Cnudde, C. (2013). Effect of food preservation on the grazing behavior and on the gut flora of the harpacticoid copepod Paramphiascella fulvofasciata. Ph.D. Thesis, University of Gent, Belgium. 223 pp.
479619
Cnudde, C.
2013
Effect of food preservation on the grazing behavior and on the gut flora of the harpacticoid copepod Paramphiascella fulvofasciata.
Ph.D. Thesis, University of Gent, Belgium
223 pp.
Publication
Available for editors
In the era of rapidly changing natural environments, there is an urgent need for understanding biodiversity-ecosystem functioning. Trophic interactions play a key role in structuring the ecosystem. In marine systems, the feeding ecology of the larger-sized species i.e. (top) predators of food webs, is fairly well documented, yet at the basal level of food webs, the complexity of grazer interactions is much higher and trophic linkages are potentially still missing. In this PhD thesis, the focus is on trophic interactions between harpacticoid copepods and bacteria.
The meiofauna (organism size between 38 µm and 1 mm), and in particular harpacticoid copepods (the second most abundant group of the meiofauna, after nematodes), transfer microphytobenthos to higher trophic levels, predominantly larval and juvenile fish. Harpacticoids have highly complex feeding habits. They are able to consume a wide range of food sources, e.g. microalgae, cyanobacteria, flagellates, ciliates, mucoid substances, fungi and heterotrophic bacteria. They are therefore sometimes called ‘indiscriminate feeders’. However, laboratory feeding experiments and recently obtained in situ data, demonstrate their highly selective behaviour and their species-specific food preferences. Under experimental conditions, harpacticoids discriminated among substrates with poor- versus well-developed bacterial films although copepods are considered to be morphologically incapable of consuming small-sized particles such as bacteria. Based on their potential interaction with a broad range of food sources, the general importance of their herbivorous feeding strategy is being questioned and the recent development of dietary tracers such as stable isotopes and fatty acid analysis, now allows to investigate direct assimilation of bacterial matter or that of other food sources. Interest into the pathways of transfer of benthic bacterial matter upwards the food web, for instance with harpacticoids as intermediates, is due to the lack of insight into the general fate of the extensive benthic bacterial biomass and potential pathways of transfer to higher trophic levels are still unknown. A proportion of energy flows back to the microbial-detrital pool as copepod fecal pellets which are efficiently degraded and remineralized. Beside the upward fluxes of biomass and energy, the degradation and reminerilization of waste products resulting from grazing activity is crucial for the recycling of biomass and thus the efficiency of ecosystem functioning.
We gained insight into food utilization by harpacticoids in a heterogeneous estuarine intertidal ecosystem, into species-specific feeding patterns and into the trophic importance of bacteria for harpacticoids. Feeding ecology was studied based on both field data of the harpacticoid species assemblages and on experimental laboratory data using individual species. The process of fecal pellet degradation was investigated with focus on the contribution of internal and external fecal pellet bacteria during early degradation and remineralisation of fecal pellets. In an attempt to gain information on the presence of internal bacteria and their position in the fecal pellet, Atomic Force Microscopy and Laser Scanning Confocal Microscopy (AFM-LSCM), a high-resolution imaging tool, was applied. It offers new prospects for studying microbial degradation of copepod fecal pellets.
Harpacticoid assemblages for chapters 2 and 3 were studied at the Paulina intertidal area (Schelde estuary, The Netherlands) encompassing a gradient from tidal flat to salt marsh, from seasonal periods at five stations differing in sediment characteristics, tidal exposure, presence of vegetation, etc.
To address the structural role of environmental factors, including abiotic sediment characteristics and food-related factor, for harpacticoid assemblages and disclose resource partitioning within harpacticoid assemblages, chapter 2 presents a field study into spatial-temporal heterogeneity in resource availability and in intertidal copepod assemblage structure (density, diversity and composition). An in-depth analysis of the most influential factors for species distribution added relevant information to the autoecology of intertidal harpacticoid species. Spatio-temporal harpacticoid assemblage variation was assigned to variables relating to total organic matter, microphytobenthic biofilms (characterised by pigments and their degradation products), differences in detrital origin and NH4 + , suggesting a primary influence of food. availability and quality. Nevertheless, harpacticoid assemblages of tidal flats were seemingly more structured by abiotic factors (granulometry and tidal exposure) and especially the harpacticoid assemblage of the sand flat (station H2, species Paraleptastacus spinicauda, Asellopsis intermedia) which was highly station-specific and constant over time. Assemblages of salt marsh stations are considerably similar in copepod family composition despite of differences in salt marsh granulometry, suggesting a primary influence of food availability and food quality. Variability in Microarthridion littorale abundances is related to microphytobenthos biomass. For Ectinosomatidae and Tachidius discipes, the limited number and low correlations for all biotic and abiotic factors indicates a generalistic occurrence. For some species, linkages between habitat characteristics and species distributions were little decisive (e.g. Platychelipus littoralis, Paronychocamptus nanus, Amphiascus sp. 1). Overall, high intercorrelation between a broad range of environmental factors hinders us to draw strong conclusions about the main regulating factors for harpacticoids distribution.
Analysis of spatio-temporal variability in resource utilization by harpacticoid copepods, by means of copepod carbon isotopic profiles and fatty acid profiles (chapter 3), proved that the majority of intertidal harpacticoid species relied strongly on microphytobenthos (MPB) as a food source, with potentially finescaled selectivity among diatom species or other MPB components. In addition, harpacticoids spanned two trophic levels suggesting also an indirect pathway of MPB transfer to harpacticoids. Furthermore, intertidal harpacticoids showed dietary differences and species-specific spatio-temporal variability in food utilization with contributions of suspended particulate organic matter (Paronychocamptus nanus, Amphiascus sp. 1, Microartridion littorale), flagellates (M. littorale), and bacteria (Delavalia palustris) but not of Spartina detritus. Resource partitioning by harpacticoid assemblages occurred in all stations but was especially clear in the sand flat, comprising a diatom feeder (Asellopsis intermedia), a diatom feeder with temporal reliance on dinoflagellates (Tachidius discipes) and a bacterial feeder (Paraleptastacus spinicauda). In the muddy salt marsh, a trophic role of bacteria was found for Delavalia palustris and Cletodidae, the latter being unique by the utilization of a chemoautotrophic food source.
In chapter 4, results from a microcosm feeding experiment using 13 C-labelled bacteria, showed that bacterial feeding is linked to diatom grazing and that overall assimilation of bacterial carbon is low for all tested harpacticoid species. In contrast to the bacterivorous copepod Delavalia palustris, nonbacterivorous harpacticoid species (Nannopus palustris, Microarthridion littorale, Platychelipus littoralis) responded negatively on bacterial feeding, as deduced from their mortality and PUFA (polyunsaturated fatty acid) impoverishments. These findings suggest that bacterial biomass may complement feeding on MPB and that an exclusive bacterial diet does not meet copepod nutritional requirements. Delavalia palustris was able to biosynthesized PUFA from a bacterial diet but generally, bacteria represent a minor and low-quality food for these intertidal harpacticoid copepods.
