ABSTRACT
Ants can use twigs from fragments of tree branches as a nesting resource. The present study analyzed gatherings of ants in twigs of Albizia niopoides, a Fabaceae native to the Atlantic Forest that is used in landscaping in parks and squares in Brazil. Expeditions were performed in an urban park located in Atlantic Forest areas between February and June 2014. A total of 70 twigs with ants were collected and included 9357 workers, 2309 broods ants, 68 winged ants and 19 queens. Four subfamilies, 10 genera and 17 species/morphospecies were recorded. The species with the largest number of nests were Nylanderia sp.1, Hypoponera sp.4, and Wasmannia auropunctata. Ants of different species were found coexisting in the same twig, and Pheidole gr. tristis was the most common species found sharing a nest. Among the species recorded, only Pseudomyrmex gracilis and P. phyllophilus are arboreal; the others also live in litter. For some species, our results indicate that the twig occupation in the litter can be structured and not by chance. No correlation was found between the twig structure and the colony components.
Keywords:
Communities; Nesting; Urban park; Transient nests; Atlantic Forest
Albizia niopoides (Spruce ex Benth.) Burkart (Fabaceae: Mimosoideae) is found in tropical and subtropical areas of Brazil. It is a deciduous tree that reaches up to 35 m in height and 40–60 cm diameter at breast height (DBH), but its wood has low market value (Rossi and Sartoretto, 2014Rossi, E., Sartoretto, L.M., 2014. Propagação in vitro da farinha-seca. Pesq. Florest. Bras. 33, 45-52.). In ecological succession, it is classified as pioneer to early or late secondary and is frequently found in pastures because it does not develop under the canopy shade (Lorenzi, 2002Lorenzi, H., 2002. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 4th ed. Instituto Plantarum de Estudos da Flora.; Arce et al., 2008Arce, M.L.R., Gale, S.L., Maxted, N., 2008. A taxonomic study of Albizia (Leguminosae: Mimosoideae: Ingeae) in Mexico and Central America. An. Jardín Bot. Madrid 65, 255-305.). In urban areas, it is used in squares and parks; it has as a marked characteristic a smooth and powdery external bark, often showing holes made by wood boring beetles (Carvalho, 2009Carvalho, P.E.R., 2009. Comunicado técnico: farinha-seca Albizia niopoides. Embrapa Florestas 2, 1-8.).
Usually, ants cannot excavate plant tissue to build their nests in tree twigs, with the exception of some Pseudomyrmex and Azteca species, which can bore into tree trunks when the plant is still young (Hölldobler and Wilson, 1990Hölldobler, B., Wilson, E.O., 1990. The Ants. Harvard University Press, Cambridge, MA, pp. 732.). Ants, including arboreal species, typically use cavities made by wood boring insects to maintain and expand their colonies (Deyrup et al., 2000Deyrup, M., Davis, L., Cover, S., 2000. Exotic ants in Florida. Trans. Am. Entomol. Soc. 3, 293-326.). In the tropics, ants build their nests in different microhabitats, such as vegetation (arboreal ants), soil, and litter; other areas include under rocks, termite nests, twigs or trunks in different decomposition stages, dead vegetation, dry fruits, and galls (Hölldobler and Wilson, 1990Hölldobler, B., Wilson, E.O., 1990. The Ants. Harvard University Press, Cambridge, MA, pp. 732.; Byrne, 1994Byrne, M.M., 1994. Ecology of twig-dwelling ants in a wet lowland tropical forest. Biotropica 26, 61-72.; Cereto et al., 2011Cereto, C.E., Schmidt, G.O., Martins, A.G., Castellani, T.T., Lopes, B.C., 2011. Nesting of ants (Hymenoptera, Formicidae) in dead post-reproductive plants of Actinocephalus polyanthus (Eriocaulaceae), a herb of coastal dunes in southern Brazil. Insectes Soc. 58, 469-471.; Nakano et al., 2012Nakano, M.A., Feitosa, R.M., Moraes, C.O., Adriano, L.D.C., Hengles, E.P., Longui, E.L., Morini, M.S.C., 2012. Assembly of Myrmelachista Roger (Formicidae: Formicinae) in twigs fallen on the leaf litter of Brazilian Atlantic Forest. J. Nat. Hist. 1, 1-13.; Almeida et al., 2014Almeida, M.F.B., Santos, L.R., Carneiro, M.A., 2014. Senescent stem-galls in trees of Eremanthus erythropappus as a resource for arboreal ants. Rev. Bras. Entomol. 58, 265-272.). Many such places serve as peripheral nests for protection or to search for resources (Lanan et al., 2012Lanan, M.C., Dornhaus, A., Jones, E.I., Waser, A., Bronstein, J.L., 2012. The trail less traveled: individual decision-making and its effect on group behavior. PLoS ONE 7, 1-10.).
The twigs resulting from the fragmentation of tree branches represent a resource for many arboreal or litter ants (Carvalho and Vasconcelos, 2002Carvalho, K.S., Vasconcelos, H.L., 2002. Comunidade de formigas que nidificam em pequenos galhos da serrapilheira em floresta da Amazônia Central, Brasil. Rev. Bras. Entomol. 46, 115-121.; Fernandes et al., 2012Fernandes, T.T., Silva, R.R., Souza, D.R., Araújo, N., Morini, M.S.C., 2012. Undecomposed twigs in the leaf litter as nest-building resources for ants (Hymenoptera: Formicidae) in areas of the Atlantic Forest in the southeastern region of Brazil. Psyche (Stuttg.) 2012, 1-8.; Nakano et al., 2012Nakano, M.A., Feitosa, R.M., Moraes, C.O., Adriano, L.D.C., Hengles, E.P., Longui, E.L., Morini, M.S.C., 2012. Assembly of Myrmelachista Roger (Formicidae: Formicinae) in twigs fallen on the leaf litter of Brazilian Atlantic Forest. J. Nat. Hist. 1, 1-13.) and contribute to the maintenance of species diversity in tropical forests (Armbrecht et al., 2004Armbrecht, I., Perfecto, I., Vandermeer, J., 2004. Enigmatic biodiversity correlations: ant diversity responds to diverse resources. Science 304, 284-286.). The present study recorded ant communities that use A. niopoides twigs as a nesting resource. In addition, we discuss the relationship between the structure of the twig, the abundance and the morphological characters of individuals of the colony.
Five collection expeditions were conducted between February and June 2014 in the Max Feffer City Park. This area is an urban park that belongs to the town of Suzano (S 23°31'57"; W 46°19'24") in the state of São Paulo, Brazil. The original vegetation is Atlantic Forest and is currently permeated by exotic species and an isolated grove (0.5 ha) composed only of 50 individuals of A. niopoides (DBH = 43.88 cm; SD = 6.44 cm). All twigs in the area were inspected, but we collected only those with ants in the area of A. niopoides and individually placed in plastic bags. The sampling effort lasted for 4 h and was performed by two individuals at each collection event. To characterize the structure of the twig, it were measured the diameter, length, and total area. The diameter was obtained with a digital caliper, and the length was obtained with a simple ruler. The total area was calculated using the formula: At =twigs 2πr (r + h), where At = total area, r = radius, and h = twig length. We opened each twig and adult and broods (eggs + larvae) ants were counted. We defined the presence of a colony on a twig when the number of workers was 10 or more or when broods ants were present on the twig (Fernandes et al., 2012Fernandes, T.T., Silva, R.R., Souza, D.R., Araújo, N., Morini, M.S.C., 2012. Undecomposed twigs in the leaf litter as nest-building resources for ants (Hymenoptera: Formicidae) in areas of the Atlantic Forest in the southeastern region of Brazil. Psyche (Stuttg.) 2012, 1-8.); except when the nest was shared by two species of ants. It were measured head width, head length, and Weber's length (Silva and Brandão, 2010Silva, R.R., Brandão, C.R.F., 2010. Morphological patterns and community organization in leaf-litter assemblages. Ecol. Monogr. 80, 107-124.). We chose only those species with ≥5 nests, being measured three to five workers per nest. Ants were separated into subfamilies (Brady et al., 2014Brady, S.G., Fisher, B.L., Schultz, T.R., Ward, P.S., 2014. The rise of army ants and their relatives: diversification of specialized predatory doryline ants. BMC Evol. Biol. 14, 93.) and identified at the genus (Palacio and Fernández, 2003Palacio, E.E., Fernández, F., 2003. Claves para las subfamilias y gêneros. In: Fernández, F. (Ed.), Introducción a las hormigas de la región Neotropical. Instituto de Investigación de Recursos Biológicos Alexander Von Humboldt, Bogotá, pp. 233–260.) and species level, and morphospecies were named according to Suguituru et al. (2015)Suguituru, S.S., Morini, M.S.C., Feitosa, R.M., Silva, R.R., 2015. Formigas do Alto Tietê. Canal 6, Bauru http://canal6.com.br/formigas/.
http://canal6.com.br/formigas/...
. The vouchers were deposited at Mogi das Cruzes University (SP). Spearman correlations were used to assess the relationship between colony demographics (number of workers, broods or both), twig structure (diameter, length, and area) and character (head width, head length, and Weber's length). In all analyses, it was used the BioEstat 5.0 software (Ayres et al., 2007Ayres, M., Ayres, M., Ayres, D.L., Santos, A.A.S., 2007. BioEstat: aplicações estatísticas nas áreas das ciências bio-médicas. Version 5. Instituto de Desenvolvimento Sustentável Mamirauá, Pará, pp. 291.).
It was collected a total of 70 twigs, 9357 workers, 2309 broods ants, 68 winged ants, and 19 queens. It were registered four subfamilies, 10 genera, and 17 species/morphospecies. The species with the highest number of nests was Nylanderia sp.1 (20), followed by Hypoponera sp.4 (12) and Wasmannia auropunctata (Roger, 1863) (7). The colonies with the highest numbers of workers in total belonged to W. auropunctata (4257; mean: 608.14), Nylanderia sp.1 (2134; mean: 106.7), and Pheidole gr. tristis (1035; mean: 172.5). The twigs were an average of 1.04 cm in diameter (SD = 0.27 cm), 23.13 cm in length (SD = 11.32 cm), and 77.69 cm2 in area (SD = 42.75 cm2). It were found four winged species; Nylanderia sp.1 showed the highest number of winged ants/colony, including more than one queen per nest (Table 1).
Demographic data of ant colonies registered in A. niopoides twigs in the Atlantic Forest in southeast Brazil and the twig structure of the twigs.
It were also recorded nests shared by more than one species, and the presence of broods ants was noted. Pheidole gr. tristis was the species that most frequently shared nests, and Crematogaster arata (Emery, 1906) shared nests with two other species (Table 2); the species were sharing a single cavity. Only Pseudomyrmex gracilis (Fabricius, 1804) and P. phyllophilus (Smith, 1858) (Hymenoptera: Formicidae) are considered arboreal species. No relationship was found between colony demographics and twig structure (Table 3). Yet the nest size is related to the amount of components of the colony (Hölldobler and Wilson, 1990Hölldobler, B., Wilson, E.O., 1990. The Ants. Harvard University Press, Cambridge, MA, pp. 732.). One colonization strategy for ants that nest in twigs is to expand from the main nest featuring polydomic nests (Carvalho and Vasconcelos, 2002Carvalho, K.S., Vasconcelos, H.L., 2002. Comunidade de formigas que nidificam em pequenos galhos da serrapilheira em floresta da Amazônia Central, Brasil. Rev. Bras. Entomol. 46, 115-121.). Thus, we believe that the lack of correlation between the structure of the nest and the colony demographics is related to this strategy, since the presence of polydomic nests may account for most of the species recorded in this study, as workers and broods ants were observed (Debout et al., 2007Debout, G., Schatz, B., Elias, M., McKey, D., 2007. Polydomy in ants: what we know, what we think we know, and what remains to be done. Biol. J. Linn. Soc. 90, 319-348.; Lanan et al., 2011Lanan, M.C., Dornhaus, A., Bronstein, J.L., 2011. The function of polydomy: the ant Crematogaster torosa preferentially forms new nests near food sources and fortifies outstations. Behav. Ecol. Sociobiol. 65, 959-968.). Polydomy is fairly common among ants and has been registered in over 150 species (Debout et al., 2007Debout, G., Schatz, B., Elias, M., McKey, D., 2007. Polydomy in ants: what we know, what we think we know, and what remains to be done. Biol. J. Linn. Soc. 90, 319-348.), among them, Nylanderia, widely recorded in this study. It is an alternative for species for which the available nesting space seems to limit growth, but it is also related to an increase in foraging area (Santos and Del-Claro, 2009Santos, J.C., Del-Claro, K., 2009. Ecology and behaviour of the weaver ant Camponotus (Myrmobrachys) senex. J. Nat. Hist. 43, 1423-1435.; Schmolke, 2009Schmolke, A., 2009. Benefits of dispersed central-place foraging: an individual-based model of a polydomous ant colony. Am. Nat. 173, 772-778.; Lanan et al., 2011Lanan, M.C., Dornhaus, A., Bronstein, J.L., 2011. The function of polydomy: the ant Crematogaster torosa preferentially forms new nests near food sources and fortifies outstations. Behav. Ecol. Sociobiol. 65, 959-968.) or to polygyny (Walin et al., 2001Walin, L., Seppä, P., Sundström, L., 2001. Reproductive allocation within a polygyne, polydomous colony of the ant Myrmica rubra. Ecol. Entomol. 26, 537-546.), which has been verified in P. gracilis and Nylanderia sp.1.
Demographic data of ant species that coexist with other species in Albizia niopoides twigs in the Atlantic Forest in southeast Brazil.
Correlation between colony demographics and structure of the twig dispersed in the litter of urban parks with Albizia niopoides.
The rains represent an important stimulus for the synchronized release of winged species (Torres et al., 2001Torres, J.A., Snelling, R.R., Canals, M., 2001. Seasonal and nocturnal periodicities in ant nuptial flights in the tropics (Hymenoptera: Formicidae). Sociobiology 37, 601-626.; Santos and Del-Claro, 2009Santos, J.C., Del-Claro, K., 2009. Ecology and behaviour of the weaver ant Camponotus (Myrmobrachys) senex. J. Nat. Hist. 43, 1423-1435.), but despite the field expeditions being conducted in months considered rainy (Minuzzi et al., 2007Minuzzi, R.B., Sediyama, G.C., Barbosa, E.M., Melo Jr., J.C.F., 2007. Climatologia do comportamento do período chuvoso da região sudeste do Brasil. Rev. Bras. Meteorol. 22, 338-344.), few species were recorded as winged. The results indicate that Nylanderia sp.1 has a longer period of winged production, which can be a cause of the abundance of the genus in the tropics (LaPolla et al., 2011LaPolla, J.S., Brady, S.G., Shattuck, S.O., 2011. Monograph of Nylanderia of the world: an introduction to the systematics and biology of the genus. Zootaxa 3110, 1-9.).
With exception of the arboreal species, all of the other species recorded in the present study forage on the soil or on the soil-litter system of the Atlantic Forest (Suguituru et al., 2013Suguituru, S.S., Souza, D.R., Munhae, C.D.B., Pacheco, R., Morini, M.S.C., 2013. Diversidade e riqueza de formigas (Hymenoptera: Formicidae) em remanescentes de Mata Atlântica na Bacia Hidrográfica do Alto Tietê, SP, Brazil. Biota Neotrop. 13, 1-8., 2015Suguituru, S.S., Morini, M.S.C., Feitosa, R.M., Silva, R.R., 2015. Formigas do Alto Tietê. Canal 6, Bauru http://canal6.com.br/formigas/.
http://canal6.com.br/formigas/...
). For some species, our results indicate that this occupation can be structured and not by chance (Table 4).
Correlation between morphological characters of ants and structure of the twig of Albizia niopoides.
These ants are also found in dead Actinocephalus polyanthus (Bong) (Eriocaulaceae) plants in areas of sandbanks (Cereto et al., 2011Cereto, C.E., Schmidt, G.O., Martins, A.G., Castellani, T.T., Lopes, B.C., 2011. Nesting of ants (Hymenoptera, Formicidae) in dead post-reproductive plants of Actinocephalus polyanthus (Eriocaulaceae), a herb of coastal dunes in southern Brazil. Insectes Soc. 58, 469-471.), disperse twigs in the litter of Eucalyptus sp. and other trees (Carvalho and Vasconcelos, 2002Carvalho, K.S., Vasconcelos, H.L., 2002. Comunidade de formigas que nidificam em pequenos galhos da serrapilheira em floresta da Amazônia Central, Brasil. Rev. Bras. Entomol. 46, 115-121.; Fernandes et al., 2012Fernandes, T.T., Silva, R.R., Souza, D.R., Araújo, N., Morini, M.S.C., 2012. Undecomposed twigs in the leaf litter as nest-building resources for ants (Hymenoptera: Formicidae) in areas of the Atlantic Forest in the southeastern region of Brazil. Psyche (Stuttg.) 2012, 1-8.; Souza et al., 2012Souza, D.R., Fernandes, T.T., Nascimento, J.R.O., Suguituru, S.S., Morini, M.S.C., 2012. Characterization of ant communities (Hymenoptera: Formicidae) in twigs in the leaf litter of the Atlantic Rainforest and Eucalyptus trees in the southeast region of Brazil. Psyche (Stuttg.) 2012, 1-12.), and bamboo compartments (Fagundes et al., 2010Fagundes, R., Terra, G., Ribeiro, S.P., Majer, J.D., 2010. The bamboo Merostachys fischeriana (Bambusoideae: Bambuseae) as a canopy habitat for ants of Neotropical Montane Forest. Neotrop. Entomol. 39, 906-911.). Regarding the two arboreal species, there is the possibility that the twig already housed the colony when it fell, as Ketterl et al. (2003)Ketterl, J., Verhaagh, M., Bihn, J.H., Brandão, C.R.F., Engels, W., 2003. Spectrum of ants associated with Araucaria angustifolia trees and their relations to hemipteran trophobionts. Stud. Neotrop. Fauna Environ. 38, 199-206. described the presence of P. phyllophilus in Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae) as well as in twigs that have fallen close to the tree.
Is very common to find colonies of different species on a single plant, but not on same twig (Byrne, 1994Byrne, M.M., 1994. Ecology of twig-dwelling ants in a wet lowland tropical forest. Biotropica 26, 61-72.) and herbs (Cereto et al., 2011Cereto, C.E., Schmidt, G.O., Martins, A.G., Castellani, T.T., Lopes, B.C., 2011. Nesting of ants (Hymenoptera, Formicidae) in dead post-reproductive plants of Actinocephalus polyanthus (Eriocaulaceae), a herb of coastal dunes in southern Brazil. Insectes Soc. 58, 469-471.). Cereto et al. (2011)Cereto, C.E., Schmidt, G.O., Martins, A.G., Castellani, T.T., Lopes, B.C., 2011. Nesting of ants (Hymenoptera, Formicidae) in dead post-reproductive plants of Actinocephalus polyanthus (Eriocaulaceae), a herb of coastal dunes in southern Brazil. Insectes Soc. 58, 469-471. observed colonies of four species in the same plant but with a compartmentalized distribution in the plant. Ants of different species recorded in the present study were observed in the same cavity of the twig without forming individual clusters, suggesting that these species share the same nesting space. Twigs are transient resources, because besides the decomposition process (Byrne, 1994Byrne, M.M., 1994. Ecology of twig-dwelling ants in a wet lowland tropical forest. Biotropica 26, 61-72.), the ants with simpler nests (as twigs) move more often than those with more complex nests (McGlynn, 2012McGlynn, T.P., 2012. The ecology of nest movement in social insects. Annu. Rev. Entomol. 57, 291-308.). So these ants frequently recolonize new spaces (Byrne, 1994Byrne, M.M., 1994. Ecology of twig-dwelling ants in a wet lowland tropical forest. Biotropica 26, 61-72.). The lack of resources, along with the amount of twigs available and with holes accessible to workers, can cause the sharing of nests with other species.
Studies show that the diversity of nesting resources affects the diversity of twig-nesting ants (Armbrecht et al., 2004Armbrecht, I., Perfecto, I., Vandermeer, J., 2004. Enigmatic biodiversity correlations: ant diversity responds to diverse resources. Science 304, 284-286.), and our study shows that a relatively high number of ant species use a single species of plant as a nesting resource. Thus, given the scarcity of resources in urban areas, twigs coming from A. niopoides, which is a plant suitable for afforestation (Carvalho, 2009Carvalho, P.E.R., 2009. Comunicado técnico: farinha-seca Albizia niopoides. Embrapa Florestas 2, 1-8.), represent an alternative to maintaining the diversity of ants in urban areas. We also show that some species can coexist on the same twig. However, the mechanisms for coexistence of adults and immature ants as well as the morphological and behavioral basis still need to be investigated. In addition, there is also a need to study the size of the holes made by wood boring insects and other invertebrates associated with the nest.
Acknowledgments
Thanks to the São Paulo Research Foundation (FAPESP) (Protocol no. 2013/16861-5); the Foundation for the Support of Teaching and Research/University of Mogi das Cruzes (FAEP/UMC), the National Council for Technological and Scientific Development (CNPq) (Protocol no. 302363/2012-2) for their financial support, and the authorization system and information on biodiversity (SISBIO) (Protocol no. 45492). We also would like to thank Gabriela Procópio Camacho, Thiago Sanches R. da Silva, Alexandre Ferreira (Universidade Federal do Paraná) and Lina Maria Pedraza (Instituto de Ciencias Naturales, Bogotá, Colombia) that kindly confirmed the identification of samples, and Renata Jimenez de Almeida-Scabbia (Universidade de Mogi das Cruzes) by identification of Albizia niopoides.
References
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» http://canal6.com.br/formigas/ - Suguituru, S.S., Souza, D.R., Munhae, C.D.B., Pacheco, R., Morini, M.S.C., 2013. Diversidade e riqueza de formigas (Hymenoptera: Formicidae) em remanescentes de Mata Atlântica na Bacia Hidrográfica do Alto Tietê, SP, Brazil. Biota Neotrop. 13, 1-8.
- Torres, J.A., Snelling, R.R., Canals, M., 2001. Seasonal and nocturnal periodicities in ant nuptial flights in the tropics (Hymenoptera: Formicidae). Sociobiology 37, 601-626.
- Walin, L., Seppä, P., Sundström, L., 2001. Reproductive allocation within a polygyne, polydomous colony of the ant Myrmica rubra Ecol. Entomol. 26, 537-546.
Publication Dates
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Publication in this collection
Apr-Jun 2016
History
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Received
16 Sept 2015 -
Accepted
07 Jan 2016