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Gastrointestinal Helminths of Feral Raccoons (Procyon Lotor) in Wakayama Prefecture, Japan

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Gastrointestinal Helminths of Feral Raccoons (Procyon Lotor) in Wakayama Prefecture, Japan FULL PAPER Parasitology Gastrointestinal Helminths of Feral Raccoons (Procyon lotor) in Wakayama Prefecture, Japan Hiroshi SATO1) and Kazuo SUZUKI2) 1)Laboratory of Veterinary Parasitology, Faculty of Agriculture, Yamaguchi University, 1677–1 Yoshida, Yamaguchi 753–8515 and 2)Hikiiwa Park Center, 1629 Inari-cho, Tanabe 646–0051, Japan (Received 30 May 2005/Accepted 1 December 2005) ABSTRACT. The population and distribution of feral raccoons (Procyon lotor) are expanding in Japan after escape or release from animal- owners. Wakayama Prefecture is one of the most typically devastated areas by this exotic carnivore, particularly in the last five years after a latent distribution for more than ten years. Official control measures of feral raccoons commenced in the summer of 2002 by several municipalities, and 531 animals collected in 12 municipalities between May 2003 and April 2005 were submitted for parasito- logical examination of gastrointestinal helminths. Detected parasites included six nematodes (Physaloptera sp. [prevalence; 5.1%], Con- tracaecum spiculigerum [0.9%], Strongyloides procyonis [25.5%], Ancylostoma kusimaense [0.8%], Arthrostoma miyazakiense [0.4%], and Molineus legerae [1.1%]), seven trematodes (Isthmiophora hortensis [4.9%], echinostomatid sp. with 34–39 collar spines [1.7%], Metagonimus takahashii [12.4%], M. yokogawai [0.8%], Plagiorchis muris [0.2%], Macroorchis spinulosus [1.9%], and Consinium ten [0.2%]), one cestode (Mesocestoides sp. [0.2%]), and six acanthocephalan spp. (Centrorhynchus bazalenticus [0.2%], Centrorhynchus teres [5.5%], Sphaerirostris lanceoides [2.4%], Plagiorhynchus ogatai [0.6%], Porrorchis oti [1.5%], and Southwelina hispida [1.9%]). Most of the collected parasites are food-borne, indigenous helminth species. Physaloptera sp. has never been recorded in indigenous wild carnivores in Japan, and resembles closely P. rara, prevalent in raccoons of North America, in morphology. The position of a pair of phasmids in the posteroventral region of the adult male, however, could differentiate it from P. rara. Since Strongyloides procyonis is known to cause creeping eruption as well as intestinal infection in a healthy human volunteer, we should be concerned about the rapid increase in the population and distribution of feral raccoons in Japan from the viewpoint of public health as well. KEY WORDS: gastrointestinal helminth, Physaloptera, Procyon lotor, Strongyloides procyonis, zoonosis. J. Vet. Med. Sci. 68(4): 311–318, 2006 The population and distribution of feral raccoons (Pro- cultural loss and housebreaking, an official control and cyon lotor (Linnaeus, 1758)) in Japan are expanding after eradication program of feral raccoons commenced in the intentional or unintentional releases by animal-owners. summer of 2002 in several municipalities of Wakayama Wakayama Prefecture is one of the most typically devas- Prefecture, including Tanabe City, which has been since tated areas in this country. Miyashita [27] recorded the dis- then adopted by other municipalities. tribution of feral raccoons in 15 prefectures in Japan, Raccoons adapt to a variety of habitats, and are often including Aichi, Gifu, Hokkaido, Kanagawa and attracted to areas of human activity by food available in the Wakayama, in March 1992. Earlier data on feral raccoons farmland and garbage in the town, or by spaces under the in Wakayama Prefecture is not available. Based on a recent roof that may offer shelter [16, 24]. Considering that serious inquiry conducted by the prefectural office (August 2003; zoonoses such as leptospirosis, tularemia, rabies, cryptospo- unpublished), a chronological change in the distribution of ridiasis and Baylisascaris procyonis larva migrans, and dis- raccoons in this prefecture is as follows (50 municipalities eases to companion animals such as canine and feline in total before 1 October 2004 or the great municipal merger distemper could be transmitted by raccoons [16, 24, 47], in Heisei era [Heisei shi-cho-son-gappei], and we follow effective control measures of feral raccoons are necessary this division thoroughly in descriptions of the present not only due to direct nuisance behaviors to human activities study): feral raccoons were noticed in 5 municipalities and disturbance of local ecosystem, but also to prophylacti- (Tanabe, Nakahechi, Kamitonda, Shirahama, and Kawabe) cally remove possible health threats to residents and indige- by 1997; another 5 municipalities located in the northern nous wildlife and domestic animals. In fact, recent region of this prefecture were added to the distribution area outbreaks of fatal neurological larva migrans caused by the by 1999; feral raccoons were noticed in 21 municipalities in raccoon roundworm B. procyonis in rabbits and Japanese total by 2001; and at least in 36 municipalities by 2003. At macaques kept in zoo facilities in Japan were serious [10, present, feral raccoons are widely distributed in at least 12 38, 41, 44], emphasizing the need for pet and feral raccoons municipalities after the inquiry data mentioned above (Fig. to be under strict control of public and animal health author- 1), and the agricultural loss caused by these animals ities. increased abruptly in the last five years: the area of damage In the present study, we examined gastrointestinal helm- was approximately 10 and 142 ha, resulting in economic inths of 531 feral raccoons collected in 12 municipalities of loss amounting to 1.5 and 32.9 million JPY, in 2001 and Wakayama Prefecture to assess their possible health threats 2002, respectively. Due to apparent nuisances such as agri- to residents and indigenous animals, with special attention 312 H. SATO AND K. SUZUKI Fig. 2. Relationship between body weight and month of trapping of feral raccoons examined in the present study. The survey period is May 2003 to April 2005. was opened longitudinally, scratched carefully by glove- worn hands, and the content was washed repeatedly by sim- ple sedimentation in tap water. Sediments were checked thoroughly under a dissection microscope. Except for sev- eral worms for DNA extraction, the collected parasites were fixed in 10% neutral-buffered formalin or 70% alcohol. Parasitological examination was carried out on 245 (100 female and 145 male) and 286 (130 female and 156 male) Fig. 1. Geographic distribution of feral raccoons examined in the feral raccoons collected in 12 municipalities during the first- present study. Wakayama Prefecture, Japan, was divided into 50 municipalities (exactly saying, this division was correct year (May 2003—April 2004), and second-year period before 1 October 2004 or the great municipal merger in Heisei (May 2004—April 2005), respectively. Geographical dis- era, but we followed this division here), and 531 examined rac- tribution and monthly numbers of feral raccoons examined coons in total were trapped in Hashimoto (HSM), Yura (YRA), in the present study are shown in Figs. 1 and 2. Body weight Gibo (GBO), Kawabe (KWB), I’nami (INM), Minabe (MNB), (BW) partially reflects the age of the animal [16], and Tanabe (TNB), Nakahechi (NHC), Kamitonda (KTD), Ohtoh roughly saying, raccoons less than 2.0 kg BW were juvenile, (OHT), Shirahama (SRH), and Hikigawa (HKG). Numbers in those between 2.0 and 4.0 kg BW growing young, and those parentheses after each abbreviated municipality name indicate the number of examined raccoons. Currently, feral raccoons are more than 4.0 kg BW young and grown adults. noticed in 36 municipalities (marked by dots or dark), and are DNA extraction and polymerase chain reaction (PCR): widely distributed in at least 12 municipalities (dark). Molecular genetic characterization was conducted on echi- nostomatid trematodes to identify the species [20, 28–30]. to the raccoon roundworm and other exotic helminth spe- Amplified were segments of small and large subunit (SSU/ cies. We believe that this kind of assessment of possible LSU) ribosomal RNA genes (rDNA) with internal tran- biohazards is important also for non-specialized workers scribed spacer 1 (ITS-1) and 2 (ITS-2), and mitochondrial engaged in the control of this animal at present as well as in genes (mtDNA) such as cytochrome c oxidase subunit I the future. (COI) and nicotinamide adenine dinucleotide dehydroge- nase subunit 1 (ND1). Parasites of interest were collected as MATERIALS AND METHODS promptly as possible, and preserved in 1.5 ml Eppendorf tubes at –80°C. DNA extraction, PCR, and DNA sequenc- Parasitological examination: Raccoons were trapped ing were conducted as described in our previous work [42]. using metal cage-traps by licensed residents, euthanized Each cycle of PCR consisted of denaturation for 30 sec at using a humanitarian method, labeled individually, and 94°C, annealing for 60 sec at 62–65°C (rDNA), 52°C (COI stored individually at –20°C until zoological examination. mtDNA), or 48°C (ND1 mtDNA), and extension for 60 sec After thawing, data related to sex, age class and zoological at 72°C. This cycle was repeated 32 times. The used prim- measurements were recorded. The entire intestine distal to ers were universal ones described by others [8, 28–30, 52]. the pylorus was removed from the carcass, refrozen, and DNA sequences were aligned using the CLUSTAL W mul- sent to the laboratory for parasitological examination. The tiple alignment program [49] available on the net [clust- stomach was opened to examine food items, and the col- alw.genome.jp/]. Nucleotide sequences reported here are lected parasites were fixed in 70% alcohol. The intestine deposited and available
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