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Black skimmer parental defence against chick predation by gulls
AnOn. Behav., 1989, 38, 534 541
Black skimmer parental defenee against chick predation by gulls J A M E S S. Q U I N N *
Department of Zoology, University Of Oklahoma, Norman, OK 73019, U.S.A.
Abstract. Predation by laughing gulls, Larus atricilla, on black skimmer, Rynchops niger, chicks was observed in a Texas nesting colony. The patterns of predation differed from random in two respects: (1) significantly more attacks (both attempts and successes) were directed toward nests with two parents present than toward nests with only one parent and (2) significantlymore attempts occurred when female parents were brooding than males. Differences in gull attack rates according to sex of the parent skimmer may have been due to the considerable sexual size dimorphism in skimmers. Male skimmers are larger than laughing gulls, while female skimmers are smaller. Predation on skimmer eggs was uncommon. Solo incubating by females was significantly less frequent after the first egg's hatching than before. The decreased frequency of female solo attendance after the first hatching may represent an adaptive response to predator pressure at a time when chicks are most vulnerable to predation by gape-limited predators such as laughing gulls and would be better protected by males or both parents. The higher observed frequencies of both predation attempts and successes directed toward nests with bi-parental attendance was not predicted and may be attributable to certain unavoidable high risk activities, such as brooding exchanges and chick feeding when broods are young, which typically occur only when both parents are present.
Predation is a major source of mortality on the offspring of many bird species (Ricklefs 1969; Clark & Wilson 1981). Numerous studies have examined prey reactions to predator pressures, including behavioural responses such as living in groups (Hamilton 1971; Hoogland & Sherman 1976; Veen 1977), mobbing (Curio 1978), and giving distraction displays (Brunton 1986). If predation pressure on offspring is sufficiently strong, selection may influence parental care patterns (Harvey & Greenwood 1978). Theoretically, two important determinants of parental care and brood defence are: (1) the genetic relatedness between the parents and the brood (especially paternity; see Hamilton 1964; Trivers 1972; Alexander & Borgia 1979); (2) the reproductive value of the young relative to that of the parents (Fisher 1958; Dawkins & Carlisle 1976), a factor expected to vary with offspring age (Andersson et al. 1980). Physical capacities of the two parental sexes represent a third potentially important group of determinants of parental care. Bright male plumage in sexually dimorphic passerines may preclude the option of male participation in incubation (Verner & Willson 1969). Such constraints may in turn explain other differences *Present address: Department of Biology, Queen's University, Kingston, Ontario, K7L 3N6, Canada. 0003-3472/89/090534+08 $03.00/0
between parental care by the sexes. For example, Curio (1980) suggested that the tendency for male great tits, Parus major, to be more involved in predator mobbing than females may stem from exclusive female brooding of the young, a task that essentially renders the male less crucial to the brood's success. Parental role specialization may have tipped the balance in favour of increased male responsibility for mobbing while the young still require brooding. More recent work (Regelmann & Curio 1986) suggests that greater male involvement reflects an asymmetry in the values of the sexes to each other due to greater female mortality during breeding. Male northern mockingbirds, Mimus polyglottos, were more heavily involved in nest defence than their mates (Breitwisch 1988), a difference that was attributed to a male-biased sex ratio. Differential abilities to discourage predators between the sexes of size dimorphic species may affect parental roles. For example, the relatively large size of female raptors may enable them to defend the brood more effectively against predators (Andersson & Norberg 1981). Sexual differences in abilities to defend the brood may be especially important when predators are about the same size as the parents. Black skimmers, Rynchops niger, are colonialnesting, monogamous larids. Adult females weigh,
9 1989 The Association for the Study of Animal Behaviour 534
Quinn: Predation defence by skimmer parents on average (+__sE), 254___2-1 g, which is about 72% of the adult males, average of 349 + 3-4 g (Quinn 1988). Both sexes participate in all aspects of parental care (Erwin 1977; Burger 1981; Quinn 1988). Here I report the results of a study of a Texas nesting colony of skimmers located near a colony of laughing gulls, Larus atricilla, which are important predators of young black skimmer chicks (Blus & Stafford 1980). Laughing gulls weigh about 325 g (Dunning 1984), slightly less than male black skimmers, but considerably more than female black skimmers. Black skimmers do not mob laughing gulls, so the defence against a gull predation attempt is typically only by the individual pair under attack. I examined the hypothesis that laughing gull predation favours increased frequency of biparental attendance of skimmer broods following hatching and decreased solo attendance by the female parent after hatching begins, during the early nestling stage when the young are highly vulnerable to predation. The hypothesis assumes that: (1) nest attendance by both parents is more likely to discourage predators than the presence of solo parents, (2) solo nest attendance by male skimmers is more discouraging to predators than solo nest attendance by female skimmers, and (3) attendance patterns that are less effective at discouraging predation would be less frequent during periods of high risk to the young. Three predictions of the hypothesis are: (1) pairs will face fewer predation attempts than solo attendants, (2) solo males will face fewer predation attempts than solo females, and (3) solo attendance by females relative to males will decrease after their respective clutches begin hatching. METHODS
The study was conducted during the summer of 1983 on a dredge-material island near channel marker 66 in Lavaca Bay, Texas, U.S.A. (28~ 96~ Laughing gulls nested in the low ground vegetation, some as close as 3 m from the black skimmer study colony, which was on open substrate. Colony censuses were made every fourth day (weather permitting) prior to the beginning of the hatching period. A total of 71 skimmer nests were marked with painted wooden stakes after the first egg in each nest was found. Of these, 34 study nests
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in a central portion of the length of the colony including the full width of the colony (from the shoreline to the opposite edge of the colony) were observed closely from an observation blind located about 15 m from the edge of the colony. These nests were selected because of their visibility from the blind. Twenty-one of the 34 nests were experimentally altered for a different study (10 had one pipping egg swapped with a similar egg from a different nest; 11 had one pipping egg added). Nests that were manipulated did not differ significantly from unmanipulated nests in predation attempt rates, predation success rates, or in the proportions of attempts that were successful (Mann-Whitney U-tests). Similarly, there were no differences between the two experimental treatments; thus, manipulated nests were included in the analyses. To prevent chicks from running from the study area during researcher activities, a 0-5-m high hardware cloth fence was erected around the study area just prior to the first hatching. Such fencing apparently reduces mortality resulting from long distance fleeing (Safina & Burger 1983) and facilitates the location and observation of individual chicks (Nisbet & Drury 1972). Upon hatching, chicks were marked with feather dye (black Nyanzol or yellow picric acid) on the crown, throat, rump and sides of the face or wings, according to their sizes relative to other brood members and/or hatching dates during censuses every fourth day. Two 5-day-old chicks were banded with USF&WS numbered leg bands, and, in some cases, with colour bands to facilitate identification. Parental activities in relation to predation attempts by laughing gulls were observed from the blind for 34 skimmer pairs. Because males are so much larger than females, parental sex identity was readily discernible from body and bill sizes (Burger 1981; Quinn 1988), even when only one parent was present. Observers remained in the blind overnight (to minimize disturbance) and recorded the following observations during nearly continuous daylight hour watches: predation attempts per nest, success/ failure of each attack, sex of the parent on the nest, presence/absence of the other pair member, and parental activities during and following predation attempts. A predation attempt was defined as a dive toward the target nest that either reached the nest or was deflected by the parent's defensive flight. Because predation attempts were very brief and sudden, many records were incomplete, hence were suitable for some but not all analyses.
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Animal Behaviour, 38, 3
Predation attempt and success rates were calculated as the number of these events observed per 'brood-h' (defined as number of nests watched • number of h they were watched) in each of four age-class categories, based on the number of days since hatching (day '0' of the eldest chick): 0-3 days, 4-7 days, 8-11 days and 12-15 days. Skimmers fledge at about 25-30 days of age (Erwin 1977). Rates for diurnal patterns of predation were calculated as the number of predation events per h (standardized to account for differences in the total observation time during the different hours of the day). The sex of attending parents and whether they were incubating/brooding or standing near the nest at the time of hourly scan samples were recorded for a sub-sample of 11 nests, chosen on the basis of visibility from the blind. The time of day was recorded for each scan to allow correlation analysis between attendance patterns and predation patterns. These attendence data were collected independently of predation data. Statistical analyses were done using SAS (SAS Institute 1985) and BMDP (Dixon 1983). Sexspecific differences in nest care were tested with Wilcoxon signed-ranks tests. Associations between variables were tested with Kruskal-Wallis tests or Spearman rank correlations.
RESULTS General Description of Predation Between 17 June and 10 July 1983, 147 predation attempts by laughing gulls were recorded. Fortyeight (33%) of these resulted in the successful capture of black skimmer chicks. Here I report on 99 attempts, including 26 (26%) successful ones, that occurred at the 34-nest study area during 2804 nest-h of observation. Only one egg from the 34 study area nests was observed being preyed upon by a gull. The predatory behaviour of laughing gulls was divided into two components, patrols and predation attempts. When patrolling, gulls flew about 3 m above the skimmer colony, apparently scanning over many nests. Usually only one gullengaged in patrolling at a time, though on occasion two patrolled simultaneously. Patrolling gulls were not mobbed by skimmers. The usual response of a brooding skimmer to a patrolling gull was to remain on the nest and vocalize with a series of
0.09
0.08
0.07
0-05 "
.g_
0.04
,
o o7_ 0.0~
~ "'X
0-02
0.01
0
0-3
4-7 8-11 Brood age (days)
12-15
Figure l. Mean rate of predation attempts as a function of brood age. o: all attempts; e: successfulattempts. Bars are _+lsE.
monosyllabic barks. A predation attempt consisted of a steep dive toward one particular nest, typically resulting in physical contact with the parent skimmer or chick and/or an attempt to grasp a chick (in the gull's bill) and fly off with it, Six successful gull attacks occurred when skimmer chicks were noted as already being exposed (e.g. during feedings or nest reliefs). Often, the gull swooped down and physically rammed the brooding skimmer parent, knocking it off the nest, then seized the exposed chick and departed. Ramming was specifically recorded in four successful attacks (but full details were often not recorded). Skimmer defences against ramming included crouching on the nest and acting as a physical barrier against the ramming gull, or a more active defence involving flying a collision course towards the swooping gull and attempting to disrupt its dive. Defensive flights by solo parents necessitated leaving the chicks unprotected for a few seconds. Predation Attempt and Success Rates Predation was apparently an important source
Quinn: Predation defence by skimmerparents Table I. Parental attendance patterns as a function of black skimmer brood age Brood age (days) 0-3*
4 7t
8 11;~
12 15w
Parent BR** ST BR ST BR ST BR ST Female Male
288 326
163 175 124 86 172 186 123 66
125 18 110 125 12 95
* Pooled G comparing frequencies of brooding by males and females= 2.35, r~s. t Pooled G=0-33, NS. 2~Pooled G= 2.64, NS. wPooled G = 1.21, NS. ** Number of records from hourly scan samples of the parent's sex and activity (BR: brooding; ST: standing).
of mortality among black skimmer chicks in this colony. Of the 92 young hatching (in 34 nests), 62 (67%) disappeared before chicks reached 1 week of age. Twenty-six predations were actually observed. Predation success rates (per brood-h) varied with brood-age (Kruskal-Wallis test H = 13.1, dJ=3, P<0.01; Fig. 1), though the highest rates were during brood ages 4-7 days. Attempt rates did not vary significantly with brood-age ( H = 5-93, df= 3, NS; Fig. 1) but were highest during brood ages 4-7 days. Similarly, success rates varied with brood-age when they were based on the number ofchick-h of observation (H=13.2, df=3, P<0.01). Again, there was no trend in attempt rates per chick-h as a function of brood-age ( H = 5-75, df= 3, NS). Nests that were attended by both parents were more likely to attract predators. Biparentally attended broods were attacked more frequently than singly attended broods as measured by attempted (singly attended )?= 1.13; doubly attended 27= 2.04, N = 23 nests, Wilcoxon signedranks test, Ts = 32, P < 0.005) and successful predations (singly attended J?=0-54, doubly attended 37=1.08, N = 1 3 nests, T~=16, P<0.025). These analyses assumed an equal availability of nests attended by one or two parents. Expected values for attack rates on singly versus doubly attended nests were calculated for each nest by multiplying the number of predation events at a given brood age by the percentage of incubation records indicating double versus single attendance for that brood age. Expected values for all nests were equal
537
or greater for the singly attended condition. Thus, the analyses presented are conservative, and standardization to account for availability of doubly versus singly attended nests according to date would increase the significance. Predation attempts during chick feedings were significantly more likely to be successful (four of five) than attempts during non-feeding activities (11 of 63; Fisher's exact test, P = 0.007). Feeding of young chicks typically involves the presence of both parents (one broods while the other offers food) and requires that chicks be partially exposed. Although male and female skimmers brooded the young and stood guard near the nest for similar amounts of time within each age-class (Table I), the rate of predation attempts differed as a function of the brooding parent's sex. Attempts were significantly less frequent when the male parent was on the nest (male attended J?=0.87, female attended J?= 1-94, N = 16 nests, Ts= 22, P<0.01). This bias was especially marked when only one parent was in attendance (male attended J?= 0-25, female attended )?= 2.37, N = 8, T~= 3.5, P < 0.025). During 24 attacks on nests that were attended by both parents, there was no bias according to the sex of the adult incubating for all attempts: males and females each were incubating during 12 attempts. Comparable analyses on predation successes was complicated by the smaller number of complete observations. Sex of the brooding parent was determined in 14 such cases: six males and eight females. In three of the four predations involving solo parents, the brooding adult was female. When both parents attended and the sex of the brooding adult was known, males brooded during four predations, females during five (the number of parents attending was not recorded in one predation at a male brooded nest). Males (N= 46) were as likely to fly in chase of gulls after predation attempts as females (N= 45). When both parents were present during a gull attack with suitable observations, males defended the young on 11 occasions, females on five. The frequency of reported subjective evaluations of which sex defended the young was too low to warrant testing. To determine whether nest attendance patterns reduced the occurrence of risky solo brooding by females after hatching began (especially during early chick development), I compared nest attendance behaviour for 11 pairs observed during the 8-day period before the first egg hatched with that
Animal Behaviour, 38, 3
538
0.4
Table II. Spearman rank correlations between hourly predation success (per brood-h observed)or total attempt rates and hourly mean scan sample records* for each sex for each of the daylight hours
h
o 0.5
Predation event Successful
0.2
Brood care pattern
~- 0.1
0 _8/_7_ -6--5
I
I I I O- I -2--I 2-5 Brood age (doys)
-4--3
I
4-5
I 6-7
Figure 2. Proportion of brooding records for lone males and femalesas a function of brood-age, rn: lone males; I1: lone females. Bars are _+lSE. observed during the 8-day period thereafter (i.e. starting when the first egg in a clutch hatched). The proportion of solo male incubation/brooding records was lower before hatching 0~= 0-14_+0"02) than after, but not significantly so (_~= 0.21 + 0"037; Wilcoxon signed-ranks test T,= 19-0, NS). However, the proportion of solo female incubation/brooding records was significantly higher before hatching 0?=0.33+0-050) than after hatching 0?=0.24_+0.022; T,=10-0, P < 0.05; Fig. 2). Thus, there was a parental care shift between the incubation and chick rearing stages that consisted of a reduction in the amount of solo female attendance during the risky earlynestling stage. During the early stages of chick growth, biparental attendance typically involved one parent brooding while the other stood by the nest. There was a statistically non-significant decline in the incidence of bi-parental nest attendance with the age of the brood during the first eight days post hatching ( H = 12.8, df= 7, 0.1 > P > 0.05). To determine on a finer scale whether scheduling of nest attendance matched hourly patterns of chick predation events by gulls, I examined hourly scan-sampled attendance patterns by male and female skimmers with broods aged 0-15 days. ThE hourly patterns of predation attempts and successes were quite erratic, but showed significant positive correlations between rates of successful predation and bi-parental attendance (Table II).
rho
Lone parent brooding -0.35 Lone male brooding -0.48 Lone female brooding -0-27 Male standing byt 0.33 Female standing byt 0.51 Both attending:~ 0-64 One attending:~ -0.45 None attending$ 0-01
All attempts
(P)
rho
(P)
(0.20) (0.07) (0.33) (0.22) (0.049) (0.009) (0.09) (0.96)
-0.27 -0.45 -0-05 0.04 -0.06 0-12 -0.02 0.04
(0.32) (0.09) (0.85) (0.89) (0.84) (0.67) (0.93) (0.89)
* Collected independently of the predation data from a subset of 11 nests. ~ While mate is brooding. Includes brooding and standing by.
These correlations held also for the patterns of (non-brooding) female attendance, but not for (non-brooding) male attendance (Table II). No significant correlations were found when hourly patterns of all attempts were examined (Table II).
DISCUSSION Predation was an important source of chick mortality in this study and may be an active selection force influencing parental care patterns. Although some chick disappearances may have resulted from scavenging (i.e. death preceded removal), actual predation events by laughing gulls were observed frequently during this study. Laughing gulls appeared to be the only major predators taking young skimmers. Burger (1982) reported that laughing gulls, herring gulls, Larus argentatus, American oystercatchers, Haematopus palliatus, and a mink, Mustela vison, were active predators on black skimmers nesting on islands along the New Jersey coast. Only laughing gulls and oystercatchers were present in Lavaca Bay and I found no evidence of predation by the latter. Predation rates decreased with brood age (Fig. 1). This deline was not due merely to a decrease in the numerical availability of potential victims, and probably reflects a prey-size limitation on laughing
Quinn: Predation defence by skimmer parents gulls, which swallow fresh prey whole (see Quinn & Morris 1986). Periods of high risk to the offspring were expected to coincide with bi-parental guarding of the brood and/or deployment of care by the parent better able to reduce predation. Surprisingly, the presence of both parents did not thwart predatory attempts. Indeed it was positively related to the likelihood of predation. This apparent increase was not because bi-parental care predominated during diurnal periods of high predator activity. Once hatching began, the amount of bi-parental nest attendance decreased, presumably as a function of both: (1) the necessity to provide prey for the young at an increasing rate as metabolic needs increase (Ricklefs 1974); and (2) the broods' increasing abilities at thermoregulation (Ricklefs 1974). The association between predation events and periods of bi-parental attendance may be the result of constraints over which parents have little or no control. Certain activities (e.g. young chick feedings and possibly parental change-overs) that seem to increase the susceptibility of the young occur only when both pair members are present. Brooding change-overs reveal the contents of the nest and expose the offspring to predation attempts, especially if the parents engage in any mutual social interactions that temporarily reduce their attentiveness to the chicks. To some extent, the feeding of chicks automatically exposes them. Such exposure generally increases with chick age (personal observation) and may present opportunities for predators. Predation attempts during chick feedings, though infrequently observed, were highly successful. The low numbers of attempts observed during chick feeding may reflect the brevity, relative infrequency, and sporadic nature of that activity. Gulls were less likely to attack a skimmer nest being brooded by a male parent than one brooded by a female, supporting my second prediction. Despite this difference in attempt rates, there were no significant differences in success rates between the sexes (though that may be a consequence of few predation-success records that include brooder's sex). The larger size of male skimmers may provide a more effective defence against laughing gulls. Detailed studies of predation by intermediate-sized predators on other species with sexually dimorphic parents will test the generality of these findings. Periods of the day when bi-parental attendance was common were those periods when successful
539
predation occurred frequently in the colony as a whole. The correlation between bi-parental attendance frequency and predation success apparently resulted from a high incidence of male brooding and female attendance during periods of high predation risk. This probably reflects, in part, risks at chick feeding times. Young chicks are fed more often by their mothers than their fathers (Quinn 1988) and must emerge from under the brooding parent to take the prey. Alternatively, during periods when feedings were infrequent, brooding females with mates standing by might be effective at deterring, or discouraging predators. Such periods may yield few opportunities for predation. Predation rate as a function of time of day may simply reflect predation attempts whenever gulls perceived a possible opportunity. It follows that skimmer brooding roles should reflect the differential response by laughing gulls to male versus female parents. Specifically, male skimmers may be most effectively deployed as solo brooders of vulnerable young chicks. Although the results presented here show no difference in the chick-brooding behaviour of male and female skimmers, males are reported to engage in more brooding than females elsewhere (Burger 1981). Though patterns of parental care have been attributed to size-related differential ability to defend young (e.g. Andersson & Norberg 198t; Wiklund & Stigh 1983), alternative explanations for patterns of parenal care may or may n o t build on sexual size dimorphism, Risky nest defence by male great tits and male northern mockingbirds has been attributed to skewed adult sex ratios (Breitwisch 1988) or sex-specific differences in mortality during the breeding season (Regelmann & Curio 1986). There appears to be no evidence for skewed sex ratios in black skimmers, and sex-specific differences in mortality during breeding are not apparent (Quinn 1988). However, decreased solo female participation in the care of the young (to levels shown by males) following hatching may be due, in part, to the increased role females play in feeding very young chicks (Quinn 1988), Females delivered prey that were smaller than those delivered by males (Quinn 1988). Male skimmers fed their chicks more as their broods grew older (Quinn 1988) and presumably became less susceptible to laughing gull predation. Males delivered larger prey to the young (Quinn 1988) at a time when chicks were larger and probably more efficient at
540
Animal Behaviour, 38, 3
swallowing large prey and when their metabolic requirements were higher. Any increase in the parental efficiency regarding chick feeding may serve to accelerate chick growth to a size of reduced susceptibility to predators and other sources o f mortality. The shift in skimmer parental care patterns at the time of first hatching may be an adaptive response to predation on young chicks. O f three colonies of skimmers observed in Lavaca Bay (Quinn 1988), two were in close proximity to nesting laughing gulls. The colony lacking laughing gull neighbours was the only one at which significantly greater brood attendance by females was detected (Quinn 1988). Thus, the parental care response of decreased solo female care may be facultative, though further investigation is necessary.
ACKNOWLEDGMENTS I thank Linda A. Whittingham and David Clugston for assistance in the field. Kent Ruffin, Nance Matus and a number of others provided occasional voluntary assistance. Various drafts of this manuscript were critiqued by T o d d A. Crowl, Katherine D. Graham, Patricia Schwagmeyer, Frank Sonleitner, James N. Thompson, Bedford Vestal and especially Douglas Mock. Charles T. Snowdon, Lee C. Drickamer and two anonymous referees provided helpful comments on the submitted manuscript. Peter W. Bergstrom, Gary D. Schnell and F r a n k Sonleitner provided statistical advice. Dan H o u g h provided computer assistance and Diane Fields proof-read the manuscript. Coral McCallister prepared the figures. This paper was written as a portion of my doctoral dissertation. Financial support was generously provided by the R o b b and Bessie Welder Wildlife Foundation, the Natural Sciences and Engineering Research Council (Canada), the American Ornithologists' U n i o n (Josselyn Van Tyne Award), the Wilson Ornithological Society (Stewart Award), the American Museum of Natural History (Mac P. Smith Award), Sigma Xi (Grants in Aid of Research), the University of Oklahoma (Department of Zoology research support; Associates F u n d Research Grant; Foundation Research Grant), and the R. L. Disney International Student Scholarship. This is contribution number 329 of the Welder Wildlife Foundation.
REFERENCES Alexander, R. D. & Borgia, G. 1979. On the origin and basis of the male female phenomenon. In: Sexual Selection and Reproductive Competition in Insects (Ed. by M. S. Blum & N. A. Blum), pp. 417-440. New York: Academic Press. Andersson, M. & Norberg, R. A. 1981. Evolution of reversed sexual size dimorphism and role partitioning among predatory birds, with a size scaling of flight performance. Biol. J. Linn. Soc., 15, 105-130. Andersson, M., Wilklund, C. G. & Rundgren, H. 1980. Parental defence of offspring: a model and an example. Anita. Behav., 28, 536-542. Blus, L. J. & Stafford, C. J. 1980. Breeding biology and relation of pollutants to black skimmers and gull-billed terns in South Carolina. U.S. Fish Wildl. Serv. Spec. Sei. Rep. Wildl., 230, 1 18. Breitwisch, R. 1988. Sex differences in defence of eggs and nestlings by northern mockingbirds, Mimus polyglottos. Anita. Behav., 36, 62 72. Brunton, D. H. 1986. Fatal antipredator behavior of a killdeer. Wilson Bull., 98, 605 607. Burger, J. 1981. Sexual differences in parental activities of breeding black skimmers. Am. Nat., 117, 975 984. Burger, J. 1982. The role of reproductive success in colony-site selection and abandonment in black skimmers (Rynchops niger). Auk, 99, 109-115. Clark, A. B. & Wilson, D. S. 1981. Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. Q. Rev. Biol., 56, 253-277. Curio, E. 1978. The adaptive significance of avian mobbing. Z. Tierpsychol., 48, 175-183. Curio, E. 1980. An unknown determinant of a sex-specific atruism. Z. Tierpsychol., 53, 139 152. Dawkins, R. & Carlisle, T. R. 1976. Parental investment, mate desertion and a fallacy. Nature, Lond., 262, l 31 133. Dixon, W. J. (Ed. in chief) 1983. BMDP Statistical Software. 1983 edn. Berkeley: University of California Press. Dunning, J. B., Jr. 1984. Body weights of 686 species of North American birds. W. Bird Banding Assoc. Monogr., 1, 1-38. Erwin, R. M. 1977. Black skimmer breeding ecology and behavior. Auk, 94, 709 717. Fisher, R. A. 1958. The Genetical Theory of Natural Selection. 2nd edn. New York: Dover. Hamilton, W. D. 1964. The genetical evolution of social behaviour. I, II. J. theor. Biol., 7, 1-52. Hamilton, W. D. 1971. Geometry for the selfish herd. J. theor. Biol., 31, 295-311. Harvey, P. H. & Greenwood, P. J. 1978. Anti-predator defence strategies: some evolutionary problems. In: Behavioral Ecology: An Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 129 151. Sunderland, Massachusetts: Sinauer. Hoogland, J. L. & Sherman, P. W. 1976. Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr., 46, 33 58. Nisbet, I. C. T. & Drury, W. H. 1972. Measuring breeding success in common and roseate terns. Bird-Banding, 43, 97-107.
Quinn: Predation defence by skimmer parents Quinn, J. s. 1988. Sexual size dimorphism and parental care: a comparative study of black skimmers and Caspian terns and a computer simulation model. Ph.D. thesis, University of Oklahoma, Norman. Quinn, J. S. & Morris, R. D. 1986. Intra-clutch eggweight apportionment and chick survival in Caspian terns. Can. J. Zool., 64, 2116-2122. Regelmann, K. & Curio, E. 1986. Why do great tit (Parus major) males defend their brood more than females do? Anita. Behav., 34, 1206-1214. Ricklefs, R. E. 1969. An analysis of nesting mortality in birds. Smithson. Contrib. Zool., 9, 1-48. Ricklefs, R. E. 1974. Energetics of reproduction in birds. In: Avian Energetics (Ed. by R. A. Paynter, Jr), pp. 152292. Cambridge, Massachusetts: Nuttall Ornithological Club. Safina, C. & Burger, J. 1983. Effects of human disturbance on reproductive success in the black skimmer. Condor, 85, 164-171.
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SAS Institute Inc. 1985. SAS User's Guide." Statistics. Cary, North Carolina: SAS Institute. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man 1871 1971 (Ed. by B. Campbell), pp. 136 179. Chicago: Aldine. Veen, J. 1977. Functional and causal aspects of nest distribution in colonies of the sandwich tern (Sterna s. sandvicensis Lath.). Behav. Suppl., 20, 1-193. Verner, J. & Willson, M. F. 1969. Mating systems, sexual dimorphism, and the role of male North American passerine birds in the nesting cycle. Ornithol. Monogr., 9, 1 76. Wiklund, C. G. & Stigh, J. 1983. Nest defence and evolution of reversed sexual size dimorphism in snowy owls Nyctea scandiaca. Ornis Scand., 14, 58 62.
(Received 28 July 1988; revised 1 November 1988; MS. number: A5245)
Black skimmer parental defenee against chick predation by gulls J A M E S S. Q U I N N *
Department of Zoology, University Of Oklahoma, Norman, OK 73019, U.S.A.
Abstract. Predation by laughing gulls, Larus atricilla, on black skimmer, Rynchops niger, chicks was observed in a Texas nesting colony. The patterns of predation differed from random in two respects: (1) significantly more attacks (both attempts and successes) were directed toward nests with two parents present than toward nests with only one parent and (2) significantlymore attempts occurred when female parents were brooding than males. Differences in gull attack rates according to sex of the parent skimmer may have been due to the considerable sexual size dimorphism in skimmers. Male skimmers are larger than laughing gulls, while female skimmers are smaller. Predation on skimmer eggs was uncommon. Solo incubating by females was significantly less frequent after the first egg's hatching than before. The decreased frequency of female solo attendance after the first hatching may represent an adaptive response to predator pressure at a time when chicks are most vulnerable to predation by gape-limited predators such as laughing gulls and would be better protected by males or both parents. The higher observed frequencies of both predation attempts and successes directed toward nests with bi-parental attendance was not predicted and may be attributable to certain unavoidable high risk activities, such as brooding exchanges and chick feeding when broods are young, which typically occur only when both parents are present.
Predation is a major source of mortality on the offspring of many bird species (Ricklefs 1969; Clark & Wilson 1981). Numerous studies have examined prey reactions to predator pressures, including behavioural responses such as living in groups (Hamilton 1971; Hoogland & Sherman 1976; Veen 1977), mobbing (Curio 1978), and giving distraction displays (Brunton 1986). If predation pressure on offspring is sufficiently strong, selection may influence parental care patterns (Harvey & Greenwood 1978). Theoretically, two important determinants of parental care and brood defence are: (1) the genetic relatedness between the parents and the brood (especially paternity; see Hamilton 1964; Trivers 1972; Alexander & Borgia 1979); (2) the reproductive value of the young relative to that of the parents (Fisher 1958; Dawkins & Carlisle 1976), a factor expected to vary with offspring age (Andersson et al. 1980). Physical capacities of the two parental sexes represent a third potentially important group of determinants of parental care. Bright male plumage in sexually dimorphic passerines may preclude the option of male participation in incubation (Verner & Willson 1969). Such constraints may in turn explain other differences *Present address: Department of Biology, Queen's University, Kingston, Ontario, K7L 3N6, Canada. 0003-3472/89/090534+08 $03.00/0
between parental care by the sexes. For example, Curio (1980) suggested that the tendency for male great tits, Parus major, to be more involved in predator mobbing than females may stem from exclusive female brooding of the young, a task that essentially renders the male less crucial to the brood's success. Parental role specialization may have tipped the balance in favour of increased male responsibility for mobbing while the young still require brooding. More recent work (Regelmann & Curio 1986) suggests that greater male involvement reflects an asymmetry in the values of the sexes to each other due to greater female mortality during breeding. Male northern mockingbirds, Mimus polyglottos, were more heavily involved in nest defence than their mates (Breitwisch 1988), a difference that was attributed to a male-biased sex ratio. Differential abilities to discourage predators between the sexes of size dimorphic species may affect parental roles. For example, the relatively large size of female raptors may enable them to defend the brood more effectively against predators (Andersson & Norberg 1981). Sexual differences in abilities to defend the brood may be especially important when predators are about the same size as the parents. Black skimmers, Rynchops niger, are colonialnesting, monogamous larids. Adult females weigh,
9 1989 The Association for the Study of Animal Behaviour 534
Quinn: Predation defence by skimmer parents on average (+__sE), 254___2-1 g, which is about 72% of the adult males, average of 349 + 3-4 g (Quinn 1988). Both sexes participate in all aspects of parental care (Erwin 1977; Burger 1981; Quinn 1988). Here I report the results of a study of a Texas nesting colony of skimmers located near a colony of laughing gulls, Larus atricilla, which are important predators of young black skimmer chicks (Blus & Stafford 1980). Laughing gulls weigh about 325 g (Dunning 1984), slightly less than male black skimmers, but considerably more than female black skimmers. Black skimmers do not mob laughing gulls, so the defence against a gull predation attempt is typically only by the individual pair under attack. I examined the hypothesis that laughing gull predation favours increased frequency of biparental attendance of skimmer broods following hatching and decreased solo attendance by the female parent after hatching begins, during the early nestling stage when the young are highly vulnerable to predation. The hypothesis assumes that: (1) nest attendance by both parents is more likely to discourage predators than the presence of solo parents, (2) solo nest attendance by male skimmers is more discouraging to predators than solo nest attendance by female skimmers, and (3) attendance patterns that are less effective at discouraging predation would be less frequent during periods of high risk to the young. Three predictions of the hypothesis are: (1) pairs will face fewer predation attempts than solo attendants, (2) solo males will face fewer predation attempts than solo females, and (3) solo attendance by females relative to males will decrease after their respective clutches begin hatching. METHODS
The study was conducted during the summer of 1983 on a dredge-material island near channel marker 66 in Lavaca Bay, Texas, U.S.A. (28~ 96~ Laughing gulls nested in the low ground vegetation, some as close as 3 m from the black skimmer study colony, which was on open substrate. Colony censuses were made every fourth day (weather permitting) prior to the beginning of the hatching period. A total of 71 skimmer nests were marked with painted wooden stakes after the first egg in each nest was found. Of these, 34 study nests
535
in a central portion of the length of the colony including the full width of the colony (from the shoreline to the opposite edge of the colony) were observed closely from an observation blind located about 15 m from the edge of the colony. These nests were selected because of their visibility from the blind. Twenty-one of the 34 nests were experimentally altered for a different study (10 had one pipping egg swapped with a similar egg from a different nest; 11 had one pipping egg added). Nests that were manipulated did not differ significantly from unmanipulated nests in predation attempt rates, predation success rates, or in the proportions of attempts that were successful (Mann-Whitney U-tests). Similarly, there were no differences between the two experimental treatments; thus, manipulated nests were included in the analyses. To prevent chicks from running from the study area during researcher activities, a 0-5-m high hardware cloth fence was erected around the study area just prior to the first hatching. Such fencing apparently reduces mortality resulting from long distance fleeing (Safina & Burger 1983) and facilitates the location and observation of individual chicks (Nisbet & Drury 1972). Upon hatching, chicks were marked with feather dye (black Nyanzol or yellow picric acid) on the crown, throat, rump and sides of the face or wings, according to their sizes relative to other brood members and/or hatching dates during censuses every fourth day. Two 5-day-old chicks were banded with USF&WS numbered leg bands, and, in some cases, with colour bands to facilitate identification. Parental activities in relation to predation attempts by laughing gulls were observed from the blind for 34 skimmer pairs. Because males are so much larger than females, parental sex identity was readily discernible from body and bill sizes (Burger 1981; Quinn 1988), even when only one parent was present. Observers remained in the blind overnight (to minimize disturbance) and recorded the following observations during nearly continuous daylight hour watches: predation attempts per nest, success/ failure of each attack, sex of the parent on the nest, presence/absence of the other pair member, and parental activities during and following predation attempts. A predation attempt was defined as a dive toward the target nest that either reached the nest or was deflected by the parent's defensive flight. Because predation attempts were very brief and sudden, many records were incomplete, hence were suitable for some but not all analyses.
536
Animal Behaviour, 38, 3
Predation attempt and success rates were calculated as the number of these events observed per 'brood-h' (defined as number of nests watched • number of h they were watched) in each of four age-class categories, based on the number of days since hatching (day '0' of the eldest chick): 0-3 days, 4-7 days, 8-11 days and 12-15 days. Skimmers fledge at about 25-30 days of age (Erwin 1977). Rates for diurnal patterns of predation were calculated as the number of predation events per h (standardized to account for differences in the total observation time during the different hours of the day). The sex of attending parents and whether they were incubating/brooding or standing near the nest at the time of hourly scan samples were recorded for a sub-sample of 11 nests, chosen on the basis of visibility from the blind. The time of day was recorded for each scan to allow correlation analysis between attendance patterns and predation patterns. These attendence data were collected independently of predation data. Statistical analyses were done using SAS (SAS Institute 1985) and BMDP (Dixon 1983). Sexspecific differences in nest care were tested with Wilcoxon signed-ranks tests. Associations between variables were tested with Kruskal-Wallis tests or Spearman rank correlations.
RESULTS General Description of Predation Between 17 June and 10 July 1983, 147 predation attempts by laughing gulls were recorded. Fortyeight (33%) of these resulted in the successful capture of black skimmer chicks. Here I report on 99 attempts, including 26 (26%) successful ones, that occurred at the 34-nest study area during 2804 nest-h of observation. Only one egg from the 34 study area nests was observed being preyed upon by a gull. The predatory behaviour of laughing gulls was divided into two components, patrols and predation attempts. When patrolling, gulls flew about 3 m above the skimmer colony, apparently scanning over many nests. Usually only one gullengaged in patrolling at a time, though on occasion two patrolled simultaneously. Patrolling gulls were not mobbed by skimmers. The usual response of a brooding skimmer to a patrolling gull was to remain on the nest and vocalize with a series of
0.09
0.08
0.07
0-05 "
.g_
0.04
,
o o7_ 0.0~
~ "'X
0-02
0.01
0
0-3
4-7 8-11 Brood age (days)
12-15
Figure l. Mean rate of predation attempts as a function of brood age. o: all attempts; e: successfulattempts. Bars are _+lsE.
monosyllabic barks. A predation attempt consisted of a steep dive toward one particular nest, typically resulting in physical contact with the parent skimmer or chick and/or an attempt to grasp a chick (in the gull's bill) and fly off with it, Six successful gull attacks occurred when skimmer chicks were noted as already being exposed (e.g. during feedings or nest reliefs). Often, the gull swooped down and physically rammed the brooding skimmer parent, knocking it off the nest, then seized the exposed chick and departed. Ramming was specifically recorded in four successful attacks (but full details were often not recorded). Skimmer defences against ramming included crouching on the nest and acting as a physical barrier against the ramming gull, or a more active defence involving flying a collision course towards the swooping gull and attempting to disrupt its dive. Defensive flights by solo parents necessitated leaving the chicks unprotected for a few seconds. Predation Attempt and Success Rates Predation was apparently an important source
Quinn: Predation defence by skimmerparents Table I. Parental attendance patterns as a function of black skimmer brood age Brood age (days) 0-3*
4 7t
8 11;~
12 15w
Parent BR** ST BR ST BR ST BR ST Female Male
288 326
163 175 124 86 172 186 123 66
125 18 110 125 12 95
* Pooled G comparing frequencies of brooding by males and females= 2.35, r~s. t Pooled G=0-33, NS. 2~Pooled G= 2.64, NS. wPooled G = 1.21, NS. ** Number of records from hourly scan samples of the parent's sex and activity (BR: brooding; ST: standing).
of mortality among black skimmer chicks in this colony. Of the 92 young hatching (in 34 nests), 62 (67%) disappeared before chicks reached 1 week of age. Twenty-six predations were actually observed. Predation success rates (per brood-h) varied with brood-age (Kruskal-Wallis test H = 13.1, dJ=3, P<0.01; Fig. 1), though the highest rates were during brood ages 4-7 days. Attempt rates did not vary significantly with brood-age ( H = 5-93, df= 3, NS; Fig. 1) but were highest during brood ages 4-7 days. Similarly, success rates varied with brood-age when they were based on the number ofchick-h of observation (H=13.2, df=3, P<0.01). Again, there was no trend in attempt rates per chick-h as a function of brood-age ( H = 5-75, df= 3, NS). Nests that were attended by both parents were more likely to attract predators. Biparentally attended broods were attacked more frequently than singly attended broods as measured by attempted (singly attended )?= 1.13; doubly attended 27= 2.04, N = 23 nests, Wilcoxon signedranks test, Ts = 32, P < 0.005) and successful predations (singly attended J?=0-54, doubly attended 37=1.08, N = 1 3 nests, T~=16, P<0.025). These analyses assumed an equal availability of nests attended by one or two parents. Expected values for attack rates on singly versus doubly attended nests were calculated for each nest by multiplying the number of predation events at a given brood age by the percentage of incubation records indicating double versus single attendance for that brood age. Expected values for all nests were equal
537
or greater for the singly attended condition. Thus, the analyses presented are conservative, and standardization to account for availability of doubly versus singly attended nests according to date would increase the significance. Predation attempts during chick feedings were significantly more likely to be successful (four of five) than attempts during non-feeding activities (11 of 63; Fisher's exact test, P = 0.007). Feeding of young chicks typically involves the presence of both parents (one broods while the other offers food) and requires that chicks be partially exposed. Although male and female skimmers brooded the young and stood guard near the nest for similar amounts of time within each age-class (Table I), the rate of predation attempts differed as a function of the brooding parent's sex. Attempts were significantly less frequent when the male parent was on the nest (male attended J?=0.87, female attended J?= 1-94, N = 16 nests, Ts= 22, P<0.01). This bias was especially marked when only one parent was in attendance (male attended J?= 0-25, female attended )?= 2.37, N = 8, T~= 3.5, P < 0.025). During 24 attacks on nests that were attended by both parents, there was no bias according to the sex of the adult incubating for all attempts: males and females each were incubating during 12 attempts. Comparable analyses on predation successes was complicated by the smaller number of complete observations. Sex of the brooding parent was determined in 14 such cases: six males and eight females. In three of the four predations involving solo parents, the brooding adult was female. When both parents attended and the sex of the brooding adult was known, males brooded during four predations, females during five (the number of parents attending was not recorded in one predation at a male brooded nest). Males (N= 46) were as likely to fly in chase of gulls after predation attempts as females (N= 45). When both parents were present during a gull attack with suitable observations, males defended the young on 11 occasions, females on five. The frequency of reported subjective evaluations of which sex defended the young was too low to warrant testing. To determine whether nest attendance patterns reduced the occurrence of risky solo brooding by females after hatching began (especially during early chick development), I compared nest attendance behaviour for 11 pairs observed during the 8-day period before the first egg hatched with that
Animal Behaviour, 38, 3
538
0.4
Table II. Spearman rank correlations between hourly predation success (per brood-h observed)or total attempt rates and hourly mean scan sample records* for each sex for each of the daylight hours
h
o 0.5
Predation event Successful
0.2
Brood care pattern
~- 0.1
0 _8/_7_ -6--5
I
I I I O- I -2--I 2-5 Brood age (doys)
-4--3
I
4-5
I 6-7
Figure 2. Proportion of brooding records for lone males and femalesas a function of brood-age, rn: lone males; I1: lone females. Bars are _+lSE. observed during the 8-day period thereafter (i.e. starting when the first egg in a clutch hatched). The proportion of solo male incubation/brooding records was lower before hatching 0~= 0-14_+0"02) than after, but not significantly so (_~= 0.21 + 0"037; Wilcoxon signed-ranks test T,= 19-0, NS). However, the proportion of solo female incubation/brooding records was significantly higher before hatching 0?=0.33+0-050) than after hatching 0?=0.24_+0.022; T,=10-0, P < 0.05; Fig. 2). Thus, there was a parental care shift between the incubation and chick rearing stages that consisted of a reduction in the amount of solo female attendance during the risky earlynestling stage. During the early stages of chick growth, biparental attendance typically involved one parent brooding while the other stood by the nest. There was a statistically non-significant decline in the incidence of bi-parental nest attendance with the age of the brood during the first eight days post hatching ( H = 12.8, df= 7, 0.1 > P > 0.05). To determine on a finer scale whether scheduling of nest attendance matched hourly patterns of chick predation events by gulls, I examined hourly scan-sampled attendance patterns by male and female skimmers with broods aged 0-15 days. ThE hourly patterns of predation attempts and successes were quite erratic, but showed significant positive correlations between rates of successful predation and bi-parental attendance (Table II).
rho
Lone parent brooding -0.35 Lone male brooding -0.48 Lone female brooding -0-27 Male standing byt 0.33 Female standing byt 0.51 Both attending:~ 0-64 One attending:~ -0.45 None attending$ 0-01
All attempts
(P)
rho
(P)
(0.20) (0.07) (0.33) (0.22) (0.049) (0.009) (0.09) (0.96)
-0.27 -0.45 -0-05 0.04 -0.06 0-12 -0.02 0.04
(0.32) (0.09) (0.85) (0.89) (0.84) (0.67) (0.93) (0.89)
* Collected independently of the predation data from a subset of 11 nests. ~ While mate is brooding. Includes brooding and standing by.
These correlations held also for the patterns of (non-brooding) female attendance, but not for (non-brooding) male attendance (Table II). No significant correlations were found when hourly patterns of all attempts were examined (Table II).
DISCUSSION Predation was an important source of chick mortality in this study and may be an active selection force influencing parental care patterns. Although some chick disappearances may have resulted from scavenging (i.e. death preceded removal), actual predation events by laughing gulls were observed frequently during this study. Laughing gulls appeared to be the only major predators taking young skimmers. Burger (1982) reported that laughing gulls, herring gulls, Larus argentatus, American oystercatchers, Haematopus palliatus, and a mink, Mustela vison, were active predators on black skimmers nesting on islands along the New Jersey coast. Only laughing gulls and oystercatchers were present in Lavaca Bay and I found no evidence of predation by the latter. Predation rates decreased with brood age (Fig. 1). This deline was not due merely to a decrease in the numerical availability of potential victims, and probably reflects a prey-size limitation on laughing
Quinn: Predation defence by skimmer parents gulls, which swallow fresh prey whole (see Quinn & Morris 1986). Periods of high risk to the offspring were expected to coincide with bi-parental guarding of the brood and/or deployment of care by the parent better able to reduce predation. Surprisingly, the presence of both parents did not thwart predatory attempts. Indeed it was positively related to the likelihood of predation. This apparent increase was not because bi-parental care predominated during diurnal periods of high predator activity. Once hatching began, the amount of bi-parental nest attendance decreased, presumably as a function of both: (1) the necessity to provide prey for the young at an increasing rate as metabolic needs increase (Ricklefs 1974); and (2) the broods' increasing abilities at thermoregulation (Ricklefs 1974). The association between predation events and periods of bi-parental attendance may be the result of constraints over which parents have little or no control. Certain activities (e.g. young chick feedings and possibly parental change-overs) that seem to increase the susceptibility of the young occur only when both pair members are present. Brooding change-overs reveal the contents of the nest and expose the offspring to predation attempts, especially if the parents engage in any mutual social interactions that temporarily reduce their attentiveness to the chicks. To some extent, the feeding of chicks automatically exposes them. Such exposure generally increases with chick age (personal observation) and may present opportunities for predators. Predation attempts during chick feedings, though infrequently observed, were highly successful. The low numbers of attempts observed during chick feeding may reflect the brevity, relative infrequency, and sporadic nature of that activity. Gulls were less likely to attack a skimmer nest being brooded by a male parent than one brooded by a female, supporting my second prediction. Despite this difference in attempt rates, there were no significant differences in success rates between the sexes (though that may be a consequence of few predation-success records that include brooder's sex). The larger size of male skimmers may provide a more effective defence against laughing gulls. Detailed studies of predation by intermediate-sized predators on other species with sexually dimorphic parents will test the generality of these findings. Periods of the day when bi-parental attendance was common were those periods when successful
539
predation occurred frequently in the colony as a whole. The correlation between bi-parental attendance frequency and predation success apparently resulted from a high incidence of male brooding and female attendance during periods of high predation risk. This probably reflects, in part, risks at chick feeding times. Young chicks are fed more often by their mothers than their fathers (Quinn 1988) and must emerge from under the brooding parent to take the prey. Alternatively, during periods when feedings were infrequent, brooding females with mates standing by might be effective at deterring, or discouraging predators. Such periods may yield few opportunities for predation. Predation rate as a function of time of day may simply reflect predation attempts whenever gulls perceived a possible opportunity. It follows that skimmer brooding roles should reflect the differential response by laughing gulls to male versus female parents. Specifically, male skimmers may be most effectively deployed as solo brooders of vulnerable young chicks. Although the results presented here show no difference in the chick-brooding behaviour of male and female skimmers, males are reported to engage in more brooding than females elsewhere (Burger 1981). Though patterns of parental care have been attributed to size-related differential ability to defend young (e.g. Andersson & Norberg 198t; Wiklund & Stigh 1983), alternative explanations for patterns of parenal care may or may n o t build on sexual size dimorphism, Risky nest defence by male great tits and male northern mockingbirds has been attributed to skewed adult sex ratios (Breitwisch 1988) or sex-specific differences in mortality during the breeding season (Regelmann & Curio 1986). There appears to be no evidence for skewed sex ratios in black skimmers, and sex-specific differences in mortality during breeding are not apparent (Quinn 1988). However, decreased solo female participation in the care of the young (to levels shown by males) following hatching may be due, in part, to the increased role females play in feeding very young chicks (Quinn 1988), Females delivered prey that were smaller than those delivered by males (Quinn 1988). Male skimmers fed their chicks more as their broods grew older (Quinn 1988) and presumably became less susceptible to laughing gull predation. Males delivered larger prey to the young (Quinn 1988) at a time when chicks were larger and probably more efficient at
540
Animal Behaviour, 38, 3
swallowing large prey and when their metabolic requirements were higher. Any increase in the parental efficiency regarding chick feeding may serve to accelerate chick growth to a size of reduced susceptibility to predators and other sources o f mortality. The shift in skimmer parental care patterns at the time of first hatching may be an adaptive response to predation on young chicks. O f three colonies of skimmers observed in Lavaca Bay (Quinn 1988), two were in close proximity to nesting laughing gulls. The colony lacking laughing gull neighbours was the only one at which significantly greater brood attendance by females was detected (Quinn 1988). Thus, the parental care response of decreased solo female care may be facultative, though further investigation is necessary.
ACKNOWLEDGMENTS I thank Linda A. Whittingham and David Clugston for assistance in the field. Kent Ruffin, Nance Matus and a number of others provided occasional voluntary assistance. Various drafts of this manuscript were critiqued by T o d d A. Crowl, Katherine D. Graham, Patricia Schwagmeyer, Frank Sonleitner, James N. Thompson, Bedford Vestal and especially Douglas Mock. Charles T. Snowdon, Lee C. Drickamer and two anonymous referees provided helpful comments on the submitted manuscript. Peter W. Bergstrom, Gary D. Schnell and F r a n k Sonleitner provided statistical advice. Dan H o u g h provided computer assistance and Diane Fields proof-read the manuscript. Coral McCallister prepared the figures. This paper was written as a portion of my doctoral dissertation. Financial support was generously provided by the R o b b and Bessie Welder Wildlife Foundation, the Natural Sciences and Engineering Research Council (Canada), the American Ornithologists' U n i o n (Josselyn Van Tyne Award), the Wilson Ornithological Society (Stewart Award), the American Museum of Natural History (Mac P. Smith Award), Sigma Xi (Grants in Aid of Research), the University of Oklahoma (Department of Zoology research support; Associates F u n d Research Grant; Foundation Research Grant), and the R. L. Disney International Student Scholarship. This is contribution number 329 of the Welder Wildlife Foundation.
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Quinn: Predation defence by skimmer parents Quinn, J. s. 1988. Sexual size dimorphism and parental care: a comparative study of black skimmers and Caspian terns and a computer simulation model. Ph.D. thesis, University of Oklahoma, Norman. Quinn, J. S. & Morris, R. D. 1986. Intra-clutch eggweight apportionment and chick survival in Caspian terns. Can. J. Zool., 64, 2116-2122. Regelmann, K. & Curio, E. 1986. Why do great tit (Parus major) males defend their brood more than females do? Anita. Behav., 34, 1206-1214. Ricklefs, R. E. 1969. An analysis of nesting mortality in birds. Smithson. Contrib. Zool., 9, 1-48. Ricklefs, R. E. 1974. Energetics of reproduction in birds. In: Avian Energetics (Ed. by R. A. Paynter, Jr), pp. 152292. Cambridge, Massachusetts: Nuttall Ornithological Club. Safina, C. & Burger, J. 1983. Effects of human disturbance on reproductive success in the black skimmer. Condor, 85, 164-171.
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SAS Institute Inc. 1985. SAS User's Guide." Statistics. Cary, North Carolina: SAS Institute. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man 1871 1971 (Ed. by B. Campbell), pp. 136 179. Chicago: Aldine. Veen, J. 1977. Functional and causal aspects of nest distribution in colonies of the sandwich tern (Sterna s. sandvicensis Lath.). Behav. Suppl., 20, 1-193. Verner, J. & Willson, M. F. 1969. Mating systems, sexual dimorphism, and the role of male North American passerine birds in the nesting cycle. Ornithol. Monogr., 9, 1 76. Wiklund, C. G. & Stigh, J. 1983. Nest defence and evolution of reversed sexual size dimorphism in snowy owls Nyctea scandiaca. Ornis Scand., 14, 58 62.
(Received 28 July 1988; revised 1 November 1988; MS. number: A5245)