D. Heyneman

Intramolluscan inter-trematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological control.

Publisher Summary The study of intramolluscan single and double trematode infections has proved to be a useful approach in better understanding host–parasite relationship. Modification and disruption of snail infection with trematodes is reviewed and the parameters and characteristics of various infection combinations are described. Biologically, however, the inter-trematode reactions and the responses of the snail host offer remarkable opportunities to examine and isolate various aspects of this host–parasite relationship. The single species infection patterns differ widely between the pure sporocyst type, exemplified by S. mansoni, and the redial type, typified by P. segregatum. Characteristics of each are reviewed. Their interaction is then reviewed, based on original data and comparison with other studies. Redial predation (“direct antagonism”) is discussed in terms of relative activity, efficiency, and predatory response to triggering stimuli in the snail. Possible mechanisms of indirect antagonism are reviewed, with a fuller consideration of snail immunity as induced by these infections and measured experimentally. The parameters or characteristics of single-species infection are described and related to one another in a preliminary fashion as an “adaptation index” (AI), which includes such parameters as infection rate, period for 50% snail death, and period to cercarial shed. The trematode method is locally applicable, using indigenous strains supplied and sustained at a high level by continual reseeding with eggs of the controlling trematode (or processed faeces from the appropriate final hosts). Effective biocontrol as a self-sustaining life-cycle appears highly improbable, as is the expectation that this method can be adopted on a wide scale with the same controlling agent.

The ultrastructure of the amebocyte-producing organ in Biomphalariaglabrata

The amebocyte-producing organ (APO) in normal and echinostome-sensitized Biomphalaria glabrata was studied at the ultrastructural level. The APO in unexposed snails consists of small clusters of primary ameboblasts resting on the epithelial cells lining the pericardium. The ameboblasts are held in a loose reticulum formed by extensions from smooth muscle and few fibroblastic cells. Secondary ameboblasts and amebocytes constitute further stages of this cell line. Amebocytes, resembling cells in the snails circulation, appear in the blood sinus coursing through the interior of the APO. Exposure of snails to echinostome miracidia results in significant morphological changes in the organ. Large clusters of primary and and secondary ameboblasts appear, many of these cells undergoing mitosis. Fully activated APOs consist of masses of cells loosely arranged in zones of progressive maturation. Blood cells in activated APOs were significantly larger than those seen in normal APOs.

Life cycle of a new echinostome from Egypt, Echinostoma liei sp.nov. (Trematoda: Echinostomatidae).

A 37-spined Egyptian echinostome, Echinostoma liei sp.nov., is described in adult and larval stages. The parasite develops readily in the laboratory in chicks and ducklings, hamsters and rats. Its natural final host in or near irrigation ditches of the Nile delta involves the roof rat, Egyptian giant shrew and aquatic bird hosts. Developmental forms are described from infection of the NIH strain of Biomphalaria glabrata in the laboratory. B. alexandrina, is infected in the normal habitat in Egypt and contains both developmental stages in the heart or aorta and the hepatopancreas, and metacercariae encyst in the pericardium and kidney. E. liei sp.nov. is one of six very similar species characterized by 37 collar spines with a pattern of (3 + 2) corner spines in each lappet, six laterals on each side, and 15 dorsals in alternating rows; two pairs of dorsoventral and one small pair of ventro-lateral finfolds on the cercarial tail; and rodlike cystogenous material filling the cercarial encystation glands. In addition to distinctive intermediate-host specificity, differentiating characteristics of E. liei cercariae include presence of six sets of three flame cells each per side (total 36), seven oesophageal cells, eight penetration gland outlets on the dorsal lip of the oral sucker, and an absence of paraoesophageal gland cells as determined by intravital dyes. Significance of these and other cercarial traits is emphasized to aid in defining highly similar, but none the less distinct, sibling species.

Studies on resistance in snails: Specific resistance induced by irradiated miracidia of Echinostoma lindoense in Biomphalaria glabrata snails

Abstract In juvenile Biomphalaria glabrata snails exposed to irradiated Echinostoma lindoense miracidia, the sporocysts migrated to the heart at the same speed as did nonirradiated sporocysts in control snails. However, in each snail so exposed to irradiated miracidia, amebocyte clumps in the snails heart destroyed the sporocysts within 2–9 days post-exposure. This process induced a strong, highly specific resistance to homologous reinfection in these previously susceptible snails. The snails remained susceptible to Schistosoma mansoni and Paryphostomum segregatum (Echinostomatidae), but were partially resistant to Echinostoma paraensei and E. liei, two echinostome species closely related to E. lindoense.

Studies on resistance in snails: A specific tissue reaction to Echinostoma lindoense in Biomphalaria glabrata snails

Abstract In juvenile albino Biomphalaria glabrata snails exposed for the first time to Echinostoma lindoense miracidia, and observed to be resistant, the sporocysts migrated to the heart at the same speed as they did in susceptible snails. However, in resistant snails the sporocysts were soon destroyed in the heart by amebocyte clumps. When these snails were then re-exposed to miracidia of the same species of trematode, the sporocysts were quickly destroyed soon after miracidial penetration, chiefly in the head-foot region. This strongly accelerated tissue reaction appears to have been induced by the previous contact with the same parasite. The sensitization of the snail tissues was highly specific: the hosts remained susceptible to Schistosoma mansoni and Paryphostomum segregation (Echinostomatidae), although partial resistance was observed against Echinostoma paraensei and E. liei , which are closely related to E. lindoense .

Tissue reactions induced by Schistosoma mansoni in Biomphalaria glabrata.

In Biomphalaria glabrata with a strong natural resistance, Schistosoma mansoni sporocysts are rapidly encapsulated by granulocytes and killed, mainly by the strong phagocytic activity of the cells. Irradiated Echinostoma paraensei sporocysts seem able to suppress the function of the granulocytes. Tissue reactions in snails with self-cure demonstrate: involvement of two types of cells, granulocytes and hyalinocyte-like cells; formation of amoeba-fibrous capsules; limited tendency of granulocytes to become attracted to the parasites; a slow process of parasite destruction; and a possible involvement of humoral factors. It seems that there is partial suppression of the granulocyte function in smails with self-cure.

Schistosoma mansoni: temporary reduction of natural resistance in Biomphalaria glabrata induced by irradiated miracidia of Echinostoma paraensei.

Abstract Sporocysts developing in the heart of the snail host from irradiated Echinostoma paraensei miracidia are unable to form rediae and can survive for only a brief time. However, they still were able to reduce temporarily the strong natural resistance to Schistosoma mansoni in juveniles of a strain of Biomphalaria glabrata selected for genetic resistance to this parasite. S. mansoni primary sporocysts, unable to survive in single (control) infections in this host strain, developed successfully in most snails in which irradiated E. paraensei sporocysts were present. After the echinostome sporocysts were destroyed by host amebocytes, the snails regained their natural resistance against a new infection by miracadia of S. mansoni. Successful initiation of an infection with S. mansoni was achieved only in the presence of living irradiated echinostomes. Once the schistosome infection had become well established, however, developing primary and secondary sporocysts could survive and produce cercariae, although the protecting echinostomes had by then been destroyed. Early growth stages of the primary sporocysts apparently are more vulnerable to the snails defensive reaction and generally do not survive unless protected by irradiated E. paraensei sporocysts. After the S. mansoni sporocysts grow older, they develop their own capacity to interfere with the snails natural resistance and continue to survive and produce progeny without further protection by the echinostomes. Irradiated sporocysts have a lower capacity to interfere with the snails natural resistance than do nonirradiated sporocysts. Suitability, as distinguished in this paper from susceptibility, can be separated from resistance of the snail to trematodes by employing double infections.

Studies on resistance in snails. 7. Evidence of interference with the defense reaction in Biomphalaria glabrata by trematode larvae.

Echinostoma lindoense sporocysts that develop from irradiated miracidia normally are destroyed by amebocyte capsules in the ventricle of Biomphalaria glabrata within 10 days postexposure. The survival period of these ventricular sporocysts was considerably longer in snails that also harbored normal sporocysts of E. lindoense, Paryphostomum segregatum, or Schistosoma mansoni. Protection of irradiated E. lindoense sporocysts by the same of different trematode species is presumed to be the result of an active process by which normal sporocysts interfere with capsule formation and protect themselves and other trematode larvae from encapsulation. Homologous protection was stronger than heterologous.

Elevation of aminopeptidase activity in Biomphalaria glabrata (Mollusca) parasitized by Echinostoma lindoense (Trematoda)

Abstract Comparisons of the levels of aminopeptidase activity in the hemocytes and serum of Biomphalaria glabrata at 20 and 30 days postexposure to irradiated Echinostoma lindoense miracidia with enzyme levels in control snails have revealed that there are significant elevations in the serum of snails at both time periods postexposure. Furthermore, there is a significantly higher level of aminopeptidase activity in the serum of snails at 30 days than at 20 days postexposure. Although the biologic function of the elevated levels of serum aminopeptidase in sensitized snails remains uncertain, it is possible that this lysosomal enzyme may degrade the surface proteins of secondarily introduced parasites and thus act as a form of acquired humoral immunity.

Leukocytes of Biomphalaria glabrata: morphology and behavior of granulocytic cells in vitro.

Abstract Blood cells from Biomphalaria glabrata hemolymph were studied by phase microscopy in vitro. The most common cell is a granulocytic leukocyte, present in the hemolymph at a concentration of 334 ± 105 cells/mm3. This cell ranges in length from 14.1 ± 2.8 μm (including pseudopodia), when suspended in hemolymph, to 77.2 ± 15.1 μm, when allowed to spread on a glass substrate. Cytoplasmic inclusions and other organelles are described. Observations on the behavior of these granulocytic leukocytes in vitro confirm that a strong phagocytic response develops toward a variety of particles in the virtual absence of snail hemolymph.