Metabolic Response to Temperature Variation in the Great Tit: An

Journal of Animal Blackwell Publishing, Ltd. Ecology 2004 Metabolic response to temperature variation in 73, 967–972 the great tit: an interpopulation comparison JULI BROGGI*, MARKKU ORELL*, ESA HOHTOLA* and JAN–ÅKE NILSSON† *Department of Biology, University of Oulu, PO Box 3000, FIN-90014 Oulu, Finland; and †Department of Ecology, Animal Ecology, University of Lund, S-22362 Lund, Sweden Summary 1. We studied the resting metabolic rate (MR) from two great tit Parus major (Linnaeus) populations living in different winter regimes. Birds from the two different localities were exposed individually to +25 °C, 0 °C and −10 °C for the night in three consecutive sessions in random order. 2. Birds from Lund (Sweden) had a lower basal MR, as measured at thermoneutrality (+25 °C), than had birds from Oulu (Finland). Nevertheless, below thermoneutrality, birds from Oulu spent relatively more energy, especially at −10 °C. 3. Although the energy needed for thermoregulation decreased with increasing basal MR this relation is at a higher metabolic cost for birds in Oulu than for birds in Lund. 4. The higher basal MR in Oulu is probably a consequence of a higher maximal MR needed in the severe cold. Further, the observed MRs below thermoneutrality are lower than expected from published data. This suggests that all birds were probably hypothermic at −10 °C, particularly Lund birds, and that the use of controlled hypothermia in great tits may be more common than thought previously. Great tits seem to rely primarily on metabolic adjustment to cope with the harsh climatic conditions in the northernmost parts of its distribution. Key-words: cold acclimatization; energy management; hypothermia; resting metabolic rate; winter energetics. Journal of Animal Ecology (2004) 73, 967–972 have a capacity for increased body reserves and Introduction digestive efficiency (Rogers, Nolan & Ketterson 1993; Small birds that are resident in the temperate zone or at Geluso & Hayes 1999). Arctic latitudes are faced with strong seasonal changes Plumage insulation also changes seasonally by the in cold exposure and thermostatic costs. At the time development of new feathers during moult, and the when energetic requirements increase, available food quality and density of feathers may increase as a result decreases together with time available to acquire it. of the acclimatization processes (Middleton 1986; Root, Such factors combine to make winter an energetically O’Connor & Dawson 1991; Swanson 1991; Novoa, stressful period for resident small birds. Bozinovic & Rosenmann 1994; Cooper 2002). Further- Several adaptations help these birds to survive the more, insulation can be modulated to some extent with non-breeding season. By a process of winter acclima- changing conditions, either decreasing as a result of tization, which is primarily a metabolic improvement feather deterioration (Root et al. 1991) or increasing by in thermogenic capacity and endurance, resident birds means of plumage ptiloerection (Hohtola, Rintamäki have an enhanced cold resistance in winter compared & Hissa 1980). to that in summer (Swanson 2003). Furthermore, as In addition, birds may develop several energy-saving energy demands increase dramatically, birds typically strategies such as nocturnal hypothermia (Reinertsen 1983). Correspondence: Juli Broggi, Department of Biology, Uni- Several studies have shown a proximate role of win- versity of Oulu, PO Box 3000, FIN-90014 Oulu, Finland. ter temperature in regulating metabolism (see Swanson © 2004 British Tel: +358 85531267; Fax: +358 85531227; 2003 for review). In free-living as well as in laboratory- Ecological Society E-mail: Juli.Broggi@oulu.fi acclimated small birds, mass-specific basal metabolic 968 rate (MR) is normally higher in winter than in summer that lasted until the end of March (median 17 March). Juli Broggi et al. (Swanson 1990; Cooper & Swanson 1994; Saarela, During that period permanent snow covered the Klapper & Heldmaier 1995; Liknes & Swanson 1996; study area and the night-length decreased from 13 : 30 Liknes, Scott & Swanson 2002). Further, widespread to 10 : 40 h. bird populations wintering in temperate climates show Great tits in Lund study area live year-round in a negative relation between basal MR and temperature mixed deciduous forests, fragmented by agricultural (Dawson et al. 1983; Cuthill et al. 2000). However, the landscapes and do not rely on feeders for survival. In precise nature of the association between variation in contrast, great tits in northern Finland breed in mixed MR and variation in cold tolerance in birds remains deciduous–coniferous forest, and winter close to human obscure (see Swanson 2003 for review). settlements. During winter, they feed on human-provided Winter ranges of many species are limited by ther- food on which they are probably highly dependent for moregulatory requirements (Root 1988). Further, some their winter survival (Orell 1989). species with wide distribution ranges may experience extremely different winter conditions ranging from mild winters to extremely cold ones (Hoffmann & Blows 1994). In some cases, local adaptations may arise, while Birds in Lund were trapped soon after dusk while phenotypic flexibility usually accounts for most of the roosting in nestboxes, and brought indoors for meas- adjustments to prevailing local conditions (Ricklefs & uring during the whole night. Each bird was measured Wikelski 2002). on 3 consecutive nights and kept alone in outdoor avi- The great tit Parus major (Linnaeus) is a newcomer aries between measurement nights. The outdoor aviar- in northern Europe, and evidence from the breeding ies consisted of 12·8 m2 surface and 2·2 m high cages period suggests that it may be maladapted to the boreal with several nestboxes available for roosting, and food regions (Rytkönen & Orell 2001). This situation may be was a mixture of peanuts, sunflower seeds and animal maintained by gene flow from southern populations fat provided ad libitum. At the start of the different tem- which would prevent local adaptations to conditions perature treatments (see below), mass of individual at northern latitudes (Kvist et al. 1999). Whether this birds did not differ (repeated measures , F2,54 = argument applies to winter survival strategies awaits 0·07; P = 0·9) further research. If seasonal changes in temperature or Birds in Oulu were captured by means of funnel daylength are a major factor driving seasonal adjust- traps that were installed permanently in the study area ments of physiology, then species wintering in cold cli- and worked as feeders except when trapping (see Car- mates should have an increased seasonal physiological rascal et al. 1998 for the same procedure). Birds were adjustment with respect to their counterparts from caught shortly before dusk and kept in outdoor aviaries milder climates. between measurements as in Lund. All birds where We studied resting MR during the non-breeding sea- released after the experiments. son in great tits from two locations differing in winter conditions. By comparing populations living in different regimes of winter-severity, we aimed to elucidate which metabolic adaptations could explain differences Resting MR was measured as the average minimal oxy- in cold acclimatization. We expect birds from the north- gen consumption under post-absorptive digestive con- ernmost location to exhibit overall higher metabolic ditions during the resting phase of the daily cycle on capacity to deal with harsher conditions, and to show resting, non-growing, non-reproductive animals. Basal some adjustment in order to make this strategy less MR was considered to be the resting MR at thermon- expensive in energetic terms. eutrality (25 °C) (McNab 1997). The energetic cost of thermoregulation (ECT) was measured as the differ- ence between resting MR and basal MR and represents Materials and methods the additional MR necessary for thermoregulation. We studied wild individual great tits during the non- Resting MR was measured in terms of oxygen con- breeding season from January until March 2001. Birds sumption during the night in open-circuit respirome- were captured in two different locations in Lund (Swe- ters in both locations. Each bird was placed after dusk den) and Oulu (Finland) and their MR measured dur- in an individual sealed metabolic chamber (1·6 L) and ing 3 consecutive nights at three different temperatures. placed in the darkness of a climate cabinet at three In Lund study area (55°40′ N, 13°25′ E), winter daily different temperatures (25 °C, 0 °C and −10 °C) on 3 average temperatures ranged from −3 °C to 7 °C during consecutive nights. Some of the birds escaped from the the study period that lasted from the end of January to aviaries during the measuring period, which explains mid-March (median 23 February). During that period, the varying sample sizes in different treatments. © 2004 British night-length decreased from 15 : 30 to 12 : 10 h and The respirometer in Lund consisted of a four-channel Ecological Society, −1 Journal of Animal snow was present for about 2 weeks. In the Oulu study set with a flow of 200 mL min , and is described in Ecology, 73, area (65° N, 25°30′ E) winter daily average temperatures Lindström, Klassen & Kvist (1999) and Nilsson & Råberg 967–972 ranged from −14 °C to 0 °C during the study period (2001). The Oulu respirometer consisted of a two-channel 969 set and one oxygen analyser Servomex 1440 (UK) MR as the dependent variable, neither sex, age, date of Metabolic response that received air samples of 600 mL min−1 through a capture nor ambient mean temperature the day before to temperature valve system. Dried outdoor air was pumped to both measurement explained any significant proportion of variation metabolic chambers through mass-flow controllers the variation in basal MR. The only significant factors (Bronkhorst Hi-Tec F201C, the Netherlands) and then left in the model was area (t = 4·34; N = 39; P < 0·001) dried again before analysis. The valve system switched and mass (t = 2·90; N = 39; P = 0·006), which together in periods of 30 min between channels and outdoor explained 37·7% of the variation in basal MR.

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