Author Institution: Museum of Zoology and Department of Zoology, The University of Michigan, Ann Arbo

Alexander, Richard D.

West, Mary Jane

The Ohio Journal of Science

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SUB-SOCIAL BEHAVIOR IN A BURROWING CRICKETANUROGRYLLUS MUTICUS (DE GEER)ORTHOPTERA: GRYLLIDAEMARY JANE WEST AND RICHARD D. ALEXANDERMuseum of Zoology and Department of Zoology, The University of Michigan, Ann ArborSub-social behavior, or specialized parent-offspring interaction that terminatesbefore the offspring mature, has been noticed in a wide variety of arthropods:millipedes, centipedes, scorpions, pseudo-scorpions, crustaceans, spiders, mites,web-spinners, cockroaches, earwigs, treehoppers, shield-backed bugs, giant waterbugs, beetles, wasps, and bees. Except for wasps and bees, it has been describedin detail in only a very few cases, perhaps most notably the earwig, Forficulaauricularia L. (Fulton, 1924; Weyrauch, 1929). This is surprising in view of theextent of investigations on the truly social insects (ants, wasps, bees, and termites)and of efforts to reconstruct the sequences of change by which they have evolvedtheir distinctive characteristics: division of labor, sterile castes, and complexcommunication (Wheeler, 1923; Michener, 1953, 1958; Evans, 1958).Various authors have mentioned that some female mole crickets (Gryllotalpinae)isolate themselves in their burrows with the eggs, live beyond the hatching of theeggs, and display hyper-aggressiveness in this situation (Hayslip, 1943; Hahn,1958). Females of Brachytrupes achatinus Stoll (Brachytrupinae), the "bigbrown cricket" of India, deposit their eggs shallowly in the end of one of theirgalleries and the young nymphs leave the parental burrow a few days after hatching(Ghosh, 1912). Liebermann (1955) noted that the female short-tailed cricket,Anurogryllus muticus (De Geer) (Brachytrupinae), lives in the brood chamberuntil the second or third molt of her offspring. This paper reports some detailsof parent-offspring interactions in the short-tailed cricket, discusses their adaptivesignificance, and hypothesizes that certain morphological and behavioral charac-teristics of non-social and sub-social crickets pre-adapt for the evolution of greatercomplexity in parent-offspring interactions.We have raised five families of Anurogryllus to partial maturity in the labora-tory, and in one case were able to watch and photograph during a period of severalweeks the behavior of a female in a burrow which she had excavated in sand alongthe glass wall of a jar (fig. 1-6). This female was collected as a juvenile in Kan-nopolis, North Carolina, on May 25, 1961; she mated in early June when a malewas first placed in her cage. Single matings per female are not otherwise knownin crickets, but after mating once, this female showed only aggressive behaviortoward males that were placed in her cage and then watched continually whilethey courted her for long periods, both inside and outside burrows. During theweeks following her mating, the female excavated an underground chamber intowhich she carried particles of apple, peach, and grass supplied in the cage, andfrom which she ousted intruding males and females alike. In expelling one malewhich we had purposely introduced into her burrow she actually tore off one ofhis hind legs (fig. 2); after repairing the damage to the burrow entrance, she atethe severed leg (fig. 3). Although we have watched several thousand cricketfights involving approximately 30 species in four subfamilies and ten genera, thisis our only record of definite physical damage; and it is apparently the only clearrecord of cannibalism as a result of cricket aggression. Both facts are surprising,for the males of this species are the most successfully territorial and the leastviolent of burrowing crickets in their aggression (Alexander, 1961); additionally,in this case the male did not at all reciprocate the female's aggression. Aside fromthis species, intense aggression among crickets is known to occur only in males,and only when both individuals are hyper-aggressive.THE OHIO JOURNAL OF SCIENCE 63(1): 19, January, 1963.20 MARY JANE WEST AND RICHARD D. ALEXANDER Vol. 63On July 16, the female was found to have in her chamber a pile of 16 eggs and4 first-stage nymphs. During the next two weeks she remained in the burrow,concentrated most of her actions in the burrow chamber, and repeatedly carriedout several specific actions in connection with eggs, nymphs, food, fecal pellets,substrate particles, and external disturbances. These several actions were alter-nated with each other, and with long periods of immobility spent without exceptionnear the eggs, short exploratory trips around the burrow, and grooming of variousportions of the body.FIGURE 1. Female of Anurogryllus muticus (De Geer) in brood chamber with new pile ofcut grass stems. Note antennal contact between juvenile and female. Filled defecationchamber is at left. Egg pile is partly covered with sand near female's left front leg. Tunnelsleading into the interior of the jar in which the female is confined begin directly on her right.The female burrowed up under chunks of apple as shown and plastered substrate particlesbeing removed from the burrow alongside the apple, creating "push-ups" of the sort indicated.The female's hind leg was lost while she was a juvenile. All illustrations for this paper weredrawn from photographs made through a glass side of this female's burrow. Prints from allphotographs used will be filed with a reprint of the paper in the Orthoptera library of the InsectDivision, University of Michigan Museum of Zoology.Two kinds of eggs were deposited: normal-sized, all of which eventually hatched,and miniature (unfertilized?), all of which were eventually seized, carried off, andeaten by the juveniles. During egg-laying, the female turned so that the tip ofher abdomen was near the egg pile; immediately afterward the female alwaysturned about, picked up the new egg, and placed it on the pile. Previously laideggs were frequently palpated, mouthed (picked up, turned about in the mouth-parts, briefly inserted partway into the mouth, and dropped again or pushed away-with one foreleg), piled and repiled, and sometimes covered with food or substrateand later uncovered. Miniature eggs seized by the nymphs were sometimesretrieved temporarily by the female, which chased the nymph, seized the eggdirectly out of the nymph's mouthparts, and replaced it on the pile. Certaineggs received all or nearly all of the female's attention for extensive periods, andone egg-sized pebble was mouthed and kept on the pile for a time. The eggs ofthis cricket are shorter and more bluntly rounded at their tips than those of relatedfield crickets which inject their eggs into the soil (fig. 5).If the burrow entrance was opened or disturbed, the female immediately ranNo. 1 SUB-SOCIAL BEHAVIOR IN A CRICKET 21to it, shook her body in the manner characteristic of aggression in many kinds ofcrickets, and began to close it again by removing pieces of substrate from thetunnel wall and plastering them near the entrance with her head and forelegs.Other disturbances, such as jarring of the cage or increases in light intensity,always caused a reaction—either a slight rearing-up indicative of aggressiveresponse in a cricket (Alexander, 1961) and slight movement toward the disturbance(fig. 5), or else a change from immobility to exploratory movement or manipulatingof the eggs. If disturbed slightly when not directly over the eggs, the femaleimmediately moved to them, often beginning to palpate or mouth the eggs andmove the pile. Only the most violent substrate vibration caused her to retreatinto the interior portions of the burrow.The female showed little reaction to the young nymphs, which were gregariousand remained near the female, usually clustered on the roof of the chamber touchingher antennae or moving about her body and under it (fig. 1). When she moved,the nymphs followed. Two portions of her body seemed especially attractive:the mouthparts and the tip of her abdomen. Nymphs sometimes stood withtheir mouthparts in contact with the female's mouthparts for several seconds,and one nymph stood for about a minute on its hind legs, propped against thefemale's hind leg, with its antennae apparently against the female's miniatureexternal ovipositor. When a nymph touched the female or walked across herbody, she either gave no reaction or moved only slightly; once she pushed a nymphoff her back with a grooming movement of the hind leg. When she contacted anymph with her mouthparts, she either palpated it or actually picked it up andvery briefly manipulated it in her mouthparts in a manner resembling the mouthingof eggs. When a similar-sized Gryllus nymph was forced into her burrow, shesimilarly picked it up briefly and dropped it unhurt from the mouthparts, thenshowed no further reaction. On the five occasions that a miniature "trophic"egg was laid while we were watching, it was seized by one or more nymphs andeither eaten on the spot or carried off. The nymphs quickly gathered around theseeggs and violently competed for their possession. This competition for individualfood particles, as well as transport of food particles, and burrow excavation similarto that of the adults by removal and transport of individual substrate particles,are actions that in very young juveniles are unique to Anurogryllus; they appearin the other crickets that we have studied only during the late juvenile and adultstages. The only reaction of nymphs to normal eggs was an occasional examinationwith the mouthparts, especially with the palpi. Grass, rotten peach, and applewere also eaten by the nymphs, but without the avidity with which they consumedthe miniature eggs. The small number of normal eggs laid by this female (20 to 25compared to 100 to 300 in other crickets) may be related to her single mating;both characteristics, as well as the trophic eggs, are probably advantageous becauseof their association with transfer of the female's energy into a prolonged behavioralmaximizing of the chances of success of individual hatchlings, through both feedingand protection.Defecating behavior was remarkably consistent in the female. She backedinto the lower corner of her chamber, deposited a pellet, and resumed her positionnear the eggs. Five or ten minutes later she returned to the spot, picked up thefecal pellet, and carried it out of the chamber through one of the two exit tunnels.This happened six times during our observations. The defecation corner wasoriginally a short, downward-sloping tunnel. Later it was filled with a dark,streaked material, apparently defecatory products (fig. 1), suggesting that fecalpellets deposited before the tunnel was filled were not removed. After the tunnelwas filled, one or more pieces of substrate were often removed after removal of thefecal pellet itself. No other materials were ever carried out of the chamber, andonly food was carried into it.This female displayed the usual reactions of Anurogryllus males, females, andjuveniles to different food materials (Alexander, 1961). She burrowed up under22 MARY JANE WEST AND RICHARD D. ALEXANDER Vol. 63pieces of apple and peach (fig. 1), and removed and transported bits of them intothe chamber. She pulled and cut into short lengths long stems of grass insertedinto her burrow (fig. 4). All of these materials were then piled, usually on top ofthe eggs, but occasionally beside them (fig. 1). Within 24 hours she had alwayspiled food and eggs separately. Occasionally, the female alternated in successionthe acts of placing an egg to one side and a bit of food to the other.The female died August 1. Her offspring remained in the chamber until shewas dead, and the corpse and the juveniles both disappeared into the inner portionsof the burrow during the first night. The corpse was probably dragged away byother crickets with burrows in the cage, but under usual circumstances there islittle doubt that the female's own offspring would consume it, the female thusproviding food for her offspring not only by what she had accumulated in theburrow prior to death, but also by the presence of her own body decaying there.Some of the actions described above are known in remarkably parallel form inother sub-social insects. Interaction with eggs, for example, is almost identicalin earwigs and crickets; Weyrauch (1929) found that a female earwig acceptedproper-sized paraffin eggs but rejected pricked, rough eggs, and that eggs deprivedof parental care became moldy and discolored and did not hatch. Many arthro-pods show specialized defecatory behavior, for example, the moth ear mite, Myr-monyssus phalaenodectes Treat, in which the actions are very similar to those inAnurogryllus (Treat, 1958). Trophic eggs are well-known in ants; some queensfeed them to their first offspring, and first instar larvae are sometimes fed exclusivelyon worker-laid eggs (Brian, 1953; E. O. Wilson, personal communication). Buttrophic eggs have not been previously described in a sub-social insect.As suggested by Alexander (1961), many characteristics of burrowing cricketsseem pre-adaptive for the development of social interactions. Thus, crevice-inhabitation and territoriality, exhibited to one degree or another by nearly allsurface-dwelling crickets, concentrate activity in specific locations; without thisprerequisite, burrow elaboration, which may require days of excavation in onelocation, could not proceed. Elaboration of the burrow and of burrowing actionsin turn require increasing manipulative ability and increasingly refined sensorydiscrimination, especially with regard to size, shape, and nature of substratematerials. The manipulative actions that a female cricket uses in handling hereggs, food, nymphs, and fecal pellets all appear to be identical to elements ofburrowing actions existing in related, non-social crickets which do not transportfood or fecal pellets; and they may all have been derived from burrowing actions.If so, the burrow not only provides a suitable location for eventual ensconcementwith eggs and juveniles and their protection from some kinds of potential predators,but its evolutionary elaboration also incidentally develops capabilities prerequisitefor sub-social interactions. In addition, cutting, transport, and piling of variousfood materials is accomplished by manipulative movements which appear to derivefrom burrowing actions, and discrimination among different substrates, reflectedEXPLANATION OF FIGURES II-VIFIGURES 2-6 (top to bottom). FIGURE 2. Female ousting an intruding male from her bur-row by kicking him after tearing off his right hind leg with her mandibles. Note the male'slop-sided position, and the retracted labrum and spread mandibles of the female. FIGURE 3.Female eating the male's leg after tearing it off while ousting him. She has closed up the holeby which he left the burrow. FIGURE 4. Female cutting grass stem with her mandibles afterpulling it into her burrow. Note position of the antennae. FIGURE 5. Female responding tobright light by rearing up, approaching the glass side of the brood chamber, pressing againstit, and touching it with her forelegs and maxillary palpi. Temperature change may be involved.Note egg pile between her front legs. FIGURE 6. Juvenile crickets (probably second and thirdinstars) disturbed by breaking burrow above them. This is about the age at which the femaledies and the juveniles begin to fend for themselves. These juveniles are more plump and soft-bodied than those of most other crickets. This picture is more highly magnified than figures2-5. Drawings were prepared by Miss Suzanne Runyan, museum artist.No. 1 SUB-SOCIAL BEHAVIOR IN A CRICKETFigures 2 to 62324 MARY JANE WEST AND RICHARD A. ALEXANDER Vol. 63in different kinds of burrowing actions (Alexander, 1961), may be related toeventual discrimination between substrate and food. In this connection, deep-burrowing, sub-social crickets (Gryllotalpinae, Brachytrupinae) apparently differfrom all other crickets in that they require moist food for survival, and cannotexist on dry food and a separate water supply. This feeding restriction may berelated to the fact that sub-social females do not eat the eggs during incubation,for non-social crickets are essentially omnivorous and characteristically dig upand eat their own eggs with great relish if exposed for long periods to the ovipositionsite.Finailv, the hvper-aggressiveness which in non-social, burrowing crickets isassociated with the burrow only in the male, ana is tunctionai cnieny m insuringthat he can retain his stationary and secure signalling location, must have evolu-tionary significance with regard to the hyper-aggressiveness and invincibility oftrie sub-social female in the burrow with her eggs and offspring.All of the characteristics described above as pre-adaptive for social existencein crickets appear first in surface-dwelling, non-social crickets (Nemobius, Acheta,Gryllodes) and are increasingly evident as one compares genera that are increasinglysubterranean {Miogryllus, Gryllus, Scapsipedus) and approach in one way or anotherthe elaborate expression of sub-social behavior described here for Anurogryllus(Alexander, 1961).SUMMARYFemales of the short-tailed cricket, Anurogryllus muticus (De Geer), ensconcethemselves in burrows after mating and remain there until death, which usuallyoccurs when the juveniles have reached about the third instar. Approximately25 normal eggs are deposited in an enlarged chamber, and the female repeatedly"mouths" them and keeps them piled together. One female observed for severalweeks ousted an intruding male, piled various kinds of food separately from theeggs, defecated in a special lower tunnel, and eventually began to lay miniatureeggs. The juveniles competed violently for these eggs and eventually ate all ofthem. It is suggested that the small eggs were unfertilized, and that they representa specialization similar to the so-called "trophic" eggs of ants. Various feeding,burrowing, and aggressive actions of surface and subterranean crickets are inter-preted as pre-adaptive for the appearance of sub-social behavior.LITERATURE CITEDAlexander, R. D. 1961. Aggressiveness, territoriality, and sexual behavior in field crickets(Orthoptera: Gryllidae). Behaviour 17: 130-223.Brian, M. V. 1953. Oviposition by workers of the ant Myrmica. Physiol. Comp. Oecol. 3:26-35.Evans, H. E. 1958. The evolution of social life in wasps. Proc. Tenth Internatl. CongrEntomol. 2: 449-457.Ftxlton, B. B. 1924. Some habits of earwigs. Ann. Entomol. Soc. Am. 17: 357-367.Ghosh, C. C. 1912. The big brown cricket (Brachytrupes achatinus, Stoll). Mem. Dept.Agric. India 4: 161-182.Hahn, E. 1958. Untersuchungen uber die Lebensweise und Entwicklung der Maulwurfsgrille(Gryllotalpa vulgaris Latr.) in Lande Brandenburg. Beitr. Entomol. 8: 334—365.Hayslip, N. C. 1943. Notes on biological studies of male crickets at Plant City, Florida. FlaEntomol. 26: 33-46.Liebermann, J. 1955. Bioecologia y sistematica del grillo Argentine- de habitos subterraneosAnurogryllus muticus (De Geer) (Orth. Ensifera, Grylloidea, Gryllidae). Publ. Tecnica 12De Natura 1: 147-156.Michener, C. D. 1953. Problems in the development of social behavior and communicationamong insects. Trans. Kans. Acad. Sci. 56: 1-15.. 1958. The evolution of social behavior in bees. Proc. Tenth Internatl. CongressEntomol. 2: 441-447.Treat, A. E. 1958. Social organization in the moth ear mite. Proc. Tenth Internatl. Congress.Entomol. 2: 475-480.Weyrauch, W. K. 1929. Experimentelle analyse der Brutpflege des Ohrwurmes Forficulaauricularia L. Biol. Zentralbl. 49: 543-558.Wheeler, W. M. 1923. The social insects. Harcourt, Brace, and Co., New York. 375 p.

Sub-Social Behavior in a Burrowing Cricket Anurogryllus Muticus (De Geer) Orthoptera: Gryllidae

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Sub-Social Behavior in a Burrowing Cricket Anurogryllus Muticus (De Geer) Orthoptera: Gryllidae

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