Bacterial Suspension Feeding by Coral Reef Benthic Organisms

MARINE ECOLOGY PROGRESS SERIES Vol. 175: 285-288,1998 Published December 17 Mar Ecol Prog Ser

NOTE

Bacterial suspension feeding by coral reef benthic organisms

R.P. M. ~ak',~~',M. Joenje2, I. de Jong1s2, D. Y. M. ~ambrechts~,G. Nieuwland'

'Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1970 AB Den Burg, Texel. The Netherlands 21nstitute for Systematics and Population Biology, University of Amsterdam, The Netherlands

ABSTRACT: The l~nkagebetween the pelagic microbial loop bution of reef sponges over areas such as the Great in coral reefs and reef benthic communities needs study in Barrier Reef (Australia) and the Caribbean basin by view of changing characteristics of trop~calcoastal seas. We availability of nutrients and organic matter. Important conducted field experiments, using standard microbial techniques, to assess the uptake of natural water-borne bacteria in such hypotheses is the emphasis on the increase in (at natural densities, 0.4 to 0.6 X 106 cm-3) by 2 common Carib- heterotrophy in affected reefs. Reef sponges are well bean reef organisms, the scleractinian coral Madracismira- known for their use of water-borne living particles, bilis and the colonial ascidian Trididemnum solidun1 The such as bacteria (Reiswig 1974, Pile 1997). data show that these organisms are effective bactenal sus- Such a trophic relationship between reef organisms pension feeders. Feeding rates of 0.75 to 1.07 X log bacterial cells 100 cm-2 h-' translate into a nitrogen input of 3 to 4 nmol and water-borne bacteria, the organisms at the base of N cm-2 h-' These values indicate that a large part of the nitro- the pelagic food web (Fenchel 1987), is highly interest- gen derived from particulate sources could be supplied by ing in view of an increased terrestrial influence in the bacteria. We suggest that such efficient linkage between ocean. The majority of the organic material running these reef organisms and the pelagic microbial communities explains the increasing/continued abundance of such benthic into the sea will enter the 'microbial loop' (Azam et al. organisms on detenorating Caribbean reefs. 1983). There are few data on the linkage of reefs and pelagic bacteria, but recent data show that reef bot- KEY WORDS: Coral reef. Pelagidbenthic coupling. Bacteria . toms actively reduce concentrations of bacteria in the Suspension feeding. Heterotrophy . Ascidia . Nitrogen budget adjacent part of the reef water column (Gast et al. 1998). This suggests a possibly important pathway between large-scale oceanic eutrophication and change in reef communities. However, little attention has Vast changes in human demography and distribu- recently been paid to the trophic relation between tion are causing changes in seatvater quality along non-sponge reef benthos and pelagic bacteria (see tropical coasts, and over increasingly larger areas. Lessios & Macintyre 1997). The methodology of the Such changes in water quality can have an enormous pioneering earlier studies (see Sorokin 1993), show- impact on marine communities. One of many examples ing that corals consume pelagic bactena, is outdated is the complete disappearance of once thriving coral (Ducklow 1990). No data at all are available for reefs (Umbgrove 1939) from the Bay of Jakarta, Atlantic reefs where, for unknown reasons, significant Indonesia (Tomascik et al. 1997), but it is currently changes in reef biota are occurring (Ginsburg & Glynn hypothesised that coral reefs are corrupted on a far 1994). greater scale, such as caused by the effects of runoff Materials and methods. We present 2 field experi- from whole continents (e.g. the ongoing debate on ments, using currently standard microbial techniques, [email protected]).That characteristics of to investigate the consumption of reef water column large bodies of water influence coral reef benthic biota bactena by 2 benthic reef organisms, Madracis mirabilis over megascales has been proposed for groups such as (Duchassaing & Michelotti), a small-branched sclerac- sponges. Wilkinson (Wilkinson 1987, Wilkinson & tinian coral, and Trididemnum solidum (van Name), an Chesire 1990) explained variation in the spatial distri- encrusting colonial ascidian. These are common organisms at the reefs of Curaqao in the southern Carib- bean (Bak & Criens 1981, Bak et al. 1981, 1996b). We used fluorescently labelled bacteria (FLB, Sherr et al.

O Inter-Research 1998 Resale of fullarticle not permitfed Mar Ecol Prog Ser 175. 285-288, 1998

1987) in pllot experiments to show that bacteria are ascidian are effective bacterial suspension feeders. taken up by these organisms, e.g. captured in the Concentrations of bacteria remained constant in con- digestive zones of the mesenteries. We performed our trol conditions (Fig. 1). Bacterial growth and possible in situ experiments at a depth of 5 to 10 m, enclosing nanoflagellate/ciliate predation are either balanced or experimental colonies in ambient reef water (27°C) insignificant. Gast (1998) found bactenal growth not to containing the naturally occurring bacteria. The indi- result in appreciable changes in cell numbers at this vidual bacteria are small, <0.2 pm3, and they occurred reef over such short time scales and microbial interac- at normal densities, 0.4 to 0.6 X 106 cm-3 (Gast et al. tion, such as nanoflagellate predation, to be negligible. 1998). We measured the change in natural bacterial Bacterial suspension feeding has been reported for abundance in experimental and control cylinders. Bac- asctdians and corals (Sorokin 1978, Jnrgensen et al. teria were homogeneously distributed and do not sink 1984, Schlichter 1991, Bak et al. 1996a) but our data do out (Kinrboe 1993, Karp-Boss et al. 1996). not imply that Madracis rnlrabilis or Trididernnum For each Madracis mirabilis expenment (n = 14) we solidum actually feed on free-living individual bacte- introduced 1 small colony (mean living colony surface rla. The bacteria in our experiments were not manipu- 51 cm2) underwater into separate, open, 1 1 plexiglass lated and consequently a large part may have been cylinders. For each Tr~didemnurnsolidum experiment attached to larger invisible particles, 'hotspots' (Azam (n = 8) a small encrusting ascidian colony (mean living 1998), such as colloids and polymer particles. Such surface 47 cm2) was used. Cylinders filled with ambi- larger particles could be the main vehicles facilitating ent seawater without experimental organisms were bacterial intake. These particles disintegrate during employed as controls (n = 4 for each series) After clo- our sampling procedure but the homogeneous distrib- sure of the cylinders with 2 0-ringed lids at the start of ution of bacteria in the enclosures indicates a similar the experiment, each cylinder was sampled (3 cm3) for distribution of these particles (Wells & Goldberg 1994). bacteria through a rubber membrane that gave access We do not assume the bacterial uptake rates to rep- to the seawater in the cylinder at t = 0 and at expen- resent typical or maximum rates of bacterial suspen- mental time intervals (see abscissa of Fig. 1). Bacteria sion feeding of these organisms. However, they show were immediately fixed, in 2 cm3 sterile formaldehyde the great potential for coupling of the microbial pelagic (5%), in the sampling syringe. Samples were stained to sessile reef organisms. There are a number of con- (Acridine Orange), filtered onto 25 mm 0.2 pm Sudan siderations. Even though the experimental organisms Black stained polycarbonate filters (Nuclepore) (Hob- were allowed to recover from handling (being placed bie et al. 1977) and counted using epifluorescence in the cylinders >20 h in advance of each experiment) microscopy (Zeiss Axiophot). At least 10 grids (40 X the colonies were slightly disturbed at t = 0 and the 40 pm) and 200 cells were counted on each slide (van coral polyps, and individual ascidian modules, showed Duyl et al. 1990, Bak et al. 1995). different stages of expansion/relaxation. This is re- Results and discussion. The data show a significant flected in the variation in feeding rates of the indi- decrease in bacterial densities in the experimental vidual colonies (Table 1). None of the organisms was cylinders (Fig. l), demonstrating that the coral and the totally expanded. In addition, all experimental organ-

Table 1. Bacter~alconsumption (no X 103 h-') rates for each colony (surfaces normalised to 100 cm2)

Colony A/ladracis mirabilis Tridldernnum solidum

Fig 1 Madracls m~rabills, Tndidemnum solidunl Bacterial suspension feednng of expenmental colonies (colony surfaces normallzed to 100 cmZ)in expenmental chambers (n = 14 far M mirablhs, n = 8 for T solidurn) and bactenal denslty In controls (n = 4 for both) Vert~calbars ~ndlcateSE Bak et al.: Feeding by reef benthic organisms 287

isms were cleaned for fouling organisms and checked Acknowledgements. We are indebted to the staff of Carmabi to ensure that no clionid sponges were present. How- for their continuous support and thank Drs John C. Bythell, ever, the ascidian colonies are encrusting and they dis- Gert Jan Gast, Fleur C. van Duyl and Birthe Gade for their comments on the manuscript. Thls 1s NIOZ contribution 3338. integrate rapidly if removed from their substratum. Consequently they were used in the experiments while encrusting their natural silbstratum, thin plates of dead LITERATURE CITED coral rock, and the presence of an occasional clionid Azam F (1998) h4icrobial control of oceanic carbon flux: the sponge in the substratum cannot be ruled out. plot thickens. Science 280:694-696 There are 2 relevant questions: firstly, are such feed- Azam F, Fenchel T, Field JG, Gray JS, Meyer-Keil LA, ing rates (Fig. 1) of ecological importance and, sec- Thingstad F (1983) The ecological role of water-column ondly, is there a relation with changes in the marine microbes in the sea. Mar Ecol Prog Ser 10:257-263 environment? The ecological importance would pri- Bak RPM, Criens SR (1981) Survival after fragmentation of colonies of Madracis mirabilis, Acropora palmata and A manly be in terms of nutrient (N, P) uptake. Madracis cerr~icornis(Scleractinia) and the subsequent impact of a mirabilis and Trididemnum solidum have endosym- coral disease. Proc 4th Int Coral Reef Symp 2:221-227 bionts and large parts or all of their carbon budget will Bak RPM, Nieuwland G (1995) Long-term change in coral be supplied by these symbionts (Sybesma et al. 1981, communities along depth gradients over leeward reefs in the Netherlands Antilles. Bull Mar Sci 56:609-619 Muscatine 1990).Extrapolating the mean feeding rates Bak RPM, Sybesma J, Van Duyl FC (1981) The ecology of measured during the initial 20 min interval (Fig. l), the tropical compound ascid~anTrididemnum solidum. 11. assuming a carbon content of 20 fg cell-' (Lee & Abundance, growth and survival. Mar Ecnl Prog Ser 6: Fuhrman 1987) and a C:N:P ratio of 45:10:1 (Zweifel et 43-52 al. 1993), gives an uptake rate of 2.8 nmol N cm-' h-' Bak RPLI, van Duyl FC, Nieuwland G (1995) Organic sedi- mentation and macrofauna as forcing factors in marine for M. nlirabilis and 4.0 ninol N cm-' h-' for T solidum. benthlc nanoflagellate communities. Microb Ecol 29: These are significant amounts (cf. Bythell 1988, 1990, 173-182 Szmant 1991). A study using the coral Acropora pal- Bak RPM, Gast GJ, Joenje M, de Jong I, Lambrechts DYM, mata showed 70%, or 8.75 nmol N cm-'h-', of the total Nieuwland G (1996a) The use of fluorescently labelled bactena (FLB) in studying change in coral reef benthos fil- nitrogen budget to be derived from particulate sources ter-feeding conditions. Abstracts, 8th Int Coral Reef Symp. (Bythell 1988). Bacterial suspension feedlng at rates Smithonian Tropical Research Institute, Balboa, Panama, such as in our experiments would represent 30 to 45 % P 11 of such a particulate feeding pattern and actual uptake Bak RPh.1, Lambrechts DYM, Joenje M. Nieuwland G, Van rates, for naturally expanded colonies, could be much Veyhel MW (199613) Long-term changes on coral reefs in booming populatlons of a competitive colonial ascidian higher. Mar Ecol Prog Ser 133:303-306 It appears that Madracis mira bilis and Trididemn urn Bythell JC (1988) A total nitrogen and carbon budget for the solidum are linked through suspension feeding to the elkhorn coral Acropora palmata (Lamarck). Proc 6th Int water column bacteria. Both organisms are very com- Coral Reef Symp 2:535-540 Bythell JC (1990) Nutnent uptake in the reef-building coral mon in Curaqao on the reefs close to, and down- Acropora palmata at natural environmental concentra- current of, human activity and urban development. tions. Mar Ecol Prog Ser 68:l-2 At least one of them, T. solidum, may be positively Ducklow HW (1990) The biomass, production and fate of bac- responding to increased eutrophication. The abun- teria in coral reefs. In: Dubinsky Z (ed) Coral reefs. Else- dance of T solidum has increased exponentially over vier, Amsterd.am. p 265-290 Fenchel T (1987) Ecology-potential5 and limitations. In: the last 15 yr (Bak et al. 1996b). Such an increase is not bnne 0 (ed) Excellence in ecology, Book 1. Ecology Insti- documented for M. mirabilis. However, although other tute, Oldendorf/Luhe dominant corals have decreased in cover (e.g. Acro- Gast GJ (1998) Microbial densities and dynamics in fringing pora paln~ata,Montastraea annularis) over the reefs coral reef waters. PhD thesis, University of Amsterdam Gast GJ, Wiegman S, Wieringa E, van Duyl FC, Bak RPM in Curacao (Bak & Nieuwland 1995), M. mirabilis con- (1998) Bacte1i.a in coral reef wdter types: removal of cells, tinues to occur in extensive monospecific beds which stimulation of growth and mineralization. Mar Ecol Prog appear to remain essentially unchanged (van Duyl Ser 167:37 -45 1985, Gast unpubl.). 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Editorial responsibility. Otto Kinne (Editor), Submitted August 6, 1998; Accepted. November 18, 1998 OldendorfILuhe, Germany Proofs received from a uthor(s): December 10, 1998