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The Guild of Saprobiontic Nematodes Associated with Ants (Formicoidea)

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The Guild of Saprobiontic Nematodes Associated with Ants (Formicoidea) Research Article ISSN 2336-9744 (online) | ISSN 2337-0173 (print) The journal is available on line at www.biotaxa.org/em The guild of saprobiontic nematodes associated with ants (Formicoidea) WALTER SUDHAUS Institut für Biologie/Zoologie, Freie Universität Berlin, Königin-Luise-Str. 1–3, 14195 Berlin; E-mail: [email protected] Received 20 October 2016 │ Accepted 20 December 2016 │ Published online 29 December 2016. Abstract At least 14 different saprobiontic species of Rhabditida are intimately associated with ants on different continents. These myrmecophilous nematodes belong in particular to Diploscapter and Sclerorhabditis , and to the Oscheius Dolichura group (all "Rhabditidae"). Species of Diplogastridae and Halicephalobus (Panagrolaimidae) are rarely found in association with ants, but some records do exist. Oscheius janeti is argued here to be a separate species. Dauerlarvae of all these species invade the postpharyngeal glands of ants via the mouth (including as a result of trophallaxis) and, after some time and under suitable conditions, leave them the opposite way to complete their life cycle. These species usually propagate in the debris of ants' nests using ants as a means of dispersal (endophoresis). Species which live in certain saprobic biochores (such as slime flux) frequented by ants enter the ants to survive the unfavourable conditions of their habitat. Mostly the infestation rate is very low. Most field-collected ants contain no nematodes, and more than ten specimens are rarely found in one ant. The infestation rate increases in formicaria in the laboratory. There are some indications that dauerlarvae obtain nutrients from the carrier/host, so they may perhaps be viewed as facultatively larval parasitic. Queens, which have the potential to found a new colony, have also been documented to be infested. New nematode records from Solenopsis, from Azteca in domatia of Tococa (Melastomataceae) and Cecropia (Urticaceae), from Crematogaster in domatia of Macaranga (Euphorbiaceae), and from the fungus-growing Acromyrmex and Atta are reported . The nematode-ant relationship and distinctive organ specificity of the dauerlarvae to the postpharyngeal glands of ants has been attained by convergent evolution no less than nine times. It is expected that living together with saprobiontic nematodes in m yrmecophilous plants offers some kind of benefit to ants. Key words : Myrmecophily, domatium, nematode, life cycle, organ specificity, Diploscapter, Oscheius, Sclerorhabditis, Formicoidea, Acromyrmex, Atta, Azteca, Cladomyrma, Crematogaster, Mycetophyllax, Solenopsis. Introduction Parasitic nematodes, most often Mermithidae (several genus-taxa), but also Tetradonematidae ( Tetradonema, Myrmeconema ), Allantonematidae ( Formicitylenchus ), Seuratidae ( Rabbium ), and Physalopteridae (Skrjabinoptera ), have been recorded in various groups of ants (Poinar, 2012). The last two (usually) heteroxenous taxa utilise ants as intermediate hosts. It is also relatively easy to infect ants with species of the entomoparasitoids Heterorhabditis and Steinernema (Poinar, 2012). Alongside these parasitic relationships, phoretic or mutualistic relationships also exist between saprobiontic nematodes and ants. The occurrence of nematode dauerlarvae in the tubular postpharyngeal glands of ants completing their life cycles in the detritus of nests was first reported by Janet (1893, 1894) for Formica rufa and Lasius flavus . The species in Formica rufa was described in Janet (1894) as Pelodera janeti De Lacaze-Duthiers, then re-described in detail by de Ecol. Mont., 7, 2016, 600-613 SUDHAUS Man (1894). It was synonymized by Andrássy (1952) with Leptodera dolichura Schneider, 1866 (= Oscheius dolichura ), and this was confirmed by Wahab (1962) and Sudhaus (1976). Thus was it demonstrated that this well-known saprobiontic species found in an ecologically wide range of habitats and transported by a number of different beetles exhibits a surprising facultative relationship with ants. Wahab (1962) made a comprehensive study of this peculiar association in the laboratory of H.-J. Stammer and G. Osche (Erlangen, Germany). In the postpharyngeal glands of 16 out of 25 species of ants examined (species of Formica, Lasius, Myrmica, Tetramorium ) he found not only O. dolichura , but three more nematode species. Ants of 198 out of a total of 550 nests (= 36%) were infested. The nematodes most commonly found were Diploscapter lycostoma Völk, 1950 (in 127 nests, = 23%) and O. dolichura (in 58 nests, = 10.5%), whereas a species of the Pristionchus Lheritieri complex which Wahab identified as P. lheritieri (Maupas, 1919) was found in just 5 nests (0.9%) and Koerneria histophora (Weingärtner, 1955) was found in just 3 (0.5%). Nine nests and several individual workers, respectively, were inhabited by two different species, yet only 5 (2.5%) of the nests infested displayed a mixed occurrence of the most frequent species D. lycostoma and O. dolichura. Although these species do not specialise in different ant species, they are separated ecologically: O. dolichura was frequent in nests found in forests and D. lycostoma in those found in the open country. The four nematode species shown by Wahab (1962) to be myrmecophilous were already known from a variety of decaying substrates such as mulm (duff), slime flux, compost, and manure, and occasionally they occurred phoretically associated with different beetles. In his study they were also shown to be saprobiontic inhabitants of detritus in the nests of ants, and to exhibit an endophoretic relationship with ants. A further in-depth analysis of the association between nematodes and ants was conducted by Köhler (2008, 2012) in the laboratory of A. Fürst von Lieven and myself in Berlin. Köhler focused on the ant species Lasius brunneus , which is associated with slime flux on deciduous trees. In the heads of 114 of 262 workers (= 43.5%) he found a total of 520 dauerlarvae, of which 287 (= 55%) matured and could then be identified to species level. The most frequent nematode species found in this particular ecological situation was K. histophora (58.5%), followed by D. cf. lycostoma (29.3%), O. dolichura (10.8%) and two newly demonstrated associates of ants, Diplogasteroides spengelii de Man, 1912 and Halicephalobus similigaster (Andrássy, 1952) (both 0.7%, respectively). Most ants were uninfested, and 75% of 114 ants bearing nematodes only had 1–3 dauerlarvae in their postpharyngeal glands. The highest numbers of dauers found in ant specimens collected in the field were 20, 40, 58, and 85, respectively (Köhler, 2012), whereas Wahab (1962) rarely counted more than 20 and at most 43 nematodes per ant. In supplemental studies the two most frequent myrmecophilous species were also found in ants from North America, namely D. lycostoma in Linepithema (formerly Iridomyrmex ) humile in multiple places in California (Markin & McCoy, 1968), and O. dolichura in Camponotus herculeanus and Lasius (Acanthomyops ) claviger in Ontario (Nickle & Ayre, 1966). In addition, the description of waving juveniles covered by an "oily secretion" suggests that a species of Diplogastridae was also present in one of these ant species, as the secretion in question is unique to diplogastrids. A phoretic diplogastrid was observed by P. E. Hanson on Azteca sp. in Costa Rica (Poinar, 2011, p. 93+325). In Oregon, Poinar (2012) found dauers of an unknown diplogastrid in the postpharyngeal glands of Formica obscuriventris . The latter diplogastrid was further identified as a member of Pristonchus (Poinar, 2016). The hermaphroditic diplogastrid Pristionchus entomophagus (Steiner, 1929) was isolated from Myrmica rubra found at several sites in Maine, and a similar species was detected "in its native range in England" (Groden & Stock, 2011, Michaud, 2013). Recently, Sclerorhabditis neotropicalis Esquivel et al., 2012 was described from nests of Azteca constructor and A. xanthochroa in Cecropia obtusifolia in Costa Rica (Esquivel et al., 2012), and Diploscapter formicidae Zhao et al., 2013 was found in nests and workers of Prolasius advenus, an ant species endemic to New Zealand (Zhao et al., 2013). Kermarrec (1975) reported dauerlarvae of an undetermined species in the postpharyngeal glands of Acromyrmex octospinosus in Guadeloupe. From the shape of the dauerlarva and the structuring of its cuticle it can be identified from the photos as Pelodera cystilarva (Völk, 1950) or a very closely related species. This record is extremely unusual, as Pelodera cystilarva typically lives in compost, and its dauerlarvae rely for dispersal on sticky secretions from glands in their anterior end which they use to attach themselves to the cuticle particularly of gamasid mites. My own incidental observations on the association between saprobiontic nematodes and ants span a period of around 40 years (Sudhaus, 2016). They are summarised here and discussed in conjunction with data from the literature (fig. 1). Ecol. Mont., 7, 2016, 600-613 601 SAPROBIONTIC NEMATODES ASSOCIATED WITH ANTS Oscheius Diploscapter Sclerorhabditis Koerneria Pristionchus Diplogasteroi- Halicephalobus Panagro- gen. et dolichura lycostoma neotropicalis histophora Lheritieri group des spengelii similigaster laimus sp. sp. nov. not not known known Figure 1. Pictorial key to compare characters of nine myrmecophilous nematode species or representatives: (1) lip region and stoma, (2) median part of pharynx, (3) termianl bulb of pharynx, (4) female anal region and tail (very long tails are cut), (5) male
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