Juvenile growth in barnacles: combined effect of delayed metamorphosis and sub-lethal exposure of cyprids to low-salinity stress

Abstract

Delayed metamorphosis can affect post-metamorphic performance in a variety of marine invertebrate species, possibly through effects on larval energy reserves. Nevertheless, the consequences of the 'latent effects' of natural environmental conditions and the proximate causes of the effects have rarely been examined. We documented the combined effect of delayed metamorphosis and sub-lethal exposure of larvae to low-salinity stress on depletion of energy reserves, metamorphic success and juvenile growth rates for the estuarine barnacle Balanus amphitrite, both in the laboratory and in field outplant experiments. Acute (24 h) exposure of 0 d old cyprids to low salinity (10 psu) dramatically reduced juvenile growth rates (measured as basal diameter, dry weight and ash-free dry weight) for the first 5 d after metamorphosis, in both laboratory and field conditions, and the effects were similar to those resulting from delayed metamorphosis. There was an interaction between delayed metamorphosis and salinity effects on juvenile tissue growth rates. To determine how the negative effects of delayed metamorphosis observed in the laboratory might be modulated in the field under different nutrient conditions, we also outplanted juveniles from cyprids that had delayed metamorphosis for either 0 d (control) or 4 d at 2 intertidal sites that experienced different nutrient conditions. Surprisingly, surplus food availability in the juvenile habitat could not entirely compensate for the negative effects imposed by delayed metamorphosis on juvenile growth rates. Additionally, we examined whether or not the detrimental effects of delayed metamorphosis on growth were mediated through effects on juvenile feeding rates and feeding appendage (cirri) morphology. Interestingly, although 2 out of the 3 juvenile feeding cirri lengths were shorter than expected in delayed individuals, mean juvenile filtration rate was significantly higher in delayed individuals than in control individuals. Overall, our results emphasise that acute exposure of competent larvae to low-salinity stress negatively affects juvenile growth rates as severely as delayed metamorphosis, which may ultimately influence juvenile and adult population dynamics in the field. The cause of reduced post-metamorphic performance in young barnacles remains unclear, but does not seem to be caused by reduced capacity for feeding.

Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species

“…Interestingly, our study also revealed that high-temperature and lowsalinity environments are comparable, if not stronger, drivers of negative latent effects (on settlement) than delayed settlement in this species (55% vs. 48% reduction, respectively). Consistent with our observations, cyprid larvae of the barnacle Balanus amphitrite exhibited negative latent effects of low salinity on postmetamorphic growth that were as severe as latent effects caused by delayed metamorphosis (Thiyagarajan et al 2007). …”

“…In the barnacle Balanus amphitrite, low-salinity stress during the larval stage reduced post-metamorphic growth rates (Thiyagarajan et al 2007). In contrast, low salinity caused FIG.…”

The interactive influence of temperature and salinity on larval and juvenile growth in the gastropod Crepidula fornicata (L.)

“…Similarly, latent effects resulting from exposing larvae to low salinity have been documented in the polychaete C. teleta (Pechenik et al, 2001) and the barnacle B. amphitrite (Thiyagarajan et al, 2007). Adding the results of our study to these previously documented cases of salinity-induced latent effects lends weight to the necessity of considering the environmental conditions larvae are exposed to when attempting to predict the responses of juvenile or adult populations.…”

“…Latent effects have been documented following larval exposure to low food concentration (the gastropod Crepidula fornicata: Pechenik et al, 1996a,b), ocean acidification (the oyster Ostrea lurida: Hettinger et al, 2012), low salinity (the polychaete Capitella teleta: Pechenik et al, 2001; the barnacle Balanus amphitrite: Thiyagarajan et al, 2007), copper (the bryozoan Watersipora subtorquata: Ng and Keough, 2003) and delayed larval metamorphosis (the colonial ascidian Diplosoma listerianum: Marshall et al, 2003;B. amphitrite: Pechenik et al, 1993; the bryozoan Bugula stolonifera: Woollacott et al, 1989).…”

Proceedings of the Smithsonian Marine Science Symposium

“…Salinity reductions during presettlement periods can reduce post-metamorphic growth rates and survival for various marine invertebrates (Pechenik et al, 2001;Thiyagarajan et al, 2008). Vermeij et al (2006) tested salinity stress on Montastraea faveolata larvae and how that infl uenced subsequent post-settlement FIGURE 4.…”