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Schistosoma mansoni, Echinostoma lindoense, and Paryphostomum segregatum: Interference by trematode larvae with acquired resistance in snails, Biomphalaria glabrata
EXPERIMENTAL PARASITOLOGY 42, 343-347
(1977)
Schistosoma mansoni, Echinostoma lindoense, and Paryphostomum segregatum: Interference by Trematode Larvae with Acquired Resistance in Snails, Biomphalaria glabrata K. J. LIE AND D. HEYNEMAN The G. W. Hooper Foundation, University of California, San Francisco, California 94143, U.S.A. (Accepted
for publication
18 February
1977)
LIE, K. J., AND HEYNEMAN, D. 1977. Schistosoma mansoni, Echinostoma lindoense, and Paryphotiomum segregatum: Interference by trematode larvae with acquired resistance in snails, Biomphalaria glabrata. Experimental Parasitology 42, 343-347. Many juvenile albino Biomphalaria glabrata snails with an acquired resistance to Echinostomu lindoense again became susceptible to this trematode parasite following infection with either of two Payphostomum segregatum or Schistosoma mansoni. Previous other larval trematodes, studies have shown that trematode sporocysts are capable of interfering with juvenile and adult natural resistance to S. mansoni. We propose that a common mechanism is present that allows both juvenile and adult natural resistance and acquired resistance to trematodes in B. glabrata to be reduced strikingly by the simultaneous presence of trematode larvae in the snail host. INDEX DESCRIPTORS: Schistosoma mansoni; Echinostoma lindoense; Paryphostomum segregatum; Echinostoma parasnsei; Trematode; Biomphalaria glabrata; Snail; Acquired resistance; Natural resistance, snails; Trematode antagonism; Interference with snail resistance.
Recent studies have shown that the concurrent presence of any of several trematode larvae can interfere with the natural ( genetic) resistance of Biomphuhwia g&zbruta snails to certain trematode parasites. Echinostoma lindoense sporocysts developing from irradiated miracidia normally are rapidly encapsulated in the snail heart. However, in snails that also harbored normal sporocysts of the same species, the irradiated sporocysts were protected from encapsulation. In snails harboring ScMstosoma mansoni or Paryphostomum segregaturn, encapsulation of irradiated E. lindoense was delayed (Lie, Heyneman, and Jeong 1976). Most B. glubrata snails of a strain naturally resistant to S. munsoni became susceptible to this parasite when infected first either with Echinostoma para-
ensei, E. Mndoense, or E. liei (Lie, Heyneman, and Richards 1977). The present experiments were designed to determine whether or not a concurrent trematode infection is also able to interfere with acquired resistance in B. glaabrata, as it did with natural resistance (Lie, Heyneman, and Richards 1977). MATERIALSANDMETHODS
The parasites (Schistosoma mansoni laboratory strain, Echinostoma lindoense, and Payphostomum segregatum), snails (juvenile NIH albino BiomphaZuria glabruta from our laboratory stock) methods of exposure of snails to miracidia, irradiation of miracidia, and maintenance of snails have been described in previous papers
343 Copyright All rights
0 1977 by Academic of reproduction in any
Press, Inc. form reserved,
LSSN
0014-4894
344
LIE AND HEYNEMAN
and Kostanian 1975a; intervals used in the present experiments, (Lie, Heyneman, Lie, Heyneman, and Lim 1975b; Lie and it was unlikely that migrating sporocysts Heyneman 1975). Juvenile snails, 2 to 3 of E. lindoense were consumed by P. segmm in diameter, were sensitized to E. regatum rediae before E. lindoense could reach the heart. All snails in our experilindoense by exposing each to 10 irradiated miracidia. Each snail was then reexposed ments were examined daily under the disto 10, 20, or 50 normal S. mansoni, or to secting microscope for E. linduense sporostarting 30 hr five normal P. segregatum miracidia, 1 to cysts in the ventricle, 3 days after destruction within the venpostexposure. In cases of doubt as to the tricle of the irradiated E. lindoense sporoidentity ‘of the larvae in the ventricle, i.e., whether they were sporocysts of E. lindocysts, which could be observed through ense, small rediae of P. segregatum, or the shell under the dissecting microscope. Since destruction of the E. lindoense sporoboth, the snails were dissected and the cysts by capsule formation took place be- hearts were examined. E. lindoense is a weak antagonist to S. tween 3 to 9 days postexposure in this group of experimental snails, reexposure to mansoni, capable of consuming primary, S. mansoni or P. segregatum was done 4 but apparently not easily, destroying secondary, S. mansoni sporocysts (Lie, Heyneto 12 days after the initial exposure to irradiated E. lindoense. The snails were man, and Richards 1977). With the expoagain reexposed, this time to 50 normal sure intervals we employed, using relatively E. lindoense miracidia. The interval be- large numbers of S. mansoni miracidia, there was little possibility that all developtween first and second reexposure varied from 1 to 6 days. Two sets of control snails ing primary S. mansoni sporocysts would were used for each experiment. One con- be consumed by E. lindoense rediae before sisted of snails sensitized to E. lindoense secondary S. mansoni sporocysts could be formed. In general, this possibility was less with the same batch of miracidia used to sensitize the experimental snails, but not with longer exposure intervals, which allowed more time for secondary S. mansoni reexposed to S. mansoni or P. segregatum. They were reexposed only to the 50 norsporocysts to develop. Therefore, when the mal E. lindoense miracidia, along .with the two trematodes were given simultaneously experimental snails. The second set of con- or when an interval of only 1 to 3 days trols consisted of previously uninfected separated them, experimental snails were snails, of the same size and strain as the each exposed to 50 S. mansoni miracidia. experimentals, exposed only to 50 normal With longer intervals between exposures, E. lindoense miracidia. 20 or, rarely, only 10 S. mansoni miracidia P. segregatum is a strong predator of were used. Periodic checking of the snails E. lindoense (Lie, Basch, Heyneman, and for presence of primary and secondary S. Fitzgerald 1968). With the intervals be- mansoni sporocysts and E. lindoense was tween the reexposure to P. segregatum and carried out routinely, and all snails were dissected 30 to 32 days after exposure to the following reexposure to E. lindoense S. mansoni. that were used in these experiments, the E. lindoense larvae were able to survive RESULTS for varying periods in the ventricle before being attacked and consumed by P. segreThe results (Tables I and II) show that gatum. In general, the longer the period both Schistosoma mansoni and Paryphostobetween reexposures, the further developed mum segregatum are able to interfere with was the P. segregatum, and the shorter the an acquired resistance to Echinostoma E. lindoense survival. However, with the lindoense in Biomphalaria glabrata, render-
TREMATODE
INTERFERENCE
WITH
TABLE Interference
Number of snails positive for both parasites
345
RESISTANCE
I
with Acquired Resistance to Echinostoma lindoense in Sensitized Biomphalaria glabrata by Paryphostomum segregatum
Interval between 2nd and 3rd exposures (days)
Number of snails
SNAILS’
Number of snails positive for P. segregatum only
Number of snails positive for E. lindoense only
Juvenile
Number of snails negative for both parasites
25 25” 96
0
3
15
1 19 0
6 6 9
68 68= 31b
1
7
41
0 57
20 11 30
154 155= 83b
2-6
44 (42%)
61 (58%)
4 149 6 (7%)
45 6 77 (93%)
a Nonsensitized control snails exposed only to 50 E. Zindoense miracidia. b Sensitized control snails exposed to 50 E. lindoense miracidia.
soni was required before some of the snails again became susceptible to E. lindoense. However, even a simultaneous exposure to P. segregatum and E. Mndoense produced a breakdown of acquired resistance to E.
ing the snails again susceptible to the latter parasite. P. segregatum may be slightly more efficient than S. munsoni in reducing the snail’s acquired resistance. An interval of 1 day or more after exposure to S. manTABLE Interference
II
with Acquired Resistance to Echinostoma lindoense in Sensitized Biomphalaria glabrata by Schistosoma mansoni Number of snails positive for both parasites
Number of snails positive for X. mansoni only
Number of snails positive for E. lindoense only
Juvenile
Number of snails
Interval between 2nd and 3rd exposures
35 35a 24”
0
0
35
0 35 23
0 0 1
47 47” 316
1
6
32
0 47 2
9 0 29
30 305 16b
2
2
19
0 29 0
9 I 16
228 2505 1135
3-6
101 (47%)
114 (53%)
a Nonsensitized control snails exposed only to 50 E. Zindoense miracidia. b Sensitized control snails exposed to 5; E. lindoense miracidia,
0 232 11 (10%)
Number of snails negative for both parasites
13 18 102 (90%)
346
LIE
AND
HEYNEMAN
lindoense in some of the snails. The re- tode sporocysts. It therefore appears likely sults of S. munsoni experiments with 3 to that common factors in the resistance mechanisms exist that are vulnerable to the were pooled 6 days exposure interval (Table II). In this group, 47% of the ex- action of trematode larvae. A previous perimental snails became susceptible to E. study showed that interference with the snail’s defense by a living trematode larva lindoense, while only 10% of the control may take place even though large numsensitized snails became infected. The difbers of snail amebocytes are present, acference is statistically highly significant. Snails harboring S. mansoni along with E. companied by an activated amebocyteproducing organ (Lie and Heyneman Zindoense showed moderate to large num1976). In the presence of an “escaped’ bers of secondary S. mansoni sporocysts lindoense infection (where that were often degenerated, probably ow- Echinostoma the sporocyst is not destroyed by encaping to frequent attack by E. lindoense sulation in the ventricle of the snail), the rediae. The results of P. segregutum exinnumerable amebocytes in the snail, norperiments with 2 to 6 days exposure inmally strongly protective, appear to lose terval were also pooled (Table I). A total their ability to recognize the trematode of 42% of the experimental snails became parasite. They accumulate in areas where positive for E. lindoense, while only 7% parasites are not present, such as between of the sensitized control snails took the the lobuli of the digestive gland, and fail infection. The difference is statistically to recognize or adhere to the trematode, highly significant. E. lirwloense larvae in even when in close proximity to it. This the ventricle usually did not survive long in the presence of P. segregatum rediae, as suggests that natural (juvenile and adult) and acquired resistance might share a comthe latter quickly consumed the subordimon recognition mechanism. It is unlikely nate parasites. that loss of acquired resistance in the snails was due to stress caused by infection with DISCUSSION P. segregatum or S. mansoni. Most of the We have previously shown that various snails looked healthy and were moving and trematodes can interfere with natural re- developing normally. If stress were responsistance of Biomphalaria glabrata (Lie and sible for loss of resistance, the snails would Heyneman 1976; Lie, Heymeman, and also have lost their ability to mount a tisJeong 1976; Lie, Heyneman, and Richards sue reaction to other unrelated parasites or 1977). The present study shows that I’. other insults. Preliminary results of work segregatum and S. mansoni can also intercarried out under the same conditions as fere with acquired resistance in the snail. the present experiments show that presence Natural and acquired resistance to tremof echinostome sporocysts has little influatodes in B. glabrata appear to have a ence on the tissue reactions induced by different basis. Inheritance of adult natural the nematode Angiostrongylus mulaysienresistance is determined by a single domisis in B. glubrata M-RLc strain or by injury. nant factor (Richards 1973), while several Various species of trematode larvae infactors seem to influence the genetics of duce different degrees of interference with juvenile natural resistance (Richards and the snail’s natural resistance, though the Merritt 1972). An acquired resistance can process appears to be the same. Echinodevelop in snails previously genetically susstoma paraensei is capable of suppressing ceptible to the parasite (Lie, Heyneman, the snail’s natural resistance to Schistosoma and Lim 197513). Despite these differences, mansoni strongly and to E. lindoense modnatural and acquired resistance seem to erately (Lie, Heyneman, and Richards be easily interfered with by living trema-
TREMATODE
INTERFERENCE
The present study shows that Paryphostomum segregatum and S. munsoni both have a moderate capacity to interfere with an acquired resistance to E. lindoense. 1977).
ACKNOWLEDGMENTS For excellent technical assistance we are indebted to Mrs. Nina Kostanian, Mrs. U. Jeyarasasingam, Mr. Percy Yao, Mr. K. C. Lim, and Mr. John Chiu. This investigation was supported by the University of California International Center for Medical Research (UC ICMR) through research Grant No. AI 10051 to the Department of International Health, School of Medicine, University of California, San Francisco; by research Grant No. AI 07054; and by the United States-Japan Cooperative Medical Science Program through research Grant No. AI 08520, all from the NIAID, NIH, U.S. Public Health Service. This is publication No. 9 in a series of studies on resistance in snails. REFERENCES K. J., AND HEYNEMAN, D. 1975. Studies on resistance in snails: A specific tissue reaction to Echinostoma lindoense in Biomphalaria glabrata. International Journal of Parasitology 5, 621-626. LIE, K. J., AND HEYNEMAN, D. 1976. Studies on resistance in snails. 6. Escape of Echinostoma lindoense sporocysts from encapsulation in the snail heart and subsequent loss of the host’s ability to resist infection by the same parasite. Journal of Parasitology 62, 298-302.
LIE,
WITH
SNAILS'
RESISTANCE
347
LIE, K. J,, HEYNEMAN, D., AND JEONG, K. H. 1976. Studies on resistance in snails. 7. Evidence for interference with the defense reaction of Biomphalaria glabrata by trematode larvae. Journal of Parasitology 62, 608-615. LIE, K. J., HEYNEMAN, D., AND KOSTANIAN, N. 1975a. Failure of Echinostoma lindoense to reinfect snails already harboring that species. International Journal for Parasitology 5, 483-486. LIE, K. J., HEYNEMAN, D., AND LIM, H. K. 1975b. Studies on resistance in snails. Specifk resistance induced by irradiated miracidia of Echinostoma lindoense in Biomphalaria glabrata snails. International Journal of Parasitology 5, 627-632. LIE, K. J., HEYNEMAN, D., AND RICHARDS, C. S. 1977. Studies on resistance in snails. Interference by nonirradiated echinostoma sporocysts with natural resistance to Schistosoma mansoni in Biomphalaria glabrata. Journal of Inverteence by nonirradiated echinostome sporocysts brate Pathology 29, 118-125. LIE, K. J., BASCH, P. F., HEYNEMAN, D., AND FITZGERALD, F. 1968. Antagonism between two species of echinostomes (Paryphostomum segregatum and Echinostoma lindoense) in the snail Biomphalaria glabrata. Zeitschrift fiir Parasitenkunde 30, 117-125. RICHARDS, C. S. 1973. Susceptibility of adult Biomphalaria glabrata to Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 22, 748-756. RICHARDS, C. S., AND MERRITT, J. W., JR. 1972. Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni Mediinfection. American Journal of Tropical cine and Hygiene 21,425-434.
(1977)
Schistosoma mansoni, Echinostoma lindoense, and Paryphostomum segregatum: Interference by Trematode Larvae with Acquired Resistance in Snails, Biomphalaria glabrata K. J. LIE AND D. HEYNEMAN The G. W. Hooper Foundation, University of California, San Francisco, California 94143, U.S.A. (Accepted
for publication
18 February
1977)
LIE, K. J., AND HEYNEMAN, D. 1977. Schistosoma mansoni, Echinostoma lindoense, and Paryphotiomum segregatum: Interference by trematode larvae with acquired resistance in snails, Biomphalaria glabrata. Experimental Parasitology 42, 343-347. Many juvenile albino Biomphalaria glabrata snails with an acquired resistance to Echinostomu lindoense again became susceptible to this trematode parasite following infection with either of two Payphostomum segregatum or Schistosoma mansoni. Previous other larval trematodes, studies have shown that trematode sporocysts are capable of interfering with juvenile and adult natural resistance to S. mansoni. We propose that a common mechanism is present that allows both juvenile and adult natural resistance and acquired resistance to trematodes in B. glabrata to be reduced strikingly by the simultaneous presence of trematode larvae in the snail host. INDEX DESCRIPTORS: Schistosoma mansoni; Echinostoma lindoense; Paryphostomum segregatum; Echinostoma parasnsei; Trematode; Biomphalaria glabrata; Snail; Acquired resistance; Natural resistance, snails; Trematode antagonism; Interference with snail resistance.
Recent studies have shown that the concurrent presence of any of several trematode larvae can interfere with the natural ( genetic) resistance of Biomphuhwia g&zbruta snails to certain trematode parasites. Echinostoma lindoense sporocysts developing from irradiated miracidia normally are rapidly encapsulated in the snail heart. However, in snails that also harbored normal sporocysts of the same species, the irradiated sporocysts were protected from encapsulation. In snails harboring ScMstosoma mansoni or Paryphostomum segregaturn, encapsulation of irradiated E. lindoense was delayed (Lie, Heyneman, and Jeong 1976). Most B. glubrata snails of a strain naturally resistant to S. munsoni became susceptible to this parasite when infected first either with Echinostoma para-
ensei, E. Mndoense, or E. liei (Lie, Heyneman, and Richards 1977). The present experiments were designed to determine whether or not a concurrent trematode infection is also able to interfere with acquired resistance in B. glaabrata, as it did with natural resistance (Lie, Heyneman, and Richards 1977). MATERIALSANDMETHODS
The parasites (Schistosoma mansoni laboratory strain, Echinostoma lindoense, and Payphostomum segregatum), snails (juvenile NIH albino BiomphaZuria glabruta from our laboratory stock) methods of exposure of snails to miracidia, irradiation of miracidia, and maintenance of snails have been described in previous papers
343 Copyright All rights
0 1977 by Academic of reproduction in any
Press, Inc. form reserved,
LSSN
0014-4894
344
LIE AND HEYNEMAN
and Kostanian 1975a; intervals used in the present experiments, (Lie, Heyneman, Lie, Heyneman, and Lim 1975b; Lie and it was unlikely that migrating sporocysts Heyneman 1975). Juvenile snails, 2 to 3 of E. lindoense were consumed by P. segmm in diameter, were sensitized to E. regatum rediae before E. lindoense could reach the heart. All snails in our experilindoense by exposing each to 10 irradiated miracidia. Each snail was then reexposed ments were examined daily under the disto 10, 20, or 50 normal S. mansoni, or to secting microscope for E. linduense sporostarting 30 hr five normal P. segregatum miracidia, 1 to cysts in the ventricle, 3 days after destruction within the venpostexposure. In cases of doubt as to the tricle of the irradiated E. lindoense sporoidentity ‘of the larvae in the ventricle, i.e., whether they were sporocysts of E. lindocysts, which could be observed through ense, small rediae of P. segregatum, or the shell under the dissecting microscope. Since destruction of the E. lindoense sporoboth, the snails were dissected and the cysts by capsule formation took place be- hearts were examined. E. lindoense is a weak antagonist to S. tween 3 to 9 days postexposure in this group of experimental snails, reexposure to mansoni, capable of consuming primary, S. mansoni or P. segregatum was done 4 but apparently not easily, destroying secondary, S. mansoni sporocysts (Lie, Heyneto 12 days after the initial exposure to irradiated E. lindoense. The snails were man, and Richards 1977). With the expoagain reexposed, this time to 50 normal sure intervals we employed, using relatively E. lindoense miracidia. The interval be- large numbers of S. mansoni miracidia, there was little possibility that all developtween first and second reexposure varied from 1 to 6 days. Two sets of control snails ing primary S. mansoni sporocysts would were used for each experiment. One con- be consumed by E. lindoense rediae before sisted of snails sensitized to E. lindoense secondary S. mansoni sporocysts could be formed. In general, this possibility was less with the same batch of miracidia used to sensitize the experimental snails, but not with longer exposure intervals, which allowed more time for secondary S. mansoni reexposed to S. mansoni or P. segregatum. They were reexposed only to the 50 norsporocysts to develop. Therefore, when the mal E. lindoense miracidia, along .with the two trematodes were given simultaneously experimental snails. The second set of con- or when an interval of only 1 to 3 days trols consisted of previously uninfected separated them, experimental snails were snails, of the same size and strain as the each exposed to 50 S. mansoni miracidia. experimentals, exposed only to 50 normal With longer intervals between exposures, E. lindoense miracidia. 20 or, rarely, only 10 S. mansoni miracidia P. segregatum is a strong predator of were used. Periodic checking of the snails E. lindoense (Lie, Basch, Heyneman, and for presence of primary and secondary S. Fitzgerald 1968). With the intervals be- mansoni sporocysts and E. lindoense was tween the reexposure to P. segregatum and carried out routinely, and all snails were dissected 30 to 32 days after exposure to the following reexposure to E. lindoense S. mansoni. that were used in these experiments, the E. lindoense larvae were able to survive RESULTS for varying periods in the ventricle before being attacked and consumed by P. segreThe results (Tables I and II) show that gatum. In general, the longer the period both Schistosoma mansoni and Paryphostobetween reexposures, the further developed mum segregatum are able to interfere with was the P. segregatum, and the shorter the an acquired resistance to Echinostoma E. lindoense survival. However, with the lindoense in Biomphalaria glabrata, render-
TREMATODE
INTERFERENCE
WITH
TABLE Interference
Number of snails positive for both parasites
345
RESISTANCE
I
with Acquired Resistance to Echinostoma lindoense in Sensitized Biomphalaria glabrata by Paryphostomum segregatum
Interval between 2nd and 3rd exposures (days)
Number of snails
SNAILS’
Number of snails positive for P. segregatum only
Number of snails positive for E. lindoense only
Juvenile
Number of snails negative for both parasites
25 25” 96
0
3
15
1 19 0
6 6 9
68 68= 31b
1
7
41
0 57
20 11 30
154 155= 83b
2-6
44 (42%)
61 (58%)
4 149 6 (7%)
45 6 77 (93%)
a Nonsensitized control snails exposed only to 50 E. Zindoense miracidia. b Sensitized control snails exposed to 50 E. lindoense miracidia.
soni was required before some of the snails again became susceptible to E. lindoense. However, even a simultaneous exposure to P. segregatum and E. Mndoense produced a breakdown of acquired resistance to E.
ing the snails again susceptible to the latter parasite. P. segregatum may be slightly more efficient than S. munsoni in reducing the snail’s acquired resistance. An interval of 1 day or more after exposure to S. manTABLE Interference
II
with Acquired Resistance to Echinostoma lindoense in Sensitized Biomphalaria glabrata by Schistosoma mansoni Number of snails positive for both parasites
Number of snails positive for X. mansoni only
Number of snails positive for E. lindoense only
Juvenile
Number of snails
Interval between 2nd and 3rd exposures
35 35a 24”
0
0
35
0 35 23
0 0 1
47 47” 316
1
6
32
0 47 2
9 0 29
30 305 16b
2
2
19
0 29 0
9 I 16
228 2505 1135
3-6
101 (47%)
114 (53%)
a Nonsensitized control snails exposed only to 50 E. Zindoense miracidia. b Sensitized control snails exposed to 5; E. lindoense miracidia,
0 232 11 (10%)
Number of snails negative for both parasites
13 18 102 (90%)
346
LIE
AND
HEYNEMAN
lindoense in some of the snails. The re- tode sporocysts. It therefore appears likely sults of S. munsoni experiments with 3 to that common factors in the resistance mechanisms exist that are vulnerable to the were pooled 6 days exposure interval (Table II). In this group, 47% of the ex- action of trematode larvae. A previous perimental snails became susceptible to E. study showed that interference with the snail’s defense by a living trematode larva lindoense, while only 10% of the control may take place even though large numsensitized snails became infected. The difbers of snail amebocytes are present, acference is statistically highly significant. Snails harboring S. mansoni along with E. companied by an activated amebocyteproducing organ (Lie and Heyneman Zindoense showed moderate to large num1976). In the presence of an “escaped’ bers of secondary S. mansoni sporocysts lindoense infection (where that were often degenerated, probably ow- Echinostoma the sporocyst is not destroyed by encaping to frequent attack by E. lindoense sulation in the ventricle of the snail), the rediae. The results of P. segregutum exinnumerable amebocytes in the snail, norperiments with 2 to 6 days exposure inmally strongly protective, appear to lose terval were also pooled (Table I). A total their ability to recognize the trematode of 42% of the experimental snails became parasite. They accumulate in areas where positive for E. lindoense, while only 7% parasites are not present, such as between of the sensitized control snails took the the lobuli of the digestive gland, and fail infection. The difference is statistically to recognize or adhere to the trematode, highly significant. E. lirwloense larvae in even when in close proximity to it. This the ventricle usually did not survive long in the presence of P. segregatum rediae, as suggests that natural (juvenile and adult) and acquired resistance might share a comthe latter quickly consumed the subordimon recognition mechanism. It is unlikely nate parasites. that loss of acquired resistance in the snails was due to stress caused by infection with DISCUSSION P. segregatum or S. mansoni. Most of the We have previously shown that various snails looked healthy and were moving and trematodes can interfere with natural re- developing normally. If stress were responsistance of Biomphalaria glabrata (Lie and sible for loss of resistance, the snails would Heyneman 1976; Lie, Heymeman, and also have lost their ability to mount a tisJeong 1976; Lie, Heyneman, and Richards sue reaction to other unrelated parasites or 1977). The present study shows that I’. other insults. Preliminary results of work segregatum and S. mansoni can also intercarried out under the same conditions as fere with acquired resistance in the snail. the present experiments show that presence Natural and acquired resistance to tremof echinostome sporocysts has little influatodes in B. glabrata appear to have a ence on the tissue reactions induced by different basis. Inheritance of adult natural the nematode Angiostrongylus mulaysienresistance is determined by a single domisis in B. glubrata M-RLc strain or by injury. nant factor (Richards 1973), while several Various species of trematode larvae infactors seem to influence the genetics of duce different degrees of interference with juvenile natural resistance (Richards and the snail’s natural resistance, though the Merritt 1972). An acquired resistance can process appears to be the same. Echinodevelop in snails previously genetically susstoma paraensei is capable of suppressing ceptible to the parasite (Lie, Heyneman, the snail’s natural resistance to Schistosoma and Lim 197513). Despite these differences, mansoni strongly and to E. lindoense modnatural and acquired resistance seem to erately (Lie, Heyneman, and Richards be easily interfered with by living trema-
TREMATODE
INTERFERENCE
The present study shows that Paryphostomum segregatum and S. munsoni both have a moderate capacity to interfere with an acquired resistance to E. lindoense. 1977).
ACKNOWLEDGMENTS For excellent technical assistance we are indebted to Mrs. Nina Kostanian, Mrs. U. Jeyarasasingam, Mr. Percy Yao, Mr. K. C. Lim, and Mr. John Chiu. This investigation was supported by the University of California International Center for Medical Research (UC ICMR) through research Grant No. AI 10051 to the Department of International Health, School of Medicine, University of California, San Francisco; by research Grant No. AI 07054; and by the United States-Japan Cooperative Medical Science Program through research Grant No. AI 08520, all from the NIAID, NIH, U.S. Public Health Service. This is publication No. 9 in a series of studies on resistance in snails. REFERENCES K. J., AND HEYNEMAN, D. 1975. Studies on resistance in snails: A specific tissue reaction to Echinostoma lindoense in Biomphalaria glabrata. International Journal of Parasitology 5, 621-626. LIE, K. J., AND HEYNEMAN, D. 1976. Studies on resistance in snails. 6. Escape of Echinostoma lindoense sporocysts from encapsulation in the snail heart and subsequent loss of the host’s ability to resist infection by the same parasite. Journal of Parasitology 62, 298-302.
LIE,
WITH
SNAILS'
RESISTANCE
347
LIE, K. J,, HEYNEMAN, D., AND JEONG, K. H. 1976. Studies on resistance in snails. 7. Evidence for interference with the defense reaction of Biomphalaria glabrata by trematode larvae. Journal of Parasitology 62, 608-615. LIE, K. J., HEYNEMAN, D., AND KOSTANIAN, N. 1975a. Failure of Echinostoma lindoense to reinfect snails already harboring that species. International Journal for Parasitology 5, 483-486. LIE, K. J., HEYNEMAN, D., AND LIM, H. K. 1975b. Studies on resistance in snails. Specifk resistance induced by irradiated miracidia of Echinostoma lindoense in Biomphalaria glabrata snails. International Journal of Parasitology 5, 627-632. LIE, K. J., HEYNEMAN, D., AND RICHARDS, C. S. 1977. Studies on resistance in snails. Interference by nonirradiated echinostoma sporocysts with natural resistance to Schistosoma mansoni in Biomphalaria glabrata. Journal of Inverteence by nonirradiated echinostome sporocysts brate Pathology 29, 118-125. LIE, K. J., BASCH, P. F., HEYNEMAN, D., AND FITZGERALD, F. 1968. Antagonism between two species of echinostomes (Paryphostomum segregatum and Echinostoma lindoense) in the snail Biomphalaria glabrata. Zeitschrift fiir Parasitenkunde 30, 117-125. RICHARDS, C. S. 1973. Susceptibility of adult Biomphalaria glabrata to Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 22, 748-756. RICHARDS, C. S., AND MERRITT, J. W., JR. 1972. Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni Mediinfection. American Journal of Tropical cine and Hygiene 21,425-434.