The Aspidogastrea: A Parasitological Model III.

Authors

As discussed and illustrated in two previous knols (previous knol , and here) the two species of Aspidogastrea examined in detail possess some intriguing differences both in morphology and life cycles. The larva of

Multicotyle purvisihas a larger variety of sensory receptors than that ofLobatostoma manteri, including a pair of eyes and an anterior paired receptor complex which are absent in the latter species. It also has ten ciliary tufts and a coat of microfila, i.e., very thin processes of the tegument. The larva ofLobatostoma manteri,on the other hand, has a well developed pseudosucker absent in the former species. – Adults ofMulticotyle purvisireach a length of at least 10mm (unpressed), ofLobatostoma manteriof about 7mm (pressed) and 4mm (unpressed). The former species has a uterus coiled up in the anterior part of the body, with relatively few eggs, the latter species has a uterus filling most of the body, with a large number of eggs. The juvenile and adult of both species have a large number of marginal organs (terminal parts of glands) between the marginal alveoli of the adhesive disk. – In the following I try to explain these differences by differences in the biology, i.e., the life cycles of the species.

Multicotyle purvisi

 

Infection process and localisation in host

Rohde (1971) [1] [2]decribed the infection process of

Multicotyle purvisifrom the stomach and occasionally the anterior part of the duodenum of several species of Malayan turtles, with freshwater snails as intermediate hosts, as follows:

Eggs containing embryos at the 1-3 cell stage are laid. Larvae develop in the egg after it has escaped in the faeces of turtles into freshwater. In experiments at temperatures of 27-29 o C first hatching occurred 25 days after egg laying, at 21-28 o C first hatching occurred after 35-40 days, at 19-22 o C after 103 days. Environmental temperatures in Malaya are 21-32 o C (in the shade, lowlands). The hatching process takes only a few minutes. Hatching in cultures under normal diurnal fluctuations of light and temperatures occurs, with few exceptions, in the early hours of the morning. In cultures kept in the dark beyond the normal time of hatching, hatching occurred only after illumination. However, when cultures were kept in the dark over days, hatching occurred also without a light stimulus. – Immediately after hatching, larvae swim with usually extended anterior end, rotating around their longitudinal axis, either along the bottom or straight upwards to the surface, but also irregularly in all directions in the water. They often remain attached to the surface, slowly rotating, or sink slowly to the bottom with the posterior end directed downwards, or faster with the anterior end directed downwards. Larvae can also float in the middle of the water column rotating slowly around their longitudinal axis, carried sidewards by water currents. It sometimes remains at the bottom, appearing to “touch and feel” the substratum. – Larvae are positively phototactic and survived at 26-30 o C for 5 to over 33 hours. They reach the host less by their own movements, but rather by water currents produced by snails, which carries them into the inhaling opening.

Localisation of larvae in the snails was determined in three specimens of the snail

Pila scutata: 50 and 69 days, respectively, after infection, a larva was found in the anterior kidney chamber, 108 days after infection, a larva was found in the posterior kidney chamber of the snail. – Experiments showed that turtles become infected by ingesting infected snails. – The smallest specimens ofMulticoylefound in a large number of naturally infected turtles had 17 and 18 transverse rows of alveoli, respectively. It therefore seems that specimens must be of a certain miminum size before they become infective. Fully grown up and mature specimens have 50 transverse rows of alveoli.

 

Functional morphology

These features of the life cycle suggest that the larval eyes are responsible for phototaxis which keeps them in the water column where they can encounter snails, but they may also contribute to hatching in the morning. The paired anterior sensory complex may have the function of a balancing organ, as suggested by the ciliary structure extending into interior liquid filled cavities. The coat of microfila increases the surface area without increasing the weight, suggesting that it makes floating in the water column more effective. Ciliary tufts are necessary for swimming, which leads the larvae not directly to the snails, but into the water column where snails may inhale them. This kind of infection behaviour is possible only because the habitat of these freshwater snails is relatively undisturbed, i.e., eggs and larvae after hatching do not run a great risk of being swept away into a less favourable site by adverse currents. The numerous sensory receptors may enable the parasite to keep damage to the very delicate tissues of the host, in particular their kidneys, on which it depends for survival, at a minimum. But they may also contribute to finding the snails’ habitat, and to mate finding. – The uterus of the adult can be kept relatively short, because larvae in the eggs develop only after leaving the worm.

Lobatostoma manteri

 

Infection process and localisation in host

Rohde (1973, 1975) [3] [4]described the infection process of

Lobatostoma manteri` as follows: Eggs are laid which contain already fully developed larvae. Snails become infected by eating eggs containing larvae. In experiments, larvae hatched in the stomach of snails (Planaxis sulcatusandCerithium moniliferum) and migrated immediately along the ducts of the digestive gland into the digestive follicles.

 

Pathology

Larvae of

Lobatostomafeed on secretion and probably epithelial cells of the follicles of the digestive gland of snails. The posterior sucker and developing ventral disk are used for adhesion to the epithelium, and they contribute to its erosion. In heavy experimental infections, 47-49 and 65-66 days after infection, only small parts of the epithelium are still secretory, and the larvae live in large fused cavities. Juveniles are usually found in a cavity formed by an enlargement of the main duct and one or more (?) side ducts of the digestive gland near the stomach inCerithium moniliferum, or in the stomach and main ducts of the digestive gland ofPeristernia australiensis. They may creep from the ducts into the stomach and back into the ducts. Fish become infected by eating snails.

Rohde and Sandland (1973) [5]examined histological sections of

Cerithium moniliferumandPeristernia australiensisinfected withLobatostoma manteri. In the former species (much smaller than the latter), a single parasite is usually present, coiled up in a cavity formed by the main and one or perhaps some side ducts of the digestive gland, causing metaplasia of the duct epithelium, hyperplasia of the inter-follicular connective tissue and an increase in the number of amoebocytes, and necrosis of some glandular follicles The latter species may harbour up to six parasites in the stomach and in the large ducts of the digestive gland, with a thickening of the subepithelial connective tissue layer.

Pathogenesis caused by larval and growing

Lobatostomais illustrated in Figures 1 – 6.


Figure 1

. Young larva of

Lobatostoma manteri(47-49 days old)feeding on the digestive gland of an experimentally infectedCerithium moniliferum. Note the posterior sucker around some host tissue. Original Klaus Rohde. © Klaus Rohde


Figure 2

. Two larvae (65-67 days old) of

Lobatostoma manteriin digestive gland of experimentally infectedCerithium moniliferum. Note: functional glandular tissue replaced by necrotic (dead and dying) cells. Original Klaus Rohde. © Klaus Rohde

For comparison, normal follicles of the digestive gland of

Cerithiumare illustrated in Figure 3.


Figure 3.Cerithium moniliferum, normal follicles of digestive gland in uninfected snail. Original Klaus Rohde. © Klaus Rohde


Figure 4.

Large juvenile of

Lobatostoma manteriin the stomach of naturally infectedPeristernia australiensis. Note enlarged subepithelial tissue (hyperplasia), i.e., fibrosis (abnormally thick connective tissue) around parts of the stomach. Original Klaus Rohde. © Klaus Rohde


Figure 5

.

Peristernia australiensisinfected withLobatostoma manteri.Enlarged portion of Figure 4. Original Klaus Rohde. © Klaus Rohde


Figure 6.Cerithium moniliferumwith one large juvenileLobatostoma manteriin the digestive gland. Arrows indicate outline ofLobatostoma. Original Klaus Rohde. © Klaus Rohde

The illustrations show the considerable damage done to the hosts by the infection, although it should be pointed out that naturally infected snails never had as many parasites as experimentally infected ones. Reasons may be that snails in their natural habitat never encounter so many eggs, that heavily infected snails die, or that in natural infections later infections are suppressed by larvae or juveniles already present, either by predation of large on smaller larvae, or by tissue reactions induced by older parasites.

 

Functional morphology

In view of the pathological findings, it seems reasonable to assume that one function of the variety and number of sensory receptors may be to limit damage done to the delicate host tissue by the parasites. However, they may also play a role in mate finding. Rohde (1973) [3]discussed the adaptive value of the ventral disk: it could be an adaptation for locomotion in or on the soft tissues of the host (snails), perhaps facilitating adhesion of only small portions to a small area of the host’s tissue and preventing damage to it. Observations of digeneans and

MulticotyleandLobatostomashowed that the ventral disk is not more effective for attachment to the vertebrate intestine than the suckers of digeneans, suggesting that it is indeed an adaptation to life in molluscs. It is also very rarely used for tight attachment to the surface of containers or snails. The secretion produced by the marginal glands on the disks has not been examined, but it may be digestive, contributing to the erosion of the digestive gland follicles of the snails, as seen in histological sections. The long uterus ofLobatostomais necessary, because eggs leave the worm only after larvae infective to snails have developed in them. This is necessary because the habitat is rather “violent”, exposed to strong tidal currents, and may dry out at low tide, making rapid ingestion of eggs by snails essential.

 

 

Infection dynamics

At Heron Island, 11 species of larval digeneans were found in

Cerithium moniliferum[6]. Prevalence of infection with various Digenea andLobatostomawas monitored around the island over an extended period [5]. Only snails of the speciesCerithium moniliferum,Peristernia australiensisandPlanaxis sulcatuswere found to be infected withLobatostoma; the second species did not harbour any digeneans.Lobatostomawas found only in a small part of Shark Bay with a flat bottom formed by beachrock, and on beachrock close to it, possibly carried there by snails that had acquired their infection in Shark Bay (Fig. 7). Examination of beachrock in Shark Bay showed a large number of shell fragments, mainly ofCerithium,on it. Netting in Shark Bay yielded small Snubnosed dart,Trachinotus blochi(Fig.8). Its name is derived from the strongly developed muscles in the forehead which move the large pharyngeal plates, an adaptation to crushing the very thick shell of snails (for details and illustration see previous knol). Dissection of these fish revealedLobatostomain the small intestine and shell fragments in the stomach. Other fish caught in Shark Bay without this structure were never infected. – From January 1971 to April 1972, there was a strong decrease in the relative number of infected snails of both species. During the period of high frequency of infection,Cerithiuminfected with Digenea containedLobatostomarelatively more frequently than snails without Digenea. Snails with double infections disappeared first. Infection withLobatostomadid not affect the relative number of egg producingCerithiumduring the period of high frequency of infection.


Figure7.The distribution and infection of snails withLobatostoma manteriat Heron Island at the southern end of the Great Barrier Reef in January-April 1971. Note: beachrock around much of the island, the harbour and the moat (shallow channel) extending from the harbour area towards Shark Bay. At incoming tide, the moat fills first and fish swim from the reef edge into Shark Bay. The snailsCerithium moniliferum,Planaxis sulcatusandPeristernia australiensiswere infected withLobatostoma, but infection was practically restricted to a small area of Shark Bay with a bottom of flat beachrock (arrows), although snails occurred all around the island on beachrock and rubble. A fewLobatostomawere also found a short distance from Shark Bay, possibly acquired in Shark Bay by snails which subsequently migrated along the beachrock. Original Klaus Rohde. Vertikalphoto RAAF No.2 squadron. © Klaus Rohde


Figure 8.

Life cycle of

Lobatostoma manteri. The final hostTrachinotus blochi, the Snubnosed dart, sheds eggs ofLobatostomawith larvae infective to snails in its faeces, eggs are eaten by marine snails. Juveniles develop in the snails, which are in turn eaten by the final host. Original Klaus Rohde. © Klaus Rohde

Equilibrium or non-equilibrium ? A demographic or autecological explanation ?

In this concluding section we attempt to interpret the findings on the basis of two ecological paradigms. Walter and Hengeveld (2000, also Hengeveld and Walter 1999) [8] [9] distinguished the demographic and autecological paradigms. In the former, species are thought to to be demographically similar but have different functions in communities. Intra- and interspecific competition have great importance, leading to coevolution by optimisation processes (i.e., processes that bring about optimal adaptation to environmental conditions), to saturation of communities with species, and to equilibrium. Optimisation is thought to be possible over short time spans because the abiotic environmental component is, on average, constant.

According to the autecological paradigm, species are dissimilar entities affected by abiotic and demographic factors; optimisation is impossible because of the greatly variable environment. The demographic paradigm asks: why do so many species share the same resources; the autecological paradigm asks: how did species arise and how do they survive in a variable and heterogeneous environment; it focuses on the unique nature of adaptations and on species with their spatial responses to environmental conditions. Walter and Hengeveld claim that the two paradigms are mutually exclusive.

We ask which of the two paradigms is better suited to explain the unique adaptations of the two aspidogastreans discussed, and the distribution of

Lobatostoma.As pointed out in the first knol on Aspidogastrea, the group is very ancient, having diverged from the digenean trematodes more than 400 million years ago. Its unique features (adhesive disk, marginal glands, great variety and number of sensory receptors, no multiplication of larvae in the intermediate host) also are likely to be very ancient. It is unlikely that they have evolved as short-term adaptations to particular environments. – Possible competitors with the two aspidogastreans are larval Digenea in the snails. However, the distribution ofLobatostomaand Digenea at Heron Island clearly shows that prevalence of infection with Digenea is greatest in a small habitat which also has the heaviest infections withLobatostoma, making it unlikely that interspecific competition plays any role in determining the distribution ofLobatostomaat Heron Island. Intraspecific competition, i.e. competition between individuals ofLobatostomain the snails, may well occur, as suggested by the observation that the smallest of the three snail species infected,Cerithium moniliferum, very rarely contains more than one juvenile ofLobatostoma. More individuals simply cannot be accomodated (Fig.6). But it is difficult to see how this could have led to any of the adaptations and to the distribution of the species. Clearly, each species has features that are long-term adaptations to a particular kind of life cycle and habitat. In other words, only the autecological paradigm can explain them.

Caution is, however, necessary in accepting the statement that the two paradigms are mutually exclusive. Rohde (2005) [10] , in discussing the relative frequency of equilibrium and non-equilibrium conditions in biological systems, stressed that groups with certain characteristics will tend to exist in equilibrium, others will tend to exist in non-equilibrium. Both conditions are possible and depend on the size of populations and individuals, and on the vagility of the species. If all these are small (as in the aspidogastreans), a tendency towards non-equilibrium results [11] .

References

Rohde, K. 1971. Untersuchungen an Multicotyle purvisi Dawes, 1941 (Trematoda, Aspidogastrea). I. Entwicklung und Morphologie. Zoologische Jahrbücher, Abteilung für Anatomie, 88, 138-187. Rohde, K. 1972. The Aspidogastrea, especially Multicotyle purvisi Dawes, 1941. Advances in Parasitology, 10, 77-151. Rohde, K. 1973. Structure and development of Lobatostoma manteri sp. nov. (Trematoda, Aspidogastrea) from the Great Barrier Reef, Australia. Parasitology, 66, 63-83. Rohde, K. 1975. Early development and pathogenesis of Lobatostoma manteri Rohde (Trematoda: Aspidogastrea). International Journal for Parasitology, 5, 597-607. Rohde, K. and Sandland, R. 1973. Host-parasite relations in Lobatostoma manteri Rohde (Trematoda, Aspidogastrea). Zeitschrift für Parasitenkunde, 41, 115-136. Rohde, K. 1981. Population dynamics of two snail species, Planaxis sulcatus and Cerithium moniliferum, and their trematode species at Heron Island, Great Barrier Reef. Oecologia, 49, 344-352. Rohde, K. 1994. The origins of parasitism in the Platyhelminthes. International Journnal for Parasitology 24, 1099-1115. Walter, G.H. and Hengeveld, R. 2000. The structure of the two ecological paradigms. Acta Biotheoretica 48, 15-46. Hengeveld, R. and Walter, G.H. 1999. The two coexisting ecological paradigms. Acta Biotheoretica 47, 141-170. Rohde, K. 2005. Nonequilibrium Ecology. Cambridge University Press, Cambridge, N.Y., Melbourne, Madrid, Cape Town, Singapore, Sao Paulo. Gotelli, N.J. and Rohde, K. 2002. Co-occurrence of ectoparasites of marine fishes: a null-model analysis. Ecology Letters 5, 86-94.

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