J. Med. Entomol.

Vol. 15, nos. 5-6: 425-430

4 September

1979

© 1978 by tbe Ilishop Museum

ECTOPARASITES OF WILD CARNIVORA OF INDIANA By John O. Whitaker, Jr and Rebecca Goff! Abstract: Ectoparasites and other associates were collected from 8 species of wild carnivores occurring in Indiana. Parasites occUlTing- most often and in greatest abundance on the Gray Fox (Urocyon cinereomgenteus) were Suricatoecus quadmticeps, Cediop.\yl/t/ simplex, Clwetop.rylla lotoris, Androu/elaps fahrenholzi, and Ixodes cookei; on the Red Fox (VulPes vulpes): Ixodes cookei and C. simplex; on the Coyote (Canis latrans): Cediolisylul simplex; on the Raccoon (Procyon lotor): Trichodectes octomawlatus, Ctenoceplwlides felis, Ol'cllOpeas howardii, C. /otoris, A. fahrenholzi, Ixodes texanus, I. cookei, and Dennacentol' variabilis; on the Mink (Mustela Vl:wn): Stachiella lal'seni, LYll>:aw11Isnearcticus, A. fahl'enltolzi, Zibetlwcm'lIs o1U/atme, and I. cookei; on the Long-tailed Weasel (M IM·telafrenata): N eotl'icllOdectes111inutus,LYl1Xawrus mustelae, and L. nearctiClL\; on the Least Weasel (Mustela nivalis): Stachiella kill{.,'l; on the Striped Skunk (MePhitis mePhitis): Neotricltodectes mephitidis, A. fahl'e1lholzi, HirstionysslLS staffordi, and I. cookei; and on the Badger (Ta:ddea ta>:l/s):Neotrichodectes inter11lptofasciatus, I. cookei, D. variabilis, and H. staffordi. Some of these parasites are normally associated with the hosts whereas some appear to reflect the predatory habits of the hosts. A number of new host records are given.

probe the fur and skin while the host was viewed under a dissecting microscope at 10-70x and/or the skins were agitated in a detergent bath for approximately 1 min, followed by vacuum filtration of the supernatant (method modified from Henry & McKeever 1971). A few hosts were processed via the Hopkins dissolution technique, but this method was discontinued because of damage to the parasites. When possible, actual counts were made. Where large numbers of a given species were present, the total was estimated. RESULTS

Ten species of wild carnivores are currently known to exist in Indiana. The Bobcat, Felis rufus, is very rare, and we have not examined any specimens from the state. Data from 9 carnivore With the exception of Wilson's (1961) comprespecies are reported here. We examined at least 8 hensive paper on ticks, sucking lice and Aeas, there individuals of each species and in every case at least are relatively few reports of ectoparasites on car4 yielded parasites (TABLE1). nivores from Indiana. Mite records have been Although the sample sizes for most carnivores summarized by Whitaker & Wilson (1974), and were relatively small, a fairly large number of parFain & Hyland (1974) presented information on asite species was taken from most: 19 from the North American listrophorid mites. Emerson's Gray Fox (42 examined), 10 from the Red Fox (1972) list of the biting lice found on North Amer(14), 14 from the Raccoon (54), 11 from the Mink ican mammals, and Loomis' (1956) study of Kansas (12), 17 from the Long-tailed Weasel (16), 9 from chiggers also contain information relating to the Least Weasel (8), 6 from the Striped Skunk species found in Indiana. In addition, many other (10), 8 from the Badger (11), but only 4 from the studies dealing with the parasite fauna of restricted Coyote (15). geographic areas in North America have included Many parasites found on carnivores are picked species found on carnivores. up from prey species or dens of other mammals, and thus can yield clues as to the food and behavMATERIALS ANDMETHODS ior of the host. The 9 species of carnivores and their parasites Although mammals for this study were collected by several means, most were found as road kills. are brieAy discussed below, and forms likely obIndividuals were taken from throughout the state, tained from prey species are noted. Papers dealing but the majority were from Vigo, Tippecanoe and specifically with the ectoparasites of individual host St. Joseph counties. Animals were placed in sepa- species are also noted. The major parasites of the Gray Fox, Urocyon rate plastic bags as soon as possible after collection cinereoargenteus, were the biting louse Suricatoecus and were frozen until they could be examined in the laboratory. Most animals were examined in 1 quadraticeps; the laelapid mite Androlaelaps fahrenor both of 2 ways: dissecting needles were used to holzi; 2 Aeas, Cediopsylla simplex and ChaetopsyUa lotoris; and the tick Ixodes cookei. Of these, only the louse has any degree of host specificity. Androlae'Department of Life Sciences, Indiana State University, lapsfahrenholzi occurs regularly on many species of Terre Haute, Indiana 47809, USA.

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426

Vol. 15, nos. 5-6

Med. Entomol.

TABLE I. ECloparasiles of Vulpes vulpes n = 14

Urocyon cinereoargenteus n = 42

No. infested ECTOPARASITES

(%)

TOlal no. parasiles (no./host)

No. infested (%)

Total no. rnarasites no./host)

Procyon lotor n = 54

Canis latrans n = 15

Total no. No. infested rnarasites no./host) (%)

No. infested (%)

Total no. parasites (no./host)

4 (7.4) I (1.9) I (1.9)

10 (0.2) 1(0.02) 14,000 (2593)

I (1.9)

1 (0.02)

I (1.9)

I (0.Q2)

I (1.9) 1 (1.9)

4 (0.1) 5 (0.1)

Mites Laelapidae A ndrolaelaps fahrenholzi A. casalis Hirstionyssus staffordi H. utahensis H aemogamasus liPonyssoides H.reidi Hypoaspis leviculus Laelaps alaskensis L. kochi L. multisPinosa

6 (14.2)

24 (0.6) 1 (7.1)

1 (0.07)

Macronyssidae Ornithonyssus Ornithonyssus

wernecki bacoti

I (2.4)

4 (0.1)

2 (4.8)

7 (0.2)

Glycyphagidae APlodontopus sciuricola . Dermacarus hylandi D. hypudaei M arsuPialichus brasiliensis Scalapacarus obesus Xenoryctes latiPorus Zibethacarus ondatrae

;-

1 (7.1)

1 (0.07)

1 (7.1)

6 (0.43)

Listrophoridae ListTaphorus mexicanus Lynxacarus mustelae L. neaTcticus

Myocoptidae Myocoptes japonensis

Chiggers Euschoengastia peromysci EutTombicula alfuddugesi MicrotTombicula jonesae Neotrombicula lipovskyi N. microti N. whaTtoni

1 (6.7) 1 (2.4) 1 (2.4)

9 (0.6)

150 (3.6) 1 (0.02)

1 (7.1)

40 (2.9)

Ticks DermacentoT variabilis Ixodes cookei 1. texanus

1 (2.4) 20 (47.6)

1(0.02) 154 (3.7)

2 (14.3) 9 (64.3)

5 (0.4) 20 (1.4)

1 (6.7) 1 (6.7)

2 (0.1) 4 (0.3)

Cediopsylla simplex Chaetopsylla lotoris Ctenocephalides canis C·felis Ctenophthalmus pseudagyTtes EPitedia wenmanni Odontopsyllus multisPinosus Orclwpeas howardi O. leucopus Orapsylla antomys TamioPhila grandis

17 (40.5) 7 (16.7) 1 (2.4) 3 (7.1)

48 (1.1) 17 (0.4) 1 (0.02) 6 (0.1)

4 (28.6)

14 (1.0)

2 (13.3)

18 (1.2)

2 (4.8) 2 (4.8)

2 (0.04) 2 (0.04)

2 (4.8) 2 (4.8) 1(2.4) 1 (2.4) 1 (2.4)

3 (0.1) 3 (0.1) 2 (0.04) 1 (0.02) 1 (0.02)

6 (11.1) 9(16.7) 24 (44.4)

23 (0.4) 24 (0.4) 159 (2.9)

5 (9.3)

5 (0.1)

5 (9.3)

24 (0.4)

5 (9.3)

6 (0.1)

29 (53.7)

1609 (29.8)

Fleas 1 (7.1)

1 (7.1)

1 (0.07)

1(0.07)

Biting lice N eotrichodectes intem.IPtofasciatus N. mephitidis N. minutus Stachiella kingi S. larseni Suncatoecus quadraticeps Trichodectes octomaculatu~

-'-10 (23.8)

167 (4.0)

Sucking lice H oPlopleura erratica NeohaematoPinus sciuri

I (7.1)

1 (0.07)

I (8.3)

1(0.1)

I (8.3)

1(0.1)

1(10.0) 4 (25.0)

2 (0.2)

6 (0.4)

1(9.1)

4 (36.4) 7 (70.0) 6 (50.0)

43 (2.7) 4 (50.0)

6 (50.0)

550 (45.8)

I (6.3)

7 (0.4)

466 (58.3)

3420 (342.0)

7 (0.6)

454 (41.3)

428

J.

Med. Entomol.

Vol. 15, nos. 5-6

mammals, while I, cookei is found on many carni- The common tree squirrel flea, Orchopeas howardii, vores. The occurrence of the 2 flea species is par- was also collected. Surprisingly, the flea species ticularly interesting. C. simPlex is a rabbit flea. Its taken in the smallest numbers was the Raccoon flea, frequency and abundance on the Gray Fox indi- Chaetopsylla lotoris. Procyon is the only carnivore in cate the importance of the cottontail rabbit in the Indiana with a relatively host-specific tick species, diet of this predator. Chaetopsylla lotoris is presum- Ixodes texanus; it was the most abundant of the 3 ably a Raccoon flea. However, we found this ticks found. Two other species commonly associspecies to be relatively more abundant on the Gray ated with carnivores, I. cookei and Dermacentor varFox than on the Raccoon. It is known that the Gray iabilis, were also regularly encountered. Parasites Fox has arboreal tendencies. It seems likely that presumably acquired from prey species included the occurrence of this flea on the Gray Fox and Androlaelaps casalis and O. howardii from squirrels Raccoons indicates a mutual use of hollow trees. and Ornithonyssus wernecki from the Opossum. The occurrence of the squirrel flea Orchopeas how- Since Raccoons often use holes in hollow trees ardii on both Gray Foxes and Raccoons, but not on which squirrels and other animals also use, some of these forms may have moved onto the host from other predators, supports this view. Other parasites which may have been picked up such sites, rather than directly from prey individfrom prey species include Dermacarus hypudaei, 01'- uals. Literature dealing with the ectoparasite fauna by Johnson chopeas leucopus, and EPitedia wenmanni from small of the Raccoon was summarized rodents, Ctenophthalmus pseudagyrtes from burrow- (1970). A large number of mites, probably Hirstionyssus ing rodents or insectivores, Tamiophila grandis from chipmunks, Odontopsyllus multisPinosus from staffordi, was found on a single Raccoon (definite rabbits, and Oropsylla arctomys from the Wood- identification could not be made due to accidental over-clearing of the sample preserved). Since this chuck. Eads & Menzies (1950) and Turkowski (1974) recorded tick, flea and mite species from species is normally restricted to the Striped Skunk, the Gray Fox in Texas and Arizona, respectively, the presence of such a large number of individuals and summarized previous data from those areas. on an unnatural host is not easily explained. PerOne Red Fox, Vulpes vulpes, harbored 40 chig- haps a few individuals of H. staffordi transferred gers, Neotrombicula whartoni. The only parasites to the Raccoon by chance and subsequently mulfound on more than 1 Red Fox were the flea Ce- tiplied in the absence of competition and/or natudiopsylla simplex (also commonly found on rabbits ral immunity. However, since 3 badgers also harand the Gray Fox) and the ticks Ixodes cookei and bored H. staffordi, it seems likely that this species Dermacentor variabilis. The other forms found is simply more widespread on carnivores than precould easily have moved onto the fox from prey viously known. species: Hirstionyssus utahensis and EPitedia wenmanThe Mink, Mustela vimn, regularly harbored 3 ni from cricetid rodents, NeohaematoPinus sciuri species of mites, Lynxacarus nearcticus, Androlaelaps from squirrels, and Scalopacarus obesus from moles. fahrenholzi and Zibethacarus ondatrae; the biting Haas (1970) noted fleas from SpermoPhilus and louse, Stachiella larseni; and the tick, Ixodes cookei. Peromyscus in a Red Fox den in Wisconsin. As noted previously, A. fahrenholzi is found on Fifteen Coyotes were examined, but ectopara- many species of mammals. Lynxacarus nearcticus sites were found on only 4, including 1 species of and Z. ondatrae are generally found on certain chigger, 2 ticks and 1 flea. Only the flea species, species of Mustela and the Muskrat, respectively. Cediopsylla simplex, occurred on more than 1 Coy- The regular occurrence of Z. ondatrae is probably ote. This is the same flea that occurred most com- indicative of predation and use of burrows of the monly on the 2 species of foxes, and indicates feed- Muskrat. Stachiella larseni is restricted to the Mink, ing on cottontail rabbits. Some studies that have whereas I. cookei is common on several species of dealt with ectoparasites of Coyotes in other regions carnivores. Gorham & Griffiths (1952) have pubare Eads (1948), Ameel (1955), and Gier & Ameel lished a report concerning the diseases and parasites of Minks. ( 1959). The Raccoon, Procyon lotor, regularly harbored Only 16 Long-tailed Weasels, Mustela frenata, 1 kind of mite, the ubiquitous Androlaelaps fahrenwere examined, but 17 kinds of parasites were hob, and a host-specific biting louse, Trichodectes found. The most abundant forms were the listrooctomaculatus. Of the 3 types of fleas found, Cteno- phorid mite Lynxacarus mustelae and the biting cephalides felis, the cat flea, was the most abundant. louse Neotrichodectes minutus, although 17 individ-

1979

Whitaker & Goff: Ectoparasites of Indiana Carnivora

uals of L. nearcticus, primarily a parasite of Mink, were found on 1 Long-tailed Weasel. The large number of species recorded may indicate that Long-tailed Weasels regularly utilize a large number of prey species. Dermacarus hypudaei and Euschoengastia peromysci were likely obtained from cricetid rodents, whereas Laelaps multisPinosa and libethacarus ondatrae probably transferred from Muskrats or their burrows. The presence of Dermacarus hylandi, APlodontopus sciuricola and Hoplopleura erratica indicates predation on chipmunks. The smallest of the Indiana carnivores, Mustela nivalis, yielded a total of 9 parasite species, but the biting louse Stachiella kingi was the only regularly occurring abundant species. Androlaelaps fahrenholzi was the only other parasite recorded from more than 1 Least Weasel. Both tick species normally associated with carnivores were present, although each was found on only 1 individual. Predation on microtine rodents was suggested by the presence of 3 species of mites commonly found on microtines, Myocoptes japonensis, Listrophorus mexicanus and Laelaps alaskensis. Three hypopi of libelhacarus ondatrae found on 1 weasel were likely acquired from Muskrat burrows. Only 6 species were found on the 10 Striped Skunks, Mephitis mephitis, examined. Four of the

429

have compiled a m