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Haverkost and Gardner 2008

Haverkost and Gardner 2008

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Published by t_haverkost
J. Parasitol., 94(3), 2008, pp. 716–726 American Society of Parasitologists 2008

A REVIEW OF SPECIES IN THE GENUS RHOPALIAS (RUDOLPHI, 1819)
Terry R. Haverkost and Scott L. Gardner
The Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska 68588-0514. e-mail: slg@unl.edu
ABSTRACT:

Currently, there are 6 recognized species in the genus Rhopalias. These parasites are found in the small intestines of numerous species of marsupials throughout North and
J. Parasitol., 94(3), 2008, pp. 716–726 American Society of Parasitologists 2008

A REVIEW OF SPECIES IN THE GENUS RHOPALIAS (RUDOLPHI, 1819)
Terry R. Haverkost and Scott L. Gardner
The Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska 68588-0514. e-mail: slg@unl.edu
ABSTRACT:

Currently, there are 6 recognized species in the genus Rhopalias. These parasites are found in the small intestines of numerous species of marsupials throughout North and

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716
 J. Parasitol.,
94(3), 2008, pp. 716–726
American Society of Parasitologists 2008
A REVIEW OF SPECIES IN THE GENUS
RHOPALIAS 
(RUDOLPHI, 1819)
Terry R. Haverkost and Scott L. Gardner
The Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska 68588-0514.
e-mail: slg@unl.edu 
ABSTRACT
: Currently, there are 6 recognized species in the genus
Rhopalias
. These parasites are found in the small intestinesof numerous species of marsupials throughout North and South America. Small mistakes in various classical taxonomic workshave given rise to recent and numerous misidentifications of these species. In this work, we examine a total of 99 specimensacross all species from museum collections in an attempt to determine informative taxonomic characters to distinguish thesespecies. Despite confusion in the literature, accurate identification of these species can be achieved by observing the presence orabsence of oral and flanking spines anterior to the oral sucker.
Species of 
Rhopalias
(Trematoda: Rhopalidae) occur in thesmall intestines of marsupials throughout the Nearctic and Neo-tropical regions. Six species are currently recognized as valid.Rudolphi (1819) described
Distoma coronatum
from
Didelphismarsupialis
Linnaeus, 1758 collected by Johann Natterer inBrazil. Diesing (1850) described
Rhopalophorus horridus
from
Chironectes minimus
(Zimmermann, 1780) also collected byNatterer. Stiles and Hassall (1898) recognized that
Rhopalopho-rus
was an occupied name, and renamed the genus
Rhopalias
.Braun (1901) provided formal descriptions of both previouslydescribed species, and recognized and described another spe-cies,
Rhopalias baculifer 
, from the same material examined byDiesing (1850). Chandler (1932) described
Rhopalias macra-canthus
from North America in
Didelphis virginiana
Kerr,1792. Kifune and Uyema (1982) described
Rhopalias caballe-roi
from
D. marsupialis
and
Philander opossum
(Linnaeus,1758) in Brazil. Finally, Rivallis et al. (2004) described themost recent species in this genus,
Rhopalias caucensis
from
P.opossum
collected in Colombia.Skrjabin (1948) reproduced the descriptions of the species inthe genus and provided an identification key to the known spe-cies of 
Rhopalias
in that work, it is apparent that the labels forthe figures referring to
R. baculifer 
and
R. horridus
were re-versed. Travassos et al. (1969) reproduced the work of Skrjabin(1948), along with the mislabeled figures. In the summary work of Yamaguti (1971), Figure 1651 of 
Rhopalias coronatus
is areproduction of 
R. horridus
after Caballero (1946); this figureis in fact a representation of the currently recognized species
 R. caballeroi
. In the same work (Yamaguti, 1971), Figure1650B of 
R. coronatus
, after Caballero (1946), but attributed toBraun (1901), also appears to be a drawing of 
R. caballeroi
,but because the tentacles are covering the area where flankingspines would be found, identification to species is not possiblefrom the Figure (although it is likely
R. caballeroi
). Finally,Radev et al. (2005) offer original figures of 
R. macracanthus
drawn from specimens stored in the Manter Laboratory of Par-asitology (HWML 0844, 22422, 22423). These specimens havebeen verified by 1 of us (T.R.H.) as
R. macracanthus
, but thefigures of these specimens in Radev et al. (2005) lack the de-fining flanking spines, making them easily mistaken for
R. ca-balleroi
.The species of 
Rhopalias
are some of the most distinctiveand easily recognized trematodes of mammals. However, the
Received 16 August 2007; revised 22 October 2007; accepted 25 Oc-tober 2007.
correct identification of the species in this genus has remaineda difficult task, given the flaws in the above references and thelack of a thorough investigation of important taxonomic char-acters. Here, we intend to provide the most thorough investi-gation, to our knowledge, of the 6 currently recognized speciesin this genus.
MATERIALS AND METHODS
Specimens prepared and studied by us were stained in acetic Semi-chon’s carmine, dehydrated in an ethanol series, cleared in terpineol andxylene, and mounted in Canada balsam or gum Damar (Prichard andKruse, 1982). All other specimens studied were obtained from museumcollections including: the United States National Parasite Collection(USNPC), Beltsville, Maryland; the Harold W. Manter Laboratory of Parasitology (HWML), Lincoln, Nebraska; the Naturhistorische Muse-um Wein (NMW), Vienna, Austria; the Universidad Nacional Auto´no-ma de Me´xico (UNAM), Mexico City, Mexico; the Museo de HistoriaNatural at the Universidad Nacional Mayor de San Marcos (UNMSM),Lima, Peru; and the Kyushu University Museum (FUK), Fukuoka, Ja-pan. Due to the commonality of misidentified and mislabeled specimensthroughout the previous literature and in museum holdings, this paperdeals only with specimens that have been studied by the authors. Wedo not include a comparative table of measurements from previous stud-ies for this same reason. All measurements were taken with a ZeissUltraphot
௢ 
microscope equipped with an ocular micrometer and arepresented to the nearest micrometer unless otherwise noted; ranges arefollowed by the mean and the number of characters studied (n) is givenif different from the number of specimens studied (N). Canonical dis-criminant analysis (CDA) was performed on the natural log transfor-mations of the 23 measurements summarized in Tables I and II exclud-ing egg length and egg width using PROC CANDISC in SAS (version6.12, SAS Institute, Cary, North Carolina).
RESULTSSpecimens examined
 Rhopalias coronatus
(22 specimens total): HWML34950 (1specimen) from
Didelphis albiventris
, Paraguay; HWML70000(12 vouchers) from
P. opossum
, Santa Cruz Department, Bo-livia; HWML70002 (1 specimen) from
P. opossum
, Santa Cruz,Department, Bolivia; HWML70009 (3 vouchers) from
P. opos-sum
, Santa Cruz, Bolivia; HWML70013 (1 specimen) from
Lu-treolina crassicaudata
Berisso, Argentina; UNAM4081 (1specimen) from
Didelphis
sp., Veracruz, Mexico; USNPC14998(1 specimen) from unknown host, Panama; USNPC72792 (2vouchers) from
D. marsupialis
, El Tacal, Venezuela.
 Rhopalias horridus
: V4677 (1 neotype, 1 voucher) from
C.minimus
, Brazil.
 Rhopalias caucensis
(4 specimens total): UNAM1225 (2specimens) from
Didelphis mesamericana
, Guazacapa, Guate-
 
HAVERKOST AND GARDNER—REVIEW OF
RHOPALIAS 
717
T
ABLE
I. Measurements of 
Rhopalias
species including
R. coronatus, R. baculifer 
, and
R. horridus
by coefficient of variation (CV), distance fromthe anterior extreme to the anterior margin of the vitellaria (ANTVIT), and distance from the anterior margin of the vitellaria to the posteriormargin of the acetabulum (ACEVIT).*Character
 R. coronatus
(N
ϭ
22)
n
Mean Range CV
 R. baculifer 
(N
ϭ
8)
n
Mean Range CV
 R. horridus
(N
ϭ
2)
n
Mean Range CVTotal length 22 4,440 2,1609,360 47 8 9,369 7,12812,600 20 2 2,463 2,4342,492 2Total width 22 735 2191,584 51 8 998 8401,162 12 2 489 422556 19AcetabulumLength 22 376 150840 38 8 478 406575 14 2 157 143170 12Width 22 350 150816 42 8 508 435757 21 2 164 143184 17Oral suckerLength 22 183 93344 37 8 275 190356 20 2 86 7499 20Width 22 180 88325 37 8 249 230331 41 2 92 8699 10Cirrus sacLength 22 970 5632,219 42 8 981 8131,290 17 2 668 573762 20Width 20 203 119500 51 8 271 200344 16 2 148 134161 13Anterior testisLength 21 333 156625 42 8 1,188 7201,488 25 2 168 148188 17Width 21 167 100281 34 8 257 127336 26 2 150 143157 6Posterior testisLength 21 499 256919 39 8 1,416 8881,848 24 2 246 233260 8Width 21 149 75281 34 8 243 164312 20 2 130 125134 5OvaryLength 21 169 75344 44 8 302 181394 25 2 96 9499 3Width 20 178 88350 41 7 285 206350 20 2 99 94103 6Tentacle sacLength 21 693 3751,188 38 8 269 210319 18 2 311 305318 3Width 21 137 63238 35 8 104 63150 30 2 81 6399 31PrepharynxLength 22 39 0313 231 8 20 070 153 2 56 5459 6PharynxLength 22 202 115425 38 8 215 150281 22 2 94 86103 13Width 21 104 30244 61 8 158 104200 20 2 72 5590 34EsophagusLength 20 186 0606 101 8 0 00 0 2 128 85170 47ANTVIT 22 1,160 3313,600 72 8 1,374 1,1521,584 11 2 911 882939 4ACEVIT 22 51
Ϫ
200480 437 8 293 72480 44 2 220 134307 55Egg number 22 24 075 87 8
Ͼ
200
Ͼ
200 0 2 53 3570 47EggsLength 94 90 70108 9 36 84 6898 8 10 68 6572 3Width 94 51 3870 12 36 52 3863 10 10 43 3848 7
* N; total number of specimens;
n
; number of measurements. All data is rounded to the nearest
m.
mala; UNAM966 (1 specimen) from
D. marsupialis
, San Jose,Costa Rica; USNPC92122 (1 specimen) from
P. opossum
, Co-lombia.
 Rhopalias baculifer 
(8 specimens total): HWML35933 (2specimens) from
C. minimus
, Panama; HWML70012 (4 speci-mens) from
P. opossum
, Catemaco, Mexico; UNAM1137 (2specimens) from
P. opossum
Alajuela, Costa Rica.
 Rhopalias macracanthus
(25 specimens total): HWML22664(1 specimen) from
D. virginiana
, Tallahasee, Florida;HWML70001 (2 specimens) from
P. opossum
, Santa Cruz De-partment, Bolivia; HWML70028 (1 specimen) from
P. opos-sum
, Santa Cruz, Bolivia; HWML70003 (1 specimen) from
P.opossum
, Santa Cruz, Department, Bolivia; HWML70010 (1specimen) from
P. opossum
, Santa Cruz Department, Bolivia;UNAM1226 (6 specimens) from
D. mesamericana
, Chiapas,Mexico; UNAM2956 (1 specimen) from
D. virginiana
, Veracruz,Mexico; UNAM2957 (1 specimen) from
D. virginiana
, Veracruz,Mexico; UNAM4622 (1 specimen) from
D. virginiana
, Vera-cruz, Mexico; UNAM4625 (1 specimen) from
D. virginiana
, Ve-racruz, Mexico; UNAM968 (4 specimens) from
D. marsupialis
,Colima, Mexico; UNAM4081 (1 specimen) from
Didelphis
sp.;USNPC5745 (1 specimen) from
D. virginiana
, Washington,
 
718 THE JOURNAL OF PARASITOLOGY, VOL. 94, NO. 3, JUNE 2008
T
ABLE
II. Measurements of 
Rhopalias
species including
R. caballeroi, R. caucensis
, and
R. macracanthus
by coefficient of variation (CV), distancefrom the anterior extreme to the anterior margin of the vitellaria (ANTVIT), and distance from the anterior margin of the vitellaria to the posteriormargin of the acetabulum (ACEVIT).*Character
 R. caballeroi
(N
ϭ
37)
n
Mean Range CV
 R. caucensis
(N
ϭ
4)
n
Mean Range CV
 R. macracanthus
(N
ϭ
25)
n
Mean Range CVTotal length 37 2,283 8133,489 36 4 2,211 1,9992,471 11 25 3,683 9697,093 47Total width 37 691 3131,074 38 4 725 576799 14 25 966 3601,508 33AcetabulumLength 37 228 24319 29 4 264 210335 21 25 359 155538 28Width 37 242 138340 24 4 242 194290 20 25 341 125475 30Oral suckerLength 36 132 60256 28 4 154 125185 18 25 168 88242 28Width 36 135 75288 31 4 147 118175 20 25 185 70264 32Cirrus sacLength 36 532 170938 32 3 685 575775 15 24 1,232 3752,300 35Width 34 141 53225 33 3 193 170219 13 23 257 75375 30Anterior testisLength 37 247 33488 42 4 196 150225 17 25 346 63675 50Width 37 281 113515 48 4 293 213360 21 25 286 58475 39Posterior testisLength 37 401 70582 38 4 308 220388 23 23 523 123806 42Width 37 253 75448 51 4 222 94275 39 23 275 70430 33OvaryLength 37 129 50219 31 4 140 100160 19 25 188 88282 34Width 37 146 68233 29 4 199 150240 22 25 213 85300 32Tentacle sacLength 36 251 138358 21 3 293 275320 8 25 308 150415 28Width 36 94 38184 33 3 123 113140 12 25 139 45190 30PrepharynxLength 36 42 0105 78 4 46 0125 130 25 92 0314 86PharynxLength 36 126 59228 32 4 149 120175 19 25 170 70230 26Width 36 83 38157 42 4 92 85100 7 25 139 50205 34EsophagusLength 36 16 0114 162 4 0 00 0 25 43 0113 93ANTVIT 37 655 3131,112 34 4 695 654763 7 22 1,044 3442,300 45ACEVIT 37 14
Ϫ
153240 695 4
Ϫ
82
Ϫ
145–36
Ϫ
56 23
Ϫ
22
Ϫ
264–383
Ϫ
735Egg number 37 8 090 208 4 7 017 109 25 22 0101 141EggsLength 68 82 53105 11 4 95 9298 3 67 98 75113 7Width 68 45 3260 16 4 49 4452 7 67 55 3674 13
* N; total number of specimens;
n;
number of measurements. All data is rounded to the nearest
m.
DC; USNPC69744 (2 specimens) from
D. virginiana
, Florida;USNPC75092 (1 specimen) from
D. virginiana
, Leon County,Florida; USNPC8548 (1 specimen) (paratype) from
D. virgi-niana
, Houston, Texas.
 Rhopalias caballeroi
(37 specimens total): FUK264-1 (1specimen), FUK311 (9 specimens), FUK584 (2 specimens)(paratypes) from
D. marsupialis
, Huanuco, Peru; HWML70021(8 specimens) from
P. opossum
, Santa Cruz Department, Bo-livia; HWML35933 (3 specimens) from
C. minimus
, Panama;UNMSM1076 (5 specimens) (paratopotypes) from
P. opossum
,Huanuco, Peru; UNMSM1077 (1 specimen) (paratopotype)from
D. marsupialis
, Huanuco, Peru; HWML70014 (1 speci-men) from
L. crassicaudata
, Berisso, Argentina; UNAM4081(1 specimen) from
Didelphis
sp., Veracruz, Mexico; UNAM965(1 specimen) from
D. marsupialis
, Venezuela; USNPC92124 (5specimens) from
P. opossum
, Colombia.
Description with translation—original fromLamothe-Argumedo (1979)
Original description: Rhopalias
(Diesing, 1850) Stiles andHassall, 1898.

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