Spatial distribution of detrital resources determines the outcome of competition between bacteria and a facultative detritivorous worm

Macrobenthic deposit feeders and bacteria compete for the same detrital food resources. We hypothesize that the spatial scale at which food is distributed in the sediment is an important factor determining the outcome of this competition. Macrobenthic deposit feeders are better adapted for fast consumption of food in concentrated patches, whereas diluted food can only be exploited by bacteria. This hypothesis was tested in an experiment in which a fixed quantity of isotopically labeled algal detritus was offered to a natural bacterial community and the polychaete worm Nereis (5Hediste) diversicolor, either as a concentrated patch or mixed through the sediment matrix. Worms dominated food uptake in the concentrated treatment, while bacterial uptake was much greater in the diluted treatment. The experiment demonstrated scale-based niche differentiation between these taxonomically distant groups. It also showed that worms spatially redistributed food and made it available to bacteria in that way. Together, these mechanisms may stimulate stable co-existence through a scale-based partitioning of resources. Competition between organisms belonging to different kingdoms is an important gap in ecological studies (Hochberg and Lawton 1990). A widespread but understudied instance is the competition for organic matter between bacteria and higher organisms in aquatic sediments. Macrobenthic deposit feeders and bacteria share similar food resources, namely detrital organic matter deposited on, or buried in, sediments. Both bacteria and macrofauna are known to have a wide potential for hydrolysis and assimilation of the available organic detritus in sediments. They thus seem to directly compete for these available resources. Apart from this competition, macrofauna also ingests bacteria, resulting in omnivory (HilleRisLambers et al. 2006). However, it is unlikely that bacteria are a major food component for macrobenthic deposit feeders, at least quantitatively (Kemp 1987). Despite this potential for overlap in food resources, a detailed study of an intertidal benthic food web showed very different feeding links for macrofauna and bacteria (Van Oevelen et al. 2006). Two mechanisms are thought to influence the division of resources between macrobenthic deposit feeders and bacteria. First, as proposed by Mayer et al. (2001), resource partitioning between bacteria and animals may be explained by differences in digestive systems. Deposit feeders have high-intensity digestion within a digestive tract, whereas bacteria use a low-intensity hydrolysis based on extracellular enzymes. Within an animal digestive tract, organic matter is hydrolyzed at a rate that is two to three orders of magnitude higher than in the ambient sediment under bacterial attack. These authors suggest that the metabolic cost of the high-intensity digestive system of deposit feeders can only be compensated for when they feed on high-quality resources, whereas bacteria can live off low-quality organic matter. In addition, bacteria are also known to possess the widest range in digestive abilities, including the possibility to hydrolyze very recalcitrant substrates such as lignin, cellulose, or even crude oil. However, such compounds are relatively rare in marine sediments. Moreover, marine organic matter is generally of high quality and relatively rich in nitrogen, at least when compared to terrestrial systems (Herman et al. 1999). As an alternative hypothesis, we propose that the competitive ability of both groups depends on the spatial distribution of the food sources. The spatial distribution of food sources has been shown in theoretical studies to have a large effect on resource partitioning between large and small organisms with similar feeding requirements but a different ‘perceptive scale’ (Szabó and Meszéna 2006). The perceptive scale (Holling 1992) is the size of the window through which an organism views the world. Small patches of food are noticeable resources for small consumers but remain unnoticed (or are unexploitable) by large animals. Szábo and Meszéna (2006) show that scale of spatial resource distribution can lead to niche differentiation, even for a single resource type. Ritchie and Olff (1999) use the same principle to derive body size distributions of animals feeding on similar resources distributed spatially over several scales. The hypothesis of scale niches, resulting from resource aggregations at different scales acting as distinct resources, seems particularly applicable to the case of bacteria and macrofauna in sediments. At the perceptive scale of bacteria (on the order of micrometers) the sediment forms a very heterogeneous environment. Within this environment, bacteria are, on average, spaced some tens of micrometers apart, although 1 Present address: University of Potsdam, Institute of Biochemistry and Biology, Department of Ecology and Ecosystem Modeling, Potsdam, Germany * Corresponding author: [email protected] Limnol. Oceanogr., 54(5), 2009, 1413–1419 E 2009, by the American Society of Limnology and Oceanography, Inc.