Convergent Structure and Function of Mycelial Galleries in Two Unrelated Neotropical Plant-Ants
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Insect. Soc. DOI 10.1007/s00040-017-0554-y Insectes Sociaux RESEARCH ARTICLE Convergent structure and function of mycelial galleries in two unrelated Neotropical plant-ants V. E. Mayer1 · J. Lauth2 · J. Orivel2 Received: 29 September 2016 / Revised: 10 February 2017 / Accepted: 22 February 2017 © The Author(s) 2017. This article is published with open access at Springerlink.com Abstract The construction process and use of galleries Az. brevis may, therefore, be defense against intruders in by Azteca brevis (Myrmicinae: Dolichoderinae) inhabiting contrast to Al. decemarticulatus which uses them mainly Tetrathylacium macrophyllum (Salicaceae) were compared for prey capture. This may be due to a higher need for pro- with Allomerus decemarticulatus (Myrmicinae: Solenopsi- tein in Al. decemarticulatus compared to coccid-raising Az. dini) galleries on Hirtella physophora (Chrysobalanaceae). brevis. Though the two ant species are phylogenetically distant, the gallery structure seems to be surprisingly similar and Keywords Ant–plant interaction · Ambush structurally convergent: both are pierced with numerous behaviour · Allomerus decemarticulatus · Azteca brevis · holes and both ant species use Chaetothyrialean fungi to Chaetothyriales · Hirtella physophora · Runway galleries · strengthen the gallery walls. Al. decemarticulatus is known Tetrathylacium macrophyllum to use the galleries for prey capture and whether this is also the case for Az. brevis was tested in field experiments. We placed Atta workers as potential prey/threat on the gal- Introduction leries and recorded the behaviour of both ant species. We found considerable behavioural differences between them: The construction of independent nests, galleries, shelters, Al. decemarticulatus was quicker and more efficient at cap- and inner walls that divide nests into separate cavities is ture than was Az. brevis. While most Atta workers were a common feature in ants, particularly in arboreal species, captured after the first 5 min by Al. decemarticulatus, built to provide colonies and their resources protection significantly fewer were captured by Az. brevis even after from climatic stress, parasites, and predators (Anderson 20 min. Moreover, the captured Atta were sometimes sim- and McShea 2001). Most species use carton made from ply discarded and not taken to the nest by Az. brevis. As plant fibres and debris or soil particles as building mate- a consequence, the major function of the galleries built by rial. In the Neotropics, species from the genus Allomerus (Formicidae: Myrmicinae), as well as a species from the Electronic supplementary material The online version of this genus Azteca (Formicidae: Dolichoderinae), Az. brevis article (doi:10.1007/s00040-017-0554-y) contains supplementary Forel, are known to build particular galleries on their host- material, which is available to authorized users. plant stems; these galleries are pierced with holes (Dejean et al. 2004, 2005; Mayer and Voglmayr 2009). Moreover, * V. E. Mayer [email protected] the galleries of these ant species are reinforced with a dense net of fungal hyphae, which have been identified as mem- 1 Department of Botany and Biodiversity Research, Division bers of the ascomycete order Chaetothyriales (Mayer and of Structural and Functional Botany, University of Vienna, Voglmayr 2009; Nepel et al. 2014; Ruiz-González et al. Rennweg 14, 1030 Vienna, Austria 2 2011). Such apparent similarities in the galleries built by CNRS, UMR Ecologie des Forêts de Guyane, ant species from phylogenetically distant genera belong- AgroParisTech, CIRAD, INRA, Université de Guyane, Université des Antilles, Campus Agronomique, BP316, ing to different subfamilies raise the question whether the 97379 Kourou Cedex, France construction process and the function of the holes are also Vol.:(0123456789)1 3 V. E. Mayer et al. similar. For Allomerus spp., it is known that the galleries Allomerus decemarticulatus was studied in the area are used for prey capture with ant workers waiting inside of Petit Saut, Sinnamary, French Guiana (05°03′30″ the galleries with their heads just under the holes and man- N, 52°58′34″W) in a lowland primary rainforest. Al. dibles wide open. Prey that walk over or settle on the gal- decemarticulatus (Mayr 1878) (Myrmicinae) are minute lery are grasped by their legs, antennae, or wings, stretched (1.5–1.8 mm), tawny-coloured ants that live strictly on ant- against the gallery, killed, and taken to the nest (Dejean plants. In the study area, Al. decemarticulatus is the main et al. 2005). obligatory inhabitant of Hirtella physophora (Chrysobala- However, it has never before been investigated how Az. naceae) with a single mature colony per plant; this ant spe- brevis uses its galleries, and whether these galleries have a cies has never been found associated with other myrme- function in prey capture analogous to those built by Allo- cophytic species (Grangier et al. 2009). H. physophora is merus. Therefore, we investigated the similarities and dif- a long-lived understory treelet that has leaves with a pair ferences in the behaviour of the two ant species. We com- of domatia at the base of each lamina (Leroy et al. 2008; pared (1) the construction process and (2) experimentally Orivel et al. 2011). The species occurs mostly in patches on tested whether the holes in the galleries built by Az. brevis the upper slopes of hillsides (Solano et al. 2003). have a prey capture function analogous to those built by Al. decemarticulatus. Investigation of the galleries’ structure and construction process Materials and methods Inner gallery width, height, and hole diameter were meas- ured with calipers. The measurements were taken from Species and study sites 2-cm-long pieces of carton cut from the galleries of four different colonies of Az. brevis and two colonies of Al. Azteca brevis (Forel 1899) (Dolichoderinae) was studied decemarticulatus. Head width, head length (including in the Parque Nacional Piedras Blancas (Costa Rica) on the mandibles), and the total body length of Al. decemar- Tetrathylacium macrophyllum growing near the La Gamba ticulatus (n = 10) and Az. brevis (n = 5) workers were also Biological Research Station (08°42′46″N, 83°12′90″W) measured. (n = 4), along Rio Sardinal (08°43′48″N 83°13′28″W; The construction process of the carton galleries was n = 3) and along Rio Bolsa (08°41′06″N 83°10′35″W; studied for 15 different Az. brevis colonies during both the n = 2) in a lowland primary rainforest characterised by high dry and the rainy seasons. We removed 10-cm-long sec- annual rainfall (>5000 mm). Az. brevis is a red-brown ant, tions of the carton galleries and recorded the reconstruction ca. 4-mm-long, known only from the Pacific side of Costa of the galleries by taking a photograph twice daily during Rica, mostly in the wet forests of the southern Pacific 2 weeks. If recently developed branches of the host tree T. lowlands (Longino 2007a). The colonies are polydomous macrophyllum were easily accessible, we also monitored with cauline nests in the live stems of trees (Supplemen- the continuation of the galleries on these new shoots. tary Fig. S1). All of the nesting chambers inside the stems Similar observations were made on ten Al. decemarticu- are connected externally by an extensive system of galler- latus colonies during the rainy season. The Al. decemar- ies made of a characteristically black carton with small, ticulatus galleries were removed from the plant and gallery circular holes. Az. brevis attends large populations of coc- reconstruction was observed during 2 weeks. We docu- coid Hemiptera of the genus Cryptostigma (P. Gullan, pers. mented the construction by photographing the galleries com.) inside the stems and in the runway tunnels (Supple- every day. mentary Fig. S1C). Colonies have been found on T. macro- phyllum (Salicaceae), a tree with an average height of about 8 m (but reaching a maximum height of 15–20 m) that Testing the function of the galleries of Az. brevis and Al. grows on the Pacific slopes of Central and South America decemarticulatus from southern Costa Rica to Ecuador with its centre of distribution in the Colombian Chocó (Supplementary Fig. To test the role of the Az. brevis galleries and compare it S1A). It grows preferentially on steep slopes near rivers with that of Al. decemarticulatus galleries, leaf-cutter and streams in the primary forest (Janzen 1983). The doma- ants (e.g. Atta colombica or At. cephalotes) were taken tia are located on the stems and develop from the partial from nearby nests and placed on the galleries to exam- degeneration of the pith. In the study area, the plant can be ine the ants’ behaviour towards potential invaders or prey. colonised by various ant species (Tennant 1989), but Az. Atta individuals are among the size range of prey that Al. brevis is the only one which actively enlarges the domatia decemarticulatus can capture (Dejean et al. 2005). Since by excavating the remaining pith (Schmidt 2001). Az. brevis workers are even larger than Al. decemarticulatus 1 3 Convergent structure and function of mycelial galleries in two unrelated Neotropical… workers, we hypothesised that they should also be able to that the capture efficiency of Al. decemarticulatus and Az. capture Atta ants. brevis is the same for each time interval. The test was per- The experiment was conducted on ten Al. formed with IBM SPSS Statistics 23. decemarticulatus/H. physophora and nine Az. brevis/T. macrophyllum associations. For each plant, three separate and easily accessible branches were selected. One Atta Results individual was carefully placed with tweezers on an Allo- merus-occupied H. physophora branch as well as on the Gallery structure, construction material, and process upper side of an Azteca-occupied T. macrophyllum branch. The fate of the Atta ants was recorded after four time inter- For both species, the galleries were similar; i.e., an arched vals (5, 10, 20, 30 min) and classified into one of three dif- tunnel 2-mm-high and with an inner width of 3–4 mm.