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The effect of intraspecific competition on prey load size in the European starling, Sturnus vulgaris
Anim.Behav.,1995,49,261-264
The effect of intraspecificcompetition on prey load sizein the European starling, Sturnus vulgaris MARK
S. WITTER
School of Biological Sciences,University of Bristol, Woodland Road, Bristol BS8 I UG, UK. (Received 9 March 1994; initial acceptance 20 April 1994; final acceptance 19 August 1994: MS. number:sc-991)
Foraging in association with conspecifics entails both benefits and costs (see Pulliam & Caraco 1984). Benefits may include reduced predation risk (Hamilton 1971), through, for example, effects of dilution or predator confusion, or enhanced foraging success (Baker et al. 1981) through, for example, reduced search time. However, group foraging may also be costly because conspecifics compete for available resources (Caraco 1979), which may reduce foraging success through resource depletion or direct interference with foraging attempts. Cuthill & Kacelnik (1990) found that parental starlings took significantly lower load sizes from artificial patches of food, during central place foraging (Orians & Pearson 1979), when conspecifics were present than when the individuals foraged alone. Here, I examine experimentally the proposition that foraging starlings reduce the size of prey loads carried to the nest when feeding in the presence of increased numbers of conspecifics.Proximity of conspecifics was manipulated by altering the distribution of food resources in a patch. I also examine whether the effect of increased numbers of conspecifics acts through increased rates of aggression and/or interruption during foraging. I performed the experiment during May 1992, at a nestbox colony at Stock Lane Farm, Langford, Avon, U.K. (see Witter 1993). Nestboxeswere positioned on the outside walls of farm shedsand hen houses, approximately 1.5 m apart. In 1992, three pairs of starlings were nesting at the farm. Food was presented in three arrays, approximately 1.5 m away from a hedge along the edge of an open field directly in front of, and along a line perpendicular to, the buildings with nestboxes. I manipulated competition for food by altering the distance between four feeding trays (0.1 x O-1x 0.1 m), filled with mealworms (Tenebrio larvae), presented on a wooden board of 1 x 1 m. Feeding trays were filled regularly, with mealworms constantly superabundant, so the
birds would not experience patch depletion wl foraging. In the low- and high-competition tre ments, I placed the feeding trays at the corners centre of the board, respectively. I presented two treatments alternately at distances of 15, and 35 m from the nest; the treatment to presented first was determined by a coin toss. 1 order of the distance treatments was randomiz I repeated this procedure until three presentatic of each competition treatment had been p formed at each distance. I carried out the exp iment over 4 consecutive days, between 0800 a 1400 hours. I observed feeding behaviour at 1 patch through binoculars from inside a hide p’ itioned approximately 15 m away. A vidc camera, also located in the hide, was positioned film the presentation board and approximatj 0.5 m around its perimeter. Observations invoh noting the bird’s identity (from colour rings) a the number of mealworms present in the bill ac left the patch. These observations were record onto the video sound-track. I used the vidc recordings to determine the following three va ables. (1) The number of conspecificswithin 0.1 of the focal bird (measured from head to hes when it left the patch, which was used as measure of the number of ‘competitors’ present. distance of 0.1 m was chosen as the cut-l because observations indicated that direct into actions took place over this distance. Furthc more, using this short distance reduced t likelihood that birds would be counted ‘competitors’ where one or more birds wz present between such birds and the focal in vidual, as would occur if larger distances wz used. (2) The mean rate of aggressive interactio (interactions/min) made by all foraging birds each patch presentation. (3) The mean rate which all foraging birds left the feeding tr following an aggressive interaction but return to continue foraging before flying back to t nest; this was used as a measure of foragi
Animal Behaviour, 49, 1
262
Table I. Analysis of the effects of food dispersal(Patch) and nest-patchdistance
(Distance)on number of competitorsand load size Variable
Factor
4”
F
P
Competitors
Patch Distance Patch*Distance Patch Distance Patch*Distance
1, 3 2, 6 2, 6 1, 3 2, 6 2, 6
120.71 1.62 0.25 97.50 66.89 0.59
Load size
interruptions (interruptions/mm). The mean f SE number of birds in the field of view of the camera when load-size observations were taken was 5.2 4~0.181 (range: 1-19). The maximum number of ringed birds in the field of view at any one time was three. Thus, during the vast majority of observations, most of the ‘competitors’ were nonringed starlings (approximately 40 birds), from the surrounding areas, which regularly visited the feeding trays. Four ringed birds (two males and two females) of the six breeding at the farm visited all the treatments at all distances. The number of visits by each bird to each presentation varied between five and 19, with a total of 257 patch visits recorded. I analysed the effects of patch distance and food dispersal on number of conspecifics present around the focal birds when they left the patch and prey load sixesby a multivariate mixed-model repeated-measures analysis of variance, using MANOVA on SPSS(Hand & Taylor 1987; SPSS 1988). Patch distance (Distance) and food dispersal (Patch) are treated as fixed effects, and Bird (the focal individual) is treated as a random effect (Hand & Taylor 1987). Patterns of change with distance were investigated using orthogonal poiynomial contrasts (Hand & Taylor 1987; SPSS 1988). The three replicates at each site did not differ in either load sizeor number of competitors present (ANOVA with factors distance, patch and replicate, performed separately for each bird; load size,fi62-7o ~2.14, P>O.124, in all cases;competitors, F2,62-7o~1.08, P20.346, in all cases), so I treat all replicates together for the main analysis. Time of day also had no significant effect on load size or number of competitors, at least while observations were taken, so is not considered further in the analysis (ANOVA with factors distance and patch, and covariate time of day, performed separately for each bird: load size,
0.273 0.786 0.002
F i 62-,0<2.08, P>O.l 11, in all cases;competitors, F ,‘62M,2~1.50,P>O.262, in all cases). The resolution of the video-recordings was not sufficient to be able to identify individuals while foraging. Thus, rates of aggression and interruption could not be assigned to individuals. This potentially introduces pseudoreplication (Hurlbert 1984) into the design, because individuals may be repeatedly sampled. As a conservative measure to reduce this effect, I treat the mean value for each patch presentation as an independent datum, rather than individual acts of aggression and interruption. The manipulation of food dispersal altered the number of birds feeding near to the focal individuals; more conspecifics were in close proximity when the food trays were clumped, than when they were dispersed (clumped patch manipulation, 3.033 f 0.234; dispersed patch manipulation, 1.219 & 0.186; Table I). This indicates that the manipulation successfullyaltered the proximity of conspecifics. However, the total number of birds using the system did not differ with the patch manipulation (total number of birds present for the clumped patch manipulation: 5088 & 0.199; and dispersed patch manipulation: 5.248 +Z0.315; F 1,256=O64, P=O.424). Birds took larger load sizesthe further they were from their nests (Fig. 1, Table I). Over the range of distances investigated, load size increased at a decelerating rate with nest-patch distance (polynomial contrast for Distance, linear term, t= 11.284, P
Short Communications or 0
1
760) 5-_ .2 1 43 32lO-
=l
-Ll 15
x5
Patch distance (m) Figure1. Mean ( +SE) number of mealwormstaken at eachof the four nest-patchdistances,in the low competition (0) and high competition ( n ) treatment groups. From left to right, values are based and 38 patch visits, by four birds.
on 46, 36, 49,47,41
(Cuthill & Kacelnik 1990; Witter & Cuthill 1993). Dispersalof food within the patch also influenced load size; birds took significantly smaller loads from the patches where food was clumped (Fig. 1, Table I). Since both numbers of conspecifics present and load size were influenced by the manipulations, it is important to examine the effectson load size when numbers of conspecifics present are controlled for. In this case, load sizestill increased with increasing nest-patch distance (Roy-Bargman step-down F-test: Distance, F2,5=109.74, P
2(
6.09 f 0.740; ANOVA, with factors Distan and Patch; Patch, F,,,,=3.16, P=O.lOl; Distant F 2,,7=2.65, P=O.lll; Patch*Distance, F2,,, 1.50, P=O.262). There was a stronger indicatic that birds suffered more interruptions while fora ing in the high-competition treatment, althoug the difference is not quite significant (interruptior min, low competition, 2967 f 0.291; high camp tition, 3.00 f 0.436; Patch, F,,,,=4*03, PzO.06 Distance, F,,,,=O.20, P=O+322; Patch*Distanc Fz,,,=0.38, P=O.694). Although these trends are suggestive, it seer unlikely that these effects alone can account f the large changes in load size observed betwec patch treatments. However, even without dire aggression or overt interruptions, the presence conspecificsmay incur ‘attention costs’ (Cuthill Kacelnik 1990). That is, rate of prey gain may lowered simply because individuals have the attention to foraging distracted by the presence conspecifics. Changes in the number and proxii ity of conspecifics may also alter anti-predato strategies of the birds (Pulliam & Caraco 198~ However, changes in anti-predatory behavior such as reduced vigilance, appear unlikely explain the reduction of load size with increasi numbers of conspecifics. If foraging with co specifics reduces the risk of predation then bir may have been less vigilant and devoted mc time or attention to foraging; this may hd increased the load sizecarried to the nest, depen ing upon the specific shape of the gain functic An alternative possibility is that foraging ve close to conspecifics increases predation ri because more time or attention has to be allocat to monitoring nearby birds, with less attenti paid to predatory attack (cf. Cuthill & Kacelr 1990). In summary, the results indicate that an expe mental increase in the level of competition feeding sites decreasesthe number of prey item which starlings carry back to the nest. This PI vides evidence for a causal role of proximity conspecifics in determining load sizesduring fc aging, as suggested by the correlational data Cuthill & Kacelnik (1990). There are seve mechanisms through which this effect might mediated, which cannot be unequivocally dist guished with the present data set. Howev through whatever mechanism competition is a ing, reduced load sizes will reduce the rate which parental birds are able to provision th
Animal
264
Behi wiour,
offspring, all else being equal. This may have direct fitness consequences to the bird experiencing high levels of competition. I thank Sasha Dal1 and John Swaddle for helpful discussions. I am particularly grateful to Robert Slotow for his detailed criticisms of this and a previous version of the manuscript. I was supported by a NERC Research studentship when the experiment was carried out, and by a NERC Research Fellowship when writing the paper.
REFERENCES Baker, M. C., Belcher, C. S., Deutsch, L. C., Sherman, G. L. & Thompson, D. B. 1981. Foraging success in junco flocks and the effects of social hierarchy. Anim. Behav., 29, 137-142. Caraco, T. 1979. Time budgeting and group size: a test of a theory. Ecology, 60, 6188627. Cuthill, I. C. & Kacelmk, A. 1990. Central place foraging: a reappraisal of the ‘loading effect’. Anim. Behav., 40, 1087-1101. Hamilton, W. D. 1971. Geometry for the selfish herd. J. theor. Biol., 31, 295-311.
49, 1
Hand, D. J. & Taylor, C. C. 1987. Multivariate of Variance and Repeated Approach for Behavioural
Measures: Scientists.
a
Analysis Practical
London: Chapman & Hall. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr., 54, 187-211. Orians, G. H. & Pearson, N. E. 1979. On the theory of central place foraging. In: Analysis of Ecological Systems (Ed. by D. J. Horn, R. D. Mitchel & G. R. Stairs), pp. 154-177. Columbus: Ohio State University Press. Pulliam, H. R. & Caraco, T. 1984. Living in groups: is there an optimal group size? In: Behavioural Ecology: an Evolutionary Approach. 2nd edn (Ed. by J. R. Krebs & N. B. Davies), pp. 122-147. Oxford: Blackwell Scientific Publications. SPSS. 1988. SPSSx User’s Guide. 3rd edn. Chicago: SPSS Inc. Stephens, D. W. & Krebs, J. R. 1986. Foraging Theory. Princeton, New Jersey: Princeton University Press. Tinbergen, J. M. 198 1. Foraging decisions in the starling (Sturnus vulgaris). Ardea, 69, l-67. Witter, M. S. 1993. The ecological costs of being fat. Ph.D. thesis, University of Bristol. Witter, M. S. & Cuthill, I. C. 1993. The ecological costs of avian fat storage. Phil. Trans. R. Sot., 340, 73-92.
The effect of intraspecificcompetition on prey load sizein the European starling, Sturnus vulgaris MARK
S. WITTER
School of Biological Sciences,University of Bristol, Woodland Road, Bristol BS8 I UG, UK. (Received 9 March 1994; initial acceptance 20 April 1994; final acceptance 19 August 1994: MS. number:sc-991)
Foraging in association with conspecifics entails both benefits and costs (see Pulliam & Caraco 1984). Benefits may include reduced predation risk (Hamilton 1971), through, for example, effects of dilution or predator confusion, or enhanced foraging success (Baker et al. 1981) through, for example, reduced search time. However, group foraging may also be costly because conspecifics compete for available resources (Caraco 1979), which may reduce foraging success through resource depletion or direct interference with foraging attempts. Cuthill & Kacelnik (1990) found that parental starlings took significantly lower load sizes from artificial patches of food, during central place foraging (Orians & Pearson 1979), when conspecifics were present than when the individuals foraged alone. Here, I examine experimentally the proposition that foraging starlings reduce the size of prey loads carried to the nest when feeding in the presence of increased numbers of conspecifics.Proximity of conspecifics was manipulated by altering the distribution of food resources in a patch. I also examine whether the effect of increased numbers of conspecifics acts through increased rates of aggression and/or interruption during foraging. I performed the experiment during May 1992, at a nestbox colony at Stock Lane Farm, Langford, Avon, U.K. (see Witter 1993). Nestboxeswere positioned on the outside walls of farm shedsand hen houses, approximately 1.5 m apart. In 1992, three pairs of starlings were nesting at the farm. Food was presented in three arrays, approximately 1.5 m away from a hedge along the edge of an open field directly in front of, and along a line perpendicular to, the buildings with nestboxes. I manipulated competition for food by altering the distance between four feeding trays (0.1 x O-1x 0.1 m), filled with mealworms (Tenebrio larvae), presented on a wooden board of 1 x 1 m. Feeding trays were filled regularly, with mealworms constantly superabundant, so the
birds would not experience patch depletion wl foraging. In the low- and high-competition tre ments, I placed the feeding trays at the corners centre of the board, respectively. I presented two treatments alternately at distances of 15, and 35 m from the nest; the treatment to presented first was determined by a coin toss. 1 order of the distance treatments was randomiz I repeated this procedure until three presentatic of each competition treatment had been p formed at each distance. I carried out the exp iment over 4 consecutive days, between 0800 a 1400 hours. I observed feeding behaviour at 1 patch through binoculars from inside a hide p’ itioned approximately 15 m away. A vidc camera, also located in the hide, was positioned film the presentation board and approximatj 0.5 m around its perimeter. Observations invoh noting the bird’s identity (from colour rings) a the number of mealworms present in the bill ac left the patch. These observations were record onto the video sound-track. I used the vidc recordings to determine the following three va ables. (1) The number of conspecificswithin 0.1 of the focal bird (measured from head to hes when it left the patch, which was used as measure of the number of ‘competitors’ present. distance of 0.1 m was chosen as the cut-l because observations indicated that direct into actions took place over this distance. Furthc more, using this short distance reduced t likelihood that birds would be counted ‘competitors’ where one or more birds wz present between such birds and the focal in vidual, as would occur if larger distances wz used. (2) The mean rate of aggressive interactio (interactions/min) made by all foraging birds each patch presentation. (3) The mean rate which all foraging birds left the feeding tr following an aggressive interaction but return to continue foraging before flying back to t nest; this was used as a measure of foragi
Animal Behaviour, 49, 1
262
Table I. Analysis of the effects of food dispersal(Patch) and nest-patchdistance
(Distance)on number of competitorsand load size Variable
Factor
4”
F
P
Competitors
Patch Distance Patch*Distance Patch Distance Patch*Distance
1, 3 2, 6 2, 6 1, 3 2, 6 2, 6
120.71 1.62 0.25 97.50 66.89 0.59
Load size
interruptions (interruptions/mm). The mean f SE number of birds in the field of view of the camera when load-size observations were taken was 5.2 4~0.181 (range: 1-19). The maximum number of ringed birds in the field of view at any one time was three. Thus, during the vast majority of observations, most of the ‘competitors’ were nonringed starlings (approximately 40 birds), from the surrounding areas, which regularly visited the feeding trays. Four ringed birds (two males and two females) of the six breeding at the farm visited all the treatments at all distances. The number of visits by each bird to each presentation varied between five and 19, with a total of 257 patch visits recorded. I analysed the effects of patch distance and food dispersal on number of conspecifics present around the focal birds when they left the patch and prey load sixesby a multivariate mixed-model repeated-measures analysis of variance, using MANOVA on SPSS(Hand & Taylor 1987; SPSS 1988). Patch distance (Distance) and food dispersal (Patch) are treated as fixed effects, and Bird (the focal individual) is treated as a random effect (Hand & Taylor 1987). Patterns of change with distance were investigated using orthogonal poiynomial contrasts (Hand & Taylor 1987; SPSS 1988). The three replicates at each site did not differ in either load sizeor number of competitors present (ANOVA with factors distance, patch and replicate, performed separately for each bird; load size,fi62-7o ~2.14, P>O.124, in all cases;competitors, F2,62-7o~1.08, P20.346, in all cases), so I treat all replicates together for the main analysis. Time of day also had no significant effect on load size or number of competitors, at least while observations were taken, so is not considered further in the analysis (ANOVA with factors distance and patch, and covariate time of day, performed separately for each bird: load size,
0.273 0.786 0.002
F i 62-,0<2.08, P>O.l 11, in all cases;competitors, F ,‘62M,2~1.50,P>O.262, in all cases). The resolution of the video-recordings was not sufficient to be able to identify individuals while foraging. Thus, rates of aggression and interruption could not be assigned to individuals. This potentially introduces pseudoreplication (Hurlbert 1984) into the design, because individuals may be repeatedly sampled. As a conservative measure to reduce this effect, I treat the mean value for each patch presentation as an independent datum, rather than individual acts of aggression and interruption. The manipulation of food dispersal altered the number of birds feeding near to the focal individuals; more conspecifics were in close proximity when the food trays were clumped, than when they were dispersed (clumped patch manipulation, 3.033 f 0.234; dispersed patch manipulation, 1.219 & 0.186; Table I). This indicates that the manipulation successfullyaltered the proximity of conspecifics. However, the total number of birds using the system did not differ with the patch manipulation (total number of birds present for the clumped patch manipulation: 5088 & 0.199; and dispersed patch manipulation: 5.248 +Z0.315; F 1,256=O64, P=O.424). Birds took larger load sizesthe further they were from their nests (Fig. 1, Table I). Over the range of distances investigated, load size increased at a decelerating rate with nest-patch distance (polynomial contrast for Distance, linear term, t= 11.284, P
Short Communications or 0
1
760) 5-_ .2 1 43 32lO-
=l
-Ll 15
x5
Patch distance (m) Figure1. Mean ( +SE) number of mealwormstaken at eachof the four nest-patchdistances,in the low competition (0) and high competition ( n ) treatment groups. From left to right, values are based and 38 patch visits, by four birds.
on 46, 36, 49,47,41
(Cuthill & Kacelnik 1990; Witter & Cuthill 1993). Dispersalof food within the patch also influenced load size; birds took significantly smaller loads from the patches where food was clumped (Fig. 1, Table I). Since both numbers of conspecifics present and load size were influenced by the manipulations, it is important to examine the effectson load size when numbers of conspecifics present are controlled for. In this case, load sizestill increased with increasing nest-patch distance (Roy-Bargman step-down F-test: Distance, F2,5=109.74, P
2(
6.09 f 0.740; ANOVA, with factors Distan and Patch; Patch, F,,,,=3.16, P=O.lOl; Distant F 2,,7=2.65, P=O.lll; Patch*Distance, F2,,, 1.50, P=O.262). There was a stronger indicatic that birds suffered more interruptions while fora ing in the high-competition treatment, althoug the difference is not quite significant (interruptior min, low competition, 2967 f 0.291; high camp tition, 3.00 f 0.436; Patch, F,,,,=4*03, PzO.06 Distance, F,,,,=O.20, P=O+322; Patch*Distanc Fz,,,=0.38, P=O.694). Although these trends are suggestive, it seer unlikely that these effects alone can account f the large changes in load size observed betwec patch treatments. However, even without dire aggression or overt interruptions, the presence conspecificsmay incur ‘attention costs’ (Cuthill Kacelnik 1990). That is, rate of prey gain may lowered simply because individuals have the attention to foraging distracted by the presence conspecifics. Changes in the number and proxii ity of conspecifics may also alter anti-predato strategies of the birds (Pulliam & Caraco 198~ However, changes in anti-predatory behavior such as reduced vigilance, appear unlikely explain the reduction of load size with increasi numbers of conspecifics. If foraging with co specifics reduces the risk of predation then bir may have been less vigilant and devoted mc time or attention to foraging; this may hd increased the load sizecarried to the nest, depen ing upon the specific shape of the gain functic An alternative possibility is that foraging ve close to conspecifics increases predation ri because more time or attention has to be allocat to monitoring nearby birds, with less attenti paid to predatory attack (cf. Cuthill & Kacelr 1990). In summary, the results indicate that an expe mental increase in the level of competition feeding sites decreasesthe number of prey item which starlings carry back to the nest. This PI vides evidence for a causal role of proximity conspecifics in determining load sizesduring fc aging, as suggested by the correlational data Cuthill & Kacelnik (1990). There are seve mechanisms through which this effect might mediated, which cannot be unequivocally dist guished with the present data set. Howev through whatever mechanism competition is a ing, reduced load sizes will reduce the rate which parental birds are able to provision th
Animal
264
Behi wiour,
offspring, all else being equal. This may have direct fitness consequences to the bird experiencing high levels of competition. I thank Sasha Dal1 and John Swaddle for helpful discussions. I am particularly grateful to Robert Slotow for his detailed criticisms of this and a previous version of the manuscript. I was supported by a NERC Research studentship when the experiment was carried out, and by a NERC Research Fellowship when writing the paper.
REFERENCES Baker, M. C., Belcher, C. S., Deutsch, L. C., Sherman, G. L. & Thompson, D. B. 1981. Foraging success in junco flocks and the effects of social hierarchy. Anim. Behav., 29, 137-142. Caraco, T. 1979. Time budgeting and group size: a test of a theory. Ecology, 60, 6188627. Cuthill, I. C. & Kacelmk, A. 1990. Central place foraging: a reappraisal of the ‘loading effect’. Anim. Behav., 40, 1087-1101. Hamilton, W. D. 1971. Geometry for the selfish herd. J. theor. Biol., 31, 295-311.
49, 1
Hand, D. J. & Taylor, C. C. 1987. Multivariate of Variance and Repeated Approach for Behavioural
Measures: Scientists.
a
Analysis Practical
London: Chapman & Hall. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr., 54, 187-211. Orians, G. H. & Pearson, N. E. 1979. On the theory of central place foraging. In: Analysis of Ecological Systems (Ed. by D. J. Horn, R. D. Mitchel & G. R. Stairs), pp. 154-177. Columbus: Ohio State University Press. Pulliam, H. R. & Caraco, T. 1984. Living in groups: is there an optimal group size? In: Behavioural Ecology: an Evolutionary Approach. 2nd edn (Ed. by J. R. Krebs & N. B. Davies), pp. 122-147. Oxford: Blackwell Scientific Publications. SPSS. 1988. SPSSx User’s Guide. 3rd edn. Chicago: SPSS Inc. Stephens, D. W. & Krebs, J. R. 1986. Foraging Theory. Princeton, New Jersey: Princeton University Press. Tinbergen, J. M. 198 1. Foraging decisions in the starling (Sturnus vulgaris). Ardea, 69, l-67. Witter, M. S. 1993. The ecological costs of being fat. Ph.D. thesis, University of Bristol. Witter, M. S. & Cuthill, I. C. 1993. The ecological costs of avian fat storage. Phil. Trans. R. Sot., 340, 73-92.