Impact of a castrating trematode, Neophasis sp., on the common whelk, Buccinum undatum, in the northern Gulf of St. Lawrence

11 Pages·2000·4.2 MB·English

by  F Tetreault

Reference: Bio/. Bull. 198: 261-271. (April 2000)
Impact of a Castrating Trematode, Neophasis sp., on
Common
the Whelk, Buccinum undatum, in the
Northern Gulf of St. Lawrence
FRANCOISE TETREAULT1. JOHN H. HIMMELMAN1 *, AND LENA MEASURES2
lDepartement de biologic and GIROQ (Groupe interuniversitaire de recherches oceanographiques du
Quebec), Universite Laval. Quebec City, Quebec, Canada G1K 7P4; and 'Fisheries and Oceans
Canada, Institut Maurice-Lamontagne, Monl-Joli, Quebec, Canada G5H 3Z4
Abstract. We observed heavy tremutode infections of Lauckner, 1986), and gigantism and modifications of sec-
whelks, Buccinum undaium, from the Mingan Islands, east- ondary sexual characteristics may also occur (Rothschild,
ernCanada, by larval stages ofaspecies ofNeophasis. Only 1936, 1941; McClelland and Bourns, 1969; Mouritsen and
sexually mature whelks were infected, 23% of mature fe- Jensen, 1994; Gorbushin, 1997). Because castrating para-
males and 15% of mature males, and prevalence increased sites may decrease the number of breeding individuals
rapidly with whelk si/,e. In most cases the parasite com- within gastropod populations (Kuris, 1973, 1974; Lauckner,
pletely occupied the gonad, causing castration. The diges- 1986), infected populations may show declines or strong
tive gland wasalso infected, although toalesserdegree (0% fluctuations in abundance (Lie, 1973; Combes, 1982;
to 50% occupation), and a marked reduction in the mass of Lauckner, 1986; Huxham et ai, 1993; Lafferty. 1993).
the penis was associated with the infection. A decrease in K0ie (1969) identified fourcastrating larval trematodes in
the proportion of whelks with a highly infected digestive a Danish population of the common whelk, Buccinum iiu-
gland between May and August 1994 suggested mortality of datum L. 1758: (I) Zoogonoides viviparus (Olsson, 1868)
infected individuals. Whelks held for 12 to 15 months in the Odhner, 1902; (2) Neophasis anarrhichae (= N. lagenifor-
laboratory retained the infection but did not show significant niis) (Nicoll, 1909) Bray, 1987; (3) Cercaria buccini (Le-
mortalities (possibly because food was abundant and pred- bour, 1911); and (4) an unidentified species of Renicola,
ators absent). The larval stage of Neophasis sp. found in Cohn, 1904. The first three are found in both the gonad and
whelks was a cercaria; however, the tail easily detached. digestive gland and the fourth only in the digestive gland.
The putative infective stage (metacercaria) was not ob- Infections by Z. viviparus and N. anarrhichae result in a
served but may be present in whelks in late winterand early light grey appearance of the infected organs, whereas C.
spring. Other trematode parasites observed were adult buccini does not affect the color of the infected organs
Steringophorusfurciger in the stomach and larval Renicola (Lebour, 1911), and Renicola sp. forms light yellow bodies
sp. in the digestive gland. in the digestive gland. Other parasites ofB. undatum iden-
tified by K0ie (1969) are the turbellarian commensal Graf-
Introduction filla buccinicola (Jameson, 1897), found in the digestive
gland and stomach, and the trematode Steringophorusfur-
Parasitic castration is the partial or total inhibition of ciger (Olsson, 1867) Odhner, 1902, present only in the
gametogenesis of a host species due to the activity or stomach. Hamel (1989) observed larval trematode parasites
physical presence of a parasite (Cheng. 1983). Many larval in the gonadanddigestive gland of 15% ofadultB. undatum
trematodes castrate their gastropod hosts (Cheng, 1964; in the Mingan Islands, Gulf of St. Lawrence, eastern Can-
ada, and indicated that the characteristics of the infection
were similar to those described by K0ie (1969) for Z.
Received 12 November 1998; accepted 8 December 1999.
*To whom correspondence should be addressed. E-mail: John. viviparus and N. anarrhichae.
[email protected] In ourstudy we identified one trematode in B. undatum as
261
262 F. TETREAULT 7 AL
belonging to the genus Neophasis, which has lile cycles velop and mature to the adult stage and thus permit identi-
involving one or two intermediate hosts (gastropod, lish) fication to species.
and a teleost final host (Bray and Gibson. 1991 ). Caudate
cercaria develop in the gastropod, become l"ree-li\ing. and Materials and Methods
encyst as metacercaria in bivalve molluscs and tish that are We sampled whelks from the Mingan Islands (50 35' N,
later preyed upon by the final fish host. In \cnpliasis anar- h> vV Wi. in the northern Gulf of St. Lawrence (Fig. 1).
rhichae. B. undatum apparentlv ser\es as the onlv obligate Using scuba, we collected all whelks (buried and unburied)
iinnttehremewdhiealtkes.hoTsht.eCcearucdaaritaelcteairlcaisrisahceddewvietlhoipn twhiethriendiar.edainade twhiatthimneasurmedof10eitotheIr10simdme oifn sthewlol lHeinOgt-hmanldonwgerteranfsoeucntds
1
the noncaudate cercaria is considered a metacercaria thai parallel to the shoreline at Cap du Corbeau on Me du Havre,
does not encyst (Koie. 1973). l-'inal hosts are carnivorous one at 6 m and the other at 15 m in depth. Whelks were
teleosts belonging to the genus Anarhichas. which acquire abundant on the sediment bottom in this area. We collected
the parasite by preying on infected whelks. Encysted meta- ;:7 whelks in May 1994 and 313 in August 1994.
cercariae of an unidciitilied Xfophasis have been reported All whelks were fro/en, and later dissected to identify
on the mesenterv of American plaice. Hippoglossoides plu- and determine the prevalence of parasites. After measuring
tessoides. and in the gut of Atlantic cod. Gudu.\ morhua, the shell length of each animal, we fragmented the shell
from Canadian waters (Appy and Burt. 19X2). Brav and with a hammer to remove the soft tissues intact. Then, the
Gibson ( 1991 ) indicated that this immature trematode mav gonad. penis, remaining reproductive organs, digestive
be Neophasis burti Bray and Gibson. 1991. gland, and other body components were separated and
Biiccinum undatum is the most abundant carnivore in the weighed (after draining on paper toweling for 1(1 mm). A
henthic community in the Mingan Islands in the northern dissecting microscope was used to examine each organ tor
Gulf of St. Lawrence (Jalhert a <//.. 1989: Himmelman. parasites. In examining the gonad and digestive gland, we
1991). It is alsoofcommercial importance in the GulfofSt. pressed the tissues between two 7.5 X 7.5 cm glass plates to
Lawrence and St. Lawrence Estuary. From 1991 to 1993. facilitate the search for parasites, and visually estimated the
700 metric tons of whelks were harvested annually in Que- proportion of the organs occupied by parasites (the larvae
bec and 30% of this harvest came Irom the Mingan Islands were too abundant to he counted). Samples of larvae found
AFA
(Savard, 1994). in each infected whelk were isolated and preserved in
Several characteristics of the biologv of the common
whelk make it especially vulnerable to lisherv over-exploi-
tation. First, recoloni/ation of over-exploited sites is likely
to he slow because the whelk lacks a pelagic larval stage
and adults move only by crawling. Further, stocks arc-
limited by a slow growth rate. In the Mingan Islands,
whelks attain a shell length of 75 to SO mm. the si/e at
sexual maturity, in 6 to 8 y (Martel ci <//.. l9Sd; Savard.
1994). At present the fishery is not limited In a minimal
capture size. In 1993. 25',, of whelks collected measured
-"75 mm (Savard. 1994) and thus had not reproduced. A
decrease in the average si/e of harvested whelks has been - sir11,'
recorded in several fisherv /ones and mav indicate over-
exploitation. Although such a decrease has not yet been
observed in the Mingan Islands, it is likely to happen given
the intensity of the fishery. - 50 14'
The objective ofourstudy was to identify parasites ofthe
common whelk. Biiccinum umlatiim. in the northern Gull ol
sSta.mLpalewdrenaclearagnedntuomebvealruaotfewthheeilrkismpdaucrtinognttwheowpheerliko.dsWem - SO 12'
summer 1994 to determine the prevalence ofparasites (pro
portion of whelks infected) and to quaniil\ their effects on
differeni bod organs to addition, we studied morphologi-
cal changes in parasites over time in the lahoi.iioiv finally, h.T4(V h.T>30'
weexposed AmnK .m plaice to larval Neophasis sp. from H 1- Location ofthe study site. Cap du Corbeau. in the Minjian
undalum to determine whether larval Neophasis would de Islands in the northern dull ol Si. Lawrence. Canada.
CASTRATING TREMATODH OF WHKLKS 263
(a solution of alcohol, formalin, and acetic acid; Pritchard al.. 1986) were used since parasites were absent in imma-
and Kru.se, 1982) for later identification. ture whelks. Because the proportion of the gonad and di-
We identified parasites togenus based on the morphology gestive gland occupied by parasites varied markedly, dif-
ofdifferent stages. Preserved parasites were examined with ferent categories were used for the two organs: 0%-90%
a microscope, first without staining and then using Schei- and90%-100% classes forthegonad andfour25% classesfor
der's acetocarmine stain (Pritchard and Kruse, 1982). Fur- the digestive gland. All statistical analyses were performed
ther, to obtain the adult stages required for species identi- using the BMDP4F statistical program (Dixon, 1985).
fication of larval parasites from the gonad and digestive We compared the somatic mass and shell length of the
gland, we attempted to infect American plaice, Hippoglos- parasitized and nonparasitized whelks with a Mann-Whit-
soides platessoides, which is a host for several trematodes ney 11 test. To eliminate the confounding effect of parasit-
(Bray and Gibson, 1991). Plaice, measuring 15 to 20 cm in ismon reproductive organs and the digestive gland, we used
total length, were collected in June 1994 by trawling at a eviscerated mass, defined as the total mass minus the mass
depth of53 m near Matane (48 53' N, 67 19' W) in the St. of the digestive gland, gonad, penis, and remaining repro-
Lawrence Estuary. In November 1994, using forceps, we ductive organs. Given the slow growth of whelks, we as-
placed pieces of infected gonad, from freshly killed whelks sumed that there was no impact of sampling period on
(collected in the Mingan Islands in October 1994), into the eviscerated mass and shell length and therefore pooled the
stomachs ofsix plaice. The plaice were first anesthetized by May and August samples for the analyses.
placing them for 1-3.5 min in 2 1 of seawater containing Because the number ofopercular striae can be used as an
0.3 g of tricaine methanesulfonate (MS-222). Following estimate of age of B. imdatum (Santarelli and Gros, 1985),
treatment, the plaice were kept in well-oxygenated waterfor we used these striae to evaluate whether the age ofinfected
24 h to recuperate. The six exposed plaice were maintained and nonint'ected whelks was different. We compared the
at 25%cto 28%f salinity and 4.4 to 10.4"C for 10 to 20 d in number of operculum striae of infected and noninfected
a 130-1 tank at the Maurice-Lamontagne Institute. Four whelks using Mann-Whitney U tests.
other nonexposed plaice, which served as controls, were To evaluate the effect of parasites on the penis, we com-
maintained underthe same conditions in another 130-1 tank. pared penis mass of infected and noninfected whelks, in May
After 10 to 20 d, the plaice were killed by cervical dislo- and again in August, using Mann-Whitney U tests. To deter-
cation, dissected, and examined for intestinal trematodes. mine the effect of the parasite on penis mass, we first deter-
We also examined changes in parasitic infections over mined the regression ofpenis mass to shell length for nonin-
mm
time in 80 whelks measuring 80-110 in shell length. fected whelks and then calculated the deviation in penis mass
These specimens were collected in October 1994 from of infected whelks compared to this relationship. As the dis-
along the same two transects at Cap du Corbeau. and using tribution ofresiduals wasnormal, aStudent'sttestwas usedto
the same methods, as in May and August. These whelks test the hypothesis that the mean ofthe residuals was equal to
were maintained at 25%<>to 28%c salinity and 4.4 to 10.4C (Zar, 1984); a value different than (P < 0.05) would
in two 130-1 tanks until January 1996. Using the technique indicate that the parasite affected penis mass.
described above, we examined a first sample of 30 whelks
in November 1995 and a second sample of 45 whelks in Results
Jaannduwareyre19f9r6o.zeFnifvoerwlhaetelrkesxdaimeidnadtuiroinn.gWtheisrleacboorrdaetdortyhestsuidzye Identification ofparasites in the gonad and digestive
gland
ofcercariae and rediae in whelks collected from the field in
May and August 1994, and from the laboratory sampling in Our examination ofwhelks collected in May and August
November 1995 and January 1996, from images projected 1994 in the Mingan Islands revealed that cercariae and
through a drawing tube attached to a Leitz diaplan (X40) rediae of one species of trematode infected both the gonad
microscope using a digitizer and computer (using Sigma- and the digestive gland. The cercariae possessed an oral
scan image analysis software, version 3.90; SPSS Inc., sucker at the anterior portion of the body and a ventral
Chicago, IL). sucker in the middle of the body (Fig. 2A). They also
To evaluate the influence of sex and sampling period possessed a straight, nonfurcate tail and eyespots located
(May and August) on the prevalence ofparasites in gonadal anterolateral to the oral sucker. Rediae had only an oral
and digestive gland tissues, and on the proportion of these sucker and a small pharynx in the anterior portion of the
organs infected, we applied log-linear models adjusted to body (Fig. 2B). The shape of the cercariae varied in differ-
three-dimensional contingency tables (Legendre and Leg- ent seasons. Cercariae were most elongated in August 1994
endre, 1984). Only significantmodels were retained, and the (mean length = 395 /urn; mean width = 70 jam) and least
best model describing the data was determined using the in January 1996 (mean length = 199 jam; mean width = 98
partitioning method. For the analysis of prevalence, only jam). The tail was easily detached in May but not on the
mm
sexually mature whelks (>75 in shell length; Martel et other dates. Rediae were cylindrical and less variable in
264 i 11 iKI \i i I 1.1 \i
(Table 1 ) testing the effectofsex (S) and sampling date (M)
on prevalence (P) were significant (a = 0.05): of these.
Model B. InE = P + S + M + SM + PS, bestdescribed the
data (Table I ). This model indicated that only sex influ-
enced prevalence. Female whelks were more infected (/'
0.05) by larval Neophasis sp. than were males (22.9', \ <,
15.4%). In both sexes, prevalence markedly increased with
increasing whelk si/.e and exceeded 90% for whelks mea-
suring more than 90 mm m shell length.
The infected whelks were the largest (Figs. 4. 5I and also
seemed to be oldest (Fig. 5). Shell length was greater for
infected than noninfected whelks (Fig. 5: females: U
14.02. n = 2IS. P < 0.001: males: U = 12.40. n = 24d.
P < 0.001 ). and the same trend was indicated for eviscer-
ated mass, although it was significant only in males il-ig. 5:
females: U == 1.3. ;i - 218. P = 0.25: males: U = 6.96. ;,
246, P = 0.01). Finally, the number of operculum striae
tended to be greater for infected than noninfeclcd whelks
(Fig. 5: females: U = 4.98. n = 77. P = 0.026: males: /
3.69. n = 73. P = 0.055).
/.//(i !. nl Neophasis sp. on the whelk
' 1. Stages n! the trematode \ii>i>hini\ sp. from live tissuo <it
the whelk Buccinum umtatum. (Top) A cercaria with e\es and a straight. In all eases, the gonad was the organ most infected by
nonfurcate tail. (Bottom) A redia containing several cereanae. larval Neophasis sp. (Fig. 6). None ofthe models testing the
influence of sex and sampling date on the proportion ofthe
gonad occupied by parasites were significant. Thus, no
shapeovertime than cercariae. They were longest in August differences between females and males or between the two
1994 (mean length = 2190 /urn) and shortest in November sampling periods were indicated. In 97% of infected
1995 ( 1325 /nm). In May anil August 1994 some rediae did whelks, cercariae and rediae occupied more than 90% ofthe
not contain cercariae. whereas in November 1995 and Jan- gonad. The one individual \vHh a lowerportion ofthe gonad
uary 1996 all contained cercariae. infected by larval Neophasis sp. (20%) was a male collected
The presence in the cercarial stage ofeyes at the anterior in August 1994 (Fig. 6).
portion ofthe body and a straight, nonfurcate tail placed this The proportion of the digestive gland infected with cer-
parasite in the genus ,\c/>i>h,i\i\ iStation!. 1904). Our iden- canae and rediae was much lower than for the gonad and
tification to genus was confirmed by Dr. K. A. Bray at the exceeded 50% in only a few whelks (Fig. 6). Two log linear
British Museum of Natural History London (pers. comm.). models (Table 1 ) testing the effect ofsex and sampling date
We found no adult Neophasis in the digestive systems ofthe on the proportion of the digestive gland occupied by the
=
American plaice (Hippoglossoidesplatessoides) that we had parasite were significant (it 0.05). and the partitioning
attempted to infect, and thus we could not identify the method indicated that Model B. InF. = O + S + M +
species of Neophasis. OM + SM. best described the data ('fable I). This model
In noninfected whelks, the gonads were yellow to orange indicated that only sampling period influenced the propor-
in color, and the digestive gland was brown (Fig. 3A. Bi In tion of digestive gland occupied by the parasiie. The pro
contrast, the gonad and digestive gland of whelks inlected portion of the digestive gland occupied by larval Neophasis
with larval Neophasis sp. were light grey (Fig. 3C. Di. sp. in infected whelks dropped between May and August
owing to the color of the cercanae and rediae that replaced (Fig. 6). Forexample, 45'< ofthe infected whelks had more
thetissues. LarvaeofNeophasis sp. were alsofound in other than 25% of the digestive gland infected in May compared
reproductive organs the albumin gland of females and the to 8% in August
seminal vesicle ol males. In both May and August, the regression of penis mass to
shell length was positive for noninfected males (Fig. 7;
Prevalent < "I \eophasis \/>. in \\helk\ in the /iclil 0M.a2y9:, nP=<1202..00r1 i. b0i.n26.th/e' me0a.n001r;esAiudguualst:pe;n;i=s 9m3a,ssr2 of
Larvae of Neophasis sp weie present only in sexually infected whelks compared to the regressions for noninfected
mm
mature whelks (Fig. 4). Three of the log linear models whelks differed I I) (May: n = 21. / -- 18.514. /' -
CASTRATING TREMATODE OF WHELKS 265
Figure 3. Whelks. Biucinimi unilutiiin. with the shell removed. The gonad (g) is clearly distinct from the
digestive gland (dg) in the uninfecied female (A) and male (B) because ofdifferent coloration, whereas these
organsarelesseasily distinguished in the infectedfemale (Cl and male (D) becauseofsimilarcoloration(light
grey). Note the strong atrophy ofthe penis (p) ofthe infected male (D).
0.001; August: n= 18. t= -6.427, P < 0.001). Penis mass from the field. In January 1996. after 15 months in the
was markedly smaller for infected males (Fig. 7). laboratory. 17.4% of females (4/23) and 4.5% of males
( 1/22) were infected. The prevalence ofNeophasis sp. in the
Neophasis sp. infections in whelks in ilie laboratory laboratory whelks (dissected in November 1995 and Janu-
Whelks sampled from the laboratory in November 1995. ary 1996) tended to be greater for females than males, but
after 12 months in captivity, had larval Neophasis sp. in not significantly so (Fisher exact probability test, P =
20.0% offemales (3/15) and 0% ofmales (0/15). In one of 0.056). For females, the prevalence in the laboratory was
the three infected females, larval Neophasis sp. had invaded similartothat in the tield sampling (G = 0.39, n = 261, P =
the gills and mucus gland tissues, a condition never ob- 0.53), but was lowerfor males (Fisherexact probability test,
served in the whelks collected in May and August 1994 P = 0.039). Five whelks died during captivity, and three of
266 REAULT 7 AL
I 11 I
100
-|
(7,10)
80-
60-
40-
(48,71)
J
20-
(300,,5577))
(5,0) (5,3)(15,4) (7,9) (3,8) (4,2) (10,8)[~j| |
I
100 O
(6,4)
80-
CASTRATING TREMATODE OF WHELKS 267
50n
-2P 45-
H
268 K TtTREAULT AL
Prevalence ofNeophasis sp.
I wo hypotheses may explain the increased prevalence of
O non-infected lar\al Neoplwsis sp. with increasing si/e for sexually ma-
ture whelks (Figs. 4. 5). First, larger whelks may be more
infected frequcntK infected because thes have been exposed to
parasites for a longer time. Second, castrating trematodes
eliminate energetic demands tor reproduction and thereby
mas increase the growth rate of somatic tissues, a phenom-
ena known as gigantism (e.t;.. Rothschild. 1936. 1941: Mc-
Clelland and Bourns. 1969; Mouritsen and Jensen. 1994:
Gorbushm. 1997). That the number ofopercular striae was
greater on infected whelks than on noninfected ones (Fig. 5)
0o. '^August suggests that the infected whelks were older, which is
consistent with the first hypothesis. It this is true, the hy-
pothesis ofgigantism is not necessars to explain the positive
relation between size and infection rate. Nevertheless, a
comparison of growth rates of infected and noninfected
whelks ofsimilarsize is needed to provide a more direct test
of the gigantism hypothesis.
Giganiism has been reported primarily in short-lived gas-
tropods (Sousa. 1983). Long-lived species, such as H. nn-
ilniiiin. mas devote more energs to tissue repair and may
thereby be less likely to display giganlism when parasitized.
75 80 85 90 95 100 105 110 In whelks in the Mingan Islands, the energy required to
Shell length (mm) rNee<p>aii>rludiaM\madgigeestmaeyxtrhaecohripgorhalbleycaaunsdelattheer arebdsioarlbshtoasgtesmao-f
Kitiiire7. Relationofpenismasstoshell length for\\helkx. Hunnuiin terials through the mouth or tegument (Koie. 1971). Thus,
undatum, infected (dark circles) and noninfected (opirn circlesI h\ the rediae mas require more energs from their host than spo-
trematode Neophasis sp. in samplescollected in M.i> and August 1994. rocysts that absorb nutrients through the body wall without
damaging host tissues (Sousa. 1983: Vernherg and Vern-
berg. 1974). The effect of parasitic castration on the growth
rate of infected individuals mas further depend on host
Gibson. 1991). and all of the above-mentioned families of population density and parasite species. For instance. Gor-
fishes are present in the Mingan Islands (Thomas and Him- bushm 1997) found that the growth rate of Hydrobia \TII-
melman. 1988). Whereas members of [he genus Nco/ilumis irMi le(nds to be stunted by the parasitic tremalode Kuno-
have been reported from American plaice from the North ciiivli' pni^eneticn when host density is high, but is
Atlantic (Bray and Gibson. 1991 ). none ha\e been reported significantly increased when host density is low. In contrast,
in American plaice or other lishes from the Gulf of St. under held conditions, tremalode species from the families
Lawrence (Scott. 1975). However. Nenplmsis sp. is reported Nocotylidae and Bunocoislidae have no effect on the
from cod from the southern Gulfof St. Lawrence, although growth rate ofllnlrohiu ulvae and //. ventrosa (Gorbushm.
infections were pmbabls accidental (Appy and Hun. I9S2).
1997).
According to K0ie (1973). pleuronectiforme lish mas ac- We observed a higher prevalence of Neophasis sp. in
quire N. anarrhichtic. but the parasites do not mature and female whelks than in males in Mas and August 1994 (Fig.
infections are lost within a few days. 4). Hughes and Answer (1982) found a similar difference
The persistence of larval Neophasis sp. in whelks col- between female and male Liitoriim litlorca infected by
lected in October 1994 and maintained in the lahoratois lor trematodes. Our understanding of presalence patterns is
12 to 15 months suggests that the parasite persists in the restricted In the limited knowledge of hoss Neophasis
whelk lor long periods. Similarly. K0ie (1969) sampled muacidiae infect whelks and of the resistance of whelks to
whelks lor 12 consecutive months and concluded that the infections. Possible explanations are that females ( I ) are
parasn : in all seasons. Although we did not observe more exposed to the parasite because their actisiiies differ
tailless cercariae (metaccrcariae) during our study, this in- liom those of males (e.t>.. egg laying: feeding rates possibly
fective sta- present in whelks during late winter or vary because of greater reproductive investment. Martel ci
early spring. ui. 1986). (2) are less resistant to infections, or (3) retain
CASTRATING TREMATODE OF WHELKS 269
infections for a longer period. A greater prevalence of Otherparasites
Neophasis sp. in females than in males was furtherobserved The genus Renicola was identified in the digestive gland
in the sample collected in October 1994, which was main- of a small proportion of whelks in our study and in that of
tained in the laboratory. K0ie (1969). The sporocysts (with cercariae) of the genus
Renicola infect the digestive gland and gonads of gastro-
pods, causing castration and. in massive infections, death
Effects ofNeophasis sp. on the whelk (Stunkard. 1964). Gastropods are the first intermediate host,
and cercariae leave through the gills to encyst in the gill
In the Mingan Islands, Neophasis sp. is strongly associ- tissue of bivalves.
ated with gonadal tissues ofsexually mature whelks. In this Steringophorus fitrciger is a trematode parasite usually
respect, it is similar to the trematodes infecting the gastro- found in the stomach of flatfish (Scott, 1975: Bray and
pod Littoriiui littorea (Hughes and Answer. 1982). In con- Gibson, 1980; Scott and Scott. 1988). It feeds on the host's
trast, in Denmark, Neophasis anarrhichae infects the diges- food, and the intensity of the infection can exceed 100
tive gland of immature whelks as well as the gonad and parasites perhost individual (Polyanski, 1955). K0ie (1969)
digestive gland of mature individuals (K0ie, 1969). Studies considered its presence in the stomach ofwhelks accidental
are needed to elucidate why Neophasis sp. is absent in the and related to the similar use of food resources by whelks
digestive gland of immature whelks in the Mingan Islands. and flatfish. It likely has little effect on whelks from the
In both sampling periods, the gonads of infected whelks Mingan Islands because of its low intensity ( 1 1 parasites
were almost completely occupied by the parasite (Fig. 6). per host).
This strongly suggests rapid proliferation of the parasite Of the four trematodes infecting Buccinum undatiini in
once inside the host. In contrast, the digestive gland was the Mingan Islands, Neophasis sp. clearly has the greatest
much less infected, and percentage occupation decreased effect on its host. Although the prevalence of Steringopho-
markedly from May to August in both sexes (Fig. 6). The rus fiirciger was similar to that ofNeophasis sp., it caused
decrease could be due to either tissue repair or mortality of little or no tissue damage and did not invade the gonad.
infected whelks. K0ie (1971) observed high mortalities of Even though Renicola sp. clearly damaged the digestive
whelks infected with N, anarrhichae, suggesting that the gland of whelks, its effect on the population is probably
animals eventually die from infection. This is also sug- negligible owing to its low prevalence. In contrast, Neopha-
gested by the massive tissue damage caused by Neophasis sis sp. likely markedly affects whelk populations in the
and because scars, which would indicate healing, have not Mingan Islands, given that it castrates large numbers of
been observed (K0ie, 1971. this study). That we observed mature individuals.
no mortality ofinfected whelks kept in the laboratory for 1? In undisturbed populations, the relationship between host
months might have been because food was abundant and andcastratingparasites normally attains an equilibrium over
predators absent. A number of studies demonstrate a nega- time, as in prey/predator interactions (Curio. 1988). Addi-
tive effect oftrematode parasites on gastropods when envi- tional pressures on host populations, such as those likely to
ronmental conditions are unfavorable (Vernberg and Vern- be caused by a fishery, potentially destabilize such relation-
cbaesrtgr.at1i9ng63,tre1m9a6t7o:deSsouasrae aknndowGnleatsoonc.aus1e989d)e.athanodfstohemier Nsheioppsh.aDseisstaibnitleirzaacttiioonn ibsecaasutsreonbgotphosstihbeilciotmymfeorrctihaelwwhheellkk/
hosts (Stunkard, 1964: Lauckner. 1986). Mortality could be fishery and Neophasis infections reduce the numbers of
due directly to the parasite or indirectly to predation. Po- reproducing whelks.
tential predators of adult whelks in the Mingan Islands are
Acknowledgments
numerous and include the asteroids Leptasteriaspoluris and
Asrerias vulgaris (see Dutil, 1988); the common eider, We thank C. Berger. S. Blanchet. M. C. Giasson, P.
So/nateriii mollissinm (see Guillemette ettil.. 1992); and the Girard. and M. Vaugeois for their help in field and labora-
wolffish, Anarliichas lupus. tory work. We are grateful to D. J. Arsenault, S. Morissette.
Both our study and that of K0ie (1969) show that an and R. Rochette for valuable discussions and precious help
atrophy of the penis is associated with the presence of during the preparation of the manuscript. This study was
castrating trematodes in Bucciniim itndiitum (Fig. 7). This supported by an NSERC operating grant to John H. Him-
probably results from the destruction of the gonad, which melman.
produces sexual hormones (Caullery, 1950). The high de-
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