FORUM Debris-Carrying in Larval Chrysopidae: Unraveling Its Evolutionary History 1,2 1 3 CATHERINE A. TAUBER, MAURICE J. TAUBER, AND GILBERTO S. ALBUQUERQUE Ann. Entomol. Soc. Am. 107(2): 295Ð314 (2014); DOI: http://dx.doi.org/10.1603/AN13163 ABSTRACT Larval debris-carrying, which occurs in many insect taxa, is a remarkable behavioral trait with substantial life history signiÞcance. For the Chrysopidae, information on the topic is scattered, and the habitÕs diversity and evolutionary history are unassessed. Here, we compile a comprehensive, annotated catalog on chrysopid debris-carrying and its associated larval morphology, and we identify emerging systematic patterns of variation, from larval nakedness to the construction of elaborate packets. Then, we examine these patterns in the context of available phylogenies with two objectives: 1) to begin unraveling the evolutionary history of chrysopid debris-carrying and 2) to evaluate the current and potential role of larval morphology (including debris-carrying modiÞ- cations) in classiÞcation and phylogeny of this family. Debris-carrying: the literature revealed that debris-carrying occurs in the chrysopoid fossil record and in all three extant chrysopid subfamilies, including those proposed as basal (Nothochrysinae, Apochrysinae). Nevertheless, the familyÕs an- cestral state remains unresolved. The habit may have evolved at least once in Nothochrysinae or been lost several times. Larvae from only one genus of Apochrysinae are known, and they are debris-carriers. Each of the four tribes of the third subfamily, Chrysopinae, has distinctive debris-carrying charac- teristics. In ankylopterygine larvae, debris-carrying modiÞcations seem relatively conserved. Among the ant-associated belonopterygine genera, debris-carrying is either highly evolved or, in one case, possibly absent. Within the large chrysopine tribe, nakedness and debris-carrying appear to have evolved independently numerous times; also, some reversals may have occurred. With one possible exception, leucochrysine genera have debris-carrying larvae. Larval morphology: scrutiny of the literature showed that all chrysopid genera whose larvae are known exhibit characteristic suites of anatomical structures related to carrying debris. Moreover, larval morphology provides strong (sy- napomorphic) evidence for the monophyly of four of the seven suprageneric chrysopid taxa: the subfamily Nothochrysinae and three of the four tribes of Chrysopinae (Ankylopterygini, Belonop- terygini, and Leucochrysini). Larval morphological and debris-carrying characteristics appear to support some, but not all, previously proposed generic relationships within the tribe Chrysopini. Given the demonstrated potential advantages for including larval characters in chrysopid phylogenetic studies, it is essential to enhance the pool of available larval data. Therefore, we propose that citizen-scientists be involved in gathering veriÞable data and that systematists develop comprehensive data matrices for comparative larval studies. KEY WORDS camoußage, phylogeny, larval morphology, trash-carrying, Neuroptera Among insects, the larval habit of camoußaging or insect orders,4 including Hemiptera, Trichoptera, shielding the body with exogenous organic or inor- Lepidoptera, Coleoptera, and Neuroptera. Within the ganic material (ϭ debris-carrying) is an elaborate Chrysopidae, this behavior occurs in the majority behavioral attribute with far-reaching life history and (Ϸ65%) of genera for which larvae are known (Ap- evolutionary consequences (e.g., see Principi 1943, pendix 1), and it appears closely associated with the 1946; Eisner et al. 1978; Milbrath et al. 1993, 1994; Tauber et al. 1995b; Brandt and Mahsberg 2002; Bu- cheli et al. 2002). Examples exist in a wide range of 4 Hemiptera: Reduviidae (Butler 1923, Brandt and Mahsberg 2002); Trichoptera: most families (Wiggins 1977); Lepidoptera: Geometri- dae (Ferguson 1985), Coleophoridae (Bucheli et al. 2002, Falkovitsh 2003), Psychidae (Rhainds et al. 2009); Coleoptera: Derodontidae 1 Department of Entomology, Comstock Hall, Cornell University, (Brown and Clark 1962), Curculionidae (Gressitt et al. 1968), Ithaca, NY 14853-2601 and Department of Entomology, University of Chrysomelidae (Chaboo et al. 2008, Chaboo 2011), Endomychidae California, Davis, CA 95616. (Leschen and Carlton 1993), Sphindidae (McHugh and Kiselyova 2 Corresponding author, e-mail: [email protected]. 2003); Neuroptera: Ascalaphidae (Henry 1977); Myrmeleontidae 3 Laborato´rio de Entomologia e Fitopatologia, CCTA, Universidade (Robert Miller and Lionel Stange, personal communication), Sisyri- Estadual do Norte Fluminense, Campos dos Goytacazes, RJ, Brazil dae (Killington 1936, 1937), Chrysopidae (e.g., Smith 1926; Killington 28013-602; e-mail: [email protected]. 1936, 1937; Catalog, Supp Table 1 [online only]). 0013-8746/14/0295Ð0314$04.00/0 ᭧ 2014 Entomological Society of America 296 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 107, no. 2 evolutionary diversiÞcation of the family (Tauber and loosely to tightly constructed cloaks that partially or Tauber 1989, Tauber et al. 1993). completely cover the larval body, and very dense Much information on debris-carrying within the shields that are tightly attached and intertwined with Chrysopidae has accumulated over the past Ϸ90 yr. silken strands and that extend well beyond the outline During this period, systematic and natural history of the larval body. studies documented a wide range of variation in Furthermore, larvae show interspeciÞc variation in chrysopid debris-carrying and concomitant modiÞca- the frequency with which they carry debris: some tions in larval anatomy. However, the information has species carry debris occasionally or during a speciÞc been neither compiled nor examined in detail, and the instar, which is usually the Þrst instar (“occasional evolutionary history of debris-carrying has not been ex- debris-carriers”). Generally, the occasional debris- plored phylogenetically. To assess current knowledge carriers carry scattered pieces of material. Ideally, if and provide a foundation for future work, we: 1) assem- sufÞcient data were available, we could categorize ble, in a systematically based catalog, the dispersed lit- each species (e.g., “debris-carrier” if all instars con- erature on the larval morphology and debris-carrying sistently have a distinct covering of material; “light habits of chrysopids and their chrysopoid ancestors (Cat- debris-carrier” if all instars usually carry a few, scat- alog, Supp Table 1 [online only]); 2) search for evolu- tered fragments of material; “occasional debris-car- tionary patterns contained within the current literature; rier” if only some instars or some individuals carry 3) highlight signiÞcant Þndings for speciÞc taxa; and 4) material; or “naked” if all instars are usually without identify taxa whose poorly known larvae might yield debris). In reality, for most species, data are only especially important comparative information. sufÞcient to differentiate “naked” (without debris) Finally, despite the proven value of immatures in from “debris-carrying” in the broad sense of the term phylogenetic analysis in other insect groups (e.g., see (see Figs. 1Ð3 for examples). Oberprieler et al. 2000, Meier and Lim 2009), we In contrast to the behavioral variation above, the document their almost complete absence from numerous features of larval morphology implicated in chrysopid phylogenies. In doing so, we also provide a debris-carrying are relatively well-documented, and a rationale for using larval characters, including those broader range of taxa is included. Table 1 describes the related to debris-carrying, in phylogenetic analyses of features that are typically associated with either naked the Chrysopidae, and we offer recommendations larvae or with debris-carriers. What is especially strik- whereby specialists and citizen-scientists can cooper- ing is that larvae express great variation in these traits ate to accelerate the process. and yet no speciÞc combination of features deÞnes either of the two lifestyles. Literature. Larval debris-carrying in Chrysopidae Background has been documented for Ͼ275 yr (since Re´aumurÕs Debris-Carrying. Both the behavioral and morpho- [1737] report). Many subsequent papers referred to logical components of larval debris-carrying in the behavior, but often anecdotally and with varying chrysopids exhibit valuable taxon-speciÞc variation. amounts of detail. For some taxa, the information Although the behavior involved in constructing a dor- reßects numerous observations accumulated over sal cloak or packet (often referred to as “loading be- many years; in others, only one observation may be havior”; see Fig. 2F) is described for only a very small available. Our catalog here (Catalog, Supp Table 1 number of species, many reports have focused on the [online only]) includes all the references to larval packet as an indicator of the underlying behavior. For debris-carrying and larval morphology that we found example, in nature, larvae of most species appear to be for each chrysopid species. selective in the material they use for their coverings, Larval morphology has long been a key element in and as a consequence, the composition of the packet neuropteran systematics and phylogeny at the ordinal can be taxonomically signiÞcant. Depending on the spe- level (initiated by Withycombe [1922, 1924] and Tilly- cies, this material may include waxy ßocculence from the ard [1926], advanced by Ellis MacLeod [1960,