Arch. Environ. Contam. Toxicol. 41, 215–220 (2001) DOI: 10.1007/s002440010240

A R C H I V E S O F

Environmental Contamination a n d Toxicology © 2001 Springer-Verlag New York Inc.

Courtship Behavior of Captive American Kestrels (Falco sparverius) Exposed to Polychlorinated Biphenyls S. A. Fisher,1 G. R. Bortolotti,1 K. J. Fernie,2,3 J. E. Smits,3 T. A. Marchant,1 K. G. Drouillard,4 D. M. Bird2 1 2 3 4

Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan S7N 5E2, Canada Avian Science and Conservation Centre, McGill University, Ste Anne de Bellevue, Quebec H9X 3V9, Canada Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada Watershed Ecosystems Program, Trent University, Peterborough, Ontario K9J 7B8, Canada

Received: 22 September 2000 /Accepted: 19 March 2001

Abstract. Polychlorinated biphenyls (PCBs) adversely affect reproduction in birds. Captive adult male and female American kestrels (Falco sparverius) were studied to investigate the potential behavioral and hormonal alterations during the courtship period resulting from clinical exposure to PCBs. American kestrels ingested 7 mg/kg/body weight/bird/day of a 1:1:1 mixture of Aroclors 1248, 1254, and 1260 through their diet of day-old cockerels. The dietary dosage of Aroclors resulted in environmentally relevant total PCB residues in the eggs, averaging 34.1 ␮g/g wet weight (geometric mean). There was no difference between treatment and control birds in the circulating levels of total androgens (p ⫽ 0.44) or in 17␤-estradiol (p ⫽ 0.29), one week following pairing. Male kestrels exposed to dietary PCBs exhibited significantly more sexual behaviors (p ⫽ 0.034) and flight behaviors (p ⫽ 0.026) than the control males. Sexual behaviors of male kestrels included; nest-box inspections, solicitation of copulation, the offer of food to the female, and giving the female food. The flight behaviors of the male included; flying from one perch to another and aerial display. In addition, the frequency of male sexual behaviors were correlated (r ⫽ 0.605, p ⫽ 0.001) with total PCB residues in the eggs of their mates. A concurrent study found that these same PCB-exposed kestrels experienced a delay in clutch initiation as well as a greater number of completely infertile clutches.

Due to their lipophilic nature, polychlorinated biphenyls (PCBs) preferentially bioaccumulate and biomagnify in the higher trophic levels of the food chain (Safe 1994; Hoffman et al. 1996a), where carnivores, such as raptors, are at the top. PCB residues have been implicated as a potential factor linked to the decreased reproductive success of wild raptors (Kozie and Anderson 1991; Hoffman et al. 1996b; Clark et al. 1998; Valkama and Korpimaki 1999; Vos et al. 2000). For successful

Correspondence to: G. R. Bortolotti; email: [email protected]

reproduction to occur, a number of hormonal, physiological, and behavioral events must be timed and integrated accurately (Wingfield 1990). As breeding behaviors are under hormonal control, and because PCBs may be endocrine disruptors (Blus and Henny 1997; Vos et al. 2000), behavior may be one mechanism responsible for reproductive failure. Aberrant behavior resulting from contamination has been implicated in reproductive problems of various avian species. Risebrough and Anderson (1975) believed that captive mallards (Anas platyrhynchos) exposed to PCBs deliberately destroyed their eggs. Egg-destroying behavior was also observed in gray herons (Ardea cinerea) and was attributed to organochlorine contaminants (Milstein et al. 1970). Decreases in nest defense behavior and nest attentiveness were observed in herring gulls (Larus argentatus) contaminated with PCBs (Fox et al. 1978). Nest defense behavior was also altered in merlins (Falco columbarius) (Fyfe et al. 1976; Fox and Donald 1980) and in prairie falcons (F. mexicanus) (Fyfe et al. 1976) exposed to organochlorine contaminants, including PCBs. Captive breeding ring doves (Streptopelia risoria) exposed to organochlorines through their diet experienced a delay in clutch initiation believed to result from the prolongation and increase in male wing-flipping behavior, which acts as a solicitation for copulation (McArthur et al. 1983). Tori and Peterle (1983) examined the effect of PCBs on courtship behavior between experimentally exposed and control mourning doves (Zenaida macroura carolinensis) and found no significant differences; however, a significant delay occurred in clutch initiation. Though it is plausible that contaminants can affect wildlife populations through behavioral changes, direct proof of altered behavior in free-ranging animals is difficult to obtain (Kulig et al. 1996). Additionally, when behavioral changes are observed, determining which pollutant is the cause of the altered behavior is complex because contaminants may act synergistically (Newton and Bogan 1978; Barron et al. 1995). Therefore, research should focus on laboratory studies where the contaminants can be administered in a controlled fashion and the animals can be observed in detail. Given the title of the “white mouse” of raptors (Wiemeyer and Lincer 1987), the American kestrel (Falco sparverius) is

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an ideal study animal. This small falcon is abundant in North America, and it has been studied in detail in both wild and captive environments, resulting in a vast information base (Bird 1988). Reduced reproductive success, in the form of delayed clutch initiation and complete clutch infertility, was observed in captive American kestrels exposed to PCBs (Fernie et al. 2001). Plausible explanations for this delay in clutch initiation and clutch infertility may result from behavioral and/or endocrinological changes. Therefore, this study focuses on the behavior of PCB-exposed captive kestrels during the courtship period, as well as the plasma levels of estrogen and testosterone, two circulating sex hormones that play a crucial role in courtship behavior (Silver and Ball 1989).

Materials and Methods Captive American kestrels of known age and pedigree were studied at the Avian Science and Conservation Centre of McGill University (Quebec, Canada). Male and female kestrels were randomly assigned to the PCB-exposed group (n ⫽ 25 pairs) or control group (n ⫽ 25 pairs). Each group was fed ad libitum on the kestrels’ regular diet of day-old cockerels. Based on data of PCB residues in potential prey of wild kestrels (Environment Canada, unpublished data) and typical PCB congeners found in wild birds of the great lakes and surrounding regions (Braune and Norstrom 1989; Clark et al. 1998), a dosage level was determined that would result in environmentally relevant residue levels (Fernie et al. 2000). Dietary PCB exposure began on 18 March 1998, approximately 1 month prior to pairing. Kestrels were exposed to a mixture of Aroclors 1248:1254:1260 (1:1:1 by weight), dissolved in safflower oil at a concentration of 4.85 mg/g total PCB. An aliquot of 100 ␮l of the PCB mixture was injected intracranially into frozen– thawed day-old cockerels. American kestrels generally show a preference for consuming the heads of cockerels (I. Ritchie, personal communication). Tissue residues indicate that the birds consumed approximately 7 mg/kg body weight/per day (Fernie et al. 2000). The resulting total PCB residues in eggs averaged 34.1 ␮g/g (geometric mean) on a whole egg wet-weight basis (Fernie et al. 2001), which are similar to levels found in the eggs of wild raptors that have experienced decreased reproductive success (Clark et al. 1998; Valkama and Korpimaki 1999). Kestrels in the control group received cockerels that were injected intracranially with 100 ␮l of safflower oil. Kestrels were paired on 21 April 1998. Pairs were genetically unrelated within the past seven generations, and each kestrel had previous breeding experience as inexperienced breeders are less likely to reproduce (I. Ritchie, personal communication). Each pair was housed in an outdoor breeding pen (2.3 ⫻ 0.9 ⫻ 3.6 m), containing a nest box (0.3 ⫻ 0.3 ⫻ 0.4 m) attached to the wall of the pen, two rope perches, one wood perch, and a one-way glass window (0.1 ⫻ 0.1 ⫻ 0.3 m) for behavioral observations. The treatment and care of the kestrels was conducted in accordance with the regulations set forth by the Canadian Council on Animal Care (Olfert et al. 1993).

Behavioral Observations Behavioral observations began 2 days after pairing to allow for acclimatization. The 50 pairs were observed over a 2 day cycle. On the first day of observation 25 pairs were chosen randomly from each group (PCB n ⫽ 12 or 13, control n ⫽ 12 or 13). Six or seven control pairs and six or seven PCB-exposed pairs were chosen randomly and observed in random order in the morning between 0830 and 1100 hours, and the remaining 12 or 13 pairs were observed in the afternoon between 1500 and 1730 hours. On the second day the remaining 25

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pairs were observed, half in the morning and half in the afternoon. The 2-day cycle was repeated, but pairs that had been observed during a morning period were observed in the afternoon, and pairs that had been observed in the afternoon were observed in the morning. The protocol of the 2– day cycle was followed until clutch initiation, upon which pairs would be excluded from observation. Each observation period was 10 min in length, and the number of behaviors performed by each kestrel per period was recorded (Table 1). Previous studies on the behavior and mate choice of American kestrels were used to determine which behaviors are performed during the prenesting period (Willoughby and Cade 1964; Balgooyen 1976; Duncan and Bird 1989; Palokangas et al. 1992; Villarroel et al. 1998). Behaviors during the courtship period that are necessary for the formation of a pair bond in this monogamous falcon include nestbox inspection, which is important in establishing a mutually acceptable nest (Willoughby and Cade 1964; Duncan and Bird 1989); foodtransfers, which convey information about the provisioning ability of the male and help achieve good body condition for the female necessary for laying and incubation (Palokangas et al. 1992; Villarroel 1998); and copulations, which may infer information regarding mate quality (Willoughby and Cade 1964; Duncan and Bird 1989; Villarroel 1998), as well as being necessary for fertilization.

Egg Collection and PCB Residue Analyses The kestrels were fed three cockerels/pair, the remains of old cockerels were removed and nest boxes were checked for the presence of eggs each day between 0800 and 0830 hours. After 10 days of incubation the eggs were candled to determine their fertility. One egg from each nest was collected (see details in Fernie et al. 2000) to determine PCB residue levels, thus providing an indication of the level of contamination of the female at the time of laying (Subramanian et al. 1986; Tanabe et al. 1986). The analyses of PCB residues have been described elsewhere (Fernie et al. 2000; Drouillard et al. 2001).

Statistical Analyses The courtship data were analyzed using two temporal perspectives: Julian date, which involved calender time periods, and nesting chronology, which used the 10 days prior to clutch initiation of each pair. Pairs that were successful in laying a complete clutch (n ⱖ 4 eggs) were used in the analyses of the courtship data (n ⫽ 24 PCB-exposed; n ⫽ 25 control). The two methods of courtship analysis were performed due to the delay in clutch initiation by PCB exposed pairs (Fernie et al. 2001). The Julian date gives information about the birds from the time of pairing to the time of clutch initiation. As pairs began laying they were excluded from observation, and as a result sample sizes decreased to 18 PCB-exposed and 17 control pairs. When using the Julian date method, we divided observations into time periods and used the pairing date as the start of the courtship period. For each time period we averaged two observation periods per pair, thus spanning 4 days. As many behaviors occurred infrequently, behaviors were placed into functionally similar groups (Table 1). The two behaviors that required both of the sexes, copulation and mounting, were kept separate from the behaviors that could easily be identified as being performed by either the male or the female (Table 1). The behaviors of the PCB-exposed and control groups were compared in each of the time periods using Mann-Whitney U tests. Because differences between the two experimental groups at each time period could be small, but may have a cumulative effect, cumulative means were calculated and the Kolmogorov-Smirnov two-sample test for cumulative distributions was performed. When this test was performed, one of the PCB-

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Table 1. Behavioral categories used in courtship observation and subsequent analysis Functional Category

Female sexual behavior

Male sexual behavior

Female/male flight behaviors Female/male body care Female/male inactivity Female/male food behaviors

Behaviors Copulation Mounting Solicits copulation Nest box inspection Solicits food transfer Solicits copulation Nest box inspection Offers food to female Gives food to female Flight Aerial display Preening Stretching Sleeping Resting Retrieve food from cache Retrieve food from ground Search for food Eating

appeared to perform more sexual behaviors than control males in time period two (U ⫽ 211.5, p ⫽ 0.068). PCB-exposed male kestrels performed more inactive behaviors in time period three than the control males (U ⫽ 184.5, p ⫽ 0.028). None of the functionally similar behaviors that were analyzed indicated a difference between PCB-exposed and control female kestrels. The categories of sexual and flight behaviors are likely related, as aerial display is an important component of mate choice but it is difficult to observe in captivity as confinement does not allow for intricate flight patterns (Balgooyen 1976; Duncan and Bird 1989). The trend where PCB-exposed male American kestrels performed flight behaviors and sexual behaviors more frequently than control males for each time period (Figures 1A and 1B), suggests that there could be a cumulative effect. Therefore, cumulative means were calculated for the 17 PCB-exposed and 17 control pairs that were observed for four time periods. We could not detect any significant differences between groups (Kolmogorov-Smirnov two-sample test, all ps ⱖ0.24).

Nesting Chronology exposed birds was randomly excluded from the analyses so sample sizes would be the same at 17 in each group. The nesting chronology method considered only the 10 days prior to clutch initiation as the courtship period. As a result, all pairs are compared at the same stage of reproduction, but had different lengths of exposure time to PCBs. Forty of 49 pairs were observed four or five times, 5 pairs were observed three times, and 4 pairs were observed six times. Each behavioral variable was summed for every kestrel for all the observations, and a mean was calculated for each bird as well as for each group. As done for the Julian date method, functionally similar behaviors were grouped (Table 1) and compared using Mann-Whitney U tests.

Blood Sampling and Hormone Analysis Approximately 1 ml of blood was taken from the jugular vein of each kestrel using a heparinized needle on 28 April 1998, 7 days after pairing. The plasma was frozen immediately until analyses could be performed at the University of Saskatchewan. A radioimmunoassay technique to determine the concentration of total plasma androgens in the males and 17␤-estradiol in the females as outlined in Bortolotti et al. (1996) and Wayland et al. (1998). Levels of circulating hormones were compared between the PCB-exposed and control group using a Mann-Whitney U test for the total plasma androgens and a t test for the 17␤-estradiol, given the nature of their distributions. All data were analyzed using SPSS software (Noru˘sis 1991).

Results

Male kestrels exposed to PCBs performed more flight behaviors (U ⫽ 189, p ⫽ 0.026, x៮ ⫽ 5.12, SD ⫽ 3.75), and more sexual behaviors (U ⫽ 194.5, p ⫽ 0.034, x៮ ⫽ 1.25, SD ⫽ 1.03), than the control kestrels (flight behaviors, x៮ ⫽ 2.96, SD ⫽ 2.33; sexual behaviors, x៮ ⫽ 0.70, SD ⫽ .069). Despite the greater frequency of male sexual behaviors performed by the PCB-exposed kestrels, no differences in copulation frequency (U ⫽ 252, p ⫽ 0.32) or in the frequency of mounting (U ⫽ 244.5, p ⫽ 0.09) was found. If the difference in male sexual and flight behaviors between the two groups is real, then behaviors may vary with the degree of PCB contamination. Pairs differed in PCB exposure in part because of the propensity of individual birds to eat heads, but, more important, because of the length of time exposed before laying. The earliest contaminated pair began laying after 36 days of PCB exposure, whereas the latest began 73 days after initial exposure. Initially, PCB levels found in eggs were weakly correlated with male sexual behavior (Spearman’s rho correlation coefficient one-tailed, n ⫽ 18, r8 ⫽ 0.447, p ⫽ 0.037, Figure 2) and male flight behavior (Spearman’s rho correlation coefficient one-tailed, n ⫽ 18, r8 ⫽ 0.330, p ⫽ 0.09). However, because PCB-exposed pairs laid later in the breeding season, a partial correlation analysis was performed to test for a relationship between total PCB residues in the egg and the behavior of the male after controlling for laying date. We could not detect a correlation for male flight behavior (partial correlation coefficient, n ⫽ 18, r ⫽ 0.31, p ⫽ 0.107); however, male sexual behavior was strongly correlated with total PCB residues (partial correlation coefficient, n ⫽ 18, r ⫽ 0.605, p ⫽ 0.001).

Julian Date Functionally similar behaviors were significant in only 2 of 12 behavioral categories and they occurred during time periods two and three. Male flight behaviors were performed more frequently by PCB-exposed birds than by control birds in time period two (U ⫽ 172.5, p ⫽ 0.011), and PCB males also

Hormone Analysis No difference could be detected between the PCB-exposed and control groups with regard to the circulating levels of sex hormones in males and females at the time of courtship. The

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Fig. 2. Scatterplot graph showing the mean number of male sexual behaviors performed by PCB-exposed American kestrels in relation to the total PCB residues found in the eggs of their female partner. An even stronger correlation exists when laying date is controlled for (see Results)

Fig. 1. (A) Mean (⫾ 1 SE) number of male flight behaviors; (B) number of male sexual behaviors performed by captive American kestrels over time. (Squares and solid line ⫽ PCB, circles and dotted line ⫽ control)

circulating levels of total androgens in the males did not differ significantly between the two groups (U ⫽ 273, p ⫽ 0.44; control: x៮ ⫽ 721.9, SD ⫽ 67.9; PCB: x៮ ⫽ 671.3, SD ⫽ 95.0). We could also not detect a difference between the levels of 17␤-estradiol of females between treatment groups (t ⫽ 1.062, d.f. ⫽ 48, p ⫽ 0.29; control: x៮ ⫽ 248.88, SD ⫽ 99.26; PCB: x៮ ⫽ 218.32, SD ⫽ 104.12).

Discussion Environmental contaminants have been shown to interfere with the normal reproductive success of wildlife (Donaldson et al. 1999; Vos et al. 2000). Specifically, organochlorines have been shown to alter both the reproductive success (Kozie and Ander-

son 1991; Hoffman et al. 1996b; Clark et al. 1998; Valkama and Korpimaki 1999; Vos et al. 2000) as well as the behavior of birds (Milstein et al. 1970; Risebrough and Anderson 1975; Fyfe et al. 1976; Fox et al. 1978; Fox and Donald 1980; McArthur et al. 1983). The decreased reproductive success experienced by our American kestrels exposed to PCBs included complete clutch infertility (Fernie et al. 2001). This problem could be associated with the females in that they may not have been receptive. However, we could not detect a lack of female sexual behavior. Clutch infertility could also be a product of infrequent copulations; yet we found that PCBexposed kestrels copulated as frequently as controls. The infertility problem is perhaps more plausibly linked to infertility of the males. A previous study on kestrels from the same colony, showed a decline of 22–27% in sperm numbers per ejaculate when birds were given Mirex and a similar dose of Aroclor 1254 (Bird et al. 1983). Another difference in the reproductive performance of kestrels in our study was that PCB-exposed birds exhibited a significant delay in clutch initiation (Fernie et al. 2000), which in wild raptors generally corresponds to smaller clutches and fewer offspring produced (e.g., Valkama and Korpimaki 1999). The sexual behaviors of the male kestrel are known to play a critical role in determining the timing of egg laying (Balgooyen 1976). Our colony pairs, in which the male is a yearling and thus inexperienced, often show a delay in clutch initiation or even a failure to reproduce apparently from a lack of courtship behavior (I. Ritchie personal communication). However, all of the males in our study were 2 years or older and had all bred previously. As the male kestrels exposed to PCBs performed more sexual behaviors, it seems odd that their mates delayed clutch initiation. Tori and Peterle (1983) found that breeding mourning doves exposed to PCBs also experienced a delay in clutch initiation but there were no differences in the courtship behaviors between control and exposed pairs. McArthur et al. (1983), found that ring doves exposed to a mixture of organo-

Courtship in PCB-Exposed Kestrels

chlorines also had a lengthened courtship period. However, consistent with our results, the exposed male ring doves spent a greater amount of time performing courtship behavior (McArthur et al. 1983). The greater frequency of sexual behaviors of the PCB-exposed male kestrels was also connected with the total PCB residue levels of the egg and therefore to contamination of the female at the time of laying (Subramanian et al. 1986; Tanabe et al. 1986). Because none of the courtship behaviors of females were different between the two groups, it is seems more plausible that the delay in clutch initiation can be attributed to physiological processes other than behavior. Female Bengalese finches (Lonchura striata) showed a delay in ovulation when exposed to an organochlorine (Jeffries 1967), and birds also experience a delay in follicular growth when exposed to PCBs (Biessmann 1982; Rattner et al. 1984). Both behavior and reproduction are under hormonal control (Silver and Ball 1989), making them vulnerable to the endocrine-disrupting effects of environmental contaminants including PCBs (Blus and Henny 1997; Vos et al. 2000). We collected blood for hormone analysis at the time of the greatest difference in behavior between PCB-exposed and control birds (Figure 1A and 1B), yet the circulating levels of total androgens in males and 17␤-estradiol in females did not differ between groups. Similar results were found by in breeding ring doves, where the levels of estrogen and androgen did not differ during the midcourtship period (McArthur et al. 1983). The fact that both the PCB-exposed and control birds had similar hormone levels suggests that they were all in the same phase of the breeding season (Rehder et al. 1986; Silver and Ball 1989). Relating behavioral changes to any adverse effects on the animal is typically very difficult (Fyfe et al. 1976; Fox and Donald 1980). An investigation into the nonbehavioral physiological effects of PCBs on American kestrels may yield insight into the mechanisms of reduced reproductive success.

Acknowledgments. We thank Ian Ritchie for his help and invaluable expertise in the management of the American kestrels at the Avian Science and Conservation Centre. We thank Jennifer Willson for her dedicated assistance. SAF would like to thank the University of Saskatchewan for their financial support through a graduate fellowship. KJF thanks the University of Saskatchewan for financial support through the Isabel Marı´a Lo´pez Martı´nez Memorial Scholarship. This study was partly funded by grants from the Canadian Network of Toxicology Centres (to GRB and JES), and from the National Sciences and Engineering Research Council (to GRB).

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