Open space, not reduced herbivory, facilitates invasion of a marine macroalga, implying it is a disturbance-mediated “passenger” of change
Introduction
Invasive species are altering ecosystem structure and functioning globally, yet invasions into marine systems are understudied (Caselle et al., 2017; Dijkstra et al., 2017; Papacostas et al., 2017). Invasive species are defined as species that establish outside of their native range and negatively impact the communities they invade (Inderjit et al., 2006; Williams and Smith 2007). Macroalgae account for 20–30 % of all marine invasive species (Schaffelke et al., 2006; Schaffelke and Hewitt 2007; Thomsen et al., 2006) and can negatively impact native community biomass (for review, see Gallardo et al., 2016; Mathieson et al., 2003; Trowbridge 2001; Williams and Grosholz 2002), functioning (Chisholm and Moulin 2003; Dumay et al., 2002a; Ferrer et al., 1997; Pedersen et al., 2005), structure (Balata et al., 2004; Sánchez and Fernández 2005; York et al., 2006) and biodiversity (Piazzi et al., 2001; Stæhr et al., 2000; Schmidt and Scheibling 2006). Despite their negative impacts, mechanisms that determine the success or failure of marine algal invasions are poorly understood (Inderjit et al., 2006; Papacostas et al., 2017; Williams and Smith 2007). Marine invasions are predicted to increase with continued globalization and shifts in ocean climate (Cohen and Carlton 1998; Godwin 2003; Grosholz 2002; Kaluza et al., 2010; Seebens et al., 2013; Stachowicz et al., 2002), highlighting the need to understand factors facilitating algal invasions.
One conceptual model, where invading species are categorized as “passengers” vs. “drivers,” may provide a useful framework for studying the mechanisms underpinning success of invasive marine algae. Originally developed by MacDougall and Turkington (2005), this model defines “drivers” as species that successfully invade a community through direct interactions with native species and subsequently modify the recipient community through their success (South and Thomsen 2016). In contrast, “passengers” require environmental change that disproportionately limits or removes native species and releases previously unavailable resources in order to successfully invade. Therefore, “drivers” are predicted to cause ecosystem change whereas “passengers” take advantage of it (MacDougall and Turkington 2005; South and Thomsen 2016).
One mechanism by which invasive species can drive ecosystem change is through exploitative competition for limiting resources, while passengers are considered competitively inferior. For marine macroalgae, light, space, and nutrients are primary resources determining growth and survival (Carpenter 1990; Sousa 1979) and competitive dominance is achieved through superior exploitation of these resources (MacDougall and Turkington 2005; Seabloom et al., 2003). Traits that facilitate resource exploitation for macroalgae can be morphological (e.g., height) and/or physiological (e.g., rapid growth) (Vaz-Pinto et al., 2014). Invaders are more likely to be successful “drivers” if these traits facilitate greater resource acquisition than native competitors. In contrast, passengers proliferate when disturbances remove dominant species, facilitating colonization of newly opened space. (Connell and Slayter, 1977; Elton 1958; MacDougall and Turkington 2005; Minchinton and Bertness 2003; Moyle 1986). In marine systems, disturbances such as intense wave-action associated with storms and large-scale climatic events can remove competitively superior native algae, and studies have shown that some invasive algae are only able to colonize following disturbance (Ambrose and Nelson 1982; Bulleri et al., 2010; Scheibling and Gagnon 2006; Thompson and Schiel 2012; Valentine and Johnson 2003). However, despite its importance for understanding invasion success, experimental tests exploring the role of competitive superiority and facilitation by disturbance in the driver-passenger framework are rare for marine macroalgal invasions (South and Thomsen 2016; Williams and Smith 2007).
Resistance to herbivory is another mechanism that may facilitate the invasion success of both drivers and passengers. Herbivore resistance can occur because invasive species possess novel defenses that make them unpalatable (Callaway and Ridenour 2004; Cappuccino and Carpenter 2005) or native consumers fail to recognize newcomers as a potential food source (Keane and Crawley 2002). In both cases, native macroalgae may be preferentially consumed, reducing the strength of competition between invasive and native algae and facilitating invasion success as a result (Pulzatto et al., 2018; Vermeij et al., 2009). Herbivore resistance as an invasion mechanism is generally supported for marine macroalgae. A review of 407 algal introductions (Williams and Smith 2007) found that, although introduced algae were consumed, native species were largely preferred by generalist herbivores. Further, others have found that invasive algae are only consumed when associated with native species (Noé et al., 2018) or when native species are absent (Sumi and Scheibling 2005), or that the intensity of herbivory was not strong enough to control invader spread despite consumption by herbivores (Britton-Simmons 2004; Chavanich and Harris 2004; Conklin and Smith 2005; Vermeij et al., 2009). For example, sea urchins were not capable of controlling the rapid growth of the annual invasive alga, Undaria pinnatifida, and facilitated its spread through consumption of native species (Edgar et al., 2004; Valentine and Johnson 2003). While evaluations of herbivore resistance by macroalgal invaders are common, results may depend on herbivory intensity and whether native species are available. Therefore, further tests are needed to understand the role of herbivores in promoting invasion success, particularly for recent and/or understudied macroalgal invasions.
Native community diversity is considered a primary driver of community resistance to invasion by both drivers and passengers (Britton-Simmons 2006; Elton 1958). It is hypothesized that diverse communities reduce the chance of successful invasion because resources are more completely utilized, limiting the number of open niches that a passenger can exploit. Further, the probability of encountering a competitively superior species is higher in more diverse communities, limiting the chance a driver will be successful (Clark and Johnston 2011; Elton 1958; Stachowicz et al., 1999). Some have argued that functional diversity and the composition of native assemblages may serve as better indicators of biotic resistance than taxonomic diversity by taking into account how different species uniquely limit resources and invasion success due to differences in traits and functional roles (Arenas et al., 2006; Britton-Simmons 2006; Caselle et al., 2017; Clark et al., 2004; Dukes 2001; Vaz-Pinto et al., 2012; Villéger et al., 2008; Reed and Foster 1984). For example, canopy-forming macroalgae are capable of significantly reducing the amount of light reaching the benthos and the shading effect of canopies is species-specific (Clark et al., 2004). While the relationship between native diversity and community resistance to invasion is widely documented in other systems (Davis et al., 2000; Stachowicz et al., 2007; Vaz-Pinto et al., 2012), there is variable support for this relationship in marine invasions (Arenas et al., 2006; Dunstan and Johnson 2004; Fridley et al., 2007; Papacostas et al., 2017) and tests of community invasibility by marine macroalgae are rare (Williams and Smith, 2007). Therefore, greater understanding of whether native diversity enhances biotic resistance to marine macroalgal invasions is needed.
California has experienced multiple marine algal invasions within the last 30 years (Britton-Simmons 2004; Miller et al., 2011), with the invasion of Sargassum horneri as one of the most recent and least understood. Native to east Asia, S. horneri first appeared in southern California in 2003 and has since spread throughout the region and into Baja California, Mexico (Kaplanis et al., 2016; Marks et al., 2015). S. horneri exhibits high fecundity, rapid growth, tolerance of a wide range of environmental conditions, and an annual life-history (Kaplanis et al., 2016; Marks et al., 2015), which are characteristics that may facilitate rapid proliferation and resource exploitation following a disturbance as a “passenger”. However, there have been very few investigations of mechanisms facilitating the success of S. horneri, despite documented negative impacts (Ginther and Steele 2018; Srednick and Steele 2019; Sullaway and Edwards 2020) and its invasion into critical habitats such as giant kelp (Macrocystis pyrifera) forests. Some studies suggest that S. horneri may be a passenger taking advantage of open niches by observing differences in peak seasonal biomass and depth distributions of S. horneri compared to native species (e.g., Marks et al., 2020a). Further, Caselle et al. (2017) found that low diversity sites (urchin barrens) as well as high diversity sites with an established native algal assemblage were resistant to S. horneri invasion; however, native diversity in this study was calculated across multiple trophic levels rather than just macroalgae. To date, conclusions regarding S. horneri's invasion mechanisms and community invasibility have been correlational (Caselle et al., 2017; Marks et al., 2020a), stressing the need to experimentally evaluate whether S. horneri is able to invade as a driver or requires ecosystem change as a passenger.
There is ambiguous evidence to support herbivore resistance as an invasion mechanism for S. horneri. Some have found herbivores preferentially consume native species over S. horneri (Marks et al., 2020a), suggesting that herbivore avoidance of S. horneri may facilitate its success. Others have concluded that herbivore resistance does not explain the success of S. horneri because herbivores had no clear preference for native algae compared to S. horneri (Kaplanis et al., 2020) or congeners (Pederson et al., 2016). Finally, Caselle et al. (2017) hypothesized that areas with high levels of herbivory may be resistant to S. horneri invasion, as S. horneri abundance was very low in areas with dense herbivore populations. Based on current evidence, it is unclear whether herbivores facilitate the invasion success of S. horneri by disproportionately consuming native species or whether herbivores enhance community resistance to invasion above certain densities. Taken together, these studies motivate further investigation into the role of herbivore resistance in the invasion of S. horneri.
We experimentally evaluated how interactions with native species and herbivory influence S. horneri's invasion success. Specifically, we evaluated three hypotheses: 1) S. horneri's invasion success will differ between sites that vary in baseline native algal diversity and urchin herbivory, 2) the presence of canopy-forming algae will influence where S. horneri can invade, and 3) herbivores will consume more native M. pyrifera than S. horneri. To test these hypotheses, we conducted three field experiments on temperate rocky reefs usually dominated by the giant kelp M. pyrifera in southern California, using growth as a proxy for invasion success (Mächler and Altermatt 2012; Van Kleunen et al., 2010). We first tested whether S. horneri invasion success differed with strength of urchin herbivory and native algal diversity by conducting a 2-factor field experiment that varied site (with different levels of baseline urchin densities and native algal diversity) and urchin access. We then evaluated whether S. horneri could successfully invade established algal canopies or whether it required open space via a 2-factor field experiment that varied S. horneri size (small, medium, large) and canopy type (S. horneri, M. pyrifera, -canopy). Finally, we evaluated whether herbivore consumption of native species could facilitate S. horneri's invasion by conducting a 2-factor field experiment that varied species (M. pyrifera, S. horneri) and herbivore access.
Section snippets
Study system
All research was conducted on the leeward side of Santa Catalina Island, California, USA (Fig. 1; 33°26′40.8″N 118°29′41.2″W). Catalina rocky reefs are generally characterized by a combination of cobble, boulder, and bedrock substrate interspersed with sand and shell debris (Marks et al., 2020a). Native algal cover varies by area and species, with some areas characterized by a mixed community of abundant small (<0.5 m) understory native species (i.e., Dictyota spp., Dictyopteris undulata,
Experimental results
There was a significant difference in percent change in biomass day−1 between urchin barrier treatments (Table 1E; Fig. 2E). S. horneri grew or remained the same when protected from urchins, and lost biomass when open to herbivores. Percent change in biomass was not significantly different among sites (i.e., baseline levels of diversity or urchins), nor was there an interaction between factors.
Canopy effects on S. horneri
There were significant differences in percent change in biomass among S. horneri sizes and canopy
Discussion
We found that S. horneri is a “passenger” of environmental change and not a “driver” of its own invasion success, as S. horneri grew faster in our study when the native canopy-forming M. pyrifera was absent and slower when M. pyrifera canopy was present. To our knowledge, our study is the first to experimentally test this hypothesis, although others have hypothesized that success of S. horneri depends on exploitation of open niches rather than competitive superiority (Caselle et al., 2017;
Conclusion
Understanding mechanisms that facilitate the success of marine invasions is increasingly important as the frequency of marine invasions is projected to rise (Cohen and Carlton 1998; Grosholz 2002; Seebens et al., 2013; Stachowicz et al., 2002). We found that S. horneri likely takes advantage of disturbance to the native community as a passenger and neither algal diversity nor herbivory provide a strong explanation for invasion success. As disturbances are expected to increase in frequency and
Author's contributions
E.R.R. and P.F. conceived the ideas and designed the methodology; E.R.R. and L.L.S. collected the data; E.R.R. analyzed the data and wrote the manuscript; P.F. and L.L.S. edited the manuscript. All authors substantially contributed to the drafts and gave final approval for publication.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We would like to thank K.L. Chiquillo and A. Hailer for field support, as well as the staff at the USC Wrigley Institute for Environmental Studies for logistical assistance. Also, we would like to thank K.C. Cavanaugh and J.O. Lloyd-Smith for helpful feedback when writing this manuscript. This work was funded by the USC Wrigley Institute for Environmental Studies, the UCLA Department of Ecology and Evolutionary Biology, the Santa Monica Bay Audubon Society, the La Kretz Center for California
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