Effects of testosterone implants on pair behaviour during incubation in ...

6 downloads 0 Views 145KB Size Report
Yellow-legged Gulls during the incubation period were analysed. Free-living male gulls were implanted with testosterone (T-males), and their sexual behaviour ...
JOURNAL OF AVIAN BIOLOGY 32: 326–332. Copenhagen 2001

Effects of testosterone implants on pair behaviour during incubation in the Yellow-legged Gull Larus cachinnans Carlos Alonso-Alvarez

Alonso-Alvarez, C. 2001. Effects of testosterone implants on pair behaviour during incubation in the Yellow-legged Gull Larus cachinnans. – J. Avian Biol. 32: 326 – 332. The Yellow-legged Gull Larus cachinnans is monogamous with bi-parental incubation. In this study, the effects of high levels of plasma testosterone in male Yellow-legged Gulls during the incubation period were analysed. Free-living male gulls were implanted with testosterone (T-males), and their sexual behaviour within the pair was observed and compared with that of control pairs. Egg temperatures, length of incubation and hatching success were also analysed. T-males and their mates displayed more sexual behaviour than the controls. T-males engaged in mounting behaviour with their mates, whereas control males did not. Proportionally less time was spent incubating (in relation to time present in the colony) by T-males than control males. However, the mates of T-males did not spend more time incubating than control females to compensate for male neglect, although they did spend more time on the territory. Egg temperature in T-male nests was significantly lower than in control nests, but no significant difference in the length of incubation or hatching success between the two groups was found. In birds, the effects of high testosterone levels on male behaviour during incubation have only been analysed in a polyandrous species whose females usually do not contribute to incubation. The present results thus suggest that those males of a monogamous species with biparental incubation that sustain high testosterone levels after laying, thus reducing their contributions to incubation, will be confronted with a lack of compensation from their mates during incubation. Finally, this lack of female compensation seems to be mediated by behavioural interactions with the male rather than by her absence from the colony. C. Alonso-Al6arez, Department of Applied Biology, Estacio´n Biolo´gica de Don˜ana (CSIC), Apdo. 1056, 41080 Se6illa, Spain. E-mail: [email protected]

The courtship and mating behaviour of male birds depends to a great extent upon their plasma testosterone level (reviewed in Nelson 1995). In many avian species males show an increase in testosterone concentration during their mate’s fertile period, but values decline abruptly once incubation starts (reviewed in Beletsky et al. 1995). Thus, in males of species with more than one clutch per breeding season (with one or more mates), fluctuations in testosterone level coincide with female fertile periods (Beletsky et al. 1995). It has been suggested that a decrease in testosterone levels is adaptive since this hormone inhibits male parental care (Silverin 1980, Hegner and Wingfield 1987, Ketterson et al. 1992, Raouf et al. 1997, Moreno et al. 1999) and because sustaining high levels throughout the year may even represent a risk to the male’s survival (Nolan et al. 1992). ©

On the other hand, females mated with testosteroneimplanted males are able to increase their chick feedingfrequency in order to counterbalance reduced male provisioning. This compensation differs from one species to another, varying from complete to partial, and may or may not ensure male reproductive success (see e.g. Silverin 1980, Hegner and Wingfield 1987, Saino and Møller 1995a, Stoehr and Hill 2000). The costs and benefits of sustaining high testosterone levels have been frequently analysed in birds and a trade-off for males between, on the one hand, the benefits of extra-pair fertilisations (EPFs), and on the other, the costs of reduced parental care has been suggested (see review in Ketterson and Nolan 1999). Before the current study, the effect of high levels of plasma testosterone on the incubation behaviour of

JOURNAL OF AVIAN BIOLOGY

326

JOURNAL OF AVIAN BIOLOGY 32:4 (2001)

male birds had only been studied in the Spotted Sandpiper Actitis macularia (Oring et al. 1989). This is a polyandrous species that frequently shows only male parental care, and the cited paper analyses the behaviour of males incubating without female help. Oring et al. (1989) found a reduction in incubation constancy and an increased frequency of Extra Pair Copulation (EPC) attempts by testosterone-treated males, both of which negatively affected male reproductive success. However, it remains unclear whether female birds could compensate for the possible lack of male collaboration during incubation, and what the effects could be on pair behaviour in these circumstances. Gulls are monogamous birds with bi-parental care with a single annual brood (Cramp and Simmons 1983). Males show an abrupt decrease in copulation frequency once the clutch is completed (Brown 1967, Chardine 1987), which coincides with a noticeable decrease in the level of testosterone (Wingfield et al. 1982). Thus, I predicted that those male gulls sustaining high testosterone levels during incubation would reduce their investment in incubation behaviour. Under this scenario, we could predict a lack of female compensation since, in long-lived birds such as gulls, high investment in the current reproduction is rarely favoured because even a small reduction in the probability of future survival will reduce the chances for subsequent breeding (see Curio 1983, Pugesek and Diem 1990). In the present study, the effects of a high level of plasma testosterone in male Yellow-legged Gulls Larus cachinnans during incubation were analysed by using testosterone implants. Sexual and incubation behaviours in both male and female were observed, as well as their effects on egg temperature, length of incubation and hatching success.

Methods Capture and manipulation of gulls Eighteen male Yellow-legged Gulls were captured during the first week of the incubation period in May 1997 on Ons Island (NW Spain) using nest traps (described in Weaver and Kadler 1970). Ons Island is 4 km long (long axis) and harbours around 2000 breeding pairs. Sampling effort was spread throughout the island. Gulls’ sex was determined from body size following Bosch (1996). Seven randomly selected individuals (Tmales) were immediately implanted with testosterone pellets (25 mg, Organon Laboratories, Cambridge). The birds were anaesthetised in the field with a light dose of inhalant anaesthetic (Metofane; Pitman-Moore, Mundelein, Illinois). The pellet was then inserted through a small incision in the skin on the side beJOURNAL OF AVIAN BIOLOGY 32:4 (2001)

tween the wing and the knee and the incision sealed with a veterinary skin bond composed of cyanoacrylate (Vet-Seal; Braun, Melsungen, Germany). The procedure took about 4 min and the bird was alert and ready for release in 10 min. The control males received the same treatment (anaesthetised, skin incised and sealed) but were freed without implants (C-males). Before release the birds were ringed for future identification. The experiment was undertaken with a permit from the local authorities and did not harm the animals.

Testosterone implant characteristics The cited testosterone pellets have been used previously in studies of the behaviour and ecology of Red Grouse Lagopus scoticus (Moss et al. 1994) and Black-headed Gull Larus ridibundus (Groothuis and Meewuissen 1992). In captive Red Grouse the pellets (25 mg) disappeared within 5– 6 weeks (Moss et al. 1994). Although natural testosterone levels have not been analysed in Yellow-legged Gulls, maximum plasma levels of around 3 ng/ml and 5 ng/ml respectively have been described in Western Gulls Larus occidentalis and Black-headed Gulls (Wingfield et al. 1982, Groothuis and Meewuissen 1992). In captive male Yellow-legged Gulls, 38 mg of the same testosterone pellets resulted in a plasma concentration of 7.3 ng/ml (mean value; range: 5.1–9.5 ng/ml) for fifteen days, and the implants were removed afterwards without showing any signs of degradation (Alonso-Alvarez unpubl.).

Behavioural observations T- and C-males and their mates (T- and C-females) were observed from hides for 10 h between 0900 and 1900 five days after capture. Displays were registered according to Tinbergen’s descriptions of the Herring Gull Larus argentatus (Tinbergen 1959). Oblique-cumlong-calling, choking and head-tossing are related to sexual behaviour. The first two displays are part of the greeting ceremony of courtship, although they can occur separately, and can also be considered as aggressive displays. The last display frequently precedes mounting (Tinbergen 1959). Other observed behavioural categories were mounting (male standing on top of a female) and copulation (number of genital contacts). The number of cases of all these behaviours was divided by the time the bird was present giving the number of cases per hour. Nestdepartures were the times a bird left the nest. The number of nest-departures was divided by total time of observation (10 h). For each individual time incubating and time present on the territory were recorded as well. 327

Monitoring of incubation parameters The modal clutch size of Yellow-legged Gulls is three eggs, the adults having three incubation patches (see Drent 1970). Thus, in order to control for this variable, only pairs that had three eggs were used. Data on egg temperature were obtained from artificial eggs containing a data logger sensor (Onset Computer Corporation, Massachussets). When the artificial egg was added, one original egg was removed and placed in a two-egg nest (outside of the experimental area) to prevent the data logger recording a false temperature due to a larger than normal clutch size. After the sampling, the original egg was returned to its nest. The data logger was programmed to store 7944 temperatures for 9 h from 0900 hours. This sampling was repeated on two consecutive days after the observation day and the mean temperature in each nest was used in the statistical analysis. Length of incubation was measured as the number of days from the laying of the last egg until both the first and third egg hatched. Hatching success was the number of chicks hatched in a nest. Rates of chick survival are not reported because T-gulls were not re-captured just after hatching to remove pellets (see time of pellet dissolution above). Consequently, I cannot assess what effect testosterone had during the chick-rearing period on chick survival.

Data analysis Non-parametric statistical tests were used due to small sample sizes and non-normal distributions of most of the behavioural variables. The differences between groups in behavioural frequencies, times present, times incubating, and in mean egg temperatures were analysed with Mann-Whitney U-tests. When a particular mode of behaviour was not observed in a group, only occurrence or absence in each individual was used when comparing the groups by means of Fisher’s exact test. Moreover, comparisons within a pair were performed with the Wilcoxon matched-pairs signed-ranks test due to the mutual dependence of behaviour among parents. Means are presented 9S.E.

Results Time intervals between laying date and observation day, and between implant day and observation day did not differ between the two groups (Mann-Whitney Utests: Z =0.118, P =0.906, and Z = 0.562, P= 0.574 respectively). No correlation between these two variables and the others was statistically significant (Spearman correlation coefficients, P\0.10). Moreover, there were no differences between groups in the density of 328

Table 1. Mean 9 SE behaviour frequencies (number of cases/ hour; see Methods) in control (C-males) and testosterone implanted (T-males) male Yellow-legged Gulls during the incubation period. Activity

Nest-departures* Oblique with long callingn.s. Choking** Head-tossing** Mounting** Copulationn.s.

C-males

T-males

Mean 9SE

Mean9 SE

0.174 90.02 0.034 90.02 0.027 90.02 0 0 0

0.238 9 0.05 0.12290.09 0.455 90.18 0.36390.16 0.177 90.08 0.134 90.10

Differences between the two groups were analysed by the Mann-Whitney U-test or, when a particular behaviour was not observed in any individual of a group, the occurrence or absence of the behaviour in each individual was used to compare both groups by Fisher’s exact test. *: PB0.05; **: PB0.01.

pairs around the nest (distance to the closest nest; C-nests: mean=5.06 m9 0.94, T-nests: mean= 4.77 m9 0.78; Mann-Whitney U-test: Z= 0.19, P= 0.85). Treated pairs showed more choking, head-tossing, and mounting than controls (Tables 1 and 2), but there was no difference in male copulation behaviour (Table 1). Females were not involved in mounting or copulation other than with their mates. Two implanted males made one EPC attempt each, directed at neighbour females. T-males abandoned incubation more frequently than C-males (see nest-departures in Table 1). In relation to time present on the territory, T-males incubated less than C-males and their mates (Fig. 1a), whilst T-females spent less time incubating than C-females. Within C-pairs this variable did not differ (Fig. 1a). Time spent incubating during the 10-h observation period (Fig. 1b) showed no statistically significant difference between T-males and C-males or between the females of both groups. However, although there was no significant difference within the control pairs, Tmales incubated less than their mates. Both members of Table 2. Mean 9 SE behaviour frequencies (number of cases/ hour; see Methods) in female mates of control males (Cfemales) and of testosterone-implanted males (T-females) during the incubation period. Activity

Nest-departuresn.s. Oblique with long callingn.s. Choking** Head-tossing**

C-females

T-females

Mean 9SE

Mean9 SE

0.102 90.03 0.053 90.03 0 0

0.19590.06 0.09590.04 0.157 90.04 0.1739 0.06

Differences between the two groups in each frequency of behaviour were analysed by the Mann-Whitney U-test or, when a particular behaviour was not observed in any individual of a group, the occurrence or absence of the behaviour in each individual was used to compare both groups by Fisher’s exact test. **: PB0.01. JOURNAL OF AVIAN BIOLOGY 32:4 (2001)

30.1190.26, T-nests: mean= 30.839 0.65; Whitney U-test: Z=1.40, P= 0.181).

Mann-

Discussion

Fig. 1. Mean SE time spent incubating of time present on the territory (a) and of total observation time (10 h; b) by male Yellow-legged Gulls with testosterone implants (T-males), their mates (T-females), and control pairs (C-males and Cfemales). P-values were calculated by means of the MannWhitney U-test for comparisons between birds of the same sex and by the Wilcoxon matched-pairs signed-ranks test for comparisons within pairs (C-pairs: n=9; T-pairs: n = 7).

the C-pairs spent a similar amount of time on their territories (Fig. 2). By contrast, T-females stayed longer on the territory than their mates and also spent longer than C-females. Male time present did not differ between the two groups. Finally, the proportion of time a nest was left without an incubating parent was higher for nests of T-males (Fig. 3a; Mann-Whitney U-test: Z= 3.026, P=0.001) and mean egg temperature was lower (Fig. 3b; Mann-Whitney U-test: Z=2.382, P= 0.017). No eggs hatched in one T-nest. However, no significant difference in hatching success was detected between C- and T-pairs (C-pairs: mean=2.009 0.17, T-pairs: mean =2.0090.37; Mann-Whitney U-test: Z=0.452, P= 0.651). Hatching success in the two groups did not differ from that of a group of nonmanipulated nests (n=17), all with three eggs, in the same area (mean hatching success= 2.2390.25; MannWhitney U-tests P\ 0.20 in both cases). The length of incubation did not differ between C- and T-nests for the first egg laid (C-nests: mean=28.789 0.32, T-nests: mean=29.509 0.56; Mann-Whitney U-test: Z=1.41, P= 0.181) or for the third egg (C-nests: mean= JOURNAL OF AVIAN BIOLOGY 32:4 (2001)

In the present study, I have shown the effect of testosterone treatment on males, as well as on male and female behaviour during the incubation period. In birds, testosterone has been commonly considered a proximate mechanism in the expression of male sexual behaviour, such as visual displays or song (e.g. Borgia and Wingfield 1991, Saino and Møller 1995b, Enstrom et al. 1997), and of copulation behaviour (e.g. Balthazart et al. 1985, Borgia and Wingfield 1991). In the current study, T-males showed a higher frequency of mounting and sex-related displays such as choking or head-tossing (Tinbergen 1959) than control birds. The higher level of sexual activity in T-males could be the cause of their reduced incubation and their higher nest-departure rates. Copulation behaviour may not disappear completely in Yellow-legged Gulls during the first ten days of the incubation period (Alonso-Alvarez, unpubl. data from the same population in the previous year; see also Brown 1967 and Chardine 1987). This coincides with a period of low nest attentiveness in Herring Gulls, with eggs remaining uncovered from 5 to 30% of the time (see Drent 1970). Actually, we do not know whether such low attentiveness might be related to high testosterone values of males. Further correlational studies during this period might resolve this question. Two implanted males were involved in EPCs, but such a low number of cases prevents the analysis of this variable. Nevertheless, since a conflict between parental care and EPCs favoured by testosterone has been found

Fig. 2. Mean 9SE time present on territory during 10 h of observation by male Yellow-legged Gulls with testosterone implants (T-males), their mates (T-females), and control pairs (C-males and C-females). P-values were calculated by means of the Mann-Whitney U-test for comparisons between birds of the same sex and by Wilcoxon matched-pairs signed-ranks test for comparisons within pairs (C-pairs: n= 9; T-pairs: n=7).

329

Fig. 3. Mean proportion of time that eggs were left unincubated by yellow-legged gulls during 10 h of observation (a), and mean egg temperature during 18 h of temperature sampling (b) in nests with testosterone-implanted males or control males (Means9SE; C-nests: n=9; T-nests: n= 7).

in studies of male behaviour during the chick-rearing period (Silverin 1980, Hegner and Wingfield 1987, Ketterson et al. 1992, Saino and Møller 1995a, Raouf et al. 1997, Hunt et al. 1999), a similar effect cannot be excluded for gulls during the incubation period (as in Oring et al.’s study). EPCs are common in gulls (review in Wittenberger and Hunt 1985) and were observed before laying in the population under study (10% of all registered copulations in 1996; continuous sampling of 40 males for 16 h; Alonso-Alvarez, unpubl. data). Unfortunately, as far as I know, extra-pair fertilisations have not been demonstrated in any gull species. Therefore, a discussion in terms of a trade-off between the benefits of EPFs and the cost of reduced parental care would be much too speculative for gulls at this moment. With respect to females’ behaviour, in passerines those females mated with males with artificially elevated testosterone can fully compensate for the reduction in their partners’ feeding rate during the chick-rearing 330

period by feeding their offspring more frequently (Hegner and Wingfield 1987, Ketterson et al. 1992, Saino and Møller 1995a, Hunt et al. 1999, Stoehr and Hill 2000; but see Silverin 1980). However, in long-lived birds such as gulls, high investment in the current reproduction could reduce the number of subsequent breeding attempts (Pugesek and Diem 1990). My results confirm an absence of compensation of incubation behaviour in female Yellow-legged Gulls. Despite the fact that the incubation period might not be so energetically expensive as the chick-rearing period (Whittow 1986, Blem 2000), incubation in gulls may interfere with time needed for foraging (Galusha and Amlaner 1978, Niebuhr and McFarland 1983). Also time present in the colony without incubating could interfere with foraging. Although T-females did not incubate more than C-females, they did spend more time on their territories. An explanation for this result could be that in the present study, the sexual stimulus of the T-treated mate might have interfered with female behaviour. The effect of male behaviour on female endocrinology has been studied in a wide range of taxa (e.g., reviewed in Wingfield and Farner 1993, Wingfield et al. 1994). This hormonal change could explain the female participation in sexual activities. Specifically, it could explain the longer time spent on the territory, which in normal circumstances occurs just before egglaying (Fitch and Shugart 1984). An increase in the time females spent on the territory could perhaps negatively affect later reproductive attempts or even survival (e.g., because of abruptly decreasing fat reserves after egg-laying; Hario et al. 1991). This behaviour has never previously been reported and I suppose that the female’s longer presence in the colony might be a nonadaptive response to male behaviour. This suggests that interpretations about female contribution during experiments with testosterone-implanted males should be carefully analysed in order to disentangle adaptive female strategies from collateral effects of endocrine manipulation. To conclude, the hatching success and incubation length in T-nests did not differ from those of the controls despite the reduction in egg temperature caused by the lesser time spent incubating by the Tmales, which was not compensated for by their mates. Lee et al. (1993) suggest that there are no effects on embryonic or neonatal survival over a range of mean incubation temperatures between 33.0°C and 37.8°C in Herring Gulls. In the case of T-nests, the temperatures I recorded fell below this range. Successful hatching by 40% of chicken eggs held continuously at 27°C indicates, however, that development is still possible at very low temperatures (see Evans 1990). In summary, high levels of testosterone during incubation affected male sexual behaviour in the Yellowlegged Gull, although no higher extra-pair copulation rate was demonstrated, and reduced male incubation. JOURNAL OF AVIAN BIOLOGY 32:4 (2001)

Despite showing no negative effects on hatching success, high testosterone levels could represent a cost because reduced male incubation, without any compensation by the mate, resulted in a lower egg temperature. Acknowledgements – I am grateful to the authorities of Consellerı´a de Medio Ambente (Xunta de Galicia) for allowing us to use their installations on Ons Island. Thanks to Alberto ´ lvarez, Xim Cerda´ , Paz Cabanelas and Velando, Fernando A Micke Lockwood for many helpful discussions. I would also like to thank the staff of the Ons Island Natural Reserve for solving many logistic problems. The present experiment and that described in methods as unpublished data were performed with the legal permission (85–1997 and 325–1999) of Xunta de Galicia, Environment governmental agency.

References Balthazart, J., Schumacher, M. and Malacarne, G. 1985. Interactions of androgens and estrogens in the control of the sexual behavior in the Japanese quail. – Physiol. Behav. 35: 157–166. Beletsky, L. D., Gori, D. F., Freeman, C. and Wingfield, J. C. 1995. Testosterone and polygyny in birds. – In: Power, D. M. (ed.). Current Ornithology. Vol. 12. Plenum Press, New York, pp. 1–47. Blem, C. R. 2000. Energy balance. – In: Whittow, G. C. (ed.). Sturkie’s Avian Physiology. Academic Press, New York, pp. 327 –341. Borgia, G. and Wingfield, J. C. 1991. Hormonal correlates of bower decoration and sexual display in the satin bowerbird (Ptilonorhynchus 6iolaceus). – Condor 93: 935–942. Bosch, M. 1996. Sexual size dimorphism and determination of sex in yellow-legged gulls. – J. Field Ornithol. 67: 534– 541. Brown, R. G. B. 1967. Courtship behaviour in the lesser black-backed gull, Larus fuscus. – Behaviour 29: 122– 153. Chardine, J. W. 1987. The influence of pair-status on the breeding behaviour of the kittiwake Rissa tridactyla before egg-laying. – Ibis 129: 515–526. Cramp, S. and Simmons, K. E. L. 1983. Handbook of the Birds of Europe, The Middle East and North Africa. The Birds of Western Palearctic. Vol. 3: Waders to Gulls. – Oxford University Press, Oxford. Curio, E. 1983. Why do young birds reproduce less well? – Ibis 125: 400 –404. Drent, R. H. 1970. Functional aspects of incubation in the herring gull (Larus argentatus). – Behaviour, Supplement 17: 1 – 132. Enstrom, D. A., Ketterson, E. D. and Nolan, V. Jr. 1997. Testosterone and mate choice in the dark-eyed junco. – Anim. Behav. 54: 1135–1146. Evans, R. M. 1990. Effects of low incubation temperatures during the pipped egg stage on hatchability and hatching time in domestic chickens and ring-billed gulls. – Can. J. Zool. 68: 863–840. Fitch, M. A. and Shugart, G. W. 1984. Requirements for a mixed reproductive strategy in avian species. – Am. Nat. 124: 116– 126. Galusha, J. G. Jr. and Amlaner, C. J. Jr. 1978. The effects of diurnal and tidal periodicities in the numbers and activities of herring gulls Larus argentatus in a colony. – Ibis 120: 322 – 328. Groothuis, T. and Meewuissen, G. 1992. The influence of testosterone on the development and fixation of the form of displays in two age classes of young black headed gulls. – Anim. Behav. 43: 189–208. Hario, M., Kilpi, M. and Selin, K. 1991. Parental investment by sexes in Herring Gull: the use of energy reserves during the early season. – Ornis Scand. 22: 308– 312. JOURNAL OF AVIAN BIOLOGY 32:4 (2001)

Hegner, R. E. and Wingfield, J. C. 1987. Effects of experimental manipulations on parental investment and breeding success in male house sparrows. – Auk 104: 462– 469. Hunt, K. E., Hahn, T. P. and Wingfield, J. C. 1999. Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus). – Behav. Ecol. Sociobiol. 45: 360– 369. Ketterson, E. D. and Nolan, V. Jr. 1999. Adaptation, exaptation, and constraint: a hormonal perspective. – Am. Nat. 154: S4– S25. Ketterson, E. D., Nolan, V. Jr., Wolf, L. and Ziegenfus, C. 1992. Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in dark-eyed junco (Junco hyemalis). – Am. Nat. 140: 980– 999. Lee, S. C., Evans, R. M. and Bugden, S. C. 1993. Benign neglect of terminal eggs in herring gulls. – Condor 95: 507 – 514. Moreno, J., Veiga, J. P., Cordero, P. J. and Mı´nguez, E. 1999. Effects of parental care on reproductive success in the polygynous spotless starling Sturnus unicolor. – Behav. Ecol. Sociobiol. 47: 47– 53. Moss, R., Parr, R. and Lambin, X. 1994. Effects of testosterone on breeding density, breeding success and survival of red grouse. – Proc. R. Soc. Lond. B 258: 175– 180. Nelson, R. J. 1995. An Introduction to Behavioural Endocrinology. – Sinauer Associates, Inc., Sunderland, Massachusetts. Niebuhr, V. and McFarland, D. 1983. Nest-relief behaviour in the herring gull. – Anim. Behav. 31: 701– 707. Nolan, V. Jr., Ketterson, E. D., Ziegenfus, C., Cullen, D. P. and Chandler, C. R. 1992. Testosterone and avian life histories: effects of experimentally elevated testosterone on prebasic molt and survival in male dark-eyed juncos. – Condor 94: 364– 370. Oring, L. W., Fivizzani, A. L. and El Halawani, M. E. 1989. Testosterone-induced inhibition of incubation in the spotted sandpiper (Actitis macularia). – Horm. Behav. 23: 412 –423. Pugesek, B. H. and Diem, K. L. 1990. The relationship between reproduction and survival in known-aged California gulls. – Ecology 71: 811– 817. Raouf, S. A., Parker, P. G., Ketterson, E. D., Nolan, V. Jr. and Ziegenfus, C. 1997. Testosterone affects reproductive success by influencing extra-pair fertilizations in male darkeyed juncos (Aves: Junco hyemalis). – Proc. R. Soc. Lond. B 264: 1599– 1603. Saino, N. and Møller, A. P. 1995a. Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness. – Behav. Ecol. Sociobiol. 33: 151– 157. Saino, N. and Møller, A. P. 1995b. Testosterone correlates of mate guarding, singing and aggressive behaviour in male barn swallows, Hirundo rustica. – Anim. Behav. 49: 465– 472. Silverin, B. 1980. Effects of long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca, during the breeding period. – Anim. Behav. 28: 906– 912. Stoehr, A. M. and Hill, G. E. 2000. Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus). – Behav. Ecol. Sociobiol. 48: 407 – 411. Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): a progress report. – Behaviour 15: 1 – 70. Weaver, D. K. and Kadler, J. A. 1970. A method for trapping breeding adult gulls. – Bird-Banding 41: 28 – 31. Whittow, G. C. 1986. Energy metabolism. – In: Sturkie, P. D. (ed.). Avian Physiology. Springer-Verlag, New York, pp. 253 – 268. Wingfield, J. C. and Farner, D. S. 1993. Endocrinology of reproduction in wild species. – In: Farner, D. S., King, J.

331

R. and Parks, K. C. (eds). Avian Biology. Vol. 9. Academic Press, New York, pp. 163–327. Wingfield, J. C., Newman, A. L., Hunt, G. L. and Farner, D. S. 1982. Endocrine aspects of female-female pairing in the western gull (Larus occidentalis wymani ). – Anim. Behav. 30: 9 – 22. Wingfield, J. C., Whaling, C. S. and Marler, P. 1994. Communication in vertebrate aggression and reproduction: The role of hormones. – In: Knobil, E. and Neill, J. D. (eds).

332

The Physiology of Reproduction. Raven Press, New York, pp. 303– 342. Wittenberger, J. F. and Hunt, G. L. Jr. 1985. The adaptive significance of coloniality in birds. – In: Farner, D. S., King, J. R. and Parkes, K. C. (eds.). Avian Biology. Vol. 8. Academic Press, New York, pp: 1– 78. (Recei6ed 30 May 2000, re6ised 2 January 2001, accepted 7 April 2001.)

JOURNAL OF AVIAN BIOLOGY 32:4 (2001)