Relationships Between Invertebrate Detritivores And Gut Bacteria In Marine Systems •

ABSTRACT

Aspects of the feeding strategies and digestive invertebrate-microbial interactions of

two saltmarsh thalassinid detritivores, the mudprawn Upogebia africana (Ortmann)

and the sandprawn Callianassa kraussi Stebbing were examined. Resources available

in their respective habitats were investigated together with the feeding apparatus,

diet and digestive enzymes necessary for hydrolysis of refractory compounds of

detritus. U. africana inhabits the upper reaches of Langebaan lagoon (Geelbek),.

while C. kraussi was sampled near the mouth (Oesterwal). Both species occur

intertidally. Physical characteristics of sediment and water fluctuate more widely at

Geelbek than at Oesterwal. Geelbek also has higher mud and clay content in the

sediment, and greater particulate load in the water. The resources available in both

sediment and water from Geelbek were of greater quality (assessed by proportion of

living component, C:N ratio) and quantity. In terms of distribution ofthe resource,

quality was highest in surface sediments, while quality was greatest at burrow

linings. The mode of feeding, gut structure and diet of the two prawn species differ,

although gut throughput rates are similar (ca. 6h). U.africana is a filter feeder which

non-selectively ingests small particles which are further sorted in the modified filtertype

gastric mill into larger particles which enter the midgut, and smaller particles

which are channeled into the hepatopancreas. U. africana has a relatively large

throughput gut (fore, mid, hind) allowing large meals to be taken. This may be

related to its reliance on vascular plant detritus for both carbon and nitrogen

requirements, as shown by stable isotope analyses. By contrast, C. kraussi feeds by a

combination of deposit feeding and filter feeding. It is able to selectively ingest

larger particles such as diatoms and protozoa as well as plant detritus. It has a

typical masticating gastric mill and ingested particles are crushed in the anterior

cardiac region and filtered in the posterior pyloric region; large particles are

channeled to the hepatopancreas. The hepatopancreas is the main site of enzymatic

digestion, and C. kraussi possesses both endoglucanase and Cl-cellulase, and is

capable of hydrolysis of refractory components of detritus. Experiments using

antibiotics to prevent activity suggest that these cellulases are endogenous. C.

kraussi has a relatively small gut which is dominated in volume by the

hepatopancreas, highlighting the importance of this organ.

The presence, nature and role of gut microflora in aquatic

invertebrates is synthesized from the literature, revealing the widespread occurrence

of invertebrate-microbe associations. Different types of associations are reported to

occur and the need to investigate the significance of different populations of

bacteria in the gut is highlighted. While the taxa and physiological properties of gut

microbes of many aquatic invertebrates have been reported, very little conclusive

evidence exists as to the role of bacteria in the physiology of host invertebrates. The

gut microflora of U. africana and C. kraussi were examined by scanning electron

microscopy and culture techniques. Both prawns hosted a diverse gut bacterial

community. Of note were novel filamentous bacteria that extensively coated the

midgut walls and gut contents of both species. Both prawns harboured mats of

epimural rod bacteria in the hindgut, these being extensive in U. africana. Isolation

of gut and habitat bacteria suggests that both species of prawn maintain a gut

microflora distinct from the habitat microflora, in terms of both genera present and

digestive capabilities. Distinction between resident gut bacteria and transient gut

bacteria indicated that some habitat bacteria remain viable in the gut of U. africana,

suggesting the potentially important phenomenon of incubation. More detailed

examination of the resident bacteria observed in U. africana by transmission

electron microscopy confirmed the presence of mats of densely-packed gramnegative

epimural rod bacteria in the hindgut, and irregular shaped bacteria in the

hepatopancreas. The dominant genus isolated from the hindgut was Pseudomonas,

although members of the genus Vibrio were also isolated. Resident bacteria from

the hindgut of U. africana did not exhibit chitinase, cellulase or lysozyme activity and

are therefore unlikely to contribute to digestion of refractory material by the prawn.

Acetylene reduction assays resulted in the detection of low rates of nitrogen fixation

associated with the prawn, while relatively strong rates were found for the sediment.

It was concluded that nitrogen fixation by gut microbes is insignificant in terms of

the nitrogen budget of the prawn.

A comparative study on the gut microflora of an Australian mangrove

crab Sesanna messa that feeds on fallen mangrove tree leaves (Rhizophora stylosa)

established the presence of gut bacteria by direct counts and scanning electron

microscopy. This crab feeds on nitrogen-poor food. However, acetylene reduction

assays failed to implicate gut microbes with nitrogen acquisition. The widespread

occurrence of epimural rod bacteria in the hindguts of decapod crustaceans was

demonstrated by a SEM study of 16 species. Crustacean hindguts . clearly represent

suitable environments for colonization by micro-organisms despite the lack of

specialized structures or modifications of the gut to facilitate this. Abundance of

hindgut microflora was unrelated to the hosts taxon, habitat or geographical

collection locality, but appeared to be affected by the feeding habits of the animal.

The detritivore gut appears to be the most favourable hab_itat for microbial

colonization, and this highlights the potential role of these microbes in detritivore

nutrition.