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

Abstract

Physiological plasticity of early developmental stages is a key way by which organisms can survive and adapt to environmental change. We investigated developmental plasticity of aspects of the cardio-respiratory physiology of encapsulated embryos of a marine gastropod, Littorina obtusata, surviving exposure to moderate hypoxia (P O2 =8 kPa) and compared the development of these survivors with that of individuals that died before hatching. Individuals surviving hypoxia exhibited a slower rate of development and altered ontogeny of cardio-respiratory structure and function compared with normoxic controls (P O2 >20 kPa). The onset and development of the larval and adult hearts were delayed in chronological time in hypoxia, but both organs appeared earlier in developmental time and cardiac activity rates were greater. The velum, a transient, 'larval' organ thought to play a role in gas exchange, was larger in hypoxia but developed more slowly (in chronological time), and velar cilia-driven, rotational activity was lower. Despite these effects of hypoxia, 38% of individuals survived to hatching. Compared with those embryos that died during development, these surviving embryos had advanced expression of adult structures, i.e. a significantly earlier occurrence and greater activity of their adult heart and larger shells. In contrast, embryos that died retained larval cardio-respiratory features (the velum and larval heart) for longer in chronological time. Surviving embryos came from eggs with significantly higher albumen provisioning than those that died, suggesting an energetic component for advanced development of adult traits.

Differences in the respiratory response to temperature and hypoxia across four life-stages of the intertidal porcelain crab Petrolisthes laevigatus

“…Although our limited data set does not allow for detailed inferences about the mechanistic basis of the observed response, it does show that physiological responses to low oxygen exposure co-vary with size and life-stage. Ontogeny-related processes such as the regulation of metabolic rates (Spicer and El-Gamal 1999 ), functional changes on subunits of oxygen transport proteins (Terwilliger and Brown 1993 ; Brown and Terwilliger 1999 ) and the development of the cardiovascular system (Harper and Reiber 2006 ; Rudin-Bitterli et al 2016 ) could contribute to the variation in mass exponent in relation to oxygen tension described here. In our study, the largest life-stage (i.e.…”

Both maternal and embryonic exposure to mild hypoxia influence embryonic development of the intertidal gastropod Littorina littorea (Linnaeus, 1758)

“…Whilst lower than the O 2 saturation used in the present study, Chan et al (2008) reported a reduction in velum area under moderate hypoxia (57.5% air saturation) in planktotrophic Reticunassa (as Nassarius) festivus, contrasting with our results. Rudin-Bitterli et al (2016) proposed that enhanced plasticity in encapsulated developers, relative to those with planktotrophic modes of development, could arise from greater fluctuations in P O2 in the intertidal environment (Morris and Taylor, 1983). Here, planktotrophic L. littorea embryos, the focus of the present study, are shown to respond to relatively small reductions in dissolved oxygen, despite the supposed less extreme fluctuations these embryos are likely to experience in the water column (Agnew and Taylor, 1986).…”

“…Comparisons of embryos that hatched and those that died There were pre-hatch mortalities in all treatments (N-H: 6; H-H: 10; H-N: 5; N-N: 4), and so the opportunity was taken to compare embryos that successfully hatched with those that died to identify traits linked with successful hatching (see also Rudin-Bitterli et al, 2016). By presenting data for comparisons of those that successfully hatched and those that died, inferences can also be made over the selective advantages of morphological traits under mild hypoxia.…”

“…This hypertrophic response in respiratory surface area probably reflects an increased effort to enhance rates of oxygen uptake, and can be observed across multiple taxa, with the majority focusing on fish and amphibians (Bond, 1960;McDonald and McMahon, 1977;Burggren and Mwalukoma, 1983;Sollid et al, 2003;Chapman, 2007;Chan et al, 2008). Few studies focus on embryonic stages of gastropod molluscs (Chan et al, 2008;Rudin-Bitterli et al, 2016), and of these two studies, only one focuses on a species with a planktotrophic mode of development (Nassarius festivus). Whilst lower than the O 2 saturation used in the present study, Chan et al (2008) reported a reduction in velum area under moderate hypoxia (57.5% air saturation) in planktotrophic Reticunassa (as Nassarius) festivus, contrasting with our results.…”

“…Characterising the effects of environmental hypoxia on the early development of planktotrophic species will be of importance in predicting how these populations respond to environmental change, as these early life stages are likely to experience markedly different conditions from their mostly benthic adult life stages (Bertram and Strathmann, 1998;Díaz, 2001;Díaz and Rosenberg, 2008). Recent studies have shown that developmental exposure to reduced oxygen tensions can result in significant alterations to the timings of appearance of embryonic traits, and the size of morphological characters in developing embryos of intertidal marine gastropods (Chan et al, 2008;Rudin-Bitterli et al, 2016), and that these effects persist into later life history stages (Pechenik, 2006;Li and Chiu, 2013;Segura et al, 2014). However, the relative influences of both maternal and developmental exposure to sublethal, mild environmental hypoxia on early development of intertidal marine gastropods is not currently known.…”