Review Article |
Corresponding author: Federico Agrain ( fagrain@mendoza-conicet.gov.ar ) Academic editor: Michael Schmitt
© 2015 Federico Agrain, Matthew Buffington, Caroline Chaboo, Maria Chamorro, Matthias Schöller.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Agrain FA, Buffington ML, Chaboo CS, Chamorro ML, Schöller M (2015) Leaf beetles are ant-nest beetles: the curious life of the juvenile stages of case-bearers (Coleoptera, Chrysomelidae, Cryptocephalinae). In: Jolivet P, Santiago-Blay J, Schmitt M (Eds) Research on Chrysomelidae 5. ZooKeys 547: 133–164. https://doi.org/10.3897/zookeys.547.6098
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Although some species of Cryptocephalinae (Coleoptera: Chrysomelidae) have been documented with ants (Hymenoptera: Formicidae) for almost 200 years, information on this association is fragmentary. This contribution synthesizes extant literature and analysizes the data for biological patterns. Myrmecophily is more common in the tribe Clytrini than in Cryptocephalini, but not documented for Fulcidacini or the closely-related Lamprosomatinae. Myrmecophilous cryptocephalines (34 species in 14 genera) primarily live among formicine and myrmecines ants as hosts. These two ant lineages are putative sister-groups, with their root-node dated to between 77–90 mya. In the New World tropics, the relatively recent radiation of ants from moist forests to more xeric ecosystems might have propelled the association of cryptocephalines and ant nests. Literature records suggest that the defensive behavioral profile or chemical profile (or both) of these ants has been exploited by cryptocephalines. Another pattern appears to be that specialized natural enemies, especially parasitoid Hymenoptera, exploit cryptocephaline beetles inside the ant nests. With the extant data at hand, based on the minimum age of a fossil larva dated to 45 mya, we can infer that the origin of cryptocephaline myrmecophily could have arisen within the Upper Cretaceous or later. It remains unknown how many times myrmecophily has appeared, or how old is the behavior. This uncertainty is compounded by incongruent hypotheses about the origins of Chrysomelidae and angiosperm-associated lineages of cryptocephalines. Living with ants offers multiple advantages that might have aided the colonization of xeric environments by some cryptocephaline species.
Myrmecophily, Camptosomata, Larvae, Biology, Clytrini , Cryptocephalini
With approximately 40,000 species documented, the Chrysomelidae, commonly called leaf beetles, are one of the most diverse insect groups on Earth. They are well known as phytophages, specializing on all parts of plants, from roots to fruits and flowers. Within this broad lineage, whose origin has been dated from the Middle Jurassic (
This study focuses on the monophyletic Camptosomata branch of leaf beetles (
Camptosomates are commonly referred to as “case-bearers” because of the unusual larval behavior of retaining a maternal covering of feces around each egg, carrying and reconstructing it as a protective structure, and ultimately modifying it as a pupation chamber.
Although myrmecophilous associations can be found in at least 35 beetle families, including varied behavioral and morphological characteristics (
Ants are not the only hosts of some Camptosomata. Griburius montezuma (Cryptocephalini) has been reported as living in nets of bird (
Ant nests are considered to be well-protected environments, with storage of food items and stable microclimatic conditions.
The exploitation of ant nests presents some formidable challenges.
Existing literature on ant-camptosome associations was synthesized (Table
Taxon | Beetle species | Tribe | Source |
---|---|---|---|
Dolichoderinae ants | |||
Tapinoma erraticum Latreille | Labidostomis taxicornis (Fabricius) | CL |
|
Dorylinae ants | |||
Dorylus sp. | Clytrinae larvae follow the migrations of their hosts outside the nest during day or night | CL |
|
Formicinae ants | |||
Camponotus sp. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
|
Camponotus ligniperdus Latreille | Clytra (Clytra) quadripunctata (L.) | CL |
|
Camponotus (Latreille) | Clytra sp. | CL |
|
Camponotus melleus Say | Coscinoptera dominicana dominicana (Fabricius) | CL |
|
Camponotus (Myrmosericus) rufoglaucus Jerdon | Hockingia curiosa Selman | CL |
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Camponotus sp. | Clytrasoma maschwitzi Schöller | CL |
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Camponotus sp. | Clytra (Clytra) quadripunctata (L.) | ||
Camponotus | Clytrine | CL |
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Cataglyphis cursor Fonscolombe | Clytra (Clytraria) atraphaxidis (Pallas) | CL |
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Cataglyphis bicolor (Fabricius) | Clytra (Clytraria) atraphaxidis (Pallas) | CL |
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Cataglyphis cursor Fonscolombe | Clytra (Clytraria) atraphaxidis (Pallas) | CL |
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Cataglyphis bicolor Fabricius | Clytra (Clytraria) atraphaxidis (Pallas) | CL |
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Cataglyphis Förster | Clytra sp. | CL |
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Cataglyphis cursor Fonscolombe | Lachnaia (Lachnaia) tristigma (Lacordaire) | CL |
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Cataglyphis cursor Fonscolombe | Lachnaia (Lachnaia) tristigma (Lacordaire) | CL |
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Cataglyphis Förster | Lachnaia Chevrolat in Dejean | CL |
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Formica pallidefulva Latreille | Anomoea flavokansiensis Moldenke | CL |
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Formica sanguinea Latreille | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Formica pratensis DeGeer | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Formica fusca L. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Formica rufa L. | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica rotundata Klug | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica exsecta Nylander | Clytra (Clytra) quadripunctata (L.) | CL |
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Possibly Formica congerens Nylander | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica sanguinea Latreille | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica pratensis DeGeer | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica rufo-pratensis Forel | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica pressilabris Nylander | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica gagates Nylander | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica uralensis Ruzsky | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica sp. | Clytra (Clytra) quadripunctata (L.) | CL |
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Formica rufa L. | Clytra sp. | CL |
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Formica L. | Clytra sp. | CL |
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Formica fusca L. | Clytra sp. | CL |
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Formica fusca L. | Clytra sp. | CL |
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Formica sp. | Coscinoptera dominicana dominicana (Fabricius) | CL |
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Formica obscuripes Forel | Coscinoptera dominicana dominicana (Fabricius) | CL |
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Formica selysii Bondroit | Pachybrachis anoguttatus Suffrian (found inside the ant nest) | CR |
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Formica fusca subaenescens Emerton | Coscinoptera dominicana dominicana (Fabricius) | CL |
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Formica obscuripes Forel | Coscinoptera dominicana dominicana (Fabricius) | CL |
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Formica neoclara Emery | Coscinoptera dominicana franciscana (LeConte) | CL |
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Formica fusca subaenescens Emerton | Coscinoptera vittigera (LeConte) | CL |
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Formica fusca L. | Coscinoptera vittigera Probably C. dominicana (Fabricius) | CL |
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Formica | Clytrine | CL |
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Lasius niger L. | Cryptocephalus (Burlinius) ocellatus ocellatus Drapiez | CR |
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Lasius niger L. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius alienonigra Forst. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius alienus Forst. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius neglectus Van Loon, Boomsma & András-Falvy | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius niger L. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius niger L. | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Lasius flavus (DeGeer) | Clytra (Clytra) quadripunctata (L.) | CL |
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Lasius Latreille | Clytra sp. | CL |
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Lasius neglectus Van Loon, Boomsma & András-Falvy | Clytrinae larvae | CL |
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Lasius fuliginosus Latreille | Cryptocephalus (Burlinius) fulvus fulvus (Goeze) | CR |
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Plagiolepis sp. | Tituboea macropus (Illiger) | CL |
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Myrmicinae ants | |||
Aphaenogaster subterranea Latreille | Clytra (Clytra) laeviuscula Ratzeburg | CL |
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Aphaenogaster (Myrmica) testaceopilosa Lucas | Tituboea octosignata (Fabricius) | CL |
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Aphaenogaster testaceopilosa Lucas | Cryptocephaline | Undetermined |
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Atta mexicana (F. Smith) (Larvae saprophagous) | Megalostomis dimidiata Lacordaire | CL |
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Atta Fabricius | Megalostomis dimidiata Lacordaire | CL |
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Atta nest (digging on) | Megalostomis dimidiata Lacordaire | CL |
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Atta texana (Buckley) | Megalostomis dimidiata Lacordaire (as M. major Crotch). 2.5m depth. | CL |
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Atta | Clytrine | CL |
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Atta mexicana (F. Smith) | Pachybrachis sp. On external ant debris | CR |
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Atta mexicana (F. Smith) | Griburius sp. (misspelled as Griburium). On external ant debris, | CR |
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Crematogaster lineolata (Say) | Anomoea | CL |
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Crematogaster lineolata Say (the ants carries the eggs to their nest) | Anomoea flavokansiensis Moldenke | CL |
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Crematogaster mimosa Santschi | Hockingia curiosa Selman | CL |
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Crematogaster sjostedti Mayr | Hockingia Selman | CL |
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Crematogaster (Crematogaster) nigriceps Emery | Isnus petasus Selman | CR |
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Nest of Crematogaster peringueyi Emery | Clytrine cases | CL |
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Crematogaster sp. | Coenobius macarangae Gressitt (living on myrmecophyte) | CR |
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Crematogaster sp. | Cadmus macarangae Gressitt (living on myrmecophyte) | CR |
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Messor clivorum sevani Kar. | Clytra (Clytraria) valeriana valeriana Ménétriés | CL |
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Messor Forel | Clytra sp. | CL |
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Messor barbarus L. | Lachnaia vicina Lacordaire. | CL |
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Messor barbarus capitatus Latreille | Tituboea biguttata (Olivier) | CL |
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Messor spp. | Tituboea biguttata (Olivier) | CL |
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Messor barbarus L. | Tituboea biguttata (Olivier) | CL |
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Messor barbarus capitatus Latreille | Tituboea biguttata (Olivier) | CL |
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Messor barbara (L.) | Tituboea Lacordaire | CL |
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Messor barbara L. | Clytrine | CL |
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Mymica rugolosa Nylander, queen using larval case for colony founding | Cryptocephalus morarei (L.) | CR |
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Pheidole sp. Queen with eggs and workers on larval case | Cryptocephalus anceps Suffrian | CR |
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Tetramorium caespitum L. | Clytra sp. | CL |
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Tetramorium caespitum L. | Clytra sp. | CL |
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Tetramorium caespitum L. | Smaragdina concolor (Fabricius) | CL |
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Tetramorium vespitum L. | Smaragdina concolor (Fabricius) | CL |
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Leaf cutting ant nest | Megalostomis dimidiata Lacordaire | CL |
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Undetermined ants | |||
Eat detritus and Humus, associated with ants | Anomoea | CL |
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Myrmecophile | Clytra sp. | CL |
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Ant eggs | Clytrine | CL |
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As myrmecophiles | Clytrine | CL |
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As myrmecophiles | Clytrine | CL |
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Dead leaves in ant nests | Clytrine | CL |
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In ant nests | Clytrine | CL |
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Larvae that overwinter as ant inquilines | Clytrine | CL |
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Ant host | Coscinoptera dominicana dominicana (Fabricius) | CL |
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Ants on Acacia tolerate ants | Cryptocephaline | CR |
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Ant nests | Cryptocephalus Geoffroy | CR |
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Ant host | Helioscopa Gistel | CL |
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Associated with ants, myrmecophiles, or submyrmecophiles | Labidostomis Chevrolat in Dejean | CL |
|
As obligate or facultative ant inquilines | Lachnaia Chevrolat in Dejean | CL |
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Myrmecophilous larvae | Lachnaia italica italica Weise | CL |
|
Found in the vicinity of ant nest) | Macrolenes dentipes Olivier | CL |
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As myrmecophiles | Megalostomis Chevrolat | CL |
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Found in the vicinity of ant nest) | Pachybrachis anoguttatus Suffrian | CR |
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In ant nests | Saxinis (Boreosaxinis) saucia LeConte | CL |
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Terminology: we use the terms ‘myrmecophily’ and ‘myrmecophilous’ in a broad sense, meaning casual or intimate association of the beetle with ants. Such interactions could involve different forms, from mutualism (benefits for both associates), parasitism (host resources necessarily drained for parasite’s own reproduction), commensalism (with no direct effect on the host), predation (direct feeding/damage to the host), or inquilinism (the ‘guest’ obtains shelter and other resources from the host without damaging host). For extended definitions and discussion of the latter terms see
Figure
Our synthesis of the literature reveals that 34 species of Cryptocephalinae have been associated with ants. The following ant groups host cryptocephalines: Dolichoderinae (1 species), Dorylinae (1 species) Formicinae (13 species), Myrmicinae (16 species); 11 species were reported on an undetermined host ant. Of the latter, 4 cryptocephaline genera are included in this category for which there is no other ant record. These associations represent approximately 0.6% of current species diversity of Cryptocephalinae. In summary, 14% of the 127 Cryptocephalinae genera are associated with ants at some level, as truly myrmecophilous. We found several previously unnoticed patterns in the ant associations of camptosomate genera and species. Regarding the extent of myrmecophily within Camptosomata, we found that ant associations are documented only in two tribes, Clytrini and Cryptocephalini (Fig.
Data extracted from literature and synthesized here suggest that myrmecophily in Cryptocephalinae is rare or simply unknown, being more frequent in Clytrini (Fig.
Ant association records. Each pie chart indicates ant association records expressed as percentages, different color tones refer to each ant subfamilies as indicated in the color reference below: A–B records within the tribe CryptocephaliniC–D records within the tribe ClytriniE–F records within the whole subfamily.
Tribe / Genus | Myrmecophilous species number | Number of ant genera recorded as host |
---|---|---|
Clytrini | ||
Anomoea Agassiz | 1 + undet. | 2 + undet. |
Clytra Laicharting | 4 + undet. | 7 + undet. |
Clytrasoma Jacoby | 1 | 1 |
Coscinoptera Lacordaire | 2 | 2 + undet. |
Helioscopa Gistel | undet. | undet. |
Hockingia Selman | 1 + undet. | 2 |
Labidostomis Germar | 1 + undet. | 1 + undet. |
Lachnaia Chevrolat | 1 + undet. | 2 + undet. |
Macrolenes Chevrolat | 1 | undet. |
Megalostomis Chevrolat | 2 + undet. | 2 + undet. |
Saxinis Lacordaire | 1 | undet. |
Smaragdina Chevrolat | 1 | 1 |
Tituboea Lacordaire | 3 + undet. | 3 |
Undetermined | 11 | 5 + 6 undet. |
Cryptocephalini | ||
Cryptocephalus Geoffroy | 1 + undet. | 1 + undet. |
Cadmus Erichson | 1 | 1 |
Coenobius Suffrian | 1 | 1 |
Griburius Haldeman | 1 undet. | 1 |
Isnus Weise | 1 | 1 |
Pachybrachis Chevrolat | 1 + 2 undet. | 2 + undet. |
Undetermined | 2 | 1 + undet. |
Since most records found in the extant literature are the product of a chance finding of the beetles in association with the ant nests, and not of a directed search, it not clear how widespread ant associations really are. Below we discuss some patterns of ant associations we recognized in our synthesis. The study of myrmecophilous beetles have has revaled an extraordinary amount of adaptations (
Quality of available data. Records of myrmecophilous species summarized in Table
Taxonomic patterns of host use. All records examined here indicate that myrmecophilous cryptocephalines are specialists on the formicoid ants, a branch of Formicidae, which include the most common ant species as well as the major invasive species (
The most striking pattern that emerges from the assembled data relates to Clytra. Members of this genus have the broadest host range, with records from some of the more core formicines such as the carpenter ants (Camponotus) and Formica ants, but also from the myrmicines Aphaenogaster, Messor, and Tetramorium. While many species of Camponotus and Formica can be found commonly in forested environments (and often, in fact, co-occur), species of Messor are found in more xeric environments, and are herbivorous, seed-harvesting ants (the former are generalist predators). However,
Below we summarize some of the broad challenges of myrmecophily mentioned above (see (
1) Finding the host ant. In some Clytrini, the female oviposits on a leaf and drops the egg, after being intricately covered by feces, to the ground. Ants then carry the eggs, or the first instar larvae within its fecal case, inside the nest (
2) Living outside the nest. Some species have been found on external ant debris and are known to feed on it. The biologic meaning of this have not yet been studied, it might be that debris is a rich food source, or possibly, it provides the beetle or larvae with some sort of camouflage.
3) Trail following.
4) Entering the ant nest. All myrmecophiles must enter and remain in the ant nests without being expelled or killed (
5) Evolution towards living and surviving in ant nests. Once inside an ant nest, whether temporarily or long-term, every myrmecophile is faced with new challenges, from avoiding being detected as an enemy, to finding a safe micro-habitat within the ant complex, to finding food, and carrying on its life cycle.
5a) Avoiding being eaten by ants.Cryptocephalinae adults exhibit some typical chrysomelid defenses – chemical sequestration and secretion of toxic compounds (e.g. reflex bleeding) (
5b) Avoiding other dangerous organisms in the ant nest. In reports of associations with ants, hymenopterans are the most frequent parasitoids of eggs and larvae of the Camptosomata (
Within the proctotrupomorph Hymenoptera (most of the formerly recognized superfamilies of Parasitica; Sharkey et al. 2007) are a number of ant-specialist lineages. The Universal Chalcidoidea Database (
5c) Microhabitat specialization within the nest and diet: An ant nest presents multiple places to live, including open chambers, refuse heaps (“kitchen midden”), brood chambers or nurseries (heavily defended but high-quality food), and fungus gardens for those ants that cultivate fungi. Presently it is unknown where cryptocephaline myrmecophiles live within the ant nest. Some of these sites can offer different degrees of protection and different resources to exploit, yet nothing is known about the selection mechanism employed by myrmecophilous cryptocephalines among the different nest chambers. The only insight may be provided by the relation between the food inside the ant nest and the diet of the beetle larvae. Leaf beetles show a general pattern of adults and larvae living on the same host plants. However, some cryptocephalines show a further distinction where the larval and adult stages can have different habitats and diet; this is particularly true for Clytrini and Cryptocephalini. Some species have zoosaprophagous and phytosaprophagous larvae (
Fungi inside an ant nest can provide food or can pose a threat to cryptocephalines. Ants such as the Attini (the leafcutter ants) cultivate fungi and these fungus gardens may provide both a micro-habitat to live in and a larder of food. Fungi are commonly known to negatively affect immature stages of cryptocephalines. Yet, there is only one formal citation by
6.) Benefits for the host? Although no chemical recompense is known to be offered by myrmecophilous cryptocephalines,
Strength of host association. The strength of myrmecophilic relationships can vary, as some larvae can survive without actually entering an ants’ nest (
The reports to date suggest some degree of specialization in non-Clytra species. Megalostomis dimidiata is an Atta specialist; Anomoea, Clytrasoma (Fig.
Regarding the strength of currently known Cryptocephalines/ants associations,
Another unusual pattern to emerge from our synthesis is the case of Dorylus, a genus that includes army ants, which do not construct a typical ground nest like many other formicids, but instead, a bivouac as needed, and remain constantly in search of prey items (
Summarizing, existing evidence indicates multiple routes to myrmecophily in cryptocephalines, even if adults are above-ground herbivores and occasionally interact with ants; their immature stages (eggs, pupae and larvae) are the most exposed stages in terms of ant interaction. Myrmecophilous cryptocephalines can be found in subterranean (e.g. Megalostomis larvae found at 2.5m inside Atta nest), arboreal (e.g. Isnus in Acacia ant nests), and terrestrial (e.g. Pachybrachis on external debris of Atta nests) habitats.
Geography of ant association (Table
Genera of Cryptocephalinae by region and ant subfamily. Note all genera belong to the tribe Clytrini except for those marked with (*), which belongs to the Cryptocephalini.
Region | Formicinae | Myrmicinae | Dolichoderinae | Dorylinae | Undet. |
---|---|---|---|---|---|
Afrotropical | Hockingia | Hockingia, Isnus*, + undet. | - | Undet. | - |
Nearctic | Anomoea, Coscinoptera | Anomoea, Megalostomis | - | - | Anomoea, Coscinoptera, Lachnaia, Megalostomis, Saxinis |
Neotropical | Megalostomis, Pachybrachis* | Megalostomis, Griburius** | - | - | Helioscopa |
Oriental | Clytrasoma | ||||
Palearctic | Clytra, Cryptocephalus*, Lachnaia, Pachybrachis*, Tituboea, + undet. | Clytra, Smaragdina, Tituboea | - | - |
Clytra, Macrolenes Cryptocephalus*, Lachnaia Pachybrachis* |
Saharo- Arabian |
Clytra | Lachnaia, Tituboea | Labidostomis | - | - |
According to
Table
The evolutionary history of formicoid ants date back to the Upper Cretaceous period (
A parallel can be traced between the evolution of ants and cryptocephalines regarding climatic preferences. As mentioned above, the last major evolutionary event in ant evolution, according to
Key evolutionary steps in Camptosomata. Case-bearing and its correlated behavioral and morphological characters are a complex synapomorphy distinguishing the clade Cryptocephalinae + Lamprosomatinae within Chrysomelidae. It is the most obvious defense mechanism of these immature stages (
Recently,
Unraveling the evolutionary patterns of the habitat and diets shift in adults and larvae, as well as understanding, the multiple behavioral and morphological adaptations of ant-loving cryptocephalines will require extensive field work and inter-disciplinary approaches. The relationship with ants suggests the acquisition of ethological and morphological characters that are currently poorly studied. Some basic research activities include: field observations; experiments using artificial ant nests; and detailed morphological studies of the adults and immature stages. Also, the study of the degree of the association (facultative vs. obligate), the effects of this association on host plant choice (i.e. tropic selection mediated by ants), and the possibility of linked cladogenesis between ants and cryptocephaline phylogeny and diversification. Cost-benefit analysis will evaluate the role of each member in an association. Description of life cycles, as well as detailed anatomical studies of all stages are necessary, especially the study of myrmecophilous organs and the possible chemical cues involved. The behavioral, morphological, and chemical adaptations of cryptocephaline myrmecophiles are promising areas for further research.
This research was supported by the authors’ respective institutions. Agrain is grateful to CONICET for continued research support and Agencia Nacional de Promoción Científica y Técnica, Argentina (ANPCyT) for additional support to compete this work by PICT#2013-2211, and PICT#2011-2573. Chaboo is supported by the University of Kansas. Buffington and Chamorro are supported by the Systematic Entomology Laboratory, ARS-USDA. We are pleased to dedicate this paper to our esteemed colleague and chrysomelid researcher, Dr Pierre Jolivet, who has spent his professional career promoting knowledge of leaf beetles, including the relations of leaf beetles and ants. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.