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Effects of Hypoxia on Early Life History of the Stomatopod Oratosquilla Oratoria in a Coastal Sea

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Effects of Hypoxia on Early Life History of the Stomatopod Oratosquilla Oratoria in a Coastal Sea MARINE ECOLOGY PROGRESS SERIES Vol. 324: 197–206, 2006 Published October 23 Mar Ecol Prog Ser Effects of hypoxia on early life history of the stomatopod Oratosquilla oratoria in a coastal sea Keita Kodama1, 5,*, Toshihiro Horiguchi1, 5, Gen Kume1, 6, Satoshi Nagayama2, Takamichi Shimizu3, Hiroaki Shiraishi1, 5, Masatoshi Morita1, Makoto Shimizu4 1Endocrine Disrupters and Dioxin Research Project, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan 2Agriculture, Forestry and Fisheries Department, Chiba Prefectural Office, 1-1 Ichibacho, Chuou-ku, Chiba, Chiba 260-8667, Japan 3Resources and Environment Division, Kanagawa Prefectural Fisheries Technology Center, Jogashima, Misaki, Miura, Kanagawa 238-0237, Japan 4Faculty of Agriculture, University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan 5Present address: Research Center for Environmental Risk, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan 6Present address: Faculty of Fisheries, Nagasaki University, Bunkyo-machi, Nagasaki 852-8521, Japan ABSTRACT: Bottom hypoxia is considered to be one of the factors affecting the recent stock decline of the mantis shrimp Oratosquilla oratoria in Tokyo Bay, Japan. We used field surveys of the bay to investigate the spatiotemporal pattern of bottom hypoxia and the early life history of O. oratoria, and we examined the effects of bottom hypoxia on early life history by nonparametric analyses. Bottom hypoxia in Tokyo Bay began to appear in April, occupied more than half (55 to 67%) of the whole bay area in July and August, and disappeared from November onward. Newly settled juveniles appeared in September–October in the northeastern shallow coastal area, where the hypoxic bottom water had disappeared. After the hypoxia had abated, the distribution of juveniles expanded to the south- central deep area. Classification and regression tree analysis showed that the threshold level of bottom dissolved oxygen concentration for the existence of juveniles was 2.78 ml l–1, implying that hypoxia restricted the spatial distribution of juveniles. A generalized additive model showed that sampling date, bottom dissolved oxygen concentration, depth, latitude, and longitude had significant effects on the occurrence of juveniles, suggesting an adverse effect of hypoxia on the time and loca- tion of settlement of O. oratoria. Our results suggest that hypoxia is directly and/or indirectly associ- ated with mass-mortality events during early life history. KEY WORDS: Hypoxia · Settlement · Recruitment · Juvenile · Oratosquilla oratoria · Tokyo Bay Resale or republication not permitted without written consent of the publisher INTRODUCTION (e.g. fishes, crabs, or shrimps) can avoid hypoxic areas and migrate to normoxic refuges (e.g. Pihl et al. 1991, Oxygen depletion (hypoxia) in bottom water occurs Breitburg 1992, Eby & Crowder 2002, Craig & Crowder in eutrophic estuarine and coastal systems throughout 2005). This migration, however, causes contraction of the world and is a growing global problem (Diaz & the spatial distribution of motile fishes and inverte- Rosenberg 1995). Bottom hypoxia (dissolved oxygen brates to oxygenated areas, which results in higher [DO] concentration ≤ 2 ml l–1; Diaz & Rosenberg 1995) densities and substantial overlap with competitors and has various adverse effects on benthic organisms. For predators, suggesting the possibilities of higher risks of example, hypoxia induces mass mortality of sessile predation, increased competition for limited prey benthic organisms (Baden et al. 1990). Motile animals availability, and subsequent decrease in growth rate *Email: [email protected] © Inter-Research 2006 · www.int-res.com 198 Mar Ecol Prog Ser 324: 197–206, 2006 (e.g. Baden et al. 1990, Eby & Crowder 2002, Craig & An understanding of the early life history of Crowder 2005, Eby et al. 2005). In addition, hypoxia Oratosquilla oratoria and the factors affecting mortal- impairs fish reproduction; exposure of adults of the ity during each life stage is critical if we are to under- carp Cyprinus carpio to hypoxic water in a laboratory stand the mechanisms that determine the year-class experiment caused a decrease in serum levels of strength. We aimed to reveal the effects of hypoxia on testosterone, estradiol, and triiodothyronine, and this the early life history of O. oratoria — in particular on in turn resulted in deterioration of gonadal develop- the time and location of settlement and the spatial dis- ment, spawning success, fertilization success, hatching tribution of juveniles. We collected hydrographic data rate, and larval survival (Wu et al. 2003). and O. oratoria juveniles by baywide field sampling Tokyo Bay, central Japan (see Fig. 1), is a heavily and used nonparametric analyses to investigate: (1) the eutrophic area in which hypoxia occurs in the bottom temporal pattern of the spatial extent and distribution water from spring to autumn (Fujiwara & Yamada of hypoxia in the bay; (2) the spatiotemporal pattern of 2002). The mantis shrimp Oratosquilla oratoria (Crus- the occurrence of juveniles in the bay; and (3) the tacea: Stomatopoda), is one of the dominant species in effect of hypoxia on the early life history of O. oratoria. the demersal fauna of Tokyo Bay, and it is the most commercially valuable species in the bottom-trawl fisheries there (Kodama et al. 2002, 2003, 2006b). How- MATERIALS AND METHODS ever, the stock size of O. oratoria in Tokyo Bay dropped dramatically in the late 1980s and has since remained General life history traits of Oratosquilla oratoria. low (Kodama et al. 2002), resulting in hardship for the In Tokyo Bay, O. oratoria lives for at least 4 yr local fishing industry. From multivariate analyses of (Kodama et al. 2005, 2006c). Its spawning season lasts long-term biotic and abiotic data, Kodama et al. (2002) from April to September. There are 2 spawning peaks hypothesized that a decreasing trend in dissolved oxy- for the population in Tokyo Bay: the early spawning gen concentration in the bottom water of the bay may season in May by large females of body length (BL) ≥ be one of the factors causing the stock-size decline 10 cm (≥ 1 yr) and the late spawning season in August of O. oratoria and other benthic organisms there, al- by small females of 7 ≤ BL < 10 cm (0–1 yr; Kodama et though the mechanisms have remained unclear. al. 2004, 2006a) (BL is measured from the base of the In marine organisms, survival during the early life rostrum to the anterior edge of the median notch of stages (egg, larval, and juvenile stages) is considered the telson). The spawning ground of O. oratoria is the most important phase determining subsequent located in the southern part of the bay (below the line year-class strength, through the effect of predation, between the Tama River and Sodegaura; Ohtomi & starvation, and physical processes such as passive Shimizu 1991; see Fig. 1). After spawning females transportation during the egg and/or larval stages brood their eggs for 2 to 3 wk until hatching, and the (Jennings et al. 2001). Hypoxia is also a factor affecting larval phase lasts 5 to 7 wk (Hamano & Matsuura survival of the early life stages of aquatic organisms. 1984, 1987a). Therefore, it takes 7 to 10 wk from egg Experimental studies have shown that predation of laying to settlement. naked goby Gobiosoma bosc larvae by scyphomedusa Hydrographic data. To assess the effects of hypoxia Chrysaora quinquecirrha increases in hypoxic condi- on the early life history of Oratosquilla oratoria, we tions, probably as a result of impairment of the ability examined the temporal and spatial distribution and of the larvae to escape the scyphomedusa (Breitburg et spatial extent of hypoxic bottom water. Contour maps of al. 1994, 1997). Few field studies have shown the the DO concentrations in the bottom layer (<1 m above effects of hypoxia on postsettled juveniles in field situ- the sea bottom) of Tokyo Bay from April to December ations. In Chesapeake Bay, intrusion of the most 2004 were obtained from the website of the Chiba severely hypoxic water into the areas where recruit- Prefectural Fisheries Research Center (www.pref. ment of postsettled G. bosc is highest coincides with chiba.jp/laboratory/fisheries/index; in Japanese), from the peak periods of recruitment. This results in which 1 to 4 DO contour maps were available each extremely high mortality of the newly settled juveniles, month. The DO contours were generated using the com- which require higher dissolved oxygen concentrations puter software Program for Displaying Water Qualities of than do older individuals (Breitburg 1992). In the Tokyo Bay (Chuden CTI, Nagoya, Japan) with a spline Neuse River Estuary, the growth rate of juveniles of the interpolation routine. To quantify the spatial extent of Atlantic croaker Micropogonias undulatus is declining hypoxia, the proportion of hypoxic (DO ≤ 2 ml l–1) area with habitat contraction and decreased prey availabil- was calculated for each contour map by dividing the ity, which have resulted from the effects of hypoxia; number of pixels of hypoxic area by the total number of this will probably also result in a reduction in popula- pixels in the study area and multiplying by 100, using tion growth rate (Eby et al. 2005). Adobe Photoshop 5.5 image processing software. Kodama et al.: Hypoxia affects shrimp early life history 199 During juvenile sampling (see next section), we also sets that most significantly reduce the variability of the observed water temperature and salinity in the surface response variable (Clark & Pregibon 1992, Eby & (<1 m below the sea surface) and bottom (<1 m above Crowder 2002), using the juvenile presence/absence the sea bottom) layers and DO concentration in the data and the DO concentration. bottom layer, using a YSI-85 conductivity, tempe- To elucidate the spatiotemporal effect of abiotic vari- rature, and depth (CTD) probe (YSI Inc.). The monthly ables on the spatial distribution and settlement period averages for each hydrographic variable at the surface of juveniles, we used a generalized additive model and bottom of the study area were calculated.
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