Macroalgal spore dysfunction: ocean acidification delays and weakens adhesion

Abstract

Early life stages of marine organisms are predicted to be vulnerable to ocean acidification. For macroalgae, reproduction and population persistence rely on spores to settle, adhere and continue the algal life cycle, yet the effect of ocean acidification on this critical life stage has been largely overlooked. We explicitly tested the biomechanical impact of reduced pH on early spore adhesion. We developed a shear flume to examine the effect of reduced pH on spore attachment time and strength in two intertidal rhodophyte macroalgae, one calcified (Corallina vancouveriensis) and one noncalcified (Polyostea robusta). Reduced pH delayed spore attachment of both species by 40%-52% and weakened attachment strength in C. vancouveriensis, causing spores to dislodge at lower flow-induced shear forces, but had no effect on the attachment strength of P. robusta. Results are consistent with our prediction that reduced pH disrupts proper curing and gel formation of spore adhesives (anionic polysaccharides and glycoproteins) via protonation and cation displacement, although experimental verification is needed. Our results demonstrate that ocean acidification negatively, and differentially, impacts spore adhesion in two macroalgae. If results hold in field conditions, reduced ocean pH has the potential to impact macroalgal communities via spore dysfunction, regardless of the physiological tolerance of mature thalli.

Elevated CO2 Leads to Enhanced Photosynthesis but Decreased Growth in Early Life Stages of Reef Building Coralline Algae

“…The impacts of ocean acidification (OA) on adult coralline algae have been relatively well documented (Hofmann and Bischof, 2014), and there is a growing body of evidence supporting the sensitivity of the early life history stages of coralline algae to OA. In particular, recent studies have shown reduced spore germination (Bradassi et al, 2013;Ordoñez et al, 2017) and attachment (Guenther et al, 2018) and declined germling abundance [e.g., % cover, Kuffner et al (2008) growth (Roleda et al, 2015;Ordoñez et al, 2017) under elevated CO 2 conditions. However, whether metabolic processes such as photosynthesis and respiration of early life stages of CCA also show a negative response to elevated CO 2 has not been well documented.…”

“…Roleda et al (2015) tested the effects of OA on growth of temperate coralline algae recruits and found a direct negative response of crust size upon exposure to OA conditions. Studies of the early life stages of tropical (Kuffner et al, 2008;Fabricius et al, 2015;Ordoñez et al, 2017) and temperate (Bradassi et al, 2013;Roleda et al, 2015;Guenther et al, 2018) CCA have demonstrated a high vulnerability to elevated CO 2 , as well as other environmental stressors (Santelices, 1990). However, very little is known about the effects of OA on photosynthesis and the coupling between photosynthesis and growth rates in the early life stages of CCA (but see Cornwall et al, 2013).…”

Plasticity of adult coralline algae to prolonged increased temperature and pCO2 exposure but reduced survival in their first generation

“…Population persistence of macroalgae rely on spores settling and adhering onto substratum, to continue the algal lifecycle. In a study done by Guenther et al [31], reduced pH, or the increase of pCO 2 , resulted in a 40-52% delay in spore attachment and weakened the attachment strength in the coralline alga species, Corallina vancouveriensis. The previously mentioned studies examined shorter-term exposure (1 month or less) to OW and OA, either in combination or independently, and found mostly negative responses over a number of genera.…”

“…Early life history stages of organisms are thought to be the most influenced by changes in their environment [27,28]. Our knowledge on offspring or early life history stages of CCA is limited and variable, with studies finding early life history stages to be highly susceptible to combined stressors of increases in temperature and OA [29][30][31][32][33] or largely unaffected by pCO 2 when it is an independent stressor [34]. A more recent study even suggests CCA can gain tolerance to OA over multiple generations [35].…”

Ocean warming and acidification alter the behavioral response to flow of the sea urchin Paracentrotus lividus

“…The reported effects of low pH on biomechanics of noncalcified materials include no significant effect on TF mechanical properties in the starfish Asterias rubens , reduced mechanical performance of the byssus in bivalves, decreased clapping force in the scallop Pecten maximus , and lowered spore attachment in intertidal rhodophyta algae (Collard, Catarino, Bonnet, Flammang, & Dubois, ; George & Carrington, ; Guenther, Miklasz, Carrington, & Martone, ; Li, Liu, Zhan, Xie, & Zhang, ; O'Donnell, George, & Carrington, ; Schalkhausser et al, ). Behavioral studies under climate change conditions mainly concentrate on OA effects on fishes (Cripps, Munday, & McCormick, ; Dixson, Munday, & Jones, ; Domenici, Allan, McCormick, & Munday, ; Ferrari et al, ; Hamilton, Holcombe, & Tresguerres, ; Jutfelt, Bresolin de Souza, Vuylsteke, & Sturve, ; Munday et al, ; Nilsson et al, ; Simpson et al, ) and, to a lesser extent, on marine invertebrates focusing on predator–prey relationships (Bibby, Cleall‐Harding, Rundle, Widdicombe, & Spicer, ; Chan, Grünbaum, Arnberg, & Dupont, ; Dodd, Grabowski, Piehler, Westfield, & Ries, ; Manríquez et al, ).…”