J Chem Ecol (2007) 33:1663–1669 DOI 10.1007/s10886-007-9343-9
One Hundred Million Years of Chemical Warfare by Insects G. O. Poinar Jr & C. J. Marshall & R. Buckley
Received: 15 March 2007 / Revised: 3 July 2007 / Accepted: 10 July 2007 / Published online: 10 August 2007 # Springer Science + Business Media, LLC 2007
Abstract An important defensive strategy among animals is the use of chemical compounds with toxic or irritating properties. In this paper, we report the discovery of an Early Cretaceous soldier beetle (Coleoptera: Cantharidae) in Burmese amber that seemingly employed a chemical defense response against a potential predator. Six pairs of cuticular vesicles with associated gland reservoirs were extruded from the insect’s abdomen, and a secretion released from one of these covers a portion of the antenna of a second insect species, considered to be the perpetrator of the response. This is the earliest fossil record of a putative chemical defense response and suggests that chemical defense mechanisms in beetles have been in existence for at least 100 Ma. Keywords Soldier beetle . Cantharidae . Chemical defense response . Extruded vesicles . Burmese amber . Early Cretaceous
Introduction Combat between individuals involves both offensive and defensive strategies. Among animals, one important defensive strategy is the use of chemical compounds with toxic or irritating properties. While many animals use this type of warfare today, fossil evidence of chemical defenses is rare and limited to ink sacs in Pennsylvanian and Jurassic cephalopods (Boucot 1990), defensive secretions in Dominican amber soldier termites (Poinar 1998), and slime deposits from Dominican amber velvet worms (Poinar 2000). The present study reports a putative chemical defense response employed by a soldier beetle (Coleoptera: Cantharidae) in apparent response to tactile molestation by a potential predator in Early Cretaceous Burmese amber. G. O. Poinar Jr (*) : C. J. Marshall Department of Zoology, Oregon State University, Corvallis, OR 97331, USA e-mail:
[email protected]
R. Buckley 9635 Sumpter Road, Florence, KY 41042-8355, USA
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Materials and Methods The amber piece containing the beetle is rectangular, measuring 7 mm long by 4 mm wide by 2 mm deep. The fossil was collected from lignitic seams in sandstone–limestone deposits in the Hukawng Valley in Myanmar. The mine site was located on the slope of the Noije Bum hill about a mile (1.5 km) SSW of the old Khanjamaw mine site and southwest of Maingkwan (26°2′N, 96°36′E). This site is newly mined (D. Cruickshank, personal communication, December 20, 2006) and has been designated as the “Noije Bum 2001 Summit Site.” Paleontological findings from this site assigned its age to the Upper Albian (100 Ma BP) of the Early Cretaceous (Cruickshank and Ko 2003). On the basis of spectroscopic and anatomical evidence, the source of Burmese amber from this site was determined to be a member of the Araucariaceae (Poinar et al. 2007). The specimen was deposited in the amber collection of Ron Buckley under accession no. ABS66.
Results The fossil is approximately 4.5 mm in length, well preserved, complete, and in a clear piece of amber. The beetle is a member of the family Cantharidae and will be described separately. Cuticular vesicles with associated gland reservoirs were extruded from the lateral membrane on each side of the first six abdominal segments (Figs. 1a,b and 2a,c). Secretions were released from the first three vesicles on both sides of the abdomen. By far, the largest deposit (1.4 mm in length) had been released from the extruded vesicle on the right side of the first abdominal segment at the point of contact with a filiform, setaceous, multisegmented antenna belonging to an unknown, alien insect. In this deposit are a number of spherical to subspherical crystal-like bodies ranging from 22 to 34 μm in greatest diameter (Fig. 1c).
Discussion The extruded vesicles on the fossil soldier beetle are similar in size and shape to those described by Sulc (1949) on a European species of Cantharis. Soldier beetles (Coleoptera: Cantharidae) are small- to moderate-sized insects with weakly sclerotized or leathery wing covers. The relatively short-lived adult beetle is active during the day in search of food, which is mainly small insects and pollen from a variety of plants (Dillon and Dillon 1961; Crowson 1981; Daly et al. 1998). Although cantharids are widely distributed today, fossils of this group are unusual, and until the present report the oldest described fossil soldier beetles were from Baltic amber (40 Ma; Spahr 1981; Carpenter 1992). The present discovery more than doubles the previous fossil record. The structure of the antenna of the potential predator is consistent with those of members of the orders Orthoptera and Blattaria, and the antenna passes through the entire amber piece along the right side of the beetle (Figs. 1a and 2a,b). Members of the above groups that existed at that period and had this type of antennal structure were katydids, crickets, elcanids, and cockroaches, all of which have been reported in Burmese amber (Poinar et al. 2005). This insect probably extended its antennae to investigate the soldier beetle as a future meal. As soon as the beetle detected the intruder’s presence, it presumably extruded its abdominal vesicles and emitted defensive secretions (Fig. 3).
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Fig. 1 a Soldier beetle in Burmese amber showing chemical defense behavior. Lateral view showing extruded vesicles (arrows) on abdominal segments 1 to 6. Bar=800 μm. b Soldier beetle in Burmese amber showing chemical defense behavior. Detail of anterior region of beetle showing deposit from extruded vesicle on the first abdominal segment covering a portion of the foreign antenna (arrow) and the remainder of the excretion extending over the beetle’s thorax (arrowhead). Bar=370 μm. c Soldier beetle in Burmese amber showing chemical defense behavior. Crystals and crystal aggregations in the extruded deposit. Bar=45 μm
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Fig. 2 a Soldier beetle in Burmese amber. Dorsal view showing large deposit (arrows) from extruded vesicle on the right side of the body. Bar=176 μm. b Soldier beetle in Burmese amber. Detail of a portion of the alien antenna. Bar=38 μm. c Soldier beetle in Burmese amber. Extruded vesicle from the fifth abdominal segment on left side of body. Bar=21 μm
The vesicle nearest the area of direct molestation (where the foreign antenna made physical contact with the beetle) deposited the largest amount of secretion. Many insects only discharge defensive droplets adjacent to the area of tactile molestation (Blum 1981), thus conserving secretions. Some of the secretion was deposited on the orthopteroid antenna, whereas the remainder was ejected over the insect’s right shoulder (Fig. 1b). A
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Fig. 3 Proposed scenario on the bark of the resin-producing tree just before the soldier beetle was entombed. In the upper left is a blattid with one antenna extended along the right side of the beetle. The beetle is responding by everting six pairs of cuticular vesicles with associated gland reservoirs. A drop of resin in the upper right is falling on the beetle. Patches of lichens and moss are growing on the surface of the bark. We portrayed a cockroach as the bearer of the alien antenna because they occur on bark, are omnivorous, and are known from Burmese amber
moment after the beetle released its secretions, it was covered by a flow of resin. Whether the entire predator was also captured is unknown; however, its remaining antenna provides evidence of its presence. This scenario would explain why the preserved beetle was likely employing a defense response, why most of the extruded secretion came from only one everted vesicle, and how some of the secretion ended up on the perpetrator’s antenna. Chemical defense mechanisms have evolved at least 30 times in Coleoptera, including in all members of the Adephaga and in representatives of at least 20 families of Polyphaga (Blum 1981; Dettner 1987). Aside from chemicals produced in specialized glands, distasteful, emetic, or caustic compounds in insect hemolymph are also employed in defense responses (Blum 1981; Dettner 1987). Toxic hemolymph can be released from openings positioned between segments (reflexive bleeding) or via cuticular vesicles extruded from the abdomen and thorax. Some examples of chemical defense mechanisms involving cuticular vesicles in various families of beetles are listed here. Secretions expelled from extrusive sacs located on the abdomen and thorax of tenebrionid beetles contain benzoquinone, toluquinone, ethylquinone, phenols, aldehydes, and ketones (Tschinkel 1969, 1975a, b). Adult and larval leaf beetles (Chrysomelidae) respond to tactile stimulation by a potential predator by releasing hemolymph with defense compounds (Hilker and Schulz 1994) through cuticular openings positioned along the edges of the thorax and first seven abdominal segments (Pasteels et al. 1988). In disturbed galaerucine (Chrysomelidae) larvae, hemolymph is expelled from extruded dorsolateral vesicles (Bünnige and Hilker 2005). This sticky deposit, which may also contain glandular secretions, can entangle the mouthparts of invertebrate antagonists. After expelling the chemical defenses, these vesicles are retracted back into the body. Malachiinae (Melyridae) beetles also contain extrusive vesicles located on the abdominal and thoracic segments. Adults of the New Guinea genus Choresine contain secondary bioactive compounds called batrachotoxins in their hemolymph, which are apparently expelled through their protruded vesicles located on abdominal segments 1 to 6 and on the prothorax and metathorax (Dumbacher et al. 2004). It was not possible to identify the crystals in the droplet released by the fossil soldier beetle because any attempted analysis would probably destroy the specimen, but the crystals likely represent defensive chemicals. Soldier beetles of the genus Chauliognathus produce certain types of carboxylic acids as well as triglycerides and glyceride esters from
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paired exocrine glands located on the thorax and abdomen (Meinwald et al. 1968; Moore and Brown 1978; Eisner et al. 1981; Brown et al. 1988). Diterpenes have also been recovered from members of the genus Cantharis (Durvaux et al. 2007). These products seem to be unique to cantharids and could possibly be acquired by feeding on certain types of plants (Blum 1981). Today, defensive chemicals play an important survival role in insects, but just when beetles began producing toxic compounds in specialized exocrine glands is unknown. The present discovery shows that members of the family Cantharidae had established a chemical arsenal for defense some 100 Ma ago. Acknowledgements Thanks are extended to Art Boucot and Roberta Poinar for comments on earlier drafts of this study.
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