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DDE effects on reproduction of ring doves
D D E EFFECTS ON R E P R O D U C T I O N OF R I N G DOVES M . A . HAEGELE (~ RICK H . HUDSON
United States Department of the Interior, Fish and Wildlife Service, Bureau o f Sport Fisheries and Wildlife, Building 16, Denver Federal Center, Denver, Colorado, USA
ABSTRACT
Reproductive performance was measured for 126 days in twelve pairs of ring doves (Streptopelia risoria) fed a diet containing 40 ppm of p,p'-DDE and in twelve other pairs given untreated food. The DDE-treated doves took an average of 2½ times longer to renest than controls, produced 13.5 ~ .fewer eggs~clutch, had l0 ~ thinner eggs, and experienced twice as great mortality of young; all these differences were statistically significant. Hatchability was also lower but not significantly so. Control birds nested forty-nine times during the study, laying two eggs in each clutch. DDEtreated birds nested only thirty-three times, laying an average of 1.7 eggs~clutch. The combined effects of DDE on reproduction resulted in only ten young being successfully raised by DDE-treated pairs versus thirty-five being raised by controls.
INTRODUCTION
Population declines of some species of raptorial and piscivorous birds have been attributed to organochlorine pesticide residues. The residue most commonly found in high concentration is DDE (Hickey & Anderson, 1968; Anderson et al., 1969; Keith et al., 1970). Laboratory studies have shown that DDE can decrease reproductive success in mallards, Arias platyrhynchos (Heath et al., 1969), and in black ducks, Arias rubripes (Longcore et al., 1971). The DDE diets in these studies caused eggshell thinning and cracking and embryonic mortality. Although most declining species of raptorial and piscivorous birds have altricial young, pen studies of the effects of DDE on reproduction reported to date have generally been with birds that are precocial. Typical reproductive studies with precocial species have measured eggs laid, egg fertility, embryonic mortality in a mechanical incubator, and survival of the hatched young in a mechanical brooder. 53
Environ. Pollut. (4) (1973) pp. 53-57--~) Applied Science Publishers Ltd, England, 1973--Printed in Great Britain
54
M . A . HAEGELE, RICK H. HUDSON
Such investigations do not take into account the full role of the adults. For successful nesting of wild birds, adult behaviour is of great importance in the incubation of eggs and survival of the young. The present study with nesting ring doves (Streptopelia risoria), an altricial species, provided some measure of the effects of D D E on the total reproductive cycle. METHODS
All birds used in the experiments were purchased from J. W. Steinbeck, Walnut Grove, California. All test birds had successfully reared at least one brood prior to the experiment. Lehrman & Wortis (1967) showed that ring doves were more proficient at nesting after one successful reproductive cycle, but that proficiency did not increase significantly after a second cycle. Alter rearing at least one brood, all test birds were kept in isolation for three to five weeks before the experiment began. Isolation cages were steel rat cages, 20 cm wide, 29 cm deep and 18 cm high, arranged so that no dove could see any other. At the start of the experiment, 48 birds were randomly divided into two groups of twelve pairs each. The treated group received a diet of Purina* pigeon chow containing 40 ppm of p,p'-DDE, and the control group received only Purina pigeon chow. Each pair was housed in the same nesting cage throughout the 126-day treatment period. These cages, 80 cm wide, 40 cm deep and 30 cm high, were constructed of wood with wire mesh doors. Each cage was supplied with food and water ad libitum, a glass nest bowl (11 cm diameter), and pine needles for nest building. Nest bowls were cleaned and new pine needles put in the cage when all young in the bowl had died or left the nest bowl, or the eggs had not hatched after 18 days of incubation (normal incubation period is 14 days). Each cage was illuminated from 0600 to 2000 h by a 7½-watt incandescent bulb mounted on the wire mesh door. The temperature was maintained between 22°C and 24°C except for a few hours when the air conditioner malfunctioned. All pairs were observed at least once a day throughout the study to record number of eggs laid, number hatched, behaviour and mortality of young. Shell thickness of hatched eggs, and unhatched eggs after the 18th day of incubation, was measured (membranes intact) with a micrometer. Unhatched eggs were cut in half at the equator, rinsed with water until clean, and air dried for at least 24 h before measurement. RESULTS
In all parameters measured, DDE-treated ring doves showed poorer reproductive performance than controls, and most of these differences were statistically significant (Table 1). Delayed renesting was one pronounced effect of the treatment, * Reference to trade names does not imply endorsement of commercial products by the Federal Government.
DDE EFFECTS ON REPRODUCTION OF RING DOVES
55
resulting in fewer nestings and fewer eggs laid. The mean number of days between nestings (6.5 compared with 16.9) does not include the interval between the last nesting and the end of the 126-day study period. Some birds had not renested for an extended period when the study ended (one treated pair never renested and three renested only once). I f these intervals were taken into account, the delay in renesting would be even greater than the two-and-a-half fold difference shown in Table 1. TABLE 1 EFFECTS OF DIETARY D D E ON REPRODUCTION OF RING DOVES DURING A 126-DAY TREATMENTPERIOD
Statistical analysis* Controls No. o f pairs A d u l t mortality N o . times pairs nested M e a n no. days to renesting N o . eggs laid M e a n no. eggs/clutch M e a n shell thickness (p) 1st nesting 2 n d - 5 t h nestings M e a n hatchability (%) M e a n mortality o f y o u n g (%) N o . y o u n g surviving for 21 days
12 0 49 6.5 98 2 137 132 58 31 35
D D Etreated 12 0 33 16.9 57 1.7 137 123 49 64 10
Significance
Test
Significance level >
S S S S
chi 2 AOV chi 2 chi2
0-01 0.01 0.0l 0.01
NS S NS S S
AOV AOV chi 2 AOV chi 2
0.01 0.001 0.01
* S = significant, N S = n o t significant, A O V = analysis o f variance.
Clutch size and shell thickness were also significantly reduced by the treatment, although these effects did not appear until the second clutch. In the first clutch, all. but one treated pair laid two eggs (all forty-nine control clutches had two eggs), and shell thickness in the two groups was identical. The delay in D D E effects was probably due to the short exposure period before egg laying began (average 6.8 days). Hatchability was lower in the treated than in the control group, but not significantly; it was noted that none of the nine single-egg clutches hatched. However, the two-fold increase in mortality of young in the treated group was highly significant. In both the control and treated groups, most mortality occurred in the first eight days after hatching and was commonly associated with young falling out of the nest bowl on to the cage floor. Once a young bird fell out of the bowl, it was ignored by its parents and soon died from exposure and lack of food. During the study, the behaviour of all birds was observed and recorded for a half-hour period each day, but behavioural characteristics were so numerous and varied that no conclusions could be drawn about treatment effects. To determine whether D D E would adversely affect nest attendance, each day the incubating bird in each pair was removed from the nest and placed on the cage floor, and the
56
M.A. HAEGELE,RICK H. HUDSON
length of time until either the male or the female resumed incubation was measured. This was done in the first and second nestings only. No difference between control and treated birds was found. DISCUSSION A similar delay in nesting caused by dietary p,p'-DDT has also been shown by Peakall (1970) in ring doves and by Jefferies (1967) in Bengalese finch, Lonchura striata. A ten-day delay in renesting, such as occurred in our study, could lower productivity of a population of birds that had experienced a failure of their first nesting attempts, particularly in northern latitudes where the breeding season is very short. Peakall (1970) suggested a possible mechanism for intfibition of renesting. He showed that birds treated daily with DDT have a significantly lower estradiol level in the blood and a much higher level of hepatic enzyme activity. DDE has also been shown to cause microsomal enzyme induction (Conney et al., 1967). Thus, a bird receiving DDE in its diet would take longer to attain the threshold level of estradiol in the blood stream necessary to stimulate renesting. The higher mortality observed in the young of our treated birds may have also been related to the microsomal liver enzyme induction and steroid destruction. If enzyme induction caused destruction of prolactin, crop development in preparation for feeding the young may have been delayed until after the young had hatched. If the young of the treated birds were under-fed, they may have been more active in seeking food from the brooding parents and thus run a greater risk o f falling out of the nest. This is one possible explanation for the higher mortality of young in the treated group. Peakall (1970) showed that single injections of 150 mg/kg of p,p'-DDE caused ring doves to lay eggs with mean shell weights 23 ~ lower than those of controls. The eggshell thinning observed in our study with dietary DDE averaged 10~. This suggests that a single large dose is more effective than chronic exposure in causing eggshell thinning in ring doves. In the studies with ducks fed DDE (Heath et al., 1969; Longcore ei al., 1971), eggshell thinning of 13 and 23 ~ contributed, through increased shell cracking, to significantly lower reproduction. The 10~ eggshell thinning in our doves was apparently too slight significantly to lower hatchability. However, in both the duck experiments and this study, mortality of young contributed greatly to the reproductive failure of DDE-treated birds.
REFERENCES ANDERSON,D. W., HICKEY,J. J., RISEBROUGH,R. W., HUGHES,D. F. & CHRISTENSEN,R. E. (1969). Significance of chlorinated hydrocarbon residues to breeding pelicans and cormorants. Can. Fld Nat., 83, 91-112.
DDE EFFECTS ON REPRODUCTION OF RING DOVES
57
CONNEY,A. H., WELCH,R. M., KUNTZMAN,R. & BURNS,J. J. (1967). Effects of pesticides on drug and steroid metabolism. Clin. Pharmacol. Ther., 8, 2-10. HEATH, R. G., SPANN, J. W. & KREITZER, J. F. (1969). Marked D D E impairment of mallard reproduction in controlled studies. Nature, Lond., 224, 47-8. HICKEY, J. J., & ANDERSON,D. W. (1968). Chlorinated hydrocarbons and eggshell changes in raptorial and fish-eating birds. Science, N.Y., 162, 271-3. JEFFEa~ES,D. J. (1967). The delay in ovulation produced by p,p'-DDT and its possible significance in the field. Ibis, 109, 266-72. KEITH, J. O., WOODS, L. A. & HUNT, E. G. (1970). Reproductive failure in brown pelicans on the Pacific coast. Trans. N. Am. Wildl. Conf., 35th, 56-64. LEHRmAN, D. S. & WORTIS, R. P. (1967). Breeding experience and breeding efficiency in the ring dove. Anita. Behav., 15, 223-8. LONGCORE, J. R., SAMSON,F. B. • WHITTENDALE,T. W. (1971). D D E thins eggshells and lowers reproductive success of captive black ducks. Bull. Environ. Contam. & ToxicoL, 6, 485-90. PEAKALL, n . B. (1970). p,p'-DDT effect on calcium metabolism and concentration of estradiol in the blood. Science, N.Y., 168, 592-4.
United States Department of the Interior, Fish and Wildlife Service, Bureau o f Sport Fisheries and Wildlife, Building 16, Denver Federal Center, Denver, Colorado, USA
ABSTRACT
Reproductive performance was measured for 126 days in twelve pairs of ring doves (Streptopelia risoria) fed a diet containing 40 ppm of p,p'-DDE and in twelve other pairs given untreated food. The DDE-treated doves took an average of 2½ times longer to renest than controls, produced 13.5 ~ .fewer eggs~clutch, had l0 ~ thinner eggs, and experienced twice as great mortality of young; all these differences were statistically significant. Hatchability was also lower but not significantly so. Control birds nested forty-nine times during the study, laying two eggs in each clutch. DDEtreated birds nested only thirty-three times, laying an average of 1.7 eggs~clutch. The combined effects of DDE on reproduction resulted in only ten young being successfully raised by DDE-treated pairs versus thirty-five being raised by controls.
INTRODUCTION
Population declines of some species of raptorial and piscivorous birds have been attributed to organochlorine pesticide residues. The residue most commonly found in high concentration is DDE (Hickey & Anderson, 1968; Anderson et al., 1969; Keith et al., 1970). Laboratory studies have shown that DDE can decrease reproductive success in mallards, Arias platyrhynchos (Heath et al., 1969), and in black ducks, Arias rubripes (Longcore et al., 1971). The DDE diets in these studies caused eggshell thinning and cracking and embryonic mortality. Although most declining species of raptorial and piscivorous birds have altricial young, pen studies of the effects of DDE on reproduction reported to date have generally been with birds that are precocial. Typical reproductive studies with precocial species have measured eggs laid, egg fertility, embryonic mortality in a mechanical incubator, and survival of the hatched young in a mechanical brooder. 53
Environ. Pollut. (4) (1973) pp. 53-57--~) Applied Science Publishers Ltd, England, 1973--Printed in Great Britain
54
M . A . HAEGELE, RICK H. HUDSON
Such investigations do not take into account the full role of the adults. For successful nesting of wild birds, adult behaviour is of great importance in the incubation of eggs and survival of the young. The present study with nesting ring doves (Streptopelia risoria), an altricial species, provided some measure of the effects of D D E on the total reproductive cycle. METHODS
All birds used in the experiments were purchased from J. W. Steinbeck, Walnut Grove, California. All test birds had successfully reared at least one brood prior to the experiment. Lehrman & Wortis (1967) showed that ring doves were more proficient at nesting after one successful reproductive cycle, but that proficiency did not increase significantly after a second cycle. Alter rearing at least one brood, all test birds were kept in isolation for three to five weeks before the experiment began. Isolation cages were steel rat cages, 20 cm wide, 29 cm deep and 18 cm high, arranged so that no dove could see any other. At the start of the experiment, 48 birds were randomly divided into two groups of twelve pairs each. The treated group received a diet of Purina* pigeon chow containing 40 ppm of p,p'-DDE, and the control group received only Purina pigeon chow. Each pair was housed in the same nesting cage throughout the 126-day treatment period. These cages, 80 cm wide, 40 cm deep and 30 cm high, were constructed of wood with wire mesh doors. Each cage was supplied with food and water ad libitum, a glass nest bowl (11 cm diameter), and pine needles for nest building. Nest bowls were cleaned and new pine needles put in the cage when all young in the bowl had died or left the nest bowl, or the eggs had not hatched after 18 days of incubation (normal incubation period is 14 days). Each cage was illuminated from 0600 to 2000 h by a 7½-watt incandescent bulb mounted on the wire mesh door. The temperature was maintained between 22°C and 24°C except for a few hours when the air conditioner malfunctioned. All pairs were observed at least once a day throughout the study to record number of eggs laid, number hatched, behaviour and mortality of young. Shell thickness of hatched eggs, and unhatched eggs after the 18th day of incubation, was measured (membranes intact) with a micrometer. Unhatched eggs were cut in half at the equator, rinsed with water until clean, and air dried for at least 24 h before measurement. RESULTS
In all parameters measured, DDE-treated ring doves showed poorer reproductive performance than controls, and most of these differences were statistically significant (Table 1). Delayed renesting was one pronounced effect of the treatment, * Reference to trade names does not imply endorsement of commercial products by the Federal Government.
DDE EFFECTS ON REPRODUCTION OF RING DOVES
55
resulting in fewer nestings and fewer eggs laid. The mean number of days between nestings (6.5 compared with 16.9) does not include the interval between the last nesting and the end of the 126-day study period. Some birds had not renested for an extended period when the study ended (one treated pair never renested and three renested only once). I f these intervals were taken into account, the delay in renesting would be even greater than the two-and-a-half fold difference shown in Table 1. TABLE 1 EFFECTS OF DIETARY D D E ON REPRODUCTION OF RING DOVES DURING A 126-DAY TREATMENTPERIOD
Statistical analysis* Controls No. o f pairs A d u l t mortality N o . times pairs nested M e a n no. days to renesting N o . eggs laid M e a n no. eggs/clutch M e a n shell thickness (p) 1st nesting 2 n d - 5 t h nestings M e a n hatchability (%) M e a n mortality o f y o u n g (%) N o . y o u n g surviving for 21 days
12 0 49 6.5 98 2 137 132 58 31 35
D D Etreated 12 0 33 16.9 57 1.7 137 123 49 64 10
Significance
Test
Significance level >
S S S S
chi 2 AOV chi 2 chi2
0-01 0.01 0.0l 0.01
NS S NS S S
AOV AOV chi 2 AOV chi 2
0.01 0.001 0.01
* S = significant, N S = n o t significant, A O V = analysis o f variance.
Clutch size and shell thickness were also significantly reduced by the treatment, although these effects did not appear until the second clutch. In the first clutch, all. but one treated pair laid two eggs (all forty-nine control clutches had two eggs), and shell thickness in the two groups was identical. The delay in D D E effects was probably due to the short exposure period before egg laying began (average 6.8 days). Hatchability was lower in the treated than in the control group, but not significantly; it was noted that none of the nine single-egg clutches hatched. However, the two-fold increase in mortality of young in the treated group was highly significant. In both the control and treated groups, most mortality occurred in the first eight days after hatching and was commonly associated with young falling out of the nest bowl on to the cage floor. Once a young bird fell out of the bowl, it was ignored by its parents and soon died from exposure and lack of food. During the study, the behaviour of all birds was observed and recorded for a half-hour period each day, but behavioural characteristics were so numerous and varied that no conclusions could be drawn about treatment effects. To determine whether D D E would adversely affect nest attendance, each day the incubating bird in each pair was removed from the nest and placed on the cage floor, and the
56
M.A. HAEGELE,RICK H. HUDSON
length of time until either the male or the female resumed incubation was measured. This was done in the first and second nestings only. No difference between control and treated birds was found. DISCUSSION A similar delay in nesting caused by dietary p,p'-DDT has also been shown by Peakall (1970) in ring doves and by Jefferies (1967) in Bengalese finch, Lonchura striata. A ten-day delay in renesting, such as occurred in our study, could lower productivity of a population of birds that had experienced a failure of their first nesting attempts, particularly in northern latitudes where the breeding season is very short. Peakall (1970) suggested a possible mechanism for intfibition of renesting. He showed that birds treated daily with DDT have a significantly lower estradiol level in the blood and a much higher level of hepatic enzyme activity. DDE has also been shown to cause microsomal enzyme induction (Conney et al., 1967). Thus, a bird receiving DDE in its diet would take longer to attain the threshold level of estradiol in the blood stream necessary to stimulate renesting. The higher mortality observed in the young of our treated birds may have also been related to the microsomal liver enzyme induction and steroid destruction. If enzyme induction caused destruction of prolactin, crop development in preparation for feeding the young may have been delayed until after the young had hatched. If the young of the treated birds were under-fed, they may have been more active in seeking food from the brooding parents and thus run a greater risk o f falling out of the nest. This is one possible explanation for the higher mortality of young in the treated group. Peakall (1970) showed that single injections of 150 mg/kg of p,p'-DDE caused ring doves to lay eggs with mean shell weights 23 ~ lower than those of controls. The eggshell thinning observed in our study with dietary DDE averaged 10~. This suggests that a single large dose is more effective than chronic exposure in causing eggshell thinning in ring doves. In the studies with ducks fed DDE (Heath et al., 1969; Longcore ei al., 1971), eggshell thinning of 13 and 23 ~ contributed, through increased shell cracking, to significantly lower reproduction. The 10~ eggshell thinning in our doves was apparently too slight significantly to lower hatchability. However, in both the duck experiments and this study, mortality of young contributed greatly to the reproductive failure of DDE-treated birds.
REFERENCES ANDERSON,D. W., HICKEY,J. J., RISEBROUGH,R. W., HUGHES,D. F. & CHRISTENSEN,R. E. (1969). Significance of chlorinated hydrocarbon residues to breeding pelicans and cormorants. Can. Fld Nat., 83, 91-112.
DDE EFFECTS ON REPRODUCTION OF RING DOVES
57
CONNEY,A. H., WELCH,R. M., KUNTZMAN,R. & BURNS,J. J. (1967). Effects of pesticides on drug and steroid metabolism. Clin. Pharmacol. Ther., 8, 2-10. HEATH, R. G., SPANN, J. W. & KREITZER, J. F. (1969). Marked D D E impairment of mallard reproduction in controlled studies. Nature, Lond., 224, 47-8. HICKEY, J. J., & ANDERSON,D. W. (1968). Chlorinated hydrocarbons and eggshell changes in raptorial and fish-eating birds. Science, N.Y., 162, 271-3. JEFFEa~ES,D. J. (1967). The delay in ovulation produced by p,p'-DDT and its possible significance in the field. Ibis, 109, 266-72. KEITH, J. O., WOODS, L. A. & HUNT, E. G. (1970). Reproductive failure in brown pelicans on the Pacific coast. Trans. N. Am. Wildl. Conf., 35th, 56-64. LEHRmAN, D. S. & WORTIS, R. P. (1967). Breeding experience and breeding efficiency in the ring dove. Anita. Behav., 15, 223-8. LONGCORE, J. R., SAMSON,F. B. • WHITTENDALE,T. W. (1971). D D E thins eggshells and lowers reproductive success of captive black ducks. Bull. Environ. Contam. & ToxicoL, 6, 485-90. PEAKALL, n . B. (1970). p,p'-DDT effect on calcium metabolism and concentration of estradiol in the blood. Science, N.Y., 168, 592-4.