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A Heretofore Unreported Instant Color Change In a Beetle, Nicrophorus tomentosus Weber (Coleoptera: Silphidae)
Bernd Heinrich

Northeastern Naturalist, Volume 19, Issue 2 (2012): 245–352

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2012 NORTHEASTERN NATURALIST 19(2):345–352 A Heretofore Unreported Instant Color Change In a Beetle, Nicrophorus tomentosus Weber (Coleoptera: Silphidae) Bernd Heinrich* Abstract - The burying beetle Nicrophorus tomentosus (Silphidae) (Tomentose Burying Beetle) achieves an instant color change from a strikingly black and orange animal to a largely yellow one. This transformation achieves a mimicry of several species of bumblebees when they are in flight, and it is accomplished by twisting the elytra to expose their yellow undersides while simultaneously hiding the bright orange and black upper sides. The overall effect is an apparent combination of both Muellerian and Batesian mimicry of bumblebees. Introduction Most burying beetles, Nicrophorus spp., are crepuscular or nocturnal and spend the daylight hours in hiding. They feed on small animal carcasses that they find above ground, often transport them a short distance, and then bury them. They have evolved a complicated bi-parental care of their larvae (Milne and Milne 1976, Trumbo 1990) where a mated pair cooperate (Fetherston et al.1990, Trumbo 1991) in the feeding of and communication with their young. Most are solidly black but with bright orange markings on their elytra. The coloration of Nicrophorus, like that of other beetles, derives mainly from the wing covers (elytra) which evolved from a front pair of wings (Dudley 2000) that now either serve no, or only a slightly active role, in flight (Schneider 1975). Beetle elytra are often strikingly colored, and the colors serve a variety of adaptive functions such as in mimicry (Cott 1940, Ruxton et al. 2004). The colors are achieved not only by pigments but also, as in some other insects (Anderson and Richards 1942, Stavenga et al. 2011) and in some iridescently colored birds (Prum et al. 2006), due to micro-anatomical features of the integument. Such “structural” colors, based on diffraction gratings and multilayer interference, may change reversibly in some beetles due to absorption of moisture that alters the thickness of the transparent films and thus changes the reflectance spectrum (Hinton and Jarman 1972). Other animals can change colors by chromataphore movement in their skin, such as in some lizards, amphibians, fish and octopi, but the hard exoskeleton of insects precludes these rapid and spectacular physiological color changes (Bagnara and Hadley 1973). Here I report the instantaneous change in appearance to more closely resemble a bumblebee (Bombus) of the diurnally active N. tomentosus Weber (Tomentose Burying Beetle) found in North America east of the Rocky Mountains. Burying beetles of some species have been identified as convincing mimics of bumblebees in flight (Fisher and Tucherman 1986, Lane and Rothschild 1965, Milne and *Department of Biology, University of Vermont, Burlington, VT 05405; bernd.heinrich@ 346 Northeastern Naturalist Vol. 19, No. 2 Figure 1. Photograph of a Nicrophorus tomentosus at a Blarina brevicaudus Say (Shorttail Shrew) carcass. Figure 2. Photograph of a dorsal view of a Nicrophorus tomentosus in free flight as it would commonly be perceived through human eyes if it were encountered in the field—a fuzzy yellow streak. Milne 1944), and that mimicry has been attributed primarily on the basis of their flight tone, flight patterns, activity times, and body size. I here examine color change and the role of color in N. tomentosus. As with other Nicrophorus, this species has bright orange stripes on its elytra (Majka 2011), which are prominent against a black background color (Fig.1). However, N. tomentosus additionally has, like many bumblebees but unlike other silphids, a yellow pubescence on the top and undersides of its thorax. Curiously, beetles of this species appear yellow in the instant that they take flight, and the human eye then no longer detects orange as would be expected from the bright orange on their elytra. However, flight is fast and often erratic, and the orange might be easy to overlook. Nevertheless, (although fuzzy) even photographs of beetles in flight in the field (Fig. 2) consistently showed no orange. Instead, the entire dorsum of the beetle appeared to be lemon yellow, and this was invariably the case in hundreds of sightings. 2012 B. Heinrich 347 Figure 3. Diagrammatic representation of a (right) wing cover (elytron) during the sequence (1 to 6) in the twist and flip maneuver that hides the colorful dorsal coloration and exposes the yellow underside during flight. X represents the outside edge of the elytron, and • shows the inner edge at the terminal tip of the elytron. Figure 4. A Nicrophorus tomentosus at the moment of take-off as it raises its elytra at the same moment that it extends its wings from their folded position beneath the elytra (Photograph courtesy of Stephen T. Trumbo.) 348 Northeastern Naturalist Vol. 19, No. 2 Results and Discussion Unlike in most other beetles (where lifting the elytra causes them to flip into a new stable position laterally to the sides), when I slightly lifted the elytra of live or freshly killed nicrophorines (three species: N. tomentosus, N. orbicollis Say, and N. sayi Laporte) from their locked positions, they always became twisted at the hinge where they are attached to the thorax. Instead of moving straight out to the side, their outer edges moved upward, and the whole elytron then moved back. As in other beetles, elytron movement is in part linked to wing extension. After the nicrophorine elytron was up, the wing could extend and move forward and back. Extending (pulling) the wing to the side caused the elytron to flip up, thus wing opening was linked to elytron opening and twisting. Return of the elytron to its original (dorsal side up) position caused the wing to lock in with the elytral movement and return back over the abdomen. When the elytra were pushed inward to cover the abdomen, they did not assume their previous position, as is the case with other, non-nicrophorine beetles. Instead, they continued their rotation until their formerly inner edges were to the outside and the formerly outer edge inward (Fig. 3). In this manner, the elytra were thus reversed over the abdomen, with the result being that Nicrophorus expose their lemon-colored elytral undersides instead of their dorsal surface during flight. This mechanical operation, which to my knowledge occurs in no beetles other than Nicrophorus, accounts for the otherwise black and orange beetle always appearing to be yellow the moment it takes flight. In a laboratory study of the role of beetle elytra during fixed flight on 16 different species, Schneider (1975) described one type, as exemplified by the June bugs (Phyllophaga) and rhinoceros beetles (Melolonthus) (both Scarabaeidae), where the elytra moved along with the wings (though through a much lower angle) and thus may serve a small but active function in flight. In tiger beetles (Cicindela) (Carabidae), the elytra were extended laterally but remained motionless in flight. In rose chafers (Cetonia) (Scarabaeidae), the elytra remain closed over the back, and in Nicrophorus, the elytra were not only held motionless and roof-like over the back in flight as in Cetonia, but their outer edges folded up in the long axis over the abdomen (“Die Elytra werden um die Langsachse nach ober geklappt und stehen dachartig über den Abdomen ohne mitzuschwingen”). Schneider (1975) was unable to demonstrate any effects on lift of the elytral positions taken during flight, but posited instead that the elytral posture may have a possible role in steering. No other possible function for the unique elytral flight position for Nicrophorus was offered. The origin of the elytral flip mechanism is unknown, but could it aid in mimicry? Although the above elytral flip and twist mechanism, which is mechanically coupled with the wing extension, can be achieved in dead animals, it appears in N. tomentosus only during flight, when the elytra are relatively closely 2012 B. Heinrich 349 depressed over and onto the abdomen. The mechanism occurs as the wings are extended, i.e., the moment before and during flight. High-speed photography of N. tomentosus beetles during the split-second of wing opening or closing strongly reinforces the inference that it functions in bumblebee mimicry (Fig. 4). Most nicrophorid beetles are nocturnal or crepuscular, but N. tomentosus is unusual in flying in the daytime. When burying beetles are disturbed by a potential predator at a carcass, they bury themselves quickly, or feign death. While searching for carcasses, however, they must fly and as a consequence become conspicuous targets to predators such as birds. Birds avoid capturing bumblebees after learning to recognize them (Evans and Waldbauer 1982), and a diversity of flies gain protection by mimicking them (Brower et al. 1960) in often, to our eyes, precise Batesian mimicry (Wickler 1958). The mimicry is so close that few besides entomologists may differentiate some flies, especially the bumblebee-mimicking syrphids, asilids, and oestrids, from bumblebees. That a brightly-colored, orange-and-black beetle can almost instantly change in appearance to that of a bumblebee provides a compelling example of visual mimicry, which complements the aural mimicry of the bees’ flight tone (Fisher and Tucherman 1986, Lane and Rothschild 1965), as well as matching their seasonal and diurnal activity cycle. In the most recent and most detailed publication of the mimicry of carrion beetles (Fisher and Tucherman 1986), it was proposed that because of its “bright yellow thoracic pile and orange-red elytra” the models of the N. tomentosus mimicry in Ontario are the bumblebees Bombus ternarius Say and B. rufocinctus Cresson. However, since these two bumblebee species are the most common northeastern species with orange on the abdomen, they could only serve as models if it is assumed that N. tomentosus follows the conventional beetle pattern and lacks the mechanism here elucidated; the beetles’ bright orange elytral stripes are not likely to have arisen to serve in the proposed mimicry because they are made to be invisible precisely during flight, the only time a nicrophorine resembles a bumblebee. While death-feigning nicrophorines have also been suggested to mimic bumblebees, the resemblance to a dead insect is then great but that to a bee is not, and the efficacy of mimicking a dead bee is also of questionable value. I propose here instead that N. tomentosus does not specifically mimic orange-red bumblebees, but instead hides its red, and creates a phenotype that mimics seven local yellow-and-black Bombus spp. Most of the about 46 species of North American bumblebee species (Heinrich 2004) have black bodies marked with yellow pile. Although seven of these species also have varying amounts of orange setae over the gaster, that color is always bordered by yellow and is never in sharp contrast to a black band as in nicrophorines. Unlike other local nicrophorines, N. tomentosus is a lateseason flyer (July to September in northeastern America [Majka 2011]), which is precisely when the worker numbers of up to seven black-and-yellow Bombus species (B. affini Cresson, B. vagans Smith, B. bimaculatus Cresson, B. sandersoni 350 Northeastern Naturalist Vol. 19, No. 2 Franklin, B. impatiens Cresson, B. perplexus Cresson, and B. griseocollis Degeer) peak. All these species have nearly identical color patterns and are difficult to differentiate (see color plate in Heinrich 1979). Bumblebees form apparent Muellerian mimicry rings (Plowright and Owen 1980). Since the workers of all bumblebees are distasteful and they sting, I conclude that N. tomentosus may, aided by its elytral flip to show bright yellow undersides, be a credible Batesian mimic, especially of the Muellerian mimicry ring of yellow bumblebees (Fig. 5). However, the orange markings of all the nicrophorids suggest a warning function, and future experimental study is needed to find out if N. tomentosis is indeed attacked less during flight because of the coloration it achieves by the elytral flip.. Although the elytral reversal convincingly serves N. tomentosus to become a bumblebee mimic, it raises many questions about the extent, diversity, and origin of both the unique mechanism and its possible application in the other 67 nicrophorine species. A comparative taxonomic study of their seasonal, diel activity, and geographic distributions, in conjunction with the ventral elytral colors and the amount of elytral twist, should provide the answers. Figure 5. Sketch of the approximately one-second-interval sequence of a N. tomentosus walking (lower right) to flight (top) and back to perching position (right). The bumblebee (center) has the approximate color pattern of seven locally sympatric species (see text ). 2012 B. Heinrich 351 Acknowledgments I thank John C. Abbott, Alfred Newton, Stephen T. Trumbo, Derek S. Sikes, Doekele Stavenga, David L. Wagner, and an anonymous reviewer for alerting me to valuable literature, stimulating discussions, and generous help in orienting me into the fascinating biology of Nicrophorus beetles. Literature Citations Anderson, T., and A.J. Richards. 1942. An electron microscope study of the structural colors of insects. Journal of Applied Physiology 13:748–758 Bagnara, J., and M.E. Hadley. 1973. Chromatophores and Color Change: The Comparative Physiology of Animal Pigmentation. Prentice-Hall, Englewood Cliffs, NJ. 202 pp. Brower, l.P., V.Z. Brower, and P.W. Wescott. 1960. Experimental studies of mimicry. V. The reactions of toads (Bufo terrestris) to bumblebees (Bombus americanum) and their robber fly mimics (Mallophora bomboides), with a discussion of aggressive mimicry. American Naturalist 94:343–355. Cott, E. 1940. Adaptive Coloration in Animals. Methuen and Co. Ltd., London, UK. 540 pp. Dudley, R. 2000. The Biomechanics of Insect Flight. Princeton University Press, Princeton, NJ. 536 pp. Evans, D.L., and G.P. Waldbauer. 1982. Behavior of adult and naïve birds when presented with a bumblebee and its mimics. Zeitschrift fur Tierpsychologie 59:247–259. Fetherston, I.A., M.P. Scott, and J.F.A. Traniello.1990. Parental care in burying beetles; The organization of male and female brood-care behavior. Ethology 85:177–190. Fisher, R.M., and R.D. Tucherman 1986. 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The evolutionary significance of bumble bee color patterns: A mimetic interpretation. Evolution 34:622–637. Prum, R.O., T. Quinn, and R.H. Torres. 2006. Anatomically diverse butterfly scales all produce structural colors by coherent scattering. Journal of Experimental Biology 209:748–765. Ruxton, G.D., T.N. Sherrett , and M.P. Speed. 2004. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry. Oxford University Press, Oxford, UK. 260 pp. 352 Northeastern Naturalist Vol. 19, No. 2 Schneider, P. 1975. Die Flugtypen der Käfer (Coleoptera). Entomologica Germanica 1(3/4):222–231. Stavenga, D.G., B.D.Wilts, H.L. Leertouwer, and T. Harriyama. 2011. Polarized iridescence of the multilayerd elytra of the Japanese Jewel Beetle, Chrysochroa fulgidissima. Philosophical Transactions of the Royal Society of London (B) 366:709–723. Trumbo, S.T. 1990. Regulation of brood size in a burying beetle, Nicrophorus tomentosus (Silphidae). Journal of Insect Behavior 3:491–500. Trumbo, S.T. 1991. Reproductive benefits and duration of parental care in a biparental burying beetle, Nicrophorus orbicollis. Behaviour 117:82–105. Wickler, W. 1958. Mimicry in Plants and Animals. World University Library, London, UK. 255 pp.