Variability of Seawater Chemistry in a Kelp Forest Environment Is Linked to in situ Transgenerational Effects in the Purple Sea Urchin, Strongylocentrotus purpuratus

Umihiko Hoshijima,Gretchen E Hofmann

doi:10.3389/fmars.2019.00062

Umihiko Hoshijima, Gretchen E Hofmann

Open Access

https://doi.org/10.3389/fmars.2019.00062

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Abstract

While the value of giant kelp (Macrocystis pyrifera) as a habitat-forming foundation species is well-understood, it is unclear how they impact the oxygen concentration and pH of the surrounding seawater, and further, how such a dynamic abiotic environment will affect eco-evolutionary dynamics in a context of global change. Here, we profiled the nearshore kelp forest environment in Southern California to understand changes in dissolved oxygen (DO) and pH with high spatiotemporal resolution. We then examined transgenerational effects using sea urchins (Strongylocentrotus purpuratus) as our study organism. Using enclosures on the benthos, we conditioned adult sea urchins in situ at two locations - one inside the kelp forest and one outside the kelp forest. After a 11 week conditioning period timed to coincide with gametogenesis in the adults, the urchins were collected, spawned, and cultures of their progeny were raised in the laboratory in order to assess the performance of the progeny to simulated ocean acidification. In terms of the physical observations, we observed significant changes in DO and pH not only when comparing sites inside and outside of the kelp forest, but also between surface and benthic sensors at the same site. DO and pH at the benthos differed in mean, the amplitude of the diel signal, and in the profile of background noise of the signal. Ultimately, these results indicated that both DO and pH were more predictably variable inside of the kelp forest environment. On the biological side, we found that adult sea urchins inside the kelp forest produced more protein-rich eggs that developed into more pH-resilient embryos. Overall, this study in a temperate kelp forest ecosystem is one of the first studies to not only observe biological response to highly characterized environmental variability in situ, but also to observe such changes in a transgenerational context.

Highlights

We investigated the potential for a predominant form of transgenerational plasticity (TGP), maternal effects, to alter the performance of an ecologically important kelp forest grazer’s progeny in the presence or absence of a kelp forest environment in the California Current Large Marine Ecosystem (CCLME)
We found that the kelp forest environment provided a generally higher pH, higher dissolved oxygen (DO) environment throughout the water column, while introducing a more predictable diel signal and diminishing high-frequency variation
Seasonal Variation The data collected in this study showed a seasonal variation of pH and DO in a kelp forest environment, as has been reported in other studies in California Macrocystis forests (Kapsenberg and Hofmann, 2016; Koweek et al, 2017)

Summary

Introduction

The role of macrophytes in raising the pH of seawater on a local scale while locally increasing levels of dissolved oxygen (DO) (McLeod et al, 2011; Nielsen et al, 2018) has been recognized in a suite of coastal marine ecosystems (Hofmann et al, 2011; Unsworth et al, 2012; Guadayol et al, 2014; Hendriks et al, 2014; Baumann et al, 2015; Kline et al, 2015; Sorte and Bracken, 2015; Kapsenberg and Hofmann, 2016; Kroeker et al, 2016; Kwiatkowski et al, 2016; Kapsenberg et al, 2017; Silbiger and Sorte, 2018). Of note is the strong highfrequency covariation of pH and DO as multiple stressors in these nearshore environments (Frieder et al, 2012; Breitburg et al, 2015; Gunderson et al, 2016) that interact with a mosaic of coastal upwelling along the coastline (Chan et al, 2017) These patterns all suggest that adult organisms in the benthic environment, in particular, likely experience a range of pH as well as DO, and this gradient will vary in location and with proximity to macrophytes. Understanding such relationships will help to elucidate the future of these coastal oceans to complex environmental change (Gunderson et al, 2016; Vargas et al, 2017)

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