Timing matters: Sensitivity of Daphnia magna dormant eggs to fenoxycarb exposure depends on embryonic developmental stage

Abstract

Although Daphnia magna is a key species in many lentic freshwater ecosystems and is commonly used as model organism in ecology and ecotoxicology, very little is known about the effects of chemicals on their dormant life stages. Dormant eggs (ephippia) are produced when environmental conditions deteriorate, and Daphnia switch from clonal to sexual reproduction. Ephippia produced over different growing seasons can accumulate in the sediment of ponds and lakes, where they can be exposed to pesticides and other (anthropogenic) stressors. In the present study, we have investigated the effects of pesticide exposure on dormant eggs at different embryonic developmental stages and evaluated the degree of protection against pollution provided by the ephippial case. We therefore conducted a hatching experiment in which decapsulated and encapsulated dormant eggs were exposed to an insect growth regulator (fenoxycarb) at different stages during their development, both before and after activation of the eggs. In addition, we developed an analytical method to measure fenoxycarb concentrations in the dormant eggs. Fenoxycarb negatively affected development and hatching success and changed the timing of hatching in activated and in dormant eggs. Hatching characteristics as well as fenoxycarb concentrations inside the eggs differed significantly between exposure treatments. Final stages of embryonic development were most sensitive to pesticide exposure and had the highest tissue concentrations of fenoxycarb. Tissue concentrations did not differ significantly between decapsulated and encapsulated eggs, suggesting that the ephippial case offers limited or no direct protection against pesticide exposure. With this study we provide new evidence showing that pesticides can bioconcentrate in and affect D. magna dormant eggs. The severity of the effects on developing embryos depends on the timing of pesticide exposure. Our results stress the importance of considering the full life-cycle of model organisms used in ecotoxicological studies, since these are ultimately aimed at assessing risks of chemical exposure on natural aquatic ecosystems.

Diapause as escape strategy to exposure to toxicants: response of Brachionus calyciforus to arsenic

“…Previously, effects of pesticides and sedimentary metals have been observed on development and hatching success of the diapausing eggs of cladocerans Daphnia (Navis et al 2013(Navis et al , 2015Rogalski 2015). Additionally, a field study showed metals were accumulated by Daphnia ephippia (Wyn et al 2007).…”

“…These antecedents suggest that toxicants are incorporated to diapausing stages from the medium, and that even though diapausing stages facilitate the survival of aquatic organisms under extreme conditions due to suppressed metabolism, there is contradictory evidence about the resistance to toxic agents in zooplankton embryonic development when embryos are still inside protective membranes. While Alekseev et al (2010) showed great capability of diapausing eggs to resist severe pollution events in several zooplankton groups, Navis et al (2015) suggested that the cladoceran ephippium offers limited protection against pesticides dissolved in the medium. Moreover, pesticide bioconcentration in the eggs increases with exposure time during the embryonic development (Navis et al 2015).…”

“…While Alekseev et al (2010) showed great capability of diapausing eggs to resist severe pollution events in several zooplankton groups, Navis et al (2015) suggested that the cladoceran ephippium offers limited protection against pesticides dissolved in the medium. Moreover, pesticide bioconcentration in the eggs increases with exposure time during the embryonic development (Navis et al 2015). Although we could not assess the concentration of arsenic in the diapausing eggs, we observed a very high accumulation of toxicant in organisms exposed to constant arsenic concentration after several generations.…”

“…Nevertheless, because only the asexual portion of the life cycle is commonly investigated in toxicity studies, the true vulnerability of zooplankton to toxicants is often underestimated (Preston and Snell 2001;Navis et al 2015). Several studies assessed the effects of pesticides, heavy metals, and endocrine-disrupting chemicals on sexual reproductive parameters of rotifers (Snell and Carmona 1995;Preston et al 2000;Yoshinaga et al 2000;Preston and Snell 2001;Radix et al 2002;Marcial et al 2005;Ríos-Arana et al 2007) and cladocerans (Tatarazako and Oda 2007;Navis et al 2013Navis et al , 2015. Their results showed that, depending on the species and contaminants tested, reproductive parameters such as mixis ratio (i.e., proportion of sexual females relative to all females, sexual and asexual) and fertilization, and diapause parameters such as resting egg production and resting egg hatchability are among the most sensitive endpoints to assess toxicity in zooplankton species.…”

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

“…crowding or changes in photoperiod). Development of the resting stage arrests at the onset of gastrulation, at the ∼1000-cell stage (Baldass, 1941), with the embryo contained in a protective, inflexible tertiary egg membrane in addition to the two membranes found around directly developing parthenogenetic eggs (Navis et al, 2015). These ephippial embryos can then persist for periods of days to decades and be dispersed to new habitats, surviving drying, temperature extremes, anoxia and chemical exposure.…”