de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Detection, ultrastucture and phylogeny of Sclerorhabditis neotropicalis (Nematoda: Rhabditidae) nematodes associated with the Azteca ant-Cecropia tree symbiosis

Jessica Morera, Geovanni Mora-Pineda, Alejandro Esquivel, Paul Hanson, Adrián Pinto-Tomás



The nematode involved in ant-plant symbioses have been poorly studied, and originated an area of research that is now receiving increasing attention. One example is Sclerorhabditis neotropicalis, that inhabit the nests of Azteca ants in Cecropia trees. The goal of the present study is to increase our knowledge about these organisms and their possible symbiotic relationship with the ants and their host plant. The samples were collected during 2011-2013 in different locations in Costa Rica: Parque Nacional Carara (Puntarenas province), San Pedro de Montes de Oca and Highway 27 (San Jose) and La Selva Biological Station (Sarapiquí, Heredia). We examined 576 internodes from 23 plants, comprising four species of Cecropia (including one non-myrmecophyte) and five Azteca species. S. neotropicalis was found in all but one of the Azteca/Cecropia combinations examined. Queen and worker ants were placed in water in order to dislodge nematodes and the results were largely positive, suggesting that alate queens carry S. neotropicalis between trees and that workers carry them between internodes. In addition to transport, preliminary observations suggest that the ants provide masses of scraped parenchyma (possibly fertilized with feces) as a substrate for bacteria upon which the nematodes presumably feed. We also found S. neotropicalis associated with Azteca in another myrmecophyte, Cordia alliodora, suggesting that this ant/nematode association is not restricted to Cecropia. SEM photographs of S. neotropicalis were provided to supplement the original description of this species, and molecular phylogenetic analyses employing three different markers suggest that Sclerorhabditis forms a well-supported clade of bacteria-feeding nematodes associated with Azteca. Indirect evidence suggests that this is a mutualistic association, but the benefits to the ants remain unknown.


Nematodes; Symbiosis; Electron Microscopy; Cecropia; Azteca; Costa Rica


Agrawal, A. (1998). Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant. Ecology, 79, 2100-2112.

Ahmad, I., Shah, A., & Mahamood, M. (2007). Nematodes of the order Rhabditida from India. Description of Sclerorhabditis tridentatus gen. n., sp. n. (Nematoda: Rhabditidae). Journal of Nematology, 9(1), 43-47.

Altschul, S. F., Madden, T. L., Schäffer, A., A, Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Research, 25, 3389-3402.

Andrássy, I. (1984). Klasse Nematoda (Ordnungen Monhysterida, Desmoscolecida, Araeolaimida, Chromadorida, Rhabditida). Stuttgart: Fischer.

Antweb. (2016). The California Academy of Sciences, San Francisco, U.S.A.

Asghar-Shah, A., & Vaid, S. (2015). Description of Sclerorhabditis miniata n. sp. and first description of male of Diploscapter coronatus Cobb, 1913 (Nematoda: Rhabditidae). Journal of Nematology, 47(2), 153-158.

Bailey, I. W. (1922). Notes on Neotropical ant-plants I. Cecropia angulata, sp. nov. Botanical Gazette, 74, 369-391.

Barnwell, F. H. (1967). Daily patterns in the activity of the arboreal ant Azteca alfari. Journal of Ecology, 48, 991-993.

Berg, C., Franco, C., & Rosselli, P. (2005). Cecropia. Flora Neotropica, 94, 1-230.

Brosius, F. (2013). SPSS 21. MITP-Verlags GmbH & Co. KG.

Brown, F. D., D'Anna, I., & Sommer, R. J. (2011). Host-finding behavior in the nematode Pristionchus pacificus. Proceedings of the Royal Society of London B: Biological Sciences, 278, 3260-3269.

De Maeseneer, J., & D’Herde, J. (1963). Méthodes utilisées pour l’étude des anguillules libres du sol. Revue Agriculture Bruxelles, 16, 441-447.

Dejean, A., Petitclerc, F., Roux, O., Orivel, J., & Leroy, C. (2012). Does exogenic food benefit both partners in an ant-plant mutualism? The case of Cecropia obtusa and its guest Azteca plant-ants. Comptes Renus Biologies, 335, 214-219.

Esquivel, A., Abolafia, J., Hanson, P., & Pinto, A. (2012). A new species of nematode, Sclerorhabditis neotropicalis sp. n. (Rhabditida), associated with Azteca ants in Cecropia obtusifolia. Nematropica, 42(1), 163-169.

González, J., & Rodríguez, A. (2015). Cecropia. In: Hammel B E, Grayum M H, Herrera C, Zamora N (Eds.), Manual de Plantas de Costa Rica, Volumen VIII, Dicotiledóneas (Sabiaceae-Zygophyllaceae)(p. 473-479). Missouri Botanical Garden Press, St. Louis.

Janzen, D. H. (1969). Allelopathy by myrmecophytes: the ant Azteca as an allelopathic agent of Cecropia. Ecology, 50, 147-153.

Jesús-Navarrete, A. (1991). Nemátodos marinos y la actividad petrolera en la Sonda de Campeche. In: Congreso de Ciencias del Mar. Marcuba. 87, 47.

Karnovsky, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology, 27, 137.

Levene, T. (1960). Robust tests for equality of variances. In: Okin (Ed.), Contributions to Probability and Statistics. (p. 278-292). Essays in Honour of Harold Hotelling, Stanford University Press, Palo Alto, California.

Longino, J. T. (1989). Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica. Biotropica, 22(2), 126-132.

Longino, J. T. (1991a). Azteca ants in Cecropia trees: Taxonomy, colony structure, and behavior. In: C. R. Huxley & D. F. Cutler (Eds.). Ant-Plant Interactions. (p. 271-288) Oxford Univ. Press, Oxford.

Longino, J. T. (1991b). Taxonomy of the Cecropia inhabiting Azteca ants. Journal of Natural History, 25, 1571-1602.

Longino, J. T. (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.

Maschwitz, U., Fiala, B., Dumpert, K., Hashim, R., & Sudhaus, W. (2016). Nematode associates and bacteria in ant-tree symbioses. Symbiosis, 69(1), 1-7.

Oliveira, K. N., Coley, P. D., Kursar, T. A., Kaminski, L. A., Moreira, M. Z., & Campos, R. I. (2015). The effect of symbiotic ant colonies on plant growth: a test using an Azteca-Cecropia system. Journal PLOS One, 10(3), 1-13. (Recovered from doi: 10.1371/journal.pone.0120351).

Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D., & Pupko, T. (2010). GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research, 38, 15.

Poinar, G. (2012). Nematode parasites and associates of ants: past and present. Journal Psyche, 25, 1-13.

Rickson, F. R. (1971). Glycogen plastids in Müllerian body cells of Cecropia peltata a higher green plant. Science, 173, 344-347.

Rickson, F. R. (1976). Anatomical development of the leaf trichilium and Müllerian bodies of Cecropia peltata. American Journal of Botany, 63, 1266-1271.

Rocha, C. F., & Bergallo, H. G. (1992). Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs. Coelomera furiicornis on Cecropia pachystachya. Oecologia, 91, 249-252.

Ronquist, F., & Huelsenbeck, J. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.

Sagers, C. L., Ginger, S. M., & Evans, R. D. (2000). Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia, 123, 582-586.

Schupp, E. W. (1986). Azteca protection of Cecropia: ant occupation benefits juvenile trees. Oecologia, 70, 379-385.

Seinhorst, J. W. (1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica, 4, 67-69.

Shapiro, S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). BIometrika, 52, 591-611.

Sidney, S., & Castellan, N. (1988). Nonparametric Statistics for the Behavioral Sciences. Second edition. New York, McGraw-Hill.

Simpson, B. B., Helfgott, D. M., Weeks, A., & Larkin, L. (2004). Species relationships in Krameria (Krameriaceae) based on ITS sequences and morphology: implications for character utility and biogeography. Systematic Botany, 29, 97-108.

Stock, P., Campbell, J. F., & Nadler, S. (2001). Phylogeny of Steinernema travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology, 87, 877-89.

Tamura, K., Dudley, J., & Kumar, S. (2007). MEGA6: Molecular Evolutionary Genetics Analysis (MEGA) software version 6.0. Molecular Biology and Evolution, 24, 1596-1599.

Trimble, S. T., & Sagers, C. L. (2004). Differential host use in two highly specialized ant-plant associations: evidence from stable isotopes. Oecologia, 138, 74-82.

Valverde, J. P., & Hanson, P. (2011). Parenchyma: a neglected plant tissue in the Cecropia/ant mutualism. Symbiosis, 55, 47-51.

Weng, J., Nishida, K., Hanson, P., & LaPierre, L. (2007). Biology of Lissoderes Champion (Coleoptera, Curculionidae) in Cecropia saplings inhabited by Azteca ants. Journal of Natural History, 41(25-28), 1679-1695.

Webster, R., Allison, V. F., Ubelaker, J. E., & Riddle J. M. (1971) Glycerine preparation of nematode material for scanning electron microscopy. Texas Reports on Biology, 29, 433-434.


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