Innard-Drinking Caterpillars and Others

Lithograph by Ernst Haeckel displaying moths of the families Plutellidae, Alucitidae, and Pterophoridae

Of the "Big Four" orders of the Insecta (Coleoptera, Lepidoptera, Hymenoptera, and Diptera), the Lepidoptera (moths, and the diurnal moths known as "butterflies") are reputed as the most-studied and best-understood (Gaston, 1991). I have observed that this reputation (which results from the enduring appeal borne by those ever-popular insects, the Papilionoidea) is often held without question amongst the entomologically inclined—unfortunate, given its falsehood: the excellent systematic knowledge of the butterfly/macro-moth* faunas of a few scattered regions in the Northern Hemisphere is by no means a synecdoche for the state of that field with regard to the remainder of the order's constituents (Kristensen et al., 2007). The micro-moths (as the non-Macrolepidoptera* are termed), which constitute the majority of the Lepidoptera, remain undoubtedly neglected in the realm of description and taxonomy.

Tinagma gaedikei (Douglasiidae), known only in association with Miami mist (Phacelia purshii) (©microleps)

This neglect can be imputed to many factors, only one of which I choose to address here: the structural and ecological uniformity of the clade Ditrysia, which, as its members constitute the vast majority of lepidopteran species, unavoidably reflects on the order as a whole—uniformity relative to the  trio of coevally speciose orders mentioned earlier, that is. Seeming consistency in gross ditrysian ethology belies an overall profusion of ecological detail amongst them—such as the specialization to host plant often seen herein (of which the moth shown above is a prime example; Harrison, 2005). But this consistency retains an essence of truth in that imaginal† ditrysians are overwhelmingly non-feeding or nectarivorous, and soft herbivorous tubes as larvae: to quantify, the latter characteristic is applicable to 99% of lepidopterans (Pierce, 1995). This essential reality has deterred research into Lepidoptera: to a degree, the order is seen as a dull option for study in the eyes of some entomologists.

Eupithecia orichloris (Geometridae) grappling with what appears to be a staphylinid beetle

But there are many exceptions to this rule of homogeneous lepidopteran ecology: rather than feed on pollen or seeds as do most members of their genus, the inchworms within Eupithecia endemic to Hawaii are equipped with tarsal motion-attenuated sensillae and elongated claws, both used to pounce upon small prey (Montgomery, 1983); predation on auchenorrhynchans has also been observed in the caterpillars of one metalmark butterfly (Riodinidae; DeVries et al., 1992), nor can I possibly ignore the famed diversity of ant-larva-chowing myrmecophilous caterpillars among the riodinids and the closely related Lycaenidae (blues, hairstreaks, etc.) (Fiedler, 2012). Nor are predaceous larvae limited to the Macrolepidoptera: the caterpillars of certain Pyralidae are known to attack scale insects (Mann, 1969; Neunzig, 1997); and as a bagworm (Psychidae), the Panamanian Perisceptis carnivora possesses a protective case: but being a non-herbivore, it crafts its case from the remains of its prey (Davis et al., 2008).

Euclemensia bassettella photographed by Mark Dreiling

However, I primarily wrote this post with the intent of addressing the protelean parasitoids‡ among the Lepidoptera. Considering the diversity of the order (~174,000 spp.), it is no wonder that this mode of existence has evolved on multiple twigs of the lepidopteran phylogram: but it is equally remarkable—given this same diversity—that less than 0.15% of these species are parasitoids (Pierce, 1995). Although I can find no comprehensive enumeration of the number of butterflies and/or moths which exhibit the parasitoid syndrome, it does appear that such adaptations tend to originate at species level: the parasitoid of paper wasp larvae (Polistes spp.) Chalcoela pegasalis (Hodges et al., 2003) is classified within a family largely consisting of humdrum phytophages (Crambidae), as are the gelechioids Euclemensia bassettella (Cosmopterigidae) and Zenodochium coccivorella (Blastobasidae) (although blastobasid caterpillars tend more towards detritovory; Watson & Dallwitz, 2011); the hosts of both these latter moths are scale insects (Coccoidea) (Rau, 1941).

This taxonomic artifact is at odds with what is observed in another mega-diverse insect order with a scarcity of parasitoids: the Coleoptera (beetles). Only one parasitoidal lineage of these famously speciose elytron-bearers is ranked at or below generic level: namely, the genus Aleochara (Staphylinidae: Aleocharinae), which with the exception of one species, are larval ectoparasitoids of cyclorrhaphous fly pupae (Peschke & Fuldner, 1977; Peschke et al., 1996). Contrastingly, there are only two exclusively parasitoidal lepidopteran families: the related Epipyropidae and Cyclotornidae (both classified within the superfamily Zygaenoidea).

Final-instar caterpillar of Fulgoraecia exigua on acanaloniid; photographed by Gary McClellan

Epipyropids are the more speciose of the pair, and most diverse in the Oriental and Australasian ecozones (only one species is known from my native Nearctic; Covell, 2005); their hosts are planthoppers (Fulgoroidea). One species (Agamopsyche threnodes) is parthenogenetic (Perkins, 1905). Similarly to such unrelated insects as strepsipterans (not to mention mantispids and acrocerids), "planthopper parasite moths" are hypermetamorphic, with all of the attributes that this lifestyle entails: a dispersal stratagem necessitating copious broods (3,000 eggs per brood in Fulgoraecia sp.), the hatching of which may be staggered to increase chances of larvae locating hosts (Kirkpatrick, 1947); in their inaugural instar, these dispersive larvae have disproportionately large heads and thoraxes, along with tapering abdomens—upon reaching a planthopper and adhering to its abdomen with its claws, an epipyropid larva moults into a dorsally convex and heavily corrugated caterpillar which exudes an increasingly thick layer of white polyethylene-like paraffin (Marshall et al., 1977), sucking its host's innards with serrated needle-mandibles on a head that can be retracted into its owner's obese body.

Cyclotornids (consisting of five Australian species within the genus Cyclotorna; Common, 1990) exhibit strong ontogenetic parallels with the Epipyropidae. Female moths spread their eggs adjacent to ant trails (in Cyclotorna monocentra, those created by the dolichoderine Iridomyrmex purpureus); the miniscule first-instar larvae (of similar proportions to their epipyropid cousins) literally gallop along these thoroughfares (Common, 1990), which lead to aggregations of leafhoppers (Cicadellidae) farmed by I. purpureus. These cicadellids serve as initial hosts, the cyclotornid larvae oriented upon them similarly to epipyropids upon planthoppers (situated upon the abdomen below the wings): later instars (flattened and broad by comparison to the first) detach from their leafhopper hosts: exuding allomones attractive to the leafhopper-attending ants, the larvae are then borne back to the I. purpureus colony, where they reside as myrmecophiles; appeasing their hosts chemically whilst preying on the latter's brood before pupation in what is one of the more complicated ecological transitions any insect undergoes through metamorphosis (Dodd, 1912).

To conclude, not all the Lepidoptera are so uninteresting (or so deeply understood) as their repute would lead us to believe.    

*The Macrolepidoptera is a probably monophyletic (Minet, 1991) clade including not only the butterflies (Papilionoidea) and the related skippers (Hesperioidea), but also such familiar moth families as the Geometridae (inchworms), Sphingidae (sphinx moths), the diverse Noctuidae (owlet moths and others), among many.
†Adult.
‡That is, parasitoids only when immature. 
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Common, I. F. B. (1990). Moths of Australia. Melbourne: Melbourne University Press. 

Covell, C. V. (Jr.) (2005).  A Field Guide to Moths of Eastern North America. Martinsville: Virginia Museum of Natural History.

Davis, D. R.; Quintero A., D.; Cambra T., R. A.; and Aiello, A. (2008). Biology of a new Panamanian bagworm moth (Lepidoptera: Psychidae), and eggs individually wrapped in setal cases [electronic version]. Annals of the Entomological Society of America, 101(4), 689-702. Retrieved 5/18/14 from http://esa.publisher.ingentaconnect.com/content/esa/aesa/2008/00000101/00000004/art00002      

DeVries, P. J.; Chacon, I. A.; and Murray, D. (1992). Toward a better understanding of host use and biodiversity in riodinid butterflies (Lepidoptera). Journal of Research on the Lepidoptera, 31(1-2), 103-126.

Dodd, F. P. (1912). Some remarkable ant-friend Lepidoptera. Transactions of the Entomological Society of London, 1911, 577-590.

Fiedler, K. (2012). The host genera of ant-parasitic butterflies: a review. Psyche, 153975, 1-10. Retrieved 5/16/14 from http://www.hindawi.com/journals/psyche/2012/153975/ 

Gaston, K. J. (1991). The magnitude of global species richness. Conservation Biology, 5, 283-296.

Harrison, T. L. (2005). A new species of Douglasiidae (Lepidoptera) from the eastern Nearctic [electronic version]. Proceedings of the Entomological Society of Washington, 107(3), 596-603. Retrieved 5/16/14 from http://www.biodiversitylibrary.org/page/32143328#page/608/mode/1up  

Hodges, A.; Hodges, G.; and Espelie, K. E. (2003). Parasitoids and parasites of Polistes metricus Say (Hymenoptera: Vespidae) in northeast Georgia. BioOne, 96(1), n.p.

Kirkpatrick, T. W. (1947). Notes on a species of Epipyropidae (Lepidoptera) parasitic on Metaphaena species (Hemiptera: Fulgoridae) at Amani, Tanganyika [electronic version]. Proceedings of the Royal Entomological Society of London, Series A: General Entomology; 22(4-6), 61-64. Retrieved 5/25/14 from http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3032.1947.tb01108.x/abstract  

Kristensen, N. P.; Scoble, M. J.; and Karsholt, O. (2007). Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity [electronic version]. Zootaxa, 1668, 699-747. Retrieved 5/16/14 from http://www.lepidoptera.ee/images/lingid/Zootaxa1668p699.pdf    

Mann, J. (1969). Cactus-feeding insects and mites. USNM Bulletin, 256, 30-158. Retrieved 5/17/14 from http://archive.org/stream/bulletinunitedst2561969unit#page/158/mode/2up

Marshall, A. T.; Lewis, C. T.; and Parry, G. (1974). Paraffin tubules secreted by the cuticle of an insect Epipyrops anomala (Epipyropidae: Lepidoptera) [electronic version]. Journal of Ultrastructure Research, 47(1), 41-60. Retrieved 5/23/14 from http://www.sciencedirect.com/science/article/pii/S0022532074900252

Montgomery, S. L. (1983). Carnivorous caterpillars: the behavior, biogeography and conservation of Eupithecia (Lepidoptera: Geometridae) in the Hawaiian Islands [electronic version]. GeoJournal, 7(6), 549-556. Retrieved 5/16/14 from http://link.springer.com/article/10.1007%2FBF00218529 

Minet, J. (1991). Tentative reconstruction of the ditrysian phylogeny (Lepidoptera: Glossata). Entomologica Scandinavica, 22, 69-95.   

Neunzig, H. H. (1996). The Moths of North America North of Mexico, fasc. 15.4.: Phycitinae (part). Bakersfield: the Wedge Entomological Research Foundation.

Perkins, R. C. L. (1905). Leaf-hoppers and their natural enemies (Pt. II: Epipyropidae) Lepidoptera. Bulletin of the Hawaiian Sugar Planter's Association Experimental Station Entomological Series, 84(1), 75-85. 

Peschke, K. and Fuldner, D. (1977). Uebersicht und neue Untersuchungen zur Lebensweise der parasitoiden Aleocharinae (Coleoptera; Staphylinidae). Zoologische Jahrbuecher (Systematik), 104, 242-262.

Peschke, K.; Mittmann, B.; and Fuldner, D. (1996). Aleochara clavicornis, a stepping stone in the evolution of parasitoid behavior within the rove beetle genus Aleochara (Coleoptera, Staphylinidae). Proceedings of the XXth International Congress of Entomology, Firenze, August 25-31.

Pierce, N. E. (1995). Predatory and parasitic Lepidoptera: carnivores living on plants. Journal of the Lepidopterists' Society, 49, 412-453. 

Rau, P. (1941). Observations on certain lepidopterous and hymenopterous parasites of Polistes wasps [electronic version]. Annals of the Entomological Society of America, 34(2), 355-366. Retrieved 5/21/14 from http://www.researchgate.net/publication/233678369_OBSERVATIONS_ON_CERTAIN_LEPIDOPTEROUS_AND_HYMENOPTEROUS_PARASITES_OF_POLISTES_WASPS 

Watson, L. and Dallwitz, M. J. (2011). Blastobasidae. Retrieved 5/21/14 from http://delta-intkey.com/britin/lep/www/blastoba.htm 

Glimpsing Armadillo Ants

One of the favorite books of my formative years (and also the favorite, I am sure, of a few others) was Bert Hölldobler and Edward O. Wilson's tome The Ants: a synthesis of the sum total of myrmecological knowledge up to 1990, and winner of the 1991 Pulitzer Prize in non-fiction (perhaps the only straight-up textbook to have ever done so; Yee, 2004). As an incipient preadolescent entomologist, my favorite part of the book's contents was the section devoted to collated line drawings and profiles of all ant genera considered valid at the time (organized by subfamily).

Peruvian worker of T. tatusia; photograph by Erin Prado

By poring over these figures time and time again, I was gradually familiarized with the distinctive silhouettes of many an ant, solidifying the more morphologically peculiar ones in my memory (the adorably wacky Discothyrea comes to mind here). Among these more striking sketches was one detailing the morphology of a species by the name of Tatuidris tatusia, contained in the Myrmicinae: in my usual learning process, I looked the name up in the index to find if any data were contained elsewhere in the book on the taxon. But The Ants would yield no information on T. tatusia, other than that it was the sole extant member of the myrmicine (Carpenter, 1930) tribe Agroecomyrmecini. It made perfect sense to me that Tatuidris (the etymology of the name suggested the ant's epithet "armadillo"; Lacau et al., 2012) should have a tribe all to itself—what with its generally weird habitus (a combination of a prominent stinger, clubbed antennae, and distinctively heart-shaped face); but this strangeness further made me wonder whether it was genuinely myrmicine in identity (doubts that were incidentally shared by some taxonomists, as we shall see).

Aside from Tatuidris, the armadillo ants include only the extinct genera Agroecomyrmex (from Baltic amber; Wheeler, 1914) and Eulithomyrmex (from the Coloradoan Florissant Formation; Carpenter, 1935): both date to the Paleogene Period (the latter about 10 million years younger than the former; Ritzkowski, 1997; Foos & Hannibal, 1999). Their assignment to the Myrmicinae (one of the most speciose single subfamilies within the Formicidae) was made on the basis of morphological similarities to members of the tribe Phalacromyrmecini, and, to a lesser extent, Dacetini (Brown & Kempf, 1968; Brown, 1977; Bolton, 1984): these common characteristics include an expanded facial vertex and deepened scrobes* (the extension of which all the way back to the eyes is another distinctive quality of Tatuidris; Baroni Urbani & de Andrade, 2007). Right from the description of the first living agroecomyrmecine (T. tatusia) these traits were suspected of being only dubiously indicative of kinship (Brown & Kempf, 1968; Bolton, 1984): speciousness affirmed by the elevation of the Agroecomyrmecini to subfamily rank (Bolton, 2003), although the first fully cladistic analysis of T. tatusia affirmed its relation to the Dacetini and inclusion within the Myrmicinae (Baroni Urbani & de Andrade, 2007). 

Ecuadorian bullet ant (Paraponera clavata) photographed by Alex Wild (who else?)

Classifying armadillo ants within their own subfamily—as is the prevalent opinion at the moment—still begs an answer to their true phylogeny. Two opposing theories seem to have arisen on the matter of agroecomyrmecine placement within the Formicidae: one regards the subfamily as sister-group of the Myrmicinae (Bolton, 2003); the other, as within the grab-bag of "poneromorph" subfamilies (the Amblyoponinae, Ectatomminae, Heteroponerinae, Paraponerinae, Proceratiinae, and Ponerinae) which sit at the base of the "formicoid" clade in which the Myrmicinae is placed (Ward, 2009): specifically, close to the monotypic Paraponerinae (Brady et al., 2006) or near the Amblyoponinae (Rabeling et al., 2008). The results of one mainly morphological study resolve the ambiguity by deriving the Myrmicinae as both within the "poneroids" (Keller, 2011) and akin to the armadillo ants. 

Variation in pilosity patterns within T. tatusia (Donoso, 2012)

With all of this ambiguity, one can only wonder if biological data on the only extant armadillo ant would be at all informative in agroecomyrmecine phylogeny. T. tatusia has been collected throughout southern Mesoamerica and northern South America, reaching greatest abundance in upland areas (largely between 800 and 1,200 meters in altitude); the species includes multiple morphs throughout its range (which on one occasion caused the mistaken description of new species; Lacau et al., 2012) and exhibits  an unusual degree of intraspecific genetic variation: this suggests either that the population in fact consists of several cryptic species that taxonomists do not yet have the information to confidently delineate, or that it is a lineage in the process of allopatric speciation (Donoso, 2012).

Almost nothing is known of the habits of T. tatusia, given that until recently none had been observed in life: but its weirdly elongated stinger and thickly interlocking setae on the inner margins of the mandibles—not to mention intramandibular glands clustered in a manner unknown in other ants (Billen & Delsinne, 2013)—have encouraged speculation on the ant's presumably unorthodox biology. In further tantalization, the discovery of the first live colony (containing erstwhile-unknown drones and queens) revealed only that armadillo ants have a diet that does not include the following likely items:

" ... live and dead termites, millipedes, mites, various insect parts, sugar water, tuna, biscuits, live and dead fruit flies (Drosophila), live springtails, live myriapods (Chilopoda and Diplopoda) [centipedes and millipedes], live and dead Diplura, small live spiders, small live pseudoscorpions, one small snail, uncooked hen egg ... ant larvae (Gnamptogenys sp.), and live ant workers (Cyphomyrmex sp., Brachymyrmex sp.)." (Donoso, 2012)

Hence, we can only assume that T. tatudris is a most specialized predator. Of what, precisely, remains to be seen whenever science captures its next glimpse of armadillo ants. 

                           

*Cephalic slots into which antennae can be retracted.
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Baroni Urbani, C. and de Andrade, M. L. (2007). The ant tribe Dacetini: limits and constituent genera, with descriptions of new species. Annali del Museo Civico di Storia Naturale "G. Doria", 99, 1-191.

Billen, J. and Delsinne, T. (2013). A novel intramandibular gland in the ant Tatuidris tatusia (Hymenoptera: Formicidae). Myrmecological News, 19, 61-64. Retrieved 5/8/14 from http://bio.kuleuven.be/ento/pdfs/billen_delsinne_myrmnews_2013.pdf

Bolton, B. (1984). Diagnosis and relationships of the myrmicine ant Ishakidris gen. n. (Hymenoptera: Formicidae). Systematic Entomology, 9, 373-382.

Bolton, B. (2003). Synopsis and classification of Formicidae. Memoirs of the American Entomological Institute, 71, 1-370.

Brady, S. G.; Schultz, T. R.; Fisher, B. L.; and Ward, P. S. (2006). Evaluating alternative hypotheses for the early evolution and diversification of ants. Proceedings of the National Academy of Sciences of the United States of America, 103(48), 18172–18177.

Brown, W. L. (1977). An aberrant new genus of myrmicine ant from Madagascar. Psyche, 84, 218-224.

Brown, W. L. and Kempf, W. W. (1968). Tatuidris, a remarkable new genus of Formicidae (Hymenoptera). Psyche, 74, 183-190.


Carpenter, F. M. (1930). The fossil ants of North America [electronic version]. Bulletin of the Museum of Comparative Zoology, 70(1), 1-66. Retrieved 5/7/14 from http://gap.entclub.org/taxonomists/Carpenter/1930.pdf

Carpenter, F. M. (1935). A new name for Lithomyrmex Carp. (Hymenoptera) [electronic version]. Psyche, 42(2), 91. Retrieved 5/6/14 from http://www.hindawi.com/journals/psyche/1935/068604/abs/   

Donoso, D. A. (2012). Additions to the taxonomy of the armadillo ants (Hymenoptera, Formcidae, Tatuidris) [electronic version]. Zootaxa, 3503, 61-81. Retrieved 5/8/14 from http://mapress.com/zootaxa/2012/f/zt03503p081.pdf 

Foos, A. and Hannibal, J. (1999). Geology of Florissant Fossil Beds National Monument. Retrieved 5/5/14 from http://www2.nature.nps.gov/geology/education/foos/flfo.pdf    

Hölldobler, B. and Wilson, E. O. (1990). The Ants. The Belknap University Press of Harvard University Press: Cambridge.

Lacau, S.; Groc, S.; Dejean, A.; de Oliveira, M. L.; and Delabie, J. H. C. (2012). Tatuidris kapasi sp. nov.: a new armadillo ant from French Guiana (Formicidae: Agroecomyrmecinae). Psyche, 2012(2012), 926089, 1-7. Retrieved 5/8/13 from http://www.hindawi.com/journals/psyche/2012/926089/ 

Rabeling, C.; Brown, J. M.; and Verhaagh, M. (2008). Newly discovered sister lineage sheds light on early ant evolution. Proceedings of the National Academy of Sciences, USA; 105, 14913-14917.

Ritzkowski, S. (1997). K-Ar-Altersbestimmungen der bernsteinführenden Sedimente des Samlandes (Paläogen, Bezirk Kaliningrad). Metalla, Bochum; 66, 19-23.

Ward, P. S. (2009). Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae) [electronic version]. Zootaxa, 1669, 549-563. Retrieved 5/8/14 from http://wardlab.files.wordpress.com/2012/01/ward_2007c_zoootaxa.pdf 

Wheeler, W. M. (1914). The ants of the Baltic amber. Schriften der Physikalisch-Okonomischen Gesellschaft, 55(4), 56-59.

Yee, D. (2004). The Ants: Bert Hölldobler + Edward O. Wilson. Retrieved 5/7/14 from http://dannyreviews.com/h/Ants.html