3068 INTRODUCTION Each year, billions of birds fly in autumn from their breeding grounds in Eurasia to wintering grounds in Africa and return in spring, often covering many thousands of kilometers (Moreau, 1972; Biebach et al., 2000). In small passerine birds, fuel for migratory flight consists mainly of fat (between 85 and 95%) and to a lesser extent of protein (5–15%) (Klaassen and Biebach, 1994; Klaassen et al., 2000). Fuel used during flight is amassed before migration and restored while birds sojourn at stopover sites. During migration, most of these normally diurnal birds change their activity rhythm and fly at night (Berthold, 1996). If a bird’s fuel reserves are adequate, it takes off at dusk and flies non-stop, often for several hundred kilometers at a stretch (Biebach et al., 1986; Biebach et al., 2000). However, this daily rhythm changes when fuel stores run low, and the bird lands to refuel. At stopovers, birds return to diurnality (Berthold, 1996), and may maintain this activity rhythm for several days, until restored energy reserves are sufficient to resume flight (Biebach et al., 1986). Such changes in activity rhythms may occur several times during the migratory journey and are quantitatively related to a bird’s fuel reserves (Biebach, 1996). During migration, songbirds apparently expend more than twice as much energy at stopovers as in flight because the total time spent at stopovers exceeds the time spent in flight by as much as sevenfold (Hedenström and Alerstam, 1997; Wikelski et al., 2003; Bowlin et al., 2005). It is unlikely that birds can directly reduce the energy spent in flapping flight, although they can save energy by choosing when and where in the air-column to fly (Carmi et al., 1992). Theoretically, however, there are ways in which a bird might directly reduce energy expenditure during stopover, either while resting or while feeding to refuel. Studies on the rates of fat accumulation in birds, both before and during migration, have addressed potentially important means of saving energy, including changes in feeding behavior (e.g. Gwinner et al., 1985), food choice and digestive physiology (for reviews, see Bairlein, 2002; McWilliams et al., 2004), endocrine regulation of fattening (Wingfield et al., 1990), and energy balance during the fattening process (Klaassen and Biebach, 1994). However, whether migrating birds are able to reduce energy costs while refueling at stopovers, by becoming hypothermic or even entering torpor at rest, has not been explored other than in hummingbirds (Carpenter and Hixon, 1988; Hiebert, 1993). Facultative reductions in body temperature (T b ) do, however, seem to be common in birds (McKechnie and Lovegrove, 2002). Passerine birds typically maintain T b between 39°C and 44°C, which, in terms of metabolic energy, is expensive (Prinzinger et al., 1991). However, T b normally fluctuates through the day and usually decreases by 1–3°C during normothermic rest, with a concomitant saving of energy through decreased metabolic rate (MR) (Prinzinger et al., 1991; Dawson and Whittow, 2000). However, when faced with unfavorable environmental conditions, many birds may decrease their rest-phase T b significantly below normothermic values. This state, depending on its depth, is called rest-phase hypothermia (T b lowered by 3–10°C) or torpor (T b lowered by The Journal of Experimental Biology 212, 3068-3075 Published by The Company of Biologists 2009 doi:10.1242/jeb.033001 Heterothermy in small, migrating passerine birds during stopover: use of hypothermia at rest accelerates fuel accumulation Michal S. Wojciechowski 1, * and Berry Pinshow 2 1 Department of Animal Physiology, Institute of General and Molecular Biology, Nicolaus Copernicus University, PL 87-100 Torun, Poland and 2 Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Desert, 84990 Midreshet Ben-Gurion, Israel *Author for correspondence (mwojc@umk.pl) Accepted 11 July 2009 SUMMARY For small endothermic animals, heterothermy serves as an energy-saving mechanism for survival in challenging environments, but it may also accelerate fat accumulation in individuals preparing for fuel-demanding activities. This is the first study to demonstrate adaptive hypothermic responses in migrating passerines. While monitoring body temperature (T b ) of eight blackcaps (Sylvia atricapilla) by radiotelemetry, we found that during daytime T b =42.5±0.4°C (mean ± s.d.); at night T b decreased to a minimum between 33 and 40°C. We determined the lower limit for normothermy at 37.4°C and found that on 12 out of 34 bird- nights of observations under semi-natural conditions blackcaps reduced their T b below normothermic resting levels with minimum values of 33 and 34.5°C compared with rest-phase normothermic T b of 38.8±0.8°C. In birds of body mass (m b ) <16.3 g, minimum T b at night correlated with the individualʼs m b (r=0.67, P<0.01, N=17), but this was not the case in birds with m b >16.3 g. Minimum nocturnal T b did not correlate with night-time air temperature (T a ). Measurements of metabolic rate in birds subjected to a T a of 15°C showed that hypothermia of this magnitude can lead to a reduction of some 30% in energy expenditure compared with birds remaining normothermic. Our data suggest that by reducing the T b –T a gradient, blackcaps accelerate their rate of fuel accumulation at a stopover. When body energy reserves are low blackcaps may achieve this reduction by entering hypothermia. Since hypothermia, as seen in blackcaps, may lead to significant energy savings and facilitate body mass gain, we predict that it is common among small migrating passerines. Key words: heterothermy, hypothermia, passerine bird, migration, stopover, Sylvia atricapilla. THE฀JOURNAL฀OF฀EXPERIMENTAL฀BIOLOGY