Colobopsis cylindrica group

Laciny et al. 2018

Exploding Ants

C. saundersi complex
 * Colobopsis badia
 * Colobopsis corallina
 * Colobopsis saundersi
 * Colobopsis badia var. krama
 * Colobopsis badia saginata
 * Colobopsis solenobia
 * Colobopsis trieterica

Introduction
The Colobopsis cylindrica (COCY) group likely represents a monophyletic clade containing Southeast Asian ant species with distinctive hypertrophied mandibular gland reservoirs. In territorial combat, minor workers use the sticky and irritant contents of their enlarged mandibular gland reservoirs to kill or repel rival arthropods. In species where this defensive behaviour is more advanced, this happens via the characteristic suicidal “exploding” by voluntary rupture of the gastral integument (autothysis) (Cook 2008). This behaviour was first mentioned by Viehmeyer as early as 1916, and subsequently described in detail by Maschwitz and Maschwitz (1974), as well as Davidson et al. (2012), and Shorter and Rueppell (2012).

The Bornean members of the COCY group have been the subject of various ecological (e.g., Cook 2008, Davidson et al. 2007, 2009, 2016), morphological (Davidson et al. 2012, Laciny et al. 2017) and chemical (Jones et al. 2004, Hoenigsberger et al. in prep.) studies in the past.

Diagnosis
According to our morphological studies the COCY group can be defined as such: polymorphic Colobopsis with at least three distinct female castes: (i) winged, phragmotic gynes, (ii) phragmotic soldiers (doorkeepers), and (iii) minor workers with a considerable size variation; intermorphic workers may occur in addition (Laciny et al. 2017). Minor workers: Vertex highly raised above foramen. Eyes of minor worker small and flat, not breaking head sides in full-face view. Entire trunk with dense, reticulated microstructures; punctures of integument often reduced. Head with moderate, mesosoma with dense pubescence. Mesosoma (at least the pronotum, except in Colobopsis clerodendri dorsally with long undulated setae, never arranged in distinct rows. Gaster with appressed pubescence and two or three types of setae of different lengths (not arranged in rows, except at hind margin). Soldiers (not known of all taxa): differing from minor workers by enlarged heads and short appendages (antennae, palpi, legs); in most species with a clearly circumscribed head shield for phragmosis. Microsculpture and pilosity similar to minor worker.

Following this definition, the COCY group presently comprises 17 names in the rank of species, subspecies or variations, which are partly in synonymy to each other. The strong intraspecific variation of minor workers, the frequently lacking knowledge on soldiers (or gynes), and the historical descriptions of taxa from different morphs (either workers or gynes) make the species taxonomy a true challenge.

Morphology of males: The modified (enlarged) first funicular segment is presumably characteristic for males of Colobopsis. This characteristic has been described in the type species, Colobopsis truncata (Spinola, 1808), by Kutter (1977) and has been equally observed in several species of the Colobopsis cylindrica group. Males of the COCY group have previously been described for three species. However, these descriptions largely lack the necessary details to meaningfully compare taxa.


 * Colobopsis badia: Viehmeyer (1916) gives a brief description of a male from Singapore. Colouration, size, proportions of head and ocelli, as well as the enlarged first funicular segment correspond well to the examined male from Thailand.
 * Colobopsis severini (Forel, 1909): The extremely brief description of a male from the island Labuan (near Borneo) is not sufficient to draw any meaningful taxonomic conclusions.
 * Colobopsis leonardi (Emery, 1889): Karawajew (1929) gives a rather detailed description of males collected within a nest-series on Sumatra. The correct species identification by Karawajew is uncertain; the series may belong to another species of the Colobopsis leonardi complex as well. The pattern of pilosity on the gaster, with standing setae only present on the posterior half, also corresponds to our observations in males of the Colobopsis saundersi complex.

According to our knowledge, males of the Colobopsis cylindrica group can be distinguished from other Southeast Asian Colobopsis species by the relatively rich subdecumbent pilosity and the dense microreticulation of gastral tergites.

Historical Notes
A first attempt of a comprehensive classification of the species of Colobopsis (as a subgenus of Camponotus) was done by Carlo Emery. In his outstanding treatment of Formicinae (Emery 1925) he treated 58 species and established six groups to hold 49 of them (nine remained unclassified). He defined the [Camponotus (Colobopsis)] cylindricus group by a gradual variation between worker and soldier, interspecific variation of head in soldiers and females (from concave and marginate to oblique and obtuse), and generally large size. Emery included eight species presently classified as Colobopsis (Ward et al. 2016), of which Colobopsis calva, Colobopsis quadriceps, and Colobopsis smithiana are not presently assigned to this group (see below), whereas Colobopsis badia and Colobopsis corallina were not included (listed under incertae sedis). Although Emery (1925) correctly recognized the size variation of workers, he failed to recognize the unique characteristics of the soldier caste (see Laciny et al. 2017).

More species of the COCY group were subsequently described by Stitz (1925), Menozzi (1926) and Karawajew (1929, 1935). A second attempt at classification was made by McArthur (2012): His Camponotus (Colobopsis) cylindricus group consists of species with “neck attached to head well below vertex” and is broader than Emery’s (1925) cylindricus group. It includes the following species (according to current classification) that do not fit the characteristics of the COCY group in the present sense: Colobopsis anderseni, Colobopsis brachycephala, Colobopsis cotesii, Colobopsis desecta, Colobopsis excavata, Colobopsis hosei, Colobopsis mutilata, and Colobopsis quadriceps, as well as Camponotus dedalus, and Camponotus kutteri.

Species Complexes
A preliminary analysis of morphological and molecular data (unpublished) supports the division of the group into four species complexes (molecular data of one complex not available).

Colobopsis saundersi complex
We restrict the following analysis to the species of the Colobopsis saundersi complex, which includes Colobopsis explodens and can be defined by the following combination of characters observable in minor workers and soldiers: head always red or brown (not black); mesosoma moderately elongated and dorsally with some long undulated setae, at least on pronotum; node of petiole without long setae; gastral tergites with dense (in most species strongly transverse) micro-reticulation and with small hair pits (without large grooves). Soldiers and gynes (not known of all species) have a strongly truncated head, in most species with a well-defined (crested) head shield. The following names are available in this group (listed chronologically): Colobopsis badia Colobopsis corallina, Colobopsis saundersi, Colobopsis badia var. krama, Colobopsis badia saginata, Colobopsis solenobia, and Colobopsis trieterica.

Colobopsis corallina (and its synonyms Colobopsis solenobia Colobopsis trieterica) is an endemic species from the Philippines. Soldiers and gynes differ strongly from Colobopsis explodens and other taxa of the complex (as far as such morphs are known) by a very obtusely margined, not crested head shield. Minors have a bright orange colour on head, mesosoma, and petiole, often extending to gastral tergite I. Morphometrically, the examined minor workers of Colobopsis corallina (n = 31) mainly differ from those of Colobopsis explodens by a greater average length of appendages (SI 92–109 vs. 87–104; FeI 136–159 vs. 123–151; PSI 30–39 vs. 28–35).

The greatest similarity is observed between Colobopsis explodens and Colobopsis saginata, a taxon only known from a single alate gyne from Northern Borneo. The important structures of the head shield are almost identical. Although strongly different from Colobopsis explodens by pale orange brown colour, this gyne differs only by subtle morphometric characters of which the long and distally wide scape seems to be the most reliable (SI 83 vs. 78–80). The length of vein 4Rs+M is considerably longer in Colobopsis saginata than in Colobopsis explodens (WVI 65 vs. 26–58).

Colobopsis badia var. krama, described from a soldier from Java is a very poorly known taxon. We have not been able to study any further material from Java yet. The type (illustrated by AntWeb.org under CASENT0910610) differs from Colobopsis explodens. by a pale red head that strongly contrasts with the dark brown mesosoma, by a well-developed median carina of the head shield that reaches the foremargin of the clypeus, and by a stronger punctation of the preocellar area.

Colobopsis badia was described by Smith (1857) from Singapore and Sarawak (Borneo). However, the original description is too brief to draw any meaningful taxonomic conclusions. Viehmeyer (1916) describes workers of this species in more detail, also noting the secretion of a sticky liquid upon capture. He mentions a strong variability in colouration (from red to almost black with reddish head) and propodeal shape. This raises the question whether all examined specimens were truly members of the same species or perhaps belonged to one of the other, similar species of the Colobopsis saundersi complex. We examined the three syntype minor workers of Colobopsis badia in the. To fix the identity of this taxon, we have chosen the syntype from Singapore (imaged by AntWeb.org under CASENT0901897) as the lectotype of Formica badia. The two syntypes from Sarawak are in a relatively poor condition, which does not allow a complete morphometric analysis, and therefore the conspecificity with the Colobopsis badia type remains doubtful. We were not successful in obtaining fresh material of Colobopsis badia from Singapore, but a nest sample (minors only) from southern Thailand (Trang Province) which agrees well with the lectotype in morphology, especially morphometry, was available for a molecular analysis. It shows that Colobopsis badia and Colobopsis explodens are closely related, but distinct (Fig. 1). Although very similar to Colobopsis explodens in overall habitus and colouration, the examined Colobopsis badia minor workers are on average somewhat larger with less size variation (HW 1.22–1.57 vs. 1.46–1.59) and possess longer appendages (e.g., FeI 123–151 vs. 141–168; see Fig. 8a).

Biology
The behavioural observations on Colobopsis explodens conducted at KBFSC revealed multiple modes of behaviour that are either poorly studied or new to science. The diurnal activity pattern, as well as the positive influence of high temperatures correspond to the results of previous studies in related taxa (see Hamdan et al. 2013). Similarly large colonies containing several thousand individuals and extending to multiple trees and / or artificial nesting structures have also been described for other members of the genus (Federle et al. 1998, Laciny et al. 2017). However, it is still unclear whether individual workers are linked to certain parts of the colony or whether all foragers can move freely through the entire territory of the colony. An interesting and hitherto undescribed phenomenon in this regard is the presence of one or multiple “guards” at the artificial nest’s entrance: These minor workers were frequently observed to touch any incoming or leaving workers with their antennae. In some instances, returning foragers were delayed or altogether denied entrance by the guarding ants. One reason for this may be that some workers are linked to different parts of the colony. Alternatively, the observed guarding behaviour may be related to the limited capacity of the artificial nest, which is also suggested by the conspicuously balanced numbers of workers entering and leaving the nest during times of foraging activity. These behavioural patterns are hitherto undescribed and must be investigated in future studies. A further noteworthy activity observed in foraging workers was so-called “grazing” behaviour, in which minor workers were frequently seen using their mandibles to pluck and chew at various mosses, lichens, and other epiphytes on the bark of trees or other surfaces. While this activity can last for up to one hour at a time, its exact purpose remains unclear. It is possible that minor workers cut and consume parts of the plants and microorganisms or merely ingest fluids. As previous analyses of nitrogen isotopes (Davidson et al. 2016) suggest a largely plant-based diet for COCY ants, it seems likely that “grazing” contributes to their nutrition. However, other previously hypothesized modes of nutrition, such as tending of scale insects (Davidson et al. 2016) were not observed, and recent investigations on Colobopsis leonardi (Emery, 1889) (Zettel et al., ms submitted to Asian Myrmecology) even suggest a higher prevalence of carnivory in COCY ants than previously suspected.