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 hypo- thermia 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 differ-   ent 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. air. Readings were recorded every minute and later Because the MR of an individual was measured at on, minimum night averages were extracted over 3-h three different temperatures, we analysed the differences periods between 23·00 and 04·00 h for every bird. The between birds from the two areas with a repeated- closest outdoor-air reading was used as reference in measures . Of the predictor variables (area, age, order to control for any possible analyser drift. sex and date), only area explained a significant part of

In Lund CO2 was measured, whereas in Oulu it was the between subjects’ variation (F1,26 = 19·7; P < 0·001).

removed from inlet and outlet air, as CO2 was not Within subjects, MR increased significantly as the night measured. Appropriate equations for each of these con- temperature decreased (F = 171·0; P < 0·001; Fig. 1). ditions were used according to Hill (1972). The interaction between area and night temperature The different modes of capturing the birds did not was not significant (F = 0·97; P = 0·39). The same analysis bias our measurements of MR. In a sample of great but with morning mass as the dependent variable, resulted tits from Lund in 2000, birds captured either at feeders in sex (F = 16·8; P < 0·001) and to some extent area or from nestboxes, did not differ in basal MR (t-test: (F = 3·26; P = 0·084) being able to explain some of the

t27 = 0·15; P = 0·88). variation between subjects. The morning mass also Birds were measured at one constant temperature decreased with decreasing night temperature (F = 4·98; each night and the order of temperature treatments P = 0·011). was randomized, to control for possible treatment or During our measurements of energy consumption captivity effects. at temperatures below thermoneutrality, we assumed All variables full filled the requirements of normality that the total energy budget consists only of basal MR (tested with the Kolmogorov–Smirnov one sample test) and the cost of thermoregulation (ECT, see Methods). and thus parametric statistics were used in all analysis. Thus, to obtain a measure of the metabolic cost of thermoregulation we subtracted basal MR from the total energy expenditure. We found no difference between Results the two areas in this cost of thermoregulation at 0 °C (t-

The mean mass of great tits, as measured at the first test: t27 = 0·38; P = 0·7), nor could sex, age or date explain evening after capture, did not differ between the two any of the variation in a multiple regression (P > 0·5). areas (mean ± SD, Lund: 18·8 g ± 0·74; N = 24, Oulu: However, at −10 °C, birds from Oulu tended to expend 18·5 g ± 1·48; N = 17, t-test: t = 0·87; P = 0·39). The only more energy on thermoregulation than did birds from

factor remaining in a multiple regression with area, sex, Lund (t-test: t30 = 1·82; P = 0·079). Area was the only age, date of capture and ambient mean temperature on factor remaining in a multiple regression also including the day of capture was sex, males being significantly sex, age and date (sex, age and date; P > 0·4). heavier than females (t = 3·98; P < 0·001). One factor that potentially could affect the metabolic The MR of birds at 25 °C, i.e. basal MR, differed cost of thermoregulation is the level of basal MR. A

between the two areas (t-test: t37 = 3·34; P = 0·002), multiple regression with date, area, sex, age and basal Oulu birds having a higher basal MR than birds from MR still did not explain any of the variation in the Lund (Fig. 1). In a multiple regression with basal cost of thermoregulation at 0 °C (N = 29; P > 0·3 in all cases). However, at −10 °C, both area (F = 11·5; N = 32; P = 0·002) and basal MR (F = 10·1; N = 32; P = 0·004) explained a significant part (33·2%) of the variation in the metabolic cost of thermoregulation (the interaction between area and basal MR being non-significant; P = 0·55). Thus, the cost of thermoregulation decreased with increasing basal MR in both areas (Fig. 2), but this relation is at a higher overall metabolic cost of thermoregulation in the birds from Oulu compared to birds from Lund (Fig. 2).

© 2004 British Discussion −1 Ecological Society, Fig. 1. Mean (+ SE) metabolic rate (ml O2 min ) of great tits Journal of Animal spending the night in 25 °C (thermoneutrality), 0 °C and Birds in Oulu had a higher basal MR but additionally Ecology, 73, −10 °C. Black bars represent birds from Lund and open bars an overall higher MR at all temperatures. Birds in the 967–972 birds from Oulu. northernmost population have to deal with harsher 970 plumage quality at the peak of the winter. On the other Juli Broggi et al. hand, considerable differences should be invoked in order to explain the variation found. Furthermore, if insulation differences are to be expected they would rather be in the other direction, as shown in other studies with winter-acclimatized birds (Middleton 1986; Root et al. 1991; Swanson 1993; Novoa et al. 1994; Cooper 2002). As no body temperature measurements were obtained conclusions on the degree of hypothermia can be drawn, always with caution, only after certain assumptions are made. Considering that measurements were made Fig. 2. Relation between the metabolic cost of thermoregula- −1 − ° far below the thermoneutral zone, a constant insula- tion (ml O2 min ) at 10 C and the basal metabolic rate (ml O2 min−1) as measured at 25 °C. Filled circles and bold line tion value that would be maximal before starting ther- represent birds from Lund and open circles and broken line mogenesis could be assumed. In such conditions, the birds from Oulu. The relation was tested separately for Lund expected MR would be much higher than the ones we and Oulu with regression analyses, Lund: t = −3·62; N = 16; obtained, as calculated from allometric equations and P = 0·003; equation of the line: y = 2·18 − 1·44x; R2 = 0·48, Oulu: t = −2·03; N = 16; P = 0·062; equation of the line: previous data on the same species (Hissa & Palokangas y = 1·97 − 0·90x; R2 = 0·29. 1970; Peters 1983). Thus, both populations were prob- ably hypothermic at −10 °C, birds from Lund probably being in deeper controlled hypothermia than their coun- conditions (lower temperatures and shorter day lengths) terparts from Oulu, as this temperature is close to the and higher weather unpredictability, and they presum- minimum ambient temperature they may encounter. ably do this by increasing their thermogenic capacity Controlled hypothermia appears to be a last resort and endurance. Such an increase in energy expenditure to endure cold temperatures for many passerines and is probably achieved by increasing energy acquisition probably is connected to important costs (Reinertsen and digestive efficiency, i.e. increased size of the diges- 1983; Grubb. & Pravosudov 1994). As the capacity for tive tract (Piersma & Lindström 1997), in order to sup- thermogenesis also has costs, e.g. an increased basal port increases in maximal MR, which would in turn MR, a trade-off between this capacity and the use of elevate their basal MR (see Swanson 2003 for review). hypothermia may be anticipated. The optimal com- The decrease in the energetic cost of thermoregulation bination of the two strategies may depend on average (ECT) with increasing basal MR probably depends in environmental conditions resulting in using controlled part on the usage of heat, generated by the metabolism, hypothermia at the lower end of the local temperature for thermoregulation and in part because basal MR variation. This lower end of the temperature variation increases faster than energy available for work with an would be approximately −10 °C in Lund (altogether, 2 increase in total MR (Nilsson 2002). nights had this or a lower minimum temperature during The increased costs of thermoregulation in the the winter of 2001) but at much colder temperatures in northernmost population raise an interesting question. Oulu (62 nights with minimum temperatures at −10 °C We expected birds in Oulu to show a decreased ECT or below). Furthermore, a higher basal MR that would in order to cope with harsher conditions without allow a high maximal MR may reduce the options for incurring exceptionally high energetic costs. How- a decrease in body temperature. Given the small bird’s ever, in contrast to our expectations, ECT was higher high capacity for regulatory thermogenesis in general, at lower temperatures in birds from the northernmost the need for a higher basal MR appears unnecessary population. (Dawson & O’Connor 1996). It is unclear whether the Heat loss can be expressed in terms of insulation and higher resting MR is a contributing factor to these body-environment thermal gradient, both governing improvements in cold tolerance, a by-product of them the heat loss from the body below the lower critical or a separate response. temperature. Thus, the fact that birds from the south- In general, differences between the studied popula- ernmost population had a lower ECT can ultimately be tions appear to be based on metabolic adjustments, explained in two ways. At a constant ambient temper- which could be interpreted as a first step in the accli- ature, variation in ECT could either be due to differ- matization process to a new environment (Dawson ences in insulation, in body temperature, or both. Thus, et al. 1983; Swanson 1993; Ricklefs & Wikelski 2002). birds from Lund had either a higher insulation capacity Further, birds from both populations appear reluctant or a smaller temperature gradient between their body to become hypothermic, even more so in the northern- and the ambient air. In the first case, better insulation most population where individuals keep a high MR © 2004 British could be achieved by higher plumage quality per se or whenever possible. Contrary to our expectations, Ecological Society, Journal of Animal by fresher plumage. Birds from southern latitudes birds from the northernmost population used a more Ecology, 73, could afford delaying post-nuptial moult, and may also energetically expensive strategy than their southern 967–972 enjoy better foraging conditions resulting in a higher counterparts, which does not seem sustainable as 971 winter food predictability diminishes with increasing Hohtola, E., Rintamäki, H. & Hissa, R. (1980) Shivering Metabolic response latitude. In general, birds from Oulu may experience and ptiloerection as complementary cold defense responses to temperature higher food predictability than birds from Lund, as they in the pigeon during sleep and wakefulness. Journal of Com- parative Physiology, 136, 77–81. variation rely on human-provided food during winter, suggesting Kvist, L., Ruokonen, M., Lumme, J. & Orell, M. 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© 2004 British Ecological Society, Journal of Animal Ecology, 73, 967–972