Marine heatwaves facilitate invasive algae takeover as foundational kelp

Kelp forest communities along the Pacific Northwest have recently experienced dramatic climate change related impacts (Beas-Luna et al. 2020). From 2013 to 2016, the California Current System experienced an unusually high and persistent warming event, the “Warm Blob”, from Alaska southward to the coast of Baja California. In 2015–2016, this warming event was succeeded by one of the strongest El Niño Southern Oscillation (ENSO) on record (Di Lorenzo and Mantua 2016). It is now widely documented that these marine warming events influenced shifts in distribution and abundance of at least 165 taxonomic groups (e.g. Lonhart et al. 2019), canopy kelp biomass was significantly reduced (Cavanaugh et al. 2019) and community structure switched to a less complex system, characterized by species with warmer affinities (Arafeh-Dalmau et al. 2019).

Miller and Engle (2009) hypothesized that changes in the cover and/or density of M. pyrifera, caused either by climate change phenomena (e.g. ENSO events and marine heatwaves), or biologically driven changes (e.g. sea urchin overgrazing), could facilitate conditions for the recruitment of new populations of opportunistic non-native invasive species. As climate change effects would be more evident in kelp forests near the southern portion of the California Current (Beas-Luna et al. 2020), there is a need to understand how novel species will influence the structure and function of coastal marine ecosystems in this area.

Kelp forest communities near their southern distribution limit along the coast of southern California, USA and Baja California, Mexico, where Macrocystis pyrifera (Linnaeus) Agardh is the historically predominant structuring and foundational native species (Schiel and Foster 2015), have seen an increase in the spread and presence of non-native Sargassum horneri (Turner) Agardh (Marks et al. 2015; Riosmena-Rodríguez et al. 2012), and Undaria pinnatifida (Harvey) Suringar (Aguilar-Rosas et al. 2004; Silva et al. 2002) over the past decades. Both species are originally from Asia, but are now distributed in locations along the coast of California and Baja California (Aguilar-Rosas et al. 2004; Marks et al. 2015). Undaria pinnatifida and S. horneri are considered invasive species because they compete for space with native macroalgae and, once established, can induce changes in community composition and species diversity (James 2017). Here, we report the local presence and discuss potential impacts of U. pinnatifida and S. horneri at Todos Santos Islands, Baja California, Mexico.

Todos Santos Islands are located off the northwest coast of Baja California, Mexico, approximately 120 km south of the border between the USA and Mexico (Figure 1). Its surrounding waters harbor a temperate ecosystem representative of the Southern California Bight, with seasonal northwest winds that promote coastal upwelling, primary productivity and a rich and diverse trophic chain (Lynn and Simpson 1987). We evaluated shifts in the kelp community on a rocky reef at ∼10 m depth between the northern and the southern Todos Santos Islands (Figure 1). We surveyed four 30 × 2 m underwater transects using SCUBA in May 2018 and June 2019. On each transect we measured the density (individuals m⁻²) of U. pinnatifida, S. horneri and M. pyrifera larger than 15 cm.

Figure 1:

Map showing northern and southern Todos Santos Islands. Red square highlights the sampling area. Black square in inset map indicates location of Todos Santos Bay in Baja California, Mexico.

Between 2018 and 2019 we documented a dramatic population reduction of M. pyrifera in our study site, as the species declined from a mean of ∼ 0.7 individuals m⁻² in 2018 to 0 individuals m⁻² in 2019 (Figures 2 and 3). In this same site and time period, we also observed a threefold increase in the density of S. horneri, and U. pinnatifida going from absent in 2018 to ∼ 4 individuals m⁻² in 2019 (Figure 2). Aerial views of the study site show kelp canopy well extended to the water surface in 2018, while there was a total absence of canopy and exposure of bottom rocks in 2019 (Figure 3).

Figure 2:

Density changes of native Macrocystis pyrifera and two invasive kelp species between 2018 and 2019 at Todos Santos Islands, Baja California, Mexico. Lower and upper box boundaries represent the 25th and 75th percentiles, respectively, the line inside box the median, and lower and upper error lines the 10th and 90th percentiles, respectively.

Figure 3:

Composite images using AUV (drone) photography from Todos Santos Islands channel reef at 30 m altitude showing presence and absence of native Macrocystis pyrifera canopy between 2018 (native dominated) and 2019 (invasive dominated). Orthomosaic composed from ∼ 191 images, each image overlapping 80% with the neighboring photos, and with a resolution of 1.29 cm pix⁻¹ using Photoscan.

In Baja California, the marine heatwave from 2013 to 2016 led to a dramatic loss of M. pyrifera biomass (Arafeh-Dalmau et al. 2019; Cavanaugh et al. 2019) and significant changes to fish, algal and invertebrate communities (Arafeh-Dalmau et al. 2019; Beas-Luna et al. 2020). Marine heatwave events started to diminish in the summer of 2016 and were less intense through 2017. Satellite-derived data from Arafeh-Dalmau (2019) reported that, by spring and winter of 2017, kelp biomass at Todos Santos Islands had recovered to seasonal values observed before the warming events. However, Cavanaugh et al. (2019) found that, while native kelp biomass started to recover at different sites along southern Baja California, the decline continued from 2017 to 2018 at Todos Santos Islands and adjacent areas. Additionally, Arafeh-Dalmau et al. (2019) reported a threefold reduction in the number of M. pyrifera fronds before and after the warming events at Todos Santos Islands based on in situ surveys. Differences in the impact reported for native kelps at Todos Santos Islands could be explained by methodological differences to estimate M. pyrifera, (i.e. biomass vs. fronds), and the different specific study sites assessed. Regardless, this widespread native kelp canopy decline could have further facilitated invasion pathways in this benthic community, specifically for our study site.

Invasive macroalgae such as S. horneri have been observed to proliferate after disturbances that decrease the abundance or alter the distribution of native macroalgae (Sullaway and Edwards 2020). Undaria pinnatifida, an opportunistic species, grows best in absent or scarce canopy areas (James 2017). Due to its constant recruitment capacity, U. pinnatifida has an enhanced invasive potential and would thrive when conditions are suitable (≤15 °C) in open canopy areas, thus establishing persistent populations (Thornber et al. 2004). Arafeh-Dalmau et al. (2019) reported changes to the structure of subcanopy species with a high presence of U. pinnatifida after the 2013–2016 marine heatwave at Todos Santos Islands and other locations along the coast of Baja California. Similarly, the 2014–2016 marine heatwave appears to have facilitated the establishment of S. horneri populations in areas where M. pyrifera populations were previously present (Marks et al. 2015). Indeed, under laboratory and controlled field experiments it has been found that light limitation – such as that produced by these low canopy-forming invasive kelps – can hinder recruitment and juvenile survival of M. pyrifera (Beckley and Edwards 2021; Sánchez-Barredo et al. 2020).

The decrease in abundance of M. pyrifera coupled with favorable growth conditions for both U. pinnatifida and S. horneri during and after the 2014–2016 marine heatwave events likely resulted in the increased abundance observed in this study. It is yet unclear how persistent these seeming population shifts will be, but these warming events in addition to other future climate conditions such as ocean acidification (Shlenger et al. 2021) may be the onset of more profound macroalgal community structure shifts at Todos Santos Islands as, once established, both of these species can compete for space with native canopy-forming algae. Furthermore, given the influence of M. pyrifera as bio-engineers of their surrounding environment, changes to this foundational species would likely result in a novel community of understory algae, sessile species and mobile predators (Schiel and Foster 2015). Over the past decade, kelp forests and the ecosystem services they provide have deteriorated drastically. Future climate change scenarios suggest a challenging future for these temperate ecosystems. Thus, understanding response mechanisms of novel species interactions will inform adequate management strategies. Hence, further monitoring should be carried out to evaluate the long-term change of macroalgal community structure and its consequences for ecosystem functioning and services, particularly the presence and abundance of invasive kelps in the region. Such studies should focus on better understanding annual lifecycles of the invasive kelps, as well as the impacts of shifts in food availability and novel energy pathways to herbivores and throughout higher-level consumers.