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Impact of Pestarella Tyrrhena on Benthic Metabolism in Sediment Microcosms Enriched with Seagrass and Macroalgal Detritus

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Impact of Pestarella Tyrrhena on Benthic Metabolism in Sediment Microcosms Enriched with Seagrass and Macroalgal Detritus MARINE ECOLOGY PROGRESS SERIES Vol. 281: 165–179, 2004 Published November 1 Mar Ecol Prog Ser Impact of Pestarella tyrrhena on benthic metabolism in sediment microcosms enriched with seagrass and macroalgal detritus Sokratis Papaspyrou1,*, Maria Thessalou-Legaki1, Erik Kristensen2 1Department of Zoology-Marine Biology, University of Athens, Panepistimiopolis, 157 84 Athens, Greece 2Institute of Biology, University of Southern Denmark, 5230 Odense M, Denmark ABSTRACT: The impact of Pestarella (= Callianasa) tyrrhena (Decapoda: Thalassinidea), a common + – burrowing shrimp in the Mediterranean Sea on sediment–water fluxes (O2, TCO2, NH4 and NO3 + – + NO2 ), sediment characteristics (organic matter, chlorophyll a) and porewater solutes (TCO2, NH4 – – and NO3 + NO2 ) was investigated in laboratory microcosms over a period of 42 d. Microcosms con- taining homogenised fine sandy sediment were amended with either dead Posidonia oceanica leaves or fresh Ulva lactuca thalli. Reworking activity by the animal resulted in a rapid burial of surface + deposited organic matter into the sediment. Porewater profiles of both TCO2 and NH4 indicated that P. tyrrhena activities result in a significant flushing of porewater solutes. Total sediment metabolism and carbon mineralisation were enhanced in the presence of P. tyrrhena. Metabolism of P. tyrrhena individuals was approximately 3 times higher in Ulva-amended sediment, probably due to a high activity level when nutritious food sources are in excess. Accordingly, animal respiration explained approximately half of the total enhancement in Ulva-amended sediment, while microbial decompo- sition of refractory seagrass detritus contributed about 4 times more to the stimulated carbon miner- alisation than animal respiration. Despite the higher initial addition of carbon in Posidonia-amended sediment compared to Ulva-amended sediment, the amount of excess carbon mineralised was 4.7 times higher in the latter, indicating that mineralisation processes depend on the degradability rather than the quantity of the organic pool. Although P. tyrrhena excretion constituted only a minor part of the total nitrogen mineralised, macrofaunal activities were the major factor affecting total nitrogen mineralisation, and not the enrichment with organic matter. KEY WORDS: Bioturbation · Pestarella tyrrhena · Posidonia oceanica · Ulva lactuca · Benthic fluxes · Nutrient change Resale or republication not permitted without written consent of the publisher INTRODUCTION and burrowing activities, whereas mucous secretions and faecal pellet deposition introduce new reactive The role of benthic macrofauna in modifying coastal substrates for microbial decomposition (Aller et al. sediment properties, metabolism and nutrient ex- 1983, Branch & Pringle 1987, Christensen et al. 2000). change has been well documented (Aller et al. 1983, The presence of deep and complex tubes and burrows, van Duyl et al. 1992, Pelegri & Blackburn 1995, Kris- on the other hand, increases the sediment–water sur- tensen 2000). Macroinfaunal structures and activities face available for solute exchange (Koike & Mukai create a variety of physico-chemical and biological 1983, Ziebis et al. 1996). Combined with macrofaunal microenvironments with potential impact on the distri- irrigation effects, such as porewater flushing and intro- bution and composition of microbial communities, as duction of oxygen deeper in the sediment, these struc- well as rates of sediment processes. Sediment particles tures affect the vertical distribution of diagenetic reac- and organic matter are redistributed by faunal feeding tions (Aller 1994, Banta et al. 1999). Various *Email: [email protected] © Inter-Research 2004 · www.int-res.com 166 Mar Ecol Prog Ser 281: 165–179, 2004 burrow-dwelling infauna have been shown to stimu- ing decomposition and recycling of the most important late the total microbial respiration and enhance solute source of organic matter (Cebrian & Duarte 2001). exchange in sediments by 25 to 271% (Kristensen Mass occurrence and subsequent collapse of drifting 2000). The stimulatory effect depends on a number of macroalgae, on the other hand, can be a serious prob- key factors, e.g. faunal density, mobility, size and feed- lem in eutrophic coastal bays, causing mass mortality ing type, as well as quantity and quality of organic of the indigenous flora and fauna (Morand & Briand matter (van Duyl et al. 1992, Forster & Graf 1995, 1996, Herbert 1999). This serious environmental Hansen & Kristensen 1998, Banta et al. 1999, Bartoli et impact may be alleviated when burrowing infauna is al. 2000). capable of accelerating decomposition processes and, Thalassinidean shrimps represent an important com- thus, the removal of macroalgal carbon and nitrogen ponent of the marine benthos in many intertidal and (Hansen & Kristensen 1997, Bartoli et al. 2000). subtidal areas. They have been recognized for their The aim of the present study was to quantify the im- importance as bioturbators with a significant impact on pact of the thalassinidean shrimp Pestarella tyrrhena on the environment. This includes enhanced sediment decomposition of organic matter and nutrient exchange turnover, organic matter subduction and nutrient in sediments amended with 2 types of commonly en- cycling (Waslenschuk et al. 1983, Branch & Pringle countered plant detritus in coastal areas of the Mediter- 1987, Ziebis et al. 1996, Webb & Eyre 2004), altered ranean Sea. Mineralisation of fresh, easily degradable, structure of benthic bacterial and faunal communities green macroalga Ulva lactuca and of dead, more (Berkenbusch et al. 2000, Dworschak 2001) and redis- refractory, seagrass Posidonia oceanica was followed tribution of metals and contaminants (Suchanek et al. by monitoring the fluxes of TCO2, O2 and dissolved in- 1986, Abu-Hilal et al. 1988). Pestarella (= Callianassa) organic nitrogen (DIN) species across the sediment– tyrrhena (Petagna, 1972) is the most common tha- water interface for a period of 42 d. Moreover, the lassinidean shrimp inhabiting sandy and muddy sub- vertical distribution of sediment characteristics and strates in the lower intertidal and shallow subtidal porewater solutes was measured at the end of the zones along Mediterranean coasts. P. tyrrhena bur- experimental period. Our results not only provide infor- rows consist of a more or less symmetrical upper U- mation on the effect of P. tyrrhena bioturbation on shaped section and a vertical shaft in the form of a spi- solute fluxes, but also on carbon and nitrogen minerali- ral reaching a maximum depth of at least 62 cm sation stoichiometry of seagrass and macroalgal detri- (Dworschak 2001). The shaft is characterised by seg- tus in Mediterranean coastal sediments. ments of constant diameter linked to wider chambers (turning chambers) and to short side branches. The burrow shape changes over time due to the constant MATERIALS AND METHODS reworking activity by the animal. P. tyrrhena, a deposit feeder, takes up sediment from one part of the burrow, Sediment and animal collection. Sediment, animals feeds for several seconds, and then transports the and plant material were collected from an intertidal- remaining material into existing branches of the shallow subtidal sand flat at Vravrona Bay (southern burrow or out to the sediment surface creating cha- Evoikos Gulf, Aegean Sea) in May 2001. The sediment racteristic mounds (Dworschak 1987, Kapareliotis consisted of moderately organic-rich fine sand (2.2% 1996). Although comprehensive knowledge exists on organic content as loss-on-ignition, LOI), with a P. tyrrhena biology, such as burrow structures, popula- medium particle size of 0.2 mm. The mud shrimp tion dynamics, reproduction and physiology (Ott et al. Pestarella tyrrhena occurs at a mean yearly population 1976, Dworschak 1987, 2001, Thessalou-Legaki et al. density of 63 ± 9 ind. m–2, reaching 144 ind. m–2 in 1997, 1999), the effect of this important bioturbator on some cases (Thessalou-Legaki 1987). Other common, sediment–water fluxes and porewater solute distribu- but low in abundance, macrofaunal species found in tion is almost unknown. the area include other thalassinids (Upogebia pusilla, Seagrasses and macroalgae are common sources of Calliax punica), polychaetes (Notomastus latericeus, organic matter in coastal areas inhabited by thalassi- Phylo foetida, Microspio mecznikowianus, Neanthes nidean shrimps. Burrow chambers of Pestarella caudata) and amphipods (Urothoe pulchella, Erictho- tyrrhena are often loaded with seagrass detritus that nius brasiliensis) (Nicolaidou & M. T.-L. unpubl. data). originates either from in situ seagrass meadows or The macrophyte vegetation consists of scattered occur- material transported from adjacent areas. This detritus rence of the seagrass Cymodocea nodosa, mainly in is probably used directly or indirectly (by ‘gardening’) the outer part of the sand flat (Thessalou-Legaki 1987). as food (Ott et al. 1976, Dworschak 1987, 2001). Benthic microalgae, on the other hand, are most abun- P. tyrrhena may therefore have an important effect on dant in the inner part of the sand flat, but contribute the food web dynamics in such ecosystems by enhanc- only a small part to the sediment organic pool (S. P. et Papaspyrou et al.: Impact of Pestarella tyrrhena on benthic metabolism 167 al. unpubl. data). Dead leaves of another seagrass spe- each treatment were also sacrificed to determine any cies, Posidonia oceanica, are continuously transported changes in sediment and porewater conditions
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