Range expansion of a non-native , invasive macroalga Sargassum horneri ( Turner ) C . Agardh , 1820 in the eastern Pacific

Sargassum horneri (Turner) C. Agardh, 1820 is a fast growing brown alga native to shallow reefs of eastern Asia. It has spread aggressively throughout southern California, USA, and Baja California, México since it was discovered in the eastern Pacific in 2003 and poses a major threat to the sustainability of native marine ecosystems in this region. Here we present a chronology of the rapid geographic expansion of S. horneri in the eastern Pacific and discuss factors that potentially influence its spread.


Introduction
Introductions of marine non-native species continue worldwide and are expected to increase with the expansion of global trade.The spread and ecological effects of newly-established nonnative species can vary; some proliferate and compete vigorously in their introduced range and are considered "invasive" (Miller et al. 2011).Introduced marine macroalgae are no exception, although detailed records of the geographic expansion of introduced marine macroalgae are rare (Lyons and Scheibling 2009) despite there being at least 277 introduced seaweed species globally (Williams and Smith 2007).Documenting the spread of these species can be challenging given the logistical difficulties associated with sampling in subtidal habitats where they occur (e.g.time-and depth-limitations when using scuba and the expense of accessing remote sites).Yet such studies are valuable for not only documenting their distributions but also providing insight into the mechanisms influencing the spread of non-native species.
Here we present the chronology of the geographic expansion of the non-native macroalga Sargassum horneri (Turner) C. Agardh, 1820 (Fucales) along the southern region of the Pacific coast of North America, where it has spread rapidly since it was first detected in Long Beach Harbor, California, USA, in 2003 (Miller et al. 2007).We also discuss potential factors influencing the spread of this species and the implications of its invasion to native ecosystems.

Study area
The study area encompassed the shallow coastal waters of the eastern Pacific Ocean from northern California, USA, to the southern tip of Baja California, México.Much of this coast is actively monitored by government and academic researchers and citizen scientists, and is therefore an ideal region in which to document the spatio-temporal dynamics of the spread of an invasive macroalga.Miller et al. (2007) initially identified the introduced population of Sargassum discovered in Long Beach, California as S. filicinum (Harvey, 1860).This annual brown alga is monoecious, with ellipsoidal pneumatocysts, and has a narrow geographic range on the coast of western Japan (Yoshida et al. 1983;Tseng et al. 1985) and southern Korea (Lee and Yoo 1992).On the basis of molecular population studies, Uwai et al. (2009) merged S. filicinum with S. horneri, a dioecious species with spherical pneumatocysts that is widespread in the warmer waters of eastern Asia (Tseng et al. 1985).Therefore, we refer to the eastern Pacific population as S. horneri.

Study species
The morphology of S. horneri changes throughout its annual, diplonic, life cycle.Embryos develop into small plants with lateral fern-like branches anchored by a common holdfast (Figure 1A).Plants give rise to a single erect frond up to several meters in length that bears numerous vegetative blades buoyed by many small gas bladders (Yoshida 1983).Eventually, the frond ceases vertical growth and develops hundreds of reproductive receptacles (Figure 1B).Fertilization occurs when sperm penetrate an egg inside a conceptacle positioned on the surface of a receptacle.The resulting embryo is released and settles to the bottom.After embryos are shed the frond senesces and the entire thallus dies, completing the life cycle.Sexual reproduction is the only known means of propagation.Miller et al. (2007) recorded the presence of S. horneri in the eastern Pacific in southern California shortly after it was first discovered in 2003.Rapid communication, coupled with the species' conspicuous morphology and widely distributed information on its identification, facilitated the subsequent monitoring of S. horneri by many researchers in California and Baja California.

Methods
We compiled records of S. horneri from herbaria, publications, government and academic groups and trained citizen scientists monitoring subtidal and intertidal reefs in California and Baja California (Supplementary material Table S1).Its presence or absence was recorded during ecological surveys by observers trained to identify the species.Because this region is extensively and regularly monitored by many trained observers, the spread of S. horneri can be described with high spatial and temporal resolution.Using these data, we present a timeline of S. horneri spread in southern California and Baja California.

Results
Since 2003 when S. horneri was first detected in Long Beach Harbor, it has spread north and south along the mainland coast and westward across several nearshore islands (Supplemental material Table S2, Figure 2).The geographic expansion of S. horneri is characterized by isolated introductions to new islands and locations on the mainland widely separated from existing populations, followed by the steady colonization of surrounding areas.
In 2005, just two years after S. horneri was first detected in Long Beach, it was found drifting on the surface 260 km south in Todos Santos Bay, Baja California, México.One year later it was confirmed to be growing on natural reefs there, and along the coast of San Diego and the leeward side of Santa Catalina Island, California.Since then it has progressively spread north in southern California and south in Baja California.By 2007, S. horneri had spread to Isla Natividad in Baja California, 500 km south of the nearest known population.In 2013, the northern range of S. horneri reached Santa Barbara, California, 186 km northwest of Long Beach.The known northern and southern limits of the range of established populations have not changed since 2013, though additional populations were recorded within the previously established range.However, individual thalli were found floating at the surface west of the current range at Santa Rosa and San Miguel Islands in 2012 and 2015 respectively, and at multiple islands near the southern end of its range in 2015.
The abundance and persistence of the recorded populations varied.Many reports consisted of only a few individuals or groups of individuals in small patches, often at sites where S. horneri had not previously been recorded.Patchy distribution continued in subsequent years at many sites, and occasionally S. horneri was recorded at a site but not found there again.However, in some areas, such as Santa Catalina and Anacapa Islands, S. horneri spread profusely and was persistent, covering large portions of reefs with adult densities > 100 m -2 and recruit densities > 1000 m -2 for multiple years (e.g. Figure 1C).

Invasive traits
Sargassum horneri has several life history characteristics that make it well adapted for colonizing distant areas and rapidly populating an area once it is established.Thalli are buoyed by gas bladders and are capable of self-fertilization, making the establishment of new populations from long-range dispersal of a single floating thallus possible.Indeed, floating S. horneri thalli have been observed frequently off southern California and Baja California and are estimated to remain afloat for several weeks before decomposing (Yatsuya 2008).Local population growth can occur quickly because S. horneri is a fast-growing (4.46% day −1 adult blade weight maximum relative growth rate; Choi et al. 2008) and highly fecund alga (up to 50% of the biomass of a mature individual is composed of reproductive tissue; L. Marks unpublished data).Furthermore, the patchy distribution and reoccurrence of dense aggregations of S. horneri in successive years (Figure 1C) may be explained by the heavy embryos of S. horneri which, like other fucoid algae, are thought to have limited capacity for dispersal.

Dispersal vectors
The distribution and rapid spread of S. horneri is likely influenced by both natural and humanmediated dispersal.Reproductive thalli can become dislodged naturally if severed from their holdfast by grazers or strong wave action and carried to new sites on ocean currents.Divers may also dislodge thalli accidentally or intentionally, inadvertently contributing to its dispersal by either freeing them to float away or transporting them elsewhere.Boaters can dislodge thalli when setting and retrieving anchors lying in S. horneripopulated areas.Sargassum horneri is also adept at growing on a variety of both natural and manmade surfaces, so vessels fouled with S. horneri may be an effective means of transporting it to new locations as suggested by Miller and Engle (2009).The current distribution of this seaweed includes many sites that are frequently visited by boaters and divers, such as harbors or anchorages, supporting the idea that S. horneri is being transported regionally by recreational and commercial vessels.

Potential for further spread
Sargassum horneri has expanded significantly further south along the eastern Pacific coast than north, spanning 6.18 and 0.76 degrees latitude from the initial detection site in Long Beach Harbor, respectively.The thermal tolerances of S. horneri may play an important role in determining range limits in the eastern Pacific.Sea surface temperatures in its native range in western Japan and southern Korea average between about 18-22 o C (Chu et al. 1998).Baja California water temperatures typically range between 14-22 o C on the Pacific coast (Zaytsev et al. 2003), so the continued expansion of S. horneri southward along this peninsula is likely.Warmer average temperatures in the Gulf of California and mainland México will likely prevent expansion beyond the peninsula.
Ocean temperatures north of Point Conception rarely exceed 18 o C, which may prevent S. horneri from spreading further north under present ocean climate conditions.However, predictions for a warmer ocean in the future may serve to increase the northward expansion of S. horneri in the eastern Pacific.

Implications of S. horneri invasion
Sargassum horneri can be locally very abundant and highly persistent.Therefore, its continued expansion in the eastern Pacific may pose a major threat to the sustainability of native marine ecosystems.Its high growth rates and long, floating thalli may provide a competitive advantage over other macrophytes.In addition, it appears to be avoided by most herbivores (Navarro 2009;Vogt 2010), possibly due to high concentrations of phenolic compounds that have been shown to deter grazing in other fucoid algae (Steinberg 1985).Mesoinvertebrates that use macroalgae as biogenic habitat and the fish that depend on these invertebrates may also be affected by the S. horneri invasion.Research investigating the interactions between S. horneri and ecologically important species is critically needed to understand how its invasion may be altering the structure and functioning of existing ecosystems of the eastern Pacific.Continued monitoring of S. horneri distribution is essential to identify environmental factors influencing its spread and prioritize management actions.Researchers and citizen scientists can contribute to this effort by reporting observations of S. horneri occurrence to an online database and map designed to help track its spread (Marine Invasive Species Tracking website 2015).

Conclusion
The range of S. horneri has expanded rapidly in the eastern Pacific since it was first detected in 2003.Its expansion to the south has been more extensive and occurred more quickly than to the north, suggesting that it may be better suited to warmer southern waters.The prevalence of S. horneri at popular boating and diving destinations suggests that its spread is the result of multiple introductions.The life history of this species allows distant areas to be colonized by a single individual, which facilitates its spread.The high abundance and persistence of S. horneri in novel areas has heightened the awareness of its invasion potential and raised concerns about its possible adverse effects on existing ecosystems.Future research aimed at determining the environmental factors affecting its spread and the ecological and economic consequences of S. horneri invasion will provide much needed insight into the cost and need for human intervention in controlling its invasion.

Figure 2 .
Figure 2. Chronology of geographic expansion of S. horneri in the southern California, USA (A) and Baja California, México (B) regions.Each dot identifies a location where S. horneri was found attached to the substrate at least once.Each map includes observations from all previous years to display the distribution of S. horneri at each interval.The California Channel Islands are identified by number as follows: 1. San Miguel, 2. Santa Rosa, 3. Santa Cruz, 4. Anacapa, 5. San Nicolas, 6.Santa Barbara, 7. Santa Catalina, 8. San Clemente.The entire study area is outlined by the dashed line.Maps were created by P. Carlson.