Limiting factors to encapsulation: the combined effects of dissolved protein and oxygen availability on embryonic growth and survival of species with contrasting feeding strategies

Abstract

SUMMARYEncapsulation is a common strategy among marine invertebrate species. It has been shown that oxygen and food availability independently constrain embryo development during intracapsular development. However, it is unclear how embryos of species with different feeding strategies perceive these two constraints when operating jointly. In the present study, we examined the relative importance of dissolved albumen, as a food source, oxygen condition and their interaction on embryonic growth and the survival of two calyptraeid species, Crepidula coquimbensis and Crepidula fornicata, exhibiting different embryo feeding behaviours (i.e. presence vs absence of intracapsular cannibalism). Two oxygen condition treatments (normoxia and hypoxia) and three albumen concentrations (0, 1 and 2 mg l -1 ) were studied. In addition, albumen intake by embryos was observed using fluorescence microscopy. Our study shows that embryos of both species incorporated dissolved albumen but used a different set of embryonic organs. We observed that embryo growth rates in C. coquimbensis were negatively affected only by hypoxic conditions. Conversely, a combination of low albumen concentration and oxygen availability slowed embryo growth in C. fornicata. These findings suggest that oxygen availability is a limiting factor for the normal embryo development of encapsulated gastropod species, regardless of feeding behaviour or developmental mode. By contrast, the effect of dissolved albumen as an alternative food source on embryo performance may depend on the feeding strategy of the embryos.

Development of cardiovascular function in the marine gastropodLittorina obtusata(Linnaeus)

“…One of the main challenges for encapsulated embryos, such as L. obtusata, is probably O 2 supply, as embryos are often crowded within egg masses and the jelly matrix around the eggs limits O 2 diffusion (Brante et al, 2009). Furthermore, intertidal habitats are subject to large P O2 fluctuations (Truchot and Duhamel-Jouve, 1980;Agnew and Taylor, 1986) and embryos in egg masses have no possibility of avoiding hypoxic areas once the egg mass has been deposited in one location and can therefore be exposed to hypoxic conditions for longer periods.…”

“…Whilst many gastropod egg capsules are considered to be freely permeable to water (e.g. Galtsoff et al, 1937;Carriker, 1955;Pechenik, 1983), the jelly matrix enclosing the embryos has been found to constrain oxygen diffusion into the egg mass (Brante et al, 2009). Furthermore, embryos are often crowded within egg masses and are frequently exposed to large fluctuations in O 2 partial pressure (P O2 ) in the intertidal zone (Raffaelli and Hawkins, 1996).…”

Nurse egg consumption and intracapsular development in the common whelk Buccinum undatum (Linnaeus 1758)

“…Similarly, no cannibalism during development was reported in the buccinids B. cyaneum (Miloslavich and Dufresne 1994) and B. isaotakki (Ilano et al 2004), and only very rarely was it observed in the buccinid L. dirum (Rivest 1983). It has, however, been reported in some other gastropods including Crucibulum quiriquinae (Véliz et al 2001), Crepidula coquimbensis (Véliz et al 2003;Brante et al 2009) Trophon geversianus (Cumplido et al 2011) and a vermetid gastropod (Strathmann and Strathmann 2006).…”

Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia

“…However, there is also evidence of negative effects even at P O2 values similar to those we used (8 kPa), which may not be classified by ecologists as being environmental hypoxia (Vaquer-Sunyer and Duarte, 2008). While the survival of the encapsulated slipper limpet, C. coquimbensis, was not significantly affected by exposure to P O2 of ∼11.5 kPa (Brante et al, 2008), Brante et al (2009) later found that aerobic metabolism of embryos of this species and the related C. fornicata decreased significantly at P O2 <12 kPa. Similarly, development, hatching and shell secretion of the encapsulated muricid snail Chorus giganteus were all compromised by culture in seawater of P O2 ∼10 kPa (Cancino et al, 2003(Cancino et al, , 2011 and embryonic development of N. festivus was significantly delayed when cultured at a P O2 of ∼7.6 kPa (Chan et al, 2008).…”

“…The development rate of marine embryos and larvae has been linked to the maternal provisioning they receive. Brante et al (2009), for example, showed that supplying additional albumen to embryos of the slipper limpet, C. fornicata, enhanced growth rate. Although we did not measure albumen levels in the eggs of L. obtusata throughout their development, we did quantify albumen levels (measured as the diameter of albumen within the egg capsule) from images at the start of development.…”