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Transport and deposition of macrophytes to the dysphotic bottom of coastal waters
Aquatic Botany 92 (2010) 289–293
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Short communication
Transport and deposition of macrophytes to the dysphotic bottom of coastal waters Noriyuki Takai a,*, Emiri Takatsu a, Yuko Sawairi a, Tomohiro Kuwae b, Kiyoshi Yoshihara a a b
Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan Port and Airport Research Institute (PARI), Yokosuka, Kanagawa 239-0826, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2009 Received in revised form 9 November 2009 Accepted 26 January 2010 Available online 2 February 2010
Some macrophytes are transported to the deep-sea bottom and are utilized by heterotrophs in the deepsea as a food source. We inferred the transport route of macrophytes toward the deep-sea based on similarity in the species compositions of macrophyte pieces collected from the dysphotic bottom off the Izu Peninsula and the drifting macroalgae reported for the study area. We also examined whether or not the macrophytes are buried in the sediment, based on stable isotope distributions of organisms. Macrophytes collected by dredging at a depth of 100–300 m included 93 species, whereas 43 species were found by trawling at depths from 200 to 400 m. Only 15 of 76 dredged species (19.7%) that were identified to the species level were identical to the drifting macroalgal species reported for this area, whereas 15 of the 29 trawled species (51.7%) that were identified to the species level were identical to the reported drifting species. It was thus inferred that macrophytes were mainly transported through sliding along the sea bottom for the macrophytes collected by dredging and through sinking from the surface water for the macrophytes collected by trawling. The d13C of sedimentary organic matter (SOM) from the 200–300 m zone was similar to the d13C distribution of particulate organic matter in the surface water reported for the study area. The SOM in the zone likely originated from almost exclusively phytoplankton. In contrast, the 13C of SOM was significantly more enriched in shallow areas 100 m deep. We infer that not only phytoplankton but also macrophytes could supply organic matter to heterotrophs on the shallow bottom. ß 2010 Elsevier B.V. All rights reserved.
Keywords: Macroalga Transport Deposition Dysphotic bottom Drifting alga Stable isotope
1. Introduction Seaweed beds produce a large quantity of organic matter on the littoral and sublittoral bottom of coastal shallow areas (e.g., production of 1750 g C m2 y1 for Laminaria longicruris, Laminaria digitata and Agarum cribrosum; Mann, 1972). Macrophytes are abundantly deposited on the bottom around seaweed beds or get washed up on the shore. Consequently, macrophytes supply substantial nourishment to heterotrophs in shallow water ecosystems via direct digestion by herbivores and via indirect process through decomposition, physico-chemical precipitation, and microbial activity (Mann, 2000). Our concern here is transport of macrophytes toward the deepsea bottom. Some studies have presented evidence that heterotrophs in the deep-sea also utilize macrophytes as a major food source. A few Sargassum air bladders encrusted by ectoprocts were found in stomach contents of six brittlestars (Amphiophiura bullata) collected at depths of 2400–5042 m in the western Atlantic
* Corresponding author. Tel.: +81 466 84 3916; fax: +81 466 84 3689. E-mail address: [email protected] (N. Takai). 0304-3770/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2010.01.007
(Schoener and Rowe, 1970). Video observation in submarine canyons off southern California (mainly 100–550 m in depth) revealed that aggregations of macrophyte detritus were common and were associated with elevated densities of megafauna (Vetter and Dayton, 1999). Tracer experiments using 13C-labeled diatoms at two sites (850 m in depth) in the western Atlantic suggested that labile organic matter from fresh macrophyte detritus is quickly consumed by macrobenthos (Levin et al., 1999). Provided that macrophytes are an actual major food source for some deep-sea inhabitants, a constant supply of macrophytes from the euphotic zone would be essential for some deep-sea food webs. It is therefore important to elucidate the supply process for macrophyte-originating organic matter from the coastal ecosystem to the deep-sea ecosystem. Thus in the present study, we examined the species and quantity of macrophytes lying on the dysphotic bottoms in the coastal waters of the Izu Peninsula, Japan, to clarify the transport route of the macrophytes toward the deepsea. We predicted the following two potential routes: (1) sliding along the sea bottom and (2) drifting in the surface water followed by sinking. The study area has been precisely examined for species compositions of macrophytes in drifting macroalgal patches (Hirata et al., 2001). We inferred the transport route of the
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macrophytes from the shallow euphotic zone to the dysphotic zone, comparing species compositions between the drifting macrophytes and the macrophytes from the dysphotic bottoms. We also examined whether or not the macrophytes were buried in sediment of the dysphotic bottom, as determined from stable isotope ratios and elemental carbon and nitrogen contents of organisms. The burial of macrophytes means that macrophyteoriginating organic matter can be utilized as a food source for deposit-feeding benthos. Generally, the carbon isotope ratio (d13C) of primary producers reflects the concentration and the d13C signature of their inorganic carbon sources and isotope fractionation during uptake of inorganic carbon (O’Leary, 1981). The d13C distributions of macrophytes and particulate organic matter (POM) have been reported for the study area; d13C distributions mostly range from 17 to 11% for macrophytes in the surf zone and 24 to 20% for POM in the surface water (Takai et al., 2007). Therefore, we can infer the relative contribution of macrophytes and POM as organic carbon sources. The deposition of 13C-enriched species of macrophytes should increase d13C values of the sedimentary organic matter. As a secondary tracer, we also analyzed the nitrogen stable isotope ratio (d15N) of organisms. The d15N of primary producers varies with the concentration and the d15N signature of their inorganic nitrogen sources and isotope fractionation during uptake of inorganic nitrogen (Wada and Hattori, 1991). The potential variation in the d15N of organic matter at ecosystem bases provides a clue to the identity of nitrogen source of sedimentary organic matter (SOM). 2. Materials and methods The Izu Peninsula is located in the central area of the Japanese Archipelago, exposed to the open water of the Pacific Ocean. The surface water off the southeastern peninsula contains only a small quantity of nutrient (nitrate <0.6 mM) and chlorophyll a (<0.6 mg Chl a l1) originating from the Kuroshio water, except for the nutrient-rich subsurface waters where intermittent upwelling occurs (2 mM in nitrate and >1 mg l1 in Chl a) (Ishizaka et al., 1986). Macrophytes abundantly grow along the coastline in the littoral and sublittoral zone of this area. A large net production of ca. 2.9 kg dry weight m2 y1 was reported for the perennial brown alga Ecklonia cava (Yokohama et al., 1987). In Area A (348 34.90 N–348 39.00 N, 1388 55.80 E–1398 01.10 E), we collected macrophytes by dredging the sea bottom on July 8, August 5–6, October 13–15 and December 8 in 2004. The inner dimensions of the mouth of the dredge were 382 mm (width) and 100 mm (height) with a canvas sheet covering the aperture. Dredging was carried out with a research boat (R/V Suzaki II, 9 ton) for 10–20 min at each station in duplicate for every sampling month. In the second survey (August 5–6) and the third survey (October 13–15), it took 2–3 days to complete the surveys because of rough sea conditions. Difficulties in operating the boat for dredging resulted in variation of the total dredged distance from 919 to 1802 m. The dredge was hauled along four isobaths of 20, 100, 200 and 300 m. The euphotic zone in the study area has been proposed to be up to 50 m deep based on unpublished data for 1% light depth (e.g. Ishizaka et al., 1986). Therefore, we considered that the sea bottom was located in the euphotic zone for the 20 m depth zone and in the dysphotic zone for the 100–300 m depth zone. The macrophytes entangled on the frame and connecting chains of the dredge were included in the samples. We washed the samples through a 1 mm sieve on the boat and collected macrophytes from the residuals. The species of the collected macrophytes were identified to the lowest possible taxon. We multiplied the width of the dredge mouth by the total hauled distance in order to calculate the total
area dredged for each locality and subsequently calculate the dry weight per square meter for dredged macrophytes. In Area B (348 55.40 N–348 57.60 N, 1388 43.50 E–1388 45.00 E), we collected macrophytes by bottom trawling (25 mm mesh for the aperture) on 8 May 2004. This fishing gear is categorized as a firstclass hand trawl, permitted for this fishing ground by fisheries regulations. The gear uses no opener instruments such as beams and frames for the mouth of the net. During a trawling operation, the width of the net mouth gradually changes, therefore, we could not calculate the trawled area and consequently could not estimate the biomass of the collected macrophytes. In addition, we also analyzed the elemental contents of macrophytes collected in the surf zone of an embayment on April 9 and December 24 in 2004. The stable isotope ratios of identical samples were reported in the previous work (Takai et al., 2007). Surface sediments were collected with a Smith-MacIntire grab sampler in Area A and the embayment (5 m deep) on March 15 and July 13 in 2005. Samples were collected from six depth zones of 5, 10, 20, 100, 200, and 300 m. We collected the sediment from the upper 1 cm of the surface with a spatula. The macrophytes were dried at 60 8C after leaf surfaces were washed. The surface sediments were dried at 60 8C, treated with 1N HCl overnight to remove carbonate, and were dried again. These samples were ground to a fine powder with a mill. Stable isotope ratios of carbon and nitrogen were measured with a Delta Plus Advantage mass spectrometer (Thermo Finnigan) coupled to an elemental analyzer (Flash EA 1112, Thermo Finnigan). Isotope ratios, d13C and d15N, are expressed as per mil deviations from the standard as defined by the equation, (Rsample/Rstandard 1) 1000, where R = 13C/12C or 15N/14N. Belemnite (PDB) and atmospheric nitrogen were used as the isotope standards for carbon and nitrogen, respectively. The analytical precision for the isotopic analyses was 0.22% for d13C and 0.19% for d15N. Total organic carbon (TOC) content and total nitrogen (TN) content for the macrophytes and the SOM were measured with an elemental analyzer (Flash EA 1112, Thermo Finnigan). All statistical analyses were performed using Prism 4.0c (GraphPad Software). 3. Results In Area A, we dredged 101 species of macrophytes that were identified to the genus level. The macrophytes consisted of seven species of Chlorophyceae, 20 species of Phaeophyceae, 73 species of Rhodophyceae and a species of Monocotyledoneae (Spermatophyta). The number of species represented in the macrophytes from the dysphotic zone of 100–300 m deep was 73 on 8 July 2004, 56 on 5–6 August 2004, 44 on 13–15 October 2004, and 48 on 8 December 2004. A total of 93 species were collected from the dysphotic zone, with predominant appearance in the 100 m zone (91 species). The dry weight was greatest in the 100 m zone in July (426 mg m2) and August (393 mg m2). In July, the 26 most abundant species with dry weights 1.3 mg m2 represented 97.7% of the macrophytes in the zone as shown in Table 1. In October and December, the dry weight of dredged macrophytes from the 20 m zone was greater than that of the macrophytes in the 100 m zone; 552 mg m2 in October and 389 mg m2 in December. Macrophytes found in the 20 m zone for both months included a large sporophyte of the brown algae E. cava whose thick stipe remained. In comparison, the dry mass of macrophytes in the 200– 300 m zone was distinctly smaller with a maximum of 8 mg m2 for the 300 m zone in July. Macrophytes collected by trawling on 8 May 2004 consisted mostly of Phaeophyceae in weight, particularly Sargassum species (Table 2). Forty-three species and unidentified species (Laminar-
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Table 1 Elemental content, biomass, and stable isotope ratios (%) for carbon and nitrogen of macrophytes collected by dredging in the 100 m zone on 8 July 2004. The 26 most abundant species (1.3 mg m2) were analyzed. Dry weight (mg) per square meter and the C:N ratios (mol:mol) are also shown. Species
Phaeophyceae Dilophus okamurae Distromium decumbens Pachydictyon coriaceum Spatoglossum sp. Carpomitra costata Desmarestia tabacoides Ecklonia cava Sargassum hemiphyllum Sargassum macrocarpum Sargassum micracanthum Sargassum spp. Rhodophyceae Gelidium elegans Gelidium pacificum Pterocladiella capillacea Ptilophora subcostata Delisea japonica Prionitis angusta Prionitis crispata Prionitis divaricata Prionitis patens Callophyllis adhaerens Callophyllis spp. Plocamium telfairiae Schizymenia dabyi Chlorophyceae Ulva japonica Cladophora wrightiana
mg m2
C
N
C:N
C%
mg C m2
d13C
N%
mg N m2
d15N
24.5 10.1 27.6 1.5 1.3 2.7 62.8 18.1 20.1 2.0 3.7
34.5 31.4 38.9 24.5 31.2 29.9 36.3 37.7 39.6 35.8 39.7
8.44 3.17 10.74 0.37 0.40 0.82 22.80 6.83 7.96 0.72 1.45
22.6 19.7 22.0 22.6 26.1 22.3 17.1 20.2 19.5 20.6 20.3
2.6 2.6 2.5 1.7 2.5 1.9 2.3 2.1 1.9 1.7 2.1
0.64 0.26 0.68 0.03 0.03 0.05 1.43 0.37 0.38 0.04 0.08
2.8 5.0 3.5 3.0 2.8 3.6 3.8 2.3 3.5 3.9 6.2
15.4 14.3 18.4 16.4 14.8 18.7 18.6 21.3 24.4 24.0 21.7
23.1 2.5 7.7 123.0 10.4 5.7 1.4 1.4 9.9 14.1 1.3 9.2 2.8
36.8 41.3 42.4 37.2 30.9 35.1 33.4 29.7 38.5 24.9 32.6 28.3 30.6
8.52 1.02 3.24 45.80 3.21 1.99 0.48 0.40 3.82 3.52 0.42 2.61 0.86
19.7 16.9 19.2 22.3 25.2 17.2 19.2 17.6 18.4 30.3 17.8 29.5 30.2
2.8 2.4 3.4 3.0 3.6 2.8 3.2 2.1 4.1 3.3 3.2 3.6 2.4
0.65 0.06 0.26 3.64 0.37 0.16 0.05 0.03 0.41 0.47 0.04 0.33 0.07
4.4 4.7 4.9 3.8 2.4 4.1 5.0 5.1 2.4 3.7 3.3 3.4 5.6
15.2 20.3 14.6 14.7 10.1 14.5 12.3 16.5 10.9 8.8 12.0 9.1 14.9
7.8 21.7
37.2 36.2
2.91 7.84
15.7 17.3
4.9 3.3
0.38 0.71
5.7 3.1
8.8 12.8
iales spp., Sargassum spp. and Fucales spp.) totaled 555 g for the 200–400 m depth zone. Markedly abundant species included Sargassum yamamotoi, Sargassum micracanthum, Sargassum hemiphyllum, Eckloniopsis radicosa, Undaria undarioides and Sargassum macrocarpum. The d13C of macrophytes ranged from 30.3 to 15.7% for the 26 most abundant species (1.3 mg m2) collected by dredging in the 100 m zone in July (n = 26; Table 1) and from 20.6 to 11.6% for the abundant 14 species (>2.0 g per haul) collected by trawling in the 200–400 m zone (n = 31; Table 2). Takai et al. (2007) reported that the d13C of macroalgae in the surf zone ranged from 21.5 to 11.4% for 26 species. There was a significant difference among these three types of macrophytes (Kruskal–Wallis test, p < 0.0001). The analysis by Dunn’s multiple comparison test revealed a significant difference for dredged vs. trawled macrophytes (p < 0.001) and dredged vs. surf-zone macrophytes (p < 0.001), whereas the difference between trawled and surfzone macrophytes was not significant (p > 0.05). The d13C of SOM ranged from 24.6 to 18.5% on 15 March 2005 and from 20.4 to 17.3% on 13 July 2005 (Fig. 1a). The d13C of the SOM significantly decreased with the depth for both months (Spearman’s rank correlation coefficient; March, rs = 0.79, p < 0.05; July, rs = 0.83, p < 0.01). The d15N of the macrophytes ranged from 2.3 to 6.2% for the 26 most abundant dredged species in the 100 m zone in July (n = 26; Table 1) and from 3.0 to 9.7% for the 14 most abundant trawled species in the 200–400 m zone (n = 31; Table 2). Takai et al. (2007) reported that the d15N of macroalgae in the surf zone ranged from 4.7 to 7.4% for 26 species. There was a significant difference among these three types of macrophytes (Kruskal–Wallis test, p < 0.0001). An analysis by Dunn’s multiple comparison test showed a significant difference for every combination (dredged vs. trawled macrophytes, p < 0.01; dredged vs. surf-zone macrophytes, p < 0.001; trawled vs. surf-zone macrophytes, p < 0.05).
The d15N of SOM ranged from 4.4 to 6.4% in March and from 4.5 to 6.8% in July (Fig. 1b). No significant correlation was found between the depth and the d15N on either March 15 or July 13 in 2005 (Spearman’s rank correlation coefficient; March, rs = 0.67, p = 0.06; July, rs = 0.49, p = 0.19). The elemental contents of the 26 most abundant species in the 100 m zone in July averaged 34.4% (SD 4.7%; range 24.5–42.4%) for TOC and 2.8% (SD 0.8%; range 1.7–4.9%) for TN (Table 1). These values for elemental contents of dredged macrophytes were consistent with ranges for macroalgae collected from the surf zone; 24.5–42.9% for TOC and 1.7–4.9% for TN. Multiplying the percentage by the dry weight for each species, the contents of these 26 species totaled 150.3 mg C m2 and 11.6 mg N m2. The C:N ratio (mol:mol) ranged from 8.8 to 24.4 for the dredged macrophytes. Elemental contents of the main species (2.0 g) in the trawled macrophytes averaged 37.1% (SD 3.6%; range 24.0–42.3%) for TOC and 2.2% (SD 0.4%; range 1.5–3.0%) for TN (Table 2). These values were also consistent with the ranges for macroalgae from the surf zone. The C:N ratio of the trawled macrophytes ranged from 11.7 to 29.1. Elemental contents of SOM ranged from 0.07 to 0.30% for TOC and from 0.01 to 0.04% for TN. The C:N ratio of the SOM ranged from 6.8 to 16.9 (Fig. 1c). Extremely high C:N ratios of 15.6–16.9 were found for samples from the 300 m zone where the TN showed strikingly low values of 0.01%. The C:N ratio significantly increased with the water depth (Spearman correlation coefficient; March, rs = 0.78, p < 0.05; July, rs = 0.78, p < 0.05). 4. Discussion Some observations in the past studies indicated that drifting algal patches were scarce in the study area in comparison with other areas around the Japanese Archipelago (Yoshida, 1963;
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Table 2 Total dry weight (g) per haul, and elemental contents and stable isotope ratios (%) for carbon and nitrogen of macrophytes collected by bottom trawling at the depth zone of 200–400 m on 8 May 2004. The 14 most abundant species (2.0 g) including Sargassum spp. were analyzed. The C:N ratios (mol:mol) are also shown. Depth (m)
Weight
C%
d13C
N%
d15N
C:N
200 300 400
2.9 34.0 3.1
35.9 37.0 36.1
13.8 15.9 14.3
2.8 2.6 2.7
5.8 6.1 7.5
14.7 16.8 15.7
Undaria pinnatifida
300 400
2.9 5.0
36.9 36.7
17.9 14.9
2.6 2.4
5.5 7.7
16.8 17.9
Undaria undarioides
200 300 400
4.3 28.3 1.6
34.0 36.5 28.6
18.0 15.2 11.6
3.0 2.8 2.4
8.1 5.2 7.1
13.4 14.9 14.2
Sargassum piluliferum
200 300 400
1.8 9.5 1.3
24.0 37.4 36.8
14.4 14.8 20.6
2.4 1.9 2.4
9.7 5.3 4.1
11.7 23.0 17.8
Sargassum patens
400
2.7
36.1
14.6
2.1
6.0
19.8
S. macrocarpum
200 300
3.0 21.0
38.1 40.8
17.1 20.1
1.8 1.9
4.4 3.0
25.1 25.6
Sargassum siliquastrum
200 300 400
2.1 1.4 4.8
37.7 38.5 39.8
17.1 15.0 15.0
1.7 2.2 2.0
3.5 4.5 3.4
25.5 20.0 22.7
Sargassum yamamotoi
200 300 400
10.6 90.3 58.4
35.9 39.0 39.2
15.9 15.2 13.8
1.5 1.7 1.7
6.0 4.5 3.0
28.7 27.0 26.6
Sargassum yamadae
300
16.8
40.9
16.0
2.0
4.9
23.7
S. hemiphyllum
200 300 400
3.4 53.0 1.2
33.0 36.4 37.9
14.9 17.1 15.3
2.4 2.1 2.4
5.8 5.2 5.0
16.1 20.4 18.5
S. micracanthum
200 300 400
18.9 75.1 41.8
41.5 42.3 41.3
15.4 17.6 16.8
2.2 1.9 2.4
4.4 3.9 4.0
22.3 25.4 19.9
Sargassum yendoi
300
3.0
37.5
16.7
2.0
4.8
22.2
Sargassum sp. 1
200
13.4
40.1
16.7
1.6
3.7
29.1
Sargassum spp.
300 400
9.2 1.7
36.3 37.4
15.6 16.2
2.2 2.1
5.8 4.6
19.0 21.2
Species Phaeophyceae Eckloniopsis radicosa
The trawl net was towed 1833 m for the 200 m zone, 2590 m for the 300 m zone, and 1341 m for the 400 m zone.
Segawa et al., 1964). However, Hirata et al. (2001) found that a substantial quantity of drifting patches gathered along tidal fronts in the area during spring to autumn. They reported that a total of 57 macrophyte species were included in 966 drifting patches. This species composition was very different from the species compositions for the dredged macrophytes in this study. Only 15 of 76 species (19.7%) that were identified to the species level were identical to the species in the drifting patches; Dictyota dichotoma, Dilophus okamurae, Pachydictyon coriaceum, S. hemiphyllum, S. macrocarpum, S. micracanthum, Gelidium elegans, Gelidium pacificum, Hypnea japonica, Hypnea variabilis, Plocamium telfairiae, Portieria hornemannii, Campylaephora crassa, Acrosorium venulosum and Zostera marina. The only species found to be abundant in both the dredged macrophytes and the drifting patches was S. macrocarpum. This suggests that most species were transported to the dysphotic bottom through drift along the bottom, and not by sinking from the surface. In contrast, the species composition for the trawled macrophytes was more similar to the composition for the drifting patches reported by Hirata et al. (2001). Fifteen of the 29 species (51.7%) that were identified to the species level were identical to the species in the drifting patches; S. micracanthum, S. yamamotoi, Sargassum nipponicum, Sargassum yamadae, Sargassum piluliferum, Sargassum patens, S. macrocarpum, Sargassum crispifolium, S. hemiphyllum, Sargassum yendoi, Sargassum horneri, G. elegans, H. japonica, P. telfairiae, and Z. marina. These species are likely to be
delivered to the dysphotic bottom by sinking from the surface layer. Hirata et al. (2001) suggested that a large portion of the drifting algal patches were transported from seaweed beds in the coastal waters of the northern Kyushu and western Shikoku (the western Islands of the Japanese Archipelago) probably by the Kuroshio Current based on the similarity in the species compositions of the drifting algal patches. Drifting algal patches may possibly drift at sea surface for several weeks; e.g., experiments by Hobday (2000) indicated that ages of drifting Macrocystis pyrifera rafts were 63 and 109 days at maximum. A portion of the Sargassum species that were collected by trawling might have sunk onto the dysphotic bottom after lengthy drifts along the Kuroshio Current. However, the d15N signatures of the macrophytes suggest that transport from the west was small. The d15N values of the macrophytes from the dysphotic layer mainly ranged from 3 to 7% (Tables 1, 2), similar to the d15N signatures of macrophytes in the surf-zone in the study area (Takai et al., 2007). These d15N values were markedly lower than the main d15N distribution of 7–12% reported for the macroalgae in the western Seto Inland Sea (Takai, 2005). Thus, the d15N distributions suggest that the macrophytes from the dysphotic zone were mainly derived from macrophytes growing in the study area. The main organic carbon source for sea-bottom inhabitants is generally thought to be sinking particles that mainly originate from phytoplankton in surface water (e.g. Josefson and Conley,
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The C:N ratio of every type of macroalgae ranged from 8.8 to 29.1 (Tables 1 and 2), values much higher than the Redfield ratio for marine phytoplankton (molar C:N ratio of 6.6:1; Redfield et al., 1963). In contrast, the C:N ratios of the SOM in the shallower zone of 100 m deep mainly ranged from 7 to 9, only 0.4–2.4 higher than 6.6. If macrophytes are a main source, then the C:N ratio of the SOM should be much higher than 6.6 for fresh organisms derived from phytoplankton. The low values of the SOM suggest that the main carbon source for the SOM in the zone is not macrophytes but phytoplankton-originating organic matter. It is possible that a relatively small quantity of 13Cenriched macrophytes slightly increased the d13C of SOM in the shallower zone. Acknowledgements We thank E. Saito for his help in the sampling on the research boat and M. Aoki for his useful advice in the planning of this study. We are grateful to S. Kamura and A. Mikami for cooperation in species identification of macrophytes. This study was financially supported by the Grant-in-Aid for Scientific Research (No. 16780140) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT). The Open Research Center Project of Nihon University promoted by MEXT and the Sasakawa Scientific Research Grant from The Japan Science Society also provided financial support. References
Fig. 1. Depth-related changes of d13C (a), d15N (b), and C:N ratios (c) for surface sediments collected on 15 March 2005 and 13 July 2005.
1997). The importance of the phytoplankton-originating organic matter for heterotrophs within the 200–300 m zone was supported by the d13C distribution for the SOM; the d13C distribution of 24.6 to 19.3% for the SOM on the zone was similar to the distribution of POM reported for the surface and mesopelagic water (mainly 25 to 20%; Takai et al., 2007). In contrast, the SOM from the shallower zone of 100 m deep showed clearly higher d13C values of 19.6 to 17.3%. It is thus unlikely that the POM depleted in 13C is the single organic carbon source for the SOM in the shallower zone. We inferred that burial of macrophytes into the sediment caused the 13C enrichment in the shallower zones. The d13C of macroalgae in the surf zone of the study area ranged from 21.5 to 11.4% for 26 species (Takai et al., 2007). Most of the macrophytes collected from the dysphotic bottom also showed higher values with the maximum of 11.4% for Laurencia intelmedia, except for peculiarly low d13C values of 30.3 to 25.2% in five species (Tables 1 and 2). Notably, d13C for trawled macrophytes ranged from 19 to 11%. The dry weight of the macrophytes showed a maximum value of 426 mg m2 (in July), in contrast to the small values of 8 mg m2 for the 200– 300 m zone. Burial of these 13C-enriched macrophytes likely increased the d13C of SOM.
Hirata, T., Tanaka, J., Iwami, T., Ohmi, T., Dazai, A., Aoki, M., Ueda, H., Tsuchiya, Y., Sato, T., Yokohama, Y., 2001. Ecological studies on the community of drifting seaweeds in the south-eastern coastal waters of Izu Peninsula, central Japan. I: Seasonal changes of plants in species composition, appearance, number of species and size. Phycol. Res. 49, 215–229. Hobday, A.J., 2000. Age of drifting Macrocystis pyrifera (L.) C. Agardh rafts in the Southern California Bight. J. Exp. Mar. Biol. Ecol. 253, 97–114. Ishizaka, J., Takahashi, M., Ichimura, S., 1986. Changes in the growth rate of phytoplankton in local upwelling around the Izu Peninsula, Japan. J. Plankton Res. 8, 169–181. Josefson, A.B., Conley, D.J., 1997. Benthic response to a pelagic front. Mar. Ecol. Prog. Ser. 147, 49–62. Levin, L.A., Blair, N.E., Martin, C.M., DeMaster, D.J., Plaia, G., Thomas, C.J., 1999. Macrofaunal processing of phytodetritus at two sites on the Carolina margin: in situ experiments using 13C-labeled diatoms. Mar. Ecol. Prog. Ser. 182, 37–54. Mann, K.H., 1972. Ecological energetics of the sea-weed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Mar. Biol. 14, 199– 209. Mann, K.H., 2000. Ecology of Coastal Waters with Implications for Management, 2nd edn. Blackwell Science, MA. O’Leary, M.H., 1981. Carbon isotope fractionation in plants. Phytochemistry 20, 553–567. Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influence of organisms on the composition of sea-water. In: Hill, M.N. (Ed.), The Sea, vol. 2. Interscience, New York, pp. 26–77. Schoener, A., Rowe, G.T., 1970. Pelagic Sargassum and its presence among the deepsea benthos. Deep-Sea Res. 17, 923–925. Segawa, S., Sawada, T., Yoshida, T., 1964. Studies on the floating seaweeds—IX. The floating seaweeds found on the sea around Japan. J. Fac. Agric. Kyushu Univ. 21, 111–115. Takai, N., 2005. Carbon and nitrogen stable isotope ratios indicative of organic matter flow in the ecosystem of the Seto Inland Sea, Japan. Jpn. J. Ecol. 55, 269– 285 (in Japanese). Takai, N., Hirose, N., Osawa, T., Hagiwara, K., Kojima, T., Okazaki, Y., Kuwae, T., Taniuchi, T., Yoshihara, K., 2007. Carbon source and trophic position of pelagic fish in coastal waters of south-eastern Izu Peninsula, Japan, identified by stable isotope analysis. Fish. Sci. 73, 593–608. Vetter, E.W., Dayton, P.K., 1999. Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Mar. Ecol. Prog. Ser. 186, 137–148. Wada, E., Hattori, A., 1991. Nitrogen in the Sea: Forms, Abundances, and Rate Processes. CRC Press, FL. Yokohama, Y., Tanaka, J., Chihara, M., 1987. Productivity of the Ecklonia cava community in a bay of Izu Peninsula on the Pacific coast of Japan. Bot. Mag. Tokyo 100, 129–141. Yoshida, T., 1963. Studies on the distribution and drift of the floating seaweeds. Bull. Tohoku Reg. Fish. Res. Lab. 23, 141–186.
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Short communication
Transport and deposition of macrophytes to the dysphotic bottom of coastal waters Noriyuki Takai a,*, Emiri Takatsu a, Yuko Sawairi a, Tomohiro Kuwae b, Kiyoshi Yoshihara a a b
Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan Port and Airport Research Institute (PARI), Yokosuka, Kanagawa 239-0826, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2009 Received in revised form 9 November 2009 Accepted 26 January 2010 Available online 2 February 2010
Some macrophytes are transported to the deep-sea bottom and are utilized by heterotrophs in the deepsea as a food source. We inferred the transport route of macrophytes toward the deep-sea based on similarity in the species compositions of macrophyte pieces collected from the dysphotic bottom off the Izu Peninsula and the drifting macroalgae reported for the study area. We also examined whether or not the macrophytes are buried in the sediment, based on stable isotope distributions of organisms. Macrophytes collected by dredging at a depth of 100–300 m included 93 species, whereas 43 species were found by trawling at depths from 200 to 400 m. Only 15 of 76 dredged species (19.7%) that were identified to the species level were identical to the drifting macroalgal species reported for this area, whereas 15 of the 29 trawled species (51.7%) that were identified to the species level were identical to the reported drifting species. It was thus inferred that macrophytes were mainly transported through sliding along the sea bottom for the macrophytes collected by dredging and through sinking from the surface water for the macrophytes collected by trawling. The d13C of sedimentary organic matter (SOM) from the 200–300 m zone was similar to the d13C distribution of particulate organic matter in the surface water reported for the study area. The SOM in the zone likely originated from almost exclusively phytoplankton. In contrast, the 13C of SOM was significantly more enriched in shallow areas 100 m deep. We infer that not only phytoplankton but also macrophytes could supply organic matter to heterotrophs on the shallow bottom. ß 2010 Elsevier B.V. All rights reserved.
Keywords: Macroalga Transport Deposition Dysphotic bottom Drifting alga Stable isotope
1. Introduction Seaweed beds produce a large quantity of organic matter on the littoral and sublittoral bottom of coastal shallow areas (e.g., production of 1750 g C m2 y1 for Laminaria longicruris, Laminaria digitata and Agarum cribrosum; Mann, 1972). Macrophytes are abundantly deposited on the bottom around seaweed beds or get washed up on the shore. Consequently, macrophytes supply substantial nourishment to heterotrophs in shallow water ecosystems via direct digestion by herbivores and via indirect process through decomposition, physico-chemical precipitation, and microbial activity (Mann, 2000). Our concern here is transport of macrophytes toward the deepsea bottom. Some studies have presented evidence that heterotrophs in the deep-sea also utilize macrophytes as a major food source. A few Sargassum air bladders encrusted by ectoprocts were found in stomach contents of six brittlestars (Amphiophiura bullata) collected at depths of 2400–5042 m in the western Atlantic
* Corresponding author. Tel.: +81 466 84 3916; fax: +81 466 84 3689. E-mail address: [email protected] (N. Takai). 0304-3770/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2010.01.007
(Schoener and Rowe, 1970). Video observation in submarine canyons off southern California (mainly 100–550 m in depth) revealed that aggregations of macrophyte detritus were common and were associated with elevated densities of megafauna (Vetter and Dayton, 1999). Tracer experiments using 13C-labeled diatoms at two sites (850 m in depth) in the western Atlantic suggested that labile organic matter from fresh macrophyte detritus is quickly consumed by macrobenthos (Levin et al., 1999). Provided that macrophytes are an actual major food source for some deep-sea inhabitants, a constant supply of macrophytes from the euphotic zone would be essential for some deep-sea food webs. It is therefore important to elucidate the supply process for macrophyte-originating organic matter from the coastal ecosystem to the deep-sea ecosystem. Thus in the present study, we examined the species and quantity of macrophytes lying on the dysphotic bottoms in the coastal waters of the Izu Peninsula, Japan, to clarify the transport route of the macrophytes toward the deepsea. We predicted the following two potential routes: (1) sliding along the sea bottom and (2) drifting in the surface water followed by sinking. The study area has been precisely examined for species compositions of macrophytes in drifting macroalgal patches (Hirata et al., 2001). We inferred the transport route of the
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macrophytes from the shallow euphotic zone to the dysphotic zone, comparing species compositions between the drifting macrophytes and the macrophytes from the dysphotic bottoms. We also examined whether or not the macrophytes were buried in sediment of the dysphotic bottom, as determined from stable isotope ratios and elemental carbon and nitrogen contents of organisms. The burial of macrophytes means that macrophyteoriginating organic matter can be utilized as a food source for deposit-feeding benthos. Generally, the carbon isotope ratio (d13C) of primary producers reflects the concentration and the d13C signature of their inorganic carbon sources and isotope fractionation during uptake of inorganic carbon (O’Leary, 1981). The d13C distributions of macrophytes and particulate organic matter (POM) have been reported for the study area; d13C distributions mostly range from 17 to 11% for macrophytes in the surf zone and 24 to 20% for POM in the surface water (Takai et al., 2007). Therefore, we can infer the relative contribution of macrophytes and POM as organic carbon sources. The deposition of 13C-enriched species of macrophytes should increase d13C values of the sedimentary organic matter. As a secondary tracer, we also analyzed the nitrogen stable isotope ratio (d15N) of organisms. The d15N of primary producers varies with the concentration and the d15N signature of their inorganic nitrogen sources and isotope fractionation during uptake of inorganic nitrogen (Wada and Hattori, 1991). The potential variation in the d15N of organic matter at ecosystem bases provides a clue to the identity of nitrogen source of sedimentary organic matter (SOM). 2. Materials and methods The Izu Peninsula is located in the central area of the Japanese Archipelago, exposed to the open water of the Pacific Ocean. The surface water off the southeastern peninsula contains only a small quantity of nutrient (nitrate <0.6 mM) and chlorophyll a (<0.6 mg Chl a l1) originating from the Kuroshio water, except for the nutrient-rich subsurface waters where intermittent upwelling occurs (2 mM in nitrate and >1 mg l1 in Chl a) (Ishizaka et al., 1986). Macrophytes abundantly grow along the coastline in the littoral and sublittoral zone of this area. A large net production of ca. 2.9 kg dry weight m2 y1 was reported for the perennial brown alga Ecklonia cava (Yokohama et al., 1987). In Area A (348 34.90 N–348 39.00 N, 1388 55.80 E–1398 01.10 E), we collected macrophytes by dredging the sea bottom on July 8, August 5–6, October 13–15 and December 8 in 2004. The inner dimensions of the mouth of the dredge were 382 mm (width) and 100 mm (height) with a canvas sheet covering the aperture. Dredging was carried out with a research boat (R/V Suzaki II, 9 ton) for 10–20 min at each station in duplicate for every sampling month. In the second survey (August 5–6) and the third survey (October 13–15), it took 2–3 days to complete the surveys because of rough sea conditions. Difficulties in operating the boat for dredging resulted in variation of the total dredged distance from 919 to 1802 m. The dredge was hauled along four isobaths of 20, 100, 200 and 300 m. The euphotic zone in the study area has been proposed to be up to 50 m deep based on unpublished data for 1% light depth (e.g. Ishizaka et al., 1986). Therefore, we considered that the sea bottom was located in the euphotic zone for the 20 m depth zone and in the dysphotic zone for the 100–300 m depth zone. The macrophytes entangled on the frame and connecting chains of the dredge were included in the samples. We washed the samples through a 1 mm sieve on the boat and collected macrophytes from the residuals. The species of the collected macrophytes were identified to the lowest possible taxon. We multiplied the width of the dredge mouth by the total hauled distance in order to calculate the total
area dredged for each locality and subsequently calculate the dry weight per square meter for dredged macrophytes. In Area B (348 55.40 N–348 57.60 N, 1388 43.50 E–1388 45.00 E), we collected macrophytes by bottom trawling (25 mm mesh for the aperture) on 8 May 2004. This fishing gear is categorized as a firstclass hand trawl, permitted for this fishing ground by fisheries regulations. The gear uses no opener instruments such as beams and frames for the mouth of the net. During a trawling operation, the width of the net mouth gradually changes, therefore, we could not calculate the trawled area and consequently could not estimate the biomass of the collected macrophytes. In addition, we also analyzed the elemental contents of macrophytes collected in the surf zone of an embayment on April 9 and December 24 in 2004. The stable isotope ratios of identical samples were reported in the previous work (Takai et al., 2007). Surface sediments were collected with a Smith-MacIntire grab sampler in Area A and the embayment (5 m deep) on March 15 and July 13 in 2005. Samples were collected from six depth zones of 5, 10, 20, 100, 200, and 300 m. We collected the sediment from the upper 1 cm of the surface with a spatula. The macrophytes were dried at 60 8C after leaf surfaces were washed. The surface sediments were dried at 60 8C, treated with 1N HCl overnight to remove carbonate, and were dried again. These samples were ground to a fine powder with a mill. Stable isotope ratios of carbon and nitrogen were measured with a Delta Plus Advantage mass spectrometer (Thermo Finnigan) coupled to an elemental analyzer (Flash EA 1112, Thermo Finnigan). Isotope ratios, d13C and d15N, are expressed as per mil deviations from the standard as defined by the equation, (Rsample/Rstandard 1) 1000, where R = 13C/12C or 15N/14N. Belemnite (PDB) and atmospheric nitrogen were used as the isotope standards for carbon and nitrogen, respectively. The analytical precision for the isotopic analyses was 0.22% for d13C and 0.19% for d15N. Total organic carbon (TOC) content and total nitrogen (TN) content for the macrophytes and the SOM were measured with an elemental analyzer (Flash EA 1112, Thermo Finnigan). All statistical analyses were performed using Prism 4.0c (GraphPad Software). 3. Results In Area A, we dredged 101 species of macrophytes that were identified to the genus level. The macrophytes consisted of seven species of Chlorophyceae, 20 species of Phaeophyceae, 73 species of Rhodophyceae and a species of Monocotyledoneae (Spermatophyta). The number of species represented in the macrophytes from the dysphotic zone of 100–300 m deep was 73 on 8 July 2004, 56 on 5–6 August 2004, 44 on 13–15 October 2004, and 48 on 8 December 2004. A total of 93 species were collected from the dysphotic zone, with predominant appearance in the 100 m zone (91 species). The dry weight was greatest in the 100 m zone in July (426 mg m2) and August (393 mg m2). In July, the 26 most abundant species with dry weights 1.3 mg m2 represented 97.7% of the macrophytes in the zone as shown in Table 1. In October and December, the dry weight of dredged macrophytes from the 20 m zone was greater than that of the macrophytes in the 100 m zone; 552 mg m2 in October and 389 mg m2 in December. Macrophytes found in the 20 m zone for both months included a large sporophyte of the brown algae E. cava whose thick stipe remained. In comparison, the dry mass of macrophytes in the 200– 300 m zone was distinctly smaller with a maximum of 8 mg m2 for the 300 m zone in July. Macrophytes collected by trawling on 8 May 2004 consisted mostly of Phaeophyceae in weight, particularly Sargassum species (Table 2). Forty-three species and unidentified species (Laminar-
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Table 1 Elemental content, biomass, and stable isotope ratios (%) for carbon and nitrogen of macrophytes collected by dredging in the 100 m zone on 8 July 2004. The 26 most abundant species (1.3 mg m2) were analyzed. Dry weight (mg) per square meter and the C:N ratios (mol:mol) are also shown. Species
Phaeophyceae Dilophus okamurae Distromium decumbens Pachydictyon coriaceum Spatoglossum sp. Carpomitra costata Desmarestia tabacoides Ecklonia cava Sargassum hemiphyllum Sargassum macrocarpum Sargassum micracanthum Sargassum spp. Rhodophyceae Gelidium elegans Gelidium pacificum Pterocladiella capillacea Ptilophora subcostata Delisea japonica Prionitis angusta Prionitis crispata Prionitis divaricata Prionitis patens Callophyllis adhaerens Callophyllis spp. Plocamium telfairiae Schizymenia dabyi Chlorophyceae Ulva japonica Cladophora wrightiana
mg m2
C
N
C:N
C%
mg C m2
d13C
N%
mg N m2
d15N
24.5 10.1 27.6 1.5 1.3 2.7 62.8 18.1 20.1 2.0 3.7
34.5 31.4 38.9 24.5 31.2 29.9 36.3 37.7 39.6 35.8 39.7
8.44 3.17 10.74 0.37 0.40 0.82 22.80 6.83 7.96 0.72 1.45
22.6 19.7 22.0 22.6 26.1 22.3 17.1 20.2 19.5 20.6 20.3
2.6 2.6 2.5 1.7 2.5 1.9 2.3 2.1 1.9 1.7 2.1
0.64 0.26 0.68 0.03 0.03 0.05 1.43 0.37 0.38 0.04 0.08
2.8 5.0 3.5 3.0 2.8 3.6 3.8 2.3 3.5 3.9 6.2
15.4 14.3 18.4 16.4 14.8 18.7 18.6 21.3 24.4 24.0 21.7
23.1 2.5 7.7 123.0 10.4 5.7 1.4 1.4 9.9 14.1 1.3 9.2 2.8
36.8 41.3 42.4 37.2 30.9 35.1 33.4 29.7 38.5 24.9 32.6 28.3 30.6
8.52 1.02 3.24 45.80 3.21 1.99 0.48 0.40 3.82 3.52 0.42 2.61 0.86
19.7 16.9 19.2 22.3 25.2 17.2 19.2 17.6 18.4 30.3 17.8 29.5 30.2
2.8 2.4 3.4 3.0 3.6 2.8 3.2 2.1 4.1 3.3 3.2 3.6 2.4
0.65 0.06 0.26 3.64 0.37 0.16 0.05 0.03 0.41 0.47 0.04 0.33 0.07
4.4 4.7 4.9 3.8 2.4 4.1 5.0 5.1 2.4 3.7 3.3 3.4 5.6
15.2 20.3 14.6 14.7 10.1 14.5 12.3 16.5 10.9 8.8 12.0 9.1 14.9
7.8 21.7
37.2 36.2
2.91 7.84
15.7 17.3
4.9 3.3
0.38 0.71
5.7 3.1
8.8 12.8
iales spp., Sargassum spp. and Fucales spp.) totaled 555 g for the 200–400 m depth zone. Markedly abundant species included Sargassum yamamotoi, Sargassum micracanthum, Sargassum hemiphyllum, Eckloniopsis radicosa, Undaria undarioides and Sargassum macrocarpum. The d13C of macrophytes ranged from 30.3 to 15.7% for the 26 most abundant species (1.3 mg m2) collected by dredging in the 100 m zone in July (n = 26; Table 1) and from 20.6 to 11.6% for the abundant 14 species (>2.0 g per haul) collected by trawling in the 200–400 m zone (n = 31; Table 2). Takai et al. (2007) reported that the d13C of macroalgae in the surf zone ranged from 21.5 to 11.4% for 26 species. There was a significant difference among these three types of macrophytes (Kruskal–Wallis test, p < 0.0001). The analysis by Dunn’s multiple comparison test revealed a significant difference for dredged vs. trawled macrophytes (p < 0.001) and dredged vs. surf-zone macrophytes (p < 0.001), whereas the difference between trawled and surfzone macrophytes was not significant (p > 0.05). The d13C of SOM ranged from 24.6 to 18.5% on 15 March 2005 and from 20.4 to 17.3% on 13 July 2005 (Fig. 1a). The d13C of the SOM significantly decreased with the depth for both months (Spearman’s rank correlation coefficient; March, rs = 0.79, p < 0.05; July, rs = 0.83, p < 0.01). The d15N of the macrophytes ranged from 2.3 to 6.2% for the 26 most abundant dredged species in the 100 m zone in July (n = 26; Table 1) and from 3.0 to 9.7% for the 14 most abundant trawled species in the 200–400 m zone (n = 31; Table 2). Takai et al. (2007) reported that the d15N of macroalgae in the surf zone ranged from 4.7 to 7.4% for 26 species. There was a significant difference among these three types of macrophytes (Kruskal–Wallis test, p < 0.0001). An analysis by Dunn’s multiple comparison test showed a significant difference for every combination (dredged vs. trawled macrophytes, p < 0.01; dredged vs. surf-zone macrophytes, p < 0.001; trawled vs. surf-zone macrophytes, p < 0.05).
The d15N of SOM ranged from 4.4 to 6.4% in March and from 4.5 to 6.8% in July (Fig. 1b). No significant correlation was found between the depth and the d15N on either March 15 or July 13 in 2005 (Spearman’s rank correlation coefficient; March, rs = 0.67, p = 0.06; July, rs = 0.49, p = 0.19). The elemental contents of the 26 most abundant species in the 100 m zone in July averaged 34.4% (SD 4.7%; range 24.5–42.4%) for TOC and 2.8% (SD 0.8%; range 1.7–4.9%) for TN (Table 1). These values for elemental contents of dredged macrophytes were consistent with ranges for macroalgae collected from the surf zone; 24.5–42.9% for TOC and 1.7–4.9% for TN. Multiplying the percentage by the dry weight for each species, the contents of these 26 species totaled 150.3 mg C m2 and 11.6 mg N m2. The C:N ratio (mol:mol) ranged from 8.8 to 24.4 for the dredged macrophytes. Elemental contents of the main species (2.0 g) in the trawled macrophytes averaged 37.1% (SD 3.6%; range 24.0–42.3%) for TOC and 2.2% (SD 0.4%; range 1.5–3.0%) for TN (Table 2). These values were also consistent with the ranges for macroalgae from the surf zone. The C:N ratio of the trawled macrophytes ranged from 11.7 to 29.1. Elemental contents of SOM ranged from 0.07 to 0.30% for TOC and from 0.01 to 0.04% for TN. The C:N ratio of the SOM ranged from 6.8 to 16.9 (Fig. 1c). Extremely high C:N ratios of 15.6–16.9 were found for samples from the 300 m zone where the TN showed strikingly low values of 0.01%. The C:N ratio significantly increased with the water depth (Spearman correlation coefficient; March, rs = 0.78, p < 0.05; July, rs = 0.78, p < 0.05). 4. Discussion Some observations in the past studies indicated that drifting algal patches were scarce in the study area in comparison with other areas around the Japanese Archipelago (Yoshida, 1963;
N. Takai et al. / Aquatic Botany 92 (2010) 289–293
292
Table 2 Total dry weight (g) per haul, and elemental contents and stable isotope ratios (%) for carbon and nitrogen of macrophytes collected by bottom trawling at the depth zone of 200–400 m on 8 May 2004. The 14 most abundant species (2.0 g) including Sargassum spp. were analyzed. The C:N ratios (mol:mol) are also shown. Depth (m)
Weight
C%
d13C
N%
d15N
C:N
200 300 400
2.9 34.0 3.1
35.9 37.0 36.1
13.8 15.9 14.3
2.8 2.6 2.7
5.8 6.1 7.5
14.7 16.8 15.7
Undaria pinnatifida
300 400
2.9 5.0
36.9 36.7
17.9 14.9
2.6 2.4
5.5 7.7
16.8 17.9
Undaria undarioides
200 300 400
4.3 28.3 1.6
34.0 36.5 28.6
18.0 15.2 11.6
3.0 2.8 2.4
8.1 5.2 7.1
13.4 14.9 14.2
Sargassum piluliferum
200 300 400
1.8 9.5 1.3
24.0 37.4 36.8
14.4 14.8 20.6
2.4 1.9 2.4
9.7 5.3 4.1
11.7 23.0 17.8
Sargassum patens
400
2.7
36.1
14.6
2.1
6.0
19.8
S. macrocarpum
200 300
3.0 21.0
38.1 40.8
17.1 20.1
1.8 1.9
4.4 3.0
25.1 25.6
Sargassum siliquastrum
200 300 400
2.1 1.4 4.8
37.7 38.5 39.8
17.1 15.0 15.0
1.7 2.2 2.0
3.5 4.5 3.4
25.5 20.0 22.7
Sargassum yamamotoi
200 300 400
10.6 90.3 58.4
35.9 39.0 39.2
15.9 15.2 13.8
1.5 1.7 1.7
6.0 4.5 3.0
28.7 27.0 26.6
Sargassum yamadae
300
16.8
40.9
16.0
2.0
4.9
23.7
S. hemiphyllum
200 300 400
3.4 53.0 1.2
33.0 36.4 37.9
14.9 17.1 15.3
2.4 2.1 2.4
5.8 5.2 5.0
16.1 20.4 18.5
S. micracanthum
200 300 400
18.9 75.1 41.8
41.5 42.3 41.3
15.4 17.6 16.8
2.2 1.9 2.4
4.4 3.9 4.0
22.3 25.4 19.9
Sargassum yendoi
300
3.0
37.5
16.7
2.0
4.8
22.2
Sargassum sp. 1
200
13.4
40.1
16.7
1.6
3.7
29.1
Sargassum spp.
300 400
9.2 1.7
36.3 37.4
15.6 16.2
2.2 2.1
5.8 4.6
19.0 21.2
Species Phaeophyceae Eckloniopsis radicosa
The trawl net was towed 1833 m for the 200 m zone, 2590 m for the 300 m zone, and 1341 m for the 400 m zone.
Segawa et al., 1964). However, Hirata et al. (2001) found that a substantial quantity of drifting patches gathered along tidal fronts in the area during spring to autumn. They reported that a total of 57 macrophyte species were included in 966 drifting patches. This species composition was very different from the species compositions for the dredged macrophytes in this study. Only 15 of 76 species (19.7%) that were identified to the species level were identical to the species in the drifting patches; Dictyota dichotoma, Dilophus okamurae, Pachydictyon coriaceum, S. hemiphyllum, S. macrocarpum, S. micracanthum, Gelidium elegans, Gelidium pacificum, Hypnea japonica, Hypnea variabilis, Plocamium telfairiae, Portieria hornemannii, Campylaephora crassa, Acrosorium venulosum and Zostera marina. The only species found to be abundant in both the dredged macrophytes and the drifting patches was S. macrocarpum. This suggests that most species were transported to the dysphotic bottom through drift along the bottom, and not by sinking from the surface. In contrast, the species composition for the trawled macrophytes was more similar to the composition for the drifting patches reported by Hirata et al. (2001). Fifteen of the 29 species (51.7%) that were identified to the species level were identical to the species in the drifting patches; S. micracanthum, S. yamamotoi, Sargassum nipponicum, Sargassum yamadae, Sargassum piluliferum, Sargassum patens, S. macrocarpum, Sargassum crispifolium, S. hemiphyllum, Sargassum yendoi, Sargassum horneri, G. elegans, H. japonica, P. telfairiae, and Z. marina. These species are likely to be
delivered to the dysphotic bottom by sinking from the surface layer. Hirata et al. (2001) suggested that a large portion of the drifting algal patches were transported from seaweed beds in the coastal waters of the northern Kyushu and western Shikoku (the western Islands of the Japanese Archipelago) probably by the Kuroshio Current based on the similarity in the species compositions of the drifting algal patches. Drifting algal patches may possibly drift at sea surface for several weeks; e.g., experiments by Hobday (2000) indicated that ages of drifting Macrocystis pyrifera rafts were 63 and 109 days at maximum. A portion of the Sargassum species that were collected by trawling might have sunk onto the dysphotic bottom after lengthy drifts along the Kuroshio Current. However, the d15N signatures of the macrophytes suggest that transport from the west was small. The d15N values of the macrophytes from the dysphotic layer mainly ranged from 3 to 7% (Tables 1, 2), similar to the d15N signatures of macrophytes in the surf-zone in the study area (Takai et al., 2007). These d15N values were markedly lower than the main d15N distribution of 7–12% reported for the macroalgae in the western Seto Inland Sea (Takai, 2005). Thus, the d15N distributions suggest that the macrophytes from the dysphotic zone were mainly derived from macrophytes growing in the study area. The main organic carbon source for sea-bottom inhabitants is generally thought to be sinking particles that mainly originate from phytoplankton in surface water (e.g. Josefson and Conley,
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The C:N ratio of every type of macroalgae ranged from 8.8 to 29.1 (Tables 1 and 2), values much higher than the Redfield ratio for marine phytoplankton (molar C:N ratio of 6.6:1; Redfield et al., 1963). In contrast, the C:N ratios of the SOM in the shallower zone of 100 m deep mainly ranged from 7 to 9, only 0.4–2.4 higher than 6.6. If macrophytes are a main source, then the C:N ratio of the SOM should be much higher than 6.6 for fresh organisms derived from phytoplankton. The low values of the SOM suggest that the main carbon source for the SOM in the zone is not macrophytes but phytoplankton-originating organic matter. It is possible that a relatively small quantity of 13Cenriched macrophytes slightly increased the d13C of SOM in the shallower zone. Acknowledgements We thank E. Saito for his help in the sampling on the research boat and M. Aoki for his useful advice in the planning of this study. We are grateful to S. Kamura and A. Mikami for cooperation in species identification of macrophytes. This study was financially supported by the Grant-in-Aid for Scientific Research (No. 16780140) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT). The Open Research Center Project of Nihon University promoted by MEXT and the Sasakawa Scientific Research Grant from The Japan Science Society also provided financial support. References
Fig. 1. Depth-related changes of d13C (a), d15N (b), and C:N ratios (c) for surface sediments collected on 15 March 2005 and 13 July 2005.
1997). The importance of the phytoplankton-originating organic matter for heterotrophs within the 200–300 m zone was supported by the d13C distribution for the SOM; the d13C distribution of 24.6 to 19.3% for the SOM on the zone was similar to the distribution of POM reported for the surface and mesopelagic water (mainly 25 to 20%; Takai et al., 2007). In contrast, the SOM from the shallower zone of 100 m deep showed clearly higher d13C values of 19.6 to 17.3%. It is thus unlikely that the POM depleted in 13C is the single organic carbon source for the SOM in the shallower zone. We inferred that burial of macrophytes into the sediment caused the 13C enrichment in the shallower zones. The d13C of macroalgae in the surf zone of the study area ranged from 21.5 to 11.4% for 26 species (Takai et al., 2007). Most of the macrophytes collected from the dysphotic bottom also showed higher values with the maximum of 11.4% for Laurencia intelmedia, except for peculiarly low d13C values of 30.3 to 25.2% in five species (Tables 1 and 2). Notably, d13C for trawled macrophytes ranged from 19 to 11%. The dry weight of the macrophytes showed a maximum value of 426 mg m2 (in July), in contrast to the small values of 8 mg m2 for the 200– 300 m zone. Burial of these 13C-enriched macrophytes likely increased the d13C of SOM.
Hirata, T., Tanaka, J., Iwami, T., Ohmi, T., Dazai, A., Aoki, M., Ueda, H., Tsuchiya, Y., Sato, T., Yokohama, Y., 2001. Ecological studies on the community of drifting seaweeds in the south-eastern coastal waters of Izu Peninsula, central Japan. I: Seasonal changes of plants in species composition, appearance, number of species and size. Phycol. Res. 49, 215–229. Hobday, A.J., 2000. Age of drifting Macrocystis pyrifera (L.) C. Agardh rafts in the Southern California Bight. J. Exp. Mar. Biol. Ecol. 253, 97–114. Ishizaka, J., Takahashi, M., Ichimura, S., 1986. Changes in the growth rate of phytoplankton in local upwelling around the Izu Peninsula, Japan. J. Plankton Res. 8, 169–181. Josefson, A.B., Conley, D.J., 1997. Benthic response to a pelagic front. Mar. Ecol. Prog. Ser. 147, 49–62. Levin, L.A., Blair, N.E., Martin, C.M., DeMaster, D.J., Plaia, G., Thomas, C.J., 1999. Macrofaunal processing of phytodetritus at two sites on the Carolina margin: in situ experiments using 13C-labeled diatoms. Mar. Ecol. Prog. Ser. 182, 37–54. Mann, K.H., 1972. Ecological energetics of the sea-weed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Mar. Biol. 14, 199– 209. Mann, K.H., 2000. Ecology of Coastal Waters with Implications for Management, 2nd edn. Blackwell Science, MA. O’Leary, M.H., 1981. Carbon isotope fractionation in plants. Phytochemistry 20, 553–567. Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influence of organisms on the composition of sea-water. In: Hill, M.N. (Ed.), The Sea, vol. 2. Interscience, New York, pp. 26–77. Schoener, A., Rowe, G.T., 1970. Pelagic Sargassum and its presence among the deepsea benthos. Deep-Sea Res. 17, 923–925. Segawa, S., Sawada, T., Yoshida, T., 1964. Studies on the floating seaweeds—IX. The floating seaweeds found on the sea around Japan. J. Fac. Agric. Kyushu Univ. 21, 111–115. Takai, N., 2005. Carbon and nitrogen stable isotope ratios indicative of organic matter flow in the ecosystem of the Seto Inland Sea, Japan. Jpn. J. Ecol. 55, 269– 285 (in Japanese). Takai, N., Hirose, N., Osawa, T., Hagiwara, K., Kojima, T., Okazaki, Y., Kuwae, T., Taniuchi, T., Yoshihara, K., 2007. Carbon source and trophic position of pelagic fish in coastal waters of south-eastern Izu Peninsula, Japan, identified by stable isotope analysis. Fish. Sci. 73, 593–608. Vetter, E.W., Dayton, P.K., 1999. Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Mar. Ecol. Prog. Ser. 186, 137–148. Wada, E., Hattori, A., 1991. Nitrogen in the Sea: Forms, Abundances, and Rate Processes. CRC Press, FL. Yokohama, Y., Tanaka, J., Chihara, M., 1987. Productivity of the Ecklonia cava community in a bay of Izu Peninsula on the Pacific coast of Japan. Bot. Mag. Tokyo 100, 129–141. Yoshida, T., 1963. Studies on the distribution and drift of the floating seaweeds. Bull. Tohoku Reg. Fish. Res. Lab. 23, 141–186.