N23 2013 Northeastern Naturalist Notes Vol. 20, No. 4 B. Heinrich Coordinated Mass Movements of Blow Fly Larvae (Diptera: Calliphoridae) Bernd Heinrich* Abstract - I watched blow fly (Diptera: Calliphoridae) larvae in western Maine that had consumed six animal carcasses so that I could identify patterns relating to when, how, and why they left the carcasses. The blow fly larvae stayed under the carcasses on hot, dry days, and then left them on rainy nights, traveling in random directions. Following several rainless days, the larvae left the carcasses at dawn on days with heavy dew and proceeded in a single 1–2-cm-wide column directly toward the rising sun. Species composition of one larvae column was nearly all or exclusively Phormia regina. Introduction. Blow flies (Diptera: Calliphoridae) are the main consumers of animal carcasses (Greenberg and Kunich 2002). Phormia regina (Meigen) blow flies are considered common throughout North America (Whitworth 2006) and dominant in the northern portion of the United States during the summer months (Byrd and Allen 2001). Adult flies typically start to arrive at an animal carcass within minutes of the animal’s death and oviposit batches of 150–200 eggs that hatch in less than half a day at temperatures above 30 °C (Byrd and Allen 2001). After the eggs hatch, the larvae molt three times, but before the third molt they leave the carcass to bury themselves in soil to pupate (Cianci and Shelton 1990, Nabity et al. 2006). During spring and summer, they emerge as adults several days later, mate, and then take a protein meal which stimulates oogenesis (Yin et al 1993) before ovipositing and starting the cycle over again. Phormia regina larvae typically inundate a carcass and create a solid maggot mass. The larval mass generates metabolic heat that raises its temperature to 14 °C above ambient (Cianci and Sheldon 1990), and the resulting elevated temperature and temperature regulation (Stone and Gruner 2007) shorten development time (Nabity e t al 2006). Methods. I observed blow fly larvae leaving carcasses under different field conditions near the center of a one-acre clearing in mixed hardwood-conifer woodland near Weld, in western Maine, at an elevation of 425 m. The clearing offered open horizons above the tree-tops around most of the periphery. Six mammal carcasses—two Procyon lotor (L.) (Raccoon), two Erethizon dorsatus (L.) (Porcupine), and two Marmota monax (L.) Woodchuck— weighing 4–10 kg each were deposited in the open clearing on unshaded ground during daylight hours between 29 July and 14 September 2012. Day-time temperatures regularly reached above 32 °C during sunny, dry, and mostly wind-free days in late July and August, but dipped to below freezing at night in September. I cleared the ground of obstructing vegetation taller than several centimeters within a meter around the carcass so that any larvae leaving would be visible. When I collected the carcasses, it appeared that each one had been hit and killed by automotive traffic within about a day, and in spite of the time elapsed since death, I noticed no sign of blowflies in the carcasses when I deposited them at the study site. I prevented access to the carcasses by scavengers by keeping them near to my doorstep where my frequent presence deterred their disturban ce by other animals. Blow flies visited each carcass within minutes of deposition at my study site. One photograph of a 160-cm2 section of porcupine entrails showed 95 blow flies (tentatively identified by T.L.Whitworth [Washington State University, Puyallup, WA] as primarily Phormia regina, Lucilia sericata (Meigen), and Lucilia. illustris (Meigen). Within two days, the carcasses became colonized with a larval mass that I estimated to consist of tens *Department of Biology, University of Vermont, Burlington, VT 05401; bheinric@uvm.edu. Notes of the Northeastern Naturalist, Issue 20/4, 2013 2013 Northeastern Naturalist Notes Vol. 20, No. 4 N24 B. Heinrich of thousands of maggots. The resulting larvae on any one carcass at any one time were of about the same size, and grew as a cohort. Observations. I deposited a Raccoon carcass on the afternoon of 29 July at an air temperature near 32 °C, and a mass of fly larvae had enveloped the carcass by the second day. Only fur and bones remained by the third day, yet the larvae stayed underneath this layer. On the fourth day, after a cooling night with dew on the grass, a stream of tens of thousands of larvae exited from beneath the carcass within 1 h after sunrise, and proceeded in a single 1–2-cm-wide column directly toward the rising sun. When the column reached 1.5 m from the carcass, the head of this mass emigration was still progressing at 5 cm per minute. Stragglers extended to 0.6 m behind the leading head of the progression, but the carcass itself was almost maggot-free within an hour. The above observations prompted the questions of why the larvae had left the carcass, and how the behavior of thousands of individuals had become coo rdinated. Next, I placed an adult Porcupine carcass at the same place and under the same temperature conditions as before. Again, the onslaught of hundreds of blow flies occurred within several minutes, and a larval mass appeared in two days and devoured the visible traces of soft tissues in three days. Only hair, quills, some drying skin and bones were left, and again, the larvae then stayed out of the direct rays of the sun underneath these remains. However, in this case, the larvae left at night, within 1 h after a cloudburst (at 21:00 hours). But, unlike before, this nocturnal larval exodus in the rain was diffuse; thousands of larvae spread out in virtually all directions over an 8 m2 area. Apparently, the sudden moisture had cued and facilitated the mass exodus, but the absence of sun had prevented a unidirectional, en masse movement. Next, I deposited an adult Woodchuck carcass in the clearing. This carcass was also almost immediately visited by hordes of blowflies on the first day, and by the fourth day the soft tissues of the carcass were consumed. Yet the larvae stayed to again leave at night, apparently in response to rain. As with the previous carcass, the larvae leaving the dead Woodchuck also spread out diffusely in all directions. Fifty larvae that I collected after they had left the carcass all pupated within 3 days when placed on loose soil. Therefore, they had not left at that time only because they had depleted the food s ource. The fourth carcass, a second adult Porcupine, was deposited at 18:00 hours on 24 August. After the fourth day without rain, the larvae had consumed all of the visible meat, and were under the hair, bone, and dried skin remains. However, on the following morning as the sun was starting to illuminate the carcass on the dewy grass, masses of larvae gathered at the east end of the carcass at 07:00 hours. In one half hour later, they started streaming in a column directly (within one degree) toward the rising sun, and the carcass was then nearly vacated. At a second Woodchuck carcass, several constantly patrolling fly-hunting Dolichovespula maculata (L.) (White-faced Hornets) forced many flies to disperse from the carcass, and possibly as a result of White-faced Hornet presence, oviposition was extended over several days. This carcass, in contrast to the others, eventually hosted a population of variable-sized fly larvae, and on 30 August, three days after I had deposited the carcass, the larger of these larvae were leaving the carcass steadily throughout the day as individuals. The 23 larvae that left during one half-hour of continuous observation near 15:00 hours all started crawling within 5° of the direction of the sun (then at an angle of about 45° above the horizon and toward the west, i.e., the opposite direction of the larval columns that left at dawn). However, after these exoduses, large numbers of larvae remained, and during continuous observations at the same carcass the next morning from 09:00–10:00 hours, now under an overcast sky, 36 larvae left the carcass, again as individuals. These larvae did not go in any N25 2013 Northeastern Naturalist Notes Vol. 20, No. 4 B. Heinrich apparently specific direction (11 of them left toward the north, 10 to the northwest, 10 to the east, and 2 to the west). On 14 September, I deposited another adult Raccoon when the air temperature was 30 °C (White-faced Hornets were again present, but I tried to minimize their interference by routinely removing them), and a larval mass enveloped the carcass during the next 4 warm sunny days, and cool nights (less than 20 °C). No larvae left the carcass until dawn of the sixth day, after the sun had melted an overnight frost on the grass. Masses of larvae accumulated in the southeast corner of the carcass, and then proceeded in a single 1–2-cm-wide column (Fig. 1) slightly uphill toward the rising sun. At 09:15 hours, the then 1.7-m-long larval column was continuing through grass at a rate of 3 cm/min. As the column continued to advance, individuals left the group and buried themselves in the soil along the trail. At 11:05 hours, when the rising sun had dried the ground surface, only isolated larvae remained at the head of the column, which was 4.5 m from the carcass. Larvae had been burying themselves in the soil since ≈10:00 hours (those I picked from the moving column and set on soil buried themselves in seconds). The direction the larvae travelled in the column was always directly toward the sun, and as a result their track traced a smooth 60° arc over the 3h it was followed (Fig. 2); it moved from 120° from magnetic north at 07:00 hours to 180° at 11:00 hours. The next morning was also warm and sunny, and more larvae left the Raccoon carcass after the dew melted. They proceeded in the same easterly direction as those that left the day before, but these larvae travelled only up to 1.5 m before burying themselves in the soil. The larvae that exited the carcass were ≈7 mm in length; smaller larvae (≈5 mm) remained under the carcass. All but one of the 50 larvae sampled from the mass-exiting column (taken after they had travelled over 3 m) pupated within three days and then eclosed as adults in two weeks. Each of these 49 imagos was identified from specimens as Phormia regina. However, of 50 larvae taken from the cohort that had remained on the carcass after the second mass-exodus, only 5 pupated within three days. Most of the rest of the larvae pupated only weeks later, and small imagos (tentatively identified as L. illustris) eclosed either by 15 October or the following spring. Discussion. The mass exoduses of blow fly larvae from the carcasses were not likely due solely to starvation since these larvae were able to pupate and produce imagos. However, food depletion may have been a contributor for synchronous exodus; in P. regina, food depletion before completion of larval development triggers a premature migration to pupate (Byrd and Allen 2001). In the present study, under dry and hot daylight conditions, the larvae left at night right after rain, or if there was no rain, they departed the carcasses at sunrise when morning dew was still present. Sub-optimal conditions (i.e., dry and hot) apparently prevented the larvae from leaving the carcasses on which they had fed. These considerations suggest that the observed synchronous exoduses resulted when the larvae had run out of food for 1 to several days, were then detained by hot and/or dry conditions, and then left in a synchronous exodus after the ground was moistened by dew or rain. Presumably their behavior to leave in moisture helped to reduce dessication. When the sun was visible above the horizon during a synchronous exodus, all larval columns I observed started out and continued to travel unvaryingly and directly to ward it. The selective advantage for blow fly larvae leaving a carcass en masse in a column in one direction is obscure and needs further study. It is possible that moisture-loss is reduced by travelling in column-formation, because each larva is then adjacent to a moist surface (the body surface of another larva), which should reduce the rate of water loss for each 2013 Northeastern Naturalist Notes Vol. 20, No. 4 N26 B. Heinrich Figure 1. A column of Phormia regina larvae leaving a Raccoon carcass in the direction of the rising sun. The flattened (solely due to the larvae) remains of the carcass from which it came is at left. Figure 2. The white cord traces the path of the larvae seen in Figure 1 from approximately 8:30 am to approximately 11 am. Throughout this time, the larvae continued facing and traveling in the direction of the constantlychanging position of the sun. N27 2013 Northeastern Naturalist Notes Vol. 20, No. 4 B. Heinrich insect. As a consequence of retaining water longer, each larva could travel farther from the carcass before it pupates in the ground. If it is advantageous to gain distance from feeding sites, then travelling on, over, and with each other, may be critical for dispersing on drying or dry ground. I covered some larvae in powder to simulate dry conditions, and the dry larvae appeared to have difficulty moving. To increase their distance from the carcass before pupating, a larva lacking knowledge of conditions elsewhere, needs no specific direction as such, provided they travel away from the carcass. The direction of a departure line from the carcass would be arbitrary, but by orienting to the sun, all larvae would then be guaranteed to travel in a relatively straight line, one always directly away from the carcass. But if so, what could be the ultimate reason for achieving distance from t he carcass? Acknowledgments. I thank Terry L. Whitworth for species identifications, and Glen Mittelhauser for many helpful comments that greatly improved the manuscript . Literature Cited Byrd, J.H., and J.C. Allen. 2001. The development of the Black Blow Fly, Phormia regina (Meigen). Forensic Science International 120:79–88. Cianci, T.J., and J.K. Sheldon. 1990. Endothermic generation by blow-fly larvae Phormia regina developing in pig carcasses. Bulletin of the Society of Vector Ecology 15:33–40. Greenberg, B., and J. Kunich (Eds.). 2002. Entomology and the Law: Flies as Forensic Indicators. Cambridge University Press, Cambridge, UK. 306 pp. Nabity, P.D., L.G. Higley, and T.M. Heng-Moss. 2006. Effects of temperature on development of Phormia regina (Diptera: Calliphoridae) and use of developmental data in determining time intervals in forensic entomology. Journal of Medical Entomology 43:1276–1286. Stone, D.H., and S.V. Gruner. 2007. Thermoregulation in larval aggregations of carrion-feeding blow flies (Diptera; Calliphoridae). Journal of Medical Entomology 44 :516–523. Whitworth, T. 2006. Keys to the genera and species of blow flies (Diptera: Calliphora) of America North of Mexico. Proceedings of the Entomological Society of Washington 108:689–725. Yin, C.M., H. Duan, and J.G. Stoffolano, Jr. 1993. Hormonal stimulation of the brain for the control of oogenesis in Phormia regina (Meigen). Journal of Insect Physiology 39:165–171.