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CHANGES IN FORAGING BEHAVIOUR OF THE COAL (; ATER DUE TO SNOW COVER

LLUfs BROTONS

Brotons L. 1997. Changes in foraging behaviour of the Parus ater due to snow cover. Ardea 85: 249-257.

This paper studies the foraging behaviour of the Coal Tit Parus ater, a small wintering in mountain coniferous in the Pyrenees. We compared tree site use and the foraging techniques of , (1) under snowy conditions, when snow covered the outer substrates of pines, and (2) under snow-free conditions. Under snowy conditions, birds foraged in the lower and inner parts of trees, using trunks and thick branches as their main foraging substrate. During normal, snow-free conditions, birds used upper and outer parts of trees feeding mainly on pine cones and needles. Move­ ment patterns of individuals differed from one condition to the other. Dur­ ing snow free conditions, birds used more costly energy methods, mainly flight and hanging position, while in snowy conditions they used lower en­ ergy consuming methods, mainly hopping. Our results support Norberg's hypothesis (1977) that when the prospects of obtaining prey increase, for­ aging methods requiring higher energy consumption can be used. Key words: Parus ater - tree snow cover - foraging behaviour - movement patterns - energetic costs Dept. Biology (Vertebrates), University ofBarcelona, Av. Diagonal 645, 08028 Barcelona, Spain; E-mail: [email protected].

INTRODUCTION ergy expenditure (Grubb 1979, Carrascal 1988, Lens 1996, Wachob 1996) and maximize prey in­ Weather conditions are a significant factor in de­ take profitability (Pyke 1984, Stephens & Krebs termining the way in which birds interact with 1986). Although survival may be strongly in­ their environment. It is well known that climate fluenced by changes in behaviour (Jansson et at. and weather play an important role in shaping the 1981, Ekman 1984), the processes and proximate migratory patterns of birds (Baker 1978, Elkins factors associated with weather-induced shifts in 1983) and also influence many aspects of bird be­ foraging behaviour are not completely under­ haviour and ecology, such as foraging or repro­ stood. ductive patterns (Grubb 1979, Spencer 1982, El­ An example of such changes are the short­ kins 1983). lasting modifications which occur as the available In winter, birds living in northern environ­ foraging surface is decreased or altered in some ments or at high altitudes suffer the greatest pres­ way. As snow accumulates on tree surfaces, sures from a harsh climate. Small passer­ snowfalls seem to have a negative impact on bird ines are especially vulnerable to bad weather be­ foraging behaviour, by making the search for prey cause they need to forage almost continuously more difficult (Spencer 1982, Macarrone 1987, during the short winter days in order to meet their Smith 1991). When the available foraging surface minimum energy requirements (Spencer 1982). decreases, birds must adapt foraging techniques Weather conditions have been shown to influence and use of space to the new conditions. Our work­ the foraging behaviour ofcertain forest ing hypothesis, following Norberg (1977), is that in such a way that birds tend to reduce their en- in order to optimise their energy balance, individ- 250 ARDEA 85(2), 1997 uals foraging in surlace-reduced conditions will clearly dominated in numbers by the Coal Tit and, use energetically cheaper searching methods due frequently, this was their only component. to the decreased profitability of prey exploited in Foraging behaviour was monitored between these substrates. Therefore, this study seeks to January and March 1996. During this period, two clarify the effect of tree snow cover on the forag­ conditions were distinguished according to the ing behaviour of the Coal Tit, in a mountain co­ amount of snow accumulated on the trees. During niferous forest. The specific questions raised are: snowy conditions (1), a snow layer ofmore than 5 (1) does the snow accumulated on trees produce a cm covered most outer parts ofpines, whereas un­ shift in tree use, (2) do birds change their prey der snow-free conditions (2) no snow at all was searching techniques after a snowfall and (3) if noticed on tree surfaces and birds could freely so, what are the main characteristics of the choose foraging substrates. Days on which data searching techniques used in differing conditions, were collected were chosen so as to avoid inter­ and can they be related to preference of substrate mediate amounts of snow on trees. Thus situa­ used? tions were clearly differentiated, and assignment of observations to study conditions could be con­ ducted without ambiguity. During data collection STUDY AREAAND METHODS days, we walked systematically throughout the study area searching for tit flocks. When a flock The study area of about 150 ha is located in the was located we used two techniques to describe eastern Pyrenees, in the north-east the of Iberian the birds' foraging behaviour. Tree site and sub­ Peninsula, at an altitude between 1800-2100 m. strate use were described by instantaneous sam­ Mountain Pine Pinus uncinata dominates the pling of the birds' position (Carrascal 1983, Mor­ study area with Scots Pine Pinus sylvestris pre­ rison 1984), whereas searching techniques were dominant on southern slopes and at lower alti­ recorded by the continuous following of focal in­ tudes. Understory is scarce, dominated by Junip­ dividuals (Robinson & Holmes 1982). erus communis and grass. More information Instantaneous sampling describing the posi­ about the vegetation can be found in Vigo (1976). tion of Coal Tits on trees was initiated five sec­ The forest has been exploited until recently on a onds after a bird was located (to avoid the record­ long-term cycle, resulting in tree stands of differ­ ing of conspicuous behaviour). Whenever pos­ ent ages in the area. The annual precipitation is sible, consecutive observations with a 20 s delay approximately 1100 cm, around 35% falling as were taken with no more than four consecutive snow during winter months. Snow remains on the samples per individual to assure statistical inde­ ground from December to April. Usually about pendence (Carrascal 1983). Space use was meas­ five to six times a year, a precipitation of more ured with a range of variables using rank scales than 10 cm of snow occurs, leaving snow on trees (derived from CarrascaI1983), relative height (in for three to four days depending on temperature the tree, 1 to 4, from the bottom to the top), dis­ and wind speed. The winter of 1996 was espe­ tance from the trunk (1 to 4, from the trunk to the cially snowy, with 16 days on which precipitation periphery). Also the substrate (trunk, thick branch of more than 10 cm of snow fell. The Coal Tit is a > 1 cm, twig < 1 cm, needle, cone and others) and small forest passerine (body weight x = 9.22 g, SE the individual activities (foraging, bill pointing = 0.51, n = 255, unpubl. data). In the Pyrenees, downwards; or vigilance, bill pointing above the during winter it lives in flocks ofup to 70 individ­ horizontal) were recorded. uals often with up to three Crested Tits Parus Unfortunately, we obtained an insufficient cristatus, up to three Regulus regulus, amount of data on colour-ringed individuals to and solitary Certhia spp (unpubl. perlorm analysis on an individual basis. However, data). Therefore, in our study area flocks were it is very unlikely that there was a systematic dif- Brotons: FORAGING AND SNOW COVER IN THE COAL TIT 251 ference between the birds sampled under the two arthropods was measured on these substrates. conditions. Some unbanded transient birds may From six trees where Coal Tits had been seen have been sampled twice on different days of the feeding under snowy conditions, we examined 40 study, but never on the same day because we x 40 cm surface of trunk and thick branches at a changed groups after the observation of unbanded height of 1.5 m. Samples were taken by gently birds. In such cases, the time elapsed between ob­ cleaning the bark surface with a brush, and by let­ servations and the movement of individuals sug­ ting the resulting material fall into a plastic bag. gest that possible pseudoreplication of the data Later the samples were examined in the labora­ was not a problem (see also Leger & Didrichsons tory and all arthropods bigger than 1 mm were 1994). Observations were taken between 8.00 counted. Coal Tits foraging on outer canopies fed a.m. and 14.00 p.m. by the same observer so as to mainly on pine seeds in our study area (see 'Re­ avoid possible bias resulting from different inter­ sults'), and secondarily on medium-size arthro­ pretations of each variable and under similar tem­ pods, as confirmed for many other populations of perature and wind speed conditions, since these Coal Tits (Haftom 1956, Gibb 1960, Obeso 1987, factors can influence space use in forest passer­ Suhonen et ai. 1992, Cramp & Perrins 1993). ines (Grubb 1979). In total, 95 observations were Hence no prey samples from the outer parts of taken during three different periods of snow (four trees were collected in this study. sampling days), and 121 observations were taken We used Shannon's diversity index corrected during snow free conditions (nine sampling for sample size (Bowman et ai. 1971) as a meas­ days). ure of niche breadth in the distribution of posi­ Continuous sampling of focal individuals star­ tions and substrate use in trees. Statistical analy­ ted five seconds after the bird was located on the ses were performed according to Sokal & Rohlf tree. We defined a searching movement as any (1981). change in position made by a bird that was searching for prey. Number of hops, short flights « 20 cm), medium distance flights (20 cm - 1 m) RESULTS and long flights (> 1 m) were recorded as search­ ing movements. Also the number of pecks (i.e. Instantaneous sampling of birds showed that head movements directed to capture prey), hov­ when snow covered the outer tree surfaces, indi­ ers, hanging positions, number of times the bird viduals used the lower and inner parts of the trees switched from one tree to another and height of more frequently than when trees were free of visited trees were carefully registered. Each se­ snow (height, X23 = 39.41, P < 0.001; distance quence ended when the bird was lost from sight. from trunk, X23 = 80.92, P < 0.001, Fig. 1). Pine The foraging sequences of the individuals were cones and needles were the most frequently vis­ dictated to a tape recorder and transcribed later. ited substrates during snow free conditions, with Analyses only included those foraging sequences birds using other substrates infrequently, mainly longer than 25 s (x = 61 s, SE = 5.6). We pooled branches, to consume pine seeds taken from co­ sequences of the same individual collected during nes (Fig. 2). In snowy conditions, Coal Tits used a given sampling period, therefore only indepen­ trunk and thick branches as their main foraging dent observations on different individuals, mostly substrates (X25 = 92.75, P < 0.001, Fig. 2). Never­ one sequence per individual, were included in the theless, we did not find significant variation in ni­ analyses. In total, 24 of such sequences were reg­ che breadth between conditions (i.e. diversity of istered under snow-free conditions and 16 under 16 parts of the tree exploited during foraging, Ta­ snowy conditions. ble 1). Niche breadth in substrate use did decrease In order to identify the prey available for Coal in snowy conditions, thus when snow was pre­ Tits on trunks and thick branches, the number of sent, birds concentrated their foraging on fewer 252 ARDEA 85(2),1997

SNOW FREE "snow free 50 "snow

40 ~ rJ) rJ) c 30 Q) 0 rJ) rJ) ~ ctl > {) Q; rJ) .E .Q Cl 0 "Qi ..r::

trunk thick twig needle cone other branch distance from trunk_ substrate e>0.1-4.9% .5.0-9.9% .10.0-14.9% .15-25% _<25% Fig. 2. Substrate use by birds in snow-free and snowy conditions. Fig. 1. Frequency use for each of the 16 foliage re­ gions delineated by relative height and distance from trunk. Horizontal axis represents distance from the ber of hops made per flight undertaken was gre­ trunk (from left to right, on a scale of 1 to 4, trunk to ater under snowy conditions (Table 2). As a re­ periphery), and the vertical axis relative height (in­ sult, birds spend more time moving and moved creasing from bottom to top). over greater distances in snow-free conditions as usually flight takes more time and implies travel­ ling greater distances than when hopping. substrates than they did when trees were free of The number of hanging positions and pine co­ snow (Table 1). nes visited by the birds was higher under snow Continuous focal sampling of individuals free conditions. In addition, the number of pecks showed that the total number of searching move­ increased when birds foraged on snow covered ments did not differ between snowy and snow trees (Table 2). Coal Tits seldom used hovering as free conditions (Table 2). However, the propor­ a searching technique and its frequency ofuse did tion of different movement types differed greatly not differ between conditions. No differences between both conditions. The frequency of short were found in the height of trees exploited by and medium distance flights was greater in birds birds between conditions (t-test = 2.06, df = 36, foraging on snow-free surfaces, whereas the dif­ N.S.). ference in long-flight frequency remained non­ In order to obtain a better interpretation of significant (Table 2). Although the number of movement patterns and foraging data and to show hops did not differ between conditions, the num- potential associations between the variables

Table 1. Substrate use and tree site diversity of foraging niches under snow and snow free conditions. Values are the Shannon diversity index for the distribution. SD are standard deviations.

Snowy Conditions Snow free t-test p df

Diversity SD Diversity SD

Tree site 2.20 0.032 2.17 0.046 0.017 N.S. 162 Substrate 1.14 0.084 1.40 0.033 1.972 <0.05 194 Brotons: FORAGING AND SNOW COVER IN THE COAL TIT 253

Table 2. Movements and activity of Coal Tits recorded under snowy (n = 16) and snow free (n =24) conditions. SE are standard errors. Total number of movements (all types offlights plus hops), number of hops per flight (num­ ber of hops divided by total number of all types of flights). t-test corrected for different variance estimates when necessary. *: P < 0.05, **: P < 0.01, ***: P < 0.001.

Snow free conditions Snowy conditions t-test P

x SE x SE

------Pecks, no. minot 18.12 1.72 27.49 3.50 2.66 ** Short flights, no. minot 7.43 0.88 4.35 0.83 2.38 * Medium flights, no. minot 2.09 0.43 0.44 0.17 2.94 ** Long flights, no. minot 1.22 0.31 0.67 0.23 1.25 N.S. Hops, no. minot 8.33 0.81 11.09 1.49 1.76 N.S. Hovers, no. minot 0.50 0.24 1.13 0.52 1.24 N.S. Hangings, no. minot 3.62 0.52 1.53 0.51 2.72 ** Pine cones, no. minot 3.17 0.54 0.09 0.09 4.46 *** Tree changes, no. minot 1.53 0.31 0.87 0.25 1.52 N.S.

Total no. of movements, no. minot 19.14 1.41 17.1 1.91 0.85 N.S. Number of hops per flight 0.88 0.13 2.59 0.57 3.54 **

Table 3. Factor loadings resulting from PCA analyses of movement patterns of Coal Tits under snowy and snow­ free conditions. Differences between both conditions are shown in the last row. Only coefficients higher than 0.30 are shown in the table.

Variable Factor 1 Factor 2 Factor 3 Factor 4

Pecks, no. minot -0.83 Short flights, no. minot 0.52 0.62 Medium flights, no. minot 0.73 Long flights, no. minot 0.96 Hops, no. min-l -0.87 Hovers, no. minot 0.80 Hangings, no. minot 0.33 -0.79 Pine cones, no. minot 0.33 0.61 0,38 Tree changes, no. minot 0.60 0.59

Variance explained, % 24 20 18 17 t-test of factors between conditions P < 0.01 P< 0.05 N.S. N.S. measured, a principal component analyses (peA, ber of pecks and number of short and medium Battacharyya 1981) was conducted. Out of nine distance flights undertaken by birds, therefore an initial variables, four independent factors were increase in the pecking rate is correlated with a extracted to explain 78 % of the variance con­ decrease in the number of short and medium dis­ tained in the data set (Table 3). The first factor de­ tance flights (i.e. snowy conditions). The second termines a negative association between the num- factor is strongly related to movement techniques 254 ARDEA 85(2), 1997 used by birds, showing a negative association be­ and medium distance flights as their main search­ tween the number of hops and the number of ing movements. These techniques seemed clearly short flights and cones visited, thus contrasting related to movements between cones on outer flightless with aerial techniques related to pine canopies and exploitation of pine seeds (i.e. hang­ cone use. The third factor relates the number of ing positions). When outer canopies were not long flights to change of tree, indicating that available for birds due to snow cover, individuals while foraging, birds used this movement when restricted their foraging activities to trunks and switching from one tree to the next. The fourth low thick branches, resulting in a smaller diver­ factor relates use of hovers negatively with use of sity of substrates used. Under these conditions, hanging position, but the little use birds made of birds reduced the number of flights. At the same hovers detracts from the importance of this factor. time birds increased pecking rates suggesting a Because patterns of change between trees (i.e. change in prey use supported by results of arthro­ factor 3, Table 3) did not differ between condi­ pod availability on inner tree surfaces. Hence, un­ tions, but factors describing searching techniques der snowy conditions Coal Tits seemed to con­ within trees did (i.e. factors I, 2, Table 3). It centrate their search effort on small but abundant seems that according to snow cover, Coal Tits prey by reducing overall movement rates. modified searching patterns when moving within Optimal foraging models, based on the prem­ a given tree but not when switching from one tree ise that collect food in a way which max­ to the next. imises their net rate of food intake, have been In order to relate substrate use to searching quite successful in predicting the decision rules techniques it is important to know the main food by predators in a number of previous studies sources in the different parts of a tree, and so to (Royama 1970, Krebs et at. 1978, Pyke 1984, Ste­ know the main items taken by birds in different phens & Krebs 1986). Some of these studies car­ conditions. In snow-free conditions, the pecking ried out on tits have demonstrated that birds dis­ rate was significantly associated with the number tribute their search effort in relation to spatial dif­ ofcones visited (R2 =0.35, n =16, P < 0.05). This ferences in the profitability of feeding sites seems to reinforce the idea that in winter Coal (Smith & Sweatman 1974, Krebs et at. 1978). Tits fed mainly on pine seeds when foraging on Thus, more profitable and, hence, preferred sites the outer and higher parts of pines. On inner tree will be those exploited under normal conditions surfaces (i.e. trunks and thick branches), the po­ when birds are able to choose freely between sub­ tential invertebrate prey consisted nearly exclu­ strates. As the available foraging surface de­ sively ofspringtails (Collembola, Entomo­ creases, 9irds would be expected to shift to less­ brya), other groups such as spiders, were almost preferred sites containing less-rewarding prey. In absent from samples taken. Springtails were pre­ this study we have shown that when forced by sent at a very high density on inner tree surfaces (x transient snow cover of outer tree canopies, Coal = 18 individuals dm-2, SE =3.22, n =6). Mean size Tits changed substrate use and so prey choice. ofindividuals was 1.7 mm (SE =0.23, n =45). According to the morphology of species, different substrate selection for foraging often requires dif­ ferent locomotion types (Norberg 1979, Robinson DISCUSSION & Holmes 1982, Gustafsson 1988, Moreno et at. 1988). In fact niche shifts recorded in our study In snow free conditions, Coal Tits foraged in the were linked to a change in the searching tech­ outer and upper parts of pines, mainly on cones niques used by the birds. and needles as has been shown in other studies Since short flights and hanging positions are (see Cramp & Perrins 1993). Moreover, in these energetically very costly for small passerines (Al­ conditions they used hanging position and short atalo 1982, Laurent 1986, Tatner & Bryant 1986, Brotons: FORAGING AND SNOW COVER IN THE COAL TIT 255

Carlsson & Moreno 1992), movement patterns proved by Raimon Marine, Jose Luis Copete, Markku employed by Coal Tits during snowy conditions Orell, Jacint Nadal, Luc Lens, Bruno Ens and Nanette are in agreement with Norberg's hypotheses Verboven. This study was supported by a grant from (1977) that when the prospects of achieving prey the 'Parc Natural Cadf-Moixer6' and a grant from the decrease (i.e. preference decreases) lower energy 'Comissionat per a Universitats i Recerca de la Gene­ ralitat de Catalunya' to L.B. consuming searching methods will be used. Fur­ thermore, in snowy conditions a decrease in movement and flying rates and the use of the in­ REFERENCES ner parts of trees could help birds to avoid falling snow from higher canopies. Falling snow at high Alatalo R.y. 1982. Effects of temperature on foraging temperatures or under strong wind might be behaviour of small forest birds wintering in North­ harmful to birds, by affecting their flying perfor­ ern Finland. Ornis Fennica 59: 1-12. mance or directly resulting in physical damage if Baker R.D. 1978. The evolutionary ecology of animal struck directly (unpubl. data). migration. Hodder & Stoughton, London. Bhattacharyya H. 1981. Theory and methods of factor Carrascal (1988) found that some forest spe­ analysis and principal components. In: D.E. Capen cies shifted towards tree trunks after snow storms. (ed.) The use ofmultivariate statistics in studies of His results raised the role of inner tree surfaces in wildlife : 72-79. USDA Forest service. softening the negative consequences oftemporary Bowman K.O., K. Hutcheson, E.P. Odum & L.R. Shen­ harsh weather conditions. Our study clearly gives ton 1971. Comments on the distribution of indices of diversity. In: G.P. Pati!, E.C. Pielou & W.E. Wa­ support to this view for the Coal Tit. Mature fo­ ters (eds) Statistical ecology, 3: 315-366. Pennsyl­ rests, containing higher proportions of inner tree vania State University Press. substrates, may allow Coal Tits to withstand Carlson A. & J. Moreno 1992. Cost of short flights in snowy winter climate better than young pine the Willow Tit measured with doubly-labelled wa­ stands where small trees stay snow covered lon­ ter. Auk 109: 389-393. Carrascal L.M. 1983. Amilisis comparativo de cinco ger than older ones. Because hoarding tits, such sistemas de muestreo del uso del espacio en aves as the Coal Tit, store food mostly in the crevices forestales. Ardeola 30: 45-55. of inner parts of trees, the presence of the hoard­ Carrascal L.M. 1988. Influencia de las condiciones am­ ing habit reinforces the idea of tree trunks and bientales sobre la organizaci6n de la comunidad de thick branches as reserves of food in transitory aves invernante en un bosque subalpino meditemi­ neo. Dofiana, Acta Verte. 15: 111-131. adverse weather conditions (Lens et at. 1994, un­ Cramp S. & C.M. Perrins (eds) 1993. The birds of the publ. data). In conclusion, when conditions be­ Western Palearctic, 7. Oxford University Press, come more difficult for birds due to a decrease in Oxford. foraging surface, Coal Tits used available sub­ Ekman J. 1984. Density-dependent seasonal mortality strates, preyed on secondary, less-preferred prey and population fluctuations of the temperate-zone Willow Tit (Parus montanus). J. Anim. Ecol 53: and used energetically cheaper techniques. Be­ 119-134. havioural plasticity in foraging may become im­ Elkins N. 1983. Weather and bird behaviour. T. & A.D. portant, allowing birds to withstand adverse tem­ Poyser, Calton. porary conditions derived from a harsh climate. Gibb J. 1960. Populations of tits and goldcrests and their food supply in pine plantations. Ibis 102: 103-208. Grubb T.C. 1979. Factors controlling foraging strate­ ACKNOWLEDGEMENTS gies of insectivorous birds. In: J.G. Dickson, R. Connor, R. Fleet, J.A. Jackson & J.e. Kroll (eds) Pere Oller of the 'Institut Cartogratic de la Generalitat The role of insectivorous birds in forest ecosys­ de Catalunya' provided the meteorological data neces­ tems: 119-135. Academic Press, New York. sary for the study. I thank the staff of the 'Parc Natural Gustafsson L. 1988. Foraging behaviour of individual Cadf-Moixer6' for their help in the preparation of the Coal Tits, Parus ater, in relation to their age, sex and morphology. Anim. Behav. 36: 696-704. study area. Earlier drafts of the manuscript were im- 256 ARDEA 85(2), 1997

Haftorn S. 1956. Contribution to the food biology of Smith S.M. 1991. The Black-capped Chickadee. Cor­ tits especially about storing of surplus food. Part nell University Press, New York. II. The Coal Tit. K. norske Vidensk. Selsk. Skr. Soka1 R.R. & EJ. Rohlf 1981. Biometry. Freeman, San 1956(2): 1-52. Francisco. Jansson c., J. Ekman & A von Bromsen 1981. Winter Spencer R 1982. Birds in winter: an outline. Bird mortality and food supply in tits, Parus spp. Oikos Study 29: 169-182. 37: 313-322. Stephens D.W. & J.R. Krebs 1986. Foraging theory. Krebs J.R., A Kacelnik & P. Taylor 1978. Test of optimal Princeton University Press, New Jersey. sampling by foraging Great Tits. Nature 275: 27-31. Suhonen J., R.Y. Alatalo, A Carlson & J. Hoglund Laurent J.L. 1986. Winter foraging behaviour and re­ 1992. Food resource distribution and the organiza­ source availability for a guild of insectivorous tion of the Parus guild in a spruce forest. Ornis gleaning birds in a southern alpine forest. Scand.23: 467-474. Ornis Scand. 17: 347-355. Tatner P. & D.M. Bryant 1986. Flight costs of a small Leger D.W. & I.S. Didrichsons 1994. An assesment of passerine measured using doubly labeled water: data pooling and some alternatives. Anim. Behav. implications for energetic studies. Auk 103: 169­ 48: 823-832. 180. Lens L. 1996. Wind stress affects foraging site compe­ Vigo J. 1976. L'alta muntanya catalana, flora i vegeta­ titon between Crested Tits and Willow Tits. J. ci6. Montblanch-Marti, Barcelona. Avian BioI. 27: 41-47. Wachob D.G. 1996. The effect of thermal microclimate Lens L., E Adriaensen & AA Dhondt 1994. Age re­ on foraging site selection by wintering mountain lated hoarding strategies in the Crested Tit (Parus chickadees. Condor 98: 114-122. cristatus): should the cost of subordination be re­ assessed? J. Anim. Ecol. 63: 749-755. Maccarone AD. 1987. Effect of snow cover on starling SAMENVATTING activity and foraging patterns. Wilson Bull. 99: 94­ 97. Kleine vogels, zoals de Zwarte Mezen (Parus ater) die Moreno J., A Carlson & R.Y. Alatalo 1988. Winter en­ ergetics of coniferous forest tits Paridae in the in de montane naaldwouden van de Pyreneeen leven, north: implications of body size. Funct. Ecol. 2: moeten in de winter continu foerageren om te overle­ 163-170. ven. Ze hebben het waarschijnlijk extra moeilijk als de Morrison M.L. 1984. Influence ofsample size and sam­ takken van de naaldbomen door sneeuw bedekt zijn. In pling design on analyses of avian foraging behav­ deze studie werd in detail vastgelegd welke delen van ior. Condor 86: 146-150. de boom door de vogels gebruikt werden en welke foe­ Norberg R.A 1977. An ecological theory on foraging rageertechniek ze gebruikten, bij (1) aanwezigheid van time and energetics and choice of optimal food­ sneeuw, en (2) bij afwezigheid van sneeuw op de tak­ searching method. J. Anim. Ecol. 46: 511-529. ken. Van december tot april is de bodem van het bos be­ Norberg U.M. 1979. Morphology of the wings, legs dekt met sneeuw. Dagen met meer dan 10 cm sneeuw­ and tail ofthree coniferous forest tits, the and the in relation to locomotor pattern val komen meestal 5 tot 6 keer per jaar voor. Afhanke­ and feeding station selection. Phil. Trans. Roy. lijk van wind en temperatuur blijft de sneeuw 3 tot 4 Soc. Lon. 287: 131-165. dagen op de takken liggen. De winter van het onder­ Obeso J.R 1987. Uso del espacio y alimentaci6n de los zoek in 1996 was extreem met 16 dagen met meer dan Parus spp. en bosques mixtos de la sierra de Ca­ 10 cm sneeuwval. zorla. Ardeola 34: 61-77. Als de buitenste takken met sneeuw bedekt waren Pyke G.H. 1984. Optimal foraging theory: a critical re­ zochten de vogels op de starn en dikke takken, laag bij view. Ann. Rev. Ecol. Syst. 15: 523-575. de grond en in het binnenste van de boom naar voedsel Robinson S.K. & RT. Holmes 1982. Foraging behav­ (Figuur 1). Het potentiele voedselaanbod daar bestond ior of forest birds: the relationships among tactics, vrijwel uitsluitend uit zeer kleine springstaarten (ge­ diet and habitat structure. Ecology 63: 1918-1931. Royama T. 1970. Factors governing the hunting beha­ middelde lengte slechts 1.7 mm), die weI in hoge dicht­ viour and food selection of the (Parus heid voorkwamen. Bij afwezigheid van sneeuw (de major). J. Anim. Ecol. 39: 619-688. meer gangbare conditie, zelfs in de winter) waren de Smith J.M. & P.A Sweatman 1974. Food-searching be­ vogels vooral in de toppen en aan de buitenkant van de havior of titmice in patchy environments. Ecology bomen te vinden (Figuur 1), alwaar ze naar voedsel 55: 1216-1232. zochten op de naalden en de denneappels (Figuur 2). Brotons: FORAGING AND SNOW COVER IN THE COAL TIT 257

De auteur vermoedt dat de vogels daar vooral denneza­ analyse uitgevoerd (Tabel 3). Daaruit bleek dat den aten. sneeuwval vooral effect had op het fourageergedrag en Niet aIleen de plaats waar de vogels naar voedsel de verplaatsingen binnen een boom, maar niet op de zoeken, maar ook de manier waarop ze naar voedsel verplaatsingen tussen bomen. De resultaten kunnen zoeken, bleek afhankelijk van de sneeuwbedekking. goed verklaard worden door de hypothese van Norberg Als er geen sneeuw op de takken ligt gebruiken de die­ (1977) dat foerageermethoden die veel energie vragen ren foerageermethoden die veel energie kosten. Ze vlie­ alleen gebruikt zullen worden als de verwachte ener­ gen veel en hangen vaak aan de kegels (Tabel 2). Als er giewinst ook hoog is. (BJE) weI sneeuw ligt gaan de dieren over op het energetisch veel voordeliger hippen (Tabel 2). Om een beter idee van de samenhang in de verschillende foerageertech­ Received 21 October 1996, accepted 18 August 1997 nieken te krijgen werd een principale componenten Corresponding editor: Bruno J. Ens