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Offspring growth in the California gull: reproductive effort and parental experience hypotheses
A&l. Behav., 1995, 49, 641-647
Offspring growth in the California gull: reproductive effort and parental experience hypotheses National
Department
Biological
of Biology,
BRUCE H. PUGESEK Survey, Southern Science Center, 700 Cajundome Blvd. Lafayette. LA 70506, U.S.A. and The University of Southwestern Louisiana, P. 0. BO.Y 42451. Lafa.vette. LA 70504-2451, U. S. A.
(Received
28 October
1993;
inirial
final acceptance 10 February
acceptance 24 November 1993, 1994: MS. number: ~6671~)
Abstract. Measures of adult feeding and foraging behaviour in the California gull, Larus californicus, were related to the growth of their offspring. Offspring showed significantly higher growth when average feeding interval, a measure of the time interval between feedings, and feeding latency following foraging decreased. The amount of time parents foraged was positively related to offspring growth and negatively correlated with average feeding interval. Either (1) increased foraging efficiency with parental age, or (2) increased reproductive effort with age, could explain age-related differences in patterns of feeding behaviour and their impact on offspring growth. However, data on foraging time support only the hypothesis of increased reproductive effort with parental age.
hypotheses explaining why the offspring of older parents have higher growth rates than the offspring of younger parents are: (1) adults gain experience with age and thus become more efficient at foraging and (2) adults increase reproductive effort as they age (Pugesek 1983). The parental experience hypothesis (Lack 1966; Nur 1984) assumes that older adults can gather food more quickly than younger adults and are, therefore, able to provide more food to offspring. The reproductive effort hypothesis (Williams 1966; Gadgil & Bossert 1970; Pianka & Parker 1975; Charlesworth & Leon 1976) assumes that older adults provide more food to offspring by working harder at foraging. Greater effort in foraging implies a cost of reduced ability to invest in future offspring. Among seabirds, increased foraging efficiency has been suggested as an explanation for increased egg mass (Mills 1979; Mills & Shaw 1980), clutch size (Mills 1979) and offspring growth rates (Ainley & Schlatter 1972), which in turn lead to higher fledging success among older birds compared with younger birds (Ashmole 1963; Lack 1968; Nur 1984). However, none of these studies measured any behaviour patterns associated with foraging.
Studies cited as evidence of age-related increases in foraging efficiency are investigations of prey capture success rates comparing one or more sexually immature age classes to mature adults (Orians 1969; Dunn 1972; Buckley & Buckley 1974; Verbeek 1977; Ingolfsson & Estrella 1978; Morrison et al. 1978; Searcy 1978). These cross-sectional studies cannot determine whether individual breeding adults actually improve foraging skills with age (Pugesek 1984). Furthermore, in studies where several age classes of immatures were observed, the abilities of immatures improved to near parity with those of adults (Orians 1969; Ingolfsson & Estrella 1978). These results suggest that birds reach a plateau by the age of breeding, after which little improvement in firaging skills can be expected. Although skill may not improve once birds reach sexual maturity, experience with the breeding area may help them to locate sources of food more efficiently (Lack 1966; Orians 1969). Any advantage that knowledge of foraging sites might have on individual foraging efficiency may be reduced by the social nature of feeding of many seabirds. In many species, birds often lead one another to food sources (Evans 1982).
Two
0003-3472/95/030641+07
$08.00/O
c 1995 The 641
Association
for the Study
of Animal
Behaviour
642
Animal
Behaviour,
Investigations of the foraging behaviour of known-aged adults support the reproductive effort hypothesis (Pugesek 1981, 1983). Older gulls take longer foraging trips, spend greater amounts of time foraging, and conversely less time at the nest site compared with younger gulls. Older gulls also feed offspring more frequently and have shorter latencies to feed young after foraging. Previous investigations assumed that greater rates of feeding and time spent foraging translate into benefits to offspring. Here I present data relating adult feeding rates, feeding latencies and foraging time to offspring growth rates. These results combined with age-related differences in feeding and foraging behaviour published elsewhere (Pugesek 1981, 1983) are used to evaluate the parental experience and reproductive effort hypotheses. To evaluate either hypothesis it is essential to demonstrate that feeding rates and latencies are valid indicators of the amount of food delivered to offspring. I measured three patterns of feeding behaviour: feeding rate, average feeding interval (time interval between feedings), and latency to feed offspring after returning from foraging. If these patterns of feeding behaviour are good indicators of amounts of food delivered to offspring, then: (1) offspring growth should be positively related to feeding rate and negatively related to average feeding interval and feeding latency; (2) feeding rate should be negatively related to average feeding interval and feeding latency; and (3) the average feeding interval should be positively related to feeding latency (Fig. 1). If all of the above relations are satisfied, the parental experience and reproductive effort hypotheses can be evaluated by examining the relationships between the amount of time spent foraging and offspring growth and feeding behaviour. If foraging time is negatively related to offspring growth, this would indicate that some adults are more efficient than others and can obtain high growth for their offspring with less time spent foraging (parental experience hypothesis). This conclusion implies that the amount of time spent foraging is directly related to the amount of food that is transferred to offspring. Further support for the parental experience hypothesis would be obtained, therefore, if the amount of time spent foraging is negatively related to feeding rate, and positively related to average feeding ‘interval and feeding latency (Fig. 1).
49, 3 (a)
FL
FR
FL
AFI
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\
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+
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(b)
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OG
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AFI I- -‘\ FL
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+ ‘.
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+
Figure 1. The direction of relationships anticipated between variables if results support (a) the parental experience hypothesis and (b) the reproductive effort hypothesis. Variables are feeding rate (FR), average feeding interval (AFI). feeding latency (FL), offspring growth (OG) and foraging time (FT). Dashed lines enclose the relationships between patterns of feeding behaviour and offspring growth required if patterns of feeding behaviour are valid indicators of amounts of food delivered to offspring. Dotted lines enclose the relationships between foraging time and other variables required to support the respective hypotheses. If adult reproductive effort determines the amount of offspring growth, relationships opposite to those described above will be observed (Fig. 1). Foraging time should be positively related to offspring growth. In addition, foraging time should be positively related to feeding rate, and negatively related to average feeding interval and feeding latency. These results would indicate that greater amounts of offspring growth are a result of greater amounts of food provided by parents that work harder at foraging.
METHODS I collected data on California gulls, Laws californicus, nesting in 1979 and 1980 on Bamforth Lake, Albany County, Wyoming. Gulls foraged primarily at nearby lakes and the Laramie River and were largely dependent on natural food sources (Kennedy 1973; Pugesek 1983). I located adult gulls on the nesting territory and marked 29 nests with coded stakes (2 X
Pugesek: California 5 x 30 cm). I censused clutch size at staked nests every other day during egg laying. During the hatching phase, I censused nests daily. I used two-chick broods to control for variation in growth due to differences in brood size. I weighed both chicks with a 100-g Pesola scale and banded them with a numbered plastic band on the day the second chick hatched (day 1) and weighed them again 6 days later (day 6). I calculated total growth as the difference between day 6 and day 1 total brood mass. Owing to mortality of chicks at 10 nests and to inclement weather, which prevented re-weighing at two nests, the sample was reduced to 17 broods of two chicks each. I measured parental behaviour during l-h observation periods conducted within the 6-day period of offspring growth described above. I collected data between 1000 and 1400 hours and selected nests randomly for observation within this time period. I calculated feeding rate as the number of feedings per brood that occurred during each l-h observation period. Parental behaviour was not classified as feeding unless food was transferred from adult to offspring. I classified feedings separated by 1 min or more as separate feedings. I calculated the average feeding interval as the total number of minutes of attendance by both parents divided by the number of feedings. If no feedings occurred, I calculated the average feeding interval as the total number of minutes of attendance by both parents. I calculated feeding latency as the number of minutes elapsed from arrival of a parent after foraging until it began feeding offspring. In one case when feeding did not occur within 30 min the observation was terminated and a latency of 30 min was assigned. I calculated foraging time as the total number of minutes both parents foraged during the l-h observation period. Previously, I determined that parents did not rest elsewhere on or away from the breeding colony (Pugesek 1983). While absent, parents were either en route to or from the colony or actively searching for food. Thus, time away from the nest measures time spent foraging. I conducted observations from a S-m observation tower situated on the periphery of the colony. Only nests further than 35 m from the tower were observed. At these distances no disturbance to adults was noted nor was fledging success
gull ofsspring growth
643
adversely affected (Pugesek 1983; Pugesek & Diem 1983). Nests represented the sampling unit for analysis of behavioural data. Data were collected on both mates. Individuals were distinguished by deter‘mining whether they were banded or unbanded. 1 conducted one to four l-h observations of adults at each nest. No nest was measured twice on the same day and nests were selected randomly for observation over the 6&y measurement period. Data from both mates were pooled and averaged over l-h observation periods at each nest. or in the case of feeding latency, the number of observations at each nest. Because I was unable to measure all behaviour patterns during each l-h observation period the numbers of observations and the total number of sampling units for each behaviour category represent a subset of the total sample of 17 nests. For example, when the foraging parent did not return to the nest during the observation period, I was unable to obtain a measure of feeding latency. In addition, I was unable to observe feedings when parents stepped behind shrubs during part of the observation period, however, 1 was able to measure attendance of parents for measures of foraging time. Total observations and sampling units obtained for each variable were as follows: feeding rate and average feeding interval: 26 h of observation at 11 nests (range: 14 h); feeding latency: 17 observations at 11 nests (range: 14 observations); foraging time: 31 h of observation at 12 nests (range: l-4 h). I used regression analyses to examine relationships between the behaviour of each mated pair and the growth of their offspring. I used Pearson’s product-moment correlation to investigate associations between patterns of behaviour. One adult at each nest had been previously banded and was of known age (3-17 years old). The band number of each bird was read with a spotting scope at the time the nests were marked. The ages of banded parents were determined later from banding records. Ages of mates on this colony are highly correlated (Pugesek & Diem 1986) and it was assumed that mates were the same or nearly the same age. Preliminary regression analyses related parental age to offspring growth and parental behaviour. Considerable variation exists in these variables with respect to parental age (Pugesek 1983) and in the small sample presented here, no significant relationships were found. This diminishes the probability that
Animal
644
Behaviour,
relationships between offspring growth and parental behaviour described in the Results are due to autocorrelation with parental age. Adult gulls at the 10 nests that were dropped from analysis because their offspring died before day 6 may have been less-efficient foragers than those used in the study. If less-efficientadults were excluded from the study, thereby biasing results, they should be younger than those that remained in the study. One-way ANOVA was performed on the two groups and no significant differences were found in the ages of the 10 adults not used in the study compared with the 17 used in the study. It is assumed here that the chicks of adults that were excluded from the study died as a result of predation events and that the deaths were not related to the foraging efficiency of the parents. I tested data for violations of assumptions of the statistical tests performed and applied transformations as necessary (Sokal & Rohlf 1969).
49, 3
280
- (a)
Y= 347.3 -4.0x
_:! 80 1
I
30
280
3
Feeding rate was positively related to total growth of chicks; however, the relationship was not significant (9 = 0.3 1, F, ,9=4.04, DO.07; regression equation: Y= 128.8+52.2x). The lack of signiticance was due, in part, to the low number of possible values of the feeding rate measure. Only four rates of feeding occurred (0.5, 0.7, 1.0 and 2.0 feedings/h). Offspring growth declined with increasing average feeding interval (Fig. 2a; ?=0.42, F,;1.9=6.46,PcO.05). Latencies to feed were inversely related to total offspring growth (Fig. 2b; ?=0.49, Fl ,=8.57, PcO.05). Thus, chicks gained lessweight’ if their parents waited longer to feed them. Foraging time was positively related to offspring growth (Fig. 2~; ?=0.35, F,,,,=5.48, PcO.05; total chick mass square-root transformed). Chicks tended to have high gains in mass if their parents quickly rotated guarding and foraging activities but low gains if both parents spent long periods together at the nest. Feeding latency was not significantly related to any of the behavioural variables measured (Table I). Average feeding interval decre?sed as feeding rate increased (Pearson’s r= - 0.76, N= 10, PcO.01). Feeding rate was not significantly correlated with foraging time. Average feeding interval was negatively correlated with foraging time (Pearson’s r= - 064, N= 10, PcO.05).
.
d
60
1
* Y= 223.12 -4.1X
6)
240
,
40 50 Average feeding interval (min)
i 200 E +j 2 u
160 120 I 10
,
280
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Cd
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30
+ 6.2X
240 -
sob
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20 Feeding latency (min)
0
RESULTS
1
240
.
I 50
*
I
55 Foraging time (min)
Figure2. Total growth of (a) average feeding (c) foraging time.
Ll
60
of two-chick broods as a function interval, (b) feeding latency and
DISCUSSION Feeding Rehaviour
and Offspring
Growth
Two of the expected relationships between patterns of feeding behaviour were not significant; that between feeding latency and feeding rate, and that between feeding latency and average feeding interval. The high correlation between feeding rate and average feeding interval indicates that the variables provided similar measures of the frequency of offspring feeding. While feeding rate measured the absolute number of feedings in a given time period, the average feeding interval measured the feeding interval per minute of
Pugesek: California Table I. Correlations
between
behavioural Feeding
Feeding Average Feeding Foraging
rate feeding latency time
interval
variables rate
with Average
sample
sizes followed
feeding
interval
645 by significance Feeding
level
latency
Foraging
time
rz
N
P
rz
N
P
r2
N
P
rz
1.0 - 0.76 - 0.66 0.20
10 7 10
0.01 0.11 0.58
I.0 0.55 -064
I 10
0.20 0.05
1.0 - 0.21
8
0.61
1.0
parental attendance at the nest. The former was a poorer predictor of offspring growth, in part, becauseonly four feeding rates were observed. Despite small sample sizes, average feeding interval was significantly related to total offspring growth and feeding rate was positively related to total offspring growth. Thus, frequency of feeding was a good indicator of the amount of food transfer to offspring. The amount of food provided by adults at each feeding may explain additional variation in growth rate. None the less, earlier observations (Pugesek 1981, 1983) that older gulls feed offspring more frequently than younger gulls are clearly related to faster growth and higher survival among their offspring (Pugesek1981, 1983). Older adults have significantly lower feeding latencies compared with younger adults at all measured offspring ages (l-45 days). This relationship holds regardless of whether comparisonsof age groups include data on all brood sizes (Pugesek 1983) or only brood sizes of two (Pugesek1990). Results here indicate that shorter feeding latencies are indicative of greater offspring growth. Parental Experience Hypotheses
gull offspring growth
and Reproductive
Effort
Either hypothesis, increased parental experience or increased reproductive effort, could explain why older adults feed chicks more frequently and sooner after returning from foraging trips. Younger adults may feed their chicks less frequently because they are less-efficient foragers. They may withhold food after returning from foraging becausetheir crops are not full enough to Provide the necessary stimulation to regurgitate, or because their crops are frequently empty. Another explanation for low feeding rates among Youngeradults is that they are less experienced at
recognizing and responding to chick signals for feeding than are older adults. The mechanisms responsible for this form of parental experience and those of increased reproductive effort with age, however, are not mutually exclusive (Pugesek 1983). The mechanism that produces increased reproductive effort with age is unknown. Reproductive effort may increase with age because adults require a period of 9 years or more to develop the necessary parental behaviour, or reproductive effort may increase, for example, because hormone levels increase with age. That a learning period of 9 or more years is required to successfully respond to offspring is arguable (Pugesek 1981). Age-related increasesin hormone levels could produce an identical increased responsivenessto offspring. Data on foraging time do not support the parental experience hypothesis. Efficient adults did not provide more feedings to offspring per unit time spent foraging than adults of lesser efficiency. In addition, offspring growth was not negatively related to foraging time and thus efficient adults did not transfer greater amounts of food to their offspring with less foraging effort. Although it would be clearly advantageous for adults to spend extra time guarding offspring while not engaged in foraging activities, low values of foraging time should not be construed as such an activity. Gulls that do so actually defend offspring less frequently and experience higher offspring mortality compared with gulls that spend little time at the nest site (unpublished data). It could be argued that highly efficient adults also spend more time foraging than less-efficient adults, thereby maximizing the benefit obtained in foraging and expenditure of reproductive effort. In this case, increased efficiency would both enhance and be masked by the relationship found
646
Animal Behaviour, 49, 3
between foraging time and offspring growth. However, adults of known age were used here and no autocorrelation was found between parental age and behavioural measures including foraging time (see Methods). This means that some of the adults that spent great amounts of time foraging were young and that some of the adults that spent little time foraging were old. Under these circumstances, the younger adults that spent great amounts of time foraging would have to be more efficient than their older counterparts. The parental experience hypothesis requires conversely that foraging efficiency improves as individuals age and thus individuals gain skill and experience necessary to confer greater reproductive success. Data on foraging time support the reproductive effort hypothesis. Gulls that transferred greater amounts of food to offspring did so by foraging longer than gulls that provided less food to their offspring. Younger adults spend less time foraging than do older adults (Pugesek 1981, 1983). Greater amounts of foraging clearly benefit offspring in terms of increased growth. However, to fully qualify as reproductive effort, increased foraging must result in a cost to the adult in terms of reduced ability to invest in future offspring (i.e. greater adult mortality). Older gulls may experience greater mortality if greater amounts of time spent away from the colony in foraging activities are more risky compared with resting at the nest site. Several observations indicate that the breeding colony is safer for adults than is the surrounding area. Coyote, Canis latrans, tracks have been observed to approach but never penetrate the colony. Numerous golden eagle, Aquilu chrysuetos, attacks on gulls have been observed. The majority of those attacks have been on gulls in flight to or from the colony; many of which have been successful as evidenced by visual observation and by gull carcassesfound in the area surrounding the colony. Only two attacks have been observed by eagles at the colony. In one instance, an eagle captured an adult gull but was forced to drop it by approximately 100 mobbing gulls. In another attempt, the eagle was forced to leave the colony by mobbing gulls before it could capture’ any prey. The fact that gulls do not rest away from the breeding colony (Pugesek 1983) further supports the conclusion that time spent away from the colony, including foraging, is risky.
The most serious threat to adult survival is probably the energetic drain of provisioning offspring (Pugesek 1987, 1990). Adults lose body mass throughout the course of the breeding season (Coulson et al. 1983; Monaghan et al. 1989; Pugesek & Diem 1990). The period of maximum adult mortality coincides with the end of the breeding season in herring gulls, Larus argentatus (Coulson et al. 1983; Monaghan & Metcalfe 1986) suggesting that the energy drain of reproduction results in mortality. Thus, not only the amount of time adults spend in foraging activities but how they divide the proceeds between themselves and offspring may influence their survival. When older adults provide more food to offspring with frequent feedings they are, conversely, retaining less for themselves. Parents feed their offspring partially digested boluses of food, Longer feeding latencies mean that adults retain food in the crop for extended periods of time. Presumably, more energy will be assimilated by the adult and less will be available for offspring when feeding latencies are longer. Thus, higher feeding frequencies and shorter feeding latencies among older adults support the reproductive effort hypothesis if older adults lose more body mass and risk death as a result of these behavioural differences. Older California gulls lose significantly more body mass and have lower survival compared with younger gulls at Barnforth Lake (Pugesek 1987; Pugesek & Diem 1990) indicating that this is the case. However, further study is required to make a direct causal link between behavioural differences and loss of body mass among adults of known age and between behavioural differences and mortality among adults. ACKNOWLEDGMENTS I thank Deborah Fuller, Scott Hatch, Joseph Jell and Ziad Malaeb for comments on early drafts of the manuscript. I also thank Francesca Cuthbert and Hugh Drummond for their insightful reviews of an early draft of this paper. Research support came from grants from NSF (DEB 791997), Sigma Xi, Wilson Ornithological Society, Chapman Foundation and NIA (T32-AGO01 lo03). I thank the U.S. Fish and Wildlife Service,the Arapaho National Wildlife Refuge and the
Pugesek:
California
Wyoming Game and Fish Department for their cooperation with ongoing research.
REFERENCES Ainley, D. G. & Schlatter, R. B. 1972. Chick raising ability in adelie penguins. Auk, 89, 559-566. Ashmole, N. P. 1963. The biology of the wideawake or sooty tern Sterna fiscata on Ascension Island. Ibis, 103,297-364. Buckley, F. G. & Buckley, P. A. 1974. Comparative feeding ecology of wintering adult and juvenile royal terns (Aves: Laridae, Stemidae). Ecology, 55, 1053-1063. Charlesworth, B. & Leon, J. A. 1976. The relationship of reproductive effort to age. Am. Nat., 110,449-459. Couison, J. C., Monaghan, P., Duncan, N., Sheddon, C. B. & Thomas. C. S. 1983. Seasonal changes in the herring gull in Britain: weight, moult and mortality. Ardea, 71, 235-244. Dunn, E. K. 1972. Effect of age on the fishing ability of sandwich terns Sterna sandvicensis. Ibis, 114,36&366. Evans, R. M. 1982. Foraging-flock recruitment at a black-billed gull colony: implications for the information center hypothesis. Auk, 99, 24-30. Gadgil, M. & Bossert, W. 1970. Life historical consequences of natural selection. Am. Nat., 104, l-24. Ingolfsson, A. & Estrella, B. T. 1978. The development of shell cracking behavior in herring gulls. Auk, 95, 577-579. Kennedy, J. R. 1973. A study of the breeding colony of California gulls (Larus californicus), Bamforth Lake, Albany County, Wyoming. M.S. thesis, University of Wyoming. Lack, D. 1966. Population Studies of Birds. Oxford: Clarendon Press. Lack, D. 1968. Ecological Adaptations for Breeding Birds. London: Methuen. Mills, J. A. 1979. Factors affecting the egg size of red-billed gulls Larus novaehollandiae scooulinus. Ibis. 121, 53-67: Mills, J. A. & Shaw, P. W. 1980. The influence of age on laying date, clutch size, and egg size of the whitefronted tern, Sterna striata. N. Z. Jl Zool., 7, 147-153. Monaghan, P. & Metcalfe, N. B. 1986. On being the right size: natural selection and body size in the herring gull. Evolution, 40, 10961099.
gull
offspring
growth
641
Monaghan, P., Uttley, J. D., Burns, M. D., Thaine, C. & Blackwood, J. 1989. The relationship between food supply, reproductive effort and breeding success in arctic terns Sterna paradisaea. J. Anim. Ecol., 58, 261-274. Morrisson, M. L., Slack, R. D. & Shanley, E., Jr. 1978. Age and foraging ability relationships of olivaceous cormorants. Wilson Bull., 90, 414422. Nur, N. 1984. Increased reproductive success with age in the California gull: due to increased effort or improved skill. Oikos. 43. 407408. Orians, G. H. 1969. Age &id hunting success in the brown pelican (Pelicanus occidentalis). Anim. Behav., 17,316319. Pianka, E. R. & Parker, W. S. 1975. Age-specific reproductive tactics. Am. Nat., 109, 453-464. Pngesek, B. H. 1981. Increased reproductive effort with age in the California gull (Larus cahyornicus). Science, 212, 822-823. Pugesek, B. H. 1983. The relationship between parental age and reproductive effort in the California gull (Larus californicus). Behav. Ecol. Sociobiol., 13, 161-171. Pugesek, B. H. 1984. Age-specific reproductive tactics in the California gull. Oikos, 43, 409410. Pugesek, B. H. 1987. Age-specific survivorship in relation to clutch size and fledging success in California gulls. Behav. Ecol. Sociobiol., 21, 217-221. Pugesek, B. H. 1990. Parental effort in the California gull: tests of parentoffspring conflict theory. Behav. Ecol. Sociobiol., 27, 211-215. Pugesek, B. H. & Diem, K. L. 1983. A multivariate study of the relationship of parental age to reproductive success in California gulls. Ecology, 64, 829-839. Pugesek, B. H. & Diem, K. L. 1986. Ages of mated pairs of California gulls. Wilson Bull., 98, 61&612. Pugesek, B. H. & Diem, K. L. 1990. The relationship between reproduction and survival in known-aged California gulls. Ecology, 71, 81 l-817. Searcy, W. A. 1978. Foraging success in three age classes of glaucous-winged gulls. Auk, 95, 587-588. Sokal, R. R. & Rohlf, F. J. 1969. Biometry. San Francisco: W. H. Freeman. Verbeek, N. A. M. 1977. Comparative feeding behaviour of immature and adult herring gulls. Wilson Bull., 89,415421. Williams, G. C. 1966. Adaptation and Natural Selection. Princeton, New Jersey: Princeton University Press.
Offspring growth in the California gull: reproductive effort and parental experience hypotheses National
Department
Biological
of Biology,
BRUCE H. PUGESEK Survey, Southern Science Center, 700 Cajundome Blvd. Lafayette. LA 70506, U.S.A. and The University of Southwestern Louisiana, P. 0. BO.Y 42451. Lafa.vette. LA 70504-2451, U. S. A.
(Received
28 October
1993;
inirial
final acceptance 10 February
acceptance 24 November 1993, 1994: MS. number: ~6671~)
Abstract. Measures of adult feeding and foraging behaviour in the California gull, Larus californicus, were related to the growth of their offspring. Offspring showed significantly higher growth when average feeding interval, a measure of the time interval between feedings, and feeding latency following foraging decreased. The amount of time parents foraged was positively related to offspring growth and negatively correlated with average feeding interval. Either (1) increased foraging efficiency with parental age, or (2) increased reproductive effort with age, could explain age-related differences in patterns of feeding behaviour and their impact on offspring growth. However, data on foraging time support only the hypothesis of increased reproductive effort with parental age.
hypotheses explaining why the offspring of older parents have higher growth rates than the offspring of younger parents are: (1) adults gain experience with age and thus become more efficient at foraging and (2) adults increase reproductive effort as they age (Pugesek 1983). The parental experience hypothesis (Lack 1966; Nur 1984) assumes that older adults can gather food more quickly than younger adults and are, therefore, able to provide more food to offspring. The reproductive effort hypothesis (Williams 1966; Gadgil & Bossert 1970; Pianka & Parker 1975; Charlesworth & Leon 1976) assumes that older adults provide more food to offspring by working harder at foraging. Greater effort in foraging implies a cost of reduced ability to invest in future offspring. Among seabirds, increased foraging efficiency has been suggested as an explanation for increased egg mass (Mills 1979; Mills & Shaw 1980), clutch size (Mills 1979) and offspring growth rates (Ainley & Schlatter 1972), which in turn lead to higher fledging success among older birds compared with younger birds (Ashmole 1963; Lack 1968; Nur 1984). However, none of these studies measured any behaviour patterns associated with foraging.
Studies cited as evidence of age-related increases in foraging efficiency are investigations of prey capture success rates comparing one or more sexually immature age classes to mature adults (Orians 1969; Dunn 1972; Buckley & Buckley 1974; Verbeek 1977; Ingolfsson & Estrella 1978; Morrison et al. 1978; Searcy 1978). These cross-sectional studies cannot determine whether individual breeding adults actually improve foraging skills with age (Pugesek 1984). Furthermore, in studies where several age classes of immatures were observed, the abilities of immatures improved to near parity with those of adults (Orians 1969; Ingolfsson & Estrella 1978). These results suggest that birds reach a plateau by the age of breeding, after which little improvement in firaging skills can be expected. Although skill may not improve once birds reach sexual maturity, experience with the breeding area may help them to locate sources of food more efficiently (Lack 1966; Orians 1969). Any advantage that knowledge of foraging sites might have on individual foraging efficiency may be reduced by the social nature of feeding of many seabirds. In many species, birds often lead one another to food sources (Evans 1982).
Two
0003-3472/95/030641+07
$08.00/O
c 1995 The 641
Association
for the Study
of Animal
Behaviour
642
Animal
Behaviour,
Investigations of the foraging behaviour of known-aged adults support the reproductive effort hypothesis (Pugesek 1981, 1983). Older gulls take longer foraging trips, spend greater amounts of time foraging, and conversely less time at the nest site compared with younger gulls. Older gulls also feed offspring more frequently and have shorter latencies to feed young after foraging. Previous investigations assumed that greater rates of feeding and time spent foraging translate into benefits to offspring. Here I present data relating adult feeding rates, feeding latencies and foraging time to offspring growth rates. These results combined with age-related differences in feeding and foraging behaviour published elsewhere (Pugesek 1981, 1983) are used to evaluate the parental experience and reproductive effort hypotheses. To evaluate either hypothesis it is essential to demonstrate that feeding rates and latencies are valid indicators of the amount of food delivered to offspring. I measured three patterns of feeding behaviour: feeding rate, average feeding interval (time interval between feedings), and latency to feed offspring after returning from foraging. If these patterns of feeding behaviour are good indicators of amounts of food delivered to offspring, then: (1) offspring growth should be positively related to feeding rate and negatively related to average feeding interval and feeding latency; (2) feeding rate should be negatively related to average feeding interval and feeding latency; and (3) the average feeding interval should be positively related to feeding latency (Fig. 1). If all of the above relations are satisfied, the parental experience and reproductive effort hypotheses can be evaluated by examining the relationships between the amount of time spent foraging and offspring growth and feeding behaviour. If foraging time is negatively related to offspring growth, this would indicate that some adults are more efficient than others and can obtain high growth for their offspring with less time spent foraging (parental experience hypothesis). This conclusion implies that the amount of time spent foraging is directly related to the amount of food that is transferred to offspring. Further support for the parental experience hypothesis would be obtained, therefore, if the amount of time spent foraging is negatively related to feeding rate, and positively related to average feeding ‘interval and feeding latency (Fig. 1).
49, 3 (a)
FL
FR
FL
AFI
’I-
‘l,+
\
OGI+ L-------------
-
‘A -
Jq
+
+
AFI
FL
(b)
:-
FR
OG
‘1 -
OG
I ‘.
AFI I- -‘\ FL
i I-
‘l,,
+ ‘.
-1
+ OG IL--_-___------1
-‘\
$y-+
-
-
+
Figure 1. The direction of relationships anticipated between variables if results support (a) the parental experience hypothesis and (b) the reproductive effort hypothesis. Variables are feeding rate (FR), average feeding interval (AFI). feeding latency (FL), offspring growth (OG) and foraging time (FT). Dashed lines enclose the relationships between patterns of feeding behaviour and offspring growth required if patterns of feeding behaviour are valid indicators of amounts of food delivered to offspring. Dotted lines enclose the relationships between foraging time and other variables required to support the respective hypotheses. If adult reproductive effort determines the amount of offspring growth, relationships opposite to those described above will be observed (Fig. 1). Foraging time should be positively related to offspring growth. In addition, foraging time should be positively related to feeding rate, and negatively related to average feeding interval and feeding latency. These results would indicate that greater amounts of offspring growth are a result of greater amounts of food provided by parents that work harder at foraging.
METHODS I collected data on California gulls, Laws californicus, nesting in 1979 and 1980 on Bamforth Lake, Albany County, Wyoming. Gulls foraged primarily at nearby lakes and the Laramie River and were largely dependent on natural food sources (Kennedy 1973; Pugesek 1983). I located adult gulls on the nesting territory and marked 29 nests with coded stakes (2 X
Pugesek: California 5 x 30 cm). I censused clutch size at staked nests every other day during egg laying. During the hatching phase, I censused nests daily. I used two-chick broods to control for variation in growth due to differences in brood size. I weighed both chicks with a 100-g Pesola scale and banded them with a numbered plastic band on the day the second chick hatched (day 1) and weighed them again 6 days later (day 6). I calculated total growth as the difference between day 6 and day 1 total brood mass. Owing to mortality of chicks at 10 nests and to inclement weather, which prevented re-weighing at two nests, the sample was reduced to 17 broods of two chicks each. I measured parental behaviour during l-h observation periods conducted within the 6-day period of offspring growth described above. I collected data between 1000 and 1400 hours and selected nests randomly for observation within this time period. I calculated feeding rate as the number of feedings per brood that occurred during each l-h observation period. Parental behaviour was not classified as feeding unless food was transferred from adult to offspring. I classified feedings separated by 1 min or more as separate feedings. I calculated the average feeding interval as the total number of minutes of attendance by both parents divided by the number of feedings. If no feedings occurred, I calculated the average feeding interval as the total number of minutes of attendance by both parents. I calculated feeding latency as the number of minutes elapsed from arrival of a parent after foraging until it began feeding offspring. In one case when feeding did not occur within 30 min the observation was terminated and a latency of 30 min was assigned. I calculated foraging time as the total number of minutes both parents foraged during the l-h observation period. Previously, I determined that parents did not rest elsewhere on or away from the breeding colony (Pugesek 1983). While absent, parents were either en route to or from the colony or actively searching for food. Thus, time away from the nest measures time spent foraging. I conducted observations from a S-m observation tower situated on the periphery of the colony. Only nests further than 35 m from the tower were observed. At these distances no disturbance to adults was noted nor was fledging success
gull ofsspring growth
643
adversely affected (Pugesek 1983; Pugesek & Diem 1983). Nests represented the sampling unit for analysis of behavioural data. Data were collected on both mates. Individuals were distinguished by deter‘mining whether they were banded or unbanded. 1 conducted one to four l-h observations of adults at each nest. No nest was measured twice on the same day and nests were selected randomly for observation over the 6&y measurement period. Data from both mates were pooled and averaged over l-h observation periods at each nest. or in the case of feeding latency, the number of observations at each nest. Because I was unable to measure all behaviour patterns during each l-h observation period the numbers of observations and the total number of sampling units for each behaviour category represent a subset of the total sample of 17 nests. For example, when the foraging parent did not return to the nest during the observation period, I was unable to obtain a measure of feeding latency. In addition, I was unable to observe feedings when parents stepped behind shrubs during part of the observation period, however, 1 was able to measure attendance of parents for measures of foraging time. Total observations and sampling units obtained for each variable were as follows: feeding rate and average feeding interval: 26 h of observation at 11 nests (range: 14 h); feeding latency: 17 observations at 11 nests (range: 14 observations); foraging time: 31 h of observation at 12 nests (range: l-4 h). I used regression analyses to examine relationships between the behaviour of each mated pair and the growth of their offspring. I used Pearson’s product-moment correlation to investigate associations between patterns of behaviour. One adult at each nest had been previously banded and was of known age (3-17 years old). The band number of each bird was read with a spotting scope at the time the nests were marked. The ages of banded parents were determined later from banding records. Ages of mates on this colony are highly correlated (Pugesek & Diem 1986) and it was assumed that mates were the same or nearly the same age. Preliminary regression analyses related parental age to offspring growth and parental behaviour. Considerable variation exists in these variables with respect to parental age (Pugesek 1983) and in the small sample presented here, no significant relationships were found. This diminishes the probability that
Animal
644
Behaviour,
relationships between offspring growth and parental behaviour described in the Results are due to autocorrelation with parental age. Adult gulls at the 10 nests that were dropped from analysis because their offspring died before day 6 may have been less-efficient foragers than those used in the study. If less-efficientadults were excluded from the study, thereby biasing results, they should be younger than those that remained in the study. One-way ANOVA was performed on the two groups and no significant differences were found in the ages of the 10 adults not used in the study compared with the 17 used in the study. It is assumed here that the chicks of adults that were excluded from the study died as a result of predation events and that the deaths were not related to the foraging efficiency of the parents. I tested data for violations of assumptions of the statistical tests performed and applied transformations as necessary (Sokal & Rohlf 1969).
49, 3
280
- (a)
Y= 347.3 -4.0x
_:! 80 1
I
30
280
3
Feeding rate was positively related to total growth of chicks; however, the relationship was not significant (9 = 0.3 1, F, ,9=4.04, DO.07; regression equation: Y= 128.8+52.2x). The lack of signiticance was due, in part, to the low number of possible values of the feeding rate measure. Only four rates of feeding occurred (0.5, 0.7, 1.0 and 2.0 feedings/h). Offspring growth declined with increasing average feeding interval (Fig. 2a; ?=0.42, F,;1.9=6.46,PcO.05). Latencies to feed were inversely related to total offspring growth (Fig. 2b; ?=0.49, Fl ,=8.57, PcO.05). Thus, chicks gained lessweight’ if their parents waited longer to feed them. Foraging time was positively related to offspring growth (Fig. 2~; ?=0.35, F,,,,=5.48, PcO.05; total chick mass square-root transformed). Chicks tended to have high gains in mass if their parents quickly rotated guarding and foraging activities but low gains if both parents spent long periods together at the nest. Feeding latency was not significantly related to any of the behavioural variables measured (Table I). Average feeding interval decre?sed as feeding rate increased (Pearson’s r= - 0.76, N= 10, PcO.01). Feeding rate was not significantly correlated with foraging time. Average feeding interval was negatively correlated with foraging time (Pearson’s r= - 064, N= 10, PcO.05).
.
d
60
1
* Y= 223.12 -4.1X
6)
240
,
40 50 Average feeding interval (min)
i 200 E +j 2 u
160 120 I 10
,
280
Y = -175.9
Cd
45
30
+ 6.2X
240 -
sob
J
20 Feeding latency (min)
0
RESULTS
1
240
.
I 50
*
I
55 Foraging time (min)
Figure2. Total growth of (a) average feeding (c) foraging time.
Ll
60
of two-chick broods as a function interval, (b) feeding latency and
DISCUSSION Feeding Rehaviour
and Offspring
Growth
Two of the expected relationships between patterns of feeding behaviour were not significant; that between feeding latency and feeding rate, and that between feeding latency and average feeding interval. The high correlation between feeding rate and average feeding interval indicates that the variables provided similar measures of the frequency of offspring feeding. While feeding rate measured the absolute number of feedings in a given time period, the average feeding interval measured the feeding interval per minute of
Pugesek: California Table I. Correlations
between
behavioural Feeding
Feeding Average Feeding Foraging
rate feeding latency time
interval
variables rate
with Average
sample
sizes followed
feeding
interval
645 by significance Feeding
level
latency
Foraging
time
rz
N
P
rz
N
P
r2
N
P
rz
1.0 - 0.76 - 0.66 0.20
10 7 10
0.01 0.11 0.58
I.0 0.55 -064
I 10
0.20 0.05
1.0 - 0.21
8
0.61
1.0
parental attendance at the nest. The former was a poorer predictor of offspring growth, in part, becauseonly four feeding rates were observed. Despite small sample sizes, average feeding interval was significantly related to total offspring growth and feeding rate was positively related to total offspring growth. Thus, frequency of feeding was a good indicator of the amount of food transfer to offspring. The amount of food provided by adults at each feeding may explain additional variation in growth rate. None the less, earlier observations (Pugesek 1981, 1983) that older gulls feed offspring more frequently than younger gulls are clearly related to faster growth and higher survival among their offspring (Pugesek1981, 1983). Older adults have significantly lower feeding latencies compared with younger adults at all measured offspring ages (l-45 days). This relationship holds regardless of whether comparisonsof age groups include data on all brood sizes (Pugesek 1983) or only brood sizes of two (Pugesek1990). Results here indicate that shorter feeding latencies are indicative of greater offspring growth. Parental Experience Hypotheses
gull offspring growth
and Reproductive
Effort
Either hypothesis, increased parental experience or increased reproductive effort, could explain why older adults feed chicks more frequently and sooner after returning from foraging trips. Younger adults may feed their chicks less frequently because they are less-efficient foragers. They may withhold food after returning from foraging becausetheir crops are not full enough to Provide the necessary stimulation to regurgitate, or because their crops are frequently empty. Another explanation for low feeding rates among Youngeradults is that they are less experienced at
recognizing and responding to chick signals for feeding than are older adults. The mechanisms responsible for this form of parental experience and those of increased reproductive effort with age, however, are not mutually exclusive (Pugesek 1983). The mechanism that produces increased reproductive effort with age is unknown. Reproductive effort may increase with age because adults require a period of 9 years or more to develop the necessary parental behaviour, or reproductive effort may increase, for example, because hormone levels increase with age. That a learning period of 9 or more years is required to successfully respond to offspring is arguable (Pugesek 1981). Age-related increasesin hormone levels could produce an identical increased responsivenessto offspring. Data on foraging time do not support the parental experience hypothesis. Efficient adults did not provide more feedings to offspring per unit time spent foraging than adults of lesser efficiency. In addition, offspring growth was not negatively related to foraging time and thus efficient adults did not transfer greater amounts of food to their offspring with less foraging effort. Although it would be clearly advantageous for adults to spend extra time guarding offspring while not engaged in foraging activities, low values of foraging time should not be construed as such an activity. Gulls that do so actually defend offspring less frequently and experience higher offspring mortality compared with gulls that spend little time at the nest site (unpublished data). It could be argued that highly efficient adults also spend more time foraging than less-efficient adults, thereby maximizing the benefit obtained in foraging and expenditure of reproductive effort. In this case, increased efficiency would both enhance and be masked by the relationship found
646
Animal Behaviour, 49, 3
between foraging time and offspring growth. However, adults of known age were used here and no autocorrelation was found between parental age and behavioural measures including foraging time (see Methods). This means that some of the adults that spent great amounts of time foraging were young and that some of the adults that spent little time foraging were old. Under these circumstances, the younger adults that spent great amounts of time foraging would have to be more efficient than their older counterparts. The parental experience hypothesis requires conversely that foraging efficiency improves as individuals age and thus individuals gain skill and experience necessary to confer greater reproductive success. Data on foraging time support the reproductive effort hypothesis. Gulls that transferred greater amounts of food to offspring did so by foraging longer than gulls that provided less food to their offspring. Younger adults spend less time foraging than do older adults (Pugesek 1981, 1983). Greater amounts of foraging clearly benefit offspring in terms of increased growth. However, to fully qualify as reproductive effort, increased foraging must result in a cost to the adult in terms of reduced ability to invest in future offspring (i.e. greater adult mortality). Older gulls may experience greater mortality if greater amounts of time spent away from the colony in foraging activities are more risky compared with resting at the nest site. Several observations indicate that the breeding colony is safer for adults than is the surrounding area. Coyote, Canis latrans, tracks have been observed to approach but never penetrate the colony. Numerous golden eagle, Aquilu chrysuetos, attacks on gulls have been observed. The majority of those attacks have been on gulls in flight to or from the colony; many of which have been successful as evidenced by visual observation and by gull carcassesfound in the area surrounding the colony. Only two attacks have been observed by eagles at the colony. In one instance, an eagle captured an adult gull but was forced to drop it by approximately 100 mobbing gulls. In another attempt, the eagle was forced to leave the colony by mobbing gulls before it could capture’ any prey. The fact that gulls do not rest away from the breeding colony (Pugesek 1983) further supports the conclusion that time spent away from the colony, including foraging, is risky.
The most serious threat to adult survival is probably the energetic drain of provisioning offspring (Pugesek 1987, 1990). Adults lose body mass throughout the course of the breeding season (Coulson et al. 1983; Monaghan et al. 1989; Pugesek & Diem 1990). The period of maximum adult mortality coincides with the end of the breeding season in herring gulls, Larus argentatus (Coulson et al. 1983; Monaghan & Metcalfe 1986) suggesting that the energy drain of reproduction results in mortality. Thus, not only the amount of time adults spend in foraging activities but how they divide the proceeds between themselves and offspring may influence their survival. When older adults provide more food to offspring with frequent feedings they are, conversely, retaining less for themselves. Parents feed their offspring partially digested boluses of food, Longer feeding latencies mean that adults retain food in the crop for extended periods of time. Presumably, more energy will be assimilated by the adult and less will be available for offspring when feeding latencies are longer. Thus, higher feeding frequencies and shorter feeding latencies among older adults support the reproductive effort hypothesis if older adults lose more body mass and risk death as a result of these behavioural differences. Older California gulls lose significantly more body mass and have lower survival compared with younger gulls at Barnforth Lake (Pugesek 1987; Pugesek & Diem 1990) indicating that this is the case. However, further study is required to make a direct causal link between behavioural differences and loss of body mass among adults of known age and between behavioural differences and mortality among adults. ACKNOWLEDGMENTS I thank Deborah Fuller, Scott Hatch, Joseph Jell and Ziad Malaeb for comments on early drafts of the manuscript. I also thank Francesca Cuthbert and Hugh Drummond for their insightful reviews of an early draft of this paper. Research support came from grants from NSF (DEB 791997), Sigma Xi, Wilson Ornithological Society, Chapman Foundation and NIA (T32-AGO01 lo03). I thank the U.S. Fish and Wildlife Service,the Arapaho National Wildlife Refuge and the
Pugesek:
California
Wyoming Game and Fish Department for their cooperation with ongoing research.
REFERENCES Ainley, D. G. & Schlatter, R. B. 1972. Chick raising ability in adelie penguins. Auk, 89, 559-566. Ashmole, N. P. 1963. The biology of the wideawake or sooty tern Sterna fiscata on Ascension Island. Ibis, 103,297-364. Buckley, F. G. & Buckley, P. A. 1974. Comparative feeding ecology of wintering adult and juvenile royal terns (Aves: Laridae, Stemidae). Ecology, 55, 1053-1063. Charlesworth, B. & Leon, J. A. 1976. The relationship of reproductive effort to age. Am. Nat., 110,449-459. Couison, J. C., Monaghan, P., Duncan, N., Sheddon, C. B. & Thomas. C. S. 1983. Seasonal changes in the herring gull in Britain: weight, moult and mortality. Ardea, 71, 235-244. Dunn, E. K. 1972. Effect of age on the fishing ability of sandwich terns Sterna sandvicensis. Ibis, 114,36&366. Evans, R. M. 1982. Foraging-flock recruitment at a black-billed gull colony: implications for the information center hypothesis. Auk, 99, 24-30. Gadgil, M. & Bossert, W. 1970. Life historical consequences of natural selection. Am. Nat., 104, l-24. Ingolfsson, A. & Estrella, B. T. 1978. The development of shell cracking behavior in herring gulls. Auk, 95, 577-579. Kennedy, J. R. 1973. A study of the breeding colony of California gulls (Larus californicus), Bamforth Lake, Albany County, Wyoming. M.S. thesis, University of Wyoming. Lack, D. 1966. Population Studies of Birds. Oxford: Clarendon Press. Lack, D. 1968. Ecological Adaptations for Breeding Birds. London: Methuen. Mills, J. A. 1979. Factors affecting the egg size of red-billed gulls Larus novaehollandiae scooulinus. Ibis. 121, 53-67: Mills, J. A. & Shaw, P. W. 1980. The influence of age on laying date, clutch size, and egg size of the whitefronted tern, Sterna striata. N. Z. Jl Zool., 7, 147-153. Monaghan, P. & Metcalfe, N. B. 1986. On being the right size: natural selection and body size in the herring gull. Evolution, 40, 10961099.
gull
offspring
growth
641
Monaghan, P., Uttley, J. D., Burns, M. D., Thaine, C. & Blackwood, J. 1989. The relationship between food supply, reproductive effort and breeding success in arctic terns Sterna paradisaea. J. Anim. Ecol., 58, 261-274. Morrisson, M. L., Slack, R. D. & Shanley, E., Jr. 1978. Age and foraging ability relationships of olivaceous cormorants. Wilson Bull., 90, 414422. Nur, N. 1984. Increased reproductive success with age in the California gull: due to increased effort or improved skill. Oikos. 43. 407408. Orians, G. H. 1969. Age &id hunting success in the brown pelican (Pelicanus occidentalis). Anim. Behav., 17,316319. Pianka, E. R. & Parker, W. S. 1975. Age-specific reproductive tactics. Am. Nat., 109, 453-464. Pngesek, B. H. 1981. Increased reproductive effort with age in the California gull (Larus cahyornicus). Science, 212, 822-823. Pugesek, B. H. 1983. The relationship between parental age and reproductive effort in the California gull (Larus californicus). Behav. Ecol. Sociobiol., 13, 161-171. Pugesek, B. H. 1984. Age-specific reproductive tactics in the California gull. Oikos, 43, 409410. Pugesek, B. H. 1987. Age-specific survivorship in relation to clutch size and fledging success in California gulls. Behav. Ecol. Sociobiol., 21, 217-221. Pugesek, B. H. 1990. Parental effort in the California gull: tests of parentoffspring conflict theory. Behav. Ecol. Sociobiol., 27, 211-215. Pugesek, B. H. & Diem, K. L. 1983. A multivariate study of the relationship of parental age to reproductive success in California gulls. Ecology, 64, 829-839. Pugesek, B. H. & Diem, K. L. 1986. Ages of mated pairs of California gulls. Wilson Bull., 98, 61&612. Pugesek, B. H. & Diem, K. L. 1990. The relationship between reproduction and survival in known-aged California gulls. Ecology, 71, 81 l-817. Searcy, W. A. 1978. Foraging success in three age classes of glaucous-winged gulls. Auk, 95, 587-588. Sokal, R. R. & Rohlf, F. J. 1969. Biometry. San Francisco: W. H. Freeman. Verbeek, N. A. M. 1977. Comparative feeding behaviour of immature and adult herring gulls. Wilson Bull., 89,415421. Williams, G. C. 1966. Adaptation and Natural Selection. Princeton, New Jersey: Princeton University Press.