Latent effects of hypoxia on the gastropod Crepidula onyx

Abstract

Despite the importance of latent effects in marine invertebrates, no study has considered how larval exposure to hypoxia may have lasting impacts on the individual in later life history stages. In this study, we exposed larvae of the gastropod Crepidula onyx to 2, 3, and 6 mg O 2 l −1 , measured the larval size and total lipid content, transplanted the newly settled individuals to the field, and finally, determined the growth rate, dry weight, and filtration rate of the juveniles after 2 wk in the field. The experiments were conducted separately at low and high larval food concentrations. Under the low food concentration, both hypoxic treatments increased the time needed for the larvae to be competent to metamorphose. When they did, however, they had a size and total lipid content similar to the control larvae. The latent effects of early hypoxia exposure on juvenile growth were evident. The juvenile growth rate was reduced by ca. 14 and 10% in the 2 and 3 mg O 2 l −1 treatments, respectively. The mean dry weight and filtration rate were also significantly reduced in the hypoxic treatments. However, there was no discernible effect on larvae or juveniles when the food concentration during the larval stage was doubled, suggesting that the latent effects of hypoxia can be offset by larval access to high algal concentration. This study suggests that periodic hypoxic events and the resulting exposure of organisms to hypoxia during their early development may have effects that persist across the life history.

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework

“…Stressor events with decreased latency (less lag time) may be more likely to exhibit synergisms or antagonisms. For example, short latencies (2 weeks) in stressors (hypoxia and limited resource availability) applied to gastropod larvae have shown latent effects (Li & Chiu, ). Greater temporal delays between stressors may thus be more likely to result in additive (and therefore predictable) responses, as we found with Olympia oysters.…”

Latent Effects: Surprising Consequences of Embryonic and Larval Experience on Life after Metamorphosis

“…Along these same lines, the study by Li and Chiu (2013) that was referred to earlier showed that exposing the larvae of Crepidula onyx to hypoxic stress reduced post-metamorphic growth and filtration rates, but only when the stressed larvae had also been reared at a reduced food concentration; larvae exposed to hypoxic stress under high food conditions showed normal post-metamorphic growth, suggesting that having abundant nutrients prior to metamorphosis ameliorated the latent impact of hypoxic stress. Perhaps abundant embryonic nutrient stores also account for the remarkable lack of latent effects seen when brooded embryos of the polychaete Capitella teleta were exposed to severe hypoxia for up to 96 hours .…”

“…As hypoxic conditions become increasingly widespread in coastal marine environments around the world, due to climate change and the increasing output of organic wastes and agricultural nutrients (Wu, 2002;Zhang et al, 2013), interest in the potential consequences of spreading hypoxic stress continues to grow. For the calyptraeid gastropod Crepidula onyx, exposing well-fed (2 × 10 5 cells ml -1 ) larvae to oxygen levels as low as 2 mg O 2 l -1 for eight to ten days had no significant impact on the growth rates of field-transplanted juveniles (Li and Chiu, 2013). However, when larvae of this species were exposed to the same level of low-oxygen stress but at reduced food levels (1 × 10 5 cells ml -1 ), subsequent juvenile growth rates and filtration rates were significantly reduced compared with those exhibited by control individuals, even though there were no significant differences in the size or lipid content of juveniles from the different treatment groups at metamorphosis (Li and Chiu, 2013).…”

“…For the calyptraeid gastropod Crepidula onyx, exposing well-fed (2 × 10 5 cells ml -1 ) larvae to oxygen levels as low as 2 mg O 2 l -1 for eight to ten days had no significant impact on the growth rates of field-transplanted juveniles (Li and Chiu, 2013). However, when larvae of this species were exposed to the same level of low-oxygen stress but at reduced food levels (1 × 10 5 cells ml -1 ), subsequent juvenile growth rates and filtration rates were significantly reduced compared with those exhibited by control individuals, even though there were no significant differences in the size or lipid content of juveniles from the different treatment groups at metamorphosis (Li and Chiu, 2013). Thus latent effects were observed following the exposure of larvae to the combined stresses of low food and reduced oxygen, but were not observed if the larvae had been well-fed when exposed to the same levels of hypoxic stress.…”

“…Such species may be especially useful models for studying the underlying basis for latent effects. The larvae and juveniles of Crepidula fornicata, for example, can be routinely reared in the laboratory with 0 to 7% mortality (Pechenik and Lima, 1984;Pechenik and Tyrell, 2015;Bashevkin and Pechenik, 2015); the larvae are large at hatching (typically 400-450 µm in shell length) and grow quickly; can be easily induced to metamorphose when competent (Pechenik and Gee, 1993); and grow rapidly following metamorphosis (up to about 200 µm per day for the first week or so after metamorphosis) with high survival (Pechenik, 1984;Pechenik et al, 1996a;Bashevkin and Pechenik, 2007;Hettinger et al, 2012;Li and Chiu, 2013;Rahma n et al, 2014). For example, in a study referred to earlier (Emlet and Sadro, 2006) in which rearing nauplius larvae of the barnacle Balanus glandula at a low food concentration led to reduced post-metamorphic survival and growth, those reductions were correlated with reduced lipid and protein content of the pre-metamorphosed cyprids (Emlet and Sadro, 2006), supporting a simple energetics-limitation hypothesis for the observed reduction in juvenile growth rates.…”