EUROPEAN RABBITS ORYCTOLAGUS CUNICULUS (L.) IN SOUTHWESTERN AUSTRALIA

J. Parasitl., 85(5), 1999 p. 803-808 C American Sciety f Parasitlgists 1999 EVALUATION OF THE ASSOCIATION OF PARASITISM WITH MORTALITY OF WILD EUROPEAN RABBITS ORYCTOLAGUS CUNICULUS (L.) IN SOUTHWESTERN AUSTRALIA Russell P. Hbbs, Laurie E. Twigg*, Aileen D. Ellit, and Amanda G. Wheeler* Divisin f Veterinary and Bimedical Sciences, Murdch University, Murdch WA 6150, Australia ABSTRACT: Abundances f the parasitic nematdes Trichstrngylus retrtaefrmis and Passalurus ambiguus, and 8 Eimeria species were estimated by fecal egg and cyst utput in 12 discrete free-ranging ppulatins f wild rabbits (Oryctlagus cuniculus) in suthwestern Australia. Cmparisns f parasite egg and cyst cunts were made between thse rabbits knwn t have survived at least 2 m after fecal samples were cllected and thse rabbits that did nt survive. There were significant negative relatinships between parasite egg and cyst cunts and survival when all age grups and cllectin perids were pled fr several species f cccidia and fr T. retrtaefrmis. Hwever, when the same cmparisns were made within rabbit age grups and within cllectin perids, there were very few significant differences even where sample sizes were quite large. The differences indicated by the pled analysis fr cccidia were mst likely due t an uneven hst age distributin with respect t survival, cmbined with an uneven distributin f the cyst cunts with rabbit age. The result fr T. retrtaefrmis was similarly affected but by a seasnal pattern. Parasitism by nematdes and cccidia did nt appear t be an imprtant mrtality factr in these rabbit ppulatins, at least at the range f hst densities we examined. This suggests that ther factrs must have been respnsible fr the bserved pattern f density-dependent regulatin in these rabbits. There is increasing interest in the rle f infectius diseases in regulating their hst ppulatins. In rder t regulate hst ppulatins, parasites must cause a decrease in survival, r fecundity, r bth, and their abundance shuld increase with increasing hst density at least ver mst f the range in abundance f their hsts (Sctt and Dbsn, 1989). Current ppulatin mdels fr macrparasites cntain assumptins that dis- 1999). These techniques allwed the relatinship f parasite abundance with hst survival t be examined fr the nematdes T. retrtaefrmis, which is suspected f regulating rabbit ppulatins (Bull, 1964; Dunsmre, 1981), and P. ambiguus, which Received 21 May, 1998; revised 23 February 1999; accepted 23 February 1999. * Vertebrate Pest Research Services, Agriculture Western Australia, and Vertebrate Bicntrl CRC, Bugainvillea Avenue, Frrestfield, WA 6058, Australia. is cnsidered nnpathgenic (Sulsby, 1982). The relatinship was als examined fr the 8 mst prevalent species f cccidia (Eimeria spp.) in these rabbits (Hbbs and Twigg, 1998), sme f which are knwn t cause mrtality in labratry studies (Cudert et al., 1995). MATERIALS AND METHODS ease agents such as parasites increase hst mrtality (Andersn Details f the study area, experimental design, and parasitlgical and May, 1979; Rberts et al., 1995), but there have been very methds are given in Twigg et al. (1998) and Hbbs et al. (1999), few field studies that have tested this assumptin (fr discussin respectively. Rabbit numbers were determined by live-trapping and represent the minimum number f animals knwn t be alive (MNKA) at see Gulland [1995]). the site fr each cllectin perid. Althugh hst ppulatins were mnitred every mnth, fecal samples were cllected nly 6 times during In 1992, a field experiment was established t measure the effect f reducing the fertility f female rabbits Oryctlagus 1994-1996. All rabbits were individually tagged. Fr each cllectin cuniculus (L.) n rabbit abundance. The experiment was carried perid, rabbits were deemed t be survivrs if they were knwn t be ut in the suthwest f Western Australia (Twigg et al., 1998). alive fr at least 2 m after the mean cllectin time (Table I). In the sterility trial, female rabbits were surgically sterilized by tubal ligatin Twelve discrete rabbit ppulatins were created by a cmbinatin f rabbit-prf fences and maintenance f buffer znes. in the prprtin f 0%, 40%, 60%, and 80%, with 3 replicates f each treatment. Sham peratins were included such that 80% f females Breeding stps (warrens) were cnfined t areas f native shrub received sme frm f surgery. habitat adjacent t the pasture where rabbits fed. Thus, the experimental rabbits were living under essentially natural cndi- f the prprtin f rabbits that survived, against rabbit abundance We tested the density dependence f survival by regressin analysis (MNKA). Each data pint crrespnds t a single site (rabbit ppulatin) at 1 cllectin perid. Data pints based n less than 10 rabbits tins. All rabbits were live-trapped at 4-6 weekly intervals that allwed fr repeated nndestructive sampling f parasite abundance by fecal egg cunts. In cntrast, mst parasitlgical tween parasite abundance and hst mrtality. The first methd used were excluded. Tw methds were used t explre the relatinship be- studies f wild mammal ppulatins invlve the destructive regressin analysis f survival against site means f lg-transfrmed fecal egg and cyst cunts. The secnd was based n individual rabbits sampling f hsts fr the determinatin f actual parasite numbers by pstmrtem (e.g., Dunsmre and Dudzinski, 1968; Gul- and simply cmpared fecal egg and cyst cunts f survivrs t that f nnsurvivrs, regardless f site. Cmparisns were made using nnparametric Mann-Whitney U-tests. Because egg cunts f the nemaland, 1992). Fecal egg cunts are effective in detecting patterns in parasite abundance related t the age and sex f the hst and tdes were fund t be influenced by seasn (Hbbs et al., 1999), and seasnal differences fr Trichstrngylus retrtaefrmis and bth cccidian cyst cunts and hst mrtality were strngly influenced by the age f the hst (Twigg et al., 1998; Hbbs et al., 1999), Passalurus ambiguus in Eurpean rabbits (Hbbs et al., 1999). samples were split by sampling perid (time) and rabbit age fr further The abundance f cccidia (Eimeria spp.) in rabbit ppulatins statistical analysis. Significance levels were set at P - 0.01. can als be estimated by fecal cyst utput (Hbbs et al., Survival f rabbits RESULTS The estimated survival f rabbits fr each age grup ver the 6 cllectin perids is shwn in Table II. These estimates were based nly n the rabbits included in the parasitlgical study frm which fecal samples were btained. Trends in the changes in rabbit abundance were similar between sterility levels (Fig. 1). Rabbit numbers increased at the end f 1994, declined ver 803

804 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 5, OCTOBER 1999 TABLE I. Cllectin dates and the dates used t determine the survival f rabbits fr each f the 6 fecal cllectin perids.* Cllec- Mean tin cllectin Date fr perid Cllectin dates date survival A 11 Oct-7 Dec 1994 24 Oct 94 1 Jan 95 B 28 Feb-5 Apr 1995 10 Mar 95 1 Jun 95 C 1 Aug-13 Sep 1995 20 Aug 95 1 Nv 95 D 27 Sep-10 Nv 1995 9 Oct 95 1 Jan 96 E 22 Nv-7 Dec 1995 28 Nv 95 1 Feb 96 F 27 Feb-11 Apr 1996 9 Mar 96 20 May 96 * Rabbits were scred as survivrs fr the cllectin perid if they were knwn t be alive at the subsequent survival date. 180 160 - Z 140- z e 120- N Cn c 100-3 80-. 60-40- 20- A B C D E F the first half f 1995, then increased late in 1995 befre declining ver the summer/autumn f 1996. Survival was generally highest in adults and lwest in kittens (Table II). Survival in subadults was slightly higher n average than fr kittens. Survival was highest fr all age grups in early spring (August) 1995. Fr the kittens, there was very pr survival frm early summer (Nvember-December) 1995 int late summer 1996, a time when survival fr the ther age grups was quite high. Sites with high rabbit numbers generally had relatively lw survival (Fig. 2), suggesting density-dependent regulatin f the scrutiny f the regressin suggests that the relatinship may be due t the seasnality f bth infectin and rabbit mrtality, hst ppulatins. rather than a direct effect f parasite abundance n mrtality. Nematde parasites There was a negative regressin f rabbit survival against T. retrtaefrmis egg cunts (P = 0.002), but fr the nnpathgenic P. ambiguus, the slpe was psitive (P = 0.004) (Fig. 3). The negative slpe fund fr T. retrtaefrmis is indicative f a relatinship between infectin and mrtality. Hwever, clser 0 SO N D J F M A M J J A S O N D J F M A 1994 I 1995 I 1996 Mean Cllectin Date FIGURE 1. Ppulatin sizes fr each f the samples f rabbits estimated frm trapping data (minimum number knwn alive at that plt fr that cllecting perid), pltted against mean date f cllectin. Plts are labeled accrding t sterilizatin regime. Slid pints n the graph are late summer samples (March 1995, 1996) where survival f adult rabbits was high and fecal egg utput lw, and if these are cnsidered separately, the regressin slpes are nt significantly different frm 0 (summer, P = 0.661; ther, P = 0.055). Cnversely, with P. ambiguus the nly samples that had high mean egg cunts were the summer samples, and if summer and ther samples are cnsidered TABLE II. Cmparisns f Trichstrngylus retrtaefrmis egg cunts between rabbit survivrs and nnsurvivrs.* Mann- Sampling Survival Sample sizes Gemetric mean epg Whitney Sampling Survival Whitney U Age grup perid (%) Nnsurvivrs Survivrs Nnsurvivrs Survivrs significance Kittens 50-699 g A 56 23 29 13.77 6.08 0.093 C 71 26 63 7.06 9.19 0.659 D 37 38 22 7.42 12.78 0.313 E 20 40 10 7.77 13.85 0.427 A-F 49 131 125 7.83 8.99 0.564 Subadults 700-1,199 g A 47 43 38 22.55 20.15 0.639 C 74 8 23 23.93 29.37 0.416 D 62 40 64 22.60 25.92 0.588 E 49 36 34 27.00 25.62 0.893 A-F 56 139 177 19.14 20.42 0.591 Adults >1,199 g A 79 17 63 18.86 13.45 0.378 B 69 35 78 6.61 3.12 0.010 C 90 11 96 19.21 8.73 0.162 D 82 15 69 11.70 13.65 0.559 E 64 43 75 13.63 11.22 0.931 F 83 38 183 8.01 5.26 0.110 A-F 78 159 564 10.76 7.48 0.016 All ages A-F 67 429 866 11.83 9.49 0.020 * Rabbits were scred as survivrs fr the samplin mass. Summer samples in kittens and subadults were nt tested due t lw sample sizes.

zx HOBBS ET AL.-PARASITISM AND MORTALITY OF RABBITS 805 0) c 0. 0 1.0 0.9-0.8-0.7-0.6-0.5-0.4-0 Or < ' F(1,s7) =9.20 v? p = 0.004 + r2 =0.139 00 * 0 O d + + x ^ X*A x 0 + X * v X * x + A + x. A W Octber 1994 March 1995 August 1995 Octber 1995 Nvember 1995 March 1996 1.0-4 =c 0.9-2_ 0.8-03 0.7- e. 0.6- - 0.5-0.4- a. Trichstrngylus retrtaefrmis? I I I I I I ' v'0 0 F(1,57) = 10.62 V v p= 0.002 _ 0, A 0+ r2 = 0.396 0 x ~ * X A \ + ZA A Octber 1994 March 1995 August 1995 Octber 1995 Nvember 1995 March 1996 0.3- + a+ A 0.3- A + A+ 0n2.... 0 20 40 60 80 100 120 140 160 180 Hst ppulatin size (MNKA) 0.2 0.z 4 I I I I I I 0.6 0.8 1.0 1. 2 1.2 1.4 1.6 1.8 Mean Lg (1 +Egg Cunt) FIGURE 2. Scatterplt and regressin line f the prprtin f rabbits that survived versus rabbit abundance (minimum number knwn alive) fr site and cllecting perid where there was at least 10 fecal samples. Dates used in calculating the prprtin f rabbits surviving are shwn in Table I. separately, slpes were nt significantly different frm 0 (summer, P = 0.264; ther, P = 0.322). Egg cunts f T. retrtaefrmis fr surviving rabbits were cmpared with cunts f nnsurvivrs using nnparametric Mann-Whitney U-tests. There were insufficient kittens r subadults frm the late summer (March 1995, 1996) cllectins, but f the remaining 14 cmparisns, nly 1 prduced a significant difference (Table II), and that was the case with the lwest egg cunts. There were n significant differences fr P. ambiguus (data nt shwn). Cccidian parasites Regressins f rabbit survival against lgarithms f the means f cyst cunts had significantly negative slpes in 5 species and a psitive slpe fr 1 species (Table III). Significant regressin slpes may have been due t the fact that cyst meria pirifrmis was mre abundant in adult rabbits (Hbbs et TABLE III. Slpes, F-values, significance f slpe, and r2 fr the regressin f the prprtin f rabbits that survived n the lgarithm f al., 1999), and this culd accunt fr the psitive slpe. With the mre direct apprach f cmparing cyst cunts means f fecal cyst cunts, fr sites and cllectin perids with sam- sizes f at least 10 rabbits.* f rabbit survivrs and nnsurvivrs (Table IV), rabbit mrtal-plity fr 5 f the 8 species f cccidia was assciated with higher cyst cunts, when all age grups and sampling perids were pled. Hwever, because rabbit survival is lwest in kittens (Twigg et al., 1998), and mst species f cccidia are mre abundant in kittens (Hbbs et al., 1999), significant assciatins were inevitable and can neither imply nr exclude causality. Therefre samples were split by age grup. Only 1 species (Eimeria media) was assciated with mrtality in subadult rabbits, and 1 different species (Eimeria perfrans) in adults, when sampling perids were pled. There were n such assciatins in kittens. After samples were further split by cllecting perid, because survival differed between cllecting perids, very few C. 0.8 0.7?-.07._? 0.6 0.5. 0.4 assciatins remained (Table IV), even thugh sample sizes reb. Passalurus ambiguus 0.4 0.6 + xx A v Octber 1994 March 1995 August 1995 Octber 1995 Nvember 1995 March 1996 Mean Lg (1 +Egg Cunt) FIGURE 3. Scatterplt and regressin line f the prprtin f rabbits that survived versus mean f the lgarithm f number f (a) Trichstrngylus retrtaefrmis and (b) Passalurus ambiguus eggs per g feces (epg), fr each f the cllectin perids where fecal samples were cllected frm at least 10 rabbits per site. Survival dates used in calculating the prprtin f rabbits that survived are given in Table I. The F- value, significance f the regressin slpe (P), and r2 values are shwn fr each graph. cunts differed between age grups (Hbbs et al., 1999). Fr mained quite high. Particularly ntewrthy is the similarity f all f the cccidia species with negative slpes, abundance was cyst cunts between surviving and nnsurviving kittens, because kittens are subject t the greatest mrtality. In subadult lwest in adult rabbits. Fr example, Eimeria intestinalis was fund in very few rabbits lder than 4 m (Hbbs et al., 1999). rabbits, high cunts f E. intestinalis and E. media were assciated with mrtality. In adult rabbits, high cunts f E. per- Late summer samples (March) had very few yung rabbits and, therefre, lw mean abundance f E. intestinalis. Rabbit survival was als relatively high in late summer. In cntrast, frans were assciated with mrtality in late summer (March) Ei- Species Slpe F Pt r2 Eimeria exigua -0.101 1.69 ns 0.032 Eimeria perfrans -0.124 6.77 0.012 0.115 Eimeria intestinalis -0.279 10.98 0.002 0.174 Eimeria pirifrmis 0.213 9.80 0.003 0.159 Eimeria media -0.200 9.38 0.004 0.153 Eimeria fiavescens 0.047 0.39 ns 0.007 Eimeria magna -0.144 4.20 0.046 0.075 Eimeria stiedai -0.147 8.32 0.006 0.138 * Sample size fr each f the regressins is 54 cases. Survival dates used in estimating the prprtin f rabbits that survived are given in Table I. t ns = Nt significant.

TABLE IV. Cmparisns f Eimeria spp. cyst cunts between survivrs and nnsurvivrs.* Cllectin Survival Sample E. flaves- Age grup perid (%) size E. exigua E. perfrans E. intestinalis E. pirifrmis E. media cens E Kittens Subadults Adults 50-699 g A 56 52 ns ns ns ns ns ns C 71 89 ns ns ns ns ns ns D 37 60 ns ns ns ns ns ns All perids 51 233 ns ns ns ns ns n 700-1,199 g A 47 81 ns ns ns ns 0.006 ns D 62 104 ns ns ns ns ns ns E 49 38 ns ns 0.010 ns ns ns All perids 56 284 ns ns ns ns 0.005 n >1,199 g A 79 80 ns ns ns ns ns ns B 69 113 ns 0.002 ns ns ns ns C 90 107 ns ns ns ns ns ns D 82 84 ns ns ns ns ns ns E 64 81 ns ns ns ns ns ns ns F 83 221 ns ns ns ns ns ns All perids 79 686 ns 0.0003 ns ns ns n All age grups All perids 68 1,203 ns <0.0001 <0.0001 <0.0001t <0.0001 ns < * Rabbits were scred as survivrs fr the cllecting perid if they were knwn t be alive at the date fr survival. Rabbit age grups were determined by bdy mass. Sum kittens and subadults were nt tested due t lw sample sizes. Kitten samples in perid E and subadult samples in perid C were nt tested due t lw sample sizes with f Mann-Whitney U-tests are given fr each case where P was less than r equal t 0.01, therwise it is marked ns. Unless therwise indicated, significant values indicate th than nnsurvivrs. t Survivrs with higher cyst cunt.

HOBBS ET AL.-PARASITISM AND MORTALITY OF RABBITS 807 1995. Althugh high cunts f Eimeria stiedai were als assciated with higher mrtality in early summer 1995, nly 7 adult rabbits were infected at this perid, s the assciatin must be regarded with sme suspicin. DISCUSSION Althugh the abundance f P. ambiguus was nt expected t be assciated with rabbit mrtality, T. retrtaefrmis is a knwn pathgen f Eurpean rabbits (Barker and Frd, 1975). Other species f Trichstrngylus have als been assciated with mrtality, fr example in dmestic sheep (Grdn, 1950) and wild red gruse (Hudsn et al., 1992). Althugh Bull (1964) and Dunsmre (1981) have shwn that T. retrtaefrmis can reduce fecundity and weight gain in rabbits, there have been n field studies that indicate that this species affects survival f Eurpean rabbits. Furthermre lasn and Bag (1988) fund n evidence that T. retrtaefrmis had any effect n mrtality, fecundity, r weight gain in muntain hares (Lepus timidus) in Sctland. In ur study, rabbit mrtality did nt appear t be assciated with high egg cunts f T. retrtaefrmis. In experimental infectins, several species f cccidia are knwn t cause mrtality in Eurpean rabbits (Bull, 1958; Cudert et al., 1995). There have als been claims that cccidia, particularly E. stiedai, are assciated with rabbit mrtality in the wild (Tyndale-Bisce and Williams, 1955; Bull, 1958; Dunsmre, 1971). Hwever, these studies were based n destructive sampling, s rabbit survival was nly able t be inferred. Furthermre, cnclusins in these field studies were based n bservatins that cccidia were mst abundant at the shwn in Table IV d indicate that higher cyst cunts f sme species f cccidia are assciated with reduced survival at thse times when survival was lwer than nrmal. Thus, it ANDERSON, R. M., AND R. M. MAY. 1979. Ppulatin bilgy f infectius diseases. Part I. Nature 280: 361-367. is pssible that E. media caused mrtality in subadult rabbits BARKER, I. K., AND G. E. FORD. 1975. Develpment f atrphic enterit in late spring 1994, and E. intestinalis in late spring 1995. Similarly, E. perfrans may have increased mrtality f adults inretrtaefrmis. Jurnal f Cmparative Pathlgy 85: 427-435. in the small intestines f rabbits infected with Trichstrngylus late summer 1995. We fund n evidence that ther species BULL, P. C. 1958. Incidence f cccidia (Sprza) in wild rabbits, Oryctlagus cuniculus (L.), in Hawke's Bay, New Zealand. New were assciated with mrtality, and it appears that ther factrs Zealand Jurnal f Science 1: 289-328. may have caused mst f the mrtality in ur study.. 1964. Eclgy f helminth parasites f the wild rabbit Oryctlagus cuniculus (L.) in New Zealand. New Zealand Department The prtcl used in the present study that allwed a direct measure f the assciatin f parasitism with survival was similar t that used by Mykytwycz (1962) n an enclsed ppu- COUDERT, P., D. LIcIS, AND E DROUET-VIARD. 1995. Eimeria species f Scientific and Industrial Research Bulletin 158, 147 p. and strains f rabbits. In Guidelines n techniques in cccidisis latin near Canberra. He was unable t shw any differences research, J. Eckert, R. Braun, M. W. Shirley, and P. Cudert (eds.). in cyst utput between survivrs and nnsurvivrs n a within-litter basis. Fr many f his analyses, all species f cccidia were pled; hwever, E. stiedai was the mst cmmn species in his yung rabbits. Mykytwycz (1962) did find that the rabbits that were disappearing frm his site were thse at that age when E. stiedai was mst prevalent, but he was able t shw that ther factrs such as predatin and myxmatsis were mre imprtant causes f mrtality. We suggest that ther factrs may have caused the mrtality patterns in the studies f Tyndale-Bisce and Williams (1955), Bull (1958), and Dunsmre (1971). Parer (1977) fund that the highest mrtality rate fr rabbits at a site with a drier climate in suth-central New Suth Wales was in kittens aged 21-30 days ld, befre the nset f cccidisis, s in that area als, ther factrs must have been mre imprtant causes f mrtality. Other studies in semiarid areas f Australia have either discunted r ignred parasitism as a significant cause f mrtality (Wd, 1980; Richardsn and Wd, 1982; Wheeler and King, 1985). In a survey f rabbit ppulatin dynamics in Australia and New Zealand, Gilbert et al. (1987) cncluded that while diseases and predatrs may exert a large influence n ppulatin size in sme circumstances, there was n cmmn pattern acrss sites. Cudert et al. (1995) have warned that in rabbits there is n crrelatin between cyst excretin and severity f disease and have recmmended that cyst cunts nly be used when ther methds are nt available, such as in field studies like urs. It is quite pssible therefre that cccidisis was a majr mrtality factr in ur rabbits, but that it was nt pssible t detect this using ur methds. Hwever, in ur study, we culd nt demnstrate a clear relatinship between parasitism and hst density (Hbbs et al., 1999). We were able t find little evidence fr a relatinship between mrtality and nematde egg cunts r cccidian cyst cunts. We therefre cnsider that factrs ther than parasitism caused mst f the bserved mrtality. time f high mrtality, particularly in the age grup experiencing that mrtality. Thus, Bull (1958) and Dunsmre (1971) sug- ACKNOWLEDGMENTS We thank ur numerus clleagues fr their assistance with gested that E. stiedai wuld be particularly imprtant in kittens varius aspects f this study, particularly the cllectin f fecal frm litters brn late in the breeding seasn. In ur study situatin, Twigg et al. (1998) have shwn that late-brn kittens pellets. We als thank Ian Rbertsn and Andrew Thmpsn fr their helpful cmments n the manuscript. This study was suffered increased mrtality als. Hwever, we culd find n funded by the Agriculture Prtectin Bard, WA (AWA) and evidence that cyst cunts were higher in late-brn kittens the CRC fr Bilgical Cntrl f Vertebrate Pest Ppulatins (Kruskal-Wallis tests, data nt shwn) r that cccidia were and was cnducted under Animal Ethics apprval frm Agriculture Western Australia (91AL58). assciated with this reduced survival, with the pssible exceptin f E. media and E. intestinalis (Table IV). The results LITERATURE CITED Eurpean Cmmissin Agricultural Bitechnlgy, Luxemburg, p. 52-73. DUNSMORE, J. D. 1971. A study f the bilgy f the wild rabbit in climatically different regins in eastern Australia. IV. The rabbit in the suth castal regin f New Suth Wales, an area in which parasites appear t exert a ppulatin-regulating effect. Australian Jurnal f Zlgy 19: 355-370.. 1981. The rle f parasites in ppulatin regulatin f the

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