Leaf-cutter shrimp: Microbial gardens in marine sediments

Burrowing ghost shrimps (Crustacea: Decapoda: Thalassinidea) are among the most common macro-infauna animals in estuarine and marine sediments, where they play a central role in regulating the characteristics of the sediment bed. Their bioturbation is closely linked to their particle-feeding mode. In order to more fully understand the nutrition of this cryptic annuals the complex burrows will therefore be examined. The most enigmatic feature in the burrows of several species is the presence of debris chambers: special sections inside the burrow that are filled with organic material in different stages of degradation and/or with coarse sediment. Two hypotheses are proposed to explain the function of these aggregations: A "hoard hypothesis" involving a nutritional demand is opposed by a "dump hypothesis", which interprets the chambers as a collection of waste interfering with the animal. Our own examinations and observations and literature studies lead us to support the hoard hypothesis. A function as a microbial fermenter - in which the animals, as gardeners, foster the growth of a symbiotic microorganism community and thus exploit their broad enzymatic capabilities - is proposed. The objective of this study is to test the microbial gardening hypothesis and to describe the environmental conditions of sediment bottoms under which debris chambers are formed by thalassinidean-species. By answering questions derived from a theoretical analysis of microbial gardening using in situ and laboratory approaches we expect to obtain the evidence needed to elucidate this important yet unresolved aspect of crustacean ecology. Ten tasks are formulated to describe the sediment environment of the shrimp, to describe the content and origin of the debris in the chambers, as well as to determine the intake of organic matter into the burrow by the shrimp, the specific constituents and structure of the microorganism community, and the presence of substances essential to shrimp nutrition based on biochemical composition. Furthermore, the gardening activities of the shrimp will be monitored with regard to the created physiochemical milieu and the nutritional value and genesis of the community inside the chamber. Finally, we will attempt to prove that the organic matter which is tended in the chambers by the shrimp is actually assimilated. A microbial gardening behaviour analogue to that displayed by leaf-cutter ants has not yet been proven for crustacea.

The chambers filled with plant remains found in the sand burrows of marine mud shrimps (Thalassinidea) have been studied. Their origin, use to the shrimp and genesis has been tackled using field and laboratory methods in two thalassinid species. We found that the chambers are built by the shrimps for feeding purposes, similar to a hoard. When made available by waves, seagrass leaves and algae are caught by the shrimps which wait at their burrows openings and are then brought into specialised debris chambers. One species studied, the Mediterranean Pestarella tyrrhena does then not further tend this plant debris, it leaves it in 15 to 20 cm sand depth and may later return to consume small parts of it but may also find other neighboured shrimps` hoards during their frequent diggings through the sediment. The other species which shows a similar caching behaviour, the Caribbean Corallianassa longiventris, cares for the introduced plant debris continuously. The leaves are cut into small pieces within several weeks and are frequently transported from one to another chamber nearby with different chemical conditions. Low oxygen and pH values and high sulfide concentrations prevail in such chambers. The plant fragments are continuously scraped and bitten with the shrimps` mouthparts, they get smaller and 6 g(dry weight) debris are consumed within about 100 days as witnessed in narrow aquaria in which the animals lived for several years. A specialised group of bacteria and small nematode worms live inside the burrows of the shrimp which may contribute to the enhanced nutrient and vitamin levels which we found in the debris chambers and in the lining of the burrow walls.