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Mass sedimentation of the swimming crab Charybdis smithii (Crustacea: Decapoda) in the deep Arabian Sea
Deep-Sea Research II 47 (2000) 2673}2685
Mass sedimentation of the swimming crab Charybdis smithii (Crustacea: Decapoda) in the deep Arabian Sea Bernd Christiansen *, Antje Boetius GEOMAR, Wischhofstr. 1-3, 24148 Kiel, Germany Baltic Sea Research Institute, Seestr. 15, 18119 Rostock-Warnemu( nde, Germany Received 26 April 1999; received in revised form 18 November 1999; accepted 30 November 1999
Abstract During cruise Meteor 33/1 in the northern Arabian Sea in September/October 1995, large numbers of the portunid crab Charybdis smithii were observed swimming in the open ocean. In a photographic survey at three abyssal stations in the northern Arabian Sea (NAST, WAST, CAST), even higher densities of Charybdis smithii } up to 1 crab m\ } were found dead on the sea #oor. Average sizes of the crabs were around 34}44 mm carapace width, indicating that the animals died prematurely, before returning to the breeding grounds presumable on the shelves of India or Oman. The average weight of the crabs was 10}14 g wet weight. From the photographic quanti"cation it can be deduced that these large food falls represent a signi"cant carbon input of at least 10}30% of the annual #ux of POC as measured in sediment traps in this region. The exceptionally high microbial chitinase activity in the surface sediment layers detected at the same stations indicates that this energy is utilized and channelled into the deep-sea benthic food web of the deep Arabian Sea. There are frequent observations of dense Charybdis smithii swarms in the Arabian Sea from di!erent years; however, it is not certain whether such large food falls as observed during M 33/1 are regular seasonal events that repeat each year. 2000 Elsevier Science Ltd. All rights reserved.
1. Introduction The portunid crab Charybdis smithii is one of the very few swimming crabs that are frequently found in the open ocean. It is endemic to the Indian Ocean, where it can * Corresponding author. Current address: Institut fuK r Hydrobiologie und Fischereiwissenschaft, Zeiseweg 9, D-22765 Hamburg, Germany. Tel.: #49-42838-6686; fax: #49-42838-6696. E-mail address: [email protected] (B. Christiansen). 0967-0645/00/$ - see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 0 4 4 - 8
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form massive swarms dominating the standing stock of pelagic micronekton (Zamorov et al., 1991; van Couwelaar et al., 1997). These swarms of Charybdis have a major predatory impact on the pelagic fauna (Spiridonov, 1994) and have been found to clear the bait o! longlines in the Arabian Sea within a few hours (Merrett, 1968). A similar behaviour has been reported for the stomatopod Oratosquilla investigatoris in the Gulf of Aden and the equatorial western Indian Ocean (Losse and Merrett, 1971). However, the life cycle, the regional distribution, and the biology of Charybdis smithii are not completely understood. Zamorov et al. (1991) proposed that reproduction takes place o!shore after the SW monsoon, and that the larvae are transported with the monsoonal currents until they eventually return to the African shelf. By contrast, van Couwelaar et al. (1997) found evidence for a 1-yr life cycle for Charybdis smithii, with breeding of crabs from October to January on the continental shelves o! India, Oman, and probably also o! Africa, dispersal of the larvae o!shore with the NE monsoonal currents and the formation of pelagic swarms from July to August, after which the adults return to the breeding areas on the continental shelves. Van Couwelaar et al. (1997) propose a high mortality of 90% for the adult crabs before they return to the breeding grounds. There are several reports that the swarms of Charybdis smithii are an important food item for large pelagic "sh such as tuna (e.g., Spiridonov, 1994). Based on the discovery of portunid carapaces on the sea #oor and of dead crabs and parts of crabs in sediment traps, van Couwelaar et al. (1997) suggest that Charybdis smithii also may contribute to the vertical carbon #ux, but up to now no quantitative observations on the presence of carcasses of this species on the deep-sea #oor were available. During cruise Meteor 33/1 in September/October 1995 to the Arabian Sea, a megafauna survey was conducted at three stations in the open ocean. Along photographic transects at water depths of 3000}4000 m, we discovered large numbers of dead Charybdis smithii lying on the sea #oor, which we were able to analyse quantitatively. This mass sedimentation of the swimming crab Charybdis smithii likely induced a rise in benthic microbial enzymatic activity during this period in the northern Arabian deep sea.
2. Material and methods 2.1. Megafauna survey During cruise Meteor 33/1 to the Arabian Sea in September/October 1995, a videocontrolled epibenthic sledge (fototrawl, Christiansen and Nuppenau, 1997) and a deep-sea observation system (DOS, Christiansen, 1993) were used to sample epibenthic megafauna and to perform photographic transects. Fig. 1 shows the sampling stations in the Arabian Sea, and Table 1 presents the station data. The DOS was employed once at station NAST. The fototrawl was used twice at station WAST and once at station CAST. Each haul delivered a total of 800 frames.
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Fig. 1. Area of investigation.
The camera of the DOS was oriented perpendicular to the sea #oor. The photographed area was calculated from the lens data and the distance from the lens to the sea #oor (Christiansen, 1993). The distance to the sea #oor was estimated visually from the photographs and from the videos with the help of a weight hanging 3 m below the DOS. The size of the photographed area in the frames from the fototrawl transects was measured using a Canadian grid based on the elevation of the camera, the camera angle, and the lens data (Christiansen and Thiel, 1992). At NAST, an area of 2100 m was analysed, at WAST 1100 m, and at CAST 930 m. Crabs lying on the sea #oor were counted, and their density was estimated by dividing their number by the area photographed. Only crabs with an apparently intact carapace and at least some legs attached were counted. The Canadian grids were also used to measure the width of Charybdis smithii carapaces on frames from fototrawl transects. Only crabs clearly visible in the foreground of the frames and properly oriented were measured. Crab sizes on DOS photographs were calculated from size measurements on the frames, lens data, and distance to sea #oor.
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Table 1 Station data. The dates are given as day.month.year. The positions given for the DOS and the FT represent the starting positions of each haul Station
Gear no.
Date
Latitude
Longitude
Water depth (m)
NAST WAST WAST CAST NAST NAST NAST WAST WAST WAST CAST CAST CAST CAST CAST
DOS-9 FT-35 FT-36 FT-37 MC-01 MC-04 MC-06 MC-08 MC-12 MC-15 MC-16 MC-17 MC-18 MC-19 MC-21
27.09.1995 29.09.1995 30.09.1995 12.10.1995 24.09.1995 25.09.1995 26.09.1995 01.10.1995 04.10.1995 05.10.1995 08.10.1995 09.10.1995 09.10.1995 10.10.1995 10.10.1995
20300.00 N 16325.10 N 16310.04 N 14324.10 N 20300.02 N 19356.00 N 19359.94 N 16314.95 N 16312.97 N 16311.70 N 14324.93 N 14324.90 N 14324.97 N 14323.01 N 14325.94 N
065335.00 E 060343.80 E 060329.80 E 064333.50 E 065335.10 E 065338.00 E 065341.05 E 060330.92 E 060316.01 E 060318.40 E 064334.06 E 064331.94 E 064332.10 E 064334.05 E 064334.68 E
3186 3996 4028 3949 3185 3158 3164 4028 4034 4034 3943 3944 3943 3949 3941
DOS: deep-sea observation system. FT: fototrawl. MC: multiple corer.
2.2. Benthic microbial activities Sediment cores were obtained from several multiple corer hauls at each station (Table 1) and immediately subsampled for enzymatic activity and biomass of the benthic bacteria. The enzymatic activity (EEA) of the extracellular hydrolytic enzyme chitobiase was measured #uorometrically (Hitachi F}2000 spectro#uorometer) according to Boetius and Lochte (1994), using the methylumbelliferone (MUF)-labelled substrate MUF-N-acetyl-b-glucosaminide (Sigma, 100 lM). The enzyme assays were run in time-course experiments with three determinations during 2}4 h. The subsamples removed at each time point were centrifuged for 10 min (2800 g) at 03C. The supernatants were transferred into disposable UV-cuvettes (Ratiolab) and the #uorescence of MUF was measured at 365 nm excitation and 445 nm emission wavelength. Relative units of #uorescence were calibrated with 5 standard concentrations between 20 and 300 nM of MUF (Serva). Enzyme activity was calculated from the average of the changes in #uorescence during the time-course experiment (2}3 intervals). Subsamples for the determination of bacterial numbers and biomass were prepared according to the method of Velji and Albright (1985). Bacterial numbers were determined by epi#uorescence microscopy (ZEISS AXIOSKOP) after staining with acridine orange (Meyer-Reil and KoK ster, 1992).
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2.3. Enrichment experiment The top 4.5 cm of bulk sediment from several cores of one multiple corer were combined in a sterile glass bottle and diluted with an equal part of sterile "ltered (0.2 lm) bottom water. The sediment slurry was mixed thoroughly by shaking the bottle. One portion without additional substrate served as control. The rest of the sediment slurry was divided into smaller sterile glass bottles. A "rst subsample was removed for further analysis of microbial activities and biomass, representative of the conditions at day 0. The other portions were enriched with di!erent amounts of puri"ed chitin #akes from shrimp shells. Each bottle was thoroughly mixed and portions of 70 ml each were poured into sterile polyethylene (PE) bags so that one bag was available for each time interval. The PE bags were closed by welding and incubated in pressure vessels at in situ temperature of 23C and in situ pressure of 400 bar. The sediments were not stirred. At each time interval a pressure vessel was opened and the PE bags were removed. Analysis of enzymatic activities followed immediately. For bacterial numbers, 1 ml of the subsample was "xed in 9 ml of 2% formaldehyde solution and stored at 43C for later analysis in the home laboratory.
3. Results and discussion During cruise Meteor 33/1, swimming crabs were frequently observed at the sea surface at stations WAST and CAST as far as 1000 km from the shelves of Oman and India. They were obviously feeding on plankton and often attacked baited hooks laid out for "shing. At stations NAST and WAST they occurred in densities of approximately 0.1 Ind m\ as observed visually from the ship's deck during daytime. A few specimens were sampled from the surface waters and identi"ed as Charybdis smithii McLeay. The "rst hauls with the fototrawl and an otter trawl conducted at station WAST caught several kg of dead swimming crabs, which looked rather intact. First, we mistakenly regarded these crabs as pelagic contamination of the catch of abyssal animals recovered with the epibenthic net of the fototrawl and with the otter trawl, comprising mainly ophiuroids, sponges and holothurians. However, the photographs of the deep-sea #oor at station NAST (3190 m depth), WAST (4050 m) and CAST (3950 m) gave evidence of large amounts of swimming crabs lying dead on the sea #oor in di!erent states of decay (Fig. 2). Most specimens appeared to be rather intact, but single legs, parts of legs or broken carapaces were also seen. Table 2 gives the number of swimming crabs counted on the four photographic transects in the Arabian Sea. The stations sampled di!er clearly in the mean abundance of swimming crabs. Lowest abundances were found at station NAST with a mean of 0.04 Ind m\. At station WAST, the abundance of swimming crabs amounted to ca. 1 Ind m\, whereas station CAST lay in-between with 0.2 Ind m\. These di!erences were highly signi"cant (p(0.001; ANOVA with post hoc tests on squareroot-transformed data). Considering the patchy distribution of Charybdis smithii swarms in the Arabian Sea (van Couwelaar et al., 1997), this may re#ect the abundance of crabs in the surface layers or regional di!erences in mortality, but we
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Fig. 2. Photograph of dead Charybdis smithii on the sea #oor at station CAST.
cannot exclude also a temporal e!ect with regard to sampling date and time of mass sedimentation. The carapace width of 6 swimming crabs recovered from the sea #oor at station WAST was between 40 and 52 mm and the wet weight between 10 and 14 g. The size measurements from the photographs revealed median carapace widths of 34 mm at stations WAST and CAST and of 44 mm at station NAST (Fig. 3). We assume that most of the observed variance within stations is due to methodological constraints, and that the di!erence between the stations as well as the discrepancies between the photographic and the direct measurements can be attributed to the di!erent methods used for the size measurements.
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Table 2 Densities of Charybdis smithii at the sea #oor. Only crabs visible on the photographs with an apparently complete carapace and at least some legs attached to it were counted and their density was calculated Station
Haul no.
Number of frames
Specimens counted
Mean abundance (Ind m\)
Standard error
NAST WAST CAST
DOS 09 FT-35#FT-36 FT-37
483 1412 709
82 1077 185
0.04 0.95 0.20
0.004 0.031 0.015
Fig. 3. Box plot of carapace widths of Charybdis smithii as calculated from photographs.
The size range of dead crabs as estimated from the sea-#oor photographies, at least at stations WAST and CAST, seems fairly consistent with the size-frequency distribution detected during the R.V. Baldrige cruise in July}August 1995 in the upper 150 m of the ocean, with average sizes of the crabs of around 32 mm (van Couwelaar et al., 1997). However, considering a systematic underestimation of carapace widths on the photographs at WAST and Cast, as suggested by the comparison of direct vs. photographic measurements, the mean size of crabs on the sea #oor would be ca. 8}10 mm bigger than that from the R.V. Baldrige cruise. We propose that the death of the crabs preceded our sampling by only a couple of weeks, i.e. that sedimentation of carcasses started in mid-September. The guts of the crabs recovered with the epibenthic sledge were still complete and the muscle #esh was relatively "rm. In an experiment on the decay of shrimp in sea water kept at 203C, Briggs and Kear (1994) observed that the exoskeleton would stay visually intact for at least one week, but that most of the carapace degrades within eight weeks. The relatively small size of the crabs indicates that a large part of the swarm might have consisted of premature individuals. According to van Couwelaar et al. (1997) the
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crabs with an average size of 34}44 mm would need 1}2 further moults before reaching maturation. Thus, the crabs observed on the sea #oor had died before returning to the breeding grounds at the shelves of India or Oman. Our observations are the "rst evidence of a mass mortality of portunid crabs in the open ocean. Van Couwelaar et al. (1997) report "ndings of a few remnants of swimming crabs in sediment traps moored by R.V. Tyro at 1032}3047 m on the Somali continental margin and in the Somali Basin. At the open ocean station WAST, a small specimen of a swimming crab was caught in the deep trap moored 1000 m above bottom (T. Rixen, pers. comm.). Furthermore, crab bodies and pieces were observed on the sea #oor of the shelves and slopes of the Indian Ocean; however, it was not clear whether these were moults or carcasses of the crabs (van Couwelaar et al., 1997). These relatively scarce observations of sedimented crabs compared to the abundant "ndings of crab remnants in the stomachs of tuna and other large pelagic "sh led to the hypothesis that the mortality of adult swimming crabs is mainly caused by predation (Zamorov et al., 1991). Mass strandings of Charybdis smithii have been observed along the shores of South Africa, the reason for their death probably being unusual water temperatures (van Couwelaar et al., 1997 and literature therein). However, the reason for the death of the Charybdis swarms in the open ocean after the SW-monsoon remains unknown. There was no indication of extraordinary water temperatures or other hydrographical features at this time in the Arabian Sea in 1995 (Weller et al., 1998). Other possible causes for the mass mortality of the swimming crabs could be food shortage, toxic algal blooms, which have been frequently observed in the Northern Arabian Sea, or upwelling of anoxic waters from the oxygen minimum zone. However, such events are unlikely to extend in an area as large as was covered by our observations. Thus, it remains an open question whether death and sedimentation of the swimming crabs occur regularly as part of their life cycle, as does the formation of dense swarms in the surface waters. At station WAST, the density of approximately 1 crab m\ at the sea #oor is equivalent to a carbon biomass of ca. 1 g m\, assuming a mean carapace width of 40 mm, which corresponds to a wet weight of 10 g (van Couwelaar et al., 1997). Since no data on the carbon content of Charybdis smithii are available, we used a standard carbon/wet weight ratio of 10% for this calculation. Accordingly, the mean organic carbon pool in the form of dead crabs at NAST was 0.04 g m\, at CAST 0.2 g m\. There are strong indications that the crab carcasses do not accumulate on the sea #oor over a longer time period, but stem from the swarming season of one year. On sea-bottom photographs of the same area from Meteor cruise 31/3 in March 1995, no remains of Portunidae could be detected (U. Witte, pers. comm.). Assuming that all these dead crabs originate from one season's swarming, the biomass of C. smithii on the sea #oor observed after the SW-monsoon would be a minimum estimate for the annual #ux to the sea #oor by this species at the respective station. Compared with the average POC #ux of 3.2 g m\ yr\ measured with sediment traps at station WAST by Haake et al. (1993), the sinking carcasses of C. smithii would add at least 30% to the estimated annual POC supply at this station. At station CAST, the annual carbon #ux by C. smithii adds at least 10% to the annual C #ux of 1.9 g m\ yr\ measured in sediment traps there by Haake et al. (1993).
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Most of the carbon input by the crabs is in the form of chitin, which makes up approximately 20% of their dry weight (Smith et al., 1975; Hirano, 1989). No recognizable pieces of crab shells were discovered in deeper sediment layers of bottom samples recovered by box corers and multiple corers, indicating a complete degradation of the crab carcasses. Chitin is the most abundant polysaccharide in the marine environment; however, due to its low preservation potential it does not accumulate in marine sediments. Despite the fact that chitin is resistant to most chemical and physical agents, it is quickly dissolved by chitinolytic enzymes (Gooday, 1990). How is this large food fall utilized by benthic organisms? The typical abyssal megafauna at station WAST was predominantly composed of ophiuroids as well as of holothurians and porifera (Christiansen, unpublished). A massive euphausiid dead body rain serving as the main food source for abyssal ophiuroids was discovered in the South Atlantic Ocean (Sokolova, 1994). Accordingly, ophiuroids may utilize the dead crabs in the Arabian Sea, but in the photographs we never saw an ophiuroid in contact with a crab. Baited cameras deployed at stations NAST, WAST and CAST attracted "sh, penaeid prawns, amphipods and galatheid crabs (Janssen et al., 2000), which may be other potential consumers of the crab bodies. However, not many animals are able to digest chitin, which makes up a large fraction of the crab-POC, and probably most of them harbour chitinolytic microorganisms in their guts (Deming and Baross, 1993). Thus, it is likely that bacteria utilize much of the crab-POC. Bacteria can only take up small molecules; thus, the production of extracellular hydrolytic enzymes speci"c for the cleavage of substrates like chitin or cellulose is a prerequisite for their use as energy and nutrient source. Enrichment experiments with deep-sea sediments have shown that the natural microbial assemblages may produce high amounts of chitinolytic enzymes within days when chitin becomes available as a substrate. The bacteria may then utilize this C#N source with relatively high growth e$ciencies (Boetius and Lochte, 1996). Investing in the energyconsuming synthesis and excretion of enzymes is only bene"cial if the energy loss is compensated for by the gain in readily available products. The calculations of Vetter and Deming (1994) indicate that secretion of enzymes can only result in an energy gain via uptake of produced hydrolysate when external concentrations of polymeric substrates are very high. The amount of chitin introduced by the sedimentation of a crab to a square metre of sediment (approximately 1 g) is well above the background value of chitin in deep-sea sediments of 0.1 mg m\ (Poulicek and Jeuniaux, 1989). Consistent with our "ndings, high chitinolytic enzyme activities were detected in the sediments of the northern Arabian Sea, substantially exceeding those in other oceans as well as those in the Arabian Sea at other times of the year. To track the changes in activity potentials that were not related to variation in microbial biomass, biomassspeci"c extracellular enzyme activity (EEA) of the chitobiase was calculated, dividing hydrolysis rates by bacterial numbers. Fig. 4 shows the distribution of speci"c activities of the extracellular enzyme chitobiase in the Arabian Sea after the SWmonsoon in 1995, when the mass sedimentation of Charybdis was observed, compared to the activities during and after the NE-monsoon in 1997 and 1998. Speci"c chitobiase activities at two abyssal stations in the NE-Atlantic in summer 1996 and
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Fig. 4. Speci"c activity of the extracellular enzyme chitobiase in surface sediments of the Arabian Sea and the NE-Atlantic (0}1 cm). The black columns represent values measured in sediment samples of stations where dead crabs were occurring (CAST, NAST and WAST; M33/1, September/October 1995). Data from the NE Atlantic (station BIOTRANS, 4560 m, and BENGAL, 4810 m) are shown for comparison (M36/6, September/October 1996; M42/2, July/August 1998). No estimation of a standard error was possible because only 1}3 samples of bacterial biomass were analysed per station and cruise.
autumn 1998 are also shown for comparison. The activity per cell of chitobiase was twice as high in the Northern Arabian Sea in 1995 as during other times when no remnants of swimming crabs were detected at the sea #oor during megafauna surveys conducted with a TV observation system (U. Witte, pers. comm.). Furthermore, the biomass and the oxygen consumption of the sediment infauna at WAST were extremely high after the SW-monsoon in 1995, indicating a respiratory carbon demand which exceeded the POC input estimated via sediment traps approximately twofold (U. Witte, pers. comm.). However, in the "eld samples, bacterial cell numbers at sediment surface (0}1 cm) at NAST (1.3;10 cells cm\), WAST (1.4;10 cells cm\) and CAST (1.2;10 cells cm\) were not substantially increased in September 1995 compared to samples from other times (February/March 1998, April/May 1997, Boetius et al., 2000). Thus, we presume that the crab carcasses may add signi"cantly to the food supply of the benthic community and that a large fraction of this input is channelled to higher benthic organisms grazing on the bacteria. The e!ect of such a chitin enrichment on microbial activities in the sediment was tested on a sediment sample obtained at station NAST, where the highest speci"c chitobiase EEA was recorded in the "eld during the cruise M33/1 in September/October 1995. Approximately, 0.3 mg of coarse chitin #akes per ml of sediment slurry was added and the samples were incubated under in situ pressure and temperature. This is similar to the amount of chitin introduced by the fall of one crab to one square metre of sea #oor. To compare directly microbial chitobiase activity in the "eld with that in the experiment, biomass-speci"c EEA of the hydrolases was calculated. In the incubation of unenriched sediment, which served as control, speci"c EEA of chitobiase remained on a constantly low level during 32 d (Fig. 5). The speci"c chitobiase EEA of enriched sediment increased by an order of magnitude from day 7 to day 21. After 10 d, the level of enzyme activity reached in the enrichment
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Fig. 5. Enrichment experiments with di!erent amounts of chitin. The plots show the change in chitobiase activity over time in (a) a slurry of sediment obtained from station NAST (M 33/1) and (b) a slurry of sediment obtained from station SAST during another cruise (SO-118, 1997).
experiment was comparable to the speci"c EEA of chitobiase at stations NAST and WAST in September/October 1995 after the sedimentation of the crabs. After day 21, chitobiase EEA decreased again. During a later cruise (SO-118 in 1997), another enrichment experiment was performed with sediments from the relatively oligotrophic station SAST in the southern Arabian Sea. The addition of di!erent amounts of chitin induced chitobiase to di!erent levels relative to the availability of this substrate (Fig. 5). Again, the speci"c EEA of chitobiase increased by an order of magnitude within 10 d and decreased after 3 weeks. As indicated by these experiments and earlier observations (Boetius and Lochte, 1996, and literature therein), chitin is an important substrate for bacteria in deep-sea sediments and even high amounts as introduced by large food falls will be quickly remineralized. It remains unknown whether this event of large swarms of Charybdis smithii sinking to the sea #oor occurs each season at a level comparable to 30% of the annual carbon
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#ux, as was observed in autumn 1995. Nevertheless, our observation adds to the list of extreme and unexpected phenomena linking the upper ocean to the deep-sea #oor in the form of large food falls. Other intriguing examples are the discovery of a sunken whale carcass populated by animals related to vent communities (Smith et al., 1989; Smith, 1992), the mass sedimentation of Scyphomedusae fed upon by Ophiuroida (Jumars, 1976), the input of macroalgal debris and wood consumed and populated by various deep-sea animals (Gage and Tyler, 1991 and references therein). These cases all have in common that they cannot be accounted for by conventional estimates of vertical #ux but may be important in the supply and structuring of the abyssal benthic communities which were found to react directly to such events despite their unpredictable occurrence.
Acknowledgements We thank the crew of R.V. Meteor for their assistance during sampling. V. Spiridonov and three anonymous reviewers made useful comments on the manuscript. The investigation was partly supported by the Deutsche Forschungsgemeinschaft and the Bundesministerium fuK r Forschung und Technologie.
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Jan{en, F., Treude, T., Witte, U., 2000. Scavenger assemblages under di!ering trophic conditions: a case study in the deep Arabian Sea. Deep-Sea Research II 47, 2999}3026. Jumars, P.A., 1976. Deep-Sea species diversity: does it have a characteristic scale? Journal of Marine Research 34, 217}246. Losse, G.F., Merrett, N.R., 1971. The occurrence of Oratosquilla investigatoris (Crustacea: Stomatopoda) in the pelagic zone of the Gulf of Aden and the equatorial western Indian Ocean. Marine Biology 10, 244}253. Merrett, N.R., 1968. Tuna longline survey in the equatorial Western Indian Ocean. East African Agricultural and Forestry Journal 34, 17}65. Meyer-Reil, L.A., KoK ster, M., 1992. Microbial life in pelagic sediments: the impact of environmental parameters on enzymatic degradation of organic material. Marine Ecology Progress Series 81, 65}72. Poulicek, M., Jeuniaux, C., 1989. Chitin biomass in marine sediments. In: Skjak-Brek, G., Anthonsen, T., Sandford, P. (Eds.), Chitin and Chitosan. Elsevier, London, pp. 151}160. Smith, C.R., 1992. Whale falls: chemosynthesis on the deep sea#oor. Oceanus 35, 74}78. Smith, C.R., Kukert, H., Wheatcroft, R.A., Jumars, P.A., Deming, J.W., 1989. Vent fauna on whale remains. Nature 341, 27}28. Smith Jr., K.L, Harbison, G.R., Rowe, G.T., Cli!ord, C.H., 1975. Respiration and chemical composition of Pleuroncodes planipes (Decapoda: Galatheidae): energetic signi"cance in an upwelling system. Journal of the Fisheries Research Board of Canada 32, 1607}1612. Spiridonov, V.A., 1994. The swimming crabs (Crustacea, Brachiura Portunidae) of submerged rises and insular shelves of the Atlantic and the Indian Ocean. In: Kuznetzov, A.P., Mironov, A.N. (Eds.), Bottom Fauna of Seamounts. Proceedings of the P.P. Shirshov Institut of Oceanology, Vol. 129, Moscow, pp. 126}152 (in Russian). van Couwelaar, M., Angel, M.V., Madin, L.P., 1997. The distribution and biology of the swimming crab Charybdis smithii McLeay, 1838 (Crustacea; Brachyura; Portunidae) in the NW Indian Ocean. Deep-Sea Research II 44, 1251}1280. Velji, M.A., Albright, L.J., 1985. Microscopic enumeration of marine bacteria of seawater, marine sediment, fecal matter and kelp blade samples following pyrophosphate and ultrasound treatments. Canadian Journal of Microbiology 32, 121}126. Vetter, Y.A., Deming, J., 1994. Extracellular enzyme activity in the Arctic Northeast Water polynya. Marine Ecology Progress Series 114, 23}34. Weller, R.A., Baumgartner, M.F., Josey, S.A., Fischer, A.S., Kindle, J.C., 1998. Atmospheric forcing in the Arabian Sea during 1994}1995: observations and comparisons with climatology and models. Deep-Sea Research II 45, 1961}1999. Zamorov, V.V., Spiridonov, V.A., Rudnev, G.P., 1991. On the mass migration to the pelagial and the distribution of the Indian Ocean swimming crab Charybdis smithi McLeay (Crustacea, Portunidae) during the pelagic phase of its life-cycle. Zoologitcheskii Zhurnal 70, 39}42 (in Russian).
Mass sedimentation of the swimming crab Charybdis smithii (Crustacea: Decapoda) in the deep Arabian Sea Bernd Christiansen *, Antje Boetius GEOMAR, Wischhofstr. 1-3, 24148 Kiel, Germany Baltic Sea Research Institute, Seestr. 15, 18119 Rostock-Warnemu( nde, Germany Received 26 April 1999; received in revised form 18 November 1999; accepted 30 November 1999
Abstract During cruise Meteor 33/1 in the northern Arabian Sea in September/October 1995, large numbers of the portunid crab Charybdis smithii were observed swimming in the open ocean. In a photographic survey at three abyssal stations in the northern Arabian Sea (NAST, WAST, CAST), even higher densities of Charybdis smithii } up to 1 crab m\ } were found dead on the sea #oor. Average sizes of the crabs were around 34}44 mm carapace width, indicating that the animals died prematurely, before returning to the breeding grounds presumable on the shelves of India or Oman. The average weight of the crabs was 10}14 g wet weight. From the photographic quanti"cation it can be deduced that these large food falls represent a signi"cant carbon input of at least 10}30% of the annual #ux of POC as measured in sediment traps in this region. The exceptionally high microbial chitinase activity in the surface sediment layers detected at the same stations indicates that this energy is utilized and channelled into the deep-sea benthic food web of the deep Arabian Sea. There are frequent observations of dense Charybdis smithii swarms in the Arabian Sea from di!erent years; however, it is not certain whether such large food falls as observed during M 33/1 are regular seasonal events that repeat each year. 2000 Elsevier Science Ltd. All rights reserved.
1. Introduction The portunid crab Charybdis smithii is one of the very few swimming crabs that are frequently found in the open ocean. It is endemic to the Indian Ocean, where it can * Corresponding author. Current address: Institut fuK r Hydrobiologie und Fischereiwissenschaft, Zeiseweg 9, D-22765 Hamburg, Germany. Tel.: #49-42838-6686; fax: #49-42838-6696. E-mail address: [email protected] (B. Christiansen). 0967-0645/00/$ - see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 0 4 4 - 8
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form massive swarms dominating the standing stock of pelagic micronekton (Zamorov et al., 1991; van Couwelaar et al., 1997). These swarms of Charybdis have a major predatory impact on the pelagic fauna (Spiridonov, 1994) and have been found to clear the bait o! longlines in the Arabian Sea within a few hours (Merrett, 1968). A similar behaviour has been reported for the stomatopod Oratosquilla investigatoris in the Gulf of Aden and the equatorial western Indian Ocean (Losse and Merrett, 1971). However, the life cycle, the regional distribution, and the biology of Charybdis smithii are not completely understood. Zamorov et al. (1991) proposed that reproduction takes place o!shore after the SW monsoon, and that the larvae are transported with the monsoonal currents until they eventually return to the African shelf. By contrast, van Couwelaar et al. (1997) found evidence for a 1-yr life cycle for Charybdis smithii, with breeding of crabs from October to January on the continental shelves o! India, Oman, and probably also o! Africa, dispersal of the larvae o!shore with the NE monsoonal currents and the formation of pelagic swarms from July to August, after which the adults return to the breeding areas on the continental shelves. Van Couwelaar et al. (1997) propose a high mortality of 90% for the adult crabs before they return to the breeding grounds. There are several reports that the swarms of Charybdis smithii are an important food item for large pelagic "sh such as tuna (e.g., Spiridonov, 1994). Based on the discovery of portunid carapaces on the sea #oor and of dead crabs and parts of crabs in sediment traps, van Couwelaar et al. (1997) suggest that Charybdis smithii also may contribute to the vertical carbon #ux, but up to now no quantitative observations on the presence of carcasses of this species on the deep-sea #oor were available. During cruise Meteor 33/1 in September/October 1995 to the Arabian Sea, a megafauna survey was conducted at three stations in the open ocean. Along photographic transects at water depths of 3000}4000 m, we discovered large numbers of dead Charybdis smithii lying on the sea #oor, which we were able to analyse quantitatively. This mass sedimentation of the swimming crab Charybdis smithii likely induced a rise in benthic microbial enzymatic activity during this period in the northern Arabian deep sea.
2. Material and methods 2.1. Megafauna survey During cruise Meteor 33/1 to the Arabian Sea in September/October 1995, a videocontrolled epibenthic sledge (fototrawl, Christiansen and Nuppenau, 1997) and a deep-sea observation system (DOS, Christiansen, 1993) were used to sample epibenthic megafauna and to perform photographic transects. Fig. 1 shows the sampling stations in the Arabian Sea, and Table 1 presents the station data. The DOS was employed once at station NAST. The fototrawl was used twice at station WAST and once at station CAST. Each haul delivered a total of 800 frames.
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Fig. 1. Area of investigation.
The camera of the DOS was oriented perpendicular to the sea #oor. The photographed area was calculated from the lens data and the distance from the lens to the sea #oor (Christiansen, 1993). The distance to the sea #oor was estimated visually from the photographs and from the videos with the help of a weight hanging 3 m below the DOS. The size of the photographed area in the frames from the fototrawl transects was measured using a Canadian grid based on the elevation of the camera, the camera angle, and the lens data (Christiansen and Thiel, 1992). At NAST, an area of 2100 m was analysed, at WAST 1100 m, and at CAST 930 m. Crabs lying on the sea #oor were counted, and their density was estimated by dividing their number by the area photographed. Only crabs with an apparently intact carapace and at least some legs attached were counted. The Canadian grids were also used to measure the width of Charybdis smithii carapaces on frames from fototrawl transects. Only crabs clearly visible in the foreground of the frames and properly oriented were measured. Crab sizes on DOS photographs were calculated from size measurements on the frames, lens data, and distance to sea #oor.
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Table 1 Station data. The dates are given as day.month.year. The positions given for the DOS and the FT represent the starting positions of each haul Station
Gear no.
Date
Latitude
Longitude
Water depth (m)
NAST WAST WAST CAST NAST NAST NAST WAST WAST WAST CAST CAST CAST CAST CAST
DOS-9 FT-35 FT-36 FT-37 MC-01 MC-04 MC-06 MC-08 MC-12 MC-15 MC-16 MC-17 MC-18 MC-19 MC-21
27.09.1995 29.09.1995 30.09.1995 12.10.1995 24.09.1995 25.09.1995 26.09.1995 01.10.1995 04.10.1995 05.10.1995 08.10.1995 09.10.1995 09.10.1995 10.10.1995 10.10.1995
20300.00 N 16325.10 N 16310.04 N 14324.10 N 20300.02 N 19356.00 N 19359.94 N 16314.95 N 16312.97 N 16311.70 N 14324.93 N 14324.90 N 14324.97 N 14323.01 N 14325.94 N
065335.00 E 060343.80 E 060329.80 E 064333.50 E 065335.10 E 065338.00 E 065341.05 E 060330.92 E 060316.01 E 060318.40 E 064334.06 E 064331.94 E 064332.10 E 064334.05 E 064334.68 E
3186 3996 4028 3949 3185 3158 3164 4028 4034 4034 3943 3944 3943 3949 3941
DOS: deep-sea observation system. FT: fototrawl. MC: multiple corer.
2.2. Benthic microbial activities Sediment cores were obtained from several multiple corer hauls at each station (Table 1) and immediately subsampled for enzymatic activity and biomass of the benthic bacteria. The enzymatic activity (EEA) of the extracellular hydrolytic enzyme chitobiase was measured #uorometrically (Hitachi F}2000 spectro#uorometer) according to Boetius and Lochte (1994), using the methylumbelliferone (MUF)-labelled substrate MUF-N-acetyl-b-glucosaminide (Sigma, 100 lM). The enzyme assays were run in time-course experiments with three determinations during 2}4 h. The subsamples removed at each time point were centrifuged for 10 min (2800 g) at 03C. The supernatants were transferred into disposable UV-cuvettes (Ratiolab) and the #uorescence of MUF was measured at 365 nm excitation and 445 nm emission wavelength. Relative units of #uorescence were calibrated with 5 standard concentrations between 20 and 300 nM of MUF (Serva). Enzyme activity was calculated from the average of the changes in #uorescence during the time-course experiment (2}3 intervals). Subsamples for the determination of bacterial numbers and biomass were prepared according to the method of Velji and Albright (1985). Bacterial numbers were determined by epi#uorescence microscopy (ZEISS AXIOSKOP) after staining with acridine orange (Meyer-Reil and KoK ster, 1992).
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2.3. Enrichment experiment The top 4.5 cm of bulk sediment from several cores of one multiple corer were combined in a sterile glass bottle and diluted with an equal part of sterile "ltered (0.2 lm) bottom water. The sediment slurry was mixed thoroughly by shaking the bottle. One portion without additional substrate served as control. The rest of the sediment slurry was divided into smaller sterile glass bottles. A "rst subsample was removed for further analysis of microbial activities and biomass, representative of the conditions at day 0. The other portions were enriched with di!erent amounts of puri"ed chitin #akes from shrimp shells. Each bottle was thoroughly mixed and portions of 70 ml each were poured into sterile polyethylene (PE) bags so that one bag was available for each time interval. The PE bags were closed by welding and incubated in pressure vessels at in situ temperature of 23C and in situ pressure of 400 bar. The sediments were not stirred. At each time interval a pressure vessel was opened and the PE bags were removed. Analysis of enzymatic activities followed immediately. For bacterial numbers, 1 ml of the subsample was "xed in 9 ml of 2% formaldehyde solution and stored at 43C for later analysis in the home laboratory.
3. Results and discussion During cruise Meteor 33/1, swimming crabs were frequently observed at the sea surface at stations WAST and CAST as far as 1000 km from the shelves of Oman and India. They were obviously feeding on plankton and often attacked baited hooks laid out for "shing. At stations NAST and WAST they occurred in densities of approximately 0.1 Ind m\ as observed visually from the ship's deck during daytime. A few specimens were sampled from the surface waters and identi"ed as Charybdis smithii McLeay. The "rst hauls with the fototrawl and an otter trawl conducted at station WAST caught several kg of dead swimming crabs, which looked rather intact. First, we mistakenly regarded these crabs as pelagic contamination of the catch of abyssal animals recovered with the epibenthic net of the fototrawl and with the otter trawl, comprising mainly ophiuroids, sponges and holothurians. However, the photographs of the deep-sea #oor at station NAST (3190 m depth), WAST (4050 m) and CAST (3950 m) gave evidence of large amounts of swimming crabs lying dead on the sea #oor in di!erent states of decay (Fig. 2). Most specimens appeared to be rather intact, but single legs, parts of legs or broken carapaces were also seen. Table 2 gives the number of swimming crabs counted on the four photographic transects in the Arabian Sea. The stations sampled di!er clearly in the mean abundance of swimming crabs. Lowest abundances were found at station NAST with a mean of 0.04 Ind m\. At station WAST, the abundance of swimming crabs amounted to ca. 1 Ind m\, whereas station CAST lay in-between with 0.2 Ind m\. These di!erences were highly signi"cant (p(0.001; ANOVA with post hoc tests on squareroot-transformed data). Considering the patchy distribution of Charybdis smithii swarms in the Arabian Sea (van Couwelaar et al., 1997), this may re#ect the abundance of crabs in the surface layers or regional di!erences in mortality, but we
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Fig. 2. Photograph of dead Charybdis smithii on the sea #oor at station CAST.
cannot exclude also a temporal e!ect with regard to sampling date and time of mass sedimentation. The carapace width of 6 swimming crabs recovered from the sea #oor at station WAST was between 40 and 52 mm and the wet weight between 10 and 14 g. The size measurements from the photographs revealed median carapace widths of 34 mm at stations WAST and CAST and of 44 mm at station NAST (Fig. 3). We assume that most of the observed variance within stations is due to methodological constraints, and that the di!erence between the stations as well as the discrepancies between the photographic and the direct measurements can be attributed to the di!erent methods used for the size measurements.
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Table 2 Densities of Charybdis smithii at the sea #oor. Only crabs visible on the photographs with an apparently complete carapace and at least some legs attached to it were counted and their density was calculated Station
Haul no.
Number of frames
Specimens counted
Mean abundance (Ind m\)
Standard error
NAST WAST CAST
DOS 09 FT-35#FT-36 FT-37
483 1412 709
82 1077 185
0.04 0.95 0.20
0.004 0.031 0.015
Fig. 3. Box plot of carapace widths of Charybdis smithii as calculated from photographs.
The size range of dead crabs as estimated from the sea-#oor photographies, at least at stations WAST and CAST, seems fairly consistent with the size-frequency distribution detected during the R.V. Baldrige cruise in July}August 1995 in the upper 150 m of the ocean, with average sizes of the crabs of around 32 mm (van Couwelaar et al., 1997). However, considering a systematic underestimation of carapace widths on the photographs at WAST and Cast, as suggested by the comparison of direct vs. photographic measurements, the mean size of crabs on the sea #oor would be ca. 8}10 mm bigger than that from the R.V. Baldrige cruise. We propose that the death of the crabs preceded our sampling by only a couple of weeks, i.e. that sedimentation of carcasses started in mid-September. The guts of the crabs recovered with the epibenthic sledge were still complete and the muscle #esh was relatively "rm. In an experiment on the decay of shrimp in sea water kept at 203C, Briggs and Kear (1994) observed that the exoskeleton would stay visually intact for at least one week, but that most of the carapace degrades within eight weeks. The relatively small size of the crabs indicates that a large part of the swarm might have consisted of premature individuals. According to van Couwelaar et al. (1997) the
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crabs with an average size of 34}44 mm would need 1}2 further moults before reaching maturation. Thus, the crabs observed on the sea #oor had died before returning to the breeding grounds at the shelves of India or Oman. Our observations are the "rst evidence of a mass mortality of portunid crabs in the open ocean. Van Couwelaar et al. (1997) report "ndings of a few remnants of swimming crabs in sediment traps moored by R.V. Tyro at 1032}3047 m on the Somali continental margin and in the Somali Basin. At the open ocean station WAST, a small specimen of a swimming crab was caught in the deep trap moored 1000 m above bottom (T. Rixen, pers. comm.). Furthermore, crab bodies and pieces were observed on the sea #oor of the shelves and slopes of the Indian Ocean; however, it was not clear whether these were moults or carcasses of the crabs (van Couwelaar et al., 1997). These relatively scarce observations of sedimented crabs compared to the abundant "ndings of crab remnants in the stomachs of tuna and other large pelagic "sh led to the hypothesis that the mortality of adult swimming crabs is mainly caused by predation (Zamorov et al., 1991). Mass strandings of Charybdis smithii have been observed along the shores of South Africa, the reason for their death probably being unusual water temperatures (van Couwelaar et al., 1997 and literature therein). However, the reason for the death of the Charybdis swarms in the open ocean after the SW-monsoon remains unknown. There was no indication of extraordinary water temperatures or other hydrographical features at this time in the Arabian Sea in 1995 (Weller et al., 1998). Other possible causes for the mass mortality of the swimming crabs could be food shortage, toxic algal blooms, which have been frequently observed in the Northern Arabian Sea, or upwelling of anoxic waters from the oxygen minimum zone. However, such events are unlikely to extend in an area as large as was covered by our observations. Thus, it remains an open question whether death and sedimentation of the swimming crabs occur regularly as part of their life cycle, as does the formation of dense swarms in the surface waters. At station WAST, the density of approximately 1 crab m\ at the sea #oor is equivalent to a carbon biomass of ca. 1 g m\, assuming a mean carapace width of 40 mm, which corresponds to a wet weight of 10 g (van Couwelaar et al., 1997). Since no data on the carbon content of Charybdis smithii are available, we used a standard carbon/wet weight ratio of 10% for this calculation. Accordingly, the mean organic carbon pool in the form of dead crabs at NAST was 0.04 g m\, at CAST 0.2 g m\. There are strong indications that the crab carcasses do not accumulate on the sea #oor over a longer time period, but stem from the swarming season of one year. On sea-bottom photographs of the same area from Meteor cruise 31/3 in March 1995, no remains of Portunidae could be detected (U. Witte, pers. comm.). Assuming that all these dead crabs originate from one season's swarming, the biomass of C. smithii on the sea #oor observed after the SW-monsoon would be a minimum estimate for the annual #ux to the sea #oor by this species at the respective station. Compared with the average POC #ux of 3.2 g m\ yr\ measured with sediment traps at station WAST by Haake et al. (1993), the sinking carcasses of C. smithii would add at least 30% to the estimated annual POC supply at this station. At station CAST, the annual carbon #ux by C. smithii adds at least 10% to the annual C #ux of 1.9 g m\ yr\ measured in sediment traps there by Haake et al. (1993).
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Most of the carbon input by the crabs is in the form of chitin, which makes up approximately 20% of their dry weight (Smith et al., 1975; Hirano, 1989). No recognizable pieces of crab shells were discovered in deeper sediment layers of bottom samples recovered by box corers and multiple corers, indicating a complete degradation of the crab carcasses. Chitin is the most abundant polysaccharide in the marine environment; however, due to its low preservation potential it does not accumulate in marine sediments. Despite the fact that chitin is resistant to most chemical and physical agents, it is quickly dissolved by chitinolytic enzymes (Gooday, 1990). How is this large food fall utilized by benthic organisms? The typical abyssal megafauna at station WAST was predominantly composed of ophiuroids as well as of holothurians and porifera (Christiansen, unpublished). A massive euphausiid dead body rain serving as the main food source for abyssal ophiuroids was discovered in the South Atlantic Ocean (Sokolova, 1994). Accordingly, ophiuroids may utilize the dead crabs in the Arabian Sea, but in the photographs we never saw an ophiuroid in contact with a crab. Baited cameras deployed at stations NAST, WAST and CAST attracted "sh, penaeid prawns, amphipods and galatheid crabs (Janssen et al., 2000), which may be other potential consumers of the crab bodies. However, not many animals are able to digest chitin, which makes up a large fraction of the crab-POC, and probably most of them harbour chitinolytic microorganisms in their guts (Deming and Baross, 1993). Thus, it is likely that bacteria utilize much of the crab-POC. Bacteria can only take up small molecules; thus, the production of extracellular hydrolytic enzymes speci"c for the cleavage of substrates like chitin or cellulose is a prerequisite for their use as energy and nutrient source. Enrichment experiments with deep-sea sediments have shown that the natural microbial assemblages may produce high amounts of chitinolytic enzymes within days when chitin becomes available as a substrate. The bacteria may then utilize this C#N source with relatively high growth e$ciencies (Boetius and Lochte, 1996). Investing in the energyconsuming synthesis and excretion of enzymes is only bene"cial if the energy loss is compensated for by the gain in readily available products. The calculations of Vetter and Deming (1994) indicate that secretion of enzymes can only result in an energy gain via uptake of produced hydrolysate when external concentrations of polymeric substrates are very high. The amount of chitin introduced by the sedimentation of a crab to a square metre of sediment (approximately 1 g) is well above the background value of chitin in deep-sea sediments of 0.1 mg m\ (Poulicek and Jeuniaux, 1989). Consistent with our "ndings, high chitinolytic enzyme activities were detected in the sediments of the northern Arabian Sea, substantially exceeding those in other oceans as well as those in the Arabian Sea at other times of the year. To track the changes in activity potentials that were not related to variation in microbial biomass, biomassspeci"c extracellular enzyme activity (EEA) of the chitobiase was calculated, dividing hydrolysis rates by bacterial numbers. Fig. 4 shows the distribution of speci"c activities of the extracellular enzyme chitobiase in the Arabian Sea after the SWmonsoon in 1995, when the mass sedimentation of Charybdis was observed, compared to the activities during and after the NE-monsoon in 1997 and 1998. Speci"c chitobiase activities at two abyssal stations in the NE-Atlantic in summer 1996 and
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Fig. 4. Speci"c activity of the extracellular enzyme chitobiase in surface sediments of the Arabian Sea and the NE-Atlantic (0}1 cm). The black columns represent values measured in sediment samples of stations where dead crabs were occurring (CAST, NAST and WAST; M33/1, September/October 1995). Data from the NE Atlantic (station BIOTRANS, 4560 m, and BENGAL, 4810 m) are shown for comparison (M36/6, September/October 1996; M42/2, July/August 1998). No estimation of a standard error was possible because only 1}3 samples of bacterial biomass were analysed per station and cruise.
autumn 1998 are also shown for comparison. The activity per cell of chitobiase was twice as high in the Northern Arabian Sea in 1995 as during other times when no remnants of swimming crabs were detected at the sea #oor during megafauna surveys conducted with a TV observation system (U. Witte, pers. comm.). Furthermore, the biomass and the oxygen consumption of the sediment infauna at WAST were extremely high after the SW-monsoon in 1995, indicating a respiratory carbon demand which exceeded the POC input estimated via sediment traps approximately twofold (U. Witte, pers. comm.). However, in the "eld samples, bacterial cell numbers at sediment surface (0}1 cm) at NAST (1.3;10 cells cm\), WAST (1.4;10 cells cm\) and CAST (1.2;10 cells cm\) were not substantially increased in September 1995 compared to samples from other times (February/March 1998, April/May 1997, Boetius et al., 2000). Thus, we presume that the crab carcasses may add signi"cantly to the food supply of the benthic community and that a large fraction of this input is channelled to higher benthic organisms grazing on the bacteria. The e!ect of such a chitin enrichment on microbial activities in the sediment was tested on a sediment sample obtained at station NAST, where the highest speci"c chitobiase EEA was recorded in the "eld during the cruise M33/1 in September/October 1995. Approximately, 0.3 mg of coarse chitin #akes per ml of sediment slurry was added and the samples were incubated under in situ pressure and temperature. This is similar to the amount of chitin introduced by the fall of one crab to one square metre of sea #oor. To compare directly microbial chitobiase activity in the "eld with that in the experiment, biomass-speci"c EEA of the hydrolases was calculated. In the incubation of unenriched sediment, which served as control, speci"c EEA of chitobiase remained on a constantly low level during 32 d (Fig. 5). The speci"c chitobiase EEA of enriched sediment increased by an order of magnitude from day 7 to day 21. After 10 d, the level of enzyme activity reached in the enrichment
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2683
Fig. 5. Enrichment experiments with di!erent amounts of chitin. The plots show the change in chitobiase activity over time in (a) a slurry of sediment obtained from station NAST (M 33/1) and (b) a slurry of sediment obtained from station SAST during another cruise (SO-118, 1997).
experiment was comparable to the speci"c EEA of chitobiase at stations NAST and WAST in September/October 1995 after the sedimentation of the crabs. After day 21, chitobiase EEA decreased again. During a later cruise (SO-118 in 1997), another enrichment experiment was performed with sediments from the relatively oligotrophic station SAST in the southern Arabian Sea. The addition of di!erent amounts of chitin induced chitobiase to di!erent levels relative to the availability of this substrate (Fig. 5). Again, the speci"c EEA of chitobiase increased by an order of magnitude within 10 d and decreased after 3 weeks. As indicated by these experiments and earlier observations (Boetius and Lochte, 1996, and literature therein), chitin is an important substrate for bacteria in deep-sea sediments and even high amounts as introduced by large food falls will be quickly remineralized. It remains unknown whether this event of large swarms of Charybdis smithii sinking to the sea #oor occurs each season at a level comparable to 30% of the annual carbon
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#ux, as was observed in autumn 1995. Nevertheless, our observation adds to the list of extreme and unexpected phenomena linking the upper ocean to the deep-sea #oor in the form of large food falls. Other intriguing examples are the discovery of a sunken whale carcass populated by animals related to vent communities (Smith et al., 1989; Smith, 1992), the mass sedimentation of Scyphomedusae fed upon by Ophiuroida (Jumars, 1976), the input of macroalgal debris and wood consumed and populated by various deep-sea animals (Gage and Tyler, 1991 and references therein). These cases all have in common that they cannot be accounted for by conventional estimates of vertical #ux but may be important in the supply and structuring of the abyssal benthic communities which were found to react directly to such events despite their unpredictable occurrence.
Acknowledgements We thank the crew of R.V. Meteor for their assistance during sampling. V. Spiridonov and three anonymous reviewers made useful comments on the manuscript. The investigation was partly supported by the Deutsche Forschungsgemeinschaft and the Bundesministerium fuK r Forschung und Technologie.
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