Crematogaster borneensis group

In SE Asia, Crematogaster species, mainly from a single clade, are engaged with host plants of the euphorb tree genus Macaranga in one of the most species-rich obligate ant-plant symbioses found worldwide. In these mutualistic associations, the ants defend the trees against herbivores and overgrowing vegetation (Fiala et al., 1994; Itioka et al., 2000.

Species

 * Crematogaster borneensis
 * Crematogaster captiosa
 * Crematogaster claudiae
 * Crematogaster decamera
 * Crematogaster hullettii
 * Crematogaster linsenmairi
 * Crematogaster maryatii
 * Crematogaster roslihashimi

Introduction
Crematogaster borneensis-group Crematogaster have ten antennal segments and all are monomorphic. This is in contrast to the other three described species belonging to the former Decacrema from SE-Asia (Crematogaster angulosa, Crematogaster biformis and Crematogaster cephalotes) that all have dimorphic workers. Body size may vary strongly within species although this is dependent on colony size (e.g. TL ranges from ~ 2.1 mm to 3.3 mm in Crematogaster captiosa workers). Thus, especially in workers relative measures (e.g. SI or RLEG) are more important characters than absolute measurements (e.g. SL or LHT). Workers collected from small colonies are also lighter in colour. In queens shade of body coloration is a useful character, as are absolute measures. If possible, queens should be used for determination as worker characteristics are sometimes less distinctive.

Three further species of the former subgenus Decacrema have been collected and described from the distributional range of the Crematogaster-Macaranga association: Crematogaster angulosa, Crematogaster biformis and Crematogaster cephalotes. These three species are not associated with Macaranga. Propodeal spines of Crematogaster angulosa and C. cephalotes are considerably stronger and also longer in proportion to the thorax in comparison to obligately Macaranga-associated Crematogaster species, which may be an adaptation to the life-style in the latter group (Fiala & Maschwitz, 1990). In contrast to the Macaranga-associated Crematogaster borneensis-group species all three species are dimorphic and possess a pronounced metanotal groove.

Species identification of Macaranga-associated Crematogaster (Crematogaster borneensis-group) is easier and more conclusive based on queens as they possess more distinct characters than workers (i.e. length of compound eyes and the ocelli). Female sexuals can often be collected easily and should be collected together with workers. Queens tend to be in the lower part of the stem in small host plants recently colonized. Once Macaranga hosts grow larger the queen remains in the lower part of the lignified tree trunks and then becomes almost inaccessible (Feldhaar et al., 2003b). Nonetheless, virgin queens can often be collected together with workers by cutting off a larger branch of the host. After the reproductive stage has been reached by the colony, female as well as male sexuals are often present and can often be found in the proximal part of the branches close to tree trunks. In this way sexuals can be collected without destroying the whole colony. Crematogaster (Crematogaster borneensis-group) associated with Macaranga have never been observed away from their hosts, with the exception of queens and males during mating flights. Colonies never extend over more than one host tree. Identity of the host-plant can help to confirm species identification; a myrmecologist with limited knowledge of Macaranga species should at least pay attention to whether the host plant´s stem is covered by a glaucous wax-cover or not as most Macaranga-associated Decacrema species will either colonize waxy or non-waxy hosts.

Most of the diversity of the species is apportioned between the decamera-subgroup and the captiosa-subgroup. The placement of Crematogaster maryatii is unclear. In the molecular phylogeny based on mitochondrial DNA this species does not cluster with either group and came out most basal. Based on nuclear DNA (elongation factor 1α) (Feldhaar et al., 2010) this species is not separated from species of the captiosa-group. However, queen morphology and life-history characters resemble that of the decamera-group. Small size of queens and workers and early onset of reproduction may be a convergent trait though as this seems to enable usage of less productive and slow growing host plants (Feldhaar et al. 2010). Therefore, we currently do not place C. maryatii in either group.

Species subgroups were designated based on morphological characters of the queen caste, i.e. queens of the decamera-subgroup are smaller (WL ranging from 1.7 to 2.3 mm) and have relatively smaller compound eyes (EL<0.5 mm) than queens of the captiosa-subgroup (WL ranging from 2.2 to 2.9 mm and EL > 0.5 mm) (Feldhaar et al., 2003a; Feldhaar et al., 2010)

Crematogaster decamera subgroup

 * Crematogaster decamera
 * Crematogaster hullettii
 * Crematogaster roslihashimi

Species of the Crematogaster decamera-group typically have relatively small workers and queens that are dark brown in colour. The compound eyes are smaller than 0.5 mm in diameter (EL) and eye length usually comprises less than one third of head length (REL < 0.35). Diameter of the median ocellus of queens always smaller than the distance between the two lateral ocelli (OW < OD1). Propodeal spines of workers are absent in C. decamera and C. roslihashimi and only very short in C. hullettii. Species only colonize Macaranga hosts of the section Pachystemon.

Crematogaster captiosa subgroup

 * Crematogaster borneensis
 * Crematogaster captiosa
 * Crematogaster claudiae
 * Crematogaster linsenmairi

Species of the Crematogaster (Decacrema) captiosa-subgroup have relatively large queens with large compound eyes with EL > 0.5 mm (except for Crematogaster claudiae (EL 0.45 – 0.5 mm) whose queens are generally smaller than the queens of the other species within this group). Queens are medium to light brown in colour. Workers of Crematogaster borneensis, Crematogaster linsenmairi and Crematogaster captiosa possess long and acute propodeal spines.

Crematogaster claudiae has an intermediate morphology of species belonging to the captiosa and the decamera-group. Queens are intermediate in size (HW, HL, WL and EL) and workers possess none or only very short propodeal spines in contrast to the long and acute propodeal spines of workers of the other three species in the captiosa-group. As it clusters with species of the captiosa group in molecular phylogenies based on mitochondrial DNA (Feldhaar et al., 2003a, Feldhaar et al., 2010) and is known to hybridize with C. captiosa locally (Feldhaar et al., 2010, we have placed this species into this group.

Natural History
As extensive work on this ant-plant symbiotic system has been conducted over the last decades, we here summarize only some important aspects (for a detailed compilation see e.g. Feldhaar et al., 2010 and references therein). All associations between Crematogaster borneensis group species and Macaranga begin by newly mated foundress queens swarming and searching for a suitable host for colonization. Mating flights are presumably nocturnal and occur all year round (personal observation, B. Fiala and H. Feldhaar). After localization of a host-plant, probably by chemical cues (Inui et al., 2001; Jürgens et al., 2006), single queens enter the plant by chewing an entrance hole into an internode. The hole is sealed from the inside and colony founding is claustral. The first emerging workers open up the internode from inside and start foraging for food provided by the plant, i.e. food bodies (Beccarian bodies) and extrafloral nectar as well on honeydew from specific coccids living in the interior of the stem (Fiala & Maschwitz, 1991; Fiala & Maschwitz, 1992). Whereas several colonies may be founded simultaneously on a seedling, only a single colony dominates each host due to competitive replacement. Ant colonies grow as available nesting space and food provisioning increases with the growth of the host-plant. Workers are never found leaving their host for foraging.

Crematogaster borneensis group ants are generally monogynous and monandrous (Feldhaar et al., 2005; Feldhaar et al., 2010). There are exceptions, though, with Crematogaster decamera and Crematogaster captiosa regularly turning secondarily polygynous (Feldhaar et al., 2000). Furthermore, associations of unrelated foundresses may lead directly to polygynous colonies in Crematogaster linsenmairi in habitat patches with strong nest site limitation (Feldhaar et al., 2005).

All the obligately Macaranga-associated Crematogaster borneensis group species colonize host species belonging to the sections Pachystemon and Pruinosae within the genus Macaranga (Blattner et al., 2001; Davies et al., 2001). The section Winklerianae that is endemic to Borneo is exclusively colonized by a species that we had named Crematogaster morphospecies 8 in former publications by our group (Fiala et al., 1999). This species belongs to a different subclade of the genus Crematogaster and was never found on Macaranga species of sections Pachystemon or Pruinosae. Since its placement within the genus Crematogaster is still unclear we have not included this species in the present study. Three Macaranga species (Macaranga puncticulata, and, in part of their range, Macaranga lamellata and Macaranga griffithiana) were found to be specifically inhabited by different species of the genus Camponotus (Maschwitz et al., 1996; Federle et al., 1998a; Federle et al., 1998b; Maschwitz et al., 2004).

The associations of ants and plants are not strictly species-specific, as each of the eight species inhabits between two to seven different Macaranga hosts over their whole distributional range. From the plants´ point of view, each species of Macaranga is obligately associated with up to three different Crematogaster (Crematogaster borneensis-group) species (with exception of M. winkleri and M. winkleriella that are always colonized only by C. msp. 8) (Fiala et al., 1999; Feldhaar et al., 2003a; Feldhaar et al., 2003b). Nonetheless, non-random recurring association patterns between the two groups are stable over a wide geographic range (Fiala et al., 1999; Feldhaar et al., 2003a; Feldhaar et al., 2003b; Quek et al., 2004; Quek et al., 2007). Macaranga hosts generally show a smaller geographic distribution in comparison to the ants, and a higher degree of endemism. In contrast, four out of the eight species of Crematogaster (Crematogaster borneensis-group) occur over the whole distributional range of this ant-plant association comprising Malaya, Sumatra and Borneo and some smaller islands in the Sunda-region (Fiala et al., 1999; Quek et al., 2007). These widespread species of Crematogaster (Crematogaster borneensis-group) often inhabit different Macaranga species in different regions and may also colonize more than one host plant species within a region (Fiala et al., 1999; Feldhaar et al., 2003a; Feldhaar et al., 2003b; Quek et al., 2004; Quek et al., 2007). However, at most three Macaranga species per site are inhabited by a particular ant species. The ant species each colonize a non-random subset of Macaranga-species that shares specific morphological traits (Fiala et al., 1999; Quek et al., 2004; Feldhaar et al., 2010). Macaranga-hosts form two distinct groups with host plants whose stems are covered with an epicuticular wax-bloom and non-waxy hosts lacking such coating, with the exception of a few hosts that have only a slight wax-cover (M. glandibracteolata) or produce wax-blooms only as large trees (M. indistincta) (Blattner et al., 2001). Only “wax-runners” are able to walk on the slippery, waxy plant surfaces, whereas workers of the other species will either drop off the plant or can only move very slowly on such host stems (Federle & Brüning, 2005; Federle et al., 1997). Wax-running ability is a species-specific trait facilitated by a combination of morphological, locomotory and behavioural adaptations (Federle & Brüning, 2005). A second trait influencing ant colonization involves stems that need to be actively excavated, versus naturally hollow stems (Feldhaar et al., 2010). In the former, energy expenditure during colonization may be higher for the ant partner. Thus, host species with stems that need to be actively excavated tend to be colonized by species of the captiosa-subgroup with larger queens. As a consequence, hosts of the solid-stemmed section Pruinosae are solely colonized by queens of the captiosa-subgroup. These hosts can only be colonized when seedlings are taller than approximately 50 cm. Hosts are then more strongly lignified in comparison to the small and relatively thin-tissued seedlings Macaranga species of the section Pachystemon that develop swollen internodes for ant colonization. The larger size of queens, their presumably stronger mandibles and their greater energy reserves enable queens of the captiosa-subgroup to also found colonies in tips of branches of large, abandoned Macaranga hosts. This behaviour was never observed for queens of the decamera-subgroup and C. maryatii (Feldhaar et al., 2003b).