Vascular epiphytes and host trees of ant-gardens in an anthropic landscape in southeastern Mexico

Abstract

Ant-gardens (AGs) are considered one of the most complex mutualist systems between ants and plants, since interactions involving dispersal, protection, and nutrition occur simultaneously in them; however, little is known about the effects of the transformation of ecosystems on their diversity and interactions. In five environments with different land use within an anthropic landscape in southeastern Mexico, we investigated the diversity and composition of epiphytes and host trees of AGs built by Azteca gnava. A total of 10,871 individuals of 26 epiphytic species, associating with 859 AGs located in 161 host trees, were recorded. The diversity and composition of epiphytes tended to be different between environments; however, Aechmea tillandsioides and Codonanthe uleana were the most important species and considered true AG epiphytes, because they were the most frequent, abundant, and occurred exclusively in AGs. Other important species were the orchids Epidendrum flexuosum, Coryanthes picturata, and Epidendrum pachyrachis, and should also be considered true AG epiphytes, because they occurred almost exclusively in the AGs. The AG abundance in agroforestry plantations was similar or even greater than in riparian vegetation (natural habitat). The AGs were registered in 37 host species but were more frequent in Mangifera indica and Citrus sinensis. We conclude that true epiphytes of A. gnava AGs persist in different environments and host trees, and even these AGs could proliferate in agroforestry plantations of anthropic landscapes.

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References

  1. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol S 38:567–593. doi:10.1146/annurev.ecolsys.38.091206.095818

    Article  Google Scholar 

  2. Blüthgen N, Verhaagh M, Goitía W, Jaffé K, Morawetz W, Barthlott W (2000) How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229–240. doi:10.1007/s004420000449

    Article  PubMed  Google Scholar 

  3. Callaway RM, Reinhart KO, Moore GW, Moore DJ, Pennings SC (2002) Epiphyte host preferences and host traits: mechanisms for species-specific interactions. Oecologia 132:221–230. doi:10.2307/4223331

    Article  Google Scholar 

  4. Catling PM (1995) Evidence for partitioning of Belezean ant nest substrate by a characteristic flora. Biotropica 27:535–537

    Article  Google Scholar 

  5. Catling PM (1997) Influence of aerial Azteca nests on the epiphyte community of some Belizean orange orchards. Biotropica 29:237–242

    Article  Google Scholar 

  6. Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. doi:10.1890/11-1952.1

    Article  PubMed  Google Scholar 

  7. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. doi:10.1890/13-0133.1

    Article  Google Scholar 

  8. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x

    Article  Google Scholar 

  9. Clarke KR, Gorley RN (2015) PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth

    Google Scholar 

  10. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org. Accessed April 2015

    Google Scholar 

  11. Davidson DW (1988) Ecological studies of neotropical ant gardens. Ecology 69:1138–1152. doi:10.2307/1941268

    Article  Google Scholar 

  12. De Beenhouwer M, Aerts R, Honnay O (2013) A global meta-analysis of the biodiversity and ecosystem service benefits of coffee and cacao agroforestry. Agric Ecosyst Environ 175:1–7. doi:10.1016/j.agee.2013.05.003

    Article  Google Scholar 

  13. Dejean A, Corbara B, Snelling RR, Belin M (1997) Les jardins de fourmis de Guyane française: relations entre arbres-supports, épiphytes et fourmis. Acta Bot Gallica 144:333–345. doi:10.1080/12538078.1997.10515378

    Article  Google Scholar 

  14. Dejean A, Corbara B, Orivel J, Snelling RR, Delabie JHC, Belin-Depoux M (2000) The importance of ant gardens in the pioneer vegetal formations of French Guiana (hymenoptera: Formicidae). Sociobiology 35:425–440

    Google Scholar 

  15. Dejean A, Corbara B, Orivel J, Leponce M (2007) Rainforest canopy ants: the implications of territoriality and predatory behavior. Funct Ecosyst Commun 1:105–120

    Google Scholar 

  16. Delabie JHC (1990) The ant problems of cocoa farms in Brazil. In: Vandermeer RK, Jaffé K, Cedeno A (eds) Applied myrmecology: a world perspective. Westview Press, Colorado, pp. 555–569

    Google Scholar 

  17. Denis D, Orivel J, Hora RR, Chameron S, Fresneau D (2006) First record of polydomy in a monogynous ponerine ant: a means to allow emigration between Pachycondyla goeldii nests. J Insect Behav 19:279–291. doi:10.1007/s10905-006-9024-5

    Article  Google Scholar 

  18. Díaz-Padilla G, Ruiz-Corral JA, Medina-García G, Cano-García MA, Serrano-Altamirano V (2006) Estadísticas climáticas básicas del estado de Tabasco (Período 1961–2003). INIFAP-CIRGOC, Veracruz

    Google Scholar 

  19. Floren A, Wetzel W, Staab M (2014) The contribution of canopy species to overall ant diversity (hymenoptera: Formicidae) in temperate and tropical ecosystems. Myrmecol News 19:65–74

  20. Flores-Palacios A, García-Franco JG (2001) Sampling methods for vascular epiphytes: their effectiveness in recording species richness and frequency. Selbyana 22:181–191

    Google Scholar 

  21. Giraudoux P (2015) pgirmess: data analysis in ecology. R package version 1.6.2. http://CRAN.R-project.org/package=pgirmess. Accessed April 2015

  22. Gradstein SR, Nadkarni NM, Kromer T, Holz I, Nöske N (2003) A protocol for rapid and representative sampling of vascular and non-vascular epiphyte diversity of tropical rain forests. Selbyana 24:105–111

    Google Scholar 

  23. Haberman SJ (1973) The analysis of residuals in cross-classified tables. Biometrics 29:205–220

    Article  Google Scholar 

  24. Haddad NM, Brudvig LA, Clobert J et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1. doi:10.1126/sciadv.1500052

  25. Hágsater E, Soto-Arenas MÁ, Salazar GA, Jiménez-Machorro R, López-Rosas M, Dressler R (2005) Las orquídeas de México. Instituto Chinoín, Ciudad de México

    Google Scholar 

  26. Holtum JM, Winter K (2005) Carbon isotope composition of canopy leaves in a tropical forest in Panama throughout a seasonal cycle. Trees 19:545–551. doi:10.1007/s00468-005-0413-8

    CAS  Article  Google Scholar 

  27. Hsieh TC, Ma KH, Chao A (2013) iNEXT online: interpolation and extrapolation Version 1.0. http://chao.stat.nthu.edu.tw/blog/software-download. Accessed July 2015

  28. Johansson D (1974) Ecology of vascular epiphytes in West African rain forest. Acta Phytogeogr Suec 59:1–136

    Google Scholar 

  29. Jost L (2006) Entropy and diversity. Oikos 113:363–375. doi:10.1111/j.2006.0030-1299.14714.x

    Article  Google Scholar 

  30. Kaufmann E, Maschwitz U (2006) Ant-gardens of tropical Asian rainforests. Naturwissenschaften 93:216–227. doi:10.1007/s00114-005-0081-y

    CAS  Article  PubMed  Google Scholar 

  31. Kaufmann E, Weissflog A, Hashim R, Maschwitz U (2001) Ant-gardens on the giant bamboo Gigantochloa scortechinii (Poaceae) in West-Malaysia. Insect Soc 48:125–133. doi:10.1007/pl00001754

    Article  Google Scholar 

  32. Kleinfeldt SE (1978) Ant-gardens: the interaction of Codonanthe crassifolia (Gesneriaceae) and Crematogaster longispina (Formicidae). Ecology 59:449–456. doi:10.2307/1936574

    Article  Google Scholar 

  33. Kreft H, Köster N, Küper W, Nieder J, Barthlott W (2004) Diversity and biogeography of vascular epiphytes in Western Amazonia, Yasuní, Ecuador. J Biogeogr 31:1463–1476. doi:10.1111/j.1365-2699.2004.01083.x

    Article  Google Scholar 

  34. Krömer T, Kessler M, Gradstein SR, Acebey A (2005) Diversity patterns of vascular epiphytes along an elevational gradient in the Andes. J Biogeogr 32:1799–1809. doi:10.1111/j.1365-2699.2005.01318.x

    Article  Google Scholar 

  35. Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129. doi:10.1007/bf02289694

    Article  Google Scholar 

  36. Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29:107–116. doi:10.1016/j.tree.2013.12.001

    Article  PubMed  Google Scholar 

  37. Longino JT (1986) Ants provide substrate for epiphytes. Selbyana 9:100–103

    Google Scholar 

  38. Longino JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491:1–63

    Google Scholar 

  39. Madison M (1979) Additional observations on ant-gardens in Amazonas. Selbyana 5:107–115

    Google Scholar 

  40. Marini-Filho OJ (1999) Distribution, composition, and dispersal of ant gardens and tending ants in three kinds of central Amazonian habitats. Trop Zool 12:289–296

    Article  Google Scholar 

  41. Martínez-Meléndez N, Pérez-Farrera MA, Flores-Palacios A (2008) Estratificación vertical y preferencia de hospedero de las epífitas vasculares de un bosque nublado de Chiapas, México. Rev Biol Trop 56:2069–2086

    Google Scholar 

  42. Mayer VE, Frederickson ME, McKey D, Blatrix R (2014) Current issues in the evolutionary ecology of ant-plant symbioses. New Phytol 202:749–764. doi:10.1111/nph.12690

    Article  PubMed  Google Scholar 

  43. Meyer D, Zeileis A, Hornik K (2015) vcd: visualizing categorical data. R package version 1:4–2 http://CRAN.R-project.org/package=vcd. Accessed April 2015

    Google Scholar 

  44. Morales-Linares J (2012) Diversidad y conservación de orquídeas en plantaciones de cacao del sureste de México. Dissertation, Instituto de Ecología, A.C.

  45. Mougi A, Kondoh M (2012) Diversity of interaction types and ecological community stability. Science 337:349–351. doi:10.1126/science.1220529

    CAS  Article  PubMed  Google Scholar 

  46. Mueller-Dombois D, Ellenberg H (1974) Aims and methods of vegetation ecology. John Wiley & Sons, New York

    Google Scholar 

  47. Nieder J, Engwald S, Klawun M, Barthlott W (2000) Spatial distribution of vascular epiphytes (including Hemiepiphytes) in a lowland amazonian rain forest (Surumoni rane plot) of southern Venezuela. Biotropica 32:385–396. doi:10.1111/j.1744-7429.2000.tb00485.x

    Article  Google Scholar 

  48. Nieder J, Prosperí J, Michaloud G (2001) Epiphytes and their contribution to canopy diversity. Plant Ecol 153:51–63. doi:10.1023/a:1017517119305

    Article  Google Scholar 

  49. Offenberg J (2015) Review: ants as tools in sustainable agriculture. J Appl Ecol 52:1197–1205. doi:10.1111/1365-2664.12496

    Article  Google Scholar 

  50. Oksanen J et al (2015) Vegan: community ecology package. R package version 2:3 http://CRAN.R-project.org/package=vegan. Accessed April 2015

    Google Scholar 

  51. Orivel J, Dejean A (1999) Selection of epiphyte seeds by ant-garden ants. Ecoscience 6:51–55

    Google Scholar 

  52. Orivel J, Leroy C (2011) The diversity and ecology of ant gardens (Hymenoptera: Formicidae; Spermatophyta: Angiospermae). Myrmecol News 14:73–85

  53. Paolucci LN, Solar RRC, Leal LC (2016) Proximity shapes similarity in epiphytic composition of Neotropical ant gardens. J Trop Ecol 32:325–329. doi:10.1017/S0266467416000298

    Article  Google Scholar 

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

    Book  Google Scholar 

  55. Salazar-Conde E, Zavala-Cruz J, Castillo-Acosta O, Cámara-Artigas R (2004) Evaluación espacial y temporal de la vegetación de la Sierra Madrigal, Tabasco, México (1973–2003). Inv Geo Bol Inst Geo UNAM 54:7–23

  56. Sanford WW (1968) Distribution of epiphytic orchids in semi-deciduous tropical forest in southern Nigeria. J Ecol 56:697–705

    Article  Google Scholar 

  57. Schmit-Neuerburg V, Blüthgen N (2007) Ant-garden epiphytes are protected against drought in a Venezuelan lowland rain forest. Ecotropica 13:93–100

    Google Scholar 

  58. Vandermeer J, Perfecto I, Philpott S (2010) Ecological complexity and pest control in organic coffee production: uncovering an autonomous ecosystem service. Bioscience 60:527–537. doi:10.1525/bio.2010.60.7.8

    Article  Google Scholar 

  59. Vantaux A, Dejean A, Dor A, Orivel J (2007) Parasitism versus mutualism in the ant-garden parabiosis between Camponotus femoratus and Crematogaster levior. Insect Soc 54:95–99. doi:10.1007/s00040-007-0914-0

    Article  Google Scholar 

  60. Vásquez-Bolaños M (2015) Taxonomía de Formicidae (Hymenoptera) para México. Métodos en Ecología y Sistemática 10:1–53

    Google Scholar 

  61. Wolda H (1981) Similarity indices, sample size and diversity. Oecologia 50:296–302. doi:10.1007/BF00344966

    Article  Google Scholar 

  62. Woods CL, Cardelús CL, DeWalt SJ (2015) Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J Ecol 103:421–430. doi:10.1111/1365-2745.12357

    Article  Google Scholar 

  63. Youngsteadt E, Baca JA, Osborne J, Schal C (2009) Species-specific seed dispersal in an obligate ant-plant mutualism. PLoS One 4:e4335. doi:10.1371/journal.pone.0004335

    Article  PubMed  PubMed Central  Google Scholar 

  64. Yu DW (1994) The structural role of epiphytes in ant gardens. Biotropica 26:222–226

    Article  Google Scholar 

  65. Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

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Acknowledgements

Thanks to Thomas Castellanos Gómez and Darvelio Alvarado Gómez for the assistance in the field, and to Luis Quiróz Robledo, Gibrán Pérez, and Dora L. Martínez Tlapa for their support in the identification and assembly of the ants. We also thank to Michelle Ramos Robles and Rosario Landgrave Ramírez for their support to elaborate Fig. 1, and to Miguel Á. García Martínez for his comments on the analysis of similarity of species. María E. Sánchez Salazar contributed with the English translation of the manuscript. The first author was supported by a CONACYT fellowship (No. 250340) and INECOL (20030-10144). We also appreciate the suggestions made to the manuscript by four anonymous reviewers.

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Correspondence to Jonas Morales-Linares.

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Communicated by: Alain Dejean

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Morales-Linares, J., García-Franco, J.G., Flores-Palacios, A. et al. Vascular epiphytes and host trees of ant-gardens in an anthropic landscape in southeastern Mexico. Sci Nat 103, 96 (2016). https://doi.org/10.1007/s00114-016-1421-9

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Keywords

  • Agroforestry plantations
  • Chiapas, diversity
  • Riparian vegetation
  • Species composition
  • Tabasco