The role of temperature and maternal ration in embryo survival: using the dumpling squid Euprymna tasmanica as a model

Abstract

Using a ‘model’ sepiolid, Euprymna tasmanica, this study investigated the role of maternal nutritional and thermal history on egg quality and subsequent embryo survival. E. tasmanica is a multiple spawner, therefore it was possible to track egg quality and hatching success over successive spawning episodes. A two-factor orthogonal experimental design, involving two feeding levels (high and low rations) and two temperatures (summer and winter), was implemented with half of the replicates used to explore embryonic development and the remaining half examining egg-yolk quality via fatty acid analysis. Differences in reproductive output and embryo mortality were largely attributed to maternal ration and not temperature. Females maintained on low ration produced smaller clutches, consisting of smaller eggs and exhibiting higher embryo mortality rates than high ration females. Both batch fecundity and relative hatching success declined over successive clutches. Lipid content was also significantly lower in low ration females, however, the relative quality in terms of lipid and fatty acid constituents was maintained regardless of treatment and spawning frequency. It is suggested that elevated embryo mortality rate in eggs spawned by low-fed females was a function of insufficient maternally derived yolk resources to fuel embryogenesis. Results indicate that maternal nutritional and reproductive history are important determinates for offspring survival, potentially having significant effects on the magnitude of subsequent recruitment events in squid populations.

Introduction

Definitive links between size, age and condition of mature females and embryo/larval survival have been identified in a diverse range of marine taxa Bayne et al., 1975, Laine and Rajasilta, 1999, Keckeis et al., 2000, Jimmy et al., 2002, McCormick, 1999, McCormick, 2003. Recent studies have suggested that maternal nutritional history has a large influence on embryonic development and offspring competency through the sequestering and provisioning of yolk resources Laine and Rajasilta, 1999, McCormick, 2003. Maternal temperature effects, through interactions with food availability, are also considered important determinates of offspring size (McKee and Ebert, 1996) and potentially larval competency. As a result, fluctuations in environmental conditions, particularly food availability, experienced during the females' reproductive season, can have significant flow on effects to the subsequent population structure (Kerrigan, 1997).

Non-overlapping, sub-annual cephalopod populations exhibit considerable spatial and temporal variation in recruitment (Pierce and Boyle, 2003). This variation is expected to be strongly affected by environmental conditions, particularly affecting the early life stages Boyle and Boletzky, 1996, Pierce and Boyle, 2003. Currently little is known about processes of early mortality, however, quantitative data exist for the southern calamary Sepioteuthis australis indicating that natural embryo mortality rates vary considerably over the spawning season (Steer et al., 2002, Steer, 2004. S. australis spawns multiple clutches over a relatively short spawning period and also exhibits substantial variation in the size and number of ovulated eggs Jackson and Pecl, 2003, Pecl, 2001). Research investigating egg-yolk lipids in the cuttlefish Sepia officinalis revealed that lipid quantity varies with egg size, suggesting that differences in egg quality may exist (Boucaud and Galois, 1990). Significant differences in egg quality, in terms of lipid content, were also found in squid eggs collected from different sites (Boyle et al., 2001). The lipid requirements for correct cephalopod development are not understood, however, phospholipids and long-chained polyunsaturated fatty acids, particularly EPA (20:5ω3) and DHA (22:6ω3), are likely to be essential constituents Boucaud and Galois, 1990, Navarro and Villanueva, 2000, Navarro and Villanueva, 2003, Boyle et al., 2001. Therefore, it would be beneficial to investigate whether spatial and temporal fluctuations in embryo mortality are linked to egg quality spawned by females from different nutritional and thermal environments.

Attributing S. australis embryo mortality to maternal nutritional and thermal history in the field is logistically challenging. This is largely due to the difficulties associated with linking females with spawned eggs and ascertaining the females’ history. Furthermore, the relative condition of the female may be confounded by her reproductive status. Serial spawning females exhibit no clear physiological record of previous spawning events Sauer et al., 1999, Moltschaniwskyj and Semmens, 2000 and therefore it is virtually impossible to determine whether spawned eggs are from the first or last spawning episode. In the serial spawning Atlantic cod, Gadus morhua, egg size and quality varies throughout successive spawning events Chambers and Waiwood, 1996, Ouellet et al., 2001. This variation is attributed to changes in female condition over the spawning season with past reproductive investments influencing future investments (Kjesbu et al., 1996). Therefore, when determining the flow on effects of maternal condition, through to egg quality and subsequent embryo survival in multiple spawners, the females' reproductive history must be considered.

Due to the logistical difficulties associated with maintaining large, highly mobile, cephalopods in captivity (Hanlon, 1990) and assessing links between maternal condition and hatching success in field populations, it is necessary to use a ‘model’ species conducive to manipulative experimentation. The southern dumpling squid Euprymna tasmanica (Sepiolidae) was chosen in this study, as it is a small multiple spawning cephalopod that is easily collected and reared in captivity. Using this species, this study aimed to describe the relationship between the nutritional and thermal environment in which females are exposed and the quantity and quality of the eggs and embryos produced over successive clutches.