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In Situ Observations of a Doliolid Bloom in a Warm Water

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In Situ Observations of a Doliolid Bloom in a Warm Water LIMNOLOGY and Limnol. Oceanogr. 60, 2015, 1763–1780 VC 2015 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. OCEANOGRAPHY on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10133 In situ observations of a doliolid bloom in a warm water filament using a video plankton recorder: Bloom development, fate, and effect on biogeochemical cycles and planktonic food webs Kazutaka Takahashi,*1 Tadafumi Ichikawa,2 Chika Fukugama,1 Misaki Yamane,1 Shigeho Kakehi,3 Yuji Okazaki,3 Hiroshi Kubota,2 Ken Furuya1 1Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan 2Research Center for Fisheries Oceanography and Marine Ecosystem, National Fisheries Research Institute, Fukuura, Kanazawa-ku, Yokohama, Japan 3Fisheries Management and Oceanography Division, Tohoku National Fisheries Research Institute, Shiogama, Japan Abstract We investigated distribution patterns of a doliolid (Dolioletta gegenbauri) bloom in relation to the physical environment using a video plankton recorder in the Oyashio–Kuroshio mixed water region. Using 12 km trans- ects, doliolid blooms were encountered at a horizontal scale of about 2–3 km, which corresponds to submeso- scale physical events. Doliolids were also consistently encountered in the subsurface layer above the pycnocline in warmer (> 14C) and higher-salinity (> 34) water masses, and seawater density was the most critical factor affecting distribution depth. Compared to previous studies, the density and biomass of the blooms observed in this study (77 mgC m23 and 4600 inds m23) were highest in the open ocean. Bloom formation consisted of two phases; first, the seeding population of a nurse stage increased rapidly to 2000 inds m23 by asexual reproduc- tion, followed by asexual production of phorozooids. Estimated population clearance rates revealed that these dense patches could potentially sweep the surrounding water within 2–3 d. The incidence of exhausted and shrunken zooids was significantly correlated with patch density, suggesting that mortality was due to overgraz- ing. Shrunken doliolids appeared to sink below the pycnocline, corresponding to 8–17% of the particulate organic carbon flux at 150 m. Hydromedusae, pelagic polycheates, and sapphirinid copepods preyed on the doliolids. These results indicate that doliolids, which were seeded by populations originating from the Kur- oshio, formed dense blooms in response to submesoscale physical events and would alter the sinking particle properties (i.e., biological pump) and the epipelagic food web structure through their grazing and mortality. An important goal of marine ecology studies is to under- Doliolids are pelagic tunicates with a complex life cycle that stand the distribution patterns of marine organisms and the includes polymorphic asexual and sexual reproductive stages structure and functioning of pelagic ecosystems, as doing so (Paffenhofer€ and Koster€ 2011); having both stages means that can be used to predict how environmental changes and doliolids are capable of responding to favorable conditions by human activities will impact the distribution patterns of producing offspring quickly (Deibel 1998; Deibel and marine fauna and the biology of the ocean (Kiørboe 2011). Paffenhofer€ 2009). As doliolids are nonselective filter feeders Within this context, the ephemeral, patchy, and sporadic that feed on particulate organic matter ranging in size from nature of doliolid blooms makes these events very difficult to bacteria to copepod eggs (Crocker et al. 1991; Paffenhofer€ investigate in any detail (Deibel and Paffenhofer€ 2009). et al. 1995), they are considered to have a marked effect on plankton community structure and biogeochemical cycles in *Correspondence: [email protected] the area where their blooms occur (Deibel 1985; Paffenhofer€ et al. 1995). This is an open access article under the terms of the Creative Commons Despite their potential significance in pelagic ecosystems, Attribution-NonCommercial-NoDerivs License, which permits use and distri- bution in any medium, provided the original work is properly cited, the use relatively little is known about the factors that cause doliolid is non-commercial and no modifications or adaptations are made. blooms and the fate of the blooms. Given the sudden Additional Supporting Information may be found in the online version of appearance and disappearance of blooms by asexual repro- this article. duction, doliolids are considered to be adapted to event- 1763 Takahashi et al. Development and fate of doliolid boom Fig. 1. Satellite images of (A, C) surface-water temperature and (B, D) Chl a concentrations around sampling area for late May 2009 (8-d composite) derived from MODIS Aqua data (Ocean Watch, NOAA). Transect lines for VPR observations are also shown. scale rather than seasonal-scale changes in environmental pling is often not sufficient to reveal the vertical and conditions (Deibel and Lowen 2012). For example, in the horizontal scales of doliolid patchiness. To overcome these South Atlantic Bight (SAB) off the coast of Florida, U.S.A., problems, nonintrusive and consecutive optical sampling high rates of phytoplankton production in response to techniques are considered preferable. Paffenhofer€ et al. upwelling are a primary condition necessary for the occur- (1991) observed the vertical profiles of doliolids by video rence of doliolid blooms along the continental shelf (Deibel filming from a manned submersible. More recently, the 1985; Paffenhofer€ et al. 1995). Deibel and Paffenhofer€ (2009) three-dimensional mesoscale structural characteristics of a concluded that thaliacean blooms (doliolids and salps) salp swarm (Thalia democratica) was captured using an opti- require a broad, shallow continental shelf, a strong boundary cal plankton recorder (Everett et al. 2011). Although these current with eddies and meanders, and along-shelf winds studies successfully clarified some of the factors affecting the that promote upwelling. However, as patches of thaliaceans distribution of thaliacean patches, the resolution of their also occur in the open ocean (Tsuda and Nemoto 1992; analyzes was not sufficient for relating the patch dynamics Takahashi unpubl), further investigations on the patch of the patches to environmental factors. We, therefore, dynamics of thaliacean blooms in relation to the physical attempted to accurately clarify the distribution patterns of oceanographic conditions are necessary. In particular, knowl- doliolid blooms in relation to the hydrographical conditions edge of the factors affecting the termination process and fate in the Oyashio–Kuroshio mixed water region in the North- of the bloom is crucial to our understanding of the role of eastern Pacific using a video plankton recorder (VPR). In doliolid blooms in marine biogeochemical cycles. doing so, we sought to infer the processes underlying the In addition to their sporadic occurrence, the fragile gelati- development, fate, and effect of the doliolid bloom on the nous bodies of doliolids make them difficult to collect using biogeochemical cycle and planktonic food web. nets, further complicating investigations on the ecology of these organisms. In particular, information on the nurse stage, which is critical for asexual reproduction and conse- Methods quently for causing blooms, is very difficult to obtain as the Field research dorsal cadophore is typically lost when sampling is per- This study was conducted onboard the R. V. Soyo-Maru formed using nets. In addition, the resolution of net sam- of the Fisheries Research Agency from 29 May 2009 to 2 1764 Takahashi et al. Development and fate of doliolid boom 2 June 2009 in the Oyashio–Kuroshio mixed water region in Phorozooids : BL ¼ 2:7406DOR 1 1:1363; R ¼ 0:70892 ðÞn ¼ 113 the Northwestern Pacific Ocean (Fig. 1). We deployed a (2) VPR (Color Auto-VPR, SeaScan), which captures images using a charge-coupled device camera at a resolution of The equation used for gonozooids (Eq. 1) was also applied 1024 3 1024 pixels and 15 frames per second along two to oozooids and unidentified solitary zooids when their transect lines across a warm water filament during day- images were not taken from lateral side. The number of time (07: 36–14: 53 h). The field of view of the image was trophozooids on the dorsal cadophore of nurses (NT) was calibrated to 37.9 3 37.9 3 89.0 mm (height 3 width 3 determined based on the length of the cadophore (LC in depth, 37.04 lmpixel21), giving an image volume of mm) using the following equation (Eq. 3) applied to in-focus 127.8 mL and objects within this field were confirmed to images of nurses that were captured along the two observa- be captured as in-focus images (Ichikawa 2008). The VPR tion transects: was towed from the starboard side of the vessel at a speed N ¼ 2:2525L0:8966; R2 ¼ 0:75976 ðÞn ¼ 118 (3) of 2–3 knots and continuously lowered and raised 16–18 T C times between the surface and a depth of 50 m along the During the manual sorting of the images, potential two 12 km- to 14 km-long transects. Cable release and doliolid predators were also identified. heaving speed were approximately 0.2 m s21.TheVPR system also included a CTD sensor (MCTD, Falmouth Sci- Biomass and potential clearance capacity entific), which logged temperature and salinity data. Using the length frequency data of doliolids, we esti- Chlorophyll a (Chl a) concentration was measured with mated the carbon biomass and potential clearance capacity
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