ARTHROPOD BIOLOGY Natural History and Behavior of Nordus fungicola (Sharp) (Coleoptera: Staphylinidae)

STYLIANOS CHATZIMANOLIS1

Division of Entomology, Natural History Museum/Biodiversity Center and Department of Ecology and Evolutionary Biology Snow Hall, 1460 Jayhawk Blvd., University of Kansas, Lawrence, KS 66045Ð7523

Ann. Entomol. Soc. Am. 96(3): 225Ð230 (2003) ABSTRACT Details on the natural history and behavior of Nordus fungicola (Sharp) in Barro Colorado Island, Panama are presented. These beetles have bright coloration and wave their abdomen conspicuously. They feed on small drosophilid ßies or ßy larvae, and the typical grooming behavior after feeding is described. Beetles interacted aggressively with ants of the genus Ectatomma, and a preliminary experiment shows that beetles may use chemical secretions for defense. MaleÐmale and maleÐfemale interactions, and copulatory courtship are described. Males were not observed guarding females after mating. Females are not receptive after copulation.

KEY WORDS behavior, copulatory courtship, Staphylinidae, Nordus fungicola

Nordus fungicola (SHARP) BELONGS to the rove beetle cm in length) staphylinids ßy vigorously around rot- family Staphylinidae (Staphylininae: Staphylinini: ting fruitfalls and fungi during the day, frequently Xanthopygina), which consists of Ͼ46,200 described landing on the surrounding vegetation where they species (Newton et al. 2001) and represents one of the engage in a variety of behavioral interactions with most dramatic radiations in the history of life. Despite conspeciÞcs and others. The aim of this paper is to the fact that staphylinids are abundant and surely provide data about the natural history and behavior of ecologically important in many microhabitats (Ashe these beetles. 1998), very little is known about their behavior and ecology. Knowledge on the behavior and natural his- Materials and Methods tory of the Xanthopygina is so limited that for many of the genera (e.g., Elmas and Allostenopsis)wedonot Field observations were made on Barro Colorado even know the habitat in which they occur. A few Island (BCI), Panama, from 8 June to 12 August 2000 seminal studies suggest that their great diversity is and from 5 July to 13 July 2001 between 0900 and accompanied by a diverse array of complex behavioral 1800 h. Analysis of feeding, mating behavior, and other patterns, often mediated by chemical communication interactions was based on Þeld observation, videotape or secretions from complex and highly specialized recordings (Sony Hi8, Tokyo, Japan), and photo- gland systems (Peschke 1987, Alcock and Forsyth graphic slides. Ten adults were kept in a metal cage (30 1988, Forsyth and Alcock 1990a,b, Alcock 1991, Pe- by 30 by 30 cm) in a shaded area of the laboratory schke et al. 1996, Betz 1999). clearing for observations during the night. The genus Nordus has a neotropical distribution and Beetles interact with ants of the genus Ectatomma currently includes 36 species. N. fungicola is ideal for (Formicidae) on rotting fruits in the forest. To test the studying the natural history and behavior of a rove role of chemical secretions on the antÐbeetle inter- beetle. It is abundant in certain localities (e.g., Barro actions, 82 beetles were collected and killed by freez- Colorado Island, Panama) and can be easily found in ing (Ϫ15ЊC). Twenty-nine beetles were kept in n- the lowland tropical rainforests of southern Costa Rica hexane for6htoremove nonpolar hydrocarbons from and Panama, because it is a diurnal beetle that is their external cuticle and afterward were placed in an commonly visible on top of rotting fruits and mush- oven for 12 h to remove the n-hexane. I presented rooms. treated beetles (hexane extraction, presumably with- Adults of N. fungicola (Fig. 1) are easily recognized out nonpolar hydrocarbons) and frozen but untreated by their striking colors. The head, pronotum, and beetles (presumably still containing nonpolar hydro- elytra are brilliant golden-red, and the abdomen is carbons) to ants of the genus Ectatomma as food by shining black with patches of whitish pubescence and placing them in the pathway between the ant colony a bright yellow apex. These relatively large (up to 1.5 and the rotting fruits of Gustavia superba Berg (Lecythidaceae). The pathways were new every day 1 E-mail: [email protected]. and were established by the ants before the beginning

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moves the abdomen from side to side but did not mention an up-and-down movement. When disturbed by sudden movement and perhaps loud noises, N. fungicola ßew away and landed on the surrounding vegetation, usually within a meter of their previous place. Sometimes (N ϭ 40) when individuals of N. fungicola were on vegetation surrounding rotting fruits and fungi, they performed a 360Њ turn lasting 1 min, periodically waving their abdomen. Individuals of N. fungicola used mostly the middle and hind legs for walking, and when standing, the front legs almost never touched the substrate. The front legs were used for grooming and feeding (described be- low). Approximately 10 N. fungicola were kept in a metal cage for a period of 2 wk. The captured adults were not active at night; at this time they remained motionless on the walls of the metal cage while being grouped together within a radius of 3 cm. Both sexes have a pair of apicolateral tergal glands Fig. 1. N. fungicola on leaves in Barro Colorado Island, beneath abdominal segment VIII that were everted Panama. Reprinted from Chatzimanolis 2000, with permis- when the beetle waved its abdomen and were visible sion from the Journal of the Kansas Entomological Society. with the aid of a 200-mm telephoto lens. Secretions from these glands were bright yellow, had a piquant of the trials. Only one beetle was presented at a time, smell, and left a brownish stain on human skin, which the ant involved in the interaction was removed from suggests the presence of quinones (Peschke and Met- the colony after the trial, and not Ͼ10 beetles were zler 1982). Also, when the beetles were under stress, presented per colony. they secreted a brownish ßuid from the mouth. More detailed results of the chemical analyses of both chem- ical secretions will be presented elsewhere. Results Grooming. Grooming behavior always took place General. Adult beetles ßew vigorously around rot- immediately after food intake and also occurred at ting fruits on the forest ßoor (palm or G. superba)or other intervals. The front legs (especially the setae on fungi. On landing on the substrate, they always (N ϭ the protarsi and the protibiae) were used to clean the 590) raised their abdomens over their backs (Fig. 2) mouthparts and the head in a circular motion, starting and waved them antero-posteriorly four or Þve times, behind the head and ending at the mouthparts. The followed by a slower side to side movement, and prom- protarsi of both males and females are greatly en- inently displayed the brilliant yellow apex of the ab- larged, and effective grooming might be a function of domen. All other species of staphylinid beetles ob- these enlarged tarsi. The head turned right and left to served in the Þeld waved the abdomen up and down facilitate the movement of the front legs. The middle only; they were never observed to wave their abdo- legs were used to clean the hind legs and to brush off men in a left-right motion. Forsyth and Alcock (1990a) the elytra and the Þrst abdominal segments, while the reported that Leistotrophus versicolor (Gravenhorst) hind legs were used to clean the rest of the abdomen. When cleaning the abdomen, the beetles curved the last abdominal segments downward to reach the more apical segments. Also, the hind and fore legs were rubbed against each other. The hind wings were folded beneath the elytra with the help of the up- wardly bent abdomen. Feeding. Adult beetles of both sexes stalked and attacked drosophilid ßies (N ϭ 196) on a variety of substrates. Most commonly, the substrate was rotting fruits of palm or rotting fruits of G. superba, but the beetles also exhibited this behavior on mushrooms (N ϭ 5), monkey feces (N ϭ 2), and on fruit piles of banana and watermelon created by the observer ei- ther in the laboratory or in the Þeld. N. fungicola slowly approached the drosophilid ßies with small “steps” until one-half a centimeter away, and then quickly attacked by extending the front legs, mandibles, head, and thorax toward the ßy. The Þnal strike was given Fig. 2. N. fungicola waving its abdomen. usually with the enlarged protarsi and more rarely May 2003 CHATZIMANOLIS:NATURAL HISTORY OF Nordus fungicola 227

Fig. 4. Touching the tips of the abdomen is a typical maleÐmale interaction. Fig. 3. Mating almost always occurs near sources of food. When a female landed on the substrate, the closest with the mandibles. The beetle manipulated the cap- male attempted to mate with her. Females sometimes tured ßy with its front legs and mandibles and chewed (N ϭ 10) avoided copulation by rapidly waving their and sucked its body. Many beetles in the family abdomens when the male tried to mount them. There Staphylinidae, like most predaceous terrestrial arthro- was no apparent courtship before copulation except pods (Cohen 1995), feed by extraoral digestion. Adults that males slowly approached females from behind were observed eating three to four drosophilid ßies in and touched their antennae to the female abdomen for sequence, and if undisturbed afterward, remained at 1 s before attempting to mount. the site for Ϸ15Ð20 min without any apparent activity. The following description of copulatory courtship Beetles never tried to attack and seemed to avoid was the same for all mating events observed. Beetles interactions with ßies larger than or equal in size to the mated in a parallel position, with the male on top of the common house ßy (Musca domestica L.). female, for Ϸ69.5 Ϯ 1.2 s. During the Þrst phase of Adults attacked other ßy larvae, especially the lar- copulation, both middle legs of the male simulta- vae of Ptecticus nigrifrons Enderlein (Stratiomyidae) neously tapped the last abdominal segments of the in G. superba fruits (N ϭ 18) (Chatzimanolis 2000). female slowly and both front legs simultaneously They also used their mandibles to cut open rotting tapped the Þrst segments of her abdomen. The male mushrooms (N ϭ 5) to extract ßy larvae. The larvae of jerked his body forward and dorsally at periodic in- N. fungicola similarly fed on ßy immatures in G. su- tervals. All the above movements were relatively slow. perba fruits (unpublished data). Adults were also ob- After Ϸ30Ð40 s (time varied in different mating served eating dead, rotting moths (N ϭ 2) and simi- events), the male started jerking his body more rapidly larly decomposed crickets (N ϭ 3). and tapped on the femaleÕs body more quickly; this Mating. In total, 15 mating events were observed, 4 marked the initiation of the second phase. In both of which were recorded with a camcorder. Mating was phases the frequency of tapping with the front legs observed only near sources of food and in particular on was about twice the frequency of tapping with the G. superba fruits (N ϭ 11), on leaves near a dead middle legs. This general pattern of copulatory court- cricket (N ϭ 3) (Fig. 3), and on monkey feces (N ϭ ship, consisting of two distinct phases, is similar to that 1). On three occasions, a large aggregation of beetles described for Megalopus armatus Lacordaire (Co- was observed on rotting G. superba fruits. I sampled leoptera: Chrysomelidae) (Eberhard and Marin 1996) the beetles from three of these aggregations and found and in a very general way to that of other insects and that there was a male biased sex ratio (9:1, 10:1, and arachnids (Eberhard 1991, 1994). 11:1, respectively). In these cases, males did not de- In four different mating events, another male tried fend a speciÞc territory on the fruits and kept moving to displace the male that was mating and attach himself constantly. to the female by curving his body and attempting to In these aggregations, males were not aggressive to replace the copulating maleÕs genitalia with his own. each other and were never observed Þghting with These attempts were unsuccessful. their mandibles. When one male encountered an- After mating, the pair usually (N ϭ 13/15) repeat- other, they faced each other and approached until edly touched each other with the tips of their abdo- they were approximately a half-centimeter apart. mens and separated a few seconds later. Females did They turned rapidly, almost 90Њ, repeatedly touching not try to mate again with the same or another indi- each other with the apices of their abdomens (Fig. 4) vidual for as long as observations were possible. Fe- for less than2s(N ϭ 57). males left the fruit pile after a few minutes and ovi- 228 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 3

Table 1. Acceptance of beetles with and without nonpolar hydrocarbons

Beetles rejected Beetles accepted as food as food Nonpolar hydrocarbons 1a 28 absent Nonpolar hydrocarbons 12 31 present

a FisherÕs exact test (P ϭ 0.01). posited in a different fruit pile, away from the fruit pile of the mating event. A unique phenomenon present in these beetles is the large aggregations of males (although rarely ob- Fig. 5. The last abdominal sterna of N. fungicola. The served; only three times in a period of 12 wk) on white arrow points on the “v” shape modiÞcation of the rotting fruits of G. superba. This system cannot really eighth sternum. be deÞned as leks, because females can use the ßy larvae in the fruits as a food resource and because it is Discussion not clear if there is differential mating success among males, but rather is a scramble competition system, Betz (1999) described the grooming behavior for probably without aggression, that may arise because of various Stenus (Coleoptera: Staphylinidae) species, the high density of rival males on fruits. and Valentine (1973) described the general patterns Interactions with Other Insect Species. When an- of grooming behavior in Coleoptera. Betz (1999) men- tioned that the main role of the self-grooming behav- other insect approached, the beetles generally started ior was to spread pygidial secretions over the entire oscillating their antennae in a vertical plane (0 to 45Њ) body, which could act as fungicides, antimicrobics, or at an increased rate. They also waved their abdomens even make the beetles unpalatable to predators. This faster for a period of a few seconds. may be the case in Nordus as well, because the groom- Adults of N. fungicola were extremely aggressive ing behavior in Nordus is almost identical to that de- (i.e., attacked with their mandibles) when interacting scribed by Betz (1999) for Stenus. with adults of a related xanthopygine, Xenopygus ana- Recently, Betz and Mumm (2001) published data lis (Erichson) (N ϭ 7) and other staphylinids (N ϭ 4). on the predatory legs of Philonthus marginatus (O. These beetles share the same habitat (i.e., rotting Mu¨ ller) (Staphylinidae). He described the functional fruits) with N. fungicola but are rarely seen because morphology of the legs and especially how they are they tend to be under or inside the substrate. The used to capture prey. N. fungicola appears to have aggressive behaviors were observed in those rare in- similar front legs (with greatly expanded tarsi, see Fig. stances when they appeared on the surface of the 1), and observations in the Þeld suggest that the same substrate. Beetles did not interact with dung beetles mechanisms that operate in Philonthus are present in (N ϭ 20) or cockroaches (N ϭ 3) that were also N. fungicola. present on rotting fruits. Nordus, along with Elmas and Allostenopsis, are the Both N. fungicola and ants of the genus Ectatomma only genera in the subtribe Xanthopygina (total of 37 fed while on rotting G. superba fruits. Ants fed on the genera) with relatively big eyes (in proportion with actual fruit, whereas the beetles fed on ßies and ßy the rest of the head). Among these genera, Nordus has larvae that were on or in the fruits. The beetles and proportionally the biggest eyes, and these could be a ants only interacted if they were less than 1 cm apart. strong aid in the pursuit of prey. However, I was not If an ant approached a beetle, the beetle would im- able to tell if the beetle oriented its longitudinal body axis with the prey, so it is not clear if there was a visual mediately turn its abdomen toward the ant and rapidly alignment with the prey stimulus. wave it back and forth multiple times (N ϭ 32). In the ϭ Males of all species of the genus Nordus have well- vast majority of instances (N 25 of 32; 78.1%) the ant developed secondary sexual characters that are absent left immediately. from most other genera in the subtribe Xanthopygina. To test whether chemical substances are involved in These secondary sexual characters are extreme mod- the interaction, a preliminary experiment was made in iÞcations of the apical margins of the seventh and which beetles with and without nonpolar hydrocar- eighth abdominal sterna (Fig. 5). These structures are bons on their bodies were offered to the ants as a displayed when male beetles wave their abdomens, source of food (see Materials and Methods). The re- physically contact other individuals in maleÐmale in- sults are shown in Table 1. These results demonstrate teractions, and in postmating maleÐfemale interac- that ants more often rejected beetles that had non- tions. Eberhard and Marin (1996) argued that a Þrst polar hydrocarbons on their bodies (Fisher exact test, step in determining the function of a sexually dimor- P ϭ 0.01) than beetles lacking nonpolar hydrocarbons. phic character is to see if it is used in maleÐmale or May 2003 CHATZIMANOLIS:NATURAL HISTORY OF Nordus fungicola 229 maleÐfemale interactions. He stated that if the struc- waving of the abdomen of Nordus may be unique for ture is displayed in maleÐfemale interactions in a way xanthopygines or even staphylinids. The phylogenetic that would increase the femaleÕs perception of it, then position of Nordus is still enigmatic within the Xan- this structure is likely to have a role in sexual selection thopygina, and for that reason, it is difÞcult to place by female choice. If, however, the structure is used in the above behavioral observations in a phylogenetic maleÐmale combat in a way that will increase their context. The absence of other behavioral observations mating success, then it is likely to have a role in sexual in Xanthopygina makes it difÞcult to place the above selection by male combat. In this case, however, these behavioral observations even in a taxonomic context. sexually dimorphic structures do not seem to be used in any of the above instances. MaleÐmale interactions appeared not to be aggres- Acknowledgments sive and to not affect male mating success. There is, I thank J. S. Ashe, M. S. Engel, C. D. Michener, Allan H. however, the hypothesis that males interact with Smith-Pardo, M. G. Rightmyer, R. L. Rodriguez-S., chemical secretions and thus their behavior might be W. T. Wcislo, and two anonymous reviewers for helpful aggressive. The maleÐfemale interaction, besides mat- comments. I also thank the satellite bar on Barro Colorado ing, is only postcopulatory, because before copulation, Island and especially B. Denise Hardesty for their support the male sexual characters do not come into contact and ideas. Financial support was provided by a 10-wk grad- uate fellowship (Smithsonian Institution), a H. B. Hunger- with the females. One can argue that males display ford Travel Grant (Program of Entomology, Ecology and their secondary sexual characters to females by wav- Evolutionary Biology, University of Kansas), a Tinker Award ing their abdomens, but these structures are relatively (Center for Latin American Studies, University of Kansas), small and it is doubtful that females can actually see and a NSF PEET Grants (DEB-9521755 and DEB-9978110) them from a distance of a few centimeters. Also, it is awarded to J. S. Ashe. This is contribution no. 3283 from the not clear if the maleÕs secondary sexual structures Snow Entomological Collection, Division of Entomology, contact the femaleÕs abdomen during copulation and Natural History Museum, University of Kansas. if they have any role during copulation. Males of N. fungicola do not guard females after References Cited mating as do males of the related staphylinids Ontho- lestes cingulatus (Gravenhorst) (Alcock 1991), L. ver- Alcock, J. 1991. Adaptive mate-guarding by males of Ont- sicolor (Alcock and Forsyth 1988), and genus Eumi- holestes cingulatus (Coleoptera: Staphylinidae). J. Insect crota (Ashe 1987). Females of all of the above species Behav. 4: 763Ð771. Alcock, J., and A. Forsyth. 1988. Post-copulatory aggression except N. fungicola are receptive immediately after toward their mates by males of the rove beetle Leistotro- mating, and so the beneÞt to males of guarding females phus versicolor (Coleoptera, Staphylinidae). Behav. Ecol. immediately after copulation is high. N. fungicola fe- Sociobiol. 22: 303Ð308. males, however, are not receptive after mating and Ashe, J. S. 1987. Egg chamber production, egg protection also do not oviposit at the mating site (like L. versi- and the clutch size among fungivorus beetles of the genus color), and thus, there is no need for males to be Eumicrota (Coleoptera: Staphylinidae) and their evolu- involved in such a high-cost behavior as mate-guard- tionary implications. Zool. J. Linn. 90: 255Ð273. ing. Ashe, J. S. 1998. Subfamily Aleocharinae. In D. R. Maddison An interesting aspect of the biology of N. fungicola and W. P. Maddison (eds.). Tree of life: a distributed internet resource containing information about phylog- is chemical communication. The preliminary experi- eny and biodiversity (http://tolweb.org/tree?groupϭ ment presented here suggests the use of secretions for Aleocharinae&contgroupϭStaphylinidae). chemical defense in interspeciÞc interactions. A factor Betz, O. 1999. A behavioural inventory of adult Stenus spe- not taken into consideration here is the waving of the cies (Coleoptera: Staphylinidae). J. Nat. His. 33: 1691Ð abdomen (the bright yellow tip could a strong visual 1712. signal) and the inßuence it could have in combination Betz, O., and R. Mumm. 2001. The predatory legs of Phi- with the chemical secretion in repelling the ants. Fur- lonthus marginatus (Coleoptera: Staphylinidae): func- ther experimental manipulation is needed to deter- tional morphology and tarsal ultrastructure. Arthr. Struct. mine if the behavior exhibited by the ants is caused Dev. 30: 77Ð97. Chatzimanolis, S. 2000. An association between Ptecticus ni- only by the release of chemical substances by N. fun- grifrons (Diptera: Stratiomyidae) and Nordus fungicola gicola or by a combination of the chemical and visual (Coleoptera: Staphylinidae). J. Kans. Entomol. Soc. 73: signals. It is not clear, however, if there is chemical 232Ð234. communication in intraspeciÞc interactions, either Cohen, A. C. 1995. Extra-oral digestion in predaceous ter- between males or between males and females. restrial arthropods. Annu. Rev. Entomol. 40: 85Ð103. This study establishes the ground plan for the be- Eberhard, W. G. 1991. Copulatory courtship and cryptic havioral interactions of N. fungicola, although much female choice in insects. Biol. Rev. 66: 1Ð31. more work must be done in all the several aspects of Eberhard, W. G. 1994. Evidence for widespread courtship the behavior described above. It is yet unknown if all during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution. 48: species of Nordus exhibit similar behaviors. Although 711Ð733. some of the behavioral aspects (for example grooming Eberhard, W. G., and M. C. Marin. 1996. Sexual behavior or mating behavior) described above are expected to and the enlarged hind legs of male Megalopus armatus be similar in other genera of the subtribe, other as- (Coleoptera, Chrysomelidae, Megalopodinae). J. Kans. pects like the chemical interactions or the peculiar Entomol. Soc. 69: 1Ð8. 230 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 3

Forsyth, A., and J. Alcock. 1990a. Ambushing and prey-lur- Peschke, K., and M. Metzler. 1982. Defensive and phero- ing as alternative foraging tactics of the ßy-catching rove monal secretion of the tergal gland of Aleochara curtula. beetle Leistotrophus versicolor (Coleoptera: Staphylini- J. Chem. Ecol. 8: 773Ð783. dae). J. Insect Behav. 3: 703Ð718. Peschke, K., P. Friedrich, C. Cantert, and M. Metzler. 1996. Forsyth, A., and J. Alcock. 1990b. Female mimicry and re- The use of the tergaldefensive secretion in male intra- source defense polygyny bymales of a tropical rove bee- sexual aggression of the rove beetle, Aleochara curtula tle, Leistotrophus versicolor (Coleoptera: Staphylinidae). (Coleoptera: Staphylinidae), measured by closed-loop- Behav. Ecol. Sociobiol. 26: 325Ð330. stripping-analyses and tandem bioassay-mass fragmen- Newton, A. F., M. K. Thayer, J. S. Ashe, and D. S. Chandler. tography. Chemoecology. 7: 24Ð33. 2001. Staphylinidae, pp. 272Ð418. In R. H. Arnett, Jr. and Valentine, B. D. 1973. Grooming behavior in Coleoptera. M. C. Thomas (eds.), American beetles, vol. 1. CRS Press, Coleopts. Bull. 27: 63Ð73. Boca Raton, FL. Peschke, K. 1987. Male aggression, female mimicry and fe- male choice in the rove beetle, Aleochara curtula (Co- Received for publication 16 September 2002; accepted 6 leoptera, Staphylinidae). Ethology. 75: 265Ð284. February 2003.