, 468–474.CrossRefGoogle Scholar
MacArthur, RH and Pianka, ER (1966) On optimal use of a patchy environment. American Naturalist 100, 603–609.CrossRefGoogle Scholar
Magrin, GO, Marengo, JA, Boulanger, JP, Buckeridge, MS, Castellanos, E, Poveda, G and Vicuña, S (2014) Central and South America. In Barros, VR et al. (eds), Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, pp. 1499–1566.Google Scholar
McIver, JD (1991) Dispersed central place foraging in Australian meat ants. Insectes Sociaux 38, 129–137.CrossRefGoogle Scholar
Melo, Y, Machado, SR and Alves, M (2010) Anatomy of extrafloral nectaries in Fabaceae from dry-seasonal forest in Brazil. Botanical Journal of the Linnean Society 163, 87–98.CrossRefGoogle Scholar
Murcia, C (1995) Edge effects in fragmented forests: implications for conservation. Trends in Ecology and Evolution 10, 58–62.CrossRefGoogle ScholarPubMed
Murray, JM (1938) An investigation of the interrelationships of the vegetation, soils and termites. South African Journal of Science 35, 288–297.Google Scholar
Nichol, P and Hall, L (1988) Characteristics of nectar secretion by extrafloral nectaries of Ricinus communis. Journal of Experimental Botany 39, 573–586.CrossRefGoogle Scholar
Oliveira, FMP, Andersen, NA, Arnan, X, Ribeiro-Neto, JD, Arcoverde, GB and Leal, IR (2019) Effects of increasing aridity and chronic anthropogenic disturbance on seed dispersal by ants in Brazilian Caatinga. Journal of Animal Ecology, in press.CrossRefGoogle ScholarPubMed
Orians, GH and Pearson, NE (1979) On the theory of central place foraging. In Horn, DJ, Mitchell, RD and Stairs, GR (eds), Analysis of Ecological Systems. Columbus, OH: Ohio State University Press, pp. 155–177.Google Scholar
Oster, GF and Wilson, EO (1978) Caste and Ecology in the Social Insects. Princeton, NJ: Princeton University PressGoogle ScholarPubMed
Pacini, E, Nepi, M and Vesprini, JL (2003) Nectar biodiversity: a short review. Plant Systematic Evolution 238, 7–21.CrossRefGoogle Scholar
Pennington, RT, Lavin, M and Oliveira-Filho, A (2009) Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology, Evolution, and Systematics 40, 437–457.CrossRefGoogle Scholar
Pfeiffer, M and Linsenmair, KE (1998) Polydomy and the organization of foraging in a colony of the Malaysian giant ant Camponotus gigas (Hym./Form.). Oecologia 117, 579–590.Google Scholar
Potts, SG, Vulliamy, B, Dafni, A, Ne’eman, G, O’Toole, C, Roberts, S and Willmer, P (2003) Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure. Oikos 101, 103–112.CrossRefGoogle Scholar
Pyke, GH, Pulliam, HR and Charnov, EL (1977) Optimal foraging: a selective review of theory and tests. Quarterly Review of Biology 52, 137–154.CrossRefGoogle Scholar
Reis, DQA (2016) Influência de perturbações antrópicas crônicas e mudanças climáticas na diversidade estrutural de plantas com nectários extraflorais em uma floresta seca. Master’s Thesis; Universidade Federal de Pernambuco, Recife.Google Scholar
Ribeiro, EMS, Arroyo-Rodríguez, V, Santos, BA, Tabarelli, M and Leal, IR (2015) Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. Journal of Applied Ecology 52, 611–620.CrossRefGoogle Scholar
Rico-Gray, V and Oliveira, PS (2007) The Ecology and Evolution of Ant–Plant Interaction. Chicago, IL: University of Chicago Press.CrossRefGoogle Scholar
Rico-Gray, V, Garcia-Franco, JG, Palacios-Rios, M, Iz-Castelazo, C, Parra-Tabla, V and Navarro, JA (1998) Geographical and seasonal variation in the richness of ant-plant interactions in Mexico. Biotropica 30, 190–200.CrossRefGoogle Scholar
Rito, KF, Arroyo-Rodríguez, V, Queiroz, RT, Leal, IR and Tabarelli, M (2017) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. Journal of Ecology 105, 828–838.CrossRefGoogle Scholar
Rodal, MJN, Sampaio, EVSB, Figueiro, MA and Figueiredo, MA (1992) Manual sobre métodos de estudo florístico e fitossociológico. Brasília, DF: SBB.Google Scholar
Schoener, TW (1971) Theory of feeding strategies. Annual Review of Ecology, Evolution, and Systematics 2, 369–404.CrossRefGoogle Scholar
Schoener, TW (1979) Generality of the size-distance relation in models of optimal feeding. American Naturalist 114, 902–914.CrossRefGoogle Scholar
Silva, JD, Tabarelli, M, Fonseca, MD and Lins, LV (2004) Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Brasília, DF: Universidade Federal de Pernambuco.Google Scholar
Silva, JMC, Leal, IR and Tabarelli, M (2017) Caatinga: The Largest Tropical Dry Forest Region in South America. Cham: Springer.CrossRefGoogle Scholar
Singh, SP (1998) Chronic disturbance: a principal cause of environmental degradation in developing countries. Environmental Conservation 25, 1–2.Google Scholar
Siqueira, FFS, Ribeiro-Neto, JD, Tabarelli, M, Andersen, AN and Wirth, R, Leal, IR (2017) Leaf-cutting ant populations profit from human disturbances in tropical dry forest in Brazil. Journal of Tropical Ecology 33, 337–344.CrossRefGoogle Scholar
Sociedade Nordestina de Ecologia (2002) Projeto técnico para a criação do Parque Nacional do Catimbau/PE. Recife.Google Scholar
Stephens, DW and Krebs, JR (1986) Foraging Theory. Princeton, NJ: Princeton University Press.Google Scholar
Traniello, JFA (1989) Foraging strategies of ants. Annual Review of Entomology 34, 191–210.CrossRefGoogle Scholar
Van Wilgenburg, E and Elgar, MA (2007) Colony characteristics influence the risk of nest predation of a polydomous ant by a monotreme. Biological Journal of the Linnean Society 92, 1–8.CrossRefGoogle Scholar
Wagner, D and Fleur Nicklen, E (2010) Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: does extrafloral nectar attract ant nests and thereby enhance plant nutrition? Journal of Ecology 98, 614–624.CrossRefGoogle Scholar
Weber, MG and Keeler, KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Annals of Botany 111, 1251–1261.CrossRefGoogle ScholarPubMed
Whitford, WG, Martinez-Turanzas, G and Martinez-Meza, E (1995) Persistence of decertified ecosystems: explanations and implications. Environmental Monitoring and Assessment 37, 319–332.CrossRefGoogle Scholar
Zhang, S, Zhang, Y and Keming, MA (2015) The equal effectiveness of different defensive strategies. Scientific Reports 5, Art. no. 13049.Google ScholarPubMed