Evolutionary and biological patterns can be obscured by inadequate or ill-defined terminology, especially when referring to ecological interactions. For example, cecidogenous (gall-inducing) species are considered ecosystem engineers, promoting structures rich in nutrients that create distinct microhabitats with many organisms interacting with the galls and gall inducers. These interactors are classified as members of a guild, and are described according to location, attribute, or activity of the host species. Guilds often do not typically have strict or clearly defined boundaries, nor do they need to be taxonomically interconnected. Cecidophage, inquilines, and kleptoparasite guilds appear to be poorly understood and misinterpreted. Herein, we bring an overview of the features that might help conceptualize and differentiate these interactions. We suggest that some cases described in the literature might be reassessed, and clear criteria proposed to distinguish among these 3 guilds associated with galls.
Galls are alterations in plant tissue due to feeding or other stimuli induced by organisms such as insects, mites, and viruses, among others (Dreger-Jauffret & Shorthouse 1992); however, insects are the most common cause (Maia & Fernandes 2004). Hypertrophy and hyperplasia in plant cells bring about changes (Dreger-Jaufret & Shorthouse 1992), resulting in the formation of gall tissues that are rich in nutrients and consequently possess a higher nutritional value than the original host plant tissue (Price et al. 1987).
Because of nutrient richness and ability to provide a differentiated microhabitat, galls serve as a resource for many organisms. In addition, galls house the inducer while serving as a resource for its natural enemies. However, the gall system encompasses a complex web of organisms that interact with each another and have been referred to as guilds (Mani 1964; Sanver & Hawkins 2000).
Sugiura and Yamazaki (2009) constructed a brief conceptual review of these guilds with an emphasis on Coleopteran and Lepidopteran cecidophages. These guilds can be divided into 2 groups: organisms that interact with galls and can interact secondarily with the inducer, and those that interact directly with the inducer. The first group can be separated into inquilines, cecidophages, and successors. The second would be predators, parasitoids, symbionts, and kleptoparasites (Fig. 1, adapted from Sugiura & Yamazaki 2009). Among all these organisms, predators, parasitoids, symbionts, and successors appear to be well delimited in the literature. Nevertheless, 3 groups of organisms interacting inside a gall structure may appear to have confusing roles due to terminological problems.
Predators and parasitoids are some of the culprits responsible for gall-inducer mortality. Birds and various insects can be gall-inducer predators (Craig et al. 2007), whereas several parasitoids (e.g., Chalcidoidea, Ichneumonoidea) are known for attacking the immatures of gall inducers (Stone et al. 2002). Ecologically, parasitoids are reported as the primary top-down control for populations of gall-inducing insects (Toma & Mendonça 2014). Their role appears to be clear and unequivocal, interacting in a straightforward manner with gallers only (trophically), although parasitoids can end up using the gall as a refuge in the process as well.
Successors are organisms that use the gall after the inducer leaves it (Mani 1964). These are very common in conspicuous galls that remain connected to plants over a long period of time; these organisms are mostly mites, spiders, thrips, beetles, and springtails. They apparently use gall tissues for food and shelter, but dead or decaying gall tissue is probably attacked by fungi that also serve as food. Successors may form specific food webs within the abandoned gall and are clear examples of the engineering effect that gallers have on host plants (Sanver & Hawkins 2000).
Inquilines and cecidophages are incapable of producing their own galls but feed off gall tissues (Mani 1964). Inquilines install themselves on galls in a way that might or might not be fatal to the inducers and may prompt the formation of new gall tissue. Cecidophages, on the other hand, simply consume gall tissues. Like inquilines, they do not attempt to kill the inducer; however, they are unable to promote the production of new tissues (Caltagirone 1964). Kleptoparasitism is the theft of a resource (i.e., the gall) by another organism that can be initiated by the abandonment of a gall or death of the gall inducer (Mound & Morris 2000). Figure 1 illustrates this interaction between guilds associated with the gall/gall-inducing system. Previous characterizations of these 3 gall-associated guilds have appeared to be too broad even though different literature sources have frequently used them distinctly, often without adequate criteria. Herein, we endeavor to provide a more complete conceptual definition of these guilds that incorporates clear and unambiguous terminology in order to allow for its consistent use in the literature.
DIFFERENTIATING CECIDOPHAGES , IN QUILINES , AND KLEPTO-PARASITES
Previously, the context of galls and their interactions with inquilines and cecidophages were characterized by Mani (1964) within an evolutionary context. This author pointed out that inquilines must have acquired their habits from gall-inducing ancestors, whereas cecidophages evolved independently. On the other hand, Mound and Morris (2000) studied kleptoparasitic thrips of other gall-inducing thrips and reported that the kleptoparasites killed the gall inducers; this was not the case for inquiline thrips that do not disturb the inducer.
Although the works cited above provide some tools for distinguishing among the guilds, none use multiple non-superposed parameters capable of completely differentiating organisms into one or the other category. In contrast, we propose the use of 5 interaction parameters: food habit; coexistence with the inducer; production of new tissues; phylogenetic relationship with the inducer; and mobility obtained from the literature to conceptualize and differentiate cecidophages, inquilines, and kleptoparasites from each other. A summary of the information is presented in Table 1.
Food habit is the primary characteristic that separates kleptoparasitism from the other 2 interactions. Cecidophages and inquilines are exclusively phytophages (Caltagirone 1964; Ronquist 1994), whereas kleptoparasites interact directly with the inducer, and when they do not chase the inducer away, they kill it, demonstrating omnivorous habits (Mound & Morris 2000; Luz et al. 2015).
Parameters used to differentiate interactions of inquilinism, cecidophagy, and kleptoparasitism of galls, as compiled from the literature.
COEXISTENCE WITH THE INDUCER
Inquilines coexist with the gall inducer when they both feed on the same tissue; e.g., the hymenopteran inquiline Periclistus pirata Osten Sacken (Hymenoptera: Cynipidae) on stem galls of Diplolepis nodulosa Beutenmüller (Hymenoptera: Cynipidae) (Brooks & Shorthouse 1997). If inquilines do not feed on the same tissues as inducers but modify the tissues, they can be called gall modifiers. Generally, when both organisms belong to the same insect order they are usually non-lethal, but if they are from different taxa, inquilines can become lethal to the inducer, e.g., Rhoophilus loewi Mayr (Hymenoptera: Cynipidae) on Scyrotis (Lepidoptera: Cecidosidae) galls (Van Noort et al. 2007). On the other hand, cecidophages may coexist with inducers by feeding internally or externally on the gall, and are lethal only when feeding on too much gall tissue, killing the inducer by starvation, or inadvertently opening up the gall. Kleptoparasitism is the only interaction where there is no possibility of coexistence with the inducer (Luz et al. 2015).
PRODUCTION OF NEW TISSUES
The primary characteristic that differentiates inquilinism from the other guilds is their stimulation of the host plant to produce new tissue in galls (Brooks & Shorthouse 1997). This action increases the amount of resources (plant tissue) the gall possesses. This relationship can be beneficial to the inducers (Lászlò & Tóthmérész 2006) when they belong to the same taxon (at least to the level of order). This is because both feed on the nutritive tissue in the same way. If inducers and gall producers of different insect orders encounter one another, their interaction is lethal. Hymenoptera, Diptera, Coleoptera, and Lepidoptera induce the formation of different kinds of gall tissues; inquilines associated with a specific tissue type are compatible with the insect order it belongs to. However, when inquilines occupy galls with incompatible tissue, they modify it. This new tissue then may not be compatible with the initial gall inducer (Van Noort et al. 2007). Moreover, inquilines can also change the shape and color of the gall (Brooks & Shorthouse 1997; Ferraz & Monteiro 2003). This characteristic does not apply to all inquilines but only to those that are gall modifiers. On the other hand, cecidophages and kleptoparasites are incapable of inducing new tissue production or modifying the gall phenotype.
PHYLOGENETIC RELATIONSHIP WITH THE INDUCER
Mani (1964) made the first distinction between inquilines and cecidophages by suggesting that gall tissue feeding inquilines evolved this trait from gall-inducing ancestors, whereas cecidophages evolved the habit of feeding on gall tissue independently. Evidence for this comes from the fact that some inquilines can modify gall tissue and stimulate production of new tissues. Not all inquilines that have a phylogenetic association to the inducer are gall modifiers, as in Trotteria (Microthyriaceae: Cecidomyidae) gall producing Cecidomyidae (Gagné 2004). Cecidophages can consume original gall tissue internally, but more commonly externally, differing from inquilines that exclusively consume gall tissue internally.
It is possible also to find inquilines that modify gall tissues that are not phylogenetically closely related to the initiator of the galls they occupy (Van Noort et al. 2007); members of this group belong to the Cynipidae. These hymenopterans have evolved from gall-inducing ancestors with some species attacking inducers other than gallflies (Stone et al. 2002).
Studies by Morris et al. (2000), Bono (2007), and Luz et al. (2015) also have suggested that kleptoparasites may bear a close relationship to inducers because they have the same nutritive tissue compatibility or may have evolved from gall-inducing ancestors (e.g., kleptoparasitc thrips) (Morris et al. 2000). However, more studies must be undertaken to reach a firmer conclusion.
Inquilines occupy only a single gall where they remain through their immature stage (Stone et al. 2002); cecidophages are more mobile, using 1 or more galls for feeding (Sugiura & Yamazaki 2009), whereas kleptoparasites, though mobile, normally utilize a single gall (Luz et al. 2015).
The major nomenclature problem appears to focus around the term “inquilinism.” Historically, all organisms associated with galls that were not predators or parasitoids were placed in this guild (Redfern & Askew 1992). However, it is important to recognize that more than 1 guild that can occupy the “house” of an inducer and must be separated following clear criteria so that biological and evolutionary patterns are not confused.
Moreover, inquilines also have been confused with cecidophages and successors. Nevertheless, successors do not interact with inducers in time, and cecidophages should be considered organisms that may not possess a close phylogenetic association with the inducer, and which are able to feed off more than 1 gall, and are incapable of stimulating new gall tissue production. The largest confusion between inquilines and cecidophages occurs for Coleoptera and Lepidoptera. Probably many of the designated “inquilines” in these 2 orders are actually cecidophages; they do not modify the gall, are not sedentary, and do not have a close phylogenetic relationship with the inducer.
Another problem with the term inquiline can be found in Thysanoptera research. As well-characterized as they are in the literature, the designation of inquilinism in thrips does not fit the broad characterization suggested here. However, we suggest researchers studying Thysanoptera may consider favoring the characterization criteria of inquilinism proposed here, in what seems to us to be a more clearly set of defined terms.
Another important aspect that must be taken into account, primarily by taxonomists that have described cecidogenic species, is that an insect collected directly from a gall may not be an inducer but an inquiline, cecidophage, or a kleptoparasite; this situation can be very common in galls collected from a single sample or period of the yr. Most often these mistakes would involve inquilines, and less frequently cecidophages, because the former are more common and in similar taxa but the latter are mobile.
The inadequate use of the aforementioned terminologies can lead to a poor understanding of interactions in gall-associated guilds. Researchers that work with these systems must take care to distinguish the guilds associated with their components. Unknowingly, many designate all individuals as inquilines, causing great confusion in the literature and erroneous interpretations about the significance of this diversity. In summary, we believe that future research using the criteria suggested in our review could be able to resolve and clarify semantic problems in the specific literature associated with these guilds. It is also anticipated that ecological and evolutionary hypotheses concerning these groups can then emerge with greater clarity.
Thanks to Adriano Cavalleri (Fundação Universidade de Rio Grande), Geraldo Soares (Universidade Federal do Rio Grande do Sul), and Rosy Isaias (Universidade Federal de Minas Gerais) for critically reading the first draft of the manuscript. F. A. Luz was supported by a CAPES (Comissão de Aperfeiçoamento de Pessoal do Nível Superior) Doctoral Program Fellowship. M. Mendonça is supported by a CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) Productivity grant (309616/2015-8).
- Bono J. 2007. Patterns of kleptoparasitism and inquilinism in social and nonsocial Dunatothrips on Australian Acacia.Ecological Entomology32: 411–418. Google Scholar
- Brooks SE, Shorthouse JD. 1997. Developmental morphology of stem galls of Diplolepis snodulosa (Hymenoptera: Cynipidae) and those modified by the inquilines Periclis tuspirata (Hymenoptera: Cynipidae) on Rosa blanda (Rosaceae).Canadian Journal of Botany76: 365–381. Google Scholar
- Caltagirone LE. 1964. Notes on the biology, parasites, and inquilines of Pontania pacifica (Hymenoptera: Tenthredinidae), a leaf-gall incitant on Salix lasiolepis.Annals of the Entomological Society of America57: 279–291. Google Scholar
- Craig TP, Itami JK, Horner JD. 2007. Geographic variation in the evolution and coevolution of a tritrophic interaction.Evolution61: 1137–1152. Google Scholar
- Dreger-Jauffret F, Shorthouse JD. 1992. Diversity of gall-inducing insects and their galls, pp. 8– In Shorthouse JD, Rohfritsch O [eds.], Biology of Insect Inducing Galls.University Press, New York, USA. Google Scholar
- Ferraz FFF, Monteiro RF. 2003. Complex interactions envolving a gall midge Myrciamyia maricaensis Maia (Diptera, Cecidomyiidae), phytophagous modifiers and parasitoids.Revista Brasileira de Zoologia20: 433–437. Google Scholar
- Gagné RJ. 2004. A catalog of the Cecidomyiidae (Diptera) of the World.Memoirs of the Entomological Society of Washington25: 1–408. Google Scholar
- Lászlò Z, Tóthmérész B. 2006. Inquiline effects on a multilocular gall community.Acta Zoologica Academia e Scientiarum Hungaricae52: 373–383. Google Scholar
- Luz FA, Gonçalves GL, Becker VO, Moreira GRP. 2015. Natural history, molecular phylogeny and taxonomy of a new kleptoparasitic gelechiid moth associated with Melastomataceae galls in Southern Brazil.Journal of Natural History49: 1849–1875. Google Scholar
- Maia VC, Fernandes GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil).Brazilian Journal of Biology64: 423–445. Google Scholar
- Mani MS. 1964. Ecology of Plant Galls.Dr. W. Junk, The Hague, The Netherlands. Google Scholar
- Miyatake T, Kuba H, Yukawa J. 2000. Seasonal occurrence of Bactrocera scutellata (Diptera: Tephritidae), a cecidophage of stem galls produced by Lasioptera sp. (Diptera: Cecidomyiidae) on wild gourds (Cucurbitaceae).Annals of the Entomological Society of America93: 1274–1279. Google Scholar
- Morris DC, Mound LA, Schwarz MP. 2000. Advenathrips inquilinus: a new genus and species of social parasites (Thysanoptera: Phlaeothripidae).Australian Journal of Entomology39: 53–57. Google Scholar
- Mound LA, Morris DC. 2000. Inquilines or kleptoparasites? New phlaeothripine Thysanoptera associated with domicile-building thrips on Acacia trees.Australian Journal of Entomology39: 130–137. Google Scholar
- Price PW, Fernandes GW, Waring GL. 1987. Adaptive nature of insect galls.Environmental Entomology16: 15–24. Google Scholar
- Redfern M, Askew RR . 1992. Plant galls. Naturalists' Handbooks 17.Richmond Publishing, Slough, United Kingdom. Google Scholar
- Ronquist F. 1994. Evolution of parasitism among closely related species: phylogenetic relationship and the origin of inquilinism in gall wasps (Hymenoptera: Cynipidae).Evolution48: 241–266. Google Scholar
- Sanver D, Hawkins BA. 2000. Galls as habitats: the inquiline communities of insect galls.Basic and Applied Ecology1: 3–11. Google Scholar
- Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae).Annual Review of Entomology47: 633–668. Google Scholar
- Sugiura S, Yamazaki K. 2009. Gall-attacking behavior in phytophagous insects, with emphasis on Coleoptera and Lepidoptera.Terrestrial Arthropod Reviews2: 41–61. Google Scholar
- Toma TSP, Mendonça JrMdeS. 2014. Population ecology of galling arthropods in the Neotropics, pp. 69-98 In Fernandes GW, Santos JC [eds.], Neotropical Insect Galls.Springer, New York, USA. Google Scholar
- Van Noort S, Stone GN, Whitehead VB, Nieves-Aldrey JL. 2007. Biology of Rhoophilus loewi (Hymenoptera: Cynipoidea: Cynipidae), with implications for the evolution of inquilinism in gall wasps.Biological Journal of the Linnaean Society90: 153–172. Google Scholar