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(Sciurus Carolinensis) with the Contraceptive Agent Diazacontm

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(Sciurus Carolinensis) with the Contraceptive Agent Diazacontm Integrative Zoology 2011; 6: 409-419 doi: 10.1111/j.1749-4877.2011.00247.x 1 1 2 2 3 Feeding of grey squirrels (Sciurus carolinensis) with the contraceptive 3 4 4 5 agent DiazaConTM: effect on cholesterol, hematology, and blood 5 6 6 7 chemistry 7 8 8 9 9 10 10 1 2 1 3 11 Christi A. YODER, Brenda A. MAYLE, Carol A. FURCOLOW, David P. COWAN and 11 12 Kathleen A. FAGERSTONE1 12 13 13 1 2 14 National Wildlife Research Center, Fort Collins, Colorado, USA, Forest Research, Alice Holt Lodge, Farnham, Surrey, UK and 14 15 3Central Science Laboratory, Sand Hutton, York, UK 15 16 16 17 17 18 18 19 Abstract 19 20 Grey squirrels (Sciurus carolinensis) are an invasive species in Britain and Italy. They have replaced native 20 21 red squirrels (Sciurus vulgaris) throughout most of Britain, and cause damage to trees. Currently, lethal con- 21 22 trol is used to manage grey squirrel populations in Britain, but nonlethal methods might be more acceptable to 22 23 the public. One such method is contraception with 20,25-diazacholesterol dihydrochloride (DiazaConTM). Di- 23 24 azaConTM inhibits the conversion of desmosterol to cholesterol, resulting in increasing desmosterol concentra- 24 25 tions and decreasing cholesterol concentrations. Because cholesterol is needed for the synthesis of steroid repro- 25 26 ductive hormones, such as progesterone and testosterone, inhibition of cholesterol synthesis indirectly inhibits 26 27 reproduction. Desmosterol is used as a marker of efficacy in laboratory studies with species that do not repro- 27 28 duce readily in captivity. Grey squirrels were gavaged with a DiazaConTM solution for 2 days, and then fed Di- 28 29 azaConTM-coated peanuts for an additional 8 days at target doses of 50 and 100 mg DiazaConTM per kg body 29 30 weight. There was a significant difference in cholesterol concentrations in the treatment groups compared to the 30 31 control group. Cholesterol was reduced by ≥40% for 2 months in both treatment groups. There were no differ- 31 32 ences among groups with respect to blood chemistry and hematology parameters, and mean values are reported. 32 33 The mean overall dose of DiazaConTM received was 29.0 ± 1.6 and 55.3 ± 4.3 mg/kg in the low (50 mg/kg) and 33 34 high dose (100 mg/kg) groups, respectively. DiazaConTM might provide an effective, acceptable alternative to 34 35 lethal control. 35 36 36 TM 37 Key words: 20,25-diazacholesterol dihydrochloride, cholesterol, contraception, DiazaCon , grey squirrel. 37 38 38 39 39 40 40 41 INTRODUCTION late 1800s (Middleton 1932) and to northern Italy dur- 41 42 ing the mid- to late-1900s. Grey squirrels compete with 42 The grey squirrel (Sciurus carolinensis) was intro- 43 native red squirrels (Sciurus vulgaris) and have replaced 43 duced to Britain and Ireland from North America in the 44 them throughout much of Britain and Ireland (Lloyd 44 45 1983; Gurnell 1987; Gurnell & Pepper 1993, O’Teangana 45 46 et al. 2000). Without effective control, they will poten- 46 47 tially do the same in Italy (Currado 1998; Bertolino et 47 48 al. 2008). 48 Correspondence: Christi A. Yoder, 212 Pike’s Peak 49 Grey squirrels evolved in the mixed oak forest of 49 Place, Longmont, CO 80504, USA. 50 North America and are physiologically more adapted to 50 51 Email: [email protected] neutralizing phytotoxins in acorns, allowing them to use 51 © 2011 ISZS, Blackwell Publishing and IOZ/CAS 409 C.A. Yoder et al. 1 these more efficiently (Kenward & Holm 1989, 1993). The objectives of the present study were to determine 2 In areas where both species are present, grey squirrels the minimum dose of DiazaConTM in grey squirrels that 3 raid red squirrel caches of seed, leading to reduced re- would sufficiently reduce plasma cholesterol with no 4 productive and juvenile recruitment rates for red squir- adverse health effects. Body weight, complete blood 5 rels (Wauters et al. 2002; Gurnell et al. 2004). Grey counts and blood chemistry were used to monitor gen- 6 squirrels also carry Squirrelpox virus, which is lethal to eral health. We also wanted to establish baseline data 7 red squirrels but has little effect on grey squirrels (Rush- on hematology and blood chemistry of grey squirrels as 8 ton et al. 2000; Sainsbury et al. 2000; Tompkins et al. 2002; very little information exists in the published literature. 9 Thomas et al. 2003; McInnes et al. 2006). Grey squir- 10 rels also cause bark stripping damage to trees (Kenward MATERIALS AND METHODS 11 1983; Rowe & Gill 1985; Dagnall et al. 1998), and this 12 can have serious economic impacts as well as influence The study protocol was reviewed and approved by 13 the National Wildlife Research Center’s Animal Care woodland composition (Mayle et al. 2009). TM 14 and Use Committee. DiazaCon was provided by the Despite their impact on red squirrel populations, 15 Avitrol Corporation (Tulsa, OK). Grey squirrels (48) grey squirrels are well liked by the public where there 16 were imported from Oklahoma. Squirrels were individ- 17 are no red squirrels. This might be because grey squir- ually housed indoors in cages equipped with a 45 cm 18 rels are often the only wild mammal seen by the pub- length of PVC pipe capped on one end for use as a nest 19 lic. Although lethal control methods are currently used, cavity. The light cycle throughout the study was 14 h 20 the public is more amenable to nonlethal control mea- of daylight and 10 h of darkness. Squirrels were main- 21 sures, such as live-trapping and contraception (Barr et tained on a maintenance diet of nuts (peanuts, almonds, 22 al. 2002). Translocation is not an option in Britain be- pecans and hazelnuts), cracked corn and fruit through- 23 cause, as an introduced species, grey squirrels may not out the study, except where otherwise noted, with water 24 be released once caught. Contraception offers a poten- freely available. 25 tial nonlethal option for reducing the rate of spread of Squirrels were ranked by weight and randomly as- 26 the grey squirrel, limiting the risk of Squirrelpox virus signed to treatment groups such that each treatment 27 disease transmission and reducing tree damage. group consisted of 16 animals. Each squirrel was fitted 28 Immunocontraception based upon a sperm-antigen with a fingerling ear tag with a unique identifying code. 29 approach has been investigated for the grey squirrel There were 3 treatment groups as follows: (1) control; 30 (Moore et al. 1997), but an effective single dose agent (2) 50 mg DiazaConTM per kg body weight; and (3) 100 31 with a long-term effect through oral delivery is not yet mg DiazaConTM per kg body weight. Squirrels were han- 32 available. Potential oral contraceptives with a short-term dled for all procedures by placing them in DecapiCones 33 effect exist, but have not been tested on squirrels. One (Braintree Scientific). 34 such contraceptive is 20,25-diazacholesterol dihydro- DiazaConTM gavage solutions were prepared such 35 chloride (DiazaConTM). that they contained either 50 mg DiazaConTM or 100 36 TM TM DiazaCon inhibits the conversion of desmoster- mg DiazaCon per 1 mL of water. Squirrels were then 37 ol to cholesterol, increasing desmosterol concentrations gavaged according to each animal’s individual body 38 and decreasing cholesterol concentrations (Yoder et al. weight such that each animal received either 50 mg/kg 39 TM 2004). Because cholesterol is needed for the synthe- or 100 mg/kg DiazaCon . Squirrels were gavaged us- 40 sis of steroid reproductive hormones, such as progester- ing a straight 20 gauge 7.6 cm stainless steel feeding 41 one and testosterone, inhibition of cholesterol synthe- needle with a 2.25 mm diameter ball on the tip. All an- 42 sis indirectly inhibits reproduction. Many wild species imals were gavaged on days 1 and 2 of the study. On 43 for which fertility control could provide a practical the second day of gavaging, it became apparent that the 44 handling of the animals was causing them significant 45 management tool do not reproduce readily in captivi- ty; therefore, desmosterol is used as a marker of efficacy stress. On the second day, 2 squirrels died after being 46 handled. Therefore, peanuts coated with DiazaConTM 47 in laboratory studies with these species (Johnston et al. TM were used for the remaining 8 days of treatment. The 2 48 2003). DiazaCon has been used successfully to inhib- it reproduction in mice, rats and prairie dogs (Hikim & squirrels that died during gavaging were not replaced in 49 the study. To allow for recovery, there were 35 days be- Chakraborty 1986; Singh & Chakravarty 2003; Nash et 50 tween the last day of gavaging and the first day of feed- 51 al. 2007). 410 © 2011 ISZS, Blackwell Publishing and IOZ/CAS Effect of DiazaConTM on grey squirrels ing treated peanuts. It was determined that DiazaConTM month is the minimum time desired for DiazaConTM to 1 should have been mostly eliminated from the squirrels’ be effective in the field. Blood samples collected af- 2 systems by 35 days after gavage. This was based on the ter the first month were more spread out because all that 3 squirrels having only received 2 doses of DiazaConTM, was needed was to determine how many months Di- 4 cholesterol and desmosterol results from 5 and 19 days azaConTM could still be detected in the blood. Choles- 5 after gavaging, and prior data for mice and rats (P Nash, terol concentrations were monitored for 3 months post- 6 unpubl. data).
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