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First Evidence of Wasp Brood Development Inside Active Nests of a Termite with the Description of a Previously Unknown Potter Wasp Species

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First Evidence of Wasp Brood Development Inside Active Nests of a Termite with the Description of a Previously Unknown Potter Wasp Species Received: 19 July 2020 | Revised: 2 September 2020 | Accepted: 9 September 2020 DOI: 10.1002/ece3.6872 NATURE NOTES First evidence of wasp brood development inside active nests of a termite with the description of a previously unknown potter wasp species Helder Hugo1,2,3 | Marcel G. Hermes4 | Bolívar R. Garcete-Barrett5,6 | Iain D. Couzin1,2,3 1Centre for the Advanced Study of Collective Behaviour, University of Abstract Konstanz, Konstanz, Germany Potter wasps (Vespidae: Eumeninae) are known to exhibit not only sophisticated 2 Department of Collective Behaviour, preying strategies but also a remarkable ability to manipulate clay during nest build- Max Planck Institute of Animal Behavior, Konstanz, Germany ing. Due to a mixture of plasticity in building behavior and flexibility in substrate 3Department of Biology, University of preferences during nest building, the group has been reported nesting in a variety Konstanz, Konstanz, Germany of places, including decaying nests abandoned by termite species. Yet, evidence of 4Department of Biology, Universidade Federal de Lavras, Lavras, Brazil wasps nesting inside senescent termite mounds is poorly reported, and to date, ac- 5Museo Nacional de Historia Natural del counts confirming their presence inside active colonies of termites are absent. Here, Paraguay, San Lorenzo, Paraguay we address a novel intriguing association between two species from the Brazilian 6Department of Biology, Universidad Nacional de Asunción, San Lorenzo, Cerrado: a previously unknown potter wasp (nest invader) and a termite species (nest Paraguay builder). Besides scientifically describing Montezumia termitophila sp. nov. (Vespidae: Correspondence Eumeninae), named after its association with the termite Constrictotermes cypher- Helder Hugo, Max Planck Institute of Animal gaster (Silvestri, 1901) (Termitidae: Nasutitermitinae), we provide preliminary infor- Behavior, Universitätsstraße 10, 78467 Konstanz, Germany. mation about the new species' bionomics by including (a) a hypothetical life cycle Email: [email protected] based on the evidence we collected and (b) a footage showing the first interaction Funding information between a recently ecloded wasp and a group of termites. In doing so, we attempt to HH was supported by the Deutscher provoke relevant discussions in the field and, perhaps, motivate further studies with Akademischer Austauschdienst (DAAD) and the Max Planck Society. MGH is a the group. Finally, we describe a solution to efficiently detect and sample termitophil- CNPq fellow (process 304102/2018-0), ous species from termite nests, an intrinsic yet challenging task of any studies dealing and visiting trips to the NHM and MNHN were granted by Fundação Amazônica de with such a cryptic biological system. Defesa da Biosfera (FDB) upon the Brazilian Refauna Project. IDC acknowledges KEYWORDS support from the NSF (IOS-1355061), brood development, Constrictotermes cyphergaster, Montezumia, Nasutitermitinae, symbioses, the Office of Naval Research grant (ONR, N00014-19-1-2556), the Struktur- und Vespidae Innovationsfunds für die Forschung of the State of Baden-Württemberg, the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy–EXC 2117-422037984, and the Max Planck Society. Helder Hugo and Marcel G. Hermes contributed equally to this work. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2020;10:12663–12674. Konstanzer Online-Publikations-System (KOPS) www.ecolevol.org | 12663 URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-1l44rou3j46vs6 12664 | HUGO ET AL. 1 | INTRODUCTION existence of such mimicry strategies illustrate how evolution may shape nest invaders into true specialists, experts in deceiving the A species’ ability to persist locally and over time depends on its ca- termite builder (examples in Cunha et al., 2015; Oliveira et al., 2018; pacity to successfully breed and give rise to subsequent generations. Pisno et al., 2019; Rosa et al., 2018). The arms race between builder This definition seems to hold irrespective of major transitions in evo- and nest invader, driven by adaptations and counteradaptations lution (Maynard Smith & Szathmáry, 1995), being observed in solitary, from both sides (Dawkins & Krebs, 1979), is thought to produce gregarious, semisocial, and eusocial organisms. Among the variety cases in which the symbiosis is taken to another level, where one of of evolved strategies for developing immatures into adult individu- the species—if not both—ends up relying exclusively on the other for als, nest building has evolved independently across taxa into many survival. Such a dependency on a host is exhibited by some second- forms. The variation in nest architecture includes, but is not limited ary termite species (e.g., inquilines) and a number of other insects to, structures built by single individuals on top of pre-existing nests (e.g., termitophiles), which gain entry to the termite nest when host (such as in the species here reported), conglomerates of reproduc- colonies are still alive. However, because a termite construction is tive cells assembled by semisocial organisms (Bohart & Stange, 1965; likely to persist in the wild long after its colony dies, another great Lopes & Noll, 2019; West-Eberhard, 2005), and large-scale nests number of species opportunistically use abandoned nests as shelter collectively built by massive eusocial colonies (Eggleton, 2010; (Costa et al., 2009), becoming occasional occupants (Wilson, 1971). Hölldobler & Wilson, 1990; Seeley & Morse, 1976). Yet, despite the Together, these facts seem to indicate that regardless of the current variety of strategies, groups taxonomically independent and, there- status of its colony, a single termite nest will most likely attract a fore, evolving under seemingly unique selective pressures may still large number of foreign species throughout its time of existence. coincide in their nesting location. In fact, while a number of spe- Potter wasps (Vespidae: Eumeninae), known for their strik- cies settle in proximity and coexist harmoniously, in some cases in ing ability to shape clay during nest building, have been reported complete absence of interdependency (e.g., plesiobiosis, Kanizsai nesting in a variety of substrates (Cowan, 1991; Garcete-Barrett & et al., 2013), a relatively smaller group is known to “cheat” by de- Hermes, 2013; Hermes et al., 2015), including decaying nests of ter- liberately using a physical structure built by another species (Nash mites abandoned by the builder species (Batra, 1979). Curiously, to & Boomsma, 2008; Uboni et al., 2012). In termites, arguably one of date, there is no evidence of nesting by wasp species inside active the most successful builders in nature (Wilson, 1971), this pattern colonies of termites. Such a pattern, upon first glance, could be in- has been long and recurrently observed (Collins, 1980; Kistner, 1969, terpreted as a result of nesting preferences exhibited by the group. 1979, 1990; Mathews, 1977; Redford, 1984); nests built by a single However, except for some knowledge of bees as “guests” in termite builder species, and thus meant to house primarily nestmates, be- nests (for examples of species in Apidae, see Carrijo et al., 2012), lit- coming a hub of opportunistic invasive species. tle is known about the remainder clades of Hymenoptera, such as Because nest building is presumably a costly and time-consum- Vespidae, which may ultimately contribute to a misrepresentation of ing process (Korb & Linsenmair, 1999), one would expect that species the habits exhibited by the group. other than the builder would attempt to avoid such a commitment In this study, we describe a new species of potter wasp from and take advantage of pre-existing constructions, either “gently” the Brazilian Cerrado, Montezumia termitophila sp. nov. (Vespidae: (e.g., nest sharing) or “by force” (e.g., nest usurpation). Theoretically, Eumeninae), and report the first record of brood development by a while in the former approach invaders must find a way to stably co- wasp species inside active nests of the termite Constrictotermes cy- exist with their hosts, the latter only requires a hostile takeover in phergaster (Silvestri, 1901) (Termitidae: Nasutitermitinae). In addition which the builder is killed off and replaced by the invader. Although to reporting the unusual nesting site of the new wasp species, we practical, such a binary simplification should be considered care- discuss relevant yet poorly understood proximate causes of such a fully; in reality, the outcome of an association between species over development. Additionally, to add notes on the species’ biology and time is more likely to transit in a continuum between the extremes. potentially stimulate further studies, we propose a life cycle for the In either case, what seems fairly consistent is the fact that nest in- new wasp based on the evidence we collected. Finally, we provide a vaders are somehow lured by specific benefits associated with the protocol for detecting and sampling termitophilous species from ter- host nest. Indeed, besides providing shelter, nests may be a pool of mite nests, an intrinsic but challenging task that, if poorly conducted, valuable resources that drive trophic interactions,
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