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Adoption as a conservation strategy for the magnificent frigatebird (Fregata magnificens).

In colonial birds that nest in trees and have altricial chicks (i.e., chicks without feathers and with eyes closed at hatching), early stages of parental care have been suggested to involve indirect recognition of chicks based on location of nest. Thus, a chick at the nest is treated as progeny, independent of its origin (Waldman, 1988). Presumably, movement of chicks between nests rarely occurs in nature. However, adoption is present naturally in some ardeids (Milstein et al., 1970), raptors (Poole, 1982; Bustamante and Hiraldo, 1990; Donazar and Ceballos, 1990), and storks (Redondo et al., 1995), but benefits of this behavior to fitness are uncertain. Furthermore, human-induced adoption in waterbirds has been successful when predation of nests has occurred (e.g., piping plovers Charadrius melodus; Midura et al., 1991). Thus, induced adoption could be used as a conservation strategy in seabirds whose populations have declined.

The magnificent frigatebird (Fregata magnificens)isa synchronously breeding and colonial-nesting seabird that has the longest period of parental care among all seabirds. The 3 months of biparental care of their single altricial chick is followed by 9-14 months of uniparental care by the mother (Diamond, 1972, 1973; osorno, 1999; Osorno and Szekely, 2004).

The magnificent frigatebird is listed as a high conservation concern by the North American Waterbird Conservation Plan because a decline in populations is suspected (Kushlan et al., 2002). The main breeding colonies on Mexican islands are in hurricane-prone regions in which environmental stresses, such as tropical storms, are common (National oceanic and Atmospheric Administration, http://csc-s-maps-q.csc.noaa.gov/ hurricanes/viewer.html). Storms can cause <83% mortality of chicks in a breeding season. Because unsuccessful parents rarely attempt to breed again in the same breeding season (osorno, 1996) and the species apparently does not exhibit adoption behavior under natural conditions (A. A. Lecona, in litt.), induced adoption could be used as a conservation strategy.

Inducing adoption requires understanding the kin-recognition process of the species. Because the magnificent frigatebird is a colonial species with altricial chicks, indirect mechanisms to identify chicks based on location of nests likely are used by parents during early stages of biparental care (A. A. Lecona, in litt.). Whereas, during uniparental care, direct recognition of offspring through calls is required because females must feed their fledging chicks (osorno, 1996). Our goal was to determine if induced adoptions were possible, based on the hypothesis that a foreign chick placed in the failed nest of foster parents is treated as kin during the period of biparental care to explore if induced adoption could be used as a management strategy.

Behavioral studies of magnificent frigatebirds were conducted (Madsen et al., 2007; Gonzalez-Jaramillo and de la Cueva, 2010) during the breeding season of November 2001-April 2002 on Isla Isabel, (21[degree]52'N, 105[degree]54'W), Pacific Ocean, Nayarit, Mexico. On Isla isabel, the main cause of death of chicks or failure of nests is intraspecific interference (Osorno, 1996). During our studies, we identified three orphaned chicks of different ages (orphaned chicks X, Y, and Z). When 19, 32, and 105 days old, respectively, these chicks were abandoned due to unknown causes. We also identified three breeding pairs of adults (foster-parents A, B, and C) whose chick had died (Table 1). We made three attempts to induce adoption of chicks. In late December 2001, we placed orphaned-chick X into the nest of foster-parents A, and in early January 2002, we placed orphaned-chicks Y and Z into nests of foster-parents B and C, respectively. Although we did not measure size of chicks, we estimated length of ulna (Table 1) using the ulna size-age curve calculated during the breeding season in 2001-2002 (Gonzalez-Jaramillo and de la Cueva, 2010).

Before onset of adoption trials, orphaned-chicks X and Y had been attacked in their original nests by adults for 3 consecutive days, while orphaned-chick Z had been placed into an artificial nest and fed by researchers for 3 weeks. Chicks acclimatize to humans, and 1 year before our study one chick was raised successfully by fishermen and administrative personal of the island to independence. During the first 6 weeks of nesting, one parent is constantly at the nest (Osorno, 1996); therefore, we placed chicks directly into nests of foster parents with either the male (foster-parents A) or female (foster-parents B and C) on the nest. In all three instances, foster parents did not seem to be aware of the death of their chick, because they kept attending the nest as if their chick was alive. Time between death of the chick of foster parents and start of adoption trials was 3 h for foster-parents A, 16 h for foster-parents B, and 15 min for foster-parents C. Time between when chicks were orphaned and adoption trials was 3 days for orphaned-chicks X and Y and 3 weeks for orphaned-chick Z.

We considered that the foster parent accepted the chick when it showed protective behavior toward the orphaned chick, i.e., when the parent sat on the chick covering it with its chest. In contrast, we considered that the foster parent did not accept the chick or the chick did not accept its foster parent, when either showed aggressive behaviors, i.e., constant parent-chick or chick-parent pecking from the moment the chick was placed in the nest until the chick was removed. In every instance, we o served the nest until recognition behavior was exhibited. After this, we visited the nest every 15-30 min to monitor behavior of foster parents and the orphaned chick until acceptance or rejection. Upon rejection, the chick was removed from the nest.

The time between placing the orphaned chick in the nest of foster parents and onset of recognition behavior toward the chick was 3 min for chick X, 15 min for chick Y, and <1 min for chick Z. Only one adoption was successful, as chick X was accepted and effectively provisioned and protected y foster-parents A until a tropical storm occurred in early April 2002 and almost all chicks on the island died, including chick X; the other two attempts failed (Ta le 1).

Our observations suggest that adoptions during the period of biparental care are possible and application of adoptions as a management strategy for conservation should be considered. However, because our study was based on few observations (n = 3), a more thorough investigation is needed.

in our successful adoption, difference in age between the orphaned and deceased chick was the smallest of all three pairs in our study, the male was on the nest, and a short time passed since the chick to be adopted was orphaned. Thus, we identified potential factors that might contribute to success or failure of an adoption: difference in size and age between the orphaned and the deceased chick; sex of the foster parent on the nest; discriminatory ability of the chick to be adopted; and time elapsed between when the chick was orphaned and onset of the trial. Adoption could be an important conservation strategy for breeding populations of magnificent frigate-birds, especially in regions with occurring environmental stresses or in colonies where productivity could fall below historical averages.

We thank Comision Nacional de Areas Naturales Protegidas and administrators of Isla Isabel National Park for permission and logistical support. CS thanks V. Madsen for support. Suggestions of two anonymous reviewers are appreciated.

Literature Cited

BUSTAMANTE, J., AND F. HIRALDO. 1990. Adoptions of fledglings by black and red kites. Animal Behaviour 39:804-806.

DIAMOND, A. W. 1972. Sexual dimorphism in breeding cycles and unequal sex ratio in magnificent frigate-birds. Ibis 114:395398.

DIAMOND, A. W. 1973. Notes on the breeding biology and behavior of the magnificent frigatebird. Condor 75:200-209.

DONAZAR, J. A., and O. CEBALLOS. 1990. Acquisition of food by fledging Egyptian vultures, Neophron percnopterus, by nest-swiching and acceptance by foster parents. ibis 132:603-617.

GONZALEZ-JARAMILLO, M., AND H. DE LA CUEVA. 2010. Natural streamer asymmetry in male magnificent frigatebirds Fregata maggnificensinfluence on mate selection and male parental care performance. Marine Ornithology 38:85-90.

KUSHLAN, J. A., M. J. STEINKAMP, K. C. PARSONS, J. CAPP, M. ACOSTACRUZ, M. COULTER, I. DAVIDSON, L. DICKSON, N. EDELSON, R. ELLIOT, R. M. ERWIN, S. HATCH, S. KRESS, R. MILKO, S. MILLER, K MILLS, R. PAUL, R. PHILLIPS, J. E. SALIVA, B. SYDEMAN, J. TRAPP, J. WHEELER, AND K. WOHL. 2002. Waterbird conservation for the Americas: the North American waterbird conservation plan. Version 1. United States Fish and Wildlife Service National Publications Clearinghouse, Washington, D.C.

MADSEN, V., T. DABELSTEEN, D. OSORIO, AND J. L. OSORNO. 2007. Morphology and ornamentation in male magnificent frigatebirds: variation with age class and mating status. American Naturalist 169:S93-S111.

MIDURA, A. M., S. M. BEYER, AND H. J. KILPATRICK. 1991. An observation of human-induced adoption in piping plovers. Journal of Field Ornithology 62:429-431.

MILSTEIN, P., S. LE, Y. PRESTT, AND A. A. BELL. 1970. The breeding cycle of the grey heron. Ardea 58:171-257.

OSORNO, J. L. 1996. Evolution of breeding behavior in the magnificent frigatebird: copulatory pattern and parental investment. Ph.D. dissertation, University of Florida, Gainesville.

OSORNO, J. L. 1999. Offspring desertion in the magnificent frigatebird: are males facing a trade off between current and future reproduction? Journal of Avian Biology 30:335-341.

OSORNO, J. L., AND T. SZEKELY. 2004. Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females. Animal Behaviour 68:337-342.

POOLE, A. 1982. Breeding ospreys feed fledglings that are not their own. Auk 99:781-784.

REDONDO, T. F., S. TORTOSA, AND L. ARIAS DE REYNA. 1995. Nest switching and alloparental care in colonial white storks. Animal Behaviour 49:1097-1110.

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Submitted 11 August 2010. Accepted 10 May 2012. Guest Associate Editor was James C. Bednarz.

Monica Gonzalez-Jaramillo, Christian Schloegl, Horacio de la Cueva *

Departamento de Ecologia y Sistemaatica Terrestres. El Colegio de la Frontera Sur, Avenida Rancho Poligono 2a, Parque Industrial Lerma, C.P. 24500, San Francisco de Campeche, Campeche, Mexico (MGJ)

Konrad Lorenz Research Station, Gruenau im Almtal and Department of Behavioural Biology, University of Vienna, Vienna, Austria (CS)

Biologia Experimental y Aplicada, Centro de Investigacion Cientifica y Educacion Superior de Ensenada, Km 107, Carretera Tijuana-Ensenada, Mexico, P.O. Box 434844, San Diego, CA 92143-4844 (HC)

* Correspondent: lujastro@yahoo.com
Table 1--Characteristics and recognition of deceased and orphaned
chicks associated with attempts to induce adoption of
orphaned chicks by magnificent frigatebirds (Fregata maggnificens)
at Isla Isabel, Nayarit, Mexico, during the breeding season 2001-2002.

           Deceased chick     Orphaned chick       Difference

           Age at   Length              Length             Length
Foster     death    of ulna     Age     of ulna    Age     of ulna
parents    (days)    (cm)     (days)     (cm)     (days)    (cm)

A            11       4.1     22 (X)      5.3       11       1.2
B            3        3.2     35 (Y)      6.8       32       3.6
C            42       6.9     126 (Z)    23.2       84      16.3

          Components of recognition

          Identity of     Parental       Decision and
Foster     signal of      perception    application of
parents    orphaned      of signal of    recognition
             chick        orphaned
                            chick

A         Vocalization       Yes        Acceptance (a)   Protection
B         Vocalization       Yes        Rejection (b)    Aggression
C         Vocalization       Yes        Rejection (b)    Aggression (b)
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Title Annotation:Notes
Author:Gonzalez-Jaramillo, Monica; Schloegl, Christian; de la Cueva, Horacio
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Sep 1, 2012
Words:1848
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