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Clumping versus spacing out: Experiments on nest predation in fieldfares (Turdus pilaris)
Anim. Behav ., 1978, 26, 1 20 7 -1212
CLUMPING VERSUS SPACING OUT : EXPERIMENTS ON NEST PREDATION IN FIELDFARES (TURDUS PILARIS) BY MALTE ANDERSSON & CHRISTER G . WIKLUND Department of Zoology, University of Gothenburg, 400 33 Gothenburg 33, Sweden
Abstract. Fieldfares (Turdus pilaris), which nest solitarily as well as in colonies, offer an opportunity to assess within one species the relative advantages of clumping versus spacing out . An experiment with artificial, egg-baited nests showed that predation in the absence of fieldfares was higher on clumped than on scattered nests. In another experiment, we tested whether artificial nests run a higher risk of predation near solitary fieldfare pairs than near fieldfare colonies . Nest predation was higher near solitary fieldfare pairs than outside and inside fieldfare colonies. The risk probably was higher outside than inside colonies . Communal antipredator attacks is the likely cause of reduced predation near colonies . Even solitary fieldfare pairs confer some degree of protection, because predation was lower at artificial nests near solitary fieldfare pairs than at nests without neighbouring fieldfares . Predation is one of the most important selective pressures influencing the optimal spacing pattern in a population . For cryptic prey in open habitats, Tinbergen et al . (1967), Croze (1970) and Goransson et al . (1975) showed experimentally that predation by corvids and larids increased with the local prey density . 'Areaconcentrated search' (Smith 1974) by the predator after prey capture seemed to be the cause . Krebs (1971) and Dunn (1977) found a positive correlation between predation and nest density in great tits (Parus major), as did Fretwell (1972) in field sparrows (Spizella pusilla) . Predation therefore seems to favour spacing out in prey whose main defence is to avoid detection . A theoretical model by Taylor (1976) gave the same prediction. Treisman (1975) reviewed and developed models for the evolution of gregariousness in response to predation . In species with communal anti-predator attacks, the defence efficiency may increase with the number of defenders (Kruuk 1964 ; Andersson 1976), which favours higher local prey densities . The dispersion pattern optimal with respect to avoiding predation in uniform habitats therefore should tend towards well spaced, `solitary' individuals in vulnerable species, and towards clumped `colonies' in species with efficient communal defence. Other selective pressures, in particular on foraging efficiency, may obscure such a trend and make it visible only among species differing in defence strategy while having similar ecology in other respects . Nest predation was the major nesting mortality factor in the bird species treated by Ricklefs (1969). Probably partly as a consequence
of heavy predator pressure, the open, accessible nests of many forest-breeding passerine birds are well spaced and hidden by strategic positioning and cryptical structure (Lack 1968) . Among European species, the fieldfare is an exception . It usually breeds in colonies of 5 to 20 pairs (e.g. Hohlt 1957 ; Lubcke 1975), and the nest appears more conspicuous than in other species, including Turdidae . In the similarly sized North American Brewer's blackbird (Euphagus cyanocephalus), colonial breeding improves the foraging efficiency, whereas the anti-predatory effect seems to vary with the shape of the colony (Horn 1968) . In fieldfares, colonial breeding might reduce predation, because colony members deter approaching predators by communal attacks (Bezzel 1975 ; Furrer 1975 ; Mester 1976) . On the other hand, in the presence of predators using `area-concentrated search', clumping might increase the risk of nest detection, and the net effect is hard to predict . This study, which focuses on the egg stage of the breeding cycle, examines (a) whether the higher risk of predation in clumped rather than in scattered prey populations, previously demonstrated in open habitats, also applies in a structurally more complex forest habitat ; and (b) if, in spite of this, fieldfares can reduce nest predation by breeding in colonies. Experiment I Methods The first experiment tests whether artificial birds' nests in trees run a higher risk of predation when clumped than when scattered . We used two groups of nests : (Ia) 20 `solitary' nests, 1207
ANIMAL BEHAVIOUR, 26, 4
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each several 100 m from the nearest artificial nest or fieldfare nest ; (Ib) 49 `colonial' nests, distributed in seven hexagonal colonies (Fig. 1), each with seven nests 20m apart, a spacing similar to that in fieldfare colonies . To avoid systematic differences in location, we selected 27 places in fieldfare breeding habitat, and allocated the colonies and solitary nests among these places by drawing random numbers . The artificial nests, 15 cm in diameter, 5 cm high, and made of dry grass, were stabilized and attached with thin iron wire to the base of a branch 4 to 6 m above the ground . This is within the height range of fieldfare nests, but lower than their average . The artificial nests were about half as voluminous as fieldfare nests and less conspicuous, differences which should not be important because our tests will be based on comparisons between nests of identical structure . Each nest was baited with two japanese quail (Coturnix c . Japonica) eggs with length x width about 33 x 26 mm, 10 % larger values than for fieldfare eggs . Quail eggs like fieldfare eggs are cryptically coloured, although with larger and darker patches (see Montevecchi 1976). All experiments were performed during the same period in a mosaic of mainly deciduous forest (dominated by oak, Quercus robur) and suburban areas E and SE of Gothenburg, SW Sweden . The nests were placed in position on 11 May 1977 (experiment II) and 12 May (experiment I), when most fieldfare pairs had started or finished laying, whereas hatching had not begun . Deciduous trees were bare, but birches (Betula pubescens and B. verrucosa), the 40
0
Fig. 1 . Hexagonal arrangement of the seven artificial nests in one of the seven `colonies' of experiment I .
earliest species, had half-grown leaves at the end of experiments one week later . A mirror on a 5-m rod was used to inspect each artificial nest for a few seconds . The risk of attracting predators during these daily short visits was probably low. Potential nest predators were crows (Corvus corone cornix), magpies (Pica pica), jays (Garrulus glandarius), woodpeckers (Dendrocopos major), squirrels (Sciurus vulgaris) and small mustelids. Our tests of differences in the risk of predation at different nest categories are based on the survival time of each individual nest . Nests which still survived on the day of last inspection (day n) were designated a survival time of n+ 1 days . Differences between groups are examined with Fisher's permutation test, which has optimum properties (Od6n & Wedel 1975) . Because the direction of the predicted effects can be specified, we use one-tailed tests. A nest with two eggs can be defined as predated either when the first egg has disappeared or when both have been taken . The present results are based on the former definition, but since the two eggs of a nest usually disappeared on the same day, the second definition gives almost identical results. The possibility of demonstrating differences in the risk of predation for different prey categories is highly dependent on the procedure used in recording predation (Montevecchi 1976) . Because the present method employs the survival time of each nest, it should usually be more efficient than tests based on one final inspection of the prey population . Result The predation pattern in the two groups of nests is shown in Fig . 2. The risk of predation was significantly higher for colonial nests (P = 0. 0098), as indicated by the steeper slope of the corresponding cumulative distribution . All eggs in the 49 colonial nests disappeared within four days, whereas the eggs in three of the 20 solitary nests remained after six days . Closer examination of the temporal sequence of predation at colonial nests offers additional information (Table I). The nests within a colony tended to become plundered in close temporal proximity, and in five of the seven colonies, the eggs disappeared from all nests on the same day . Experiment II Methods This experiment tests if the risk of predation is (1) lower at central than at peripheral arti-
ANDERSSON & WIKLUND : NEST PREDATION IN FIELDFARES
ficial nests in a fieldfare colony, and (2) lower at peripheral and/or central colony nests than at nests near solitary fieldfare pairs . There seems to be a gradual transition between solitary and colonial breeding in fieldfares, most colonies containing 5 to 20 clumped nests with 10 to 40 m nearest neighbour distances, sometimes with a few nests farther away . Before the experiment, we arbitrarily assigned all nests with nearest neighbour distance greater than 75 m as solitary (our previous observations indicated that the efficiency of communal defence with larger distances is small), and the remainder as colonial . The experimental groups included : (Ila) 23 nests, each 20 m from a solitary fieldfare pair ; (IIb) 28 `peripheral' nests, each 20 m from the nearest nest in a fieldfare colony, and outside the convex polygon joining or including the nests of the colony (Fig . 3) ; (Ilc) 28 `central' nests, each 20 m from the nearest nest in a fieldfare colony, and inside the convex polygon of the colony . The artificial nests in groups lib and Hc were placed in 14 fieldfare colonies, two nests of each category per colony . In other
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respects they were constructed, baited, located and treated as in experiment I . The fieldfare colonies had an average size of 8 .1 nests (ss _ 0-28) . Result The result of experiment II is summarized in the cumulative distributions of Fig. 4. The risk of predation was significantly lower for both central and peripheral artificial nests at fieldfare colonies than for nests near solitary fieldfare pairs (P = 0.0003 and P = 0 . 038 respectively) . As predicted for a species with communal defence, the risk was lower for central than for peripheral nests, but the difference is not quite significant (P = 0 . 053). Taken together, experiments I and II shed light on whether the presence of the parents increases or reduces the risk of predation at a solitary fieldfare nest . In relation to nest predators, the parents have at least two potential effects : (a) their presence may direct the attention of predators to the nest area ; (b) by mobbing, they may chase away searching predators . Depending on the relative importance of these effects, the parents may increase or decrease the risk of nest predation . Due to their efficient anti-predator attacks one would expect the parent fieldfares to reduce the risk of predation . If so, solitary artificial nests (experiment I) should be more vulnerable than artificial nests near solitary fieldfare pairs (experiment II) . Predation turns out to be higher on solitary artificial nests (P = 0 . 03 ; Fig . 5), so the presence of a solitary fieldfare pair tends to reduce the risk of predation on the artificial nests .
solitary nests
Discussion Predation at artificial nests was (a) higher on colonial than on solitary nests away from fieldfares, (b) lower in presence than in absence of a
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Table I. Temporal Sequence of Predation in the Seven Colonies No . of nests plundered on day no .
0 1 2 3 4 5 6 day Fig. 2. The pattern of predation at `solitary' and `colonial' artificial nests in experiment I . (The colonial nest remaining on day 3 disappeared on day 4.) Predation is significantly higher at colonial nests. (The number of remaining nests in this and the following figures is given on a log scale. A constant risk of predation therefore would result in a straight line in the absence of stochastic influences .)
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solitary fieldfare pair, (c) higher near solitary fieldfare pairs than near fieldfare colonies and (d) probably also higher on peripheral than on central nests at fieldfare colonies . To what degree do these results apply for real fieldfare nests? No comparison of the risks of predation on solitary and colonial fieldfare nests has been published. In a Lapland birch forest a total of seven solitary fieldfare nests during 1971 to 1977 produced no fledglings, whereas 431 colonial nests produced on average roughly 1 . 7 fledglings per nest (Wiklund, in preparation) . A higher risk of predation for solitary nests therefore seems to apply for real fieldfare nests as well, but further studies are needed. The risk of predation certainly differs quantitatively between artificial nests and fieldfare nests, because they differ in structure and location (page 1208), and because the fieldfares defend their nests, whereas artificial nests are protected only indirectly due to their proximity to real nests. However, qualitative differences in the
risk of predation between categories of artificial nests are more likely to be representative for the corresponding fieldfare nests . The activities of the parents may give away the position of the nest and increase the risk of nest predation (Horn 1968). The opposite effect
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Fig. 4. The pattern of predation at artificial nests near solitary fieldfare pairs, and 'inside' and 'outside' fieldfare colonies (experiment II) . Predation is significantly higher at nests near solitary fieldfare pairs than at either of the two categories of colonial nests .
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, Fig . 3 . Arrangement of the four artificial nests at one of the fieldfare colonies in experiment II. The colony has been delimited by the dotted convex polygon joining or including the fieldfare nests. Distances in metres.
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day Fig . 5 . The pattern of predation at artificial nests near solitary fieldfare pairs, and away from fieldfares . Predation is significantly lower at nests near fieldfare pairs .
ANDERSSON & WIKLUND : NEST PREDATION IN FIELDFARES
of fieldfare pairs probably is a consequence of their efficient (alas) defaecation attacks (Hohlt 1957 ; Furrer 1975 ; Mester 1976), which may destroy the water-deterrent capacity of the predator's plumage and thereby even kill large birds such as buzzards (Bezzel 1975) . This remarkable defence ability is probably a key factor favouring breeding in colonies, as done by the majority of fieldfare pairs (Hohlt 1957 ; Liibcke 1975 ; and this study) . Combined attacks from many birds should increase their defence efficiency, which may explain why the risk of nest predation is lower at fieldfare colonies than at solitary pairs, and probably lower for central than for peripheral colony nests . Another possible explanation (pointed out to us by J. Krebs) is that fieldfares might tend to form colonies in protected border areas between predator territories (compare Mech 1977) . However, we have found several fieldfare colonies, including the largest one of the present study, containing an active nest of hooded crow within its borders . Yet crows start breeding earlier than fieldfares, so this seems an unlikely explanation. The risk of predation has been studied for different prey spacing patterns . Tinbergen et al. (1967) showed that after a crow had located a group of experimental eggs, the risk of predation increased with their density, probably due to `area-concentrated search' (Smith 1974) by the predator . Croze (1970) generalized this result, showing that predation on artificial larvae was greater in crowded than in scattered populations . For artificial birds' nests at low densities on the ground, Gdransson et al . (1975) found that predation increased with nest density . Smith (1974) showed how foraging blackbirds (T . merula), upon prey capture, changed move lengths, angles of turn and overall speed of movement so that they tended to remain near the previous capture point . This supports the idea of Tinbergen et al . (1967) about areaconcentrated predator search . Similar predator behaviour may have caused the temporal clumping of predation in experiment I, which showed that scattered artificial nests in forests run a lower risk of predation than clumped nests at densities similar to that in fieldfare colonies . The result therefore expands the range of situations (reviewed by Curio 1976) where spacing out has been shown to reduce predation on prey whose main defence is to avoid detection. In gull colonies, reduced predator success was associated with increased anti-predator attack frequency (Kruuk 1964) and number of defen-
1 21 1
ding gulls (Andersson 1976) . Breeding success was lowest for peripheral, and highest for central pairs in a blackheaded gull (Larus ridibundus) colony, probably partly due to superior defence inside it (Patterson 1965) . Kruuk (1964) showed that egg predation was lower within than outside the colony . Fuchs (1977) and Veen (1977) found that eggs were more vulnerable on the fringe of, or outside, sandwich tern (Sterna sandvicensis) colonies than inside them. In the bank swallows (Riparia riparia), predation on experimentally exposed young was lower close to the nests at the bank face than away from it (Hoogland & Sherman 1976) . Lower predation on central than on peripheral colony nests has been recorded in several other species (review in Hoogland & Sherman 1976) . The present results point to similar conclusions for fieldfares . Efficient anti-predator defence by colonial fieldfares might even improve the breeding success of other species nesting nearby . Merlins (Falco columbarius) produced more young when nesting near fieldfare colonies (Wiklund,1979. This was probably a consequence of reduced nest predation, not of improved food supply, because merlins rarely took fieldfares . On the other hand, the breeding success of jackdaws (Corvus monedula) nesting near a fieldfare colony was reduced, probably because they were treated as nest predators, and were harassed when attempting to feed the young (Hdgstedt 1977). Gdransson et al . (1975) demonstrated a reduced risk of predation at artificial nests near breeding lapwings (Vanellus vanellus), another species with efficient anti-predator defence . To conclude, communal anti-predator attacks seem to be an important means of reducing nest predation in many colonial bird species . An aberrant case, where colonial breeding seems not to reduce predation, was described by Lemmetyinen (1971) . Several hypotheses (reviewed in Wilson 1975) have been raised on the relative advantages of solitary versus colonial breeding, but experimental comparisons of solitary and colonial members of the same species have been lacking . Experiment II showed that the risk of predation is markedly higher for artificial nests near solitary fieldfare pairs than near colonies ; this probably applies for real fieldfare nests as well . The result therefore demonstrated one out of several possible advantages of colonial over solitary breeding. Yet some fieldfare pairs breed solitarily, so colonial breeding may not be as superior as suggested by our experiment, which
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ANIMAL BEHAVIOUR, 26, 4
concerned egg predation only . Nesting fieldfares are subject to other kinds of predation as well . We found remains of five adult fieldfares taken by predators on colony nests, a kind of predation also recorded by Hohlt (1957) and Liibcke (1975) . Perhaps adult and/or nestling predation is higher in the conspicuous colonies than at solitary nests. Another possibility is that an exceptionally good, defendable feeding area might induce a pair to breed solitarily and defend a feeding territory (compare Brown 1964) . In examining the relative advantages of solitary versus colonial breeding in fieldfares, food and foraging need to be studied in addition to predation . Until this has been done, it is not clear whether colonial breeding in fieldfares is mainly a defence mechanism, or whether it also enhances foraging. Acknowledgments We thank Jan Ekman, Anders Enemar and Duncan MacSwain for helpful discussions and suggestions, Bo Eriksson, Olle Nerman, Arne Ran and Bjorn Rosander for statistical advice, Hans Nyma .n for help in making the artificial nests, and Aino Wahlstrom for drawing the figures . REFERENCES Andersson, M . 1976 . Predation and kleptoparasitism by skuas in a Shetland seabird colony. Ibis, 118, 208217. Bezzel, E. 1975 . Die Wirksamkeit der Kotattacken der Wacholderdrossel (Turdus pilaris) auf Greifvogel . J. Orn., 116, 488-489 . Brown, J . L. 1964 . The evolution of diversity in avian territorial systems . Wilson Bull., 76, 160-169. Croze, H. 1970 . Searching image in carrion crows . Z. Tierpsychol., Beih . 5, 1-85. Curio, E . 1976. The Ethology of Predation . Berlin Springer . Dunn, E . 1977 . Predation by weasels (Mustela nivalis) on breeding tits (Parus spp .) in relation to the density of tits and rodents . J. Anim . Ecol., 46, 634-652. Fretwell, S. D . 1972. Populations in a Seasonal Environment. Princeton : Princeton University Press . Fuchs, E . 1977. Predation and anti-predator behaviour in a mixed colony of terns Sterna sp. and blackheaded gulls Larus ridibundus with special reference to the sandwich tern Sterna sandvicensis . Ornis Scand., 8, 17-32 . Furrer, R. K . 1975 . Haufigkeit and Wirksamkeit des Angriffsverhaltens bei der Wacholderdrossel Turdus pilaris . Orn . Beob., 72, 1-8 . Goransson, G., Karlsson, J ., Nilsson, S . G. & Ulfstrand, S . 1975 . Predation on bird's nests in relation to antipredator aggression and nest density : an experimental study . Oikos, 26,117-120.
Hogstedt, G . 1977 . Aggressiva bjorktrastar reducerar hiickningsutfallet for kaja . Anser, 16, 143-145 . Hoh1t, H . 1957. Studien an einer suddeutschen Population der Wacholderdrossel (Turdus pilaris L .) . J. Orn ., 98, 71-118 . Hoogland, J. L . & Sherman, P . L. 1976. Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr., 46, 33-58 . Horn, H . 1968 . The adaptive significance of colonial nesting in the Brewer's blackbird (Euphagus cyanocephalus). Ecology, 49, 682-694. Krebs, J . R. 1971 . Territory and breeding density in the great tit, Parus major L . Ecology, 52, 2-22 . Kruuk, H. 1964. Predators and anti-predator behaviour of the black headed gull (Larus ridibundus L.). Behaviour, Suppl. 11, 1-129. Lack, D . 1968. Ecological Adaptations for Breeding in Birds. London : Methuen . Lemmetyinen, R. 1971 . Nest defence behaviour of common and arctic terns and its effects on the success achieved by predators . Ornis Fenn ., 48,13-24 . Lbbcke, W . 1975. Zur Okologie and Brutbiologie der Wacholderdrossel (Turdus pilaris). J. Orn., 116, 281-296 . Mech, L. D. 1977 . Wolf-pack buffer zones as prey reservoirs . Science, 198, 320-321 . Mester, H. 1976. Defensive Defakation in der Vogelwelt . Orn . Beob., 73, 99-108 . Montevecchi, W . M . 1976 . Field experiments on the adaptive significance of avian eggshell pigmentation. Behaviour, 58, 26-39. Oden, A . & Wedel, H . 1975 . Arguments for Fisher's permutation Test . Ann . Statist., 3, 518-520 . Patterson, I . J . 1965. Timing and spacing of broods in the black-headed gull Larus ridibundus. Ibis, 107, 433459. Ricklefs, R. E . 1969 . An analysis of nesting mortality in birds . Smithsonian Contributions to Zoology, 9, 1-48 . Smith, J. N . M . 1974 . The food searching behaviour of two European thrushes . R. The adaptiveness of the search patterns. Behaviour, 49, 1-61 . Taylor, J. R. 1976. The advantage of spacing out . J. theor. Biol., 59, 485-490. Tinbergen, N., Impekoven, M. & Franck, D. 1967. An experiment on spacing-out as a defence against predation. Behaviour, 28, 307-321 . Treisman, M . 1975 . Predation and the evolution of gregariousness. I . Models for concealment and evasion. Anim . Behav ., 23, 779-800. Veen, J. 1977 . Functional and causal aspects of nest distribution in colonies of the sandwich tern (Sterna s. sandvicensis Lath.) Behaviour ; Suppl. 20, 1-93 . Wiklund, C. G . 1979 . Increased breeding success in merlins nesting in fieldfare colonies. Ibis 121, in press . Wilson, E. O . 1975 . Sociobiology . Cambridge, Mass . : Belknap Press of Harvard University Press . (Received 7 December 1977 ; revised 13 February 1978; MS. number : 1696)
CLUMPING VERSUS SPACING OUT : EXPERIMENTS ON NEST PREDATION IN FIELDFARES (TURDUS PILARIS) BY MALTE ANDERSSON & CHRISTER G . WIKLUND Department of Zoology, University of Gothenburg, 400 33 Gothenburg 33, Sweden
Abstract. Fieldfares (Turdus pilaris), which nest solitarily as well as in colonies, offer an opportunity to assess within one species the relative advantages of clumping versus spacing out . An experiment with artificial, egg-baited nests showed that predation in the absence of fieldfares was higher on clumped than on scattered nests. In another experiment, we tested whether artificial nests run a higher risk of predation near solitary fieldfare pairs than near fieldfare colonies . Nest predation was higher near solitary fieldfare pairs than outside and inside fieldfare colonies. The risk probably was higher outside than inside colonies . Communal antipredator attacks is the likely cause of reduced predation near colonies . Even solitary fieldfare pairs confer some degree of protection, because predation was lower at artificial nests near solitary fieldfare pairs than at nests without neighbouring fieldfares . Predation is one of the most important selective pressures influencing the optimal spacing pattern in a population . For cryptic prey in open habitats, Tinbergen et al . (1967), Croze (1970) and Goransson et al . (1975) showed experimentally that predation by corvids and larids increased with the local prey density . 'Areaconcentrated search' (Smith 1974) by the predator after prey capture seemed to be the cause . Krebs (1971) and Dunn (1977) found a positive correlation between predation and nest density in great tits (Parus major), as did Fretwell (1972) in field sparrows (Spizella pusilla) . Predation therefore seems to favour spacing out in prey whose main defence is to avoid detection . A theoretical model by Taylor (1976) gave the same prediction. Treisman (1975) reviewed and developed models for the evolution of gregariousness in response to predation . In species with communal anti-predator attacks, the defence efficiency may increase with the number of defenders (Kruuk 1964 ; Andersson 1976), which favours higher local prey densities . The dispersion pattern optimal with respect to avoiding predation in uniform habitats therefore should tend towards well spaced, `solitary' individuals in vulnerable species, and towards clumped `colonies' in species with efficient communal defence. Other selective pressures, in particular on foraging efficiency, may obscure such a trend and make it visible only among species differing in defence strategy while having similar ecology in other respects . Nest predation was the major nesting mortality factor in the bird species treated by Ricklefs (1969). Probably partly as a consequence
of heavy predator pressure, the open, accessible nests of many forest-breeding passerine birds are well spaced and hidden by strategic positioning and cryptical structure (Lack 1968) . Among European species, the fieldfare is an exception . It usually breeds in colonies of 5 to 20 pairs (e.g. Hohlt 1957 ; Lubcke 1975), and the nest appears more conspicuous than in other species, including Turdidae . In the similarly sized North American Brewer's blackbird (Euphagus cyanocephalus), colonial breeding improves the foraging efficiency, whereas the anti-predatory effect seems to vary with the shape of the colony (Horn 1968) . In fieldfares, colonial breeding might reduce predation, because colony members deter approaching predators by communal attacks (Bezzel 1975 ; Furrer 1975 ; Mester 1976) . On the other hand, in the presence of predators using `area-concentrated search', clumping might increase the risk of nest detection, and the net effect is hard to predict . This study, which focuses on the egg stage of the breeding cycle, examines (a) whether the higher risk of predation in clumped rather than in scattered prey populations, previously demonstrated in open habitats, also applies in a structurally more complex forest habitat ; and (b) if, in spite of this, fieldfares can reduce nest predation by breeding in colonies. Experiment I Methods The first experiment tests whether artificial birds' nests in trees run a higher risk of predation when clumped than when scattered . We used two groups of nests : (Ia) 20 `solitary' nests, 1207
ANIMAL BEHAVIOUR, 26, 4
1 20 8
each several 100 m from the nearest artificial nest or fieldfare nest ; (Ib) 49 `colonial' nests, distributed in seven hexagonal colonies (Fig. 1), each with seven nests 20m apart, a spacing similar to that in fieldfare colonies . To avoid systematic differences in location, we selected 27 places in fieldfare breeding habitat, and allocated the colonies and solitary nests among these places by drawing random numbers . The artificial nests, 15 cm in diameter, 5 cm high, and made of dry grass, were stabilized and attached with thin iron wire to the base of a branch 4 to 6 m above the ground . This is within the height range of fieldfare nests, but lower than their average . The artificial nests were about half as voluminous as fieldfare nests and less conspicuous, differences which should not be important because our tests will be based on comparisons between nests of identical structure . Each nest was baited with two japanese quail (Coturnix c . Japonica) eggs with length x width about 33 x 26 mm, 10 % larger values than for fieldfare eggs . Quail eggs like fieldfare eggs are cryptically coloured, although with larger and darker patches (see Montevecchi 1976). All experiments were performed during the same period in a mosaic of mainly deciduous forest (dominated by oak, Quercus robur) and suburban areas E and SE of Gothenburg, SW Sweden . The nests were placed in position on 11 May 1977 (experiment II) and 12 May (experiment I), when most fieldfare pairs had started or finished laying, whereas hatching had not begun . Deciduous trees were bare, but birches (Betula pubescens and B. verrucosa), the 40
0
Fig. 1 . Hexagonal arrangement of the seven artificial nests in one of the seven `colonies' of experiment I .
earliest species, had half-grown leaves at the end of experiments one week later . A mirror on a 5-m rod was used to inspect each artificial nest for a few seconds . The risk of attracting predators during these daily short visits was probably low. Potential nest predators were crows (Corvus corone cornix), magpies (Pica pica), jays (Garrulus glandarius), woodpeckers (Dendrocopos major), squirrels (Sciurus vulgaris) and small mustelids. Our tests of differences in the risk of predation at different nest categories are based on the survival time of each individual nest . Nests which still survived on the day of last inspection (day n) were designated a survival time of n+ 1 days . Differences between groups are examined with Fisher's permutation test, which has optimum properties (Od6n & Wedel 1975) . Because the direction of the predicted effects can be specified, we use one-tailed tests. A nest with two eggs can be defined as predated either when the first egg has disappeared or when both have been taken . The present results are based on the former definition, but since the two eggs of a nest usually disappeared on the same day, the second definition gives almost identical results. The possibility of demonstrating differences in the risk of predation for different prey categories is highly dependent on the procedure used in recording predation (Montevecchi 1976) . Because the present method employs the survival time of each nest, it should usually be more efficient than tests based on one final inspection of the prey population . Result The predation pattern in the two groups of nests is shown in Fig . 2. The risk of predation was significantly higher for colonial nests (P = 0. 0098), as indicated by the steeper slope of the corresponding cumulative distribution . All eggs in the 49 colonial nests disappeared within four days, whereas the eggs in three of the 20 solitary nests remained after six days . Closer examination of the temporal sequence of predation at colonial nests offers additional information (Table I). The nests within a colony tended to become plundered in close temporal proximity, and in five of the seven colonies, the eggs disappeared from all nests on the same day . Experiment II Methods This experiment tests if the risk of predation is (1) lower at central than at peripheral arti-
ANDERSSON & WIKLUND : NEST PREDATION IN FIELDFARES
ficial nests in a fieldfare colony, and (2) lower at peripheral and/or central colony nests than at nests near solitary fieldfare pairs . There seems to be a gradual transition between solitary and colonial breeding in fieldfares, most colonies containing 5 to 20 clumped nests with 10 to 40 m nearest neighbour distances, sometimes with a few nests farther away . Before the experiment, we arbitrarily assigned all nests with nearest neighbour distance greater than 75 m as solitary (our previous observations indicated that the efficiency of communal defence with larger distances is small), and the remainder as colonial . The experimental groups included : (Ila) 23 nests, each 20 m from a solitary fieldfare pair ; (IIb) 28 `peripheral' nests, each 20 m from the nearest nest in a fieldfare colony, and outside the convex polygon joining or including the nests of the colony (Fig . 3) ; (Ilc) 28 `central' nests, each 20 m from the nearest nest in a fieldfare colony, and inside the convex polygon of the colony . The artificial nests in groups lib and Hc were placed in 14 fieldfare colonies, two nests of each category per colony . In other
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respects they were constructed, baited, located and treated as in experiment I . The fieldfare colonies had an average size of 8 .1 nests (ss _ 0-28) . Result The result of experiment II is summarized in the cumulative distributions of Fig. 4. The risk of predation was significantly lower for both central and peripheral artificial nests at fieldfare colonies than for nests near solitary fieldfare pairs (P = 0.0003 and P = 0 . 038 respectively) . As predicted for a species with communal defence, the risk was lower for central than for peripheral nests, but the difference is not quite significant (P = 0 . 053). Taken together, experiments I and II shed light on whether the presence of the parents increases or reduces the risk of predation at a solitary fieldfare nest . In relation to nest predators, the parents have at least two potential effects : (a) their presence may direct the attention of predators to the nest area ; (b) by mobbing, they may chase away searching predators . Depending on the relative importance of these effects, the parents may increase or decrease the risk of nest predation . Due to their efficient anti-predator attacks one would expect the parent fieldfares to reduce the risk of predation . If so, solitary artificial nests (experiment I) should be more vulnerable than artificial nests near solitary fieldfare pairs (experiment II) . Predation turns out to be higher on solitary artificial nests (P = 0 . 03 ; Fig . 5), so the presence of a solitary fieldfare pair tends to reduce the risk of predation on the artificial nests .
solitary nests
Discussion Predation at artificial nests was (a) higher on colonial than on solitary nests away from fieldfares, (b) lower in presence than in absence of a
colonial nests
Table I. Temporal Sequence of Predation in the Seven Colonies No . of nests plundered on day no .
0 1 2 3 4 5 6 day Fig. 2. The pattern of predation at `solitary' and `colonial' artificial nests in experiment I . (The colonial nest remaining on day 3 disappeared on day 4.) Predation is significantly higher at colonial nests. (The number of remaining nests in this and the following figures is given on a log scale. A constant risk of predation therefore would result in a straight line in the absence of stochastic influences .)
Colony 1 2 3 4 5 6 7
1
2
3
4
7 1
5
1
7 7 7 7 2
5
1 210
ANIMAL BEHAVIOUR, 26, 4
solitary fieldfare pair, (c) higher near solitary fieldfare pairs than near fieldfare colonies and (d) probably also higher on peripheral than on central nests at fieldfare colonies . To what degree do these results apply for real fieldfare nests? No comparison of the risks of predation on solitary and colonial fieldfare nests has been published. In a Lapland birch forest a total of seven solitary fieldfare nests during 1971 to 1977 produced no fledglings, whereas 431 colonial nests produced on average roughly 1 . 7 fledglings per nest (Wiklund, in preparation) . A higher risk of predation for solitary nests therefore seems to apply for real fieldfare nests as well, but further studies are needed. The risk of predation certainly differs quantitatively between artificial nests and fieldfare nests, because they differ in structure and location (page 1208), and because the fieldfares defend their nests, whereas artificial nests are protected only indirectly due to their proximity to real nests. However, qualitative differences in the
risk of predation between categories of artificial nests are more likely to be representative for the corresponding fieldfare nests . The activities of the parents may give away the position of the nest and increase the risk of nest predation (Horn 1968). The opposite effect
30
W
V
o~
20
c
0
nests outside fieldfare Co ornes
E
c
10 nests near solitary fieldforre
v
rs
E C
5 0 1 2 3 4 5 6 7
day P
20
• C P
fieldfare nest central nest peripheral nest
.•
Fig. 4. The pattern of predation at artificial nests near solitary fieldfare pairs, and 'inside' and 'outside' fieldfare colonies (experiment II) . Predation is significantly higher at nests near solitary fieldfare pairs than at either of the two categories of colonial nests .
• 20 30
LA 20 W C
solitary nests near solitary fieldfare pairs
of
c
C .5
10 .40
5 20
E
solitary nests away from fieldfare pairs
V
C
3
, Fig . 3 . Arrangement of the four artificial nests at one of the fieldfare colonies in experiment II. The colony has been delimited by the dotted convex polygon joining or including the fieldfare nests. Distances in metres.
0 1 2 3 4 5 6 7
day Fig . 5 . The pattern of predation at artificial nests near solitary fieldfare pairs, and away from fieldfares . Predation is significantly lower at nests near fieldfare pairs .
ANDERSSON & WIKLUND : NEST PREDATION IN FIELDFARES
of fieldfare pairs probably is a consequence of their efficient (alas) defaecation attacks (Hohlt 1957 ; Furrer 1975 ; Mester 1976), which may destroy the water-deterrent capacity of the predator's plumage and thereby even kill large birds such as buzzards (Bezzel 1975) . This remarkable defence ability is probably a key factor favouring breeding in colonies, as done by the majority of fieldfare pairs (Hohlt 1957 ; Liibcke 1975 ; and this study) . Combined attacks from many birds should increase their defence efficiency, which may explain why the risk of nest predation is lower at fieldfare colonies than at solitary pairs, and probably lower for central than for peripheral colony nests . Another possible explanation (pointed out to us by J. Krebs) is that fieldfares might tend to form colonies in protected border areas between predator territories (compare Mech 1977) . However, we have found several fieldfare colonies, including the largest one of the present study, containing an active nest of hooded crow within its borders . Yet crows start breeding earlier than fieldfares, so this seems an unlikely explanation. The risk of predation has been studied for different prey spacing patterns . Tinbergen et al. (1967) showed that after a crow had located a group of experimental eggs, the risk of predation increased with their density, probably due to `area-concentrated search' (Smith 1974) by the predator . Croze (1970) generalized this result, showing that predation on artificial larvae was greater in crowded than in scattered populations . For artificial birds' nests at low densities on the ground, Gdransson et al . (1975) found that predation increased with nest density . Smith (1974) showed how foraging blackbirds (T . merula), upon prey capture, changed move lengths, angles of turn and overall speed of movement so that they tended to remain near the previous capture point . This supports the idea of Tinbergen et al . (1967) about areaconcentrated predator search . Similar predator behaviour may have caused the temporal clumping of predation in experiment I, which showed that scattered artificial nests in forests run a lower risk of predation than clumped nests at densities similar to that in fieldfare colonies . The result therefore expands the range of situations (reviewed by Curio 1976) where spacing out has been shown to reduce predation on prey whose main defence is to avoid detection. In gull colonies, reduced predator success was associated with increased anti-predator attack frequency (Kruuk 1964) and number of defen-
1 21 1
ding gulls (Andersson 1976) . Breeding success was lowest for peripheral, and highest for central pairs in a blackheaded gull (Larus ridibundus) colony, probably partly due to superior defence inside it (Patterson 1965) . Kruuk (1964) showed that egg predation was lower within than outside the colony . Fuchs (1977) and Veen (1977) found that eggs were more vulnerable on the fringe of, or outside, sandwich tern (Sterna sandvicensis) colonies than inside them. In the bank swallows (Riparia riparia), predation on experimentally exposed young was lower close to the nests at the bank face than away from it (Hoogland & Sherman 1976) . Lower predation on central than on peripheral colony nests has been recorded in several other species (review in Hoogland & Sherman 1976) . The present results point to similar conclusions for fieldfares . Efficient anti-predator defence by colonial fieldfares might even improve the breeding success of other species nesting nearby . Merlins (Falco columbarius) produced more young when nesting near fieldfare colonies (Wiklund,1979. This was probably a consequence of reduced nest predation, not of improved food supply, because merlins rarely took fieldfares . On the other hand, the breeding success of jackdaws (Corvus monedula) nesting near a fieldfare colony was reduced, probably because they were treated as nest predators, and were harassed when attempting to feed the young (Hdgstedt 1977). Gdransson et al . (1975) demonstrated a reduced risk of predation at artificial nests near breeding lapwings (Vanellus vanellus), another species with efficient anti-predator defence . To conclude, communal anti-predator attacks seem to be an important means of reducing nest predation in many colonial bird species . An aberrant case, where colonial breeding seems not to reduce predation, was described by Lemmetyinen (1971) . Several hypotheses (reviewed in Wilson 1975) have been raised on the relative advantages of solitary versus colonial breeding, but experimental comparisons of solitary and colonial members of the same species have been lacking . Experiment II showed that the risk of predation is markedly higher for artificial nests near solitary fieldfare pairs than near colonies ; this probably applies for real fieldfare nests as well . The result therefore demonstrated one out of several possible advantages of colonial over solitary breeding. Yet some fieldfare pairs breed solitarily, so colonial breeding may not be as superior as suggested by our experiment, which
1 21 2
ANIMAL BEHAVIOUR, 26, 4
concerned egg predation only . Nesting fieldfares are subject to other kinds of predation as well . We found remains of five adult fieldfares taken by predators on colony nests, a kind of predation also recorded by Hohlt (1957) and Liibcke (1975) . Perhaps adult and/or nestling predation is higher in the conspicuous colonies than at solitary nests. Another possibility is that an exceptionally good, defendable feeding area might induce a pair to breed solitarily and defend a feeding territory (compare Brown 1964) . In examining the relative advantages of solitary versus colonial breeding in fieldfares, food and foraging need to be studied in addition to predation . Until this has been done, it is not clear whether colonial breeding in fieldfares is mainly a defence mechanism, or whether it also enhances foraging. Acknowledgments We thank Jan Ekman, Anders Enemar and Duncan MacSwain for helpful discussions and suggestions, Bo Eriksson, Olle Nerman, Arne Ran and Bjorn Rosander for statistical advice, Hans Nyma .n for help in making the artificial nests, and Aino Wahlstrom for drawing the figures . REFERENCES Andersson, M . 1976 . Predation and kleptoparasitism by skuas in a Shetland seabird colony. Ibis, 118, 208217. Bezzel, E. 1975 . Die Wirksamkeit der Kotattacken der Wacholderdrossel (Turdus pilaris) auf Greifvogel . J. Orn., 116, 488-489 . Brown, J . L. 1964 . The evolution of diversity in avian territorial systems . Wilson Bull., 76, 160-169. Croze, H. 1970 . Searching image in carrion crows . Z. Tierpsychol., Beih . 5, 1-85. Curio, E . 1976. The Ethology of Predation . Berlin Springer . Dunn, E . 1977 . Predation by weasels (Mustela nivalis) on breeding tits (Parus spp .) in relation to the density of tits and rodents . J. Anim . Ecol., 46, 634-652. Fretwell, S. D . 1972. Populations in a Seasonal Environment. Princeton : Princeton University Press . Fuchs, E . 1977. Predation and anti-predator behaviour in a mixed colony of terns Sterna sp. and blackheaded gulls Larus ridibundus with special reference to the sandwich tern Sterna sandvicensis . Ornis Scand., 8, 17-32 . Furrer, R. K . 1975 . Haufigkeit and Wirksamkeit des Angriffsverhaltens bei der Wacholderdrossel Turdus pilaris . Orn . Beob., 72, 1-8 . Goransson, G., Karlsson, J ., Nilsson, S . G. & Ulfstrand, S . 1975 . Predation on bird's nests in relation to antipredator aggression and nest density : an experimental study . Oikos, 26,117-120.
Hogstedt, G . 1977 . Aggressiva bjorktrastar reducerar hiickningsutfallet for kaja . Anser, 16, 143-145 . Hoh1t, H . 1957. Studien an einer suddeutschen Population der Wacholderdrossel (Turdus pilaris L .) . J. Orn ., 98, 71-118 . Hoogland, J. L . & Sherman, P . L. 1976. Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr., 46, 33-58 . Horn, H . 1968 . The adaptive significance of colonial nesting in the Brewer's blackbird (Euphagus cyanocephalus). Ecology, 49, 682-694. Krebs, J . R. 1971 . Territory and breeding density in the great tit, Parus major L . Ecology, 52, 2-22 . Kruuk, H. 1964. Predators and anti-predator behaviour of the black headed gull (Larus ridibundus L.). Behaviour, Suppl. 11, 1-129. Lack, D . 1968. Ecological Adaptations for Breeding in Birds. London : Methuen . Lemmetyinen, R. 1971 . Nest defence behaviour of common and arctic terns and its effects on the success achieved by predators . Ornis Fenn ., 48,13-24 . Lbbcke, W . 1975. Zur Okologie and Brutbiologie der Wacholderdrossel (Turdus pilaris). J. Orn., 116, 281-296 . Mech, L. D. 1977 . Wolf-pack buffer zones as prey reservoirs . Science, 198, 320-321 . Mester, H. 1976. Defensive Defakation in der Vogelwelt . Orn . Beob., 73, 99-108 . Montevecchi, W . M . 1976 . Field experiments on the adaptive significance of avian eggshell pigmentation. Behaviour, 58, 26-39. Oden, A . & Wedel, H . 1975 . Arguments for Fisher's permutation Test . Ann . Statist., 3, 518-520 . Patterson, I . J . 1965. Timing and spacing of broods in the black-headed gull Larus ridibundus. Ibis, 107, 433459. Ricklefs, R. E . 1969 . An analysis of nesting mortality in birds . Smithsonian Contributions to Zoology, 9, 1-48 . Smith, J. N . M . 1974 . The food searching behaviour of two European thrushes . R. The adaptiveness of the search patterns. Behaviour, 49, 1-61 . Taylor, J. R. 1976. The advantage of spacing out . J. theor. Biol., 59, 485-490. Tinbergen, N., Impekoven, M. & Franck, D. 1967. An experiment on spacing-out as a defence against predation. Behaviour, 28, 307-321 . Treisman, M . 1975 . Predation and the evolution of gregariousness. I . Models for concealment and evasion. Anim . Behav ., 23, 779-800. Veen, J. 1977 . Functional and causal aspects of nest distribution in colonies of the sandwich tern (Sterna s. sandvicensis Lath.) Behaviour ; Suppl. 20, 1-93 . Wiklund, C. G . 1979 . Increased breeding success in merlins nesting in fieldfare colonies. Ibis 121, in press . Wilson, E. O . 1975 . Sociobiology . Cambridge, Mass . : Belknap Press of Harvard University Press . (Received 7 December 1977 ; revised 13 February 1978; MS. number : 1696)