Maternal Transfer

Aquatic organisms like the apple snail Pomacea maculata can take up contaminants. Like heavy metals from their surrounding environment (water, sediment, periphyton). However, individuals may already start out (at birth) with a metal body burden due to maternal transfer. As has been demonstrated for some passerine birds, harmful trace elements such as lead (Pb). Copper (Cu) and cadmium (Cd) can be maternally transferred to eggs in a tissue concentration-dependent manner (i.e., concentrations in eggs would be correlated with concentrations in females) (Dauwe et al., 2006; Lagisz & Laskowski, 2008).

Other factors may also govern amounts of metal transferred from adult females to offspring. A study by Tsui and Wang (2004) that examined uptake. And elimination routes of mercury (Hg) in the freshwater cladoceran Daphnia magna found. That methylmercury (MeHg) content in neonates was dependent on the age of the females. As well as on the MeHg body burden in females. The maternal metal transfer can be used in biomonitoring, as demonstrated by Yu et al. (2011) which showed that egg Cu concentrations were useful. As an indicator of female Cu exposure in the red-eared slider turtle (Trachemys scripta elegans).

Maternal transfer of metals is an important mechanism by. Which females can transfer potentially hazardous metals to their offspring (Sellin & Kolok, 2006). Maternal transfer may represent the most important route of exposure for P. maculata eggs which are laid aerially (Hopkins et al., 2006). And therefore not exposed to contaminants in water and sediment. In addition to having a negative impact on the offspring. This transfer could benefit the adults since they may use it.

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As a strategy for eliminating contaminants from their body - as seen for inorganic mercury and methylmercury in D. magna (Tsui & Wang, 2004). This phenomenon is termed maternal offloading whereby females transfer a portion of their accumulated contaminants to their offspring during reproduction (Lyons & Lowe, 2013). While this has been observed in fish and crustaceans, metal transfer is likely to differ among animal groups – thus the same phenomenon may not occur in the apple snail P. maculata.

The mode of reproduction dictates transfer of nutrients to offspring, as seen in some elasmobranch fishes (Hamlett et al., 2005). Such a dependence on mode of reproduction can similarly be expected for maternal transfer of metals. Fertilization in P. maculata occurs internally, followed by oviparous development (Barnes et al., 2008). Pomacea canaliculata, a close relative of P. maculata. Is an iteroparous species laying multiple clutches of eggs during its reproductive season (Bachmann, 1960).

The Pomacea species (P. maculata) that is the focus of my research, has similar reproductive strategies and exhibits a 4:9 male: female sex ratio. Female snails lay a large number of eggs. The number of eggs per clutch ranges from a few hundred to as many as ~4500 and averages ~1500 (Barnes et al., 2008; Burks et al., 2010; Sutton et al., 2017). The phenomenon of multiple spawning is characteristic of an opportunistic reproductive strategy (Chiarello-Sosa et al., 2016).

Oviposition strategies may affect maternal transfer of contaminants. Investment of resources in gonadal development is substantially higher in semelparous species. Than in iteroparous ones in any given year and the former may therefore transfer more metals to their offspring (Calow, 1979; Drevnick et al., 2006). All members of the Ampullariidae family live in freshwater. And their diverse oviposition strategies include laying egg masses either underwater. At the water surface, or above the waterline.

Pomacea species occupy benthic and pelagic habitats and their adults lay calcareous. And conspicuously-colored egg masses on hard substrates or vegetation above the waterline (Gamarra-Luques et al., 2013; Smith et al., 2015). Exposure to air is critical for the eggs to mature and develop fully (Burks et al., 2010).

Considered a critical innovation that has contributed to the diversification of Pomacea to become the most species-rich genus of the family (Hayes et al., 2009; Heras et al., 2007), that strategy prevents the eggs from attack by aquatic predators. Aerial predators are far fewer in number. The fire ant Solenopsis geminata is the only reported predator of Pomacea eggs (Dreon et al., 2013). In addition to exposure to non-aquatic predators, the aerial oviposition strategy exposes the eggs to other environmental stressors such as sunlight and desiccation.

A number of adaptations have occurred to overcome the adverse conditions associated with the aerial environment in which embryogenesis occurs. One such adaptation involves the perivitelline fluid (PVF). This PVF is produced by the female albumen gland, and P. maculata eggs are encased in this fluid upon oviposition (Barnes et al., 2008)

In contrast to the situation for the vitellins of other invertebrates, PVF proteins (or perivitellins) are fully functional once synthesized in the albumen gland (Cadierno et al., 2017). Vitellogenins, the precursor form of vitellins, are synthesized in the digestive gland of P. canaliculata, released into circulation and taken up by the ovary and incorporated into the developing oocyte by a heterosynthetic (outside the ovary) mechanism (Chen et al., 1999; Dreon et al., 2002).

Developing embryos rely mostly on PVF for acquiring photoprotective, antioxidant and antitrypsin properties (Heras et al., 2007). The PVF also provides embryos with nutrients and predator defenses during development (Cadierno et al., 2018). Perivitellins may also serve roles in metal detoxification pathways. It is possible that the physicochemical properties of the PVF affect the form in which metals are present and transform them into an inert form similar to the situation of biotransformation of polybrominated diphenyl ethers (PBDEs) in the adult common sole (Solea solea) (Munschy et al., 2017).

In contrast, the PVF surrounding the embryos may also act as an efficient shield against direct metal exposure. This function was observed in the case of Sepia officinalis where most of the metals taken up by the eggs remained associated with the capsule membrane of the eggs (Bustamante et al., 2004).

In typical egg-laying species, contaminant transfer from parents to offspring could potentially come from both the male and the female (i.e. from sperm and egg). The larger size of ovum relative to the sperm indicates that maternal contribution is likely to exceed the paternal contribution to the developing embryo. Moreover, the female contributes vitellogenins to the ovum, and these vitellogenins may interact with contaminants. J. Gao (2016) showed that nanoparticles (NPs) bind to vitellogenin in plasma of smallmouth bass (Micropterus dolomieu).

This binding facilitated NP transport to developing follicles within the ovaries, which in turn might result in maternal transport to embryos. A case study on the zebrafish Danio rerio with polystyrene nanoparticles (PSNPs) showed the presence of PSNPs 24 hours post fertilization in the yolk sac of maternally-exposed embryos but not paternally-exposed ones (Pitt et al., 2018). This demonstrates both to the potential for trans-generational contaminant transfer, and the likelihood that the maternal contribution will dominate this contaminant transfer.

Males might transfer contaminants to females at mating, as is the case for the moth Gluphisia septentrionis where ‘puddler’ males provide their mate with a nuptial gift of sodium (Adler & Pearson, 1982; Smedley & Eisner, 1996), which can then be transferred to the offspring. The potential for paternal transfer was also demonstrated in a study which looked at sex-specific effects of Cd exposure on reproductive success of fathead minnows (Pimephales promelas); this study found that paternal exposures to Cd led to greater offspring mortality than was the case for maternal exposures (Sellin & Kolok, 2006).

This chapter will investigate the phenomenon of parental transfer of heavy metals like Cu from adult P. maculata snails to their egg masses. An initial set of experiments (described later in materials and methods) will assess the occurrence of paternal metal transfer. If there is an evidence of this phenomenon, subsequent experiments will look into the relative Cu contributions by the father and the mother to their offspring.

To achieve this, mating pairs of snails will be exposed to elevated Cu concentrations under greenhouse conditions and allowed to lay multiple egg masses to quantify the occurrence and effects of the metal transfer. If the earlier experiment shows no evidence of paternal transfer, subsequent experiments will be done with Cu-exposed females. Levels of Cu will be quantified in the gonads and all egg masses laid.

Maternal transfer of metals may differ between batches within the same generation. A dilution effect may be involved, whereby the first batch of eggs following exposure contains the highest metal burden and decreases across consecutive batches. This phenomenon was seen in a Daphnia magna transgenerational study involving selenium (Se) where the maternal transfer of Se in the second and third batches was higher than that of fourth to tenth batches (Lam & Wang, 2006).

This may be a matter of lower metal levels in the female, with the increase in time after exposure. However, the phenomenon of maternal offloading also predicts that the female transfers the maximum burden to the first laid egg mass. Whether a dilution effect is involved will be investigated by comparing Cu levels among batches of P. maculata eggs and relating these to metal levels in the female snails.

Metal exposure in egg-laying females could interfere with calcium (Ca) levels in females and reduce Ca transfer to their egg during oogenesis, as seen in two species of passerine birds (Espin et al., 2016). Exposure to heavy metals is often accompanied by significant decreases in Ca.

Mechanistically, metals may be interfering with Ca transport or storage processes (e.g. by affecting Ca2+ transport proteins) or a metal ion may substitute for Ca at functionally important Ca-binding sites such as calmodulin (Pounds, 1984). To investigate if Cu exposure is affecting Ca levels in the eggs, we will quantify levels of Ca in egg masses and calculate a Cu/Ca ratio. We will do this for all egg masses produced and compare these ratios, as well as Ca levels, among sequential egg masses.

Since transfer of metals to the next generation could have a negative fitness consequence in the offspring, it is important to determine how much of the metal that is transferred to eggs ends up in the offspring. In the case of the apple snail eggs, this means also investigating whether the metals are discarded with the perivitelline fluid (PVF) when juveniles hatch out. If the metals are discarded with the PVF, they are not directly incorporated in the embryo and do not pass down to the next generation. To look into this, we will quantify levels of Cu in the PVF and in the individual eggs after dissolution of the PVF.

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