Non-indigenous species (NIS) represent a major concern to marine scientists as the ecosystem in which they arrive in is modified adversely. This change takes place through the ecological interactions they establish with the native species and through direct or indirect physical or chemical changes in the habitat itself. The speed of habitat change is also coupled to the stability or resilience of the ecosystem, so the impact can have different scales in space and time [1] .

While experimental work supports the idea that diverse communities show greater resistance to invasion, it is not clear if this results from resource use complementarity, or from an increasing occurrence of suppressive species in more diverse communities [2] . To understand the mechanisms driving this response, interest has shifted from species richness to the functional roles that species or groups of species play. Functional groups are defined as non-phylogenetic grouping of species that perform similarly in an ecosystem based on a set of common biological attributes. Functional groups can be defined in relation to either the contribution of species to ecosystem processes, such as carbon or water cycling, or the response of species to changes in environmental variables, such as climatic variables or disturbance [3] . The number and identity of functional groups within a community may dictate the level of invasibility, implying that the invasion of a coastal habitat will only be promoted through loss of a whole functional group rather than the loss of one or a few members of that group [2] .

As marine ecosystems are relatively open, with fewer limits than terrestrial systems to organism dispersal and energy flow, the irreversible impacts of exotic species have profound consequences on ecological systems [2] . Macroalgae are considered to be especially worrying NIMS (non-indigenous marine species) as they may alter eco- system structure and function by monopolizing space, developing into ecosystem engineers, changing food webs, and spreading beyond their initial point of introduction through efficient dispersal capacities [4] [5] . The success of a non-indigenous species depends on its mode of reproduction, growth rate and dispersive potential [6] [7] .

The fucoid genus Sargassum is monoecious, highly fecund, and possesses vesicles that allow the reproductive fronds produced annually to drift with currents and inoculate new locations [7] - [9] . Due to its ability to colonize hard and soft substrata, the total area of marine sediments open to occupation by members of the genus Sargassum is vast, and cumulative habitat modification could be very significant [10] . The main barrier to colonization of the rock is the presence of algal cover [11] .

Once established, these species can accumulate high biomass and thus become a strong competitor for space and light [12] . Sargassum invasions have significantly impacted the structure of indigenous algal communities in North America and Europe, through competitive displacement and/or exclusion [7] [13] . Several studies have reported the reduction of functional groups, like the thick leathery and coarsely branched algae and native understory algae through strong competitive interactions with adult individuals of S. muticum [7] [14] - [17] .

Sargassum horneri is native from Asia, and distributed in Japan, Korea, Hong Kong (China), Chinese Taipei and China Mainland [18] . It was observed in Catalina Island, California, in 2003 [19] . In Baja California, well- established populations of this species were observed in Todos Santos Bay in 2007 [20] , from where it had extended along the temperate waters of the Baja California Peninsula [21] . However, no description exists of the population structure of S. horneri in Mexican waters. For this reason, we decided to study the annual growth cycle inside the Todos Santos bay. We were also interested in assessing the ecological impact of this non-indi- genous algal species on the structure of the local community of macroalgae. For this purpose, we selected two locations that differed in substrate type and wave exposure degree, and measured the seasonal influence of Sea Surface Temperature (SST), Photosynthetically Active Radiation (PAR), and air-exposure hours, on S. horneri density and biomass. Simultaneously, we determined the changes in the species composition, density, and biomass of the local macroalgae community. Algal species were classified into functional groups to identify if their number and types differed as a function of the presence or absence of S. horneri. We expected S. horneri to be better represented in the most exposed site, where its high density and biomass would result in a significant reduction of macroalgae, density, and biomass, and a change in species composition. We anticipated the loss or reduction of the canopy forming species, representing the more morphologically complex functional forms.

Following the annual cycle of maximum values during summer, and minimum values during winter, surface water temperature varied between 15.5˚C and 21.1˚C, and irradiance between 22.8 and 55.2 mol∙m⁻²∙d⁻¹. Air exposure hours varied by one order of magnitude between sites, with a total of 77 ± 0.5 hours at RB, and 685 ± 53 hours at RP. Winter was the season with more exposure hours at RB, and spring had the highest number of exposure hours at RP.

We found highly significant differences in annual mean S. horneri density and biomass between sites (P < 0.001), but not between tidal depths at any site (P > 0.05), and only at RP there were significant differences between sampled seasons (P < 0.05). At RB the invasive alga was present during October, November, and March, with an irregular distribution along the sampled depths. Its average density was 2 ± 0.94 individual m⁻², and average biomass, 4 ± 0.95 g DW m⁻². At RP, S. horneri was present during all sampled months, except June, but because of bad weather we could not collect samples in April. Also at this site, S. horneri vertical distribution was irregular. Average density was 10 ± 0.96 individual m⁻², with the lowest value during summer, 4 ± 0.9 individual m⁻², and the highest during autumn, 17 ± 0.98 individual m⁻². Average biomass for all the study period at RP was 102 ± 0.97 g DW m⁻², with the lowest values in summer, 12 ± 0.96 g DW m⁻², and the highest in spring, 292 ± 0.98 g DW m⁻².

At RB there were no significant correlations between S. horneri density and biomass with the environmental variables, but at RP, S. horneri density and biomass were negatively correlated with SST: (r = −0.34, P < 0.001), and (r = −0.53, P < 0.001) respectively; biomass was also negatively correlated with PAR (r = −0.25, P < 0.05). Air exposure hours yield no significant correlations with the biological data set either at RB or at RP.

Our results show that there are important site differences in the presence of S. horneri inside the Todos Santos bay and its effects on the macroalgae community. At Rincón de Ballenas, the invasive alga was not present all year round, and had low density and biomass values. However, its presence resulted in a significant reduction in the macroalgae density, biomass, species richness and diversity. The corticated macrophytes and the foliose functional forms were severely reduced by the presence of the invasive alga. On the other hand, at Rancho Packard, the presence of S. horneri was more continuous throughout the year, and this non-indigenous species reached high density and biomass values. Despite this, there only were marginally significant effects of its presence on the local macroalgae community, and higher density, biomass, and diversity values were found when S. horneri was present. Most of the functional forms were represented, even when S. horneri was present. Despite these notorious site differences, at both locations, the highest biomass corresponded to the articulated calcareous functional form.

With respect to sites differences, we know that RB is characterized by reduced wave exposure and soft sediment, represented by loose gravel. In contrast, at RP, wave exposure is slightly higher and the substrate is represented by solid rock. Although S. horneri has the rare ability to colonize both, hard and soft substrate [10] , our data indicate that at the Todos Santos bay, S. horneri grows better on hard substrate. This is in agreement with [7] , whoat Limfjorden, Denmark, found a strong correlation between the cover of S. muticum and the presence of hard substrate. Although we did not find significant differences with depth, [7] , found that the difference in cover between shallow, 0 - 2 m, and deep, 2 - 6 m, waters, was regulated by the amount of hard substrate.

Water movement has been considered a seasonally important variable which affects standing biomass, thallus size, morphology and, possibly, fertility [36] [37] . Although we did not made direct measurements of water movement, [29] used numerical simulation models to predict ocean surface waves inside the Todos Santos bay, and results of her study show a higher wave energy at RP, where we found the healthier populations of S. horneri. However, in Obama bay, Japan, [38] found that the S. horneri populations from the sheltered coast had longer primary laterals, and plants had higher weight, than those from the exposed shore. In situ measurements of wave exposure are needed at Todos Santos bay, to determine if our two study sites can be considered to be in a protected shore. For the northern coast of Spain [9] , found that wave exposure was not significant for S. muticum growth and survivorship. In contrast, [39] , for the foliose algae of South Wales, and [37] , for the populations of S. polyceratium in Curaçao, found that foliose algae were more abundant where wave-action was greater and during the cooler months of the year.

Reference [39] also found that algal survival was greater and growth was faster under conditions of increased moisture, decreased emersion, and decreased temperatures and light regimes during low tide. However, in our study we could not find a significant correlation between S. horneri density and biomass with tidal exposure, despite the high number of exposure hours at RP. The fact that S. horneri grows at the high intertidal at RP (Figure 2), and that at this site exposure hours were greater during spring, could help explain the negative correlation between density and biomass with water temperature and irradiance, in agreement with [39] . The negative correlation between these two biological variables with irradiance could also be due to a high epiphyte load, as found by [40] for three species of Sargassum in Hawaii. The negative correlation with water temperature is in agreement with [38] [41] [42] , among others, and is characteristic of temperate species.

The ephemeral nature of the individual patches of S. horneri at RB, could be understood using the physical and biological arguments that have been presented to explain the colonization and establishment patterns of the genus Sargassum: anomalously warm sea water temperatures and their subsequent effects on food web in the region [43] ; the disturbance represented by the presence of sand and its negative impact on recruits survival [16] ; the unsuitability of smaller stones, gravel and sand, as substrate for grown specimens [7] , and highly localized propagule dispersal and settlement [44] . For Gracillaria verrucosa, [45] found than an exponential decline in settlement densities and short dispersal distances was partly due to the diffusive environment found in the shallow subtidal.

The strong seasonality that characterizes the genus Sargassum has been mainly attributed to sea water temperature, and photoperiod, with regional variations due to latitudinal gradients [43] [46] - [48] . “Autumn-fruiting type” and “spring-fruiting type” populations of S. horneri have been described for the Seto Inland Sea, Japan by [47] . For both populations it has been considered that the shortening of day length around the autumn equinox, is the possible cue to start the growth phase, characterized by the rapid increase in thallus length. Simultaneously, water temperature starts its autumn reduction [47] . However, it is now considered that the difference in seasonality between these two populations does not reflect a phenotypic plasticity, but a genotypic difference [42] .

The lifetime of the autumn-fruiting type is considered to have four phases, according to the rates of increase in length and morphogenetic stages: I―formation of early leaves, from December to May; II―differentiation of stems, from May to September; III―rapid elongation of stems and lateral branches, from September to December; IV―senescence phase, after December. In contrast, the spring-fruiting type has two growth phases and a senescence phase: I―from April to September; II―September to March, and III―senescence phase after March [47] . The selected populations of S. horneri at Todos Santos bay, corresponds to the spring-fruiting type, like the Japanese populations described by [38] , and [47] for the Seto Inland Sea, and the populations of S. filicinum, now S. horneri, at Long Beach Harbor [19] , and the California Channel Islands [49] . The sampled populations in Todos Santos bay show the lowest density and biomass values, when compared to reported values for S. horneri (Table 3).

When we analyzed the effects of the presence of the invasive alga on the local macroalgae community, we were surprised by the fact that at RB, where S. horneri was only present a few months and, showed low density and biomass values, there were significant differences between the macroalgae community structure when S. horneri was present versus when it was absent. The presence of the invasive algae resulted in significant reductions in macroalgae density, biomass, S and. On the other hand, at RP, where S. horneri had a more continuous presence throughout the year, and reached higher density and biomass values, the comparison between the macroalgae community structure under the presence and absence conditions was only marginally significant. The macroalgae showed higher density, biomass, and when S. horneri was present.

It seems that the macroalgae community at RB was more susceptible to invasion, than the one at RP. To understand the invasion process, it is necessary to analyze the number and identity of the functional groups present [2] . At RB there was a loss of functional diversity, with most of the species belonging to the foliose and corticated macrophytes functional groups being present only when S. horneri was absent (Table 1), while at RP, most of the species, and functional forms, remained when the non-indigenous alga was present (Table 2).

As indicated by [7] , during an invasion process, the community structure is affected by the increasing abundance of the invasive alga, and by the changes in the remaining community. After the invasion of S. muticum in Limfjorden, Denmark, [7] found that members of the coarsely branched and thick leathery algae tended to decrease consistently over time, as a result of competition. Reference [2] found that canopy species, regardless of their density, suppressed invader biomass, while crustose species promoted invasibility. Turf and subcanopy species effects were similar to those of the canopy species, but less intense [2] . Competitive suppression is mainly due to light competition [17] [51] [52] with space competition becoming important in a later stage [52] .

At RB, only two species belonging to the leathery macrophyte functional form (canopy) were present, with most of the corticated macrophytes (subcanopy), and all of the foliose (turf), being gone when S. horneri was present. In contrast, at RP, the macroalgae community seems to stand well the presence and abundance of the non-indigenous alga, as most species, and most functional forms remained present, regardless of the presence of S. horneri. It is important to note that what we refer to as the local macroalgal community has already being modified, as we found S. muticum at both sites. S. muticum persist under presence or absence of S. horneri, so no competition seems to exist between these two species, but this needs to be assessed in the field.

The already altered macroalgae communities we found inside the Todos Santos bay, are dominated by the articulated calcareous, functional form with the highest biomass at both sites (Figure 4 and Figure 6). This functional form corresponds to what [2] refer to as turf-forming species, which are recognized for being primary space-holders with limited vertical height (usually ~5 cm length). Algal turf has the ability to monopolize space and persist under a wide range of environmental conditions, and its thickness, rather than its cover, seems to be the most affected by the intensity of disturbance and smothering by sediments [53] . The rapid growth of turf- dominated assemblages provides its capability to compete for space and recover from disturbance [54] .

Our results do not fully support our hypothesis. As in RP, where the highest density and biomass values of S. horneri were found, there was not the significant reduction in macroalgae density, biomass, S and we expected; on the contrary, density, biomass, and showed higher values when the non-indigenous alga was present (Figure 5). This unexpected result could be due to the fact that the native community had already been altered by the early invasion of S. muticum, with the most resilient species and functional forms remaining in place. One of the most important changes we noticed is the severe reduction of the canopy forming species at both sites, confirming the fact that the local macroalgae community has already been modified, in agreement with [7] . A long-term monitoring, with more study sites, is needed to fully comprehend the changes that the local macroalgae communities are experiencing along the Baja California peninsula.

The National Science and Technology Council of Mexico (CONACYT) provided a Master of Science scholarship to G. I. Cruz-Trejo. E. Gil (IIO-UABC) did the topographic work. L. E. Ángeles-Gónzalez, and C. Cabrera (CICESE) helped with data analyses. F. Ponce (CICESE) did the figures. The research was funded with CICESE’s internal funding.

Giuliana I. Cruz-Trejo,1 1,Silvia E. Ibarra-Obando,Luis E. Aguilar-Rosas,Miriam Poumian-Tapia,Elena Solana-Arellano, (2015) Presence of Sargassum horneri at Todos Santos Bay, Baja California, Mexico: Its Effects on the Local Macroalgae Community. American Journal of Plant Sciences,06,2693-2707. doi: 10.4236/ajps.2015.617271