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How and Why Do Insects Migrate? Richard A How and Why Do Insects Migrate? Richard A. Holland, et al. Science 313, 794 (2006); DOI: 10.1126/science.1127272 The following resources related to this article are available online at www.sciencemag.org (this information is current as of March 6, 2007 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/cgi/content/full/313/5788/794 This article cites 13 articles, 6 of which can be accessed for free: http://www.sciencemag.org/cgi/content/full/313/5788/794#otherarticles This article has been cited by 1 article(s) on the ISI Web of Science. This article appears in the following subject collections: Ecology http://www.sciencemag.org/cgi/collection/ecology on March 6, 2007 Information about obtaining reprints of this article or about obtaining permission to reproduce this article in whole or in part can be found at: http://www.sciencemag.org/about/permissions.dtl www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright c 2006 by the American Association for the Advancement of Science; all rights reserved. The title SCIENCE is a registered trademark of AAAS. MIGRATION AND DISPERSAL 35. K. Bo¨hning-Gaese, L. I. Gonzales-Guzman, J. H. Brown, 38. H. Mouritsen, T. Ritz, Curr. Opin. Neurobiol. 15, 406 (2005). tion literature. Valuable suggestions were provided by two Evol. Ecol. 12, 767 (1998). 39.IamverygratefultoJ.Ba¨ckman for advice and help with anonymous referees. This work was supported by the 36. S. Johnsen, K. J. Lohmann, Nat. Rev. Neurosci. 6, 703 (2005). figures, T. Fransson for providing Fig. 1 basis, J. Metcalfe for Swedish Research Council. 37. W. Wiltschko, R. Wilschko, J. Comp. Physiol. A 191, 675 information, and the Royal Institute of Navigation and (2005). D. Grocott for extensive information about animal naviga- 10.1126/science.1129048 describe insect movements; instead, all long-range PERSPECTIVE movements of insects would be considered ‘‘migrations’’ (1, 7, 10, 11). How and Why Do Insects Migrate? Migration by vertebrates is often viewed as a mechanism for exploiting high-quality resources Richard A. Holland,1,3 Martin Wikelski,1* David S. Wilcove1,2 that are available during only a portion of the year [typically the breeding season (7, 10)]. In the case Countless numbers of insects migrate within and between continents every year, and yet we know very of insect migrations, which we define here as little about the ultimate reasons and proximate mechanisms that would explain these mass repeated phenomena of directional movement that movements. Here we suggest that perhaps the most important reason for insects to migrate is to are cyclical in nature, the ultimate reasons are less hedge their reproductive bets. By spreading their breeding efforts in space and time, insects clear. If insects are not able to return to a high- distribute their offspring over a range of environmental conditions. We show how the study of quality patch in a subsequent year, then why individual long-distance movements of insects may contribute to a better understanding of migrate at all? Although considerable progress migration. In the future, advances in tracking methods may enable the global surveillance of large has been made toward understanding patterns of insects such as desert locusts. insect migration (1, 11), especially with respect to certain moths (12), the ultimate selection pressures arge-scale movements of insects have round-trip journey that returns them to the area resulting in these spectacular and ubiquitous move- enormous implications for human welfare from which they departed. Even in the case of the ments remain mysterious. Intuitively, one expects L(1), including catastrophic losses of crops monarch butterfly (Danaus plexippus)(Fig.1A), migratory movements to evolve only when the on March 6, 2007 (2), the spread of diseases to people and livestock one of the best-studied migratory insects, few if any fitness benefits exceed those of remaining in the (3), and the provisioning of essential ecosystem of the individuals wintering in Mexico return to current habitat (13). Whether this reasoning applies services such as crop pollination (4). In sheer num- their natal areas. Instead, monarchs repopulate in the case of insect migrations is unclear. Because bers of individuals, insect migration far outweighs northern latitudes through a process of intergenera- insects do not have to provide long-term care for other migratory phenomena (5). Moreover, in terms tional migration, whereby successive broods ad- their offspring, they can in theory reproduce in of total moving biomass, the migrations of indi- vance northward (8, 9). Thus, return migration, the their natal area, along a migratory route, or in a vidual insect species rival and sometimes outstrip most common type of migration in birds and mam- discrete ‘‘winter range.’’ This differentiates them the largest extant herds and flocks of some well- mals (7), has yet to be documented in insects. from the classic vertebrate return-migration model. known migratory mammals and birds (Table 1). By spreading their breeding efforts both spatially www.sciencemag.org And yet there is at least one fundamental difference Migration Strategies in Insects and temporally, insects have the ability to ‘‘hedge between insect and most vertebrate migrations Researchers accustomed to viewing long-range their bets’’ by distributing their offspring across a (6, 7): As a rule, individual insects do not make a animal movements through the prism of classic range of areas and conditions that may be return (i.e., round-trip) migration would likely amenable for future reproduction (14). 1 2 Department of Ecology and Evolutionary Biology, Woodrow categorize many so-called insect migrations as To determine whether this bet-hedging hy- Wilson School, Princeton University, Princeton NJ 08544, USA. 3Institute for Integrative and Comparative Biology, dispersal events (6). Entomologists, however, pothesis is a valid explanation for most (or any) University of Leeds, Leeds LS2 9JT, UK. would disagree. Indeed, major reviews of this sub- insect migrations, one would need to know the Downloaded from *To whom correspondence should be addressed. E-mail: ject in the entomological literature have recom- reproductive output (and, ideally, success) of [email protected] mended abandonment of the term ‘‘dispersal’’ to individual insects along their migratory route. Do Table 1. Biomass of migrating animals. Class Species Location Size of herd, swarm, or flock Biomass (tons) Source (reference) Insects Darner (dragonfly), Argentina 4–6 billion 4000 (15) Aeshna bonariensis Monarch butterfly, Winter grounds 100–200 million 40–80 (39, 40) Danaus plexippus in Mexico Desert locust, Africa, Middle 109–1011 200,000 (5) Schistocerca gregaria East, Asia Mammals Wildebeest, Serengeti, 1.3 million 280,000 (41) Connochaetes taurinus Kenya and Tanzania, Africa Mexican free-tailed bat, Carlsbad Cavern, 20 million 300 (42) Tadarida brasiliensis mexicana New Mexico, North America Birds Lesser sandhill crane, Platte River, 450,000 1440 (43) Grus c. canadensis Nebraska, North America 794 11 AUGUST 2006 VOL 313 SCIENCE www.sciencemag.org SPECIALSECTION individual insects simply continue to migrate until turally important pests [e.g., desert locust, Schis- sequent years (21). If migratory insects do not they die from exhaustion, or do they terminate their tocerca gregaria (18) (Fig. 1B)] is that insects are make round-trip journeys, then it is unlikely they migration when reaching a suitable habitat? That often facultative migrants that respond to changes develop navigational mechanisms based on expe- is, do they simply move along a habitat cline and in habitat availability, quality, and level of rience (22). Yet, in the case of monarch butterflies, spread out their propagules, or do they search for a crowding (17, 19). A large majority of insects that winter sites are highly localized year after year spatial peak in the reproductive landscape, as most migrate do so pre-reproductively, suggesting that (22), suggesting some tight control of spatial move- long-distance migratory birds do (6)? For exam- such migration is in response to some indication ments across the 3000 km of North American ple, green darner dragonflies (Anax junius) that reproduction will be suboptimal in the natal landmass. To find their wintering sites, an environ- engage in spectacular autumn migrations along area (17). This behavior may represent a multi- mental cue or a genetic vector engrained in an the eastern seaboard of the United States (15). generational bet-hedging strategy that allows the endogenous program similar to that used by juve- Many of the females captured in the fall are offspring to avoid overcrowding or deteriorating nile migrating birds (6) is presumably employed. gravid, yet we do not know whether a given environmental conditions. Spatial heterogeneity of Insects that migrate in the flight boundary layer female is traveling to a particular site or region the habitat—in particular, the existence of good (23), below the prevailing winds, must have a to lay its eggs, or whether it is slowly moving and bad patches—may also select for migratory mechanism to maintain a heading. This has been south and laying a portion of its eggs in suitable behavior as a bet-hedging strategy (14). However, proposed for monarch butterflies, with a 1- per day ponds along the way. There is no shortage of too little is currently known about the strategies of change accounting for the orientation of these questions to challenge (or frustrate) researchers individual insects to generalize about the ultimate animals through the course of a year (9). However, interested in insect migration. factors responsible for the movements of megatons more recent data do not fully support this hypoth- Despite the importance of knowing the be- of insects within and between continents.
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