Windows of vulnerability: Seasonal mismatches in exposure and resource identity determine ocean acidification’s effect on a primary consumer at high latitude

Abstract

It is well understood that differences in the cues used by consumers and their resources in fluctuating environments can give rise to trophic mismatches governing the emergent effects of global change. Trophic mismatches caused by changes in consumer energetics during periods of low resource availability have received far less attention, although this may be common for consumers during winter when primary producers are limited by light. Even less is understood about these dynamics in marine ecosystems, where consumers must cope with energetically costly changes in CO2‐driven carbonate chemistry that will be most pronounced in cold temperatures. This may be especially important for calcified marine herbivores, such as the pinto abalone (Haliotis kamschatkana). H. kamschatkana are of high management concern in the North Pacific due to the active recreational fishery and their importance among traditional cultures, and research suggests they may require more energy to maintain their calcified shells and acid/base balance with ocean acidification. Here we use field surveys to demonstrate seasonal mismatches in the exposure of marine consumers to low pH and algal resource identity during winter in a subpolar, marine ecosystem. We then use these data to test how the effects of exposure to seasonally relevant pH conditions on H. kamschatkana are mediated by seasonal resource identity. We find that exposure to projected future winter pH conditions decreases metabolism and growth, and this effect on growth is pronounced when their diet is limited to the algal species available during winter. Our results suggest that increases in the energetic demands of pinto abalone caused by ocean acidification during winter will be exacerbated by seasonal shifts in their resources. These findings have profound implications for other marine consumers and highlight the importance of considering fluctuations in exposure and resources when inferring the emergent effects of global change.

Standing Crop, Turnover, and Production Dynamics of Macrocystis pyrifera and Understory Species Hedophyllum nigripes and Neoagarum fimbriatum in High Latitude Giant Kelp Forests

“…Such species-specific differences suggest that these co-occurring understory kelps employ distinct 'strategies' in the timing and magnitude of their resource mobilization for growth. In this system, these phenological differences in basal production may be critical to sustaining certain consumers' energetic demands during the more physiologically stressful winter season (Kroeker et al 2021).…”

“…As a result, when understory kelp FSC was relatively high (such as during summer 2018), the relative proportion of C and N production by these species compared to giant kelp was notably increased. Prior work in this system has shown that pinto abalone (Haliotis kamtschatkana), a common rocky reef grazer, experience higher growth rates when fed a mixed algal diet consisting of several kelp species than when fed a diet of M. pyrifera alone (Kroeker et al 2021). Given that M. pyrifera dwarfed understory kelp species in terms of both FSC and productivity at sites not undergoing phase shifts, even modest increases in the relative productivity of any understory kelp species would provide a valuable, diverse source of nutrition to the primary consumer community.…”

“…Understanding kelp production capacity in these habitats is needed to correct the geospatial bias of the data that currently inform global estimates of seaweed productivity. High latitude environments are seasonally dynamic, where variation in seawater temperature, pCO 2 , storms, light, and nutrient availability impact macroalgal physiology (Graham et al 2007, Kroeker et al 2021. The long photoperiod of the high latitude spring and summer contributes to seasonally high rates of production for some macroalgal species (Druehl and Wheeler 1986, van Tussenbroek 1989, Brown et al 1997, Nielsen et al 2014).…”

“…As ocean acidification and warming overlay onto current environmental variability at high latitudes, the responses of marine producers may vary by season (Graiff et al 2015, Wahl et al 2020. Further, consumers in these systems will experience heightened susceptibility to stressful conditions in particular seasons (Kroeker et al 2021). Ecological theory suggests that the resilience of these ecosystems will hinge on both the abundance and diversity of basal production that is available to support consumers under such enhanced stress (Bernhardt and Leslie 2013, Gaylord et al 2015, Doubleday et al 2019.…”

“…We surveyed all unique M. pyrifera sporophytes (hereafter, "plants"; Bolton 2016) within two permanent 30 × 2 m transects at the 5-7 m depth (MLLW) contour and counted the total number of fronds extending >1 m above the holdfast (hereafter, "frond density"). To determine the relationship between frond density and total wet mass (g), we collected and measured M. pyrifera plants (excluding their holdfasts) in summer 2017 (N = 16) and winter 2018 (N = 10; Kroeker et al 2021). We used a linear model to test the effect of season (winter and summer) on the relationship between frond density and wet mass.…”