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The effects of needle loss in coniferous forests in South-west Sweden on the winter foraging behaviour of willow tits Parus montanus
Biological Conservation .58 (1991) 357-366
The Effects of Needle Loss in Coniferous Forests in South-west Sweden on the Winter Foraging Behaviour of Willow Tits Parus montanus Mikael Hake Division of Animal Ecology, Department of Zoology, University of Gothenburg, Box 25059, S-400 31 Gothenburg, Sweden (Received 13 July 1990; revised version received 1 March 1991; accepted 5 March 1991)
ABSTRACT The foraging behaviour of the willow tit Parus montanus was studied in two coniferous forest areas in S W Sweden, showing high (H) and low (L) percentages of needle loss, respectively. The needle loss is presumed to be accelerated mainly by air pollution and leads to (1) thinning of the tree canopies which could make birds easier for predators to detect and (2) reduction in the abundance of arthropods, which are important food of wintering passerines. Willow tits foraging in pine Pinus sylvestris in the Harea spent proportionally more time scanning for predators and less time handling prey than individuals in the L-area. In the H-area the tits also joined larger mixed-species flocks which included more species. These responses are interpreted as increased time stress in damaged forest but nevertheless the birds showed no tendency to lower their body mass. The results are discussed in relation to winter survival and the consequences of needle loss for bird populations in coniferous forests.
INTRODUCTION Air pollutants are presumed to be the main cause of widespread forest decline in northern Europe (Lichtenthaler, 1984; Blank, 1985; Nihlg~rd, 1985). The trees may be affected by direct deposition of pollutants (Lindberg et al., 1986) or by acidification o f the soil, which causes root damage and 357 BioL Conserv. 0006-3207/91/$03-50 © 1991 Elsevier SciencePublishers Ltd, England. Printed in Great Britain
358
Mikael Hake
disturbance in the uptake of nutrients (see Berd6n et al., 1987, for a review). In conifers this leads to increased needle loss, making the tree canopies and the branches 'thinner' (Westman & Lesinski, 1986). Several studies have pointed to potential negative effects on birds due to pollution and acidification of aquatic habitats (see Eriksson, 1984, 1987, for a review), and although evidence is weak and contradictory (Eriksson et al., 1989) there are indications of decreased reproduction (Barr, '1986) and growth (Glooschenko et al., 1986). Similar effects have been reported from terrestrial environments (Nyholm & Myhrberg, 1977; Nyholm, 1981; Sawicka-Kapusta et al., 1986), but nothing is known about the indirect effects of pollution acting through, for instance, trophic interactions or behaviour. Further, little attention has been paid to the wintering period, which may be critical, especially for small passerines living in temperate areas (Jansson et al., 1981; Ekman, 1984). This study concerns the willow tit Parus montanus, with some ancillary data on the crested tit P. cristatus, two species that are largely confined to coniferous forest, and thus may be affected by forest decline. The populations of several tit species of coniferous forest, for example the crested tit, willow tit, coal tit Parus ater (Nohr et al., 1986; Hake & Eriksson, 1990) and Siberian tit P. cinctus (J/irvinen & V~iis/inen, 1979; Virkkala, 1990), have declined lately, but little is known of the mechanisms. However, these decreases cannot be ascribed to any pesticide, so biological mechanisms could be important (see Virkkala, 1990, for indirect effects of forest management). Such mechanisms could include behaviour important for survival, especially in the winter when food supply decreases and energy demand is high (Jansson et aL, 1981; Jansson & von Br6mssen, 1981). During winter both food availability and the risk of being preyed upon are crucial to survival (Jansson et al., 1981; Ekman, 1984). The tits spend almost all the daytime foraging, and the foraging time is divided into different activities, mainly searching for food, handling prey and scanning for predators. These proportions make up the birds' daily 'time budget' (Ekman, 1987). It is known that coniferous dieback and needle loss lead to decreased abundance of spiders (Gunnarsson, 1988, 1990), which are an important food for wintering tits (Askenmo et al., 1977; Jansson &von Br6mssen, 1981; Gunnarsson, 1983) and, in January-February, may make up about 80% of the prey taken by goldcrests Regulus regulus (Hogstad, 1984). Moreover, thinning of the tree canopies could make the birds more vulnerable to predation from sparrowhawks Accipiter nisus and pygmy owls Glaucidium passerinum, which are the main predators on the birds in winter (Ekman, 1984, 1986). If winter survival is governed by a balance between predation and starvation risks, the birds may be sensitive to the changed structure of the trees and one might expect them to change their behaviour (i.e. their time
Needle loss and foraging behaviour of wintering tits
359
budget) in response to the changed habitat. This study analyses the effects of needle loss in coniferous forests on the behaviour of the willow tit.
METHODS The study sites are two coniferous forest areas in SW Sweden, showing high (H) and low (L) percentages of needle loss, respectively. Magnitudes of needle loss were determined using the results of two flight-photography surveys of forest decline, made by the Regional Forestry Commissions in the counties of Halland, G6teborg and Bohus/,~,lvsborg (Schlyter, 1988; Skogsv~trdsstyrelserna i G6teborgs och Bohus och ,~lvsborgs l/in, 1989). The locations of the study areas are shown in Fig. 1. Although geographically separated by about 25 km, the two areas had similar woodland of spruce Picea abies and pine Pinus sylvestris, and were at the same elevation above sea level. The most important difference was the percentage of needle loss, which was much higher in the H-area (Table 1). A total of 26 willow tits and 25 crested tits in the L-area, and 38 willow tits and 22 crested tits in the H-area, were captured, using mist nets and song playback, during September-December 1987 and September-November 1988. The birds were ringed and individually colour-marked, allowing separation of the flocks within each area. Flocks rarely leave their territories
y/
tg I.-atea H-area
,
l
l
,
i
km
Fig. 1. Location of the study areas.
1~
Mikael Hake
360
TABLE 1
Magnitude of Needle Loss in the Study Sites
Locality
Proportions of trees damaged a (Number of trees classified) Spruce
Pine
L-area
0.421 (994)
0'373 (319)
H-area
0.529 (376)
0"667 (414)
12"6"**
61"3"**
X2~
Proportion of trees with needle loss >20% in older stands (>60 years) (data from a flight-photography survey of coniferous tree damage made by the Regional Forestry Commissions in the county of Halland and the county of G6teborg and Bohus/~,lvsborg). b ~(z test; *** p < 0.001.
and are almost always made up of the same individuals (Ekman, 1979). For a comparison of biometrical measures of birds from the two localities wing length was measured with a ruler to the nearest 0.5 m m and weight was recorded by a Pesola spring balance to the nearest 0-1 g. The time budget of willow tits, feeding in pine, was recorded during December-January 1988/89 using Ekman's delayed point count technique (Ekman, 1987). Once a willow tit had been spotted in a pine I started an electronic metronome and recorded the activity of the bird exactly five seconds later. By this method it is possible to avoid discovery bias (Bradley, 1985), as the birds are sufficiently active to change their behaviour in the time period between detection and recording (Ekman, 1987). One observation per bird and tree was allowed, and after one observation another individual was searched for at random and recorded in the same way. By this method the observations may be treated as statistically independent. The bird was regarded as 'searching' when the bill was kept below and 'scanning' when the bill was kept above the horizontal level. If the bird had food in its bill it was classed as 'handling'. All other behaviour (e.g. fighting, preening, resting) was considered as 'other activity'. Scanning behaviour is hardly ever used for searching overhead branches (Ekman, 1987, personal observations), but if the bird immediately flew off to an overhead branch after being recorded as scanning the observation was excluded. Observations were taken only if the bird was in a standing position. The records were made on the flock level, i.e. I distinguished the different flocks but not the individuals, except that no subsequent records were made of the same individual (see above). Each flock
Needle loss and foraging behaviour of wintering tits
361
(six in the L-area and five in the H-area) was recorded twice (two trials), and the proportions of the time budget were calculated only if the number of observations in the trial exceeded 20. A mean of the two trials was then calculated for each flock, and the mean time budget of the two areas compared. In total, 585 observations were made--331 in the L-area and 254 in the H-area. To test if the birds compensated for the presumed higher exposure in the H-area, flock sizes and the number of species included in the mixed-species flocks were recorded in both areas and compared. This was often difficult as the individuals in the flocks were often numerous and scattered. However, it was possible to count some flocks accurately when the birds passed an open area such as a track or bog.
RESULTS The main difference between areas was in the proportion of time spent 'scanning'. When foraging in pine willow tits in the H-area spent 40% of the time 'scanning', compared with 31% in the L-area. This difference was significant (p = 0.004). The birds seemed to compensate for the increased scanning time by a decrease in the handling time, which also differed significantly between areas at 17% and 24%, respectively (p<0.026). In contrast, the time spent 'searching' did not differ, and was about 43% in both areas (Table 2). The results from the L-area support those of Ekman (1987), who, for the willow tit, found a similar time budget at the same time of year in the same area. Both willow tits and crested tits joined mixed-species flocks. Other species that frequently joined these flocks included goldcrests, coal tits, tree-creepers Certhiafamiliaris, great titsParus major and blue tits P. caeruleus. In the Harea flocks were larger and, on average, contained about 29 individuals compared to 20 in the L-area (p < 0.02). The number of species included in TABLE 2 Time Budgets (_+standard errors) of Willow Tits Foraging in Pine
Locality
L-area H-area Ua
Time proportion Searching +_SE
Scanning +_SE
Handling + SE
Other activity +_SE
0-432 _+0.016 0-426 + 0-015 14 NS
0-310 _ 0.019 0.403 _+0.016 1"*
0.241 _+0.019 0.172 +_0.016 4*
0.013 _+0.008 0.004 _+0.004 10 NS
Mann-Whitney U-test; *p < 0"026, **p = 0.0043.
Mikael Hake
362
TABLE 3
Number of Individuals and Species in Mixed-Species Flocks (n = number of flocks counted) Locality
Individuals +-SD (n)
Species +_SD (n)
L-area H-area Ua
19"8 -+ 12.5 (17) 29.1 _+8"3 (15) 69*
4-1 + 1'5 (17) 5.9-1- 1"5 (15) 54**
a Mann-Whitney U-test; *p < 0.05, **p < 0.02.
TABLE 4
Biometrics of Willow Tits and Crested Tits Captured in the Two Study Areas during the Winter Seasons 1987/88 and 1988/89 (n = number of birds measured) Species
Sex
Wing length (mm)
Weight (g)
L-area +_SD (n) H-area + SD (n)
L-area +_SD (n) H-area +__SD (n)
P. montanus
M F
65-7+0"8 (13) 62.4+0"9 (16)
65"6+0"8 ( 2 1 ) 62-3+0-8 (17)
11'6+0"4 (12) 10"9+0"3 (16)
11"8+0"5 (17) 10.9___0.4(12)
P cristatus
M F
64"9+0"8 (13) 61-2+0'5 (12)
65-2+ 1"1 ( 1 4 ) 61-9+0'7 (8)
11-8-t-0"6 (13) 10"9+0"8 (11)
11"4+0.5 (8) 10"5+0"3 (5)
Individuals of the two species were divided by sex because males and females are sexdimorphic (J. Ekman, pers. comm.).
the flocks also differed significantly--about four versus six, respectively (p < 0.05, see Table 3). Single birds were almost never seen in the H-area but were not u n c o m m o n in the L-area. Despite behavioural differences, no biometrical differences between individuals captured in the two areas could be detected (Table 4).
DISCUSSION
The foraging behaviour of willow tits differed significantly in the two areas as regards the proportion of the time budget devoted to scanning and handling. These results suggest either (1) an increased r i s k o f predation forcing the birds to be more vigilant by reducing other activities or (2) improved foraging conditions allowing less time for handling and more time for other activities. In December-February spiders are almost the only animal prey that occur in the trees and are the most important food for the
Needle loss and foraging behaviour of wintering tits
363
birds (Jansson & yon Br6mssen, 1981). Gunnarsson (1988, 1990) found a lower spider density on branches with low needle density from the same two areas. Furthermore, there were no indications of an increase in the proportions of other prey items that might demand less handling time in the H-area (B. Gunnarsson, pers. comm.). These results refute the suggestion that feeding behaviour was affected by improved foraging conditions, and indicate that the birds faced higher predator exposure. Increased risk of predation did not cause the birds to lower their body mass. This would be one conceivable response to increased exposure if starvation risk is balanced against the risk of predation, as a fat bird is less manoeuvrable (Lima, 1986). However, a low body mass implies greater risk of starvation, which might be fatal during cold nights in winter (Jansson et al., 1981; Ekman, 1984). Rather, the tits responded by joining mixed-species flocks. Thereby they could maintain protection from predators without having to suffer an increased starvation risk as individual scanning time decreases when the flock size becomes larger (Pulliam, 1973; Caraco, 1979; Pulliam & Millikan, 1982; Ekman, 1987; Hogstad, 1988). It is likely that this is the only reason why larger flocks are formed as tits live on limited and dispersed food (Askenmo et al., 1977; Jansson & von Br6mssen, 1981). They cannot benefit from improved foraging conditions when joinihg a flock, as an increase in individual intake rate is possible only if the food occurs in discrete patches which are too ephemeral to be depleted (Hake & Ekman, 1988). However, the cost of sharing resources with other flock members may be smaller for tits than for species that live on a more patchily distributed food resource, as do many finches (Fringillidae), for example (Pulliam & Millikan, 1982; Clark & Mangel, 1984, 1986; Hake & Ekman, 1988), and their response to increased exposure may be different. There were no indications of higher levels of predator activity in the Harea which could have accounted for the difference in behaviour. Three sparrowhawks were seen during the study, two in the L-area and one in the H-area; pygmy owls were not seen in either of the areas but are known to breed in the region (Jansson et al., 1981; Ekman, 1984, 1986; SOF, 1990). It thus seems that the birds in the H-area really are affected by some change in the habitat compared to the L-area, forcing them to behave differently. The most likely explanation is the difference in the proportion of needle loss. Even if other differences between the two study areas exist, needle density should be the most important, especially in mid-December and January, i.e. when observations of the time budgets were taken. During this time the birds feed almost exclusively in the upper half of mature pines (Jansson, 1982; Ekman, 1987, personal observations) and must rely on the needle density for protection against predators. Furthermore, it seemed that the birds were quite severely affected, as they compensated for the increased
364
Mikael Hake
visibility both by joining mixed-species flocks and by increasing the proportion of time spent scanning. The results indicate that acidic aerial deposition may not only cause accumulation of toxic substances in body tissues of birds (Sawicka-Kapusta et al., 1986) which might reduce the rate of reproduction (Nyholm, 1981; Barr, 1986) but also accelerate forest decline, which can affect patterns of bird behaviour that are important for survival. The consequence of this could be a lower winter survival in areas affected by forest decline, which might result in a decrease in population levels, since winter survival seems closely linked to behaviour (Ekman, 1984, 1987). ACKNOWLEDGEMENTS I thank Per Angelstam, Jan Ekman, Mats Eriksson, Bengt Gunnarsson and an anonymous referee for valuable comments on earlier drafts of this paper. I especially thank J.E. and B.G. for helpful advice and stimulating discussions during the progress of this study. Data on forest damage was provided by the Regional Forestry Commissions in the counties of Halland, GSteborg and Bohus, and Alvsborg. The study was supported by the Swedish National Environmental Protection Board grants to C. Askenmo and B. Gunnarsson.
REFERENCES Askenmo, C., von Br6mssen, A., Ekman, J. & Jansson, C. (1977). Impact of some wintering birds on spider abundance in spruce. Oikos, 28, 90--4. Barr, J. F. (1986). Population dynamics of the common loon Gavia immer associated with mercury-contaminated waters in Northwestern Ontario. Can. Wildl. Serv. Occ. Pap., No. 56, 1-25. Berdrn, M., Nilsson, S., Rosrn, K. & Tyler, G. (1987). Soil Acidification--Extent, Causes and Consequences. National Swedish Environmental Protection Board, Report No. 3292. Blank, L. W. (1985). A new type of forest decline in Germany. Nature, Lond., 314, 311-4. Bradley, D. W. (1985). The effect of visibility bias on time budget estimates of niche breadth and overlap. Auk, 102, 493-9. Caraco, T. (1979). Time budgeting and group size: a theory. Ecology, 60, 611-7. Clark, C. W. & Mangel, M. (1984). Foraging and flocking strategies: information in an uncertain environment. Amer. Nat., 123, 626--41. Clark, C. W. & Mangel, M. (1986). The evolutionary advantages of group foraging. Theoret. Popul. Biol., 30, 45-75. Ekman, J. (1979). Coherence, composition and territories of winter social groups of the willow tit Parus montanus and the crested tit P. cristatus. Ornis Scand., 10, 56-8.
Needle loss and foraging behaviour of wintering tits
365
Ekman, J. (1984). Density-dependent seasonal mortality and population fluctuations of the temperate-zone willow tit Parus montanus. J. Anita. Ecol., 53, 119-34. Ekman, J. (1986). Tree use and predator vulnerability of wintering passerines. Ornis Scand., 17, 261-7. Ekman, J. (1987). Exposure and time use in willow tit flocks: the cost of subordination. Anita. Behav., 35, 445-52. Eriksson, M. O. G. (1984). Acidification of lakes: effects on waterbirds in Sweden. Ambio, 13, 260-2. Eriksson, M. O. G. (1987). Some effects of freshwater acidification on birds in Sweden. ICBP Tech. Pubis, No. 6. Eriksson, M. O. G., Henriksson, L. & Oscarson, H. G. (1989). Metal contents in liver tissues of non-fledged goldeneye Bucephala clangula ducklings: a comparison between samples from acidic, circumneutral, and limed lakes in south Sweden. Arch. Environ. Contain. ToxicoL, 18, 255-60. Glooschenko, V., Blancher, E, Herskowitz, J., Fulthorpe, R. & Rang, S. (1986). Association of wetland acidity with reproductive parameters and insect prey of eastern kingbird Tyrannus tyrannus near Sudbury, Ontario. Water, Air, Soil Pollut., 30, 553-67. Gunnarsson, B. (1983). Winter mortality of spruce-living spiders: effects of spider interactions and bird predation. Oikos, 40, 226-33. Gunnarsson, B. (1988). Spruce-living spiders and forest decline; the importance of needle-loss. Biol. Conserv., 43, 309-19. Gunnarsson, B. (1990). Vegetation structure and the abundance and size distribution of spruce-living spiders. J. Anita. Ecol., 59, 242-53. Hake, M. & Ekman, J. (1988). Finding and sharing depletable patches: when group foraging decreases intake rates. Ornis Scand., 19, 275-9. Hake, M. & Eriksson, M. O. G. (1990). Passerine birds and their prey affected by forest dieback: a tentative work model. Fauna Norv. Set. C, Cinclus, Suppl., 1, 13-6. Hogstad, O. (1984). Variation in numbers, territoriality and flock size of a goldcrest Regulus regulus population in winter. Ibis, 126, 296-306. Hogstad, O. (1988). Advantages of social foraging in willow tits Parus montanus. Ibis, 130, 275-83. Jansson, C. (1982). Food supply, foraging, diet and winter mortality in two coniferous forest tit species. PhD thesis, University of Gothenburg. Jansson, C. & yon BrSmssen, A. (1981). Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds. Holarct. Ecol., 4, 82-93. Jansson, C., Ekman, J. & yon Br6mssen, A. 0981). Winter mortality and food supply in tits Parus ssp. Oikos, 37, 313-22. J~irvinen, O. & V/iis~inen, R. A. (1979). Changes in bird populations as criteria of environmental changes. Holarct. Ecol., 2, 75-80. Lichtenthaler, H. K. (1984). Luftschadstoffe als Ausl6ser des Baumsterbens. Naturw. Rdsch., 37, 271-7. Lima, S. L. (1986). Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology, 67, 377-85. Lindberg, S. E., Lovett, G. M., Richter, D. D. & Johnson, D. W. (1986). Atmospheric deposition and canopy interactions of major ions in a forest. Science, N.Y., 231, 141-5.
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Nihlg~rd, B. (1985). The ammonium hypothesis--an additional explanation to the forest dieback in Europe. Ambio, 14, 2-8. Nyholm, N. E. I. (1981). Evidence of involvement of aluminium in causation of defective formation of eggshells and impaired breeding in wild passerine birds. Environ. Res., 26, 363-71. Nyholm, N. E. I. & Myhrberg, H. E. (1977). Severe eggshell defects and impaired reproductive capacity in small passerines in Swedish Lapland. Oikos, 29, 336-41, Nohr, H., Hansen, K. & Braae, L. (1986). Fuglene som indikator for skovdod? Fugle, 6, 25 (in Danish). Pulliam, H. R. (1973). On the advantage of flocking. J. Theoret. BioL, 38, 419-22. Pulliam, H. R. & Millikan, G. C. (1982). Social organization in the non-reproductive season. In Avian Biology, Vol. 6, ed. D. S. Farner, J. R. King & K. C. Parkes. Academic Press, New York, pp. 169-97. Sawicka-Kapusta, K., Kozlowski, J. & Sokolowska, T. (1986). Heavy metals in tits from polluted forests in southern Poland. Environ. Pollut., 42, 297-310. Schlyter, P. (1988). An aerial survey of forest damage on spruce and pine in Halland county, S Sweden, 1986. Report from the Regional Forestry Commission in the County of Halland (in Swedish with English summary.). Skogsv~rdsstyrelserna i G6teborgs och Bohus och .~lvsborgs l~in (1989). Fiygbildsbaserad inventering av skogsskador i G6teborgs och Bohus och ,~lvsborgs 1/in 1988. Report from the Local Forestry Commissions in the County of G6teborg and Bohus and the County of Alvsborg (in Swedish). SOF (1990). Sveriges F&glar, 2nd edn. Sveriges Ornitologiska F6rening, Stockholm (in Swedish with English summary). Virkkala, R. (1990). Effects of forestry on birds in a changing north boreal coniferous landscape. PhD thesis, University of Helsinki. Westman, L. & Lesinski, J. (1986). Kronutglesning och andra f6rdndringar i grankronan. Morfologisk beskrivning. National Swedish Environmental Protection Board, Report No. 3262 (in Swedish).
The Effects of Needle Loss in Coniferous Forests in South-west Sweden on the Winter Foraging Behaviour of Willow Tits Parus montanus Mikael Hake Division of Animal Ecology, Department of Zoology, University of Gothenburg, Box 25059, S-400 31 Gothenburg, Sweden (Received 13 July 1990; revised version received 1 March 1991; accepted 5 March 1991)
ABSTRACT The foraging behaviour of the willow tit Parus montanus was studied in two coniferous forest areas in S W Sweden, showing high (H) and low (L) percentages of needle loss, respectively. The needle loss is presumed to be accelerated mainly by air pollution and leads to (1) thinning of the tree canopies which could make birds easier for predators to detect and (2) reduction in the abundance of arthropods, which are important food of wintering passerines. Willow tits foraging in pine Pinus sylvestris in the Harea spent proportionally more time scanning for predators and less time handling prey than individuals in the L-area. In the H-area the tits also joined larger mixed-species flocks which included more species. These responses are interpreted as increased time stress in damaged forest but nevertheless the birds showed no tendency to lower their body mass. The results are discussed in relation to winter survival and the consequences of needle loss for bird populations in coniferous forests.
INTRODUCTION Air pollutants are presumed to be the main cause of widespread forest decline in northern Europe (Lichtenthaler, 1984; Blank, 1985; Nihlg~rd, 1985). The trees may be affected by direct deposition of pollutants (Lindberg et al., 1986) or by acidification o f the soil, which causes root damage and 357 BioL Conserv. 0006-3207/91/$03-50 © 1991 Elsevier SciencePublishers Ltd, England. Printed in Great Britain
358
Mikael Hake
disturbance in the uptake of nutrients (see Berd6n et al., 1987, for a review). In conifers this leads to increased needle loss, making the tree canopies and the branches 'thinner' (Westman & Lesinski, 1986). Several studies have pointed to potential negative effects on birds due to pollution and acidification of aquatic habitats (see Eriksson, 1984, 1987, for a review), and although evidence is weak and contradictory (Eriksson et al., 1989) there are indications of decreased reproduction (Barr, '1986) and growth (Glooschenko et al., 1986). Similar effects have been reported from terrestrial environments (Nyholm & Myhrberg, 1977; Nyholm, 1981; Sawicka-Kapusta et al., 1986), but nothing is known about the indirect effects of pollution acting through, for instance, trophic interactions or behaviour. Further, little attention has been paid to the wintering period, which may be critical, especially for small passerines living in temperate areas (Jansson et al., 1981; Ekman, 1984). This study concerns the willow tit Parus montanus, with some ancillary data on the crested tit P. cristatus, two species that are largely confined to coniferous forest, and thus may be affected by forest decline. The populations of several tit species of coniferous forest, for example the crested tit, willow tit, coal tit Parus ater (Nohr et al., 1986; Hake & Eriksson, 1990) and Siberian tit P. cinctus (J/irvinen & V~iis/inen, 1979; Virkkala, 1990), have declined lately, but little is known of the mechanisms. However, these decreases cannot be ascribed to any pesticide, so biological mechanisms could be important (see Virkkala, 1990, for indirect effects of forest management). Such mechanisms could include behaviour important for survival, especially in the winter when food supply decreases and energy demand is high (Jansson et aL, 1981; Jansson & von Br6mssen, 1981). During winter both food availability and the risk of being preyed upon are crucial to survival (Jansson et al., 1981; Ekman, 1984). The tits spend almost all the daytime foraging, and the foraging time is divided into different activities, mainly searching for food, handling prey and scanning for predators. These proportions make up the birds' daily 'time budget' (Ekman, 1987). It is known that coniferous dieback and needle loss lead to decreased abundance of spiders (Gunnarsson, 1988, 1990), which are an important food for wintering tits (Askenmo et al., 1977; Jansson &von Br6mssen, 1981; Gunnarsson, 1983) and, in January-February, may make up about 80% of the prey taken by goldcrests Regulus regulus (Hogstad, 1984). Moreover, thinning of the tree canopies could make the birds more vulnerable to predation from sparrowhawks Accipiter nisus and pygmy owls Glaucidium passerinum, which are the main predators on the birds in winter (Ekman, 1984, 1986). If winter survival is governed by a balance between predation and starvation risks, the birds may be sensitive to the changed structure of the trees and one might expect them to change their behaviour (i.e. their time
Needle loss and foraging behaviour of wintering tits
359
budget) in response to the changed habitat. This study analyses the effects of needle loss in coniferous forests on the behaviour of the willow tit.
METHODS The study sites are two coniferous forest areas in SW Sweden, showing high (H) and low (L) percentages of needle loss, respectively. Magnitudes of needle loss were determined using the results of two flight-photography surveys of forest decline, made by the Regional Forestry Commissions in the counties of Halland, G6teborg and Bohus/,~,lvsborg (Schlyter, 1988; Skogsv~trdsstyrelserna i G6teborgs och Bohus och ,~lvsborgs l/in, 1989). The locations of the study areas are shown in Fig. 1. Although geographically separated by about 25 km, the two areas had similar woodland of spruce Picea abies and pine Pinus sylvestris, and were at the same elevation above sea level. The most important difference was the percentage of needle loss, which was much higher in the H-area (Table 1). A total of 26 willow tits and 25 crested tits in the L-area, and 38 willow tits and 22 crested tits in the H-area, were captured, using mist nets and song playback, during September-December 1987 and September-November 1988. The birds were ringed and individually colour-marked, allowing separation of the flocks within each area. Flocks rarely leave their territories
y/
tg I.-atea H-area
,
l
l
,
i
km
Fig. 1. Location of the study areas.
1~
Mikael Hake
360
TABLE 1
Magnitude of Needle Loss in the Study Sites
Locality
Proportions of trees damaged a (Number of trees classified) Spruce
Pine
L-area
0.421 (994)
0'373 (319)
H-area
0.529 (376)
0"667 (414)
12"6"**
61"3"**
X2~
Proportion of trees with needle loss >20% in older stands (>60 years) (data from a flight-photography survey of coniferous tree damage made by the Regional Forestry Commissions in the county of Halland and the county of G6teborg and Bohus/~,lvsborg). b ~(z test; *** p < 0.001.
and are almost always made up of the same individuals (Ekman, 1979). For a comparison of biometrical measures of birds from the two localities wing length was measured with a ruler to the nearest 0.5 m m and weight was recorded by a Pesola spring balance to the nearest 0-1 g. The time budget of willow tits, feeding in pine, was recorded during December-January 1988/89 using Ekman's delayed point count technique (Ekman, 1987). Once a willow tit had been spotted in a pine I started an electronic metronome and recorded the activity of the bird exactly five seconds later. By this method it is possible to avoid discovery bias (Bradley, 1985), as the birds are sufficiently active to change their behaviour in the time period between detection and recording (Ekman, 1987). One observation per bird and tree was allowed, and after one observation another individual was searched for at random and recorded in the same way. By this method the observations may be treated as statistically independent. The bird was regarded as 'searching' when the bill was kept below and 'scanning' when the bill was kept above the horizontal level. If the bird had food in its bill it was classed as 'handling'. All other behaviour (e.g. fighting, preening, resting) was considered as 'other activity'. Scanning behaviour is hardly ever used for searching overhead branches (Ekman, 1987, personal observations), but if the bird immediately flew off to an overhead branch after being recorded as scanning the observation was excluded. Observations were taken only if the bird was in a standing position. The records were made on the flock level, i.e. I distinguished the different flocks but not the individuals, except that no subsequent records were made of the same individual (see above). Each flock
Needle loss and foraging behaviour of wintering tits
361
(six in the L-area and five in the H-area) was recorded twice (two trials), and the proportions of the time budget were calculated only if the number of observations in the trial exceeded 20. A mean of the two trials was then calculated for each flock, and the mean time budget of the two areas compared. In total, 585 observations were made--331 in the L-area and 254 in the H-area. To test if the birds compensated for the presumed higher exposure in the H-area, flock sizes and the number of species included in the mixed-species flocks were recorded in both areas and compared. This was often difficult as the individuals in the flocks were often numerous and scattered. However, it was possible to count some flocks accurately when the birds passed an open area such as a track or bog.
RESULTS The main difference between areas was in the proportion of time spent 'scanning'. When foraging in pine willow tits in the H-area spent 40% of the time 'scanning', compared with 31% in the L-area. This difference was significant (p = 0.004). The birds seemed to compensate for the increased scanning time by a decrease in the handling time, which also differed significantly between areas at 17% and 24%, respectively (p<0.026). In contrast, the time spent 'searching' did not differ, and was about 43% in both areas (Table 2). The results from the L-area support those of Ekman (1987), who, for the willow tit, found a similar time budget at the same time of year in the same area. Both willow tits and crested tits joined mixed-species flocks. Other species that frequently joined these flocks included goldcrests, coal tits, tree-creepers Certhiafamiliaris, great titsParus major and blue tits P. caeruleus. In the Harea flocks were larger and, on average, contained about 29 individuals compared to 20 in the L-area (p < 0.02). The number of species included in TABLE 2 Time Budgets (_+standard errors) of Willow Tits Foraging in Pine
Locality
L-area H-area Ua
Time proportion Searching +_SE
Scanning +_SE
Handling + SE
Other activity +_SE
0-432 _+0.016 0-426 + 0-015 14 NS
0-310 _ 0.019 0.403 _+0.016 1"*
0.241 _+0.019 0.172 +_0.016 4*
0.013 _+0.008 0.004 _+0.004 10 NS
Mann-Whitney U-test; *p < 0"026, **p = 0.0043.
Mikael Hake
362
TABLE 3
Number of Individuals and Species in Mixed-Species Flocks (n = number of flocks counted) Locality
Individuals +-SD (n)
Species +_SD (n)
L-area H-area Ua
19"8 -+ 12.5 (17) 29.1 _+8"3 (15) 69*
4-1 + 1'5 (17) 5.9-1- 1"5 (15) 54**
a Mann-Whitney U-test; *p < 0.05, **p < 0.02.
TABLE 4
Biometrics of Willow Tits and Crested Tits Captured in the Two Study Areas during the Winter Seasons 1987/88 and 1988/89 (n = number of birds measured) Species
Sex
Wing length (mm)
Weight (g)
L-area +_SD (n) H-area + SD (n)
L-area +_SD (n) H-area +__SD (n)
P. montanus
M F
65-7+0"8 (13) 62.4+0"9 (16)
65"6+0"8 ( 2 1 ) 62-3+0-8 (17)
11'6+0"4 (12) 10"9+0"3 (16)
11"8+0"5 (17) 10.9___0.4(12)
P cristatus
M F
64"9+0"8 (13) 61-2+0'5 (12)
65-2+ 1"1 ( 1 4 ) 61-9+0'7 (8)
11-8-t-0"6 (13) 10"9+0"8 (11)
11"4+0.5 (8) 10"5+0"3 (5)
Individuals of the two species were divided by sex because males and females are sexdimorphic (J. Ekman, pers. comm.).
the flocks also differed significantly--about four versus six, respectively (p < 0.05, see Table 3). Single birds were almost never seen in the H-area but were not u n c o m m o n in the L-area. Despite behavioural differences, no biometrical differences between individuals captured in the two areas could be detected (Table 4).
DISCUSSION
The foraging behaviour of willow tits differed significantly in the two areas as regards the proportion of the time budget devoted to scanning and handling. These results suggest either (1) an increased r i s k o f predation forcing the birds to be more vigilant by reducing other activities or (2) improved foraging conditions allowing less time for handling and more time for other activities. In December-February spiders are almost the only animal prey that occur in the trees and are the most important food for the
Needle loss and foraging behaviour of wintering tits
363
birds (Jansson & yon Br6mssen, 1981). Gunnarsson (1988, 1990) found a lower spider density on branches with low needle density from the same two areas. Furthermore, there were no indications of an increase in the proportions of other prey items that might demand less handling time in the H-area (B. Gunnarsson, pers. comm.). These results refute the suggestion that feeding behaviour was affected by improved foraging conditions, and indicate that the birds faced higher predator exposure. Increased risk of predation did not cause the birds to lower their body mass. This would be one conceivable response to increased exposure if starvation risk is balanced against the risk of predation, as a fat bird is less manoeuvrable (Lima, 1986). However, a low body mass implies greater risk of starvation, which might be fatal during cold nights in winter (Jansson et al., 1981; Ekman, 1984). Rather, the tits responded by joining mixed-species flocks. Thereby they could maintain protection from predators without having to suffer an increased starvation risk as individual scanning time decreases when the flock size becomes larger (Pulliam, 1973; Caraco, 1979; Pulliam & Millikan, 1982; Ekman, 1987; Hogstad, 1988). It is likely that this is the only reason why larger flocks are formed as tits live on limited and dispersed food (Askenmo et al., 1977; Jansson & von Br6mssen, 1981). They cannot benefit from improved foraging conditions when joinihg a flock, as an increase in individual intake rate is possible only if the food occurs in discrete patches which are too ephemeral to be depleted (Hake & Ekman, 1988). However, the cost of sharing resources with other flock members may be smaller for tits than for species that live on a more patchily distributed food resource, as do many finches (Fringillidae), for example (Pulliam & Millikan, 1982; Clark & Mangel, 1984, 1986; Hake & Ekman, 1988), and their response to increased exposure may be different. There were no indications of higher levels of predator activity in the Harea which could have accounted for the difference in behaviour. Three sparrowhawks were seen during the study, two in the L-area and one in the H-area; pygmy owls were not seen in either of the areas but are known to breed in the region (Jansson et al., 1981; Ekman, 1984, 1986; SOF, 1990). It thus seems that the birds in the H-area really are affected by some change in the habitat compared to the L-area, forcing them to behave differently. The most likely explanation is the difference in the proportion of needle loss. Even if other differences between the two study areas exist, needle density should be the most important, especially in mid-December and January, i.e. when observations of the time budgets were taken. During this time the birds feed almost exclusively in the upper half of mature pines (Jansson, 1982; Ekman, 1987, personal observations) and must rely on the needle density for protection against predators. Furthermore, it seemed that the birds were quite severely affected, as they compensated for the increased
364
Mikael Hake
visibility both by joining mixed-species flocks and by increasing the proportion of time spent scanning. The results indicate that acidic aerial deposition may not only cause accumulation of toxic substances in body tissues of birds (Sawicka-Kapusta et al., 1986) which might reduce the rate of reproduction (Nyholm, 1981; Barr, 1986) but also accelerate forest decline, which can affect patterns of bird behaviour that are important for survival. The consequence of this could be a lower winter survival in areas affected by forest decline, which might result in a decrease in population levels, since winter survival seems closely linked to behaviour (Ekman, 1984, 1987). ACKNOWLEDGEMENTS I thank Per Angelstam, Jan Ekman, Mats Eriksson, Bengt Gunnarsson and an anonymous referee for valuable comments on earlier drafts of this paper. I especially thank J.E. and B.G. for helpful advice and stimulating discussions during the progress of this study. Data on forest damage was provided by the Regional Forestry Commissions in the counties of Halland, GSteborg and Bohus, and Alvsborg. The study was supported by the Swedish National Environmental Protection Board grants to C. Askenmo and B. Gunnarsson.
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