The Blob marine heatwave transforms California kelp forest ecosystems

The Santa Barbara Coastal Long Term Ecological Research program has monitored benthic communities in five kelp forests seasonally since 2008 using fixed transect diver surveys, and moored sensors at each reef have recorded bottom temperatures every 15 min. Blob-associated positive bottom temperature anomalies began in winter 2014 and persisted through autumn 2016 (Fig. 1a)¹⁸. Peak temperature anomalies occurred during the summer and autumn of 2014 and 2015 (Fig. 1a), and the average temperature anomaly in autumn 2015 was +3.1 °C, equivalent to an average daily temperature of 19.6 °C. In 2014 and 2015, 91 and 69% of autumn days, respectively, were classified as heatwave days as defined by Hobday et al.²⁰. Seasonal chlorophyll-a concentration, a proxy for phytoplankton abundance, was obtained from satellite imagery at each of the five reefs over the 14-year period. The average chlorophyll-a concentration was anomalously low throughout the warming period, and exceptionally low during the springs of 2014 and 2015 (Fig. 1a), when upwelling-driven nutrient enrichment typically supports dense phytoplankton blooms.

Mean sessile invertebrate cover averaged across all sites declined 71% during the Blob, reaching a 14-year minimum of 7% in autumn of 2015 (Fig. 1b and Supplementary Fig. 1). Species richness declined 69% during the same period (Fig. 1b and Supplementary Fig. 1). The responses of invertebrates to warming were not consistent across time even though the duration and intensity of warming was similar in 2014 and 2015, suggesting that extended periods of elevated seawater temperature were not solely responsible for the most severe loss of invertebrates. For ectotherms, increases in ambient seawater temperature should be met with increases in metabolic rate and food requirements to sustain metabolism²¹. Because of their sedentary lifestyle, sessile invertebrates cannot actively forage for food or seek spatial refuge from thermal extremes, and limitations in their planktonic food supply can result in metabolic stress over extended periods^22,23. Anomalously low chlorophyll-a concentrations during the Blob (Fig. 1a), particularly in the spring of 2015, indicated that food limitation was a likely driver of invertebrate decline. Results from piecewise structural equation modeling (Fig. 2) that incorporated biological interactions with space competitors (understory macroalgae), predators (sea urchins), and foundation species (giant kelp) showed that the severity of warming had both a direct and indirect effect on the sessile invertebrate community. The proportion of heatwave days was a direct negative predictor of sessile invertebrate cover (−0.11) and species richness (−0.21). The proportion of heatwave days was an even stronger negative predictor of chlorophyll-a concentration (−0.26), yielding negative indirect effects on invertebrate cover (−0.07) and species richness (−0.05) due to the positive influence of chlorophyll-a concentration on sessile invertebrate cover (+0.26) and richness (+0.20).

Consequences of heatwaves on benthic community structure can be difficult to predict if community-level interactions exacerbate or ameliorate stressful conditions^24,25. The biomass of giant kelp, Macrocystis pyrifera, an important foundation species on temperate reefs, was not strongly impacted by the Blob in the Santa Barbara Channel (Fig. 2)^18,26, but experienced warming-induced declines at its equatorward range edge^26,27. Given the strong positive relationship between giant kelp biomass and sessile invertebrate cover (+0.40) and species richness (+0.46), future declines in giant kelp during warming events, as has been seen in other kelp forest systems^5,17, will likely contribute to sessile invertebrate declines. Similarly, loss of kelp canopy has been shown to increase understory algal cover and biomass^28,29, a strong negative predictor of invertebrate cover (−0.45) and species richness (−0.32), apparently due to increased competition between understory algae and invertebrates for space.

Invertebrate phyla did not respond equally to the Blob; some phyla experienced severe declines during the warming event while others resisted change. Bryozoans, sponges, annelids, and ascidians were particularly hard-hit and declined to their lowest percent cover during the Blob (Fig. 3, Supplementary Fig. 2). For example, in autumn 2015 bryozoans and sponges were not recorded at any site while ascidians were recorded at only one site in very low abundance (i.e. ~1% cover). The decline in the percent cover of annelids began prior to the Blob, making it difficult to attribute their low abundance in 2015 solely to warming. Bryozoans and annelids rapidly recovered following the Blob, and by 2017 their percent cover approached or surpassed pre-heatwave levels. By contrast, the recovery of sponges was considerably slower, with pre-Blob levels not evident until 2020 (Fig. 3, Supplementary Fig. 2). Mollusks were relatively unaffected by the heatwave, although their highest cover was observed in the years following the Blob, suggesting that they may have benefited from delayed indirect positive effects of warming (Fig. 3, Supplementary Fig. 2, Supplementary Fig. 4).

Although the percent cover of most sessile invertebrate phyla returned to pre-Blob levels within a couple of years after the heatwave, changes in the species composition of the sessile invertebrate community attributed to the Blob have persisted (PERMANOVA, F = 13.462, p < 0.001; Fig. 4). As positive temperature anomalies subsided in early 2016, invertebrate cover and richness steadily increased over time, peaking in the summers of 2017 and 2018 (Fig. 1). This increase in invertebrate cover was largely driven by increases in the abundance of bryozoans, and to a lesser extent, mollusks (Fig. 3, Supplementary Fig. 2, Supplementary Fig. 3, Supplementary Fig. 4). Two invasive bryozoan species accounted for much of this increase (Fig. 4). The percent cover of Watersipora subatra, a recent invader in the Santa Barbara Channel³⁰, increased after the Blob (Supplementary Fig. 3, Fig. 4; IndVal = 0.455, p < 0.001), while Bugula neritina, a long-established invader, is now substantially more abundant than its morphologically similar native relative, Bugulina californica (Supplementary Fig. 3, Fig. 4; IndVal = 0.549, p < 0.01). The increased abundance of W. subatra and B. neritina following the Blob could be due to reductions of specialized native species that otherwise would outcompete generalist invaders³¹, increased tolerance to thermally or metabolically stressful conditions, as has been demonstrated for W. subtorquata and some invasive ascidian species³², or increased recruitment of these species³³.

In addition to increases in nonnative species, the abundance of a native southern-affinity sessile gastropod, Thylacodes squamigerus, increased significantly since the onset of the Blob (IndVal = 0.711, p < 0.001; Fig. 4, Supplementary Fig. 4). As one of the few locally abundant invertebrates with a southern range extending beyond Baja California, T. squamigerus may have been preadapted to warmer temperatures. T. squamigerus also has the capacity to consume kelp detritus as an alternative food source³⁴, which may have facilitated its survival during extended periods of low plankton availability.

Though most sessile invertebrates are suspension feeders relying on the delivery of plankton and particulate organic matter for food^10,11, there are differences in life history traits and feeding strategies among benthic phyla that may result in unequal responses to marine heatwaves. Colonial species, including sponges, most bryozoans, and many ascidians, are generally shorter-lived and exhibit rapid growth rates. By contrast, anthozoan cnidarians and mollusks are generally longer-lived with slower growth³⁵, and may have specific traits (e.g., lower metabolism, energy stores, alternate feeding strategies) that enable them to survive prolonged periods of warming with anomalously low phytoplankton supply. For example, anemones are opportunistic feeders that can consume zooplankton and detritus³⁶, while colonial species such as bryozoans and ascidians may be more dependent on smaller phytoplankton³⁷, with a lower capacity to switch food sources in the event of low phytoplankton abundance. Though adult anthozoans and mollusks were generally resilient during the Blob, prolonged reductions in phytoplankton could adversely affect their populations by limiting recruitment in species with planktotrophic larvae that depend on phytoplankton for food. Increases in bryozoan cover following the Blob, particularly in two invasive species, suggests that rapid reproduction and growth may have facilitated their colonization following disturbance and increases in unoccupied space. Similar trends were observed in Mediterranean temperate reefs where traits associated with rapid growth and reproduction were significantly more common in benthic assemblages following heatwaves³⁸.

Suspension-feeding invertebrates are an essential link between pelagic and benthic food webs¹⁰, are important fisheries and aquaculture species, and are especially susceptible to environmental stressors due to the constraints in food acquisition and reproduction imposed by sessility. We found large negative impacts of warming and accompanying phytoplankton decreases on benthic suspension feeders along with persistent changes in their species composition in kelp forests of southern California, even though the major habitat-forming species, giant kelp, was relatively resilient to warming^18,26. The Blob had similar effects in altering the species composition (but not community biomass) of understory macroalgae at our study sites^18,39, which in turn, may have indirectly affected the sessile invertebrate community. We predict that increasing marine heatwaves will result in future losses and changes in species assemblages of sessile animals on temperate rocky reefs worldwide, and these transformations will likely be exacerbated by warming-induced declines in structure-forming kelps and understory macroalgae. Declines or changes in the species composition of suspension feeders may disrupt coastal food webs if the “winners” are functionally dissimilar from existing taxa. For example, heatwaves have altered functional traits in temperate reef systems through changes to benthic community structure³⁸. Additionally, introductions of tropical herbivorous fish to temperate reefs during reef tropicalization have resulted in herbivore-mediated declines of macroalgae⁴⁰, altering ecosystem function. Such functional shifts may have significant consequences for temperate reefs, including decoupling of primary production from higher trophic levels that depend on these vital primary consumers for survival.

Source: Ecology - nature.com