Griffiths, R., Double, M. C., Orr, K. and Dawson, R. J. G. Piersma, T. 1997. Do global patterns of use and 1998. A DNA test to sex most . – Mol. Ecol. 7: migration strategies co-evolve with relative investments in 1071–1075. immunocompetence due to spatial variation in parasite Hamilton, W. D. and Zuk, M. 1982. Heritable true fitness and pressure? – Oikos 80: 623–631. bright birds: a role for parasites? – Science 218: 384–386. Poulin, R. 1996. Sexual inequalities in helminth infections: a Harper, D. G. C. 1999. Feather mites, pectoral muscle condi- cost of being a male? – Am. Nat. 147: 287–295. tion, wing length and plumage coloration of passerines. – Price, P. W. 1980. Evolutionary biology of parasites. – Prince- Anim. Behav. 58: 553–562. ton University Press, Princeton. Hudson, P. J. and Dobson, A. P. 1997. Host-parasite pro- Proctor, H. and Owens, I. 2000. Mites and birds: diversity, cesses and demographic consequences. – In: Clayton, D. parasitism and coevolution. – Trends Ecol. Evol. 15: 358– H. and Moore, J. (eds). Host-parasite evolution: general 364. principles and avian models. Oxford University Press, Ox- Rosen, S., Hadani, A. and Perlstein, Z. 1988. The occurrence ford, pp. 128–154. of Megninia hologastra (Analgidae Gaud, 1974) on poultry in Israel. – Avian Pathol. 17: 921–924. Kirkpatrick, C. E., Robinson, S. K. and Kitron, U. D. 1991. Rozsa, L. 1997. Wing-feather mite (Acari: Proctophyllodidae) Phenotypic correlates of blood parasitism in the common abundance correlates with body mass of passerine hosts: A grackle. – In: Loye, J. E. and Zuk, M. (eds). -parasite comparative study. – Can. J. Zool. 75: 1535–1539. interactions: ecology, evolution and behaviour. Oxford Siikama¨ki, P., Ra¨tti, O., Hovi, M. and Bennett, G. F. 1997. University Press, Oxford, pp. 344–358. Association between haematozoan infections and repro- Komdeur, J. 1991. Cooperative breeding in the Seychelles duction in the pied flycatcher. – Funct. Ecol. 11: 176–183. warbler. – PhD thesis, University of Cambridge, Cam- Thompson, C. W., Hillgarth, N., Leu, M. and McClure, H. E. bridge. 1997. High parasite load in house finches (Carpodacus Komdeur, J. 1992. Importance of habitat saturation and terri- mexicanus) is correlated with reduced expression of a sexu- tory quality for evolution of cooperative breeding in the ally selected trait. – Am. Nat. 149: 270–294. Seychelles warbler. – Nature 358: 493–495. Walter, D. E. and Proctor, H. C. 1999. Mites: ecology, evolu- Larcher, W. 1991. Physiological plant ecology: corrected print- tion and behaviour. – University of New South Wales ing of the second edition. – Springer-Verlag, Berlin. Press, Sydney. May, R. M. and Anderson, R. M. 1978. Regulation and Walther, B. A. and Clayton, D. H. 1997. Dust-ruffling: a stability of host-parasite population interactions. II. Desta- simple method for quantifying ectoparasite loads of live bilizing processes. – J. Anim. Ecol. 47: 249–267. birds. – J. Field Ornithol. 68: 509–518.

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Foraging trip duration increases for Humboldt tagged with recording de7ices

Sabrina S. Taylor (correspondence) and Marty L. Leonard, Department of Biology, Dalhousie Uni7ersity, Halifax, NS, B3H 4J1, Canada. E-mail: [email protected] Daryl J. Boness, National Zoological Park, Smithsonian Institution, Washington, D.C., 20008, USA. Patricia Majluf, Wildlife Conser7ation Society, Armendariz 445, Lima 18, .

Marine equipped with data recording devices sometimes such as satellite tags, radio-transmitters, and time-depth show changes in their behaviour, which can indicate an recorders are increasingly used to study aspects of adverse effect of the instrument. We attached time-depth recorders (TDRs) and radio-transmitters to study foraging be- foraging behaviour including foraging trip duration, haviour in Humboldt Penguins Spheniscus humboldti and ob- foraging location, and dive characteristics. Despite the served an increase in the duration of foraging trips. We suggest valuable information that these instruments collect, that further tagging of this endangered be approached their deployment on some species can have negative with caution since this increase in trip duration may negatively affect reproductive and foraging success. effects on foraging behaviour and reproductive success (Wilson et al. 1986, Davis and Miller 1992, Watanuki et al. 1992, Hull 1997). Research on the impact of instruments on behaviour and reproductive success of penguins has produced Foraging behaviour in penguins is difficult to observe equivocal results. Several researchers have found no directly because individuals typically travel large dis- significant effect of instrument deployment on trip du- tances at sea or spend considerable time below the ration (Croxall et al. 1988, Williams et al. 1992, surface (Wilson et al. 1986). Consequently, instruments Watanuki et al. 1992, Wienecke and Robertson 1997)

JOURNAL OF AVIAN BIOLOGY 32:4 (2001) 369 whereas others have found a variety of effects including reduce wake and thus drag (Croll et al. 1991). TDRs increased foraging trip duration, decreased foraging were deployed to study foraging behaviour together efficiency, decreased fat levels, or a greater incidence of with radio-transmitters to relocate penguins in the nest abandonment (Gales et al. 1990, Hull 1997, Kirk- event that they deserted their nest. The TDRs were two wood and Robertson 1997, Pu¨tz et al. 1998). The sizes: 6.5×1.8×2.0 cm (37 g) and 8.5×1.1×2.0 cm variable effect of instruments is presumably a function (27.5 g), and the radio-transmitters were 4.0×1.0×2.5 of differences across studies in device size and shape, cm (15 g; dimensions given as length×height×width the method of attachment, and the body condition of for all devices). The sides of the TDRs were tapered to the instrumented (Watanuki et al. 1992). It is form a point and the dorsal surface of the radio-trans- therefore difficult to predict the effects of a particular mitters was angled down to form a wedge. Antennas on instrument, especially for species in which instrument the radio-transmitters were 12.5 cm long, 2 mm in deployment is new. However, because instruments po- diameter, and were on angle of 50–60° from horizontal. tentially impact foraging behaviour and reproductive The deployment of TDRs together with radio-transmit- success, it is important to assess their effect on a study ters increased a Humboldt ’s cross-sectional by study basis. This is particularly important for work area by approximately 2.7% and 2.1%. TDR type (high requiring the tagging of . or low profile) was haphazardly assigned to each pair. We attached time-depth recorders (TDRs) in combi- Penguins were re-captured after approximately two nation with radio-transmitters to endangered Hum- weeks (x¯ 9SD=16.892.11 d, range=10–19 d, n= boldt Penguins Spheniscus humboldti to examine details 23) to minimize the potential effects of chronic expo- of their foraging behaviour (Taylor 2000). In this study sure to drag (Wilson et al. 1989). we compare the length of foraging trips made by tagged The TDRs were programmed to record depth every 7 and untagged penguins to determine the effect of these s while a penguin was in contact with salt-water and to instruments on the birds. record the number of dry readings when the instrument was dry. Using the wet and dry times, we could calcu- late the duration of each foraging trip. Foraging trips Methods were defined as any period at sea which included at least one period of diving activity and ended when the This study was conducted at Punta San Juan, Peru (15° bird returned to land. Humboldt Penguins exhibited 22% S, 75° 12% W), between 21 May and 24 November two types of foraging trip hereafter referred to as day 1999. Punta San Juan is a peninsula safeguarded from trips and overnight trips. If a bird went on a foraging predators by a 1.2 km long concrete wall. Within the trip and returned on the same calendar day, we headland, there are several distinct colonies of breeding classified it as a day trip. If a bird returned on the next Humboldt Penguins. Although most penguins are sur- calendar day, we classified the trip as an overnight trip. face nesters, there are also individual crevice and bur- row nests located around the peninsula and interspersed among and within the colonies (Schwartz et al. 1999). Untagged birds At a study colony of predominantly surface nesting birds, we determined the duration of an untagged indi- Tagged birds vidual’s foraging trip by using arrival and departure Twenty-seven penguins, consisting of 13 pairs and one times from the colony during chick rearing. Individuals individual (n=14 nests), were caught inside individual were recognized by the unique spotting patterns on crevice or nests when their chicks were approx- their breasts (Scholten 1989). To match tagged and imately two to six weeks old and tagged with Mark7 untagged birds, we used observations from untagged time-depth recorders (TDRs; Wildlife Computers, Red- birds (n=30; males=15, females=15) beginning when mond, WA) and VHF radio-transmitters (Advanced their chicks were two weeks old and continuing until Telemetry Systems, Isanti, MN). Radio-transmitters fledging. Observers were present in a blind during all were glued laterally to the TDRs prior to deployment daylight hours (6:00–18:00 hours) and recorded depar- and then both instruments were glued as a unit to the ture and arrival times of untagged birds. To keep the penguin using 5-minute epoxy. The instruments were period of measurement consistent for tagged and un- glued to the dorsal feathers above the uropygial gland tagged birds, we excluded trips (71/157) in which the and below the mid-point of the penguin’s back to departure or arrival times for tagged birds were before minimize drag (Bannasch et al. 1994). Feathers at the 6:00 or after 18:00 hours. We did not enter the study anterior end of the instruments were glued over the colony or handle these birds because surface nesting instruments to create a streamlined shape and the ta- Humboldt Penguins often desert their nests when dis- pered end of the TDRs faced the penguin’s tail to turbed.

370 JOURNAL OF AVIAN BIOLOGY 32:4 (2001) Results nest and although the distances these birds had to travel were small (approx. 50–500 m), this overestima- Although TDRs were deployed on 27 birds, data from tion may mean that the actual difference between all birds were not available for analysis. We used the tagged and untagged birds was larger than observed. In dive records of 22 penguins to calculate trip duration. tagged animals, it is unclear whether the duration of For the remaining birds, TDRs failed to work (n=1) foraging trips included transit time to the nest because or birds abandoned their nests (n=4 birds). We did we do not know how long it took for the salt-water not recover a TDR from one of the four birds that switch on the TDRs to dry, which was our indication abandoned their nest. TDRs from the remaining three that the foraging trip had ended. birds were recovered after they had been attached for However, the fact that tagged Humboldt Penguins 41–96 days. These three birds made foraging trips had longer foraging trips than their untagged counter- ranging from 1 to 8 days long, a trip duration that is parts suggests that the addition of instruments may atypical of adults during the chick-rearing period. Birds have an impact on foraging behaviour. The increased that did not abandon the nest made a mixture of drag caused by the TDRs may have reduced swimming overnight and day trips (Taylor 2000). We have ex- speed (Wilson et al. 1986, 1989, Wilson and Wilson cluded these three birds from our analyses on trip 1995) and therefore the ability of the penguins to duration because we believe that the trips made by pursue prey. If penguins are less efficient at capturing these birds reflect a change to a non-breeding foraging prey because of the instruments, they may be faced with strategy rather than an effect of the instruments on the choice of reducing the amount of food supplied to foraging behaviour. their offspring or maintaining the amount of food given To analyse the data, we averaged the duration of to chicks at the expense of their own body condition. overnight and day trips during the period of tag deploy- Reduced swimming speed may also result in longer ment for each individual and compared these values for travel times to foraging areas, an effect suggested by untagged and tagged birds using unpaired t-tests. Some Wilson et al. (1989) for Adelie Penguins individuals only made overnight trips, so sample sizes adeliae. Finally, an increase in foraging trip duration for day trips are smaller. All means are presented9SD. may indicate that penguins need to consume more food Tagged penguins made significantly longer foraging to compensate for the extra energy expenditure in- trips than untagged birds for both day trips (tagged: curred by carrying an instrument. If penguins spend 9.491.8 h, untagged: 7.291.5 h, t=3.45, df=30, more time foraging to meet this need, the rate that food PB0.005) and overnight trips (tagged: 25.592.8 h, is delivered to the young may be reduced, which could untagged: 22.992.1 h, t=3.78, df=47, PB0.001). also result in malnourished chicks. An increase in en- ergy expenditure (+11%Wkg−1) was documented by Luna-Jorquera and Culik (1998) in a swim channel for Discussion Humboldt Penguins instrumented with larger MK6 time-depth recorders (7.4×5.7×3.5 cm, cross-sec- Despite the relatively small size of our instruments, tional area approximately 20.0 cm2). Although not time-depth recorders deployed in conjunction with ra- conclusive for other recording devices, these data dio-transmitters increased the length of foraging trips in provide evidence that energy expenditure increases for Humboldt Penguins by an average of 2.2 h during day instrumented Humboldt Penguins. trips and 2.6 h during overnight trips. It is not clear In addition to increases in the duration of foraging how important this increase in trip duration is, because trips, TDRs may also directly affect reproductive suc- other factors could obscure the relationship between cess in Humboldt Penguins. One bird abandoned the tagged and untagged birds. For instance, tagged pen- nest within two days of instrument deployment, two guins nested singly, apart from colonies, and untagged birds at one nest abandoned after 10 days, and the birds nested within a colony. If younger, less experi- fourth bird abandoned after 18 days. Immediate aban- enced foragers nest singly, then the differences we ob- donment suggests that handling may have caused the served may reflect the quality of individuals rather than bird to desert the nest. However, after 10–18 days, it is differences in the duration of foraging trips between difficult to know whether instrument deployment tagged and untagged birds. We were unable to match caused abandonment because Humboldt Penguins un- nest type for tagged and untagged birds because we der natural conditions desert their nests for a variety of could not observe a colony of burrow nesting birds or reasons (Taylor 2000). Given the possible causes for risk tagging surface nesting birds for fear of causing nest desertion, it is difficult to conclude that instru- nest abandonment. ments caused nest abandonment; however, given this The difference between tagged and untagged birds is risk, nest abandonment in a control group should be further obscured by the different methods used to cal- monitored in future studies. culate the duration of foraging trips in each group. Trip In this study, we examined Humboldt Penguin forag- duration in untagged birds included transit time to the ing behaviour in part because they are threatened by

JOURNAL OF AVIAN BIOLOGY 32:4 (2001) 371 fisheries and little is known about their diving activity. Croxall, J. P., Davis, R. W. and O’Connell, M. J. 1988. Diving Given the possible conservation value of identifying patterns in relation to diet of gentoo and macaroni pen- guins at South Georgia. – Condor 90: 157–167. conflicts between penguin foraging behaviour and Davis, L. S. and Miller, G. M. 1992. Satellite tracking of fishing practices, it is not clear whether changes in Adelie penguins. – Polar Biol. 12: 503–506. penguin behaviour caused by instrument deployment Gales, R., Williams, C. and Ritz, D. 1990. Foraging behaviour are acceptable. However, our results suggest that even of the , minor: initial results and assessment of instrument effect. – J. Zool. Lond. 220: small devices deployed for a short time can affect 61–85. Humboldt Penguin foraging behaviour and possibly Hull, C. 1997. The effect of carrying devices on breeding royal reduce reproductive success. To minimize drag and penguins. – Condor 99: 530–534. Kirkwood, R. and Robertson, G. 1997. The foraging ecology possibly trip length in future tagging studies, we recom- of female emperor penguins in winter. – Ecol. Monogr. 67: mend deploying TDRs without radio-transmitters to 155–176. decrease cross-sectional area and to eliminate any effect Luna-Jorquera, G. and Culik, B. M. 1998. Balancing the of the antennas (e.g. Wanless et al. 1988, Croll et al. energy budget of the Humboldt penguin: a preliminary approach. – Penguin Cons. 11 (1): 20. 1991). Furthermore, to reduce drag caused by the Pu¨tz, K., Wilson, R. P., Charrassin, J.-B., Raclot, T., Lage, J., TDRs, the tapered end of the instrument should be the Le Maho, Y., Kierspel, M. A. M., Culik, B. M. and leading edge (Bannasch et al. 1994). We placed the Adelung, D. 1998. Foraging strategy of king penguins tapered end of TDRs facing the penguins’ tails because ( patagonicus) during summer at the Crozet Islands. – Ecology 79: 1905–1921. we could create tapering at the front by gluing feathers Scholten, C. J. 1989. Individual recognition of Humboldt over the top of the instrument, thus achieving a stream- penguins. – Spheniscid Penguin Newsletter 2: 4–8. lined shape at both ends of the recorders. However, Schwartz, M. K., Boness, D. J., Schaeff, C. M., Majluf, P., Perry, E. A. and Fleischer, R. C. 1999. Female-solicited feathers may provide insufficient tapering and it is more extrapair matings in Humboldt penguins fail to produce important to produce favourable flow conditions at the extrapair fertilizations. – Behav. Ecol. 10: 242–250. leading edge of the instrument (Bannasch et al. 1994). Taylor, S. S. 2000. Parental care during chick rearing and Finally, although these suggestions may reduce the incubation in Humboldt penguins, Spheniscus humboldti. – M.Sc. thesis, Dalhousie University, Halifax, NS. impact of instruments on Humboldt Penguins, further Wanless, S., Harris, M. P. and Morris, J. A. 1988. The effect tagging efforts should be approached with caution. of radio transmitters on the behavior of common murres and razorbills during chick rearing. – Condor 90: 816–823. Acknowledgements – We thank G. Battistini, G. Mori, and N. Watanuki, Y., Mori, Y. and Naito, Y. 1992. Adelie penguin Ampuero for assistance in the field, and D. Boersma for parental activities and reproduction: effects of device size lessons in TDR deployment. We are grateful to A. Horn, S. and timing of its attachment during chick rearing period. – Iverson, C. Staicer, I. McLaren, W. Montevecchi, and two Polar Biol. 12: 539–544. anonymous reviewers for helpful comments on earlier drafts. Wienecke, B. C. and Robertson, G. 1997. Foraging space of Finally, we sincerely appreciate the financial assistance pro- emperor penguins Aptenodytes forsteri in Antarctic shelf vided by the Oregon Zoo, the Wildlife Conservation Society, waters in winter. – Mar. Ecol. Progr. Ser. 159: 249–263. the Smithsonian Institution Sisley Fund, the Friends of the Williams, T. D., Briggs, D. R., Croxall, J. P., Naito, Y. and National Zoo, the Canadian International Development Kato, A. 1992. Diving pattern and performance in relation Agency, the Manomet Center, Dalhousie University Faculty to foraging ecology in the , Pygoscelis of Graduate Studies, and NSERC. papua. – J. Zool. Lond. 227: 211–230. Wilson, R. P., Grant, W. S. and Duffy, D. C. 1986. Recording devices on free-ranging marine animals: does measurement affect foraging performance. – Ecology 67: 1091–1093. References Wilson, R. P., Coria, N. R., Spairani, H. J., Adelung, D. and Culik, B. 1989. Human-induced behaviour in Adelie pen- Bannasch, R., Wilson, R. P. and Culik, B. 1994. Hydrody- guins Pygoscelis adeliae. – Polar Biol. 10: 77–80. namic aspects of design and attachment of a back-mounted Wilson, R. P. and Wilson, M.-P. 1995. The foraging behaviour device in penguins. – J. Exp. Biol. 194: 83–96. of the Spheniscus demersus. – In: Dann, Croll, D. A., Osmek, S. D. and Bengtson, J. L. 1991. An effect P., Norman, I. and Reilly P. (eds). The penguins: ecology of instrument attachment on foraging trip duration in and management. Surrey Beatty and Sons Pty Limited, chinstrap penguins. – Condor 93: 777–779. Australia, pp. 244–265.

JOURNAL OF AVIAN BIOLOGY 32: 372–376. Copenhagen 2001

On cogniti7e conser7ation biology: why chickadees lea7e a patch of woodland

Thomas C. Grubb, Jr. and C. L. Bronson, Department of E7olution, Ecology, and Organismal Biology, The Ohio State Uni7ersity, Columbus, OH 43210-1293, USA. E-mail: [email protected]

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