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Eco-physiological study on reproduction of the range-extengded sea urchin Heliocidaris crassispina

Feng Wengping 東北大学

2020.03.25

概要

Background
The recent report of IPCC (Intergovernmental Panel on Climate Change) indicated that human activity will cause ocean warming to 1.5°C by 2030–2052 (IPCC, 2019). Despite the ocean have absorbed > 80% of the heat affecting the global climate system, increase in ocean temperature was three times slower than that in air temperatures over land (Sunday et al., 2012). And the marine organisms were more sensitive to increase in temperature than those of terrestrial species (Pörtner and Knust, 2007; Pörtner et al., 2014). Marine organisms respond to ocean warming in several ways. First, they can move (poleward extend) to new areas that become available within their thermal niche (Parmesan and Yohe, 2003; Ling et al., 2008; Poloczanska et al., 2013). Range extension may arise as a result of changes in the ecosystem structure and function of the newly extended habitat (Davis et al., 1998; Walther et al., 2002; Edwards and Richardson, 2004; Doney et al., 2012, Dawson et al., 2011) and give rise to potential threats to fisheries (Johnson et al., 2005). Second, they can adapt to climate change either via phenotypic plasticity or evolutionary changes. Phenotypic plasticity is often considered as the first response to environmental change (Munday et al., 2013; Gienapp et al., 2008), including morphological, physiological and behavioral plasticities. Evolutionary changes of marine organisms are extension of their in situ thermal niche throughout multiple generations caused by changing environment (Visser, 2008; Williams et al., 2008). Third, marine organisms can experience range contractions where a modified climate exceeds their thermal niche, followed by death.

Sea urchin is ectothermic marine animal, of which distribution and reproduction (Agatsuma et al., 2007; Ling et al., 2008; Pecorino et al., 2013), physiology (Wolfe et al., 2013; Zhao et al., 2018) and behavior (Brothers and Mcclintock, 2015) changed along with the ocean warming. Agatsuma et al. (2007) reported that the range of Hemicentrotus pulcherrimus was extended from the southern to northern coast of Hokkaido in the Sea of Japan after massive recruitment in 1989, 1990 and 1991 under high water temperatures during the larval period. The populations in the new habitats showed a fast growth rate and a defined gametogenic cycle with high gonad production in 1992 and 1993 (Agatsuma and Nakata, 2004). The range of Centrostephanus rodgersii was extended to Tasmania (Johnson et al., 2005) in the last 50–60 years and subsequently to New Zealand (Pecorino et al., 2013), due to the transport of surviving larvae (Andrew et al., 2001; Johnson et al., 2005) driven by the poleward advance of the East Australian Current (Ridgway et al., 2007). In its new habitats, C. rodgersii displays a strong seasonal cycle of gonad production and produces viable gametes (Ling et al., 2008). The gametes of the female and male can be produced synchronously (Pecorino et al., 2013). However, little is known about how range-extended species adjust to their new abiotic and biotic environments physiologically and ecologically by sex.

Heliocidaris crassispina has been intensively studied as Anthocidaris crassispina, which is found in intertidal and subtidal zones in the Pacific coastal regions around Ibaraki, in the southern Sea of Japan around Akita, and southeastern China (Shigei, 1995). It is a common herbivore in the middle part of the Sea of Japan (Hayashi et al., 2000). High densities (0.8–21.6 ind./m2) of H. crassispina were found at a depth of 7 m in Wakasa Bay in Kyoto, Japan, where is the central distribution of H. crassispina in Japan (Tsuji et al., 1994). Mesocentrotus nudus is distributed in the Pacific Ocean in Rausu, from Sagami Bay to Erimo Cape, Hokkaido, and in the Sea of Japan from Omi Island, Yamaguchi, to Soya Cape, northern Hokkaido in Japan (Kawamura, 1993; Shigei, 1995).

Before 2014, H. crassispina was rarely distributed in southwestern Oga Peninsula in Japan (Nakabayashi, pers. commun.). The range extension in Toga Bay, Oga Peninsula, Akita Prefecture in northeastern Honshu, Japan was first observed in 2014 (Nakabayashi, 2016). Thereafter, H. crassispina distributed all around Akita and also in Aomori Prefectures in the Sea of Japan and along the Tsugaru Strait in 2015 (Nakabayashi et al., 2016; Kirihara and Fujikawa, 2018). On the other hand, M. nudus, which was predominant until a couple of years ago, disappeared in shallow waters in Toga Bay along the Oga Peninsula (Mizuno and Eguchi, 2015; Ito, 2014), possibly due to their movement to the deeper waters or death at high water temperatures in summer (Tsuji et al., 1994) before 2014.

Research history
Marine organisms primarily respond to ocean warming by shifting their reproductive phenology and showing a prolonged period of reproduction (Parmesan and Yohe, 2003; Edwards and Richardson, 2004; Poloczanska et al., 2016). Such warming-induced shifts in reproduction might impact the population dynamics and demography of organisms (Edwards and Richardson, 2004; Poloczanska et al., 2016). The reproductive biology of H. crassispina has been studied since the 1960s (Kobayashi, 1969; Mori et al., 1980; Yoo et al., 1982; Sakairi et al., 1989; Yamasaki and Kiyomoto, 1993; Horii, 1997; Yatsuya and Nakahara, 2004; Urriago et al., 2016). The spawning of H. crassispina occurs synchronously between the sexes from August to September in Wakasa Bay (Yatsuya and Nakahara, 2004) and from July to August on Hirado Island, Nagasaki Prefecture, Japan (Yamasaki and Kiyomoto, 1993). In Japan, H. crassispina is harvested around Kyoto in the Sea of Japan and around Wakasa Bay in the Pacific Ocean, which is the center of its distribution (Tsuji et al., 1989). The evaluation of the reproductive strategies (Poorbagher et al., 2010, Kapsenberg et al., 2017) and population structure of range-extended sea urchins (Ling et al., 2009) would enable us to explain their adaptation to new environments at the margin of their range. In addition, comparison with sea urchins of the same species in the central range would contribute to a better understanding. However, no information on the reproduction and population structure of H. crassispina in newly extended habitat has been reported.

Sea urchins are ectothermic animals whose physiology (Wolfe et al., 2013; Zhao et al., 2018) and behavior (Brothers and Mcclintock, 2015) are negatively impacted by ocean warming. Physiological thermal tolerance limits of marine organisms play an important role in reflecting the distribution range shifts (Pörtner, 2001; Pörtner and Knust, 2007) and the organism’s adaptation in response to the warming environment (Peck, 2005; Barnes and Peck, 2008). Many studies reveal that metabolic processes of sea urchins are governed by water temperature (McBride et al., 1997; Spirlet et al., 1998; Brockington and Clarke, 2001; Hochachka and Somero, 2002; Shipigel et al., 2004). Understanding the temperature impacts on H. crassispina and M. nudus physiologically and behaviorally are fundamental to figure out the reason of replacement of M. nudus by H. crassispina in Oga Peninsula and to assess their potential distribution (Ricciardi et al., 2000; Somero, 2005; Kearney and Porter, 2009).

Compounds rich in carbon (C) were primarily used to meet the demands of metabolism in invertebrates (Elendt, 1989), and nitrogen (N) also plays an important role in metabolism (Mayor et al., 2011; Zhu et al., 2016), growth and reproduction of invertebrate (Roman, 1983; Elendt, 1989). Most researches on the seasonal changes in protein (nitrogen) and carbohydrates (carbon) of gonad and gut in sea urchin from the point of view of nutrient level, which were correlated with reproduction and food availability (Moss and Lawrence et al., 1972; Fernandez, 1998; Montero-Torreiro and Garcia-Martinez, 2003; Rocha et al., 2019). However, little research treated the changes in C and N contents of gonad and gut as an indicator, to reflect the metabolism or adaptation of sea urchin under changing environment (e.g. temperature). Additionally, Giese et al. (1959) suggested that the seasonal variability of constituents of the gonad is a key factor in asynchronous spawning between the sexes in sea urchin.

Food consumption (feeding rate) as a phenotypic trait indicates the physiological and health conditions of marine organisms (Huntingford et al., 2010). It increased along with temperature increase (McBride et al., 1997; Douke and Hamanaka, 2001; Siikavuopio et al., 2006). A number of studies have shown that feeding regulation allow marine organisms to express an advantageous adaptation for performing successfully under changing environment (e.g. ocean warming or acidification) (Saba et al., 2012; Burnell et al., 2013; Nagelkerken and Munday, 2016), and that to have a greater ecological niche width (Sobero´n and Peterson, 2005; Helaouet and Beaugrand, 2009). If the feeding of sea urchin is less sensitive to temperature, showing a large optimal temperature range, it would reflect the greater niche width and adaptability. Machiguchi et al. (1994) reported that food consumption of M. nudus decreased in winter at water temperatures of < 5°C. However, little is known on feeding of H. crassispina associated with changing temperature. In addition, comparison of the optimal temperature ranges of feeding rate between H. crassispina and M. nudus is essential to provide a clue on the replacement of the M. nudus by H. crassispina.

Righting response and Aristotle's lantern reflex reflect the phenotypic adjustments in behavior of sea urchin under the changing environment. Righting response coordinate sea urchins by the neuromuscular system, affecting the ability of the organism to survive from predators and strong surge (Kleitman, 1941; Percy, 1973). The Aristotle's lantern reflex is the ability of sea urchin to hold and to grind food (De Ridder and Lawrence, 1982). The elevated temperature suppresses the righting responses (Farmanfarmaian and Giese, 1963; Brothers and McClintock, 2015; Sherman, 2015) and lantern reflexes (Brothers and McClintock, 2015) of sea urchin. However, little study on the negative impact of low temperature on sea urchin behavior have been undertaken except for Farmanfarmaian and Giese (1963).

Recruitment of marine invertebrates is impacted by temperature (Pechenik, 1987; Hart and Scheibling, 1988; O’Connor et al., 2007). The hypothesis that thermal tolerance of planktonic propagules limits the geographical distribution of marine invertebrates is supported by the correlation between spawning temperature and successfully larval development (Andronikov, 1975; Fujisawa, 1990; Reitzel et al., 2005). Fujisawa and Shigei (1990) reported that the major spawning of H. crassispina occurred in summer at high water temperature of 17–29°C, and the increased temperature could increase the growth and development rate of embryos within the suitable temperature range (Fujisawa and Shigei,1990; Plamer, 1994; Ling et al., 2008; Pecorino et al., 2013). Understanding the temperature limits of H. crassispina from fertilization to larval development and juvenile are essential to figure out the adaptation and recruitment of H. crassispina in newly extended habitat.

Purpose
My study aims to figure out (1) the driver of the range extension, (2) temperature causing replacement of M. nudus by H. crassispina and (3) reproductive adaptation of the new extender. It is the first time to study on a new sea urchin population extended last decade.

In chapter II, the gonad development and population structure of H. crassispina between northern extended and central ranges were compared. In chapter III, the reproductive cycle and nutrient accumulation of H. crassispina in newly extended habitat were analyzed by annual changes in gonad development and C/N ratio of gonad, gut and gut content to confirm the delayed spermatogenesis and figure out the specific cause. In chapter IV, I explored the effect of temperature on early life stage of H. crassispina: the feeding and behavior of juvenile (Section 1), fertilization to larvae and their temperature limits (Section 2). In chapter V, I concluded the reproductive adaptation of H. crassispina in newly-extended habitat, and the range extension of H. crassispina in future.

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