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Behavioural and chemical mechanisms behind a Mediterranean ant–ant association
Abstract
1. Interspecific competition among ants is common, and so is competitive exclusion among dominant ant species. In contrast, specific associations between non-parasitic ant species are rare, especially in the temperate zones. As an exception, the subordinate ant Camponotus lateralis frequently co-occurs with the dominant Crematogaster scutellaris but rarely with other dominant ants.
2. This association is one of various associations between Camponotus and Crematogaster species across the world. However, the mechanisms behind these co-occurences are largely unknown.
3. In the present study, we therefore investigated the association of Ca. lateralis and Cr. scutellaris. We studied the spatial association of the nests, interspecific aggression, both species' cuticular hydrocarbon profiles, and their propensity to follow the other species' pheromone trails.
4. Crematogaster scutellaris usually attacked and displaced the generally submissive Ca. lateralis, but was significantly less aggressive at jointly used trails. Camponotus nests were always in close proximity to Crematogaster nests.
5. The cuticular hydrocarbons of both species consisted of alkanes with chain lengths between C21 and C35. The two species had 25 hydrocarbons in common, including mono-, di-, and tetramethyl alkanes. Despite this qualitative similarity, however, the quantitative hydrocarbon composition differed between the two species.
6. Camponotus lateralis followed artificial trails containing trail pheromones of Cr. scutellaris, but the latter did not follow Ca. lateralis trail pheromones. Interspecific trail-following by Camponotus, but not vice versa, has been observed in another Camponotus–Crematogaster association and may be a more general mechanism that facilitates associations between the two ant genera.
... Since ants are often well-fortified against, aggressive towards, or unpalatable for potential predators (Hölldobler & Wilson, 1990), they represent models for thousands of Batesian mimetic species from different arthropod orders, including Hemiptera, Coleoptera, non-ant Hymenoptera, Diptera, and Araneae (e.g., McIver, 1987;Oliveira & Sazima, 1984;Pekár, 2020;Pekár & Křál, 2002;Pie & Del-Claro, 2002;Rasekh et al., 2010;Reiskind, 1977;Taniguchi et al., 2005). Mimicry among ants is rare and a hitherto littlestudied topic, only less than 20 examples of ant species mimicking other ant species are known worldwide (Emery, 1886;Fisher & Peeters, 2019;Forel, 1874Forel, , 1891Gallego Ropero & Feitosa, 2014;Gobin et al., 1998;Ito et al., 2004;Menzel et al., 2010;Merrill & Elgar, 2000;Pekár et al., 2017;Powell et al., 2014;Rasoamanana et al., 2017;Schifani et al., 2022;Seifert, 2019;Wagner, 2013Wagner, , 2014Wagner, , 2019Ward, 1984Ward, , 2009. Since mimicry can only be adaptive in the presence of a model, mimic and model should occur together in time and space. ...
... In other regions, for example, over large parts of Italy, it has a blackish one like Cr. scutellaris (Olivier, 1791). It has already been hypothesized that the submissive (Borovsky et al., 2022;Marlier et al., 2004;Menzel et al., 2010) Ca. lateralis mimics the color of the regional occurring dominant and very aggressive Crematogaster model species (Seifert, 2018(Seifert, , 2019Wagner, 2013Wagner, , 2014. ...
... Trail-sharing behavior with Crematogaster, which was often observed in Ca. lateralis (Baroni Urbani, 1969;Carpintero et al., 2005;Goetsch, 1942Goetsch, , 1951Kaudewitz, 1955;Menzel et al., 2010Menzel et al., , 2014, occurs also in Ca. guanchus. Camponotus lateralis workers escape when they encounter a Crematogaster worker (Kaudewitz, 1955 ...
Mimicry, that is, the imitation of any unpalatable or defensive species by another, has been of central interest to evolutionary research since Darwin's lifetime. Two ant species, Camponotus guanchus Santschi, 1908 and Crematogaster alluaudi Emery, 1893, endemic to the Canary Islands, occur in two color‐morphs: While the head of workers is always reddish and the gaster blackish, the mesosoma (inclusive waist) is either fully reddish or fully blackish. In addition to the obvious morphological and coloration similarities, we provide evidence of mimicry: (i) Ca. guanchus was found only within the area of Cr. alluaudi. (ii) Color morphs are geographically non‐randomly distributed: Workers of both species from 16 localities of syntopic occurrences shared in eight cases a blackish and in eight cases a reddish mesosoma. Hence, Ca. guanchus mimics both local color‐morphs of Cr. alluaudi. We consider a fascinating analogy with the Mediterranean mimicry system in Camponotus lateralis (Olivier, 1792) and its model species of the Crematogaster scutellaris (Olivier, 1792) group on an island scale. Additionally, we present two endemic bug species, Perenotus stysi (Ribes et al., 2008) and P. malobae Roca‐Cusachs & Goula, 2016, as mimics of those Cr. alluaudi workers having a reddish mesosoma. Our distribution, coloration, frequency, and behavioral data as well as the analogy with Ca. lateralis and the Cr. scutellaris group suggest a Batesian‐mimicry system in which Ca. guanchus, Perenotus stysi, and P. malobae mimic the unpalatable and aggressive Cr. alluaudi as an antipredator adaptation.
... Batesian mimicry has also been reported for some other species pairs: Colobopsis truncata (Spinola 1808) / Dolichoderus quadripunctatus (Linnaeus 1771) (Wagner, 2019); Colobopsis imitans/ Crematogaster scutellaris (Olivier 1792) (Schifani et al. 2022). Similar interactions, characterised by one species attempting to access the food resources of another, have been described in several ant species, such as Gnamptogenys menadensis (Mayr 1887) and Polyrhachis rufipes Smith, F., 1858 (Gobin et al. 1998), Camponotus lateralis (Olivier 1792) and Crematogaster scutellaris (Gene, 1842;Emery, 1886Emery, , 1915Zimmermann, 1934;Goetsch, 1942Goetsch, , 1951Goetsch, , 1953Kaudewitz, 1955;Baroni Urbani, 1969;Menzel et al. 2010a), Camponotus lateralis and Crematogaster schmidti (Mayr 1853) (Stukalyuk & Radchenko 2011). When moving along trails, Camponotus lateralis orient themselves to the trail pheromone of Crematogaster scutellaris, but not vice versa (Menzel et al. 2010a). ...
... Similar interactions, characterised by one species attempting to access the food resources of another, have been described in several ant species, such as Gnamptogenys menadensis (Mayr 1887) and Polyrhachis rufipes Smith, F., 1858 (Gobin et al. 1998), Camponotus lateralis (Olivier 1792) and Crematogaster scutellaris (Gene, 1842;Emery, 1886Emery, , 1915Zimmermann, 1934;Goetsch, 1942Goetsch, , 1951Goetsch, , 1953Kaudewitz, 1955;Baroni Urbani, 1969;Menzel et al. 2010a), Camponotus lateralis and Crematogaster schmidti (Mayr 1853) (Stukalyuk & Radchenko 2011). When moving along trails, Camponotus lateralis orient themselves to the trail pheromone of Crematogaster scutellaris, but not vice versa (Menzel et al. 2010a). Crematogaster scutellaris workers were shown to attack Camponotus lateralis workers upon encounter in all cases (Menzel et al. 2010a). ...
... When moving along trails, Camponotus lateralis orient themselves to the trail pheromone of Crematogaster scutellaris, but not vice versa (Menzel et al. 2010a). Crematogaster scutellaris workers were shown to attack Camponotus lateralis workers upon encounter in all cases (Menzel et al. 2010a). The same behaviour was also recorded for the pair of Crematogaster schmidti and Camponotus lateralis (Stukalyuk & Radchenko 2011). ...
The paper examines the relationship between two ant species: Camponotus lateralis and Crematogaster schmidti in the neighboring habitat in the biocenoses of the Southern Coast of the Crimea (Ukraine). The ecological characteristics of the species are given, the structure of forage areas is described, as well as the daily activity of ants in shared habitats. It was shown that Camponotus lateralis accesses the food resources of Crematogaster schmidti using their trails. As a result of a frame-by-frame analysis of the video recordings, a number of behavioural responses have been identified for each species that it displays during interspecific contacts on the trails. It was shown that Camponotus lateralis successfully avoids contact by changing its trajectory at a distance of about 1 cm from Crematogaster schmidti workers. The aggressive reaction of Crematogaster schmidti was only recorded in few cases after antenna contacts. In most cases, Camponotus lateralis reacted more quickly than Crematogaster schmidti after antennal contact and changed its trajectory. The structural characteristics of the antennae and eyes of workers of both species were compared. Camponotus lateralis workers were shown to have longer antennae on average. The eyes of Camponotus lateralis have, on average, more facets than those of Crematogaster schmidti and, on average, more facets per unit of eye area. The significance of these morphological advantages of Camponotus lateralis for the successful use of Crematogaster schmidti trails is discussed. ABSTRAK Kajian ini menilai hubungan antara dua spesies semut Camponotus lateralis and Crematogaster schmidti di habitat sekitaran di dalam biocenoses di Pantai Selatan Crimea (Ukraine). Ciri-ciri ekologi spesies diberikan, struktur mencari makanan diperihalkan serta aktiviti harian semut di habitat yang sama. Hasil menunjukkan Camponotus lateralis mencari sumber makanan iaitu Crematogaster schmidti menggunakan laluannya. Hasil analisis frame-by-frame dari rakaman video, beberapa respon kelakuan telah dicamkan untuk setiap spesies yang menunjukkan hubungan intraspesifik di laluannya. Camponotus lateralis juga berjaya menunjukkan dan Serangga 2023, 27(3): 125-149. Stukalyuk et al. ISSN 1394-5130 125 mengelak bersentuhan dengan mengubah laluan lintasan pergerakkannya pada jarak 1 cm dari pekerja Crematogaster schmidti. Reaksi agresif Crematogaster schmidti hanya direkodkan pada beberapa kes selepas sentuhan antena. Dalam kebanyakkan kes, Camponotus lateralis reaksi dengan cepat dari Crematogaster schmidti selepas sentuhan antenna dan perubahan laluannya. Ciri struktur antenna dan mata pekerja pada kedua-dua spesies dibandingkan. Pekerja Camponotus lateralis menunjukkan antenna yang lebih panjang secara purata. Mata Camponotus lateralis secara purata, mempunyai lebih facets dari Crematogaster schmidti dan purata lebih facet per unit kawasan mata. Signifikan dari kelebihan morfologi Camponotus lateralis ini adalah kejayaan menggunakan laluan Crematogaster schmidti juga dibincangkan.
... In these species, chromatic mimicry is the prevalent mechanism, while behavioural or morphological adaptations are more rarely documented (Emery, 1886;Forel, 1886;Santschi, 1919;Gobin et al., 1998;Merril & Elgar, 2000;Ito et al., 2004;Ward, 2009;Gallego-Ropero & Feitosa, 2014;Powell et al., 2014;Pekár et al., 2017;Rasoamanana et al., 2017;Seifert, 2019a). In addition, recurrent behaviour among mimicking ant species is interspecific trail-following, which consists in the mimics regularly infiltrating into the foraging trails of the model and may lead to parasitic behaviour with regard to food resources (Emery, 1886;Santschi, 1919;Gobin et al., 1998;Ito et al., 2004;Menzel et al., 2010;Powell et al., 2014). Unlike specialized parasites (e.g. ...
... Unlike specialized parasites (e.g. Visicchio et al., 2001;Buschinger, 2009;de la Mora et al., 2020), no advanced mechanisms of chemical deception exist in most of these cases, so in the eventuality of direct encounters, the model species recognizes and attacks the mimic, which is well-equipped to escape (Goetsch, 1942(Goetsch, , 1951Kaudewitz, 1955;Gobin et al., 1998;Ito et al., 2004;Menzel et al., 2010). The vast majority of the hitherto well-documented cases come from the tropics: mimics mainly belong to diverse lineages from the Formicinae tribe Camponotini (mostly Camponotus Mayr, 1861), while their models are phylogenetically scattered, including Ectatomminae, Myrmeciinae, Myrmicinae (Crematogastrini and Stenammini) and Pseudomyrmecinae. ...
... It chromatically mimics the similar Crematogaster Lund, 1831 species, Cr. ionia Forel, 1911, Cr. scutellaris (Olivier, 1792 and Cr. schmidti (Mayr, 1853), and follows their trails (Emery, 1886;Baroni Urbani, 1969;Menzel et al., 2010;Wagner, 2014;Seifert, 2018Seifert, , 2019a. The three species are closely related with neighbouring geographic ranges and differ slightly chromatically (Blaimer, 2012). ...
The West-Palaearctic Colobopsis ant populations have long been considered a single species (Colobopsis truncata). We studied the diversity of this species by employing a multidisciplinary approach and combining data from our surveys, museum and private collections, and citizen science platforms. As a result, we have revealed the existence of a second species, which we describe as Colobopsis imitans sp. nov., distributed allopatrically from Co. truncata and living in the Maghreb, Sicily and southern Iberia. While the pigmentation of Co. truncata is reminiscent of Dolichoderus quadripunctatus, that of Co. imitans is similar to Crematogaster scutellaris, with which Co. imitans lives in close spatial association, and whose foraging trails it habitually follows, similar to Camponotus lateralis and other ant-mimicking ants. The isolation between Co. imitans and Co. truncata seems to have occurred relatively recently because of significant, yet not extreme, morphometric differentiation, and to mtDNA polyphyly. Both Co. imitans and Co. truncata appear to employ mimicry of an unpalatable or aggressive ant species as an important defensive strategy; this ‘choice’ of a different model species is motivated by biogeographic reasons and appears to act as a critical evolutionary driver of their diversification.
... Many ants also deposit pheromone trails to recruit nestmates to food sources, and these pheromones are usually species-or genus-specific (Czaczkes, Grüter, & Ratnieks, 2013). Ant workers of several species have been shown to detect heterospecific trail pheromones and to follow them to food sources (Menzel, Woywod, Blüthgen, & Schmitt, 2010;Morgan, 2009). If subordinate species were similarly able to read the trail pheromones of dominant species, they could use these chemical cues to circumvent competitive encounters. ...
... We therefore obtained the trail pheromone extract by dissecting hindguts of five freeze-killed individuals from the same colony, and immersing them in 25 ml of hexane. This method is standard practice to obtain standardized quantities of trail pheromones and test their biological activity (Attygalle & Morgan, 1985;Menzel, Woywod, et al., 2010;Morgan, 2009). ...
... Workers only followed trails in the presence of their colony-specific footprints but not trail pheromones alone. However, previous studies using pheromone extracts revealed that some ants can read heterospecific trail pheromones, even if they differ in chemical composition from their own pheromone (Menzel, Pokorny, Blüthgen, & Schmitt, 2010;Menzel, Woywod, et al., 2010). ...
Interspecific competition is an important ecological mechanism shaping the traits of the interacting species and structuring their communities. Less competitive species benefit from evading direct encounters with aggressive dominants, whereas dominant species could use cues left by subordinates to steal their resources or to chase them off. Here, we studied competitive interactions among five common and syntopic ant species in Central Europe (Formica polyctena, Formica rufibarbis, Lasius niger, Myrmica rubra and Tetramorium caespitum) and investigated their ability to react to heterospecific chemical cues. Using aggression assays, we established a clear dominance hierarchy of these species, with L. niger and F. polyctena as the most dominant species. Using Y-mazes, we then tested whether ants avoid or prefer areas with cues of either dominant or subordinate species. These cues included trail pheromones, cuticular hydrocarbons and chemical footprints. Ants of all species ignored heterospecific trail pheromone extracts, but two of the three subordinate species avoided cuticular hydrocarbons of the dominant species. In contrast, dominants either ignored or were attracted to cuticular hydrocarbon extracts of subordinates. The avoidance behaviour of the subordinates might be quantity-dependent, as footprints of the dominant species L. niger attracted two subordinates. The lowest ranking species M. rubra was unresponsive to cues of heterospecifics but avoided following the traces of their own colony members. Our study shows that ants exploit heterospecific cues either to avoid or to seek competitors and that their reaction depends on their dominance rank in the local community.
... However, there is a recurrent evolution of mimicking relationships involving dominant myrmicine ants of the genus Crematogaster as models, and formicine ants from the genera Camponotus and Colobopsis (of the Camponotini tribe) as mimics (Ito et al. 2004;Schifani et al. 2022a;Pérez-Delgado & Wagner 2024). In these cases, interactions between mimics and their models are also often characterized by trail-sharing or trail-following: model species tend to form permanent, well-defended foraging trails that the mimics exploit to hide or fi nd resources with or without the consent of the model workers (Emery 1886;Santschi 1919;Gobin et al. 1998;Ito et al. 2004;Menzel et al. 2010;Powell et al. 2014;Schifani et al. 2022a;Pérez-Delgado & Wagner 2024). In the western Palearctic, the Crematogaster scutellaris (Olivier, 1792) group is the model for ant species combining visual mimicry with trail-following in at least three cases: Camponotus lateralis (Olivier, 1792), which is a mimic of Cr. scutellaris, Cr. schmidti (Mayr, 1853), and Cr. ...
... In the western Palearctic, the Crematogaster scutellaris (Olivier, 1792) group is the model for ant species combining visual mimicry with trail-following in at least three cases: Camponotus lateralis (Olivier, 1792), which is a mimic of Cr. scutellaris, Cr. schmidti (Mayr, 1853), and Cr. ionia (Forel, 1911); Santschi, 1908, which is a mimic of Cr. alluaudi Emery, 1893; Colobopsis imitans Schifani, Giannetti, Csősz, Castellucci, Luchetti, Castracani, Spotti, Mori & Grasso, 2022, which is a mimic of Cr. scutellaris (Menzel et al. 2010;Seifert 2019;Schifani et al. 2022a;Pérez-Delgado & Wagner 2024). Co. imitans is the recently described sister species of Co. truncata (Spinola, 1808), which instead has a mimicry relationship whose model is the dolichoderine ant Dolichoderus quadripunctatus (Linnaeus, 1771). ...
The ant Crematogaster scutellaris, distributed across the western Mediterranean region and east to the west Balkans, is a visual mimicry model for various other organisms, including different other species of ants. It is an ecologically and behaviorally dominant species, foraging through large permanent trails that workers pugnaciously defend by biting and spraying a toxic secretion. Here we report on two interesting novelties discovered by monitoring Cr. scutellaris foraging trails in Tunisia: fi rst, we present the fi rst records of the mimicking ant Colobopsis imitans in the country, fi lling a distribution gap and confi rming a previous biogeographic hypothesis; second, we identifi ed the mirid Mimocoris rugicollis, whose brachypterous females are known as myrmecomorphs, as a mimic of Cr. scutellaris. Both Co. imitans and M. rugicollis were observed following or stationing near Cr. scutellaris trails, often in the presence of another mimicking ant, Camponotus lateralis. Still little is known about the ecology and behavior of most Cr. scutellaris mimics, with some species still undescribed. Further research is needed to investigate the evolutionary pressures shaping this adaptation.
... The foragers of the three species studied here followed chemical footprints of non-nestmates. Menzel et al. (2010) observed that Camponotus lateralis can distinguish nestmates from non-nestmates based on their chemical cues left in the environment. These ants are more aggressive towards ants from distant colonies, suggesting that they had become accustomed to nearby colonies. ...
... Forager ants can use cues from other colonies or species to avoid competition, by avoiding areas frequented by other ants (Wüst and Menzel 2017). Subordinate species often avoid aggression simply by avoiding contact (Menzel et al. 2010) or by appeasement behavior (Traniello 1989). In addition, the size of C. borgmeieri colonies allows ants to seek resources in different areas, avoiding competition with other species, which is common for ants with numerous colonies (Binz et al. 2014;Jaffe and Deneubourg 1992;Nicolis and Deneubourg 1999). ...
When an insect walks, it leaves chemical cues that derive from the arolium, a tarsal structure. These cues may contain important information about other species that occur in their community and can then mediate interactions of competition, predation, and information about resources with ants from their own colony. The compounds of these cues are released into the substrate in the form of chemical footprints. There are still few species studied, and little is known about the behavior of ants regarding these signals and how they use them in their interactions. Therefore, the aim of this study was to assess the behavioral strategy of different ant species when confronted with chemical footprints left by other ants, as well as identify their compounds and their relationship with the cuticular hydrocarbon profile. The experiments were performed using a Y-maze, where in one of the arms, there were chemical footprints of their own species or of other species, and the other Y arm was footprint-free. The chemical compounds of footprints and cuticle were analyzed by gas chromatography-mass spectrometry. The results show that foragers of all species detect and respond to the presence of chemical cues in the form of footprints left by other ants. Foragers of all species followed footprints of individuals of the same species both nestmates and non-nestmates; however, Neoponera villosa avoided the footprints of Cephalotes borgmeieri, and C. borgmeieri avoided the footprints of the other two species. The chemical compositions of the cuticle and footprints are related to each other and are specific to each species.
... Colonial recruitment behaviour, which allows the rapid occurrence of many individuals on a potential resource, could result in massive attacks of insect pests and undermine predator satiation-based defensive strategies [19]. Moreover, ants produce many different types of pheromones used for intra-and inter-specific communication, as well as during foraging and patrolling activities [20][21][22][23], which might be detected by the pest [17]. This makes this taxon a good candidate for biological control through TMIIs. ...
... CHCs are pheromones commonly used by ants and other insects to recognize nestmates and/or mutualists, but they may also be released in the environment and be involved, for example, in marking the home range [57,58], and they can be also used as kairomones [59]. Unfortunately, despite the fact that the CHCs of the two studied species have been analysed in previous studies (e.g., [22,35] for C. scutellaris, [60] for the T. nigerrimum complex), a comparative analysis to identify the effective molecules on available data is difficult because of the different laboratory standards used. Of note, it is very well known that the CHC profile of a colony can change very rapidly, even under the effect of very local factors, such as food sources used [35], but our results suggest that the substances triggering the effect are quite stable, as they are conserved across subfamilies. ...
Alternative methods to achieve sustainable agricultural production while reducing the use of chemical pesticides, such as biological control, are increasingly needed. The exploitation of trait-mediated indirect interactions (TMIIs), in which pests modify their behavior in response to some cues (e.g., pheromones and other semiochemicals) to avoid predation risk, may be a possible strategy. In this study, we tested the effect of TMIIs of two Mediterranean ant species, Crematogaster scutellaris and Tapinoma nigerrimum, on the oviposition behaviour of Ceratitis capitata (Diptera: Tephritidae), one of the world’s most economically damaging pests, which attacks fruits. For each ant species, we performed choice experiments using ant-scented and control plums, counting the time spent by medflies on fruits and the number of pupae emerging from them. Results of both ant species tests showed a significantly shorter time spent by ovipositing medflies on ant-exposed plums and a lower number of pupae, when compared to the control group. Our findings highlighted that the semiochemicals released by ants on plums triggered an avoidance behaviour by medfly females, leading to lower oviposition rates. This study contributes to the understanding of indirect ant–pest interactions in Mediterranean agricultural settings and points out the potential of utilising ant-borne semiochemicals in sustainable IPM strategies.
... But what if species aggregate rather than segregate? Competition between ant species is often asymmetric, with species differing in their competitiveness (Menzel et al., 2010a(Menzel et al., , 2010bSavolainen and Veps€ al€ ainen, 1988). For example, a typical ant mosaic is formed by dominant ant species, some of which (like Oecophylla) tolerate many subordinate species, while others (like Anonychomyrma) do not. ...
... Our approach may be particularly useful to search for specialised, pair-wise associations that warrant further study. Such pair-wise associations can indicate mutual tolerance, with a dominant and a submissive species (Dejean and Corbara, 2003;Majer, 1976Majer, , 1993Majer et al., 1994), or parasitic or mutualistic association (Menzel and Blüthgen, 2010;Menzel et al., 2010aMenzel et al., , 2010bOrivel et al., 1997). In our dataset, one Polyrhachis and two Pheidole species always co-occurred with the same Diacamma species, suggesting a close relationship between them and Diacamma. ...
This is the author accepted manuscript. It is currently under an indefinite embargo pending publication by Elsevier
... About 220 ant species (out of more than 13 000) are parasites of other ant species, often living in the same nest as the 'host' ( [61], figure 1a). Such parasites either exploit other species by using their pheromone trails to find the discovered food source [62] or use 'eavesdropping'-using auditory cues as information on food sources [63]. Trail following is always unilateral [62]. ...
... Such parasites either exploit other species by using their pheromone trails to find the discovered food source [62] or use 'eavesdropping'-using auditory cues as information on food sources [63]. Trail following is always unilateral [62]. Distinct classes of social parasites exist, depending on whether or not they keep their brood separate from the host, and whether or not they kill the queen (see [61] for a review). ...
This special feature results from the symposium 'Ants 2016: ant interactions with their biotic environments' held in Munich in May 2016 and deals with the interactions between ants and other insects, plants, microbes and fungi, studied at micro-and macroevolutionary levels with a wide range of approaches, from field ecology to next-generation sequencing, chemical ecology and molecular genetics. In this paper, we review key aspects of these biotic interactions to provide background information for the papers of this special feature. After listing the major types of biotic interactions that ants engage in, we present a brief overview of ant/ant communication, ant/plant interactions, ant/fungus symbioses, and recent insights about ants and their endosymbionts. Using a large molecular clock-dated Formi-cidae phylogeny, we map the evolutionary origins of different ant clades' interactions with plants, fungi and hemiptera. Ants' biotic interactions provide ideal systems to address fundamental ecological and evolutionary questions about mutualism, coevolution, adaptation and animal communication.
... But what if species aggregate rather than segregate? Competition between ant species is often asymmetric, with species differing in their competitiveness (Menzel et al., 2010a(Menzel et al., , 2010bSavolainen and Veps€ al€ ainen, 1988). For example, a typical ant mosaic is formed by dominant ant species, some of which (like Oecophylla) tolerate many subordinate species, while others (like Anonychomyrma) do not. ...
... Our approach may be particularly useful to search for specialised, pair-wise associations that warrant further study. Such pair-wise associations can indicate mutual tolerance, with a dominant and a submissive species (Dejean and Corbara, 2003;Majer, 1976Majer, , 1993Majer et al., 1994), or parasitic or mutualistic association (Menzel and Blüthgen, 2010;Menzel et al., 2010aMenzel et al., , 2010bOrivel et al., 1997). In our dataset, one Polyrhachis and two Pheidole species always co-occurred with the same Diacamma species, suggesting a close relationship between them and Diacamma. ...
Ecological communities are structured by competitive, predatory, mutualistic and parasitic interactions combined with chance events. Separating deterministic from stochastic processes is possible, but finding statistical evidence for specific biological interactions is challenging. We attempt to solve this problem for ant communities nesting in epiphytic bird’s nest ferns (Asplenium nidus) in Borneo’s lowland rainforest. By recording the frequencies with which each and every single ant species occurred together, we were able to test statistically for patterns associated with interspecific competition. We found evidence for competition, but the resulting co-occurrence pattern was the opposite of what we expected. Rather than detecting species segregation—the classical hallmark of competition—we found species aggregation. Moreover, our approach of testing individual pairwise interactions mostly revealed spatially positive rather than negative associations. Significant negative interactions were only detected among large ants, and among species of the subfamily Ponerinae. Remarkably, the results from this study, and from a corroborating analysis of ant communities known to be structured by competition, suggest that competition within the ants leads to species aggregation rather than segregation. We believe this unexpected result is linked with the displacement of species following asymmetric competition. We conclude that analysing co-occurrence frequencies across complete species assemblages, separately for each species, and for each unique pairwise combination of species, represents a subtle yet powerful way of detecting structure and compartmentalisation in ecological communities.
... The colony combination is given as 'resident–intruder', e.g. AB resident: Pat_A; intruder: Pat_B F. Menzel et al. allomones (D'Ettorre et al. 2000), submissive behaviour (e.g., flight), or combinations thereof (D'Ettorre and Heinze 2001; Lenoir et al. 2001; Menzel et al. 2010b). Surprisingly, however, none of these strategies are employed by parabiotic ants. ...
... Thereby, they reduce their viscosity and maintain their fluidity even with long hydrocarbon chains. In Crematogaster levior A, we found similar traits: longer chain lengths and higher abundances of alkenes and alkadienes than in the non-parabiotic Crematogaster species studied so far (Menzel et al. 2010b; Oettler et al. 2008). The existence of different chemotypes in both neotropical species is notable. ...
Mutualistic, commensalistic or parasitic interactions are unevenly distributed across the animals and plants: in certain taxa, such interspecific associations evolved more often than in others. Within the ants, associations between species of the genera Camponotus and Crematogaster evolved repeatedly and include trail-sharing associations, where two species share foraging trails, and parabioses, where two species share a nest without aggression. Camponotus and Crematogaster may possess life-history traits that favour the evolution of associations. To identify which traits are affected by the association, we investigated a neotropical parabiosis of Ca. femoratus and Cr. levior and compared it to a paleotropical parabiosis and a trail-sharing association. The two neotropical species showed altered cuticular hydrocarbon profiles compared to non-parabiotic species accompanied by low levels of interspecific aggression. Both species occurred in two chemically distinct types. Camponotus followed artificial trails of Crematogaster pheromones, but not vice versa. The above traits were also found in the paleotropical parabiosis, and the trail-following results match those of the trail-sharing association. In contrast to paleotropical parabioses, however, Camponotus was dominant, had a high foraging activity and often fought against Crematogaster over food resources. We suggest three potential preadaptations for parabiosis. First, Crematogaster uses molecules as trail pheromones, which can be perceived by Camponotus, too. Second, nests of Camponotus are an important benefit to Crematogaster and may create a selection pressure for the latter to tolerate Camponotus. Third, there are parallel, but unusual, shifts in cuticular hydrocarbon profiles between neotropics and paleotropics, and between Camponotus and Crematogaster.
... Escalating conflicts leading to injury or death are limited through avoidance, ritualized fights or when ant species with different rhythms of activity share food sources (Hölldobler and Wilson, 1990;Orivel and Dejean, 2002;van Wilgenburg et al., 2005). Also, by frequently displaying submissive behaviour or feigning death (thanatosis), dominated workers from species coexisting with very aggressive dominant ants suffer only brief and less harmful attacks (Langen et al., 2000;Grangier et al., 2007;Abril and Gomez, 2009;Menzel et al., 2010). ...
... Nevertheless, the decision to fight or not with a neighbour resides in (1) colony-mate recognition (the role of the CCs), (2) the behaviour of the workers (submissive or not) and (3) ecological characteristics of each species based on their propensity to compete for the same resources and the threat they represent. Indeed, DEP and NNE occur based on the potential costs and benefits related to foraging for food and territorial defence (Langen et al., 2000;Grangier et al., 2007;Abril and Gomez, 2009;Menzel et al., 2010). ...
... Superficially, these nests resemble xenobiotic parasitism, but the parabiotic partners are thought to coexist in a mutualism, with both species benefitting from the nesting association. This has been measured by quantifying the contribution of each species to foraging, nest defense, and third party mutualisms, such as with plants or honeydew producers32333435. However, one unmeasured cost of the parabiotic relationship could arise from a compromised recognition system. ...
... In particular, the social symbiosis has likely been facilitated by each species using unique informational channels, by producing a different range of chemical cues and maintaining species-specific colony odors. This may be one reason that these social symbioses are so rare amongst social insects, and yet so common amongst Camponotus ants [33,60] who have repeatedly evolved both heterospecific tolerance and unusual long-chain hydrocarbons [40]. Interference in the recognition system, a potential cost of living together, is minimized by such chemical innovations. ...
Social organisms rank among the most abundant and ecologically dominant species on Earth, in part due to exclusive recognition systems that allow cooperators to be distinguished from exploiters. Exploiters, such as social parasites, manipulate their hosts' recognition systems, whereas cooperators are expected to minimize interference with their partner's recognition abilities. Despite our wealth of knowledge about recognition in single-species social nests, less is known of the recognition systems in multi-species nests, particularly involving cooperators. One uncommon type of nesting symbiosis, called , involves two species of ants sharing a nest and foraging trails in ostensible cooperation. Here, we investigated recognition cues (cuticular hydrocarbons) and recognition behaviors in the parabiotic mixed-species ant nests of and in North-Eastern Amazonia. We found two sympatric, cryptic chemotypes in the population, with one type in each parabiotic colony. Although they share a nest, very few hydrocarbons were shared between and either chemotype. The hydrocarbons were also unusually long-chained branched alkenes and dienes, compounds not commonly found amongst ants. Despite minimal overlap in hydrocarbon profile, there was evidence of potential interspecific nestmate recognition - ants were more aggressive toward non-nestmates than nestmates. In contrast to the prediction that sharing a nest could weaken conspecific recognition, each parabiotic species also maintains its own aggressive recognition behaviors to exclude conspecific non-nestmates. This suggests that, despite cohabitation, parabiotic ants maintain their own species-specific colony odors and recognition mechanisms. It is possible that such social symbioses are enabled by the two species each using their own separate recognition cues, and that interspecific nestmate recognition may enable this multi-species cooperative nesting.
... including the ability to deter an invasive ant species (such as Linepithema humile)(HOLWAY 1999), competition for nest sites in the lab (LIVINGSTON & PHILPOTT 2010), or aggressive responses toward dead ants(MENZEL & al. 2010). ...
There is a long tradition of community ecologists using interspecific dominance hierarchies as a way to explain species coexistence and community structure. However, there is considerable variation in the methods used to construct these hierarchies, how they are quantified, and how they are interpreted. In the study of ant communities, hierarchies are typically based on the outcome of aggressive encounters between species or on bait monopolization. These parameters are converted to rankings using a variety of methods ranging from calculating the proportion of fights won or baits monopolized to minimizing hierarchical reversals. However, we rarely stop to explore how dominance hierarchies relate to the spatial and temporal structure of ant communities, nor do we ask how different ranking methods quantitatively relate to one another. Here, through a review of the literature and new analyses of both published and unpublished data, we highlight some limitations of the use of dominance hierarchies, both in how they are constructed and how they are interpreted. We show that the most commonly used ranking methods can generate variation among hierarchies given the same data and that the results depend on sample size. Moreover, these ranks are not related to resource acquisition, suggesting limited ecological implications for dominance hierarchies. These limitations in the construction, analysis, and interpretation of dominance hierarchies lead us to suggest it may be time for ant ecologists to move on from dominance hierarchies.
... A total of 22 CHCs were recorded by GC-MS analysis in the chemical profile of the ants. An example of a GC-MS chromatogram is reported in Fig 2 (see Ref [73] for a description of cuticular signatures in C. scutellaris). The most abundant compounds were linear alkanes, monomethylated alkanes, dimetyhylated alkanes and alkenes. ...
Nest-mate recognition plays a key role in the biology of ants. Although individuals coming from a foreign nest are, in most cases, promptly rejected, the degree of aggressiveness towards non nest-mates may be highly variable among species and relies on genetic, chemical and environmental factors. We analyzed intraspecific relationships among neighboring colonies of the dominant Mediterranean acrobat ant Crematogaster scutellaris integrating genetic, chemical and behavioral analyses. Colony structure, parental relationships between nests, cuticular hydrocarbons profiles (CHCs) and aggressive behavior against non nest-mates were studied in 34 nests located in olive tree trunks. Bayesian clustering analysis of allelic variation at nine species-specific microsatellite DNA markers pooled nests into 14 distinct clusters, each representing a single colony, confirming a polydomous arrangement of nests in this species. A marked genetic separation among colonies was also detected, probably due to long distance dispersion of queens and males during nuptial flights. CHCs profiles varied significantly among colonies and between nests of the same colony. No relationship between CHCs profiles and genetic distances was detected. The level of aggressiveness between colonies was inversely related to chemical and spatial distance , suggesting a 'nasty neighbor' effect. Our findings also suggest that CHCs profiles in C. scutellaris may be linked to external environmental factors rather than genetic relationships.
... Although there was obvious aggression in the studied parabioses, the overall aggression level was still much lower than between non-parabiotic species (Blüthgen & Fiedler, 2004;Menzel et al., 2008bMenzel et al., , 2010b. The parabiotic species frequently ignored each other (particularly at honey baits), and Crematogaster aggression mainly consisted of gaster-lifting, which indicates an aggressive state but does not necessarily deter or harm Camponotus (Fig. S1, Video S1). ...
1. Mutualisms are important drivers of co‐evolution and speciation. However, they typically imply costs for one or both partners. Each partner consequently tries to maximise benefits and minimise costs. Mutualisms can therefore develop towards commensalism or parasitism if one partner fails to provide sufficient benefits. This is particularly likely in diffuse interactions, where multiple species can associate with each other. If costs and benefits of a species vary with the identity of the partner species, this may result in a geographical mosaic of co‐evolution.
2. In the present study, inter‐specific interactions in two parabiotic associations of ants were studied (Hymenoptera: Formicidae). One Crematogaster species was associated with one of two closely related Camponotus species. We assessed cost and benefits by studying behavioural interactions, foraging behaviour, and nest defence in the associations.
3. While parabioses had been shown to be mutualistic, evidence was found for exploitation and aggressive competition between species. In spite of apparent costs of being exploited, we found no benefits for one partner ( Crematogaster ). The magnitude of potential costs to Crematogaster varied between the two Camponotus species.
4. We conclude that the cost/benefit ratio for Crematogaster varies between the two Camponotus partners, and between environmental conditions. Parabiosis can thus fluctuate between mutualism, commensalism, and parasitism, with Crematogaster being the species that may have higher costs than benefits.
5. We suggest that geneflow in the Crematogaster population hinders local adaptation to the resulting mosaic of locally varying selection pressures. This study demonstrates how diffuse interactions and environmental variation can result in a complex of local selection pressures.
Species interactions such as competition, antagonism and mutualism are thought to promote diversification in phenotypic traits and thus significantly contribute to species diversity on Earth. Cuticular hydrocarbons (CHCs) are the major components of the waxy layer covering basically all terrestrial arthropods. Most importantly they protect insects from desiccation and act as agents of chemical communication. The communication functions of CHCs are especially important in social insects, such as ants, bees, wasps or termites. Amongst other functions, ants use CHC profiles to identify mutualistic partner species. A special form of such a mutualism is parabiosis, i.e. two ant species mutualistically sharing the same nest. In this thesis, I investigate the causes and consequences for the divergence of CHC profiles in the parabiotic ant species Crematogaster levior and Camponotus femoratus from the South American rainforest. In Chapter 1, I elucidate the species status of chemically diverged morphs of the ants of both genera mentioned above and discuss which role CHCs could have mediating speciation. I conclusively demonstrate that both, Cr. levior and Ca. femoratus, in fact consist of two cryptic species that, despite only slight morphological differences, strongly differ in their CHC profiles and their genetic background. By in detail investigating CHC differences within and between the cryptic species, I identify several ultimate causes for variation of the CHC profiles in Chapter 2. Especially the parabiotic lifestyle led to strong changes such as elongations of the carbon backbone of the CHCs, in both cryptic species of Ca. femoratus, but only one of Cr. levior. Although the cryptic species are closely related, they show vastly different CHC profiles, which is why I further investigated if gene expression differences at the site of CHC biosynthesis might explain this in Chapter 3. In this chapter, I identify several candidate genes and their expression patterns as proximate causes for the CHC variation. In many cases I am able to show that the gene expression differences between the cryptic species are mirrored in the differences observed in their CHC profiles. The strong differences in CHC profiles are likely to have consequences for nestmate recognition and aggression behavior, which is why I investigated recognition within and between the cryptic species of Cr. levior in Chapter 4, trying to identify which substances or structural CHC classes are involved. In line with the hypothesis that elongations of the carbon backbone of CHCs make the molecules harder to perceive, I found that CHC extracts of the shorter-chained Cr. levior species were probably more perceivable and thus treated more aggressively. In Chapter 5, I examine if the species divergence was accompanied by trophic niche partitioning a) between the mutualistic partners and b) between the cryptic species of Cr. levior and Ca. femoratus. Here, the results imply that competition between the mutualists is mediated by a discovery- dominance trade-off and differences in the trophic niche. The differences between the cryptic species, however, were very subtle suggesting that there is either niche differentiation in dimensions I did not investigate so far or that these cryptic species might be an example for ‘neutral species’. Finally, in Chapter 6, I provide an overview on the levels and magnitude of variation in CHC profiles in ants, but also other insects. By reviewing up-to-date literature, I provide detailed insights into sources of fixed and plastic variation on the levels of individuals, social insect colonies, populations and species. Furthermore, I discuss which factors may lead to adaptive CHC changes and how these could be constraint by biosynthetical and biophysical mechanisms. In conclusion, this thesis unravels the existence of cryptic species using integrative taxonomy, provides important insights into the complexity of selection pressures shaping the evolution of CHC profiles and identifies several candidate genes that could be involved in divergence of such profiles. The divergence in CHC profiles could play an important role in mediating speciation. However, it is yet unclear if chemical differences mediated mate choice and led to prezygotic reproductive isolation or if the CHC profiles diverged through reinforcement after speciation. While CHC divergence enabling assortative mating would allow speciation even in sympatry, allopatric populations might diverge through isolation-by-distance, genetic drift or local adaptation reinforcing CHC differences. Furthermore, this thesis identifies the cryptic species of parabiotic ants as an interesting model system to examine how ecologically similar species might avoid competitive exclusion and potentially for the investigation of ‘neutral processes’ mediating species coexistence in tropical ecosystems.
1. The potential for competition is highest among species in close association. Despite net benefits for both parties, mutualisms can involve costs, including food competition. This might be true for the two neotropical ants Camponotus femoratus and Crematogaster levior, which share the same nest in a presumably mutualistic association (parabiosis).
2. While each nest involves one Crematogaster and one Camponotus partner, both taxa were recently found to comprise two cryptic species that show no partner preferences and seem ecologically similar. Since these cryptic species often occur in close sympatry, they might need to partition their niches to avoid competitive exclusion.
3. Here, we investigated first, is there interference competition between parabiotic Camponotus and Crematogaster, and do they prefer different food sources under competition? And second, is there trophic niche partitioning between the cryptic species of either genus?
4. Using cafeteria experiments, neutral lipid fatty acid and stable isotope analyses, we found evidence for interference competition, but also trophic niche partitioning between Camponotus and Crematogaster. Both preferred protein‐ and carbohydrate‐rich baits, but at protein‐rich baits Ca. femoratus displaced Cr. levior over time, suggesting a potential discovery‐dominance trade‐off between parabiotic partners. Only limited evidence was found for trophic differentiation between the cryptic species of each genus.
5. Although we cannot exclude differentiation in other niche dimensions, we argue that neutral dynamics might mediate the coexistence of cryptic species. This model system is highly suitable for further studies of the maintenance of species diversity and the role of mutualisms in promoting species coexistence.
While foraging, animals can form inter- and intraspecific social signalling networks to avoid similar predators. We report here that foragers of different native Asian honey bee species can detect and use a specialized alarm pheromone component, benzyl acetate (BA), to avoid danger. We analysed the volatile alarm pheromone produced by attacked workers of the most abundant native Asian honey bee, Apis cerana and tested the responses of other bee species to these alarm signals. As compared to nest guards, A. cerana foragers produced 3.38 fold higher levels of BA. In foragers, BA and (E)-dec-2-en-1-yl acetate (DA) generated the strongest antennal electrophysiological responses. BA was also the only compound that alerted flying foragers and inhibited A. cerana foraging. BA thereby decreased A. cerana foraging for risky sites. Interestingly, although BA occurs only in trace amounts and is nearly absent in sympatric honeybee species (respectively only 0.07% and 0.44% as much in A. dorsata and A. florea), the
Interactions between animals are not restricted to direct encounters. Frequently, individuals detect the proximity of others through cues unintentionally left by others, such as prey species assessing predation risk based on indirect predator cues. However, while the importance of indirect cues in predator–prey interactions has been intensely studied, their role in interactions among competitors, and their consequences for community structure, are little known to date. Ant communities are usually structured by aggressive interactions between competing species. Responding to cues of others should be useful to avoid competitors or discover food sources. In ants and other insects, such cues include chemical footprints, which they leave while walking.
Here, we investigated how different ant species respond to footprints of others. Ant colonies were confronted with footprints of other colonies or species, and the workers chose between cue‐bearing and cue‐free areas. Moreover, we determined the chemical composition of footprints, and compared the absolute quantities of footprint and cuticular hydrocarbons.
Ants of the species Lasius niger avoided footprints of non‐nestmate conspecifics, and tended to avoid footprints of two other species. We suggest that they avoided encounters with competitors to reduce costly fights. In contrast, three other ant species approached allospecific footprints, which may represent eavesdropping to find resources discovered by others. Three of the four ant species responded differently to nestmates and non‐nestmate footprints either through footprint‐following or antennation behavior. The chemical composition of footprints was species‐specific and largely congruent to cuticular hydrocarbons. Footprint quantities left by single workers represented 1/170 to 1/64 of the quantity of their cuticular hydrocarbons.
We showed that chemical footprints represent an important cue for behavioral decisions in ants. The ability to identify and respond to chemical footprints may represent an important strategy for insects to cope with competing species or colonies in their habitat.
Abstract
Behavioural responses of organisms are frequently affected by variation in resource availability. For eusocial insects, the nutritional status of the colony can modulate responses to chemical cues determining intra- and inter-colonial aggressiveness. Species co-occurrence in termites seems to be modulated by resource availability. Here, we tested the effects of resource availability on acceptance of chemical cues and aggressive behaviour in the Neotropical termite Nasutitermes aff. coxipoensis (Termitidae: Nasutitermitinae). Nasutitermes aff. coxipoensis nests were transplanted into three plots in which resource availability was manipulated over 4 months. Experiments were carried out to evaluate: (i) colony response to internal chemical cues and those of neighbouring colonies reared under the same resource levels; (ii) the choice among chemical paths of colonies reared at different resource levels; and (iii) inter-colony aggression to nestmates and to neighbouring colonies reared under the same resource levels. Our results suggest that resource availability affects acceptance of chemical cues, path choice and aggression in N. aff. coxipoensis. Resource availability may thus modulate behavioural responses influencing coexistence between termite species and other taxa at different spatial scales.
Significance statement
Environmental resource availability is known to limit a range of traits in animals and plants. Here, we report that resource availability is also responsible for changes in behavioural responses of termites. The behavioural modifications found in the present study contribute to our comprehension of ecological patterns in this important ecological group. This work increases our understanding of mechanisms of co-occurrence and coexistence of termite species, as well as patterns of termite species richness in distinct biomes.
In this study we investigated the relationship between spatial distance and intraspecific aggression in the Mediterranean tree-nesting ant Crematogaster scutellaris. Aggression tests were carried out in the field confronting group of workers (20 from each nest) collected from pairs of nests located at increasing distances one from the other (5, 10, 20, 40 and 80 meters). For each distance, 6 replicate tests, using different pairs of nests, were carried out. The probability of aggression and the time of the first aggressive event were recorded and modelled as a function of the distance between two nests using generalised linear models. Results showed that both the probability of aggression and the time of first attack were correlated to spatial distance in a complex way, having their maximum at intermediate distances between nests. The observed relationship cannot be simply interpreted according to the "dear enemy" or the "nasty neighbour" effects and contains elements in favour of both.
An essential challenge in invasion ecology is discerning the role that behavioural adaptations play in competition among species. When evaluating the impacts of invasive species, the mechanisms underlying coexistence among organisms and the displacement of organisms within a community mosaic are often ignored, yet these interactions are necessary for fully understanding these impacts. Here, we examine behavioural mechanisms underlying the coexistence and subsequent displacement of an established global invader, the Argentine ant, Linepithema humile Mayr, by the newly invasive Asian needle ant, Pachycondyla chinensis Emery. In individual and group assays, we show that the numerically and behaviourally dominant Argentine ant is less aggressive towards P. chinensis workers from adjacent versus distant nests. Moreover, we show that P. chinensis displays submissive behaviour through recurrent contact with L. humile, which may contribute to the reported displacement of L. humile in the field. Understanding the factors that drive the coexistence of these two ants may help explain how small populations of a behaviourally submissive exotic species become established.
Abstract Social parasitism is defined by the exploitation of the social mechanisms of one society by another whole society. Here, we use quantitative ecological data and experiments to identify the components of a new form of social parasitism by the recently discovered "mirror turtle ant," Cephalotes specularis. We show that C. specularis workers visually mimic and actively avoid contact with foragers of the hyperaggressive host ant Crematogaster ampla, allowing them to move freely in the extensive and otherwise defended foraging networks of host colonies. Workers from parasite colonies have immediate access to these networks by nesting exclusively within host territories, and 89% of all potential host territories were parasitized. Inside the network, parasite workers eavesdrop on the host's trail pheromones to locate and exploit food resources that are defended by the host to the exclusion of all other ants. Experiments demonstrated the unprecedented capacity of the parasite for superior foraging performance on its host's pheromone trails than on trails of its own. Considered together, the apparent Batesian-Wallacian mimicry, pheromone-based interceptive eavesdropping, kleptoparasitism, and xenobiotic nesting ecology displayed by C. specularis within the territory and foraging network of a host ant represents a novel adaptive syndrome for social exploitation.
Background
Parasitic, commensalistic, and mutualistic guests in social insect colonies often circumvent their hosts’ nestmate recognition system to be accepted. These tolerance strategies include chemical mimicry and chemical insignificance. While tolerance strategies have been studied intensively in social parasites, little is known about these mechanisms in non-parasitic interactions.
Here, we describe a strategy used in a parabiotic association, i.e. two mutualistic ant species that regularly share a common nest although they have overlapping food niches. One of them, Crematogaster modiglianii, produces an array of cuticular compounds which represent a substance class undescribed in nature so far. They occur in high abundances, which suggests an important function in the ant’s association with its partner Camponotus rufifemur.
Results
We elucidated the structure of one of the main compounds from cuticular extracts using gas chromatography, mass spectrometry, chemical derivatizations and nuclear magnetic resonance spectroscopy (NMR). The compound consists of two fused six-membered rings with two alkyl groups, one of which carries a keto functionality. To our knowledge, this is the first report on the identification of this substance class in nature. We suggest naming the compound crematoenone.
In behavioural assays, crematoenones reduced interspecific aggression. Camponotus showed less aggression to allospecific cuticular hydrocarbons when combined with crematoenones. Thus, they function as appeasement substances. However, although the crematoenone composition was highly colony-specific, interspecific recognition was mediated by cuticular hydrocarbons, and not by crematoenones.
Conclusions
Crematenones enable Crematogaster to evade Camponotus aggression, and thus reduce potential costs from competition with Camponotus. Hence, they seem to be a key factor in the parabiosis, and help Crematogaster to gain a net benefit from the association and thus maintain a mutualistic association over evolutionary time.
To our knowledge, putative appeasement substances have been reported only once so far, and never between non-parasitic species. Since most organisms associated with social insects need to overcome their nestmate recognition system, we hypothesize that appeasement substances might play an important role in the evolution and maintenance of other mutualistic associations as well, by allowing organisms to reduce costs from antagonistic behaviour of other species.
The integument of insects is generally covered with cuticular hydrocarbons (CHC). They serve multiple functions, most prominent among them waterproofing and-especially among social insects-as communication signal. CHC profiles are incredibly diverse within and across species. However, the causes for CHC variation between species, and potential selection pressures that may shape CHC profiles, are hardly understood. Here, we investigated potential selection pressures on ant CHC. We tested the hypotheses that living in association with another species (e.g., parabiosis), and the climate of the ant's habitat, affect CHC composition. We conducted a large-scale comparison of 37 Camponotus species from five continents. Our results demonstrate that closely associated ant species possess significantly longer hydrocarbons and higher proportions of methylbranched alkenes and alkadienes than non- or loosely associated species. In contrast, climatic factors had no effects. This study shows that the need to be tolerated by another species greatly affects CHC profiles.
The ant mosaic of the canopy of a Cameroonian rainforest was studied by directly sampling 167 large trees and 20 vines reaching the canopy level using a dirigible and the "canopy raft", the "canopy sled", and, when necessary, the single rope technique. Although plant species diversity was high (trees: 63 species from 29 families; vines: 9 species from 7 families), our results show an ant assemblage characterized by high abundance but low diversity (28 ant species in total). We recorded only four "dominant" ant species (i.e., species with populous colonies that build their own nests, exhibit strong territoriality, and have mutually exclusive territories distributed in a mosaic pattern). The most frequent species, Crematogaster depressa, occupied 87.4% of the trees and 85% of the vines, and its colonies reached several million workers. Other dominants were recorded at low frequencies (Crematogaster sp.1: 1.8% of the trees; Oecophylla longinoda: 6.0%; Tetramorium aculeatum: on one vine). Among the nine ant species tolerated on the territories of Cr. depressa (i.e., "non-dominant" species with smaller colonies), the workers of three species shared their trails with Cr. depressa, while Camponotus brutus, with colonies sometimes able to occupy the entire crown of a tree, rather had the status of "sub-dominant". Extrafloral nectaries (EFN) played a role in ant species distribution. The large ecological success of Cr. depressa is probably due to its ability to nest on trees with or without EFN. O. longinoda, which rarely tolerated non-dominant ant species, was significantly more frequently recorded on trees without EFN. While dominant ants depended principally on attended homopterans (Coccidae and Stictococcidae; globally: 300,000 to 700,000 individuals per tree), non-dominant species depended primarily on EFN.
Food and nesting space are the most important resources for ants and contribute strongly to the structure of ant communities. Most ants can be considered omnivores; however, differences in morphology and digestive capabilities constrain the availability of food sources and contribute to fundamental niche differentiation. Endosymbionts may play a crucial role in facilitating nitrogen uptake, nutrient balance, or food detoxification. The location and distribution of nest sites, and whether nests are static or dynamic, affect the diets that are available to ants, given their limited foraging range. Macronutrients in ant diets have been demonstrated to affect competition and territorial behaviour. When food is available continuously, territoriality and permanent nests may be favoured, while short-lived food sources require more frequent nest relocation. Consequently, nest types are highly variable, ranging from relatively persistent nests in the ground or wood cavities to dynamic, flexible bivouacs formed only by the worker's bodies.
Plesiobiosis is a rudimentary form of social symbiosis. It consists of the close proximity of nests of different social insect species. Numerous cases of plesiobiosis between ant species observed in a successional series of rocky habitats in S Finland are listed and the most interesting of them are described in detail. Among all Lasius colonies found within the whole successional series studied, as many as 8.4% were plesiobiotically associated with other ants. In the two earliest successional stages: the shore meadow and the open rocky outcrop, the proportion was nearly 12% and 10% respectively. The finding of numerous plesiobiotically related nests there is discussed in the context of the unique local habitat conditions.
Abstract The concept of ‘ant mosaics’ has been established to describe the structure of arboreal ant communities in plantations and other relatively simple forest systems. It is essentially built upon the existence of negative and positive associations between ant species plus the concept of dominance hierarchies. Whether this concept can be applied to ant communities in more complex mature tropical rain forests has been questioned by some authors. Here we demonstrate that some previous attempts to prove or disprove the existence of such ant mosaics sampled by knockdown insecticide canopy fogging in near pristine tropical forests may have been thwarted by poor statistical power and too coarse spatial resolution, and the conclusions may be highly dependent on ant species and forest stratum selected for the study. Moreover, the presence or absence of ant mosaics may be driven by the density of suitable resources. We use an intensively studied ant community in the lowland rainforests of North-East Queensland, Australia to outline processes that may lead to ant mosaic patterns, reasoning that competition for highly predictable resources in space and time such as honeydew and nectar is a fundamental process to maintain the mosaic structure. Honeydew and nectar sources, particularly their amino acids, are of crucial importance for nourishment of arboreal ant species. We use canopy fogging data from the same site in Australia and from two mature rainforests in South-East Asia to compare spatial avoidance and co-occurrence patterns implied by ant mosaics. Significant negative and positive associations were found among the three most abundant ant species in each dataset. Several problems with such spatial analyses are discussed, and we suggest that studies of ant mosaics in complex rainforest communities would benefit from a more focused approach on patterns of resource distribution and their differential utilisation by ants.
Gnamptogenys menadensis (subfamily Ponerinae) foragers use chemical trails to home to their nests. Although prey capture and retrieval are generally performed solitarily, trails seem to enhance foraging to areas rich in prey or to sugar sources. Trail laying and following are most conspicuous during nest migration. These trails are laid down by tapping the sting onto the substrate. In laboratory tests, only extracts from the Dufour's gland were readily followed. Workers of Polyrhachis rufipes (Formicinae) use the trails of G. menadensis to gain access to otherwise nonavailable sugar sources. When they encounter Gnamptogenys foragers, P. rufipes workers show a typical aggressive antennal boxing, to which Gnamptogenys reacts with a submissive behavior. This is the first report of commensalism between a ponerine and a formicine ant.
Due to the invasive character of the exotic Argentine ant (Linepithema humile), its use of aphids in trees, and the ecological importance of the Doana National Park (Spain) that is invaded by this species, we designed a study to analyze the extent of the problem with native species of arboreal ants. By searching for de visu the species that inhabited 182 cork trees, we found out that the structure of the community of native arboreal ants has been greatly influenced by interspecific competition. The introduced species L. humile and the native species Crematogaster scutellaris and Lasius brunneus are dominant, while Camponotus lateralis and Camponotus truncatus are subordinate species associated with C. scutellaris. The distribution of the species in the trees depends on these relationships. Species richness is determined by tree size, thus, when a tree is large enough all native species may appear together. However, in areas colonized by L. humile, this is the only species occupying the tree, regardless of tree size. L. humile is displacing native arboreal ant species as shown by the fact that from 1992 to 2000 the exotic species occupied 23 new cork trees (of the 182 studied) previously inhabited by native species.
A common and confusing problem in analyses of insect hydrocarbons is in making sense of complicated gas chromatograms and interpreting mass spectra since branched chain compounds differing by one or two carbons in backbone or chain length may elute from the column at nearly the same time. To address this confusing situation, relative gas chromatography (GC) retention times are presented for typical mono-, di-, tri-, and tetramethylalkanes comprising most of the commonly appearing series of homologous methyl-branched alkanes up to 53 carbons that are found in insect cuticular hydrocarbons. Typical insect-derived methylalkanes with backbones of 33 carbons were characterized by Kovats indices (KI); monomethyl alkanes elute between KI 3328 and 3374, dimethylalkanes elute between KI 3340 and 3410, trimethylalkanes elute between KI 3378 and 3437, and tetramethylalkanes elute between KI 3409 and 3459, depending upon the positions of substituents. A protocol is described for identification of methyl-branched hydrocarbons eluted from nonpolar polysiloxane DB-1 capillary GC columns. In this protocol, retention indices (KI values) are assigned to peaks, then the patterns in GC peaks that probably contain homologs are marked to assist subsequent GC-mass spectrometric (GC-MS) interpretation. Use of the KI allows assignment of likely structures and the elimination of others, with demonstrative consistency, as there are no known exceptions. Interpretation of electron ionization mass spectra can then proceed within narrowed structural possibilities without the necessity of chemical ionization GC-MS analysis. Also included are specific examples of insect hydrocarbons that were assembled from 30 years of the literature, and these are intended to help with confirmation of confusing or contradictory structures.
This study focuses on different factors affecting the level of aggression in the desert ant Cataglyphis fortis. We found that the readiness to fight against conspecific ants was high in ants captured close to the nest entrance (0- and 1-m distances). At a 5-m distance from the nest entrance the level of aggression was significantly lower. As the mean foraging range in desert ants by far exceeds this distance, the present account clearly shows that in C. fortis aggressive behavior is displayed in the context of nest, rather than food-territory defense. In addition, ants were more aggressive against members of a colony with which they had recently exchanged aggressive encounters than against members of a yet unknown colony. This finding is discussed in terms of a learned, enemy-specific label-template recognition process.
In this paper we test the influence of temperature and interference competition by dominant species on the foraging of subordinate
species in Mediterranean ant communities. We have analyzed the changes in resource use by subordinate species in plots with
different abundances of dominant ants, and in different periods of the day and the year, i.e., at different temperatures.
The expected effects of competition by dominant species on foraging of subordinates were only detected for two species in
the number of baits occupied per day, and for one species in the number of foragers at pitfall traps. In all three cases,
subordinate species were less represented at baits or in traps in plots with a high density of dominants than in plots with
a medium or low density of dominants. The number of workers per bait, and the foraging efficiency of subordinate species did
not differ in plots differing in dominant abundance. Daily activity rhythms and curves of temperature versus foraging activity
of subordinate species were also similar in plots with different abundance of dominant species, indicating no effect of dominants
on the foraging times of subordinates. Instead, temperature had a considerable effect on the foraging of subordinate species.
A significant relationship was found between maximum daily temperature and several variables related to foraging (the number
of foragers at pitfall traps, the number of baits occupied per day, and the number of workers per bait) of a number subordinate
species, both in summer and autumn. These results suggest that the foraging of subordinate ant species in open Mediterranean
habitats is influenced more by temperature than by competition of dominants, although an effect of dominants on subordinates
has been shown in a few cases. In ant communities living in these severe and variable environments, thermal tolerance reduces
the importance of competition, and the mutual exclusion usually found between dominant and subordinate species appears to
be the result of physiological specialization to different temperature ranges.
In French Guiana, parabiotic societies (natural mixed colonies) are frequently found in ant gardens. Crematogaster limata parabiotica (Myrmicinae), often associated with Camponotus femoratus (Formicinae), was found for the first time in parabiosis with ponerine ants: Pachycondyla goeldii and Odontomachus mayi. A detailed study of the relationships between Cr. l. parabiotica and O. mayi showed that each species is aggressive towards allospecific or conspecific individuals belonging to another colony, but tolerates
allospecific individuals from the multi-species society. Studies of cuticular substances of the four ant species were made
using gas chromatography. The results showed that each species, living alone or in parabiosis, possesses a specific chemical
profile. Thus, the ants are able to recognise nestmate and non-nestmate individuals of the associated species, even though
their cuticular profiles are different. The hypothesis that the nestmate allospecific profile is learned is suggested to explain
this pattern of recognition.
Ant-gardens represent a special type of association between ants and epiphytes. Frequently, two ant species can share the
same nest in a phenomenon known as ‘parabiosis’, but the exact nature (i.e., mutualistic or parasitic) of this interaction
is the subject of debate. We thus attempted to clarify the mutual costs and benefits for each partner (ants and plants) in
the Crematogaster levior/Camponotus femoratus ant-garden parabiosis. The ants’ response to experimental foliar damage to the epiphytes and to the host tree as well as
their behavior and interactions during prey capture were investigated to see if the purported parasitic status of Cr. levior could be demonstrated in either the ant-ant or in the ant-plant interactions. The results show that both species take part
in protecting the epiphytes, refuting the role of Cr. levior as a parasite of the ant-garden mutualism. During capture of large prey Ca. femoratus took advantage from the ability of Cr. levior to discover prey; by following Cr. levior trails Ca. femoratus workers discover the prey in turn and usurp them during agonistic interactions. Nevertheless, the trade-off between the costs
and benefits of this association seems then to be favorable to both species because it is known that Cr. levior benefits from Ca. femoratus building the common carton nests and furnishing protection from vertebrates. Consequently, parabiosis can then be defined
as the only mutualistic association existing between ant species, at least in ant-gardens.
Many species of territorial animals are more aggressive toward strangers than neighbors, a pattern of aggression referred
to as the ’dear-enemy phenomenon.’ In many cases, the mechanism by which neighbors are discriminated from strangers and the
function of neighbor-stranger discrimination remain controversial. We investigated the spatial patterns of inter-colony aggression
within and between two Pheidole species of seed-harvesting ants in the Mojave Desert of California by quantifying aggression between colonies in standardized
staged encounters. We also tested whether the level of fighting between workers of two colonies is affected by previous exposure
to each other. We show that neighbors (i.e., colonies less that 2.6 m away) of either species are treated less aggressively
than more distant colonies and that habituation may be a mechanism by which this discrimination is achieved. The variation
in aggression among spatially distant colonies also suggests that additional genetic or environmental factors are involved
in recognition. The function of the dear-enemy phenomenon in these ant species may be related to the greater risk to the resources
of a colony presented by strange workers than workers from a neighboring colony.
Trophobiotic interactions between ants, hemipterans and plants play an important role for all three partners. This study compared
a broad spectrum of trophobiotic associations in a tropical rainforest in Sabah, Borneo. We studied partner specificity, ant
recruitment, temporal continuity and monopolisation in 218 trophobioses, comprising 58 ant species, 62 hemipteran and over
31 plant species. The most common associations involved Dinochloa trichogona (Poaceae) with coreids and delphacids in the forest understorey, and the invasive weed Chromolaena odorata (Asteraceae) with Aphis gossypii and A. spiraeola in the open vegetation; both associations were attended by a broad spectrum of ant species. In general, associations between
hemipterans and plants were highly and significantly specialised, while ants were more opportunistic in their choices of partners,
although partitioning was also significant between ant versus hemipteran species and consequently between ant versus plant
species. The number of ant workers increased significantly, but at a declining rate, with the number of hemipterans at a trophobiosis.
Most trophobioses (96%) were only tended by a single ant species at a time and thus effectively monopolised. Occasionally
these guards were replaced by another ant species after a few weeks (11%) or during the night (34%). In order to test whether
other sugar-seeking ants as potential competitors occurred in the vicinity of trophobioses, sugar baits were placed next to
the trophobioses, on a different branch of the same plant, and on a neighbouring plant. While the hemipteran-tending ant colony
mostly monopolised the nearest sugar bait, the number of ant species on more distant baits was significantly higher. Our results
show that ant associations with honeydew-producing hemipterans may be relatively opportunistic at the community level, but
highly predictable on a smaller spatio-temporal scale in respect to recruitment to, and long term securing of this important
resource.
Hymenoptera is a very large and diverse insect order that includes the majority of both the social and the parasitic insects. With such diversity comes a variety and complexity of semiochemicals that reflect the varied biology of members of this order. This chapter reviews the chemical identification of pheromones and semiochemicals in the order Hymenoptera since 1990. For this review, the species in Hymenoptera have been classified as solitary, parasitic, or social. The chemical diversity of semiochemicals in Hymenoptera and future trends in pheromone identification are also discussed.
1. The huge diversity of symbiotic associations among animals and/or plants comprises both mutualisms and parasitisms. Most symbioses between social insect species, however, involve social parasites, while mutual benefits have been only suspected for some parabiotic associations – two colonies that share a nest.
2. In the rainforest of Borneo, we studied parabiotic associations between the ants Crematogaster modiglianii and Camponotus rufifemur. Parabiotic nests were regularly found inside hollow tree trunks, most likely initiated by Cr. modiglianii. This species frequently nested without its partner, whereas we never found non-parabiotic Ca. rufifemur nests. We experimentally investigated potential benefits, potential interference competition for food (as a probable cost), and foraging niches of both species.
3. The two species never showed aggressive interactions and amicably shared food resources. However, Cr. modiglianii had a wider temporal and spatial foraging range than Ca. rufifemur, always found baits before Ca. rufifemur and recruited more efficiently. Camponotus rufifemur probably benefited from following pheromone trails of Cr. modiglianii. In turn, Ca. rufifemur was significantly more successful in defending the nest against alien ants. Crematogaster modiglianii hence may profit from its partner’s defensive abilities.
4. In neotropical parabioses, epiphytes grown in ‘ant-gardens’ play a crucial role in the association, e.g. by stabilization of nests. Hemiepiphytic Poikilospermum cordifolium (Cecropiaceae) seedlings and saplings frequently grew in the entrances of parabiotic nests in Borneo, obviously dispersed by the ants. In cafeteria experiments, both parabiotic ants carried its elaiosome-bearing seeds into the nest. However, P. cordifolium does not provide additional nest space, contrasting with neotropical ant-gardens.
5. The parabiotic association appears beneficial for both ant species, the main benefits being nest initiation by Cr. modiglianii and interspecific trail-following (for Ca. rufifemur), and, in turn, nest defence by Ca. rufifemur (for Cr. modiglianii). However, Ca. rufifemur seems to be more dependent on its partner than vice versa.
We compared the published cuticular hydrocarbon (CHC) profiles of 78 ant species across 5 subfamilies. Almost 1,000 CHCs have been described for these species, composing 187 distinct homologous series and ten hydrocarbon groups. In descending order of occurrence were: n-alkanes > monomethylalkanes > dimethylalkanes > alkenes > dienes> trimethylalkanes> methylalkenes > methylalkadienes > trienes > tetramethylalkanes. Odd chain lengths and positions of methyl or double bonds at odd carbon numbers were far more numerous than even chain-length compounds or bond positions. Although each species possess its own unique pattern of CHCs, we found no association between CHC profile and phylogeny. The production of the biosynthetically complex compounds (e.g., methyl branched dienes) by the most primitive living ant suggests that the basic genetic architecture required to produce the rich diversity of CHCs was already present prior to their adaptive radiation. Unlike the ubiquitous n-alkanes and monomethylalkanes, there is a huge diversity of species-specific dimethylalkanes that makes them likely candidates for species and nest-mate discrimination signals.
Associations between animal species require that at least one of the species recognizes its partner. Parabioses are associations of two ant species which co-inhabit the same nest. Ants usually possess an elaborate nestmate recognition system, which is based on cuticular hydrocarbons and allows them to distinguish nestmates from non-nestmates through quantitative or qualitative differences in the hydrocarbon composition. Hence, living in a parabiotic association probably necessitates changes of the nestmate recognition system in both species, since heterospecific ants have to be accepted as nestmates.
In the present study we report highly unusual cuticular profiles in the parabiotic species Crematogaster modiglianii and Camponotus rufifemur from the tropical rainforest of Borneo. The cuticle of both species is covered by a set of steroids, which are highly unusual surface compounds. They also occur in the Dufour gland of Crematogaster modiglianii in high quantities. The composition of these steroids differed between colonies but was highly similar among the two species of a parabiotic nest. In contrast, hydrocarbon composition of Cr. modiglianii and Ca. rufifemur differed strongly and only overlapped in three regularly occurring and three trace compounds. The hydrocarbon profile of Camponotus rufifemur consisted almost exclusively of methyl-branched alkenes of unusually high chain lengths (up to C49). This species occurred in two sympatric, chemically distinct varieties with almost no hydrocarbons in common. Cr. modiglianii discriminated between these two varieties. It only tolerated workers of the Ca. rufifemur variety it was associated with, but attacked the respective others. However, Cr. modiglianii did not distinguish its own Ca. rufifemur partner from allocolonial Ca. rufifemur workers of the same variety.
We conclude that there is a mutual substance transfer between Cr. modiglianii and Ca. rufifemur. Ca. rufifemur actively or passively acquires cuticular steroids from its Cr. modiglianii partner, while the latter acquires at least two cuticular hydrocarbons from Ca. rufifemur. The cuticular substances of both species are highly unusual regarding both substance classes and chain lengths, which may cause the apparent inability of Cr. modiglianii to discriminate Ca. rufifemur nestmates from allocolonial Ca. rufifemur workers of the same chemical variety.
Social parasites are able to exploit their host's communication code and achieve social integration. For colony foundation, a newly mated slave-making ant queen must usurp a host colony. The parasite's brood is cared for by the hosts and newly eclosed slave-making workers integrate to form a mixed ant colony. To elucidate the social integration strategy of the slave-making workers, Polyergus rufescens, behavioural and chemical analyses were carried out. Cocoons of P. rufescens were introduced into subcolonies of four potential host species: Formica subgenus Serviformica (Formica cunicularia and F. rufibarbis, usual host species; F. gagates, rare host; F. selysi, non-natural host). Slave-making broods were cared for and newly emerged workers showed several social interactions with adult Formica. We recorded the occurrence of abdominal trophallaxis, in which P. rufescens, the parasite, was the donor. Social integration of P. rufescens workers into host colonies appears to rely on the ability of the parasite to modify its cuticular hydrocarbon profile to match that of the rearing species. To study the specific P. rufescens chemical profile, newly emerged callows were reared in isolation from the mother colony (without any contact with adult ants). The isolated P. rufescens workers exhibited a chemical profile closely matching that of the primary host species, indicating the occurrence of local host adaptation in the slave-maker population. However, the high flexibility in the ontogeny of the parasite's chemical signature could allow for host switching.
Using bioassays, the defensive behaviour of Crematogaster scutellaris and the biological activities of its abdominal secretion were investigated. Beside classical aggressive behaviours such as grips, C. scutellaris workers performed frequent characteristic gaster flexions during interspecific encounters, sometimes tempting to apply their abdominal secretion topically on the enemy. The toxicity of the venom of C. scutellaris to other ants greatly differed among the species tested, some being killed after the topical application of only three droplets, while others were quite resistant to a dose of 90 droplets. All ant species tested were strongly and immediately repelled by a contact between their antennae or mouthparts with the venom of C. scutellaris. Abdominal secretion was never used during intraspecific interference and workers were resistant to a topical application of the venom of their own species. Intraspecific repellency was significant but moderate compared to interspecific one. Workers of C. scutellaris were never seen using their venom during prey capture. In conclusion, the main biological activity of the abdominal secretion of C. scutellaris seems to be its repellency to other ant species. This is supported by field experiments showing that Pheidole pallidula foragers were efficiently repelled at coexploited baits, allowing the monopolization of most prey by C. scutellaris.
The mechanism by which palatable species take advantage of their similarity in appearance to those that are unpalatable, in order to avoid predation, is called Batesian mimicry. Several arthropods are thought to be Batesian mimics of social insects; however, social insects that are Batesian mimics among themselves are rare. In Malaysia we found a possible Batesian mimic in an arboreal ant species, Camponotus sp., which was exclusively observed on foraging trails of the myrmicine ant Crematogaster inflata. The bright yellow and black colouring pattern, as well as the walking behaviour, were very similar in both species. We observed general interactions between the two species, and tested their palatability and the significance of the remarkably similar visual colour patterns for predator avoidance. Prey offered to C. inflata was also eaten by Camponotus workers in spite of their being attacked by C. inflata, indicating that Camponotus sp. is a commensal of C. inflata. An experiment with chicks as potential predators suggests that Camponotus sp. is palatable whereas C. inflata is unpalatable. After tasting C. inflata, the chicks no longer attacked Camponotus sp., indicating that Camponotus sp. is a Batesian mimic of Crematogaster inflata.
The little fire ant Wasmannia auropunctata is able to develop highly dominant populations in disturbed areas of its native range, with a resulting negative impact on ant diversity. We report here on the tolerance of such populations towards several fungus-growing ants of the genus Cyphomyrmex (rimosus complex) in French Guiana. This tolerance is surprising given the usually high interspecific aggressiveness of W. auropunctata when dominant. In order to understand the mechanisms behind such proximity, aggressiveness tests were performed between workers of the different species. These behavioural assays revealed a great passivity in Cyphomyrmex workers during confrontations with W. auropunctata workers. We also found that the aggressiveness between W. auropunctata and two Cyphomyrmex species was more intense between distant nests than between adjacent ones. This dear-enemy phenomenon may result from a process of habituation contributing to the ants' ability to coexist over the long term.
Social parasites are involved in a coevolutionary arms race, which drives increasing specialization resulting in a very narrow host range. The Formicoxenus ants are a small group of social parasites with a xenobiotic lifestyle. Formicoxenus quebecensis and Formicoxenus provancheri are highly specialized ants using chemical mimicry to blend into their respective Myrmica ant host colonies. However, Formicoxenus nitidulus is unique in being able to survive in over 11 different ant host species. We observed that when live or dead F. nitidulus adults are seized by their host they are immediately dropped undamaged, despite possessing a cuticular hydrocarbon profile that differs markedly from its host. Hexane extracts of the F. nitidulus cuticle made previously acceptable prey items unattractive to their Formica host, indicating a chemical deterrent effect. This is the first time that a social parasite has been shown to exploit the generalized deterrence strategy to avoid host aggression over long periods of time. This supports the idea that coevolved and generalist diseases or parasites require fundamentally different defence mechanisms. We suggest that F. nitidulus uses its cuticular chemistry, possible alkadienes, as a novel deterrent mechanism to allow it to switch hosts easily and so become a widespread and abundant social parasite.
Ants of the genus Camponotus are able to discriminate recognition cues of colony members (nestmates) from recognition cues of workers of a different colony (non-nestmates) from a distance of 1 cm. Free moving, individual Camponotus floridanus workers encountered differently treated dummies on a T-bar and their behavior was recorded. Aggressive behavior was scored as mandibular threat towards dummies. Dummies were treated with hexane extracts of postpharyngeal glands (PPGs) from nestmates or non-nestmates which contain long-chain hydrocarbons in ratios comparable to what is found on the cuticle. The cuticular hydrocarbon profile bears cues which are essential for nestmate recognition. Although workers were prevented from antennating the dummies, they showed significantly less aggressive behavior towards dummies treated with nestmate PPG extracts than towards dummies treated with non-nestmate PPG extracts. In an additional experiment, we show that cis-9-tricosene, an alkene naturally not found in C. floridanus' cuticular profile, is behaviorally active and can interfere with nestmate recognition when presented together with a nestmate PPG extract. Our study demonstrates for the first time that the complex multi-component recognition cues can be perceived and discriminated by ants at close range. We conclude that contact chemosensilla are not crucial for nestmate recognition since tactile interaction is not necessary.
The ability to recognize group members is a key characteristic of social life. Ants are typically very efficient in recognizing non-group members and they aggressively reject them in order to protect their colonies. There are a range of different recognition mechanisms including prior association, phenotype matching, and recognition alleles. The concept of kin recognition should be considered different from that of nestmate recognition. Most of the available studies address the nestmate recognition level, namely the discrimination of nestmates from non-nestmates, independently of actual relatedness. Indirect and direct evidence identify long-chain cuticular hydrocarbons as the best candidates to act as recognition cues in ants, even if other chemical substances could also play a role, at least in some ant species. The relative importance of genetic and environmental factors on the expression and variation of the cuticular hydrocarbon profile vary among species and is linked to life history strategies.
Differences in social organization and behaviour rank ant species into a competition hierarchy (starting with superior competitors): territorials (eg the Formica rufa-group red wood ants), encounterers (eg Camponotus, Lasius niger), and submissives (eg Formica fusca). Territorials and encounterers behave aggressively against individuals of alien colonies; these species are not expected to co-occur. Submissives behave recessively and may coexist with stronger species, but their forager numbers and nest densities should decrease. Submissives showed complementary abundances with territorials in terms of forager numbers on the baits, and their nest densities within the territory increased toward its periphery. Pressure by territorial and encounter species on the baits caused the submissive species to shift from protein to carbohydrates. Territorials and encounterers had complementary occurrences on the baits. The nests of territorials were far apart, with only occasional nests of encounter species at the outskirts of the territory. In the late successional habitats of the boreal taiga biome superior territorial competitors, especially the polycalic red wood ant species, assume the role of organizing centers on ant species assemblages. -from Authors
The behavioral organization of territoriality in the green tree ant (Oecophylla smaragdina) was studied in the field of North Queensland, Australia. The establishment and maintenance of territories in O. smaragdina is based on a complex behavioral communication repertory which appears to be almost identical to that of its only living congeneric species, the African weaver ant O. longinoda. In our study areas, individual territories sometimes covered an area of up to 1500 m2 comprising 21 major trees. The polydomous nest organization makes it possible for an Oecophylla colony to patrol and crop much of the volume of the territory in a very cost efficient way. The guard and defense force which consists primarily of old workers with reduced fatbodies and ovaries, is housed in special barrack nests, located at the territorial boundary. A selective "enemy identification" seems to be the major behavioral mechanism for interspecific territoriality and for the mosaic distribution of ecologically dominant ant species.
In Chile, Camponotus morosus and Solenopsis gayi sometimes co-inhabit a single nest, seemingly in a parabiotic association. To elucidate the nature of this association we conducted behavioural tests that measured aggression between homo- and allospecific ants. These tests revealed that C. morosus was aggressive towards alien conspecific and allospecific ants, but tolerated allospecific individuals from the same parabiotic society as well as allospecific individuals from a different parabiotic colony. In contrast S. gayi was much more tolerant towards alien ants whether homo- or allospecific and irrespective of their colony of origin, parabiotic or non-parabiotic.
Chemical analyses showed that each species possess a distinct cuticular hydrocarbons profile. Moreover, each species tended to keep its specific profile even when living in association with the other species, in spite of very little acquired allospecific chemicals in C. morosus, dismissing chemical mimicry as the basis of the peaceful co-existence. We hypothesise that the switch from aggression to tolerance as a consequence of parabiotic association exhibited by C. morosus is due to a familiarisation as well as memorisation of the allospecific colonial odour. The finding that the parabiotic C. morosus was tolerant to S. gayi, even if they originated from a non-parabiotic nest points to an odour generalisation ability in this species.
Ants of the genus Formicoxenus are called xenobiotic ants because they live in close association with their Myrmica host; they cannot live independently of the host but they keep their brood apart. They forage in the host's galleries and obtain food from it through trophallaxies. They also very frequently lick the Myrmica workers and for that reason are called “shampoo ants”. The chemical basis of the integration of the parasite into the host society is studied. In the two host-parasite pairs F. provancheri/M. incompleta and F. quebecensis/M. alaskensis, chemical mimicry in the cuticular hydrocarbons was found. With adoption experiments it is shown that this mimicry was not innate but is acquired during the first days of adult life.
The African weaver ant (Oecophylla longinoda) is known to be highly aggressive toward conspecific aliens. In the study area Shimba Hills Reserve (Kenya) individual territories sometimes covered an area of up to approximately 1600 m2, comprising 17 major trees. The territorial defense is organized by an elaborate defense recruitment system, which can also be aimed against several other ant species, which are potential competitors of Oecophylla for essential resources. This selective “enemy identification” seems to be the major behavioral mechanism by which the mosaic distribution of ecologically dominant ants is regulated.
Abstract 1. The organisation of an ant assemblage inhabiting an olive orchard in central Italy was analysed and patterns of dominance among ant species were described in order to assess (i) the relationship between thermal dependency and degree of behavioural dominance, and (ii) the relationship between dominance and discovery ability.
2. Activity patterns of the most abundant species on trees were examined in a sample of 120 trees during spring and summer. The degree of behavioural dominance and the ability of different species to discover new food sources were assessed using tuna baiting on a subset of 80 trees.
3. Different ant species showed contrasting patterns of activity. Some species (such as Lasius lasioides, Camponotus lateralis, and Camponotus piceus) were most active during the warmer part of the day, while others restricted their activity to the cooler hours (Camponotus aethiops and Plagiolepis pygmaea). Some species (such as Crematogaster scutellaris) were active irrespective of the time of day.
4. No clear relationship was observed between temperature of maximal activity and degree of behavioural dominance. There was, however, a positive relationship between behavioural dominance and thermal range of activity. A positive relationship between dominance and ability to find resources, with the most behaviourally dominant and aggressive species being most efficient in finding food items, was also observed.
5. The results support the idea that the temperature–dominance relationship is much more complex in Mediterranean-type habitats than in other ecosystems. Of particular interest is the positive dominance–discovery relationship. This finding contrasts with previous investigations, which reported a negative relationship between dominance and discovery ability and suggested that this pattern plays a role in promoting the coexistence of species in ant communities.
1. Trail‐sharing between different ant species is rare and restricted to a small number of species pairs. Its underlying mechanisms are largely unknown. For trail‐sharing to occur, two factors are required: (i) one or both species must recognise the other species or its pheromone trails and (ii) both species must tolerate each other to a certain extent to allow joint use of the trail. A species that follows another's trails can efficiently exploit the other's information on food sources contained in the pheromone trails. Hence, food competition and thus aggressive interactions between a species following another's trail and the species being followed, seem likely.
2. In the present study, we investigated interspecific trail following and interspecific aggression in trail sharing associations (i) among Polyrhachis ypsilon , Camponotus saundersi , and Dolichoderus cuspidatus , and (ii) among Camponotus rufifemur and Crematogaster modiglianii . We tested whether trail‐sharing species follow each other's pheromone trails, and whether the ants tolerated or attacked their trail‐sharing partners. In both associations, we confronted workers with pheromone trails of their associated species, and, for the former association, measured interspecific aggression among the trail‐sharing species.
3. In our assays, D. cuspidatus and C. rufifemur regularly followed heterospecific pheromone trails of P. ypsilon and C. modiglianii , respectively. However, only few workers of the remaining species followed heterospecific pheromone trails. Thus, shared trails of P. ypsilon and C. saundersi cannot be explained by interspecific trail‐following.
4. Interspecific aggression among P. ypsilon , C. saundersi , and D. cuspidatus was strongly asymmetric, C. saundersi being submissive to the other two. All three species differentiated between heterospecific workers from the same or another site, suggesting habituation to the respective trail‐sharing partners. We therefore hypothesise that differential tolerance by dominant ant species may be mediated by selective habituation towards submissive species and this way determines the assembly of trail‐sharing associations.
By means of gas chromatography, gas
chromatographic coupled mass spectrometry and behavioral
analysis the major trail pheromone components from the
hindgut of the formicine species Camponotus castaneus, C.
balzani and C. sericeiventris were identified. The trail
pheromone of C. castaneus is 3,5-dimethyl-6-(1-methylpropyl)-
tetrahydro-2H-pyran- 2-one, and that of the other
two species is 3,4-dihydro-8-hydroxy-3,5,7-trimethylisocoumarin.
Although both compounds release precise trail
following behavior in the respective species, the major
recruitment signal in the three Camponotus species appears
to be formic acid discharged from the poison gland. The
composition of the Dufour gland secretions of C. castaneus
and C. sericeiventris is similar, but that of the hypertrophied
Dufour gland of C. balzani is very different from any other
Camponotus Dufour gland content described up to date: it
contains large amounts of esters, the major compound of
which is octyl hexanoate, which makes up 97% a/a of the
total volatiles.
To investigate the role of template plasticity in shaping nest-mate recognition processes in ants, we constructed experimental
mixed-species groups of Manica rubida with either Myrmica rubra, Tetramorium bicarinatum or Formica selysi. Selecting Ma. rubida as the focal species, we observed the behaviour within mixed-species groups and the transfer rates of cuticular hydrocarbons
(CHC) onto the focal ants, and we also tested the aggression of the focal species reared either alone or in association with
each of the three different species. We show that Ma. rubida workers were always amicable towards their mixed group members, as towards members of the respective parental colonies, irrespective
of the associated species. They did, however, express different levels of aggression towards single-species groups of the
other species tested, depending on the species with which they were reared. The study suggests that similarity in CHC profiles
in two species leads to a narrow template in mixed groups, while dissimilarity is followed by lower levels of aggression (a
broader template), at least against species with similar CHC compound compositions (i.e. both a broader template in the focal
ants and familiarity with the compound groups of the tested individuals operate together). This refutes the hypothesis that
ants reared in mixed-species groups are systematically more tolerant. It also demonstrates that heterospecific information
is not treated equally during development. We suggest that post-imaginal learning, template reforming and decision making
are more precisely tuned when the two species' chemical complexes are similar.
A new type of compound nest, inhabited by the small Strumigenys sp.1 (Myrmicinae) and the relatively big Diacamma sp.1 (Ponerinae), was found in Java, Indonesia. Field records as well as results of experimental studies were used to describe this association.
The compound nests were relatively frequent in the research area: 75% of the examined Diacamma sp.1 nests were also inhabited by Strumigenys sp.1. Strumigenys sp.1 is specialized on nesting in small, excavated nest chambers, in close vicinity to Diacamma sp.1, while Diacamma sp.1 does not depend on Strumigenys sp.1. The rather small workers of this myrmicine species forage for food inside the Diacamma nests as well as outside, favouring mites and collembolans as prey, but principally not rejecting any other nitrogen source. The refuse pile of Diacamma sp.1 inside the nest houses small living invertebrates and insect parts, preyed upon by Strumigenys sp.1. Given the choice between larvae of Diacamma sp.1 and mites, Strumigenys sp.1 clearly preferred the mites. Thus, the association seems to be beneficial to Strumigenys sp.1, and does not harm Diacamma sp.1.
We found two more similar compound nests: In Java, a different Strumigenys species was frequently found nesting within the nest of a Pachycondyla (Ponerinae) species. In Sabah, East Malaysia, we recorded for the first time a Pheidole (Myrmicinae) species nesting in chambers coming out of the walls of Diacamma nest chambers.
Existing classifications for compound nest associations (i.e. xenobiosis, cleistobiosis etc.) are too restricted, because they were based on a few cases. Hence, we present a list of non-normative traits describing the various types of nest symbioses by ants.
Associations between ants of the genera Crematogaster and Camponotus are found in many parts of the world. Associated species use common trails (trail sharing) or even share a common nest (parabiosis). In a tropical lowland forest in Malaysian Borneo, we studied intraspecific and interspecific aggression among the parabiotic species Crematogaster modiglianii and Camponotus rufifemur using both field and laboratory assays. Cr. modiglianii tolerated Ca. rufifemur workers from certain foreign colonies but fiercely attacked those of others. In contrast, Ca. rufifemur was tolerant even towards attacking allocolonial Cr. modiglianii workers but killed other Crematogaster species. By analogy, other Camponotus species usually attacked and killed Cr. modiglianii. Intraspecific confrontations among Ca. rufifemur colonies yielded a gradient from allocolonial tolerance to strong aggression. The aggression patterns coincide with those of Cr. modiglianii towards Ca. rufifemur workers from the same colonies. Our results suggest either that Ca. rufifemur is not able to recognize allocolonial Cr. modiglianii workers as foreign or that they are recognized but tolerated. The unilateral, species-specific but not colony-specific tolerance of Ca. rufifemur towards its partner species contrasts with highly colony-specific tolerance found among neotropical parabioses.
Evaluates the effects of exploitation and interference on the foraging behaviour of 9 species of ants in a Maryland woodlot. These species overlapped substantially in both the size and type of prey taken. Three types of encounters occurred between species at baits: attacks, avoidance, and coexistence. Camponotus ferrugineus, Lasius alienus, Prenolepis imparis and Formica subsericea fell into a dominant group, while Myrmica punctiventris, M. emeryana, Aphaenogaster rudis, Tapinoma sessile and Leptothorax curvisponus were increasingly subordinate. Subordinate species significantly reduced feeding time when in the presence of other species. Exploitative abilities of the species were studied by observing ant activity at baits. Leptothorax curvispinosus, A. rudis and the Myrmica spp. arrived first at a higher percentage of baits that did C. ferrugineus, which was significantly slower at finding new food sources. An inverse correlation was found between exploitative and interference ability, which enabled the subordinate species to obtain resources.-from Authors
Ant distribution and behavioural dominance is examined at nine sites along an elevational gradient (1400–2600 m) in south eastern Arizona, in order to classify North American species according to a functional group scheme used extensively in Australia. The functional groups are then used as a basis for determining patterns of community structure along the environmental gradient, and for comparing community structure between Australia and North America. Quantitative information on species com- position was obtained from pitfall traps, and patterns of ant abundance at tuna baits were used to determine relative behavioural dominance among taxa. A total of eighty-three species from twenty-eight genera was recorded along the elevational gradient, with site species richness ranging from four (high elevation Douglas fir forest) to thirty-three (mid elevation oak–juniper woodland). There was a strong correlation between ant abundance and richness, which was not an artefact of sampling intensity. The most common ants were species of Forelius, Monomorium, Crematogaster and Pheidole at the three desert sites, species of Formica, Pheidole and Crematogaster at the three woodland sites, and species of Prenolepis and Formica at one forest site. No species were abundant at two other forest sites. The most common species in traps also tended to be the most common species at baits. In terms of behavioural dominance, highly competitive ants included species of Solenopsis, Forelius, Monomorium and Liometopum. Species of Pheidole and Crematogaster tended to be moderately competitive, whereas species of Dory- myrmex, Myrmica, Camponotus and Formica (fusca gp) had low competitive ability. On the basis of these results and on published records of other taxa, North American ants were assigned to functional groups as follows (major taxa only given here): Dominant Dolichoderinae—Forelius, Liome- topum; Subordinate Camponotini—Camponotus; Hot Climate Specialists—Pogonomyrmex, Myrmecocystus; Cold Climate Specialists—Formica (rufa, exsecta and microgyna groups), Leptothorax, Stenamma, Lasius, Prenolepis; Cryptic Species—Smithistruma, Solenopsis (subgenus Diplorhop- trum), Acanthomyops; Opportunists—Formica (fusca group), Myrmica, Paratrechina, Dorymyrmex; Generalized Myr- micinae—Pheidole, Crematogaster, Monomorium; Specialist Predators—no major taxa. Functional group composition varied systematically along the elevation gradient: Dominant Dolichoderinae, Generalized MyrÃmicinae and Hot Climate Specialists were predominant at desert sites; Generalized Myrmicinae and Opportunists were predominant at woodland sites; and Opportunists and Cold Climate Specialists were predominant at forest sites. These patterns are consistent with published studies from elsewhere in North America. Almost all North American taxa can be matched with what appear to be ecologically equivalent taxa in Australia, and biogeographic patterns of functional group composition are broadly similar across the two continents. The major differences are that Australian ant communities are far richer in species, and are almost always dominated by dolichoderines, particularly species of Iridomyrmex. Generalized myrmicines are subdominant to dolichoderines in Australia, but are the behaviourally dominant ants throughout the warmer parts of North America. In cool-temperate North America, species of Formica (especially rufa and exsecta groups) are behaviourally dominant, as they are throughout the Palearctic. Some major features of the North American fauna can be linked to its poor representation of Dominant Dolichoderinae, including (1) the relatively low degree of physiological, morphological and behavioural specialization of Hot Climate Specialists; (2) behavioural dominance by formicines in cool-temperate habitats; and (3) the susceptibility to invasion by behaviourally dominant species such as the imported fire ant Solenopsis invicta and the Argentine ant Linepithema humile.
A system is proposed whereby ant functional groups are used as structural attributes to classify ninety-four Australian ant communities in a manner analogous to the classification of vegetation according to predominant life-forms. In terms of their responses to stress and disturbance, Dominant Dolichoderinae (DD) are considered analogous to trees, functionally subdominant Generalized Myrmicinae (GM) to shrubs and ruderal Opportunists (OPP) to grasses. Community types DDO (twenty-two sites), DD1 (twenty-two sites), DD2 (eight sites), DD3 (thirty-nine sites) and DD4 (three sites), respectively, are defined as having the relative abundance of Dominant Dolichoderinae <10%, 10-19%, 20-29%, 30-70% and >90%. They are structurally analogous to treeless plant communities, open woodlands, woodlands, forests and plantations, respectively. DDO communities are classified as DD0GM (analogous to shrublands) when Generalized Myrmicinae predominate, DD0OPP (analogous to grasslands) when Opportunists predominate and DD0CS (analogous to cold-adapted heathlands) when neither functional group is abundant. Similarly, the relative abundances of Generalized Myrmicinae and Opportunists are used to classify DD1-3 communities in a manner analogous to the classification of woodlands and open forests according to understorey type. DD3OPP communities, for example, where the relative abundance of Dominant Dolichoderinae is 30-70% and Opportunists are predominant among remaining ants, are structurally analogous to grassy forests. The distribution of ant functional groups is considered in relation to stress and disturbance by adopting Grime's (1979) triangular ordination concepts and nomenclature, with ant community structural types being analysed in terms of the relative importance of competition, stress and disturbance as factors regulating community structure. DD0 and DD1 structural types are stress-tolerant, or ruderal, communities; DD2 and DD3 types are competitive communities when Generalized Myrmicinae are abundant, and competitive ruderal or competitive stress-tolerant ruderal when Opportunists are predominant among non-dolichoderines; and DD4 communities are competitive ruderal. In temperate regions, seasonal changes in ant community structure parallel those occurring along biogeographical gradients spanning comparable temperature regimes. A positive relationship was found between the abundance of functionally dominant ants (DD + GM) and species richness. Plant and ant communities often differ from each other in their responses to the same stress or disturbance, such that there is often a poor correspondence between ant and plant community structural type at any particular site.
In Peru's Manu National Park, 10 epiphytic angiosperms from 7 plant families established principally on arboreal carton-ant nests. These "ant gardens' (AGs) were most often inhabited by parabiotic ants, Camponotus femoratus and Crematogaster cf. limata parabiotica, whose polygynous and polydomous colonies fissioned to form extensive AG aggregations. AGs tended by polydomous but probably monogynous Azteca cf. traili occurred on average in smaller isolates. All 3 ant species enriched nest gardens with vertebrate feces, but frequencies of occurrence of most AG epiphytes were lower on the less organic carton of Azteca AGs. Interspecific differences in epiphyte abundance and distribution were related to light requirements of plants and to colonizing abilities. AG aggregations occupied 16-39% of five forest habitat types present and were especially common in frequently flooded habitats and areas of high light intensity. Patchy distribution was explained partly by overrepresentation on resource trees, such as Inga and Calyptranthes (parabiotic ants) and Cordia nodosa (Azteca). Other arboreal ants, but not terrestrial ants, were markedly lower in AG aggregations, perhaps due to competition from aggressive and dominant AG ants. AGs formed principally by directed dispersal of epiphyte seeds to ant nests, where larvae fed on seed attachments without damaging seeds. AG ants also recognized and retrieved seeds of at least one AG epiphyte from feces of vertebrate fruit dispersers. Seed attractiveness may depend in part on nonnutritional cues. Preadapations of plants and ants appear to have been very important to the origin of AGs. Evidence for evolutionary specialization and coadaptation is suggestive. -from Author
Die Ameisen Mittel- und Nordeuropas Lutra Verlags- und Vertriebsgesellschaft Parasitism versus mutualism in the ant-garden parabiosis between Camponotus femoratus and Crematogaster levior Accepted 3 August 2010 © 2010 The Authors Ecological Entomology © 2010 The Royal Entomological Society
- B Seifert
- Tauer
- Germany
- A Vantaux
- A Dejean
- A Dor
- J Orivel
Seifert, B. (2007) Die Ameisen Mittel- und Nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, G¨ orlitz/Tauer, Germany. Vantaux, A., Dejean, A., Dor, A. & Orivel, J. (2007) Parasitism versus mutualism in the ant-garden parabiosis between Camponotus femoratus and Crematogaster levior. Insectes Sociaux, 54, 95–99. Accepted 3 August 2010 © 2010 The Authors Ecological Entomology © 2010 The Royal Entomological Society, Ecological Entomology, doi: 10.1111/j.1365-2311.2010.01231.x
Trail sharing between Camponotus and Cremastogaster : some comments and ideas
- C Baroni Urbani
Baroni Urbani, C. (1969) Trail sharing between Camponotus and Cremastogaster : some comments and ideas. Proceedings of the 6th Congress of the International Union for the Study of Social Insects (IUSSI), 15–20 September, 1969, Bern, pp. 11–17.
Die Ameisen Mittel-und Nordeuropas. Lutra Verlags-und Vertriebsgesellschaft
- B Seifert
Seifert, B. (2007) Die Ameisen Mittel-und Nordeuropas. Lutra Verlags-und Vertriebsgesellschaft, Gö/Tauer, Germany.
Southeast Asian ant-gardens
- E Kaufmann
Kaufmann, E. (2002) Southeast Asian ant-gardens. PhD thesis, J.-W.