GENERAL

AND

COMPARATIVE

ENDOCRINOLOGY

81, 217-226 (1991)

Reciprocal Changes in Corticosterone and Testosterone Levels following Acute and Chronic Handling Stress in the Tree Lizard, Urosaurus orna tus MICHAELC.MOORE,CHRISTOPHER Department

of Zoology,

W. THOMPSON,AND Arizona

State

University,

CATHERINE A. MARLER

Tempe,

Arizona

85287

Accepted January 17, 1990 To examine the reciprocal interactions among gonadal and adrenal steroid secretion, male tree lizards (Urosaurus ornatus) were subjected to two forms of stress. They were subjected either to the acute stress of being held in collecting bags for up to 4 hr or to the chronic stress of being maintained in individual cages in the laboratory for up to 3 weeks. In both cases, levels in stressed animals were compared to levels in free-living animals as controls. Under both conditions plasma levels of corticosterone increased and plasma levels of testosterone decreased compared to free-living controls. The response to the acute stress was much greater for both hormones than to the chronic stress, although in both cases testosterone levels changed less in response to stress than corticosterone levels. The corticosterone response to acute stress was extremely rapid with levels increasing over six-fold in the first 10 min. Plasma levels of corticosterone and testosterone were negatively correlated among individuals in the chronic stress experiment, but not in the acute stress experiment. This correlational evidence is consistent with the hypothesis of a direct effect of corticosterone levels on testosterone levels and suggests that these may only be expressed under some conditions. 0 1991 Academic Press, Inc.

It is widely accepted that exposure to stress causes an increase in glucocorticoid hormone secretion and a decrease in gonadal steroid hormone secretion in a wide variety of vertebrates (recent reviews by Greenberg and Wingfield, 1987; Wingfield, 1988; Moore and Deviche, 1988; Orchinik et al., 1988). For amphibians and reptiles, however, a critical examination of individual cases reveals that this generalization does not apply to a majority of cases. In many cases glucocorticoid hormones do not increase and in others gonadal sex steroid hormones either remain unchanged or actually increase. Furthermore, there is not always an inverse relationship between the secretion of glucocorticoid and that of gonadal hormones in all studies of stress. For many reasons, results of studies of endocrine responses to stress are difficult to generalize across species and across investigators. For example, (1) different in-

vestigators rarely use the same means of subjecting an animal to stress, (2) experiments done at different times of the day or year can yield different results, (3) males and females often respond differently, (4) domesticated animals may respond differently from nondomesticated forms, and (5) animals are often subjected to the stress of handling and captivity prior to the initiation of the stress study. All possible sources of discrepancies must be accounted for before solid interspecific comparisons can be made. Because of (1) the paucity of data regarding stress responses in poikilothermic vertebrates and (2) the need for further controlled studies to augment the data base for generalizations, we undertook a study of the endocrine stress response in the tree lizard, Urosaurus ornatus. This small (4-6 g) lizard is common at lower elevations (below 1500 m) throughout most of the arid 217 0016~6480/91 $1.50 Copyright Q 1991 by Academic Press, Inc. All rkhts of reproduction in any form resewed.

218

MOORE, THOMPSON,

southwestern United States and northwestern Mexico. In our locality, it has a prolonged breeding season with matings occurring from mid April through at least late July. Individual females may lay three to four clutches per year (Dunham, 1982; Thompson and Moore, unpublished). Prolonged drought is probably the most common natural stressor for breeding populations in our area (Thompson and Moore, unpublished; cf. Martin, 1973). Among the more successful generalizations about the occurrence of stress responses in different species is the hypothesis that stress responses will be present in species with prolonged breeding seasons but not in species with very short breeding seasons (Wingtield, 1988). The latter cannot afford the interruption if they are to have any chance of successful reproduction. This hypothesis predicts that U. ornatus will show a pronounced stress response. We tested this prediction by catching free-living male U. ornatus, subjecting them to both acute handling stress and chronic captivity stress, and determining the subsequent changes in plasma levels of corticosterone and testosterone. A difficult issue in the design of a study of responses to stress is the proper way to control for die1 variations (Lance and Lauren, 1984; Dauphin-Villemant and Xavier, 1987). The most common design is to initiate stress in all subjects at one time of day and record subsequent changes in hormone levels. However, in the absence of unstressed controls that are bled at the same time, it is impossible to determine whether the observed changes are responses to stress or are simply die1 fluctuations in hormones. When unstressed controls are unavailable, an alternative design, which we selected, is to initiate stress at staggered times so that all the animals are bled at the same time of day after having experienced various durations of exposure to stress. This controls for die1 variations in hormone levels, but does not control for differential responses to stress initiated at different

AND MARLER

times of day. We selected this design because (1) we felt it was more important to control for die1 variations and (2) it allowed us to conduct the entire acute experiment within the natural 4- to 6-hr activity period of these lizards when unstressed controls were available. In any other design, animals caught near the middle of the day and assigned to the 4-hr stress group would have been bled after natural activity had ceased and when no control samples could have been obtained. This was undesirable since studies of other reptiles have shown that plasma corticosterone levels are only elevated during the activity period (Chan and Callard, 1972; Lance and Lauren, 1984; Dauphin-Villemant and Xavier, 1987). MATERIALS

AND METHODS

Study area and animals. Both studies were conducted at the Coon Bluff Recreation Area (latitude 33“ 32’ N, longitude 111” 37’ W, elevation 500 m) along the Salt River north of Mesa, Arizona, from 26 May to 18 June 1987. This is the middle of the breeding season and other studies (Moore and Thompson, unpublished) have shown that circulating levels of corticosterone and testosterone do not change seasonally during this portion of the annual cycle in this species. The habitat consists of mature mesquite (Prosopis sp.) bosque that supports a high density of V. ornatus. Male V. ornatus are polymorphic for dewlap color and different colors appear to correspond to different male reproductive strategies (Hover, 1985; Moore and Thompson, 1990). Because males of different social status may exhibit different stress responses (Greenberg et al., 1984; Sapolsky, 1987), we confined this study to males that had orange dewlaps with a blue central spot. This is the most common color morph in this population and is characteristic of males that are resident territory holders (Moore and Thompson, 1990). Acute stress experiment. Males used in the acute stress experiment were captured by noosing on 27,28, and 29 May 1987. All animals were noosed less than 1 min after first being sighted. Animals were subjected to 4 hr, 1 hr, or 10 min of stress or were bled immediately as controls. Each animal was bled only once to avoid the confounding stress of hemodilution that would occur if animals were bled more than once. Stress consisted of holding each animal in an individual cloth bag suspended from the investigator’s belt while he searched for additional animals. All animals in the 4-hr stress group were caught at the beginning of the lizard’s daily activity period between 0757 and

219

STRESS AND REPRODUCTION 0905 hr. All animals in the I-hr stress group were caught between 0927 and 1037 hr. Animals caught between 1017 and 1301 hr were alternately assigned to the group to be held for 10 min or to the control group to be bled immediately. This staggering of the onset of stress resulted in all animals being bled between 1027 and 1306 hr. The final sample sizes were 11 animals in each of the four treatment groups. Samples of 80-100 pl of whole blood were collected by inserting a heparinized capillary tube into the orbital sinus. In all cases, blood was collected less than 1 min after first handling the lizard. Within 2 to 4 hr of being collected, the blood was separated by centrifugation and the resulting plasma decanted and frozen at - 20°C until assayed. After collection of the blood sample, each lizard was released. Chronic stress experiment. The chronic stress in this experiment was also staggered. Lizards were exposed to 3 weeks, 1 week, or 1 day of captivity or were bled in the field immediately after being noosed as controls. Each animal was bled (SO-100 )LI of whole blood) only once to avoid the confounding stress of hemodilution that would occur if animals were bled more than once. Twelve male CJ.ornatus for each of the three experimental groups were captured on 26 May, 10 June, and 17 June, respectively. In each case, males were caught between 0800 and 1200 hr, placed in a cloth bag, transported 60 km to the laboratory in an ice chest, and placed in cages the same afternoon. These animals were bled on 15 June, 17 June, and 18 June, respectively, between 1030 and 1100 hr. Ten male U. ornatus were captured on 16 June between 1005 and 1310 hr and bled immediately in the field to serve as controls. Again, the staggering allowed all animals to be bled over a 4-day period to control for seasonal variations in hormone levels. All animals were released at the collection site on 19 June after the experiment was terminated. Captive lizards were kept individually in small cages (37 X 42 x 45 cm). Each male was fed approximately 10-15 small crickets a week (as many as each would eat) and water was constantly available. The room was kept on a 14L: 10D photoperiod at a temperature of 26 * 2°C. Each lizard could regulate its body temperature to some degree by moving under or away from a clamp light with a 25-W bulb suspended 2 cm over the cage. Additional light was provided with 40-W fluorescent full-spectrum lights and blacklights suspended 14 cm over the cages. Animals were disturbed by people entering the room (1) once a day for feeding and watering and (2) an additional time on the days indicated above when animals were added to cages or blood samples were collected. On the day blood samples were collected, no one entered the animal room prior to entry of the investigators at 1030 hr. At that time, two investigators entered the room and one caught the first animal to be bled as quickly as possible. In this way, the first animal was bled within 2 min of entering the room. Blood

samples were collected from the orbital sinus. Each successive animal was bled at approximately 2-min intervals thereafter. It took 20-30 set to catch the animal in the cage and an additional 30-0 set to withdraw the blood. The time of withdrawal of each blood sample relative to when the room was first entered was recorded to determine if there was any effect of the amount of time people were present in the room before the animal was bled. Radioimmunoassays. Radioimmunoassays for testosterone and corticosterone were performed as described by Moore (1986, 1987) following ether extraction of 40 ~1 of plasma and chromatographic separation of the steroid hormones from each other and from interfering lipids on diatomaceous earth:propanediol: ethylene glycol microcolumns. Intraassay coefftcients of variation (N = 6) were 7.0% for both testosterone and corticosterone. All samples from each experiment were measured in a single assay to avoid any effect of interassay variation. Statistics. Hormone levels were log converted and then, unless stated otherwise, were analyzed by oneway analysis of variance (ANOVA) followed by the Student Newman-Keuls test. Level of significance is P < 0.05 unless stated otherwise.

RESULTS

Acute stress experiment. Levels of corticosterone (P < 0.001) and testosterone (P < 0.001) changed dramatically and inversely following exposure to acute handling stress (Fig. 1). Animals subjected to 10 min of handling stress had corticoste-

Minutes

FIG. 1. Changes in plasma levels of testosterone and corticosterone in freshly captured male Urosaurus ornatus as a function of duration of confinement stress in a collecting bag suspended from the investigator’s belt. Control values are plotted as 1 min of stress since that was the average time to withdraw a blood sample. Values shown are means * standard error.

220

MOORE,

THOMPSON,

rone levels that were already 6.6 times greater than levels of animals bled immediately after capture (P < 0.01). Corticosterone levels of animals subjected to 1 and 4 hr of stress were also significantly greater than control levels (P < 0.01 in both cases). In addition, the levels of animals subjected to 4 hr of stress were significantly greater than those of animals subjected to 10 min of stress, suggesting that corticosterone levels were continuing to rise over this time interval although at a much slower rate than during the initial 10 min of stress. Testosterone levels decreased in response to stress (P < O.OOl), but this response was not as rapid as the corticosterone response nor was the relative magnitude of change as great (Fig. 1). Testosterone levels after 10 min of stress were virtually identical to those in animals bled immediately. Although levels of testosterone had dropped substantially in animals subjected to 1 hr of stress, these levels were still not significantly different from those of either controls or animals bled after 10 min of stress. Testosterone levels were lowest in animals subjected to 4 hr of stress and these levels were significantly lower than those of animals in the other three treatment groups. There was no evidence of a relationship among individual levels of corticosterone and testosterone. Overall correlation between plasma corticosterone and testosterone, correlations at the individual time points, and correlations pooled across the four time points were not significant. Chronic stress experiment. Plasma levels of corticosterone and testosterone changed much less in response to chronic captivity stress than they did in response to acute handling stress (Fig. 2). When analyzed by ANOVA, plasma levels of corticosterone were not significantly different (Z’ = 0.097) among the treatment groups, even though they increased to over three times control levels by 21 days of captivity. However, changes in corticosterone appeared to be progressive as the duration of captivity in-

AND

MARLER

: [

40. 0 Testosterone

I

30 -.

1 I O--p-------i

T5T u’ rJ 20. $5 -I i

1

lo-

0 a

-OF 0

Corticosterone --i----------+ I 5

10

15

20

Days FIG. 2. Changes in plasma levels of testosterone and corticosterone in male Urosaurus ornatus as a function of time kept in captivity in individual cages. Control values are plotted as Day 0. Values shown are means * standard error.

creased (Fig. 2). Consistent with this suggestion, there was a significant positive regression between corticosterone levels and duration of captivity (2 = 0.11, P = 0.024). As in the acute stress experiment, the relative magnitude of the changes in testosterone was much less than in corticosterone. When analyzed by ANOVA, plasma levels of testosterone were not significantly different among the treatment groups. However, testosterone appeared to decline slightly and remain at a constant level (Fig. 2). This suggestion was weakly supported in a onetailed t test when the levels of all captive lizards on the 3 days were combined and compared to the levels of free-living controls (P = 0.049). It is interesting to note that, on the day before they were bled, the lizards subjected to 1 day of captivity stress had been held in a cloth bag for at least 4 hr and transported in a car. Thus, they had been subjected to acute capture and handling stress at least as severe as that experienced by the 4 hr group in the acute stress experiment above. The high levels of testosterone and low levels of corticosterone in the former suggest that these levels had recovered substantially after 1 night of captivity (cf. Licht et al., 1983). There was no significant effect of the time when the blood was collected relative

STRESS AND REPRODUCTION

to when the room was first entered for either corticosterone (2 = 0.036, P = 0.337) or testosterone (r = 0.001, P = 0.850) levels in a correlation analysis pooled across the 3 days samples were collected in captivity. This suggests either that the lizards were not stressed by the presence of humans in the room or that they had habituated to daily visits. The absence of a significant correlation, even in the group in captivity only 1 day, supports the former possibility. There was more evidence of individual relationships in corticosterone and testosterone in this experiment than in the acute study. Negative correlations between individual plasma levels of corticosterone and testosterone were significant overall (3 = 0.252, P = 0.0005; Fig. 3) and when pooled across the 3 days of collection in captivity (3 = 0.190, P = 0.0063). The former correlation indicates that there was an overall trend for testosterone to be lower when corticosterone was higher. The latter correlation indicates that there was a similar trend within the groups of captive animals bled on individual days and that this trend was consistent on all 3 days. DISCUSSION

These results demonstrate

that male U. to

ornatus respond rapidly and dramatically

0 Ar

0.5 -1.5

. -1.0 Log10

-0.5 (Corticosterone

0.0

0.5 Level

1 .o

1.5

(rig/ml))

FIG. 3. Relationship of plasma level of log-converted corticosterone levels and log-converted testosterone levels of male Urosaurus ornatus in the chronic captivity experiment.

221

acute handling stress with an increase in corticosterone. The rapidity of this response is equivalent to that documented in many mammals and birds. The rapidity of the response is an important issue since many naturally occurring stressors (e.g., predator attacks) are of short duration. The occurrence of this rapid response in U. OYnatus is also consistent with the predictions of the hypothesis that animals with lengthy breeding seasons will exhibit dramatic hormonal responses to stress (Wingfield, 1988). Interspecific comparisons are complicated by the factors mentioned in the introduction. We know of no other studies that have looked at rapid stress responses in poikilothermic vertebrates that have used free-living animals as controls (see Licht et al., 1983, 1985; Lance and Elsey, 1986; Whittier et al., 1987; Mahmoud et al., 1989 for studies with longer sampling intervals and free-living controls). We can therefore compare our data only to studies of animals that have been held in captivity prior to being subjected to acute handling stress. Only one study of a reptile, that of DauphinVillemant and Xavier (1987) on nonreproductive female Lucertu vivipuru, has examined the rapidity of the corticosterone response. In this sex of this species, there was no change in plasma corticosterone after 8 min of continuous blood withdrawal. If we assume that this result is not due to chronically high initial corticosterone levels due to captivity, then comparison of this finding with ours for U. ornutus illustrates that there is interspecific variation within squamate reptiles in the rapidity and magnitude of the stress response. Whittier et al. (1987) also present evidence that female Thumnophis sirtulis purietulis have little or no stress response. These results are superficially consistent with the breeding season duration hypothesis since both L. vivipuru, which occurs at high altitudes (Xavier, 1982), and T. s. purietulis, which occurs at high latitudes, have relatively short breed-

222

MOORE,

THOMPSON,

ing seasons. However, sex, reproductive condition, and time of year have also been shown to affect the stress response (Licht et al., 1983; Moore and Zoeller, 1985; Mahmoud et al., 1989) and could by themselves account for the interspecific differences. In a short-term study of confinement stress in an amphibian in captivity, F. L. Moore and Miller (1984) reported a fourfold increase in circulating corticosterone in 15 min in rough-skinned newts (Taricha grunulosa), another species with a long breeding season. Other studies that have documented the corticosterone response to stress in poikilotherms have not initiated sampling until 1 hr or later after the initiation of stress (Bradshaw, 1975; Callard, 1975; Gist and Kaplan, 1976; Licht et al., 1983; Lance and Elsey, 1986; Pickering et al., 1987; Whittier et al., 1987; Mahmoud et al., 1989). In some cases the magnitude of the response suggests that many of these species have the potential to respond as quickly as we have documented for U. ornutus; in others the low magnitude of the response suggests an inhibition of the stress response. However, until more studies are done with data on free-living animals as the baseline, comparisons will be complicated by the possibility of prestressed control animals. There is considerable variability in the baseline levels of corticosterone levels reported in various studies of reptiles. Some of this variation is due to methodological differences in the assays and some is due to the amount of presampling stress (cf. Lance and Lauren, 1984). Nevertheless, male U. ornutus have initial levels of corticosterone that are as low or lower than those reported in most other reptiles (Daugherty and Callard, 1972; Lance and Lauren, 1984; Greenberg et al., 1984; Dauphin-Villemant and Xavier, 1987; Whittier et al., 1987) including those of Scefoporusjurrovi measured in our own laboratory (Moore, 1987). Indeed, the increase in corticosterone levels in response to stress is so rapid and dramatic in U. ornutus, averaging almost 1 ng/mYmin in

AND

MARLER

the first 10 min, that it seems likely that even the levels reported in our initial samples represent an increase over the actual basal levels since it take up to a minute to collect the blood. The actual basal levels of corticosterone in U. ornutus may be extremely low. It is not known whether this contributes to the rapidity and the magnitude of the stress response in this species. It is also interesting that the levels of corticosterone after several hours of handling stress in U. ornutus are comparable to basal levels in other species; even our own measurements of the levels of S. jurrovi (Moore, 1987) where any possibility of methodological differences can be discounted. It has always been difficult to interpret interspecific differences in absolute levels of hormones. This result means either (1) that U. ornatus and S. jarrovi differ in their sensitivity to corticosterone or (2) that their sensitivity is similar and that the elevation of corticosterone in S. jarrovi reflects different metabolic requirements during its breeding season. The testosterone levels changed slowly in response to acute stress (cf. Lance and Elsey, 1986). Levels of testosterone were unchanged after 10 min and only reduced by 50% after 4 hr. The slow decline of testosterone levels could be due to a slow response in either secretion control mechanisms or clearance mechanisms. In either case, it is important to note that this study was done in the middle of the breeding season when testosterone levels are seasonally most stable, but that circulating levels in unstressed animals at this time are already 50% lower than the seasonal maximum in April (Moore and Thompson, unpublished). Despite this caveat, the lack of a rapid response in testosterone levels seems adaptive since it would seem inappropriate to interrupt testosterone-dependent reproductive function, especially spermatogenesis, in response to a relatively short duration of stress (Wingfield and Silverin, 1986; Wingfield, 1988). Since lizards usually respond

STRESS

AND

to naturally occurring acute stress, such as the presence of predators, by retreating to safety it seems unlikely that any lizard is exposed to acute stress long enough for interruption of testosterone-dependent reproductive function to occur. It is important to consider, however, that acute elevations of corticosterone can apparently inhibit sexual and aggressive behavior directly (F. L. Moore and Miller, 1984; F. L. Moore and Zoeller, 1985; Wingfield and Silverin, 1986; Tokarz, 1987). The changes in levels of both corticosterone and testosterone in response to chronic captivity were much less than to acute handling stress and were only revealed by secondary statistical analyses. The severity of the stress was obviously much reduced during chronic captivity. In fact, it is possible that the changes observed were not a response to stress at all. They may have been a response to the absence of stimuli present in the natural environment. In captivity, the males were provided with photothermal cues indicative of the breeding season, but were housed in isolation from other conspecifics, i.e., with no male-male or male-female interactions, and from other cues associated with their territory. Studies of birds have successfully accounted for differences in testosterone levels between captive and free-living males as the result of the absence of cues in captivity (Moore, 1982, 1983; Wingfield and Moore, 1987). However, in our study of U. ornatus, the observations of (1) a significant negative correlation between corticosterone and testosterone levels in individual captive males and (2) a progressive increase in corticosterone as the duration of captivity increased support the interpretation that the hormonal changes were stressrelated and not due simply to the absence of stimuli. In their studies of female L. vivipara, Dauphin-Villemant and Xavier (1987) demonstrated a corticosterone response to confinement in small cages after 1 and 18 hr.

REPRODUCTION

223

Also, they found that corticosterone was higher after 3 months of captivity than it was after 10 days. This is consistent with out observation of a progressive increase in corticosterone. Otherwise it is difficult to make comparisons since cage sizes and amount of disturbance to the animals while they are in the cages will always vary between studies. Also the response to confinement of animals with different activity patterns may vary. L. viviparu is an active, wide ranging animal while U. ornutus is more of a sit and wait predator. For the same reasons it is difficult to determine if the dramatic declines in testosterone reported for bullfrogs (Licht et al., 1983), turtles (Licht et al., 1985) and alligators (Lance and Elsey, 1986) and the dramatic increase in testosterone reported in snapping turtles (Mahmoud et al., 1989) in response to confinement are due to species or methodological differences. A final important issue concerns the extent to which reciprocal changes in corticosterone and testosterone are causally related. Several studies of nonmammalian vertebrates have shown that exogenous corticosterone can lower plasma testosterone levels to varying degrees (F. L. Moore and Zoeller, 1985; Wingfield and Silverin, 1986; Tokarz, 1987). However, at least one study has shown that under some conditions plasma levels of testosterone and corticosterone can rise simultaneously (Orchinik et al., 1988). These results suggest that the relationship is by no means simple and may vary under different conditions. In male U. ornutus, our observation that the rise in corticosterone levels occurs at least 1 hr before the decrease in testosterone levels during acute stress might superficially suggest that the rise in corticosterone causes the depression of testosterone levels. However, the lack of correlation between individual corticosterone levels and testosterone levels in this experiment suggests that these two events are at least partially independent of one another. In con-

224

MOORE.

THOMPSON,

trast, during chronic captivity, when the changes in hormone levels were much less dramatic, there was a significant relationship of individual corticosterone and testosterone levels. This suggeststhat there was a tighter relationship which is stronger evidence of a direct negative effect of increased corticosterone on plasma testosterone under these conditions. The diversity of reciprocal changes in corticosterone and testosterone suggests that there are multiple regulators of both the adrenal and the gonadal axes (Wingfield and Silverin, 1986; F. L. Moore and Deviche, 1988). Under some conditions they have reciprocal effects on one another and under other conditions compensatory responses of other regulatory pathways override these effects. For example, F. L. Moore and Zoeller (1985) demonstrated that exogenous corticosterone decreased testosterone levels and increased the hypothalamic content of GnRH in the roughskinned newt. This suggeststhat the cause of the decrease in testosterone levels was a decreased hypothalamic release of GnRH. However, simultaneous increases in testosterone and corticosterone like those reported by Orchinik ef al. (1988) in Bufo marinus could be achieved either by higher brain centers overriding the inhibitory effects of corticosterone on GnRH release by the hypothalamus or perhaps by hypothalamus-independent stimulation of the testes (e.g., Sharpe, 1984; Catiello et al., 1989). Our correlational results from U. ornatus are consistent with the hypothesis that during chronic captivity there was a direct effect of corticosterone on testosterone levels but that in the rapid response to acute stress both systems were responding at least somewhat independently. However, other less direct effects could account for these relationships (Greenberg and Wingfield, 1987; Mahmoud et al., 1989). In summary, our results in U. ornatus document one of the most rapid glucocorticoid responses to stress in any amphibian

AND

MARLER

or reptile studied so far. Our results also suggest that levels of corticosterone and testosterone return to near normal levels very quickly in captivity following acute handling stress. This indicates that chronic confinement in the cages used in our laboratory is only very mildly stressful to this species. Our correlational evidence suggests that reciprocal interactions of the adrenal and gonadal axes are complex and that direct effects may be expressed under some conditions but not others. In general, our knowledge of the endocrine response of poikilothermic vertebrates to stress is very fragmentary and the responses documented so far are diverse. Further studies are desperately needed, especially those (1) using free-living animals as controls, (2) investigating the effects of various hormonal manipulations on the stress response, and (3) investigating the response of free-living animals to naturally occurring stressors. The latter is especially needed to document the natural role of stress responses and to provide insight into their adaptive significance (Greenberg and Wingfield, 1987; Wingfield, 1988). ACKNOWLEDGMENTS This research was supported by Presidential Young Investigator Award DCB-8451641 from the National Science Foundation to M. C. Moore and by Arizona State University Graduate College Research Assistantships to both C. W. Thompson and C. A. Marler. We thank Matthew R. Brown and S. J. Schoech for valuable comments on earlier drafts.

REFERENCES Bradshaw, S. D. (1975). Osmoregulation and pituitary-adrenal function in desert reptiles. Gen. Comp. Endocrinol. 25, 230-248. Callard, G. V. (1975). Control of the interrenal gland of the fresh-water turtle, Chrysemys picta, in vivo and in vitro. Gen. Comp. Endocrinol. 25,323-331. Cariello, L., Romano, G., Spagnuolo, A., Zanetti, L., Fasano, S., Minnuci, S., Di Matteo, L., Peirantoni, R., and Chieffi, G. (1989). Molecular forms of immunoreactive gonadotropin-releasing hormones in hypothalamus and testis of the frog,

STRESS

Rana

esculenta.

Gen.

Comp.

Endocrinol.

AND

15,343-

348. Chan, S. W. C., and Callard, I. P. (1972). Circadian rhythm in the secretion of corticosterone by the desert iguana, Dipsosaurus dorsalis. Gen. Comp. Endocrinol. 18, 565-568. Daugherty, D. R., and Callard, I. P. (1972). Plasma corticosterone levels in the male iguanid lizard Sceloporus cyanogenys under the various physiological conditions. Gen. Comp. Endocrinol. 19, 69-79. Dauphin-Villemant, C., and Xavier, F. (1987). Nychthemeral variations of plasma corticosteroids in captive female Lacerta vivipara Jacquin: Intluence of stress and reproductive state. Gen. Comp. Endocrinol.

67, 292-302.

Dunham, A. E. (1982). Demographic and lie-history variation among population of the iguanid lizard Urosaurus ornatus: Implications for the study of life-history phenomena in lizards. Herpetologica 38, 208-221. Gist, D. H., and Kaplan, M. L. (1976). Effects of stress and ACTH on plasma corticosterone levels in the caiman, Caiman crocodilus. Gen. Comp. Endocrinol. 28, 413419. Greenberg, N., Chen, T., and Crews, D. (1984). Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis. Horm. Behav. 18, l-11. Greenberg, N., and Wingfield, J. C. (1987). Stress and reproduction: Reciprocal relationships. In “Hormones and Reproduction in Fishes, Amphibians and Reptiles” (D. 0. Norris and R. E. Jones, Eds.), pp. 461-505. Plenum, New York. Hover, E. L. (1985). Differences in aggressive behavior between two throat color morphs in a lizard, Urosaurus

ornatus.

Copeia

1985, 933-940.

Lance, V. A., and Elsey, R. M. (1986). Stress-induced suppression of testosterone secretion in male alligators. J. Exp. Zool. 239, 241-246. Lance, V., and Lauren, D. (1984). Circadian variation in plasma corticosterone in the American alligator, Alligator mississippiensis, and the effects of ACTH injections. Gen. Comp. Endocrinol. 54, l-7. Licht, P., Breitenbach, G. L., and Congdon, D. (1985). Seasonal cycles in testicular activity, gonadotropin, and thyroxine in the painted turtle, Chrysemys picta, under natural conditions. Gen. Comp. Endocrinol. 59, 130-140. Licht, P., McCreery, B. R., Barnes, R., and Pang, R. (1983). Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bullfrog, Rana catesbeiana. Gen. Comp. Endocrinol. 50, 124-145.

225

REPRODUCTION

Mahmoud, I. Y., Guillette, L. J., Jr., McAsey, M. E., and Cady, C. (1989). Stress-induced changes in serum testosterone, estradiol-17s and progesterone in the turtle Chelydra serpentina. Comp. Biothem.

Physiol.

A 93, 423427.

Martin, R. F. (1973). Reproduction in the tree lizard (Urosaurus ornatus) in central Texas: Drought conditions. Herpetologica 29, 27-32. Moore, F. L., and Deviche, P. (1988). Neuroendocrine processing of environmental information in amphibians. In “Processing of Environmental Information in Vertebrates” (M. H. Stetson, Ed.), pp. 19-45. Springer-Verlag, New York. Moore, F. L., and Miller, L. J. (1984). Stress-induced inhibition of sexual behavior: Corticosterone inhibits courtship behaviors of a male amphibian (Taricha

granulosa).

Horm.

Behav.

18, 400-410.

Moore, F. L., and Zoeller, R. T. (1985). Stressinduced inhibition of reproduction: Evidence of suppressed secretion of LH-RH in an amphibian. Gen.

Comp.

Endocrinol.

60, 252-258.

Moore, M. C. (1982). Hormonal response of freeliving male white-crowned sparrows to experimental manipulation of female sexual behavior. Horm.

Behav.

16, 323-329.

Moore, M. C. (1983). Effect of female sexual displays on the physiology and behaviour of male whitecrowned sparrows, Zonotrichia leucophtys. J. Zool.

199, 137-148.

Moore, M. C. (1986). Elevated testosterone levels during nonbreeding season territoriality in a fallbreeding lizard, Sceloporus jarrovi. .I. Comp. Physiol.

A 158, 159-163.

Moore, M. C. (1987). Circulating steroid hormones during rapid aggressive responses of territorial male mountain spiny lizards, Sceloporus jarrovi. Horm. Behav. 21, 511-521. Moore, M. C., and Thompson, C. W. (1990). Field endocrinology of reptiles: Hormonal control of alternative male reproductive tactics. In “Progress in Comparative Endocrinology” (A. Epple, C. G. Scanes, and M. H. Stetson, Eds.), pp. 685-690. Wiley-Liss, New York. Orchinik, M., Licht, P., and Crews D. (1988). Plasma steroid concentrations change in response to sexual behavior in Bufo marinus. Horm. Behav. 22, 338-350. Pickering, A. D., Pottinger, T. G., Carragher, J., and Sumpter, J. P. (1987). The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo

trutta

L. Gen.

Comp.

Endocrinol.

68,24%

259. Sapolsky, R. M. (1987). Stress, social status, and reproductive physiology in free-living baboons. In

226

MOORE,

THOMPSON,

“Psychobiology of Reproductive Behavior: An Evolutionary Perspective” (D. Crews, Ed.), pp. 291-322. Prentice-Hall, Engelwood Cliffs, NJ. Sharpe, R. M. (1984). Intratesticular factors controlling testicular function. Viol. Reprod. 30, 29-49. Tokarz, R. R. (1987). Effects of corticosterone treatment on male aggressive behavior in a lizard (Anolis sagrei). Horm. Behav. 21, 358-370. Whittier, J. M., Mason, R. T., and Crews, D. (1987). Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: Relationship to mating and gestation. Gen. Camp. Endocrinol. 67, 33-43. Wingtield, J. C. (1988). Changes in reproductive function of free-living birds in direct response to environmental perturbations. In “Processing of Environmental Information in Vertebrates” (M. H.

AND

MARLER

Stetson, Ed.), pp. 121-148. Springer-Verlag, New York. Wingfield, J. C., and Moore, M. C. (1987). Hormonal, social and environmental factors in the reproductive biology of free-living male birds. In “Psychobiology of Reproductive Behavior: An Evolutionary Perspective” (D. Crews, Ed.), pp. 149-175. PrenticeHall, Englewood Cliffs, NJ. Winglield, J. C., and Silverin, B. (1986). Effects of corticosterone on territorial behavior of freeliving male song sparrows Melospiza melodia. Horm. Behav. 20, 405417. Xavier, F. (1982). Progesterone in the viviparous lizard Lacerta vivipara: Ovarian biosynthesis, plasma levels, and binding to transcortin-type protein during the sexual cycle. Herpetoiogica 38, 62-70.

Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus.

To examine the reciprocal interactions among gonadal and adrenal steroid secretion, male tree lizards (Urosaurus ornatus) were subjected to two forms ...
917KB Sizes 0 Downloads 0 Views