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    Ontogeny or cortisol stress

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    © All Rights Reserved
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    4 views9 pages

    Ontogeny

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    Yira Karina Jimenez
    Ontogeny or cortisol stress

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    GENERAL AND COMPARATIVE ENDOCRINOLOGY 97, 57-65 (1995) Ontogeny of the Cortisol Stress Response in Larval Rainbow Trout ‘TeRENCE P. Barry, JEFFREY A. MALISO! N, JAMES A. HELD, AND JOHN J. PaRRISH* University of Wisconsin Aquaculture Program, Department of Food Science, 103 Babcock Hall, Madison, Wisconsin 53706; and *Department of Meat and Animat Science, 1675 Observatory Drive, Madison, Wisconsin 33706 Accepted September 27, 1994 ‘The ontogeny of the interrenal stress response in rainbow trout was characterized by measuring resting and acute-siress-induced changes in whole-body cortisol levels in em- bryos and larvae at different early developmental stages. In Experiment 1, resting cortisol levels averaged 6.0 ng/g in newly fertilized eggs, fell to less than 0.3 ngfg by the time of Iratching at Week 4 (incubation at 10°), and increased to 1.4 ngig by Week 5, Cortisol levels, did not change in response to acute stress in 3- 4, or S-week-old fish. In Experiment 2, resting cortisol averaged 1.4 ng’e in newly fertilized eggs, fell to less than 0.03 ng/g by Week 2, and then steadily increased between Weeks 3 and 6 to a peak of 4.8 ng/g before falling to 1.2 nglg by Week 7. Cortisol levels did not change in response to acute stress in 3+, 4-, or Seweek-old fish. Six-week-old fish showed a 2.3-fold increase in cortisol levels at 1 hr Poststress, indicating that the hypothalamic-pituitary-interrenal axis first develops respon- ess to stress 2 weeks after hatching and | week before the onset of exogenous feeding ‘The stress hyporesponsive period after hatching in rainbow trout may be homologous to the 2.week stress hyporesponsive period after birth in rodents, the function of which may be to maintain low, constant corticosteroid levels during a critical developmental period when these steroids can have permanent effects on neural organization. As suggested for mam- mals, this period may be a time when rainbow trout are particularly vulnerable to environ- mental effects on their subsequent development. Compared to mammals and birds, very little is known about the ontogeny of the hypothalamic—pituitary-interrenal (HPI) axis of fish (Carsia and Malamed, 1989). In mammals, an increase in adrenocortical ac- tivity occurs toward the end of gestation, and elevated corticosteroid levels at this time are required for the maturation of fetal organ systems (Liggins, 1976) and the initi- ation of parturition (Thorburn and Challis, 1979; reviewed by Carsia and Malamed, 1989). In rats, basal corticosteroid levels decrease dramatically after birth and re- main low for 2 weeks during which time stressors such as electric shock, ether, his- tamine, heat, cold, or a novel environment do not elicit increases in circulating gluco- corticoid levels as they do in adult animals (Schapiro, 1962; reviewed by Sapolsky and Meaney, 1986; DeKloet e7 al., 1988). It has been postulated that the function of this © 1995 Academie Press ne 2-week stress hyporesponsive period is to maintain constant corticosteroid levels dur- ing a critical time when these steroids can have permanent effects on neural organiza- tion and development (see Sapolsky and Meaney, 1986; DeKloet et al., 1988). In birds, glucocorticoid concentrations in adrenal tissue, allantoic fluid, and plasma indicate that the hypothalamic-pituitary- adrenal axis (HPA) first develops respon- siveness to stress midway through the em- bryonic period. Stress responsiveness grad- ually increases and then markedly rises just before hatching (reviewed by Carsia and Malamed, 1989). In some birds a stress nonresponsive period occurs after hatching that is similar to the stress hyporesponsive period of mammals but which lasts only 48 hr (Freeman and Flack, 1981; Freeman, 1982; Freeman and Manning, 1984; Wise and Frye, 1973). 37 016-6480195 $5.00 Copyright ©1985 by Academic Press, Ine AL ight of eproductin in en form reserved, 58 BARRY ET AL. In fishes, the ontogeny of interrenal cor- ticosteroid biosynthesis differs among spe- cies depending on their life history. In the lampreys Lampetra planeri and Petromy- zon marinus, for example, cortisol synthe- sis begins at metamorphosis (Weisbart, 1975; Weisbart and Youson, 1975; Seiler et al., 1983). Likewise, in the Japanese floun- der (Paralichthys olivaceus) the interrenal tissue begins to actively secrete cortisol at metamorphosis, 2 weeks after hatching (De Jesus ef al., 1991). In salmonids, however, which have relatively long developmental times in ovo and no distinct metamorpho- sis, the interrenal may be capable of corti- sol secretion prior to hatching. Embryonic rainbow trout (Oncorhynchus mykiss), for example, can synthesize cortisol from pro- gesterone as early as 1 week after fertiliza- tion (Pillai et af., 1974), and the chum salmon (Oncorhynchus keta) interrenal is also active before hatching as evident from changes in baseline whole-body cortisol (De Jesus and Hirano, 1992). Although such data indicate that the i terrenal tissue of embryonic or larval fish may be capable of producing corticoste- roids, they do not necessarily indicate that the HPI axis as a whole is integrated and capable of responding to environmental or psychological stressors with an increase in cortisol production. In adult fish, plasma cortisol levels increase 10- to 100-fold 30 min to 1 hr following an acute stressor and then slowly return to resting levels over the next 3 to 24 hr (Barton and Iwama, 1991). It is not known in any teleost species when this interrenal stress response first devel- ops (Carsia and Malamed, 1989). The pur- pose of our investigation was to document the ontogeny of the interrenal stress re- sponse in rainbow trout by subjecting fish at different developmental stages to a stan- dardized acute stressor and measuring changes in whole-body cortisol. MATERIALS AND METHODS Fish. Eggs were fertilized and incubated in }10-titer tanks with flow-through water at 10° under a 16-br light/8-hr dark photoperiod. Hatching occurred 4 weeks after fertilization (Days 27-29). Fish were fed commercial starter diet (Zeigler Brothers, Inc., War- renton, PA} beginning on Week 7 (after the 7-week-old fish had been sampled). Food was withield for 24 hr before sampling the 8 and 9-week-old larvae. Em- bryos and larvae were staged according to the method ‘of Vernier (1968). Stress test. The development of the interrenal stress response was characterized by subjecting groups of fish to an acute stress challenge test and measuring whole body cortisol 1, 3, $, and 24 hr later. To obtain Prestress cortisol levels at Time O hr, fish were quickly netted from the tank, placed into preweighed 20-ml slass scintillation vials (one to five fish per tube, de- Pending on fish size), and immediately frozen by im- mersion in a dry ice/ethanol bath. The stress challenge test consisted of netting a group of fish (~50) from each tank, holding them out of the water for 30 sec, and immediately placing them into a 0° ice bath for an additional 30 sec. The stressed fish were then placed into flow-through, S-liter recovery tanks at 10°. One, 3, 5, of 24 hr later, groups of fish were quickly netted from the recovery tanks, placed into preweighed vials, immediately frozen, and stored at — 40°. Fish weights were recorded to the nearest 0.01 g. Cortisol extraction. All fish were extracted after no more than 1 week of storage at — 40". One milliliter of| distilled water and ~1,000 dpm (25 x) of [HIcortisol in borate-BSA buffer (0.4 g boric acid, 0.2 g bovine serum albumin, and 0.1 g sodium azide per liter of water, pH 8.0) were added to the frozen fish in each vial. The fish were disrupted by ultrasonication (Heat Systems-Ultratronies, Inc., Model W-225R, Pi view, NY) and immediately refrozen by immersing the Vial in a dry icelethanol bath. Ten milliliters of diethyl ether were added to each vial. Each vial was capped, thawed, vigorously vortexed three times for I min, and centrifuged at 1000g for 5 min. The water phase was frozen in adry ice/ethanol bath and the ether decanted into a clean 20 x 150 test tube. Each sample was then extracted a second time. The test tubes were placed into 2 water bath at 45° and the ether evaporated under 4 stream of nitrogen gas. ELISA. Cortisol was measured by enzyme-linked immunoassay (ELISA) according to the procedure of Barry ef al. (1993). The assay was validated for mea- suring cortisol in whole embryonic and larval extracts by verifying that serial dilutions of these sample hibited the binding of cortisol in parallel with cortisot standards. One milliliter of cortisol-horseradish per- ‘oxidase conjugate buffer was added to each test tube, ‘The tubes were vortexed three times for | min. Corti sol was measured by ELISA in two 50-,i aliquots from each tube. Two additional $0-ul aliquots were taken to determine PH]cortisol recovery. Histology. To document the anatomical develop- tment of the interrenal tissue, three to six individuals were collected at Weeks 3, 4, 5,6, and 7and processed STRESS RESPONSE IN RAINBOW TROUT. 59 for tight microscopic examination, Unhatched em- bryos were removed from the egg, yolk sacs were re- moved, and the body cavities of the fish were opened to facilitate fixation of the intertenal tissue. ‘The fish were fixed for 24 hr in Bouin's fixative solution. The samples were processed using routine histological pro- cedures, sectioned midsagitally at 3-5 um, and stained with hematoxylin and cosin. Interrenal cells were identified on the basis of descriptions in Hibiya (1982) ‘and Yasutake and Wales (1983). Experiment 1. The objectives of the first experiment ‘were to validate the extraction and ELISA procedures. and determine the range of cortisol levels expected during early embryonic and lerval development. Eggs and sperm were obtained from the Seven Pines Hatch- ery (Lewis, WD, Eggs from 6 individual females were fertilized with the pooled milt of 12 males and reared in separate tanks. A randomized complete block design was used with the offspring from an individual female representing one block. Resting cortisol levels were measured at the time of fertilization and on Weeks 3, 4 and 5, at which times acute stress tests were also con- ducted. Experiment 2. The objective of Experiment 2 was to document the ontogeny of the cortisol stress response in rainbow trout by measuring changes in whole-body cortisol levels in embryos and larvae subjected to an acute stress. Eggs and sperm were obtained from Idaho Fish and Game (Hayspur, ID). Eggs from 6 in- dividual females were fertilized with the pooled milt of 12. males and reared in separate tanks. Bascline corti- sol levels were measured in newly fertilized eggs and 2- to 9-week-old fish. Acute stress tests were con- ‘ducted on Weeks 3 09. A randomized complete black design was used with eggs from an individual female representing one block. Because of poor fertilization rates with the eggs of two females, the number of blocks decreased from six to four after Week 5. Statistics. The data were first analyzed using Bartlett's test for homogeneity of varianee. In all cases, the data were homoscedastic and subsequently analyzed by ANOVA. Stress-induced changes in cor- tisol levels within weeks and cortisol levels within poststress time between weeks were compared using protected LSD tests RESULTS: Experiment 1. Cortisol recovery rates from extracted tissues averaged over 95%. Changes in weekly resting whole-body cor- tisol levels are shown in Fig. 1. Cortisol levels averaged 6.0 ng/g at the time of fer- tilization, decreased to 1.0 ng/g by Week 3 (P < 0.05), and fell further between Weeks 3 and 4 to less than 0.3 ng/g (P < 0.05). Fertilization Cortiso ng/e) * o 1 2 3 4 8 Time After Fertilization (weeks) Fro. I. Changes in resting whole-body cortisol lev- ‘els during early development of rainbow trout. Verti- ‘cal bars represent standard errors of the means (n 4), Asterisks indicate cortisol values significantly dif- ferent from those of the previous week (P < 0.08) Hatching occurred on Week 4. An increase in resting cortisol levels occurred between Weeks 4 and 5 to 1.4 ng/g (P < 0.05). Acute stress challenge tests were conducted on Weeks 3, 4, and 5. No significant changes in cortisol levels relative to baseline levels ‘occurred at 1, 3, 5, or 24 hr poststress (data not shown). Experiment 2. Cortisol levels at the time of fertilization were 1.4 ng/g (Fig. 2). By Week 2, resting cortisol levels had de- creased to less than 0.03 ng/g (P < 0.05) and was found at a similarly low level 3 weeks postfertilization. Cortisol increased to 0.5 ng/g between Weeks 3 and 4 (P < 0.05). Hatching occurred 4 weeks postfertiliza- tion. Between Weeks 4 and 5, resting cor- tisol levels increased to 2.2 ng/g (P < 0.05) and increased further between Weeks 5 and 6 to 4.9 ngig (P < 0.05). Cortisol levels then declined to 1.2 ng/g by Week 7 (P < 0.05) and remained at this level through Weeks 8 and 9 (Fig. 2). No significant differences in cortisol rel- ative to prestress levels were detected in 3-, 4-, or S-week-old-fish at 1, 3, 5, or 24 hr following the acute stressor (Fig. 2, 5, and 24 hr data not shown). In 6-week-old Jarvae (stage 34), there was a 2.3-fold increase in cortisol levels I-hr poststress (P < 0.05). 60 BARRY ET AL. ‘Time Post-Suress (hr) ae wim Contzat toga) Fic. 2. Changes in whole-body cortisol levels in rainbow trout in response to acute stress (30-sec handling followed immediately by a 30-sec 0° cold shock) as a function of early developmental stage. Vertical bars represent standard errors of the means (n = 6 on Weeks 3-5 and n = 4 on Weeks 6-9). Within each stage, asterisks indicate cortisol levels that are significantly (P < 0.05) different from restress levels (ie., 0 hr poststress). Fish at 7, 8, and 9 weeks of age (stages 35 and 36) also showed significant elevations in cortisol 1 hr poststress, although the ab- solute levels of cortisol at 1 hr were 54-61% lower (P < 0.05) than they were in the 6-week-old larvae (Fig. 2). The relative changes in cortisol from 0 to | hr poststress, however, were greater in a 7- to 9-week-old fish than in 6-week-old fish because the former had lower resting cortisol levels. Cortisol returned to prestress levels by 3 hr poststress in all but the 7-weck-old fish (stage 35). At no time except Week 9 were differences in cortisol detected in fish sam- pled at 3, 5, or 24 hr poststress. In 9-week- old fish, cortisol levels were significantly higher 24 hr poststress (7.1 ng/g) than they were at 3 br (3.3 ng/g). No interrenal cells were observed in fish at 3 or 4 weeks of age. Beginning on Week 5, cells that could be distinguished from the surrounding hematopoietic tissue were ob- served in the head kidney. There were very few of these cells, however, and they could not be unambiguously identified as interre- nal cells. Clearly distinguishable interrenal cells were first observed in 6-week-old fish (Fig. 3). These cells were found within the hematopoietic parenchyma and had spheri cal, darkly stained nuclei containing tinct nucleoli. In general, the interrenal cells were arranged in islets of 2 to 20 cells. Renal tubules and nucleated red blood cells were common within the hematopoietic pa- renchyma at all developmental stages ex- amined (Fig. 3). DISCUSSION Newly fertilized rainbow trout eggs con- tained high levels of cortisol that steadily declined to very low levels just before hatching. These data suggest that cortisol of maternal origin is stored in the eggs and may be used during early embryonic devel- opment, as hypothesized for several other teleosts (De Jesus ef al., 1991; De Jesus and Hirano, 1992; Yamano ef al., 1991; Hwang et al., 1992). Resting cortisol levels first in- creased at the time of hatching (stage 30), STRESS RESPONSE IN RAINBOW TROUT 61 Fic. 3. Head kidney of larval rainbow trout: (a) 5-week-old larvae (stage 32); (b) 7-week-old larvae (stage 35). Red blood cells (1), hematopoietic tissue (hp, renal tubule (k), and interrenal cells (i). 400%, indicating that larval corticosteroidogenesis probably begins at that time. These results are compatible with the report that whole- body cortisol levels increase during the first 5 days after hatching in rainbow trout (Hwang et al., 1992). Cortisol production occurred at a time when no differentiated interrenal cells were visible in the head kid- ney, suggesting that the enzymes necessary for cortisol biosynthesis may be present in undifferentiated interrenal cells. Using ra- diotracer methodology, Pillai er al. (1974) found that corticosteroid biosynthesis from exogenous progesterone increases over 40- fold between developmental stages 15 and 29. Other evidence in rainbow trout, how- ever, indicates that stage 16 embryos can- not synthesize corticosteroids from choles- terol because they lack 3B-hydroxysteroid dehydrogenase (3B-HSD) and A‘-steroid hydroxylase activities (Antila, 1984). ‘The maturation of interrenal function, there- fore, may require the development of these enzyme systems. In mammals, the maturation of fetal adre- nal function is primarily regulated by ACTH, which acts to increase the number of ACTH receptors on the adrenal cells and enhance the activities of adenylate cyclase and various steroidogenic enzymes, includ- ing 36-HSD (reviewed by Saez et al., 1984). In rainbow trout, ACTH may play a similar role in regulating interrenal cell ontogeny. Adrenocorticotrophs first appear in the rainbow trout pituitary at stage 28 (3 weeks after fertilization) and show mature immu- nostaining characteristics at stage 30 (Saga et al., 1993). The appearance of adrenocor- ticotrophs in the pituitary correlates very well with the onset of larval corticoste- roidogenesis, supporting the hypothesis that ACTH may be an important regulator of interrenal growth and differentiation (see Takahashi e¢ al., 1985; Chester Jones et al., 1969; Chester Jones and Mosley, 1980; Chester Jones and Phillips, 1986; Carsia and Malamed, 1989). A peak in resting cortisol levels occurred on Week 6, which corresponded to the on- set of stress responsiveness and the appear- ance of differentiated interrenal cells in the head kidney. A similar pattern in resting cortisol levels has been reported in devel- oping chum salmon (De Jesus and Hirano, 1992). In this species, whole-body cortisol levels increase during the latter stages of yolk sac absorption and then rapidly fall at the time of emergence (De Jesus and Hirano, 1992). Because chum salmon mi- grate to the sea soon after emergence, De 62 BARRY ET AL. Jesus and Hirano (1992) postulated that el- evated cortisol levels in preemergent fish may regulate the development of hypoos- moregulatory ability prior to downstream migration, Rainbow trout, however, do not migrate soon after emergence. We postu- late, therefore, that the preemergent corti- sol rise may regulate aspects of intermedi- ary metabolism and mediate the transition from a constant, endogenous energy source (yolk) to an intermittent, exogenous food supply. In birds and mammals, the activity of the HPA axis increases at hatching and parturition, respectively, suggesting that the maturation of adrenocortical function mMay be associated with the transition from ‘endogenous to exogenous feeding in all ver- tebrates, and that an efficient gluconeo- genic pathway regulated by a functional HPI or HPA axis may be required to main- tain glucose homeostasis during periods of fasting (see Terner, 1968; Arai and Wid- maier, 1991). Rainbow trout did not show a rise in cor- tisol in response to acute stress until 2 weeks after hatching. Nevertheless, during this 2-week period the interrenal cells are capable of corticosteroid biosynthesis (our data, Pillai ef al,, 1974; Hwang ef al., 1992), and immunoreactive ACTH is present in the pituitary (Saga er al., 1993). The lack of a stress response during this period, there- fore, may be due primarily to the immatu- rity of the higher brain and hypothalamic centers regulating the stress response. It is also possible that the adrenocorticotrophs and interrenal cells are not fully mature at this time. The stress hyporesponsive period after hatching in rainbow trout may be ho- mologous to the 2-week stress hyporespon- sive period after birth in rodents in which it has been shown that the stress hyporespon- sive period is due, at least in part, to the immaturity of all of the individual compo- nents of the HPA axis, including the brain, ituitary, and adrenal (Walker et al., 1986a; Arai and Widmaier, 1991; Walker et al., 1991). It has also been postulated that the stress hyporesponsive period in rats is a re- sult of the low levels of corticosteroid- binding globulin (CBG) in the plasma and pituitary at that time (reviewed by DeKloet et al., 1988). In the absence of CBG, corti- costeroid negative feedback at the brain and pituitary is greatly enhanced because. more free steroid is available to interact with receptors on these targets. The stress hyporesponsive period, therefore, may be due to the inability of most stressors to evoke a sufficiently large corticotropin- releasing hormone (CRH) signal to over- come corticosteroid negative feedback at the pituitary during this time (Sakly and Koch, 1983; Walker et al., 1986b; DeKloet et al., 1988; Walker et al., 1991). The on- togeny of cortisol-binding proteins has not been investigated in fish, although Piflai and Terner (1974) isolated and character- ized a corticosteroid-binding protein from. rainbow trout embryos with binding prop- erties similar to those of mammatian CBG. This protein was not detected in embryos 11 days old or younger, but was present in 30-day-old larvae (stages 29 and 30). Baseline and stress-induced cortisol lev- els were higher at Week 6 than at other times, suggesting that the interrenal may have heightened sensitivity to trophic stim- ulation at that stage of development. In birds and mammals, corticosteroid produc- tion increases abruptly during embryonic life as the result of a several-fold increase in the sensitivity of the adrenal cells to ACTH (Woods et al., 1971; Rose et al., 1982; Du- rand et al., 1985; Saez et al., 1984; Carsia er al., 1987; see Carsia and Malamed, 1989). Perhaps a similar change occurs in 6-week- old rainbow trout. Other possibilities are that the negative feedback system control- ling resting cortisol levels may be immature in 6-week-old fish, or the cortisol negative feedback setpoint is higher at that stage. Our observation that cortisol levels re- turned to prestress levels by 3 hr poststress in the 6-week-old larvae indicates that neg- ative feedback control of stress-induced STRESS RESPONSE IN RAINBOW TROUT 63 changes in cortisol was functional at that time. Taken together, these data suggest that two separate negative feedback sys- tems may differentially regulate resting and stress-induced cortisol levels in larval rain- bow trout. These could be similar to the two negative feedback systems that differ- entially regulate baseline and stress-in- duced glucocorticoid levels in mammals, so-called level-sensitive (or delayed) feed- back, and rate-sensitive (or fast) feedback, respectively (Keller-Wood and Dallman, 1984). A hypothesis that may explain why cor- tisol levels did not return to prestress levels within 3 hr in 7-week-old fish whereas they did in 6-, &, and 9-week-old fish is that the elevated prestress cortisol levels observed in the 6-week-old fish down-regulated cor- tisol receptors in the brain and pituitary that mediate stress-induced negative feed- back. Alternatively, elevated prestress cor- tisol levels in the 6-week-old fish may in- crease the levels of CBG and thereby di- minish the negative feedback signal. The secondary rise in cortisol between 3 and 24 hr poststress in the 9-week-old larvae may be an indication that these fish have devel- oped an adult-like stress response. Adult rainbow trout occasionally show a second- ary rise in cortisol between 3 and 24 hr post- stress after being placed into a novel recov- ery environment (our unpublished data; see Pottinger and Pickering, 1992). In mammals, environmental stimuli such as frequent handling, electric shocks, and exposure to light, sound, or abnormally high or low temperatures can produce long- lasting or permanent physiological, mor- phological, and behavioral effects on the developing neonatal brain and HPA axis (Ader et al., 1968; Ader and Grota, 1969, 1973, Ader, 1970; Doupe and Patterson, 1982; Meaney ez al., 1985; Meyer, 1985; Sa- polsky and Meaney, 1986; Sapolsky er al., 1986; DeKloet et al., 1988). Such handling generally produces animals that are highly tolerant of stressors as adults (above cited references; Pedersen and Jeppesen, 1990; Hilakivi-Clarke et al., 1991). We hypothe- size that appropriate, well-timed environ- mental or biochemical treatments could have similar effects on the developing HPI axis of teleosts, thereby producing stress- tolerant fish useful for intensive aquacul- ture for food production (see Fevolden et al., 1991; Maule et al., 1989). As suggested by DeKloet et al. (1988) for mammals, the stress hyporesponsive period may consti- tute a “window of vulnerability’” when such manipulations may be most effective in permanently changing stress responsive- ness. ACKNOWLEDGMENTS ‘We thank Idaho Fish and Game for the unfertilized eggs and sperm, Dr. George Stabenfeldt and Coralie Munro of the School of Veterinary Medicine, Univer- sity of California at Davis for the antibody and conju- gate used in our cortisol ELISA, and Thomas E. Kuc- zynski and Lynn Procarione of the University of Wis- cconsin Aquaculture Program for their assistance. This research was supported in part by the University of Wisconsin-Madison College of Agricultural and Life Sciences and School of Natural Resources; the Wis- consin Department of Natural Resources; the Univer- sity of Wisconsin Sea Grant College Program, Na- tional Oceanic and Atmospheric Administration, US Department of Commerce, and the State of Wisconsin (Federal Grant NA90AA-D-SF469, Project No. R/AQ- 21). 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