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Factors Affecting Seasonal Mortality of Rosy Bitterling (Rhodeus Ocellatus Kurumeus) Embryos on the Gills of Their Host Mussel

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Factors Affecting Seasonal Mortality of Rosy Bitterling (Rhodeus Ocellatus Kurumeus) Embryos on the Gills of Their Host Mussel Popul Ecol (2005) 47:41–51 DOI 10.1007/s10144-004-0201-0 ORIGINAL ARTICLE Jyun-ichi Kitamura Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel Received: 1 June 2004 / Accepted: 4 October 2004 / Published online: 20 November 2004 Ó The Society of Population Ecology and Springer-Verlag Tokyo 2004 Abstract I investigated the seasonal change in factors asphyxiation. Increased embryo mortalities may arise affecting embryonic mortality in the rosy bitterling, through competition among embryos, between embryos Rhodeus ocellatus kurumeus, a freshwater fish that and mussel, and ambient dissolved oxygen levels. The spawns on the gills of living unionid mussels. Research optimal period for bitterling to spawn may represent a was conducted in a small pond during 1999 and 2001 in balance between two opposing factors; with positive which bitterling were provided with Anodonta sp. and negative effects of a seasonal rise in temperature mussels for spawning. Bitterling spawned between April directly affecting embryonic growth rate and oxygen and July, peaking mid–late May. Seasonal survival rate availability. of bitterling embryos in their mussel hosts was uni- modal, with a peak between late April and mid May Keywords Freshwater mussel Æ Oxygen availability Æ (about 70% of total spawnings). In mid April, survival Adaptation Æ Oviposition Æ Density dependence Æ was about 50%. The lowest survival was from late May Egg size to July (0%). Losses of bitterling embryos from mussels were identified by ejections from the mussel host. Ejections were categorized as either ejections of live embryos, or ejections of embryos that died in the Introduction mussel and were subsequently expelled from the mussel. Ejection rates of live embryos were higher in the earlier In oviparous species, embryo traits and parental ovi- part of the spawning period (early–mid April) and dead position decisions can directly affect the survival of embryo ejections in the later period (after June). The offspring and thereby affect parental fitness. However, ejection rate of live embryos was higher among younger the effects of these adaptive traits and oviposition deci- embryos earlier in the season, probably because of the sions may vary seasonally with changes in biotic and incomplete development of morphological and abiotic factors. The fitness consequence of seasonal behavioural traits associated with maintaining the em- timing of reproduction in relation to habitat quality has bryo inside the mussel gill chambers, and as a conse- been studied for insect herbivores (e.g. Hunter and quence of a more protracted developmental period at McNeil 1997) and plants (e.g. Suzuki 2002, 2003). low temperatures making them more susceptible to However, the consequences of such seasonal changes for ejection. The ejection rate of dead embryos was higher embryo mortality are not well described in fish. Under- in older embryos later in the season, and in larger standing seasonal variation in offspring mortality among mussels and at high embryo densities. The survival of oviposition sites allows an understanding of seasonal embryos in mussels was probably related to oxygen habitat choice and the consequences of seasonality for availability, with mortalities probably caused by individual fitness. Here I investigated the consequences of seasonality for offspring mortality in the bitterling, Rhodeus ocellatus kurumeus. Bitterling (family Cyprinidae, J. Kitamura subfamily Acheilognathinae) are freshwater fish that Department of Zoology, Faculty of Science, use only the interlamellar spaces of the paired inner Kyoto University, Kitashirakawa-Oiwakecho, and outer gills of living unionid freshwater mussels as Sakyo-ku, Kyoto 606-8502, Japan E-mail: [email protected] a reproductive substrate (Kanoh 1996, 2000; Aldridge Tel.: +81-75-7534077 1997, 1999; for review see Smith et al. 2004). Female Fax: +81-75-7534100 bitterling use a long ovipositor to place their eggs 42 onto the gills of a mussel through the mussel’s exhalant siphon. Male bitterling fertilize the eggs by Methods releasing sperm into the inhalant siphon of the mussel. Fertilized eggs reside in the mussel until development Study site is completed, finally emerging from the mussel as well- developed larvae. The time to complete development The field survey and experiment, and sampling of mus- sels were conducted from April–July in 1999 and 2001, inside host mussels (embryo development time) is 2 3–6 weeks. Parental bitterling do not care for their in two small artifical ponds (approximately 80 m ) cre- eggs and offspring; however, bitterling embryos in the ated more than 70 years ago in Higashiosaka and Yao gill cavity of a mussel are protected from predators City, Osaka, Japan. The bitterling population in the and typically have relatively high survival rates study ponds was identified as R. ocellatus kurumeus by (Nagata 1985). Kawamura et al. (2001) using mitochondrial gene-se- Because bitterling use a discrete spawning site that quence data. This subspecies is endemic to western Ja- can be readily manipulated, and because they display pan and listed as a critically endangered species in the remarkable morphological, physiological and behavio- Red Data Book of brackish and freshwater fishes of the ural adaptations by using mussels as spawning sites, Environment Agency of Japan (Kawamura 2003). The they represent a valuable model in behavioural, popu- study ponds were designated as sampling stations 18 and lation and evolutionary ecology (Smith et al. 2004). 23 by Kawamura et al. (2001). They are situated in the Previous studies of European bitterling (R. sericeus) foothills of Mount Ikoma-Shigi, an area listed as have provided evidence that the mortality of bitterling ‘‘invaluable wetlands to be conserved’’ by the Environ- embryos on mussel gills is positively density dependent ment Agency of Japan (Ministry of the Environment (Smith et al. 2000a, 2001). However, these studies 2002). Only this bitterling species and one freshwater estimated mortality rates over relatively short periods mussel species, Anodonta sp. B (sensu Kondo 2002), and did not consider the possibility of seasonal varia- were present in these ponds. tion in mortality rates. In addition, the results were calculated with an assumption that mortality rates of all embryo developmental stages were constant. How- Seasonal mortality of bitterling embryos in mussels ever, this assumption has never been explicitly tested, though it has important implications for estimates of The aim of this experiment was to explore the effects of density-dependent mortality of bitterling embryos and mussel characteristics (sex and size), embryo develop- the adaptive value of oviposition decisions. Density- ment time, embryo density, season and larvae size on the dependent mortality of bitterling embryos in mussels is mortality of bitterling during embryonic development in believed to arise through competition for oxygen in the their mussel host. A total of 441 and 180 mussels of mussel gill chamber (Smith et al. 2000a, b, 2001). Anodonta sp. B were collected in mid-March 1999 and Competition for oxygen may occur among bitterling 2001 respectively from the sampling pond before the embryos, between the host mussel and bitterling em- onset of the bitterling reproductive season. The mussels bryos, and between bitterling embryos and the devel- were transferred to a holding basket in the experimental oping mussel embryos, called glochidia, which are pond. The basket was half-filled with a substrate of sand brooded in the outer gill chambers of female mussels and covered with netting that prevented the bitterling (Smith et al. 2004). from obtaining access to the mussels, but allowed the Bitterling embryo mortality rates may also be related mussels to filter normally. The mean length of mussels to maternal yolk resources allocated to eggs. Yolk sup- was 67.7±5.5 (SD) mm in 1999 and 64.2±5.6 mm in ply may vary seasonally with parental changes in phys- 2001. iological condition, and is often related to diet, and/or For each replication, a group of five (until 22 April in social status, particularly if spawning periods are pro- 1999 and throughout 2001) or three (from 23 April in tracted (Kamler 1992). 1999) mussels of each sex was randomly selected from In this study I conducted a field survey and experi- the holding basket and each placed in a flowerpot (9 cm ment to estimate the seasonal change in mortality rates deep, 11 cm diameter) with a sand substrate. The flow- of bitterling embryos in mussel gill chambers. I also erpots were placed in the experimental pond, approxi- tested whether the mortality rates were affected by four mately 15–30 cm from the bank, spaced approximately variables: mussel sex and size, and bitterling embryo 10 cm apart around the pond margin and in a water development time and density in the host mussel. In depth of approximately 15–30 cm. The mussels were addition, I tested whether the effect of these four factors placed in the pond at sunset and exposed to bitterling varied among developmental stages of embryos and spawning until they were retrieved at 17:00 the follow- periods. Finally, I related embryo mortality rates to ing day. Bitterling do not spawn during the night three extrinsic variables (water temperature, dissolved- (J. Kitamura, unpublished data), so mussels were ex- oxygen levels and bitterling oviposition choice) and posed to spawning for a single day only. This procedure three intrinsic variables (condition of females and size of was conducted daily in 1999 and weekly in 2001 eggs and larvae). throughout the bitterling spawning season. 43 After exposure to bitterling spawning, the number of mussel size, embryo development time, and bitterling bitterling eggs deposited on gills of each mussel was embryo density in the host mussel. Because multiple counted by opening a 1-cm gap between the valves of the comparisons were made among variables, all significance mussel using a mussel opening device.
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