University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln
Wildlife Damage Management Conferences -- Wildlife Damage Management, Internet Center Proceedings for
2005
Development of Diazacon™ as an Avian Contraceptive
Christi Yoder USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA
Kimberly Bynum USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA
Lowell Miller USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA
Follow this and additional works at: https://digitalcommons.unl.edu/icwdm_wdmconfproc
Part of the Environmental Sciences Commons
Yoder, Christi; Bynum, Kimberly; and Miller, Lowell, "Development of Diazacon™ as an Avian Contraceptive" (2005). Wildlife Damage Management Conferences -- Proceedings. 100. https://digitalcommons.unl.edu/icwdm_wdmconfproc/100
This Article is brought to you for free and open access by the Wildlife Damage Management, Internet Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Wildlife Damage Management Conferences -- Proceedings by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln.
DEVELOPMENT OF DIAZACON™ AS AN AVIAN CONTRACEPTIVE
CHRISTI A. YODER, USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA KIMBERLY S. BYNUM, USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA LOWELL A. MILLER, USDA, APHIS, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA
Abstract: Due to increasing human-wildlife conflicts with birds and growing opposition to lethal techniques, nonlethal methods need to be developed to help manage bird populations. DiazaCon™ is a promising oral contraceptive that acts by directly inhibiting the conversion of desmosterol to cholesterol. Because cholesterol is essential for the production of the steroid reproductive hormones testosterone, progesterone, and estradiol, DiazaCon™ also indirectly inhibits the formation of these hormones. These hormones are essential for sperm and egg production, and the production of egg yolk precursors in the liver. Because DiazaCon™ is cleared slowly from the liver, its contraceptive effects are long-lasting. Initial research with Coturnix quail (Coturnix coturnix) helped determine DiazaCon’s mechanism of action. Further research showed efficacy in monk parakeets (Myiopsitta monachus) and mallards (Anas platyrhynchos). Brown-headed cowbirds (Molothrus ater), American crows (Corvus brachyrhynchos) and ring-necked doves (Streptopelia risoria) were also studied as potential candidates for DiazaCon™ contraception. Mallards and ring-necked doves were used as model species for Canada geese (Branta canadensis) and pigeons (Columba livia), respectively. DiazaCon™ application over a very short time results in long-lasting contraceptive effects, an advantage for target species, but a disadvantage for nontarget species. Care must be taken when delivering DiazaCon™ to determine what nontargets are present and how best to avoid them. Timing of delivery is also critical to ensure maximal reproductive effects, and information on the reproductive cycles of the species of interest is needed.
Key words: avian, bird, cholesterol, contraception, control, desmosterol, 20,25 diazacholesterol dihydrochloride, DiazaCon™, Ornitrol, reproduction
Proceedings of the 11th Wildlife Damage Management Conference. (D.L. Nolte, K.A. Fagerstone, Eds). 2005
INTRODUCTION al. 2003), and E. coli (Morabito et al. 2001, As human developments continue to Pennycott et al. 2002). Safety concerns grow, human-wildlife conflicts become exist at airports where birds congregate on more frequent. Health concerns exist where or near runways (Dolbeer et al. 2000, Sodhi large numbers of birds congregate and foul 2002). Birds cause agricultural damage to the area with feces. Fecal material presents grain crops (Bullard and York 1996, Avery health hazards such as histoplasmosis et al. 1998, Blackwell et al. 2003), fruits and (Stickley et al. 1987, Fischer 1995), vegetables (Tobin et al. 1991, Brugger et al. salmonella (Smith et al. 2002, Vucemilo et 1993, Cummings et al. 1998), livestock feed
190
(Mason et al. 1985, Glahn et al. 1991, Van- 1960s and early 1970s, but produced Niekerk 2003), and fish at aquaculture conflicting results. facilities (Glahn et al. 2002, Dorr et al. 2004). Breeding activities of some species HISTORICAL DIAZACON™ RESEARCH causes damage to various structures (Evans Originally, DiazaCon™ was investigated et al. 1984, Stemmerman 1988), and birds as a cholesterol-lowering agent for humans may become aggressive during breeding. (Sachs and Wolfman 1965). Human trials Birds roosting in urban areas disturb were suspended when males receiving the neighbors with noise. Because there is compound complained of an “uncomfortable growing opposition to lethal control feeling”. Research was then conducted to methods, particularly in urban areas, determine if DiazaCon™ could lower the acceptable nonlethal methods must be cholesterol content in egg yolks of eggs to developed to help in the management of be consumed by humans (Singh et al. 1972, overpopulated bird species. Contraception Dam et al. 1979, Cecil et al. 1981). is one generally acceptable nonlethal Next, DiazaCon™ was considered as a method that can be used in conjunction with potential contraceptive for feral pigeons, and other control methods (Messmer et al. 1997, was registered for such use under the trade Stout et al. 1997). name Ornitrol (Schortemeyer and Beckwith There are several characteristics that are 1970, Sturtevant and Wentworth 1970). desirable in any wildlife contraceptive agent. Research continued on species such as red- It should last for an entire breeding season winged blackbirds (Agelauis phoeniceus) and require a minimal number of days of (Lacombe et al. 1986, 1987), house treatment. Ideally, it should be reversible so sparrows (Passer domesticus) (Sanders and as not to permanently remove individuals Elder 1976, Mitchell et al. 1979), grackles from the gene pool. Oral administration is (Quiscalus quiscula) (Fringer and Granett desirable to eliminate the cost and handling 1970), Japanese quail (Powell 1966), and stress associated with capture of animals. parakeets (probably Melopsittacus Contraceptives should be safe for the undulates) (Powell 1966). These studies environment and have a minimal impact on sometimes presented conflicting results, nontarget species. Finally, contraceptives with one showing efficacy and another should be relatively inexpensive. showing little effect on the same species. A number of contraceptives have been Limited conclusions could be drawn from tested in birds, but several produced these studies because very little unacceptable results. Surgical sterilization physiological work was conducted to was used for Canada geese, but this method determine how the compound worked. The requires that geese be captured and National Wildlife Research Center (NWRC) anesthetized, and is prohibitively expensive in Fort Collins, Colorado initiated research (Converse and Kennelly 1994). Mestranol in 1997 with Coturnix quail to determine (Wentworth et al. 1968, Sturtevant 1970), α- DiazaCon’s mode of action (Yoder et al. chlorohydrin (Aire and Olusanya 1980), and 2004). triethylenemelamine (Messersmith 1971, Bhat and Maiti 1989) could permanently COTURNIX QUAIL STUDY sterilize adults and young being fed crop Coturnix quail were used as an avian milk. Research on DiazaCon™ (20,25 model species because their reproductive diazacholesterol dihydrochloride) as an cycles are easily manipulated in the avian contraceptive first occurred in the late laboratory and they have a high reproductive rate. Quail received an average of 100
191
mg/kg DiazaCon™ in feed per bird per day Desmosterol levels in treated birds rose to for 12-14 days. Testosterone, progesterone, approximately 280 µg/mL compared to 30 cholesterol, desmosterol, egg production, µg/mL in control birds. Egg production was fertility, and hatchability were monitored. decreased by 85%, fertility of laid eggs by Initially, an enzymatic test was used to 70%, and hatchability by 100%. Egg monitor cholesterol concentrations, but this production, fertility, and hatchability test was not specific enough to distinguish remained suppressed for ≥ 3 months, and between cholesterol and desmosterol. A were correlated with a 42% decrease in high performance liquid chromatography progesterone concentrations. (HPLC) method was developed to more accurately monitor cholesterol and MECHANISM OF ACTION desmosterol concentrations (Johnston et al. DiazaCon™ is structurally similar to 2001). cholesterol (Figure 1), and may The HPLC results showed a 40% competitively inhibit enzymes in the decrease in cholesterol concentrations in cholesterol biosynthesis pathway (Dietert male treated birds. Desmosterol and Scallen 1969, Counsell et al. 1971, concentrations in treated birds rose to Emmons et al. 1982). Because DiazaCon™ approximately 230 µg/mL compared to 7 mimics cholesterol, it can competitively µg/mL in control birds. Treated males were bind to enzyme substrates, with nitrogen paired with untreated females to determine substitutions in the 20 and 25 positions fertility. Fertility decreased by 41% and interfering with enzyme action. hatchability by 35%, and both remained Desmosterol is converted to cholesterol by suppressed for ≥ 3 months. Decreased the Δ24 reductase enzyme. The quail study fertility and hatchability were correlated concluded that DiazaCon™ acted to inhibit with a 37% decrease in testosterone Δ24 reductase activity (Figure 2), which concentrations. decreased cholesterol and increased Treated female quail experienced a 52% desmosterol concentrations. decrease in cholesterol concentrations.
CH CH 3 2 CH CH 2 CH 3 CH 3 CH CH CH 3 2 CH 3
HO Cholesterol
CH CH 3 2 N CH CH 3 2 CH3 CH N . 2HCL CH 3 2 CH 3
HO 20,25 Diazacholesterol dihydrochloride (DiazaCon™)
Figure 1. The chemical structure of cholesterol and DiazaCon™ (20,25 diazacholesterol dihydrochloride).
192
24 reductase OH OH DESMOSTEROL CHOLESTEROL (24-dehydroxycholesterol) Prevents conversion of desmosterol to cholesterol
DiazaCon™
Figure 2. Inhibition of the conversion of desmosterol into cholesterol by DiazaCon™.
Reductions in cholesterol concentration oviposition. Estradiol stimulates the cause reductions in steroid reproductive production of egg yolk precursors, such as hormone concentrations, which in turn vitellogenin and very low density decreases sperm and egg production. The lipoprotein, in the liver, and is also needed side chain of cholesterol is cleaved to form in some songbirds for singing behavior. the steroid hormone pregnenolone, the Although not investigated in the quail study, precursor to the steroid reproductive DiazaCon™ may also inhibit the P450 side hormones testosterone, progesterone, and chain cleavage enzyme responsible for estradiol (Figure 3). Testosterone is needed cleaving cholesterol’s side chain to form for sperm formation and breeding behavior. pregnenolone (Figure 4). Progesterone plays a role in ovulation and
CH3
P450 scc C O enzyme OH CHOLESTEROL OH PREGNENOLONE
CH3
C O OH OH
O O OH PROGESTERONE TESTOSTERONE ESTRADIOL
Figure 3. Synthesis of steroid reproductive hormones from cholesterol.
193
CH3
C O
P450 scc enzyme
OH OH
CHOLESTEROL PREGNENOLONE
Prevents conversion of cholesterol to pregnenolone
DiazaCon™
Figure 4. Inhibition of conversion of cholesterol into pregnenolone by DiazaCon™.
Radiolabel studies in pigeons show Because Diaza-Con™ appeared to have DiazaCon™ has a half-life of 28 days potential as an avian contraceptive, a study (Ranney 1968). Approximately half of on ring-necked doves was conducted during orally administered DiazaCon™ is cleared 2002 at NWRC (Yoder et al. unpublished in the feces within 24 hours. The remainder data). Doves were used as a model for is primarily stored in the liver and cleared pigeons because they required less space to slowly over time. Steroids are not water house. DiazaCon™ was coated onto a soluble, and therefore must first be mixture of hulled seeds (millet, thistle, conjugated in the liver to make them water sunflower seed hearts, peanut hearts) at rates soluble, allowing them to be cleared by of 0.03% (w/w), 0.05%, and 0.1%, and fed kidney excretion. This conjugation occurs ad libitum for 14 days. Based on predominately at the D ring of the steroid consumption data, doves received an structure. DiazaCon™ is no longer water average dose of 14.0, 25.7, and 52.5 mg/kg soluble once it enters the body, and is stored per bird per day in the 0.03%, 0.05%, and in fat like steroids. Because DiazaCon™ 0.1% groups, respectively. has nitrogen molecules present near the D Cholesterol concentrations decreased by ring, the liver cannot conjugate it 48%, 43%, and 46% in the 0.03%, 0.05%, effectively. The primary means of excretion and 0.1% groups, respectively. Desmosterol from the body is most likely via leakage of concentrations increased to 3800-5500 lipid soluble DiazaCon™ into the blood µg/mL in treated doves compared to 20 stream. This accounts for DiazaCon’s long- µg/mL in control doves. By 15 weeks post- lasting reproductive effects. treatment, the changes observed in desmosterol and cholesterol concentrations ADDITIONAL SPECIES STUDIED TO had diminished so that no difference was DATE observed between treated and control groups. No effect on reproduction was Ring-necked Doves observed during the treatment period. A
194
complete cessation of egg laying was study to identify the target dose for further observed during the treatment period in the studies was conducted using 50, 75, and 100 control group and 2 treatment groups. This mg/kg doses of DiazaCon™. Cholesterol was likely due to 2 factors. Doves have very concentrations decreased by 81%, 85%, and high inherent cholesterol concentrations. 86% in the 50, 75, and 100 mg/kg groups, Even though cholesterol was significantly respectively. Desmosterol concentrations reduced in the treatment groups, it was not increased to 600-760 µg/mL in treated birds sufficient to affect reproduction. compared to 5 µg/mL in control birds. Additionally, dove reproductive hormone Cholesterol concentrations were suppressed concentrations are strongly regulated by for ≥ 12 weeks. The target dose was visual cues (O’Connell et al. 1981, Cheng determined to be 50 mg/kg. Next, another 1986). Any decrease in breeding behaviors oral gavage study investigated differences in in the treatment groups also likely caused a cholesterol and desmosterol concentrations decrease in breeding behaviors in the control based on the number of days of treatment by group also because all birds were housed in comparing 5 and 10 days of treatment. the same room. Cholesterol concentrations decreased by 67% in both treatment groups. Desmosterol Brown-headed Cowbirds concentrations increased to 850-950 µg/mL A laboratory study on brown-headed in treated birds compared to 4 µg/mL in cowbirds was conducted in 2003 at NWRC control birds. Cholesterol concentrations (Bynum et al. unpublisheded data). were suppressed for ≥ 10 weeks. This study DiazaCon™ was coated onto a mixture of showed 5-7 days of treatment were adequate hulled seeds (millet, thistle, sunflower seed to reduce cholesterol concentrations. Ad hearts, peanut hearts) at rates of 0.0078% libitum studies proved captive pairs of monk (w/w), 0.0156%, and 0.03125%. Treated parakeets would eat adequate amounts of seed was fed ad libitum for 14 days. The DiazaCon™ coated sunflower seeds over 5 actual doses received were 8.5, 18.7, and days to prevent successful reproduction. 52.2 mg/kg per bird per day in the 0.0078%, Birds in the ad libitum study ingested an 0.0156%, and 0.03125% groups average dose of 33.7 mg/kg per bird per day. respectively. Although reproduction could Egg production was decreased in treated not be monitored in the laboratory setting, birds by 59% over a 2 month period, and no cholesterol and desmosterol concentrations eggs hatched in the treatment group. Monk were measured. Cholesterol concentrations parakeets are ideal candidates for field decreased by 85%, 86%, and 81% in the application of contraceptive techniques 0.0078%, 0.0156%, and 0.03125% groups because of their low dispersal rates, and respectively. Desmosterol concentrations their willingness to take sunflower bait from increased to 245-380 µg/mL in treated birds feeding stations. compared to 50 µg/mL in the control birds. Cholesterol concentrations remained American Crows suppressed for ≥ 1 month. Two studies on American crows were conducted during 2003 at NWRC (Yoder et Monk Parakeets al. unpublished data). Crows were gavaged Several laboratory studies using monk with 50, 75, or 100 mg/kg DiazaCon™ per parakeets were conducted in 2003 and 2004 bird per day for 14 days. Cholesterol at NWRC’s Florida field station (Yoder et concentrations decreased by 46%, 47%, and al. unpublished data). An initial gavage 52% in the 50, 75, and 100 mg/kg groups
195
respectively. Desmosterol concentrations per bird per day for the 6 consecutive day increased to 170-200 µg/mL in treated group and 63.8 mg/kg per bird per day for crows compared to 70 µg/mL in control the 5 dose group. Cholesterol crows. Cholesterol concentrations were concentrations decreased by 72% in the suppressed for ≥ 1 month. Based on the group receiving 5 doses over 10 days, and results, crows were fed scrambled eggs by 74% in the group receiving 6 consecutive treated with DiazaCon™ at a target dose of doses. Desmosterol concen-trations 50 mg/kg per bird per day for 14 days. increased to approximately 285 µg/mL in Crows received an average dose of 43.0 treated birds compared to 1 µg/mL in mg/kg per bird per day, and cholesterol control birds. Egg production was decreased by 47%. Desmosterol decreased by 97%, and hatchability by concentrations increased to 140 µg/mL in 100% in the group receiving 5 doses over 10 treated crows compared to 6 µg/mL in days. In the group receiving 6 consecutive control crows. Cholesterol and desmosterol doses, egg production was decreased by concentrations were recovered by 5 weeks 94% and hatchability by 100%. Cholesterol post-treatment. concentrations remained suppressed for ≥ 10 In 2005, a preliminary field study in weeks. This study proved it isn’t necessary California was conducted to assess various for birds to consume DiazaCon™ bait daily capture and monitoring techniques, and bait for efficacy. attractiveness (Gionfriddo et al. unpublished data). This study showed the difficulty in ADVANTAGES OF DIAZACON™ monitoring crow reproduction. Because The short application period of nests are relatively inaccessible, close DiazaCon™ is advantageous from an monitoring of nests would be difficult and operational standpoint. Research showed expensive, making an accurate assessment DiazaCon™ may be applied for as few as 5 of DiazaCon™ efficacy difficult. The bait days with efficacy. In addition, DiazaCon™ tested was not attractive to crows, and none need not be consumed on a daily basis to was consumed. It would be impossible to affect reproduction. Several doses over a target only resident crows in areas where period of time are as effective as the same winter roosts occur due to the large number number of doses on consecutive days. This of migrants. Contraception alone would be is important because birds may not visit a ineffective in reducing wintering roost sizes bait site on a daily basis. because crows disperse during breeding. It A single DiazaCon™ dose will not is unknown how large an area wintering produce reproductive effects. Absorption of crows disperse over during the breeding DiazaCon may be controlled through a season. receptor-mediated mechanism. Once the receptors are full, the rest of the DiazaCon™ Mallards passes through the gut and is excreted in the A free feeding study using mallards as a feces. Recycling of receptors is necessary to model species for Canada geese was allow more DiazaCon™ to be absorbed in conducted during 2004 at NWRC (Yoder et subsequent doses. An acute dose is likely al. unpublished data). Mallards were fed cleared from the system without much being DiazaCon™ treated waterfowl pellets (0.1% stored in the liver. Chronic dosing allows a DiazaCon™ w/w) ad libitum for either 6 level of DiazaCon™ to build up in the liver consecutive days or on 5 days over a 10 day Another advantage of DiazaCon™ is the period. The doses received were 67.6 mg/kg length of time the reproductive effects last.
196
Prior research showed DiazaCon™ effects reproductive effects (Woulfe 1967), but last ≥ 3 months in some species, enough several repeated doses have reproductive time to preclude renesting within a breeding consequences. It is critical to know what season. This allows flexibility in baiting species are in the baiting area in order to programs. Bait can be applied, for example, develop appropriate baits and better plan prior to the greening up of grass for Canada baiting operations. DiazaCon affects geese. Geese are more likely to eat bait at mammals as well as birds, so they must be this stage because they do not have other considered when determining what highly desirable food sources readily nontarget hazards are present. Some available to them. Birds not easily hazards to songbirds can be mitigated by accessible once they begin breeding can be using bait that is too large for smaller birds treated prior to breeding. This eliminates to consume. Selective placement of bait the need to search out nests for egg oiling could further eliminate hazards. For and addling programs. example, placing bait off the ground could DiazaCon™ affects both male and eliminate hazards to domestic dogs. Work female reproduction, which presents an on secondary hazards has yet to be advantage over a contraceptive that would conducted. However, a predator eating a affect only one sex. In situations where only single treated bird is unlikely to be affected males are treated, extra-pair copulations by because chronic dosing is required for untreated males still result in successful contraception (Woulfe 1967). reproduction by females. However, if both Bait development is important to males and females are treated, extra-pair increase palatability of DiazaCon™. copulations are not an issue. In situations Previous studies have coated DiazaCon™ where it is desirable to only treat one sex, onto the bait preferred by the target species. DiazaCon™ could be selectively applied Because DiazaCon™ is bitter, use of provided you had access to the desired sex. masking agents or encapsulation is needed For example, males arriving on territories to increase consumption. Allowing earlier than females could be treated DiazaCon™ to be coated onto bait, such as selectively. Conversely, if females tend to whole corn or seeds, is an advantage congregate in large flocks prior to breeding, because bait will be readily recognizable as they could be treated selectively, allowing food by target species. Another method is to males to maintain breeding territories. incorporate DiazaCon™ into extruded bait. The effects of DiazaCon™ are While this would increase palatability, it reversible, which is a highly desirable trait would likely require more prebaiting to in a wildlife contraceptive because the acclimate birds to a new food source. treated animals can be returned to the gene Toxicity was noted in DiazaCon™ pool the following season. If a nontarget treated pigeons (Elder 1964, Sturtevant and species were to eat enough DiazaCon™ bait Wentworth 1970), quail (Powell 1966, to prevent reproduction, that animal would Yoder et al. 2004), cowbirds (Bynum, not be permanently sterilized. NWRC, personal communication), and monk parakeets (Avery, NWRC, personal DISADVANTAGES OF DIAZACON™ communicagtion.). These effects include Although the long-lasting reproductive listlessness, weight loss, difficulty breathing, effect of DiazaCon is an advantage for target loss of muscle control, and death. However, species, it is a disadvantage for nontarget studies on red-winged blackbirds (Lacombe species. A single acute dose has no et al. 1986), house sparrows (Mitchell et al.
197
1979), crows, and mallards did not show any limit the length of treatment. Continuous toxic effects. use of DiazaCon™ throughout the year It is critical that dose response studies be could potentially cause other health effects performed in the laboratory on the species of during non-breeding. Because DiazaCon™ interest prior to field application of has only suppressed cholesterol for 3-4 DiazaCon™. Absorption of DiazaCon™ months in most species studied, it is ideal will differ among species, with some being for use during a single breeding season. more sensitive to DiazaCon™ than others. Contraception is a tool best used as a Although reproduction of many wild species proactive measure, or in conjunction with cannot be monitored in the laboratory, other control techniques. Because cholesterol and desmosterol concentrations population effects would not be noticeable can be used as markers of efficacy (Johnston for several years, it is desirable to first et al. 2003, Yoder et al. 2004). This allows reduce the population to an acceptable a safety range to be identified so that a target concentration, and then maintain the dose can be chosen to maximize population with contraception. If problems contraceptive effects while minimizing the are widespread over a large area, logistical risk of toxicity. problems exist. Cooperation over much of the area is needed in order to be successful. MANAGEMENT IMPLICATIONS Field studies will be conducted in the future It is important to consider the breeding with the goal of registering DiazaCon™ as biology of the species of interest to an avian contraceptive. Other species to be effectively administer DiazaCon™. considered as candidates for DiazaCon™ Increasing day lengths cause an increase in include gulls and ring-necked parakeets. testicular size. Once the testes are DiazaCon™ is a promising contraceptive reproductively mature, it takes 2-5 days for that can be added to the tools already used to maturation of a germ cell into a sperm cell manage problem avian populations. capable of fertilization. DiazaCon™ should be given to males ≥ 3 weeks before the first LITERATURE CITED copulation to prevent sperm maturation. AIRE, T.A., AND S.K. OLUSANYA. 1980. The A similar increase in ovarian size occurs response of the male domestic fowl in females in response to increased day (Gallus domesticus) to α-chlorohydrin lengths. As day length increases, there is a treatment. International Journal of slow, gradual deposition of yolk in the Andrology 3:188-192. AVERY, M.L., J.S. HUMPHREY, T.M. PRIMUS, follicle. A rapid follicular growth occurs 6- D.G. DECKER, AND A.P. MCGRANE. 11 days prior to ovulation. It takes 1998. Anthraquinone protects rice seed approximately 24 hours for an ovulated egg from birds. Crop Protection 17:225- to traverse the reproductive tract and be laid. 230. DiazaCon™ should be applied to females ≥ BHAT, G., AND B.R. MAITI. 1989. Antifertility 2 weeks prior to laying the first egg to effect of TEM (triethylenemelamine) in prevent ovulation. In order to prevent a female avian pest, the yellow-throated follicular maturation, DiazaCon™ should be sparrow (Petronia xanthocollis). applied ≥ 1 month prior to the onset of egg Archives de Biologie 100:257-262. laying. BLACKWELL, B.F., E. HUSZAR, G.M. LINZ, AND DiazaCon™ is not an appropriate tool R.A. DOLBEER. 2003. Lethal control of red-winged blackbirds to manage for non-seasonal breeders. Because of its damage to sunflower: An economic cholesterol lowering effects, it is essential to
198
evaluation. Journal of Wildlife DORR, B., D.T. KING, M.E. TOBIN, J.B. HARREL, Management 67:818-828. AND P.L. SMITH. 2004. Double-crested BRUGGER, K.E., P. NOL, AND C.I. PHILLIPS. cormorant movements in relation to 1993. Sucrose repellency to European aquaculture in eastern Mississippi and starlings: Will high-sucrose cultivars western Alabama. Waterbirds 27:147- deter bird damage to fruit? Ecological 154. Applications 3:256-261. ELDER, W.H. 1964. Chemical inhibitors of BULLARD, R.W., AND J.O. YORK. 1996. ovulation in the pigeon. Journal of Screening grain sorghums for bird Wildlife Management 28:556-575. tolerance and nutritional quality. Crop EMMONS, G.T., E.R. ROSENBLUM, J.N. PEACE, Protection 15:159-165. J.M. MALLOY, D.L. DOERFLER, I.R. CECIL, H.C., J. BITMAN, J.A. SVOBODA, AND MCMANUS, AND I.M. CAMPBELL. M.J. THOMPSON. 1981. Effects of 1982. Effects of 2025 diazacholesterol branched and straight chain amines and on cholesterol synthesis in cultured azasteroids on blood and egg cholesterol chick muscle cells: A radiogas of white leghorn chickens. Poultry chromatographic and mass Science 60:795-804. spectrometric study of the post-squalene CHENG, M.F. 1986. Female cooing promotes sector. Biomedical Mass Spectrometry ovarian development in ring doves. 9:278-285. Physiology and Behavior 37:371-374. EVANS, D., J.L. BYFORD, AND R.H. WAINBERG. CONVERSE, K.A., AND J.J. KENNELLY. 1994. 1984. A characterization of woodpecker Evaluation of Canada goose sterilization damage to houses in east Tennessee. for population control. Wildlife Society Proceedings of the Eastern Wildlife Bulletin 22:265-269. Damage Control Conference 1:325-330. COUNSELL, R.E., M.C. LU, S.E. MASRY, AND FISCHER, J.R. 1995. Human health concerns in P.A. WEINHOLD. 1971. Inhibition of the practice of wildlife damage cholesterol side-chain cleavage by management. Great Plains Agricultural azacholesterols. Biochemical Council Publication 153:21-26. Pharmacology 20:2912-2915. FRINGER, R.C., AND P. GRANETT. 1970. The CUMMINGS, J.L., P.A. POCHOP, C.A. YODER, effects of Ornitrol on wild populations AND J.E. DAVIS, JR. 1998. Potential of red-winged blackbirds and grackles. bird repellents to reduce bird damage to Proceedings of the Bird Control Seminar lettuce seed and seedlings. Proceedings 5:163-176. of the Vertebrate Pest Conference _____, A.R. STICKLEY, JR., J.F. HEISTERBERG, 18:350-353. AND D.F. MOTT. 1991. Impact of roost DAM, R., M.E. LABATE, S.W. TAM, AND C. control on local urban and agricultural CUERVO-TORRES. 1979. Effects of blackbird problems. Wildlife Society diazacholesterol, triparanol, and Β- Bulletin 19:511-522. sitosterol on egg cholesterol deposition GLAHN, J.F., B. DORR, J.J.B. HARREL, AND L. in Coturnix quail. Poultry Science KHOO. 2002. Foraging ecology and 58:985-987. depredation management of great blue DIETERT, S.E., AND T.J. SCALLEN. 1969. An herons at Mississippi catfish farms. ultrastructural and biochemical study of Journal of Wildlife Management the effects of three inhibitors of 66:194-201. cholesterol biosynthesis upon murine JOHNSTON, J.J., M.J. GOODALL, J.C. HURLEY, adrenal gland and testis. Journal of Cell C.A. YODER, AND L.A. MILLER. 2001. Biology 40:44-60. Ion pair reversed phase liquid DOLBEER, R.A., S.E. WRIGHT, AND E.C. chromatographic method for the CLEARY. 2000. Ranking the hazard quantification of DiazaCon in quail feed level of wildlife species to aviation. and quail serum. Journal of AOAC Wildlife Society Bulletin 28:372-378. International 84:634-639.
199
_____, _____, C.A. YODER, C.A. FURCOLOW, Comparative Endocrinology 44:454- D.A. GOLDADE, B.A. KIMBALL, AND 463. L.A. MILLER. 2003. Desmosterol: A PENNYCOTT, T.W., R.N. CINDEREY, A. PARK, biomarker for the efficient development H.A. MATHER, AND G. FOSTER. 2002. of 20,25-diazacholesterol as a Salmonella enterica subspecies enterica contraceptive for pest wildlife. Journal serotype typhimuruim and Escherichia of Agricultural and Food Chemistry coli 086 in wild birds at two garden sites 51:140-145. in southwest Scotland. Veterinary LACOMBE, D., A. CYR, AND J.M. BERGERON. Record 151:563-567. 1986. Effects of the chemosterilant POWELL, J.E. 1966. The effects of 20,25 ornitrol on the nesting success of red- diazacholesterol dihydrochloride (SC- winged blackbirds. Journal of Applied 12937) on the fecundity of the Japanese Ecology 23:773-779. quail and parakeets. MS Thesis, _____, AND _____. 1987. Effect of Ornitrol on University of Massachusetts, Amherst, spermatogenesis in red-winged MA, USA. blackbirds. Journal of Wildlife RANNEY, R.E. 1968. Azacosterol Management 51:596-601. hydrochloride: VI. Metabolic studies. MASON, J.R., J.F. GLAHN, R.A. DOLBEER, AND Internal research report. G. D. Searle R.F. REIDINGER, JR. 1985. Field and Company, Division of Biological evaluation of dimethyl anthranilate as a Research, Department of Metabolism. bird repellent livestock feed additive. SACHS, B.A., AND L. WOLFMAN. 1965. 20,25 Journal of Wildlife Management diazacholesterol dihydrochloride. 49:636-642. Archives of Internal Medicine 116:366- MESSERSMITH, D.H. 1971. Potential control for 372. red-winged blackbirds. Pest Control SANDERS, C.W., AND W.H. ELDER. 1976. Oral 39:35-41. chemosterilization of the house sparrow. MESSMER, T.A., L. CORNICELLI, D.J. DECKER, International Pest Control 18:4-8. AND D.G. HEWITT. 1997. Stakeholder SCHORTEMEYER, J.L., AND S.L. BECKWITH. acceptance of urban deer management 1970. Chemical control of pigeon techniques. Wildlife Society Bulletin reproduction. Transactions of the North 25:360-366. American Wildlife and Natural MITCHELL, C.J., R.O. HAYES, AND T.B. Resources Conference 35:47-55. HUGHES, JR. 1979. Effects of the SINGH, R.A., J.F. WEISS, AND E.C. NABER. chemosterilant ornitrol on house 1972. Effect of azasterols on sterol sparrow reproduction. American metabolism in the laying hen. Poultry Midland Naturalist 101:443-446. Science 51:449-457. MORABITO, S., G. DELL’OMO, U. AGRIMI, H. SMITH, W.A., J.A. K. MAZET, AND D.C. HIRSH. SCHMIDT, H. KARCH, T. CHEASTY, AND 2002. Salmonella in California wildlife A. CAPRIOLI. 2001. Detection and species: Prevalence in rehabilitation characterization of Shiga toxin- centers and characterization of isolates. producing Escherichia coli in feral Wildlife Medicine 33:228-235. pigeons. Veterinary Microbiology SODHI, N.S. 2002. Competition in the air: 82:275-283. birds versus aircraft. Auk 119:587-595. O’CONNELL, M.E., C. REBOULLEAU, H.H. STEMMERMAN, L.A. 1988. Observation of FEDER, AND R. SILVER. 1981. Social woodpecker damage to electrical interactions and androgen levels in distribution line poles in Missouri. birds. I. Female characteristics Proceedings of the Vertebrate Pest associated with increased plasma Conference 13:260-265. androgen levels in the male ring dove STICKLEY, A.R., JR., J.R. PRUITT, C.E. HUME, T. (Streptopelia risoria). General and PASS II, AND C.H. GAYLE. 1987. Decontamination of a Histoplasma
200
capsulatum-infested blackbird roost: Africa. South African Journal of Use of a sprinkler system to apply Wildlife Research 33:138-141. formalin. Proceeding of the Eastern VUCEMILO, M., V.K. VLAHOVIC, A. DOVC, J. Wildlife Damage Control Conference MUZINIC, M. PAVLAK, J. JERCIC, AND Z. 3:171-176. ZUPANCIC. 2003. Prevalence of STOUT, R.J., B.A. KNUTH, AND P.D. CURTIS. Campylobacter jejuni, Salmonella 1997. Preferences of suburban typhimurium, and avian Paramyxovirus landowners for deer management type 1 (PMV-1) in pigeons from techniques: A step towards better different regions in Croatia. Zeitschrift communication. Wildlife Society fur Jagdwissenschaft 49:303-313. Bulletin 25:348-359. WENTWORTH, B.C., B. HENDRICKS, AND J. STURTEVANT, J. 1970. Pigeon control by STURTEVANT. 1968. Sterility induced chemosterilization: Population model in Japanese quail by spray treatment of from laboratory results. Science eggs with mestranol. Journal of 170:322-324. Wildlife Management 32:879-887. _____, AND B.C. WENTWORTH. 1970. Effect WOULFE, M.R. 1967. SC-12937: A resume. on acceptability and fecundity to Research report. G. D. Searle, Skokie, pigeons of coating SC 12937 bait with IL, USA. Zein or Ethocel. Journal of Wildlife YODER, C.A., W.F. ANDELT, L.A. MILLER, J.J. Management 34:776-782. JOHNSTON, AND M.J. GOODALL. 2004. TOBIN, M.E., R.A. DOLBEER, C.M. WEBSTER, Effectiveness of twenty, twenty-five AND T.W. SEAMANS. 1991. Cultivar diazacholesterol, avian gonadotropin- differences in bird damage to cherries. releasing hormone, and chicken Wildlife Society Bulletin 19:190-194. riboflavin carrier protein for inhibiting VAN-NIEKERK, J.H. 2003. Grain selection and reproduction in Coturnix quail. Poultry flocking of rock pigeons at a cattle Science 83:234-244. feedlot in Gauteng province, South
201