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Ongoing changes in natural diversity due to anthropogenic activities can alter ecosystem functioning. Particular attention has been given to research on biodiversity loss and how those changes can affect the functioning of ecosystems, and, by extension, human welfare. Few studies, however, have addressed how increased diversity due to establishment of nonindigenous species (NIS) may affect ecosystem function in the recipient communities. Marine algae have a highly important role in sustaining nearshore marine ecosystems and are considered a significant component of marine bioinvasions. Here, we examined the patterns of respiration and light-use efficiency across macroalgal assemblages with different levels of species richness and evenness. Additionally, we compared our results between native and invaded macroalgal assemblages, using the invasive brown macroalga Sargassum muticum (Yendo) Fensholt as a model species. Results showed that the presence of the invader increased the rates of respiration and production, most likely as a result of the high biomass of the invader. This effect disappeared when S. muticum lost most of its biomass after senescence. Moreover, predictability–diversity relationships of macroalgal assemblages varied between native and invaded assemblages. Hence, the introduction of high-impact invasive species may trigger major changes in ecosystem functioning. The impact of S. muticum may be related to its greater biomass in the invaded assemblages, although species interactions and seasonality influenced the magnitude of the impact.
Natural diversity is being modified worldwide by changes such as species loss and biological invasions of NIS (Vitousek et al. 1997, Sala et al. 2000). Understanding the consequences of such changes on ecosystem functioning has become a key topic of ecological research (e.g., Worm et al. 2006, Byrnes et al. 2007, Airoldi and Bulleri 2011). The argument that biodiversity loss could lead to a reduction in global ecosystem functioning (i.e., interactions between biotic assemblages or with their abiotic environment) emerged as an issue in the early 1990s (e.g., Ehrlich and Wilson 1991, Naeem et al. 1994).
Conversely, in some systems local species richness has increased significantly due to recent establishment of NIS, although the long-term consequences of these introductions are still debated (Sax and Gaines 2003). The spread of NIS has been considered one of the strongest anthropogenic impacts on natural ecosystems by changing abiotic factors, community structure, and ecosystem properties (Mack et al. 2000, Byers 2002, Ruesink et al. 2006). Life history features of invaders may be key factors in determining the fate and the impact of invasions. For instance, invasion by canopy-forming macroalgae (e.g., Sargassum muticum, Undaria pinnatifida) may influence the structure of understory assemblages by modifying levels of light, sedimentation (Airoldi 2003) or water movement (Eckman et al. 1989). Introduced species often exhibit novel features compared to native species and may have disproportionately high impacts on native ecosystem functioning (Ruesink et al. 2006). However, positive effects linked to the presence of invasive algal hosts have also been recorded in structuring host-epiphyte association (e.g., Jones and Thornber 2010). Although the majority of the scientific studies on the biodiversity-ecosystem functioning paradigm have been done in terrestrial ecosystems (Hooper et al. 2005), recent studies have also started to investigate ecosystem consequences of biodiversity loss in marine systems (Cardinale et al. 2006, Bracken et al. 2008, Danovaro et al. 2008, Reynolds and Bruno 2012). A general theoretical framework of marine biodiversity and ecosystem functioning is well described by Boero and Bonsdorff (2007).
Primary production is the most common ecosystem process measured in species richness manipulation experiments (Hooper et al. 2005), including marine experimental approaches (e.g., Bruno et al. 2005, Griffin et al. 2009, Tait and Schiel 2011). Primary production in the ocean is an important component of global biogeochemical cycles, and transfer of energy through most food webs can be directly linked to the fixation of carbon at the primary producer level (Field et al. 1998). Primary productivity in an ecosystem is closely related to species diversity, although effects of species identity have recently been suggested as an important component of benthic marine community production (Bruno et al. 2005, 2006). The productivity–diversity relationship, however, is very complex and may present positive, negative, hump-shaped, U-shaped or nonsignificant patterns (Waide et al. 1999). Additionally, biodiversity can also influence ecosystem predictability (McGrady-Steed et al. 1997). As a result, theory predicts a reduction in the temporal or spatial variance of ecosystem properties with increasing biodiversity (Yachi and Loreau 1999, France and Duffy 2006). Although macroalgae make up a small proportion of ocean primary production, they are the dominant primary producers of rocky shore ecosystems (Mann 1973), providing an essential ecological function for aquatic life. In addition, macroalgae are considered foundation species, providing habitat that may modify abiotic and biotic processes essential to overall ecosystem function (Bruno et al. 2003, Dijkstra et al. 2012). Hence, quantifying the primary productivity of these assemblages is essential to our understanding of energetic dynamics in coastal marine systems and the factors affecting it.
Preliminary studies on photosynthesis, growth or nutrient acquisition of macroalgae have been mainly examined in laboratory experiments (Littler and Arnold 1982) using single species (see Sand-Jensen et al. 2007 for a review). More recently, several studies suggested that for a better understanding of the primary production dynamics in macroalgae, an assemblage-based approach must be considered (Binzer and Middelboe 2005, Binzer et al. 2006, Richards et al. 2011). At the assemblage level, combining species with different sizes and morphologies allows researchers to account for effects such as canopy-shading, boundary layer effects, and resource partitioning (Middelboe and Binzer 2004). In particular, canopy structure may influence assemblage production by affecting the distribution of light to photosynthetic tissues in the assemblage and consequent efficiency of light utilization (Binzer and Sand-Jensen 2002a,b). Varying functional trait composition in assemblages is known to directly regulate ecosystem processes (Díaz and Cabido 2001, McGill et al. 2006) and has been recently incorporated in biodiversity-ecosystem functioning relationships (e.g., Griffin et al. 2009, Roscher et al. 2012) rather than species richness per se. Additionally, the individual performance of species (i.e., identity effects) has been proposed to affect the magnitude of an ecosystem process in macroalgal assemblages (Arenas et al. 2009, Griffin et al. 2009), indicating a high degree of interspecific variation in macroalgal productivity (Littler and Littler 1980).
A few laboratory studies have also incorporated an assemblage perspective using natural communities (Arenas et al. 2009, Tait and Schiel 2011). Examining different components of biodiversity (e.g., biomass, richness, evenness), Arenas et al. (2009) described a positive relationship for biomass and species richness with productivity on macroalgal assemblages on small boulders bearing intertidal macroalgal assemblages. Recently, experimental studies on marine communities have analyzed photosynthesis within intact, in situ macroalgal assemblages (e.g., Miller et al. 2009, Noël et al. 2010, Tait and Schiel 2010). For example, Tait and Schiel (2010) tested for primary production in intertidal macroalgal assemblages dominated by fucoid algae and described increased primary productivity of these macroalgal assemblages with a combination of greater biomass and greater numbers of macroalgal species.
Marine coastal ecosystems are strongly affected by invasions of NIS, which together with anthropogenic disturbances can create highly altered habitats. Nonetheless, to date, there have been virtually no studies which have focused on the functional consequences of increases in species richness due to the presence of invaders in marine habitats (but see Stachowicz and Byrnes 2006). Marine macroalgae are a significant component of introduced NIS (Schaffelke et al. 2006), highlighting the importance of studies addressing interactions at this level, particularly using strong invaders, sensu Ortega and Pearson (2005).
This study aimed to investigate assemblage-level impacts of macroalgal invasions and discriminate the mechanisms promoting its impact. In particular, we intended to understand the role of a strong invader, S. muticum (Yendo) Fensholt, and assemblage structure on the dynamics of respiration and light-use efficiency of assemblages. We used synthetic assemblages of marine macroalgae, resembling those from intertidal rock pools, with varying levels of functional diversity and invader biomass. Native species with a long history of co-evolution are expected to partition resources among them and promote ecosystem functioning via resource use complementary effects. In contrast, newly introduced species probably enhance ecosystem functioning via identity effects where the influence of the invader is much greater than expected based on its relative abundance in the assemblage (Ruesink et al. 2006). Also, we expect high-diversity assemblages to enhance the predictability of respiration and light-use efficiency response of assemblages.
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This study investigated how increased diversity due to the establishment of NIS affected ecosystem functioning responses in the recipient communities. The most relevant finding was that the presence of S. muticum increased the rates of respiration and light-use efficiency of macroalgal assemblages. However, this effect was only a consequence of additional biomass and thus it disappeared when S. muticum lost most of its biomass after senescence. In addition, the increased predictability between species richness and ecosystem function found in native macroalgal assemblages disappeared in invaded assemblages.
The introduction of species with traits not found in the recipient assemblage can produce large-scale alterations of ecosystem processes and structure (Ruesink et al. 2006). In this study, S. muticum when present at elevated biomass modified respiration and light-use efficiency of assemblages. However, as a habitat modifier, S. muticum individuals may also modify a variety of other ecosystem processes (Wallentinus and Nyberg 2007). S. muticum has a high growth capacity and is known to influence assemblages by modifying levels of light (Britton-Simmons 2004, Strong et al. 2006), water movement, and temperature (Strong et al. 2006) within canopy areas. Considered an invasive species in its introduced range all around the world (Critchley et al. 1983), S. muticum varies greatly in its ability to impact native systems due to its seasonal reproduction, followed by a rapid shedding of the reproductive tissues (Arenas and Fernández 1998). In the autumn, after a substantial loss of biomass, our results suggest that S. muticum acts as a weak invader and becomes a minor component of native assemblages. In the spring, due to the elevated biomass, this species becomes dominant at the expense of native species and processes and acts as a strong invader (sensu Ortega and Pearson 2005). The different morphological forms of S. muticum individuals between seasons may have significant differences in the percentage of photosynthetic tissue, net photosynthesis, and specific growth rate, as previously demonstrated for the red alga Gracilaria tikvahiae McLachlan 1979 (Hanisak et al. 1988). Thus, these varying results between seasons are not totally unexpected, although the type of relationship may be. In a previous study using intertidal macroalgal assemblages, also in November/December, correlations with evenness were not significant for any functional variable addressed (Arenas et al. 2009), contrasting with the negative relationship found in this study. The impact of S. muticum can be related to its biomass dominance in the invaded assemblages, in agreement with the sampling effect hypothesis, i.e., the increasing probability of selecting a species with a specific property with increasing species richness (Huston 1997). It has been suggested that native species with a long history of co-evolution may influence ecosystem processes through resource use efficiency, whereas NIS effects on the recipient assemblage occurs through sampling effects (Ruesink et al. 2006).
Several studies have revealed that the effect of species diversity on ecosystem functioning depends on the system studied and the function measured (Schwartz et al. 2000, Schmid 2002, Duffy 2003). Moreover, the effects of species richness on biomass production change through time and are influenced by both selection and multispecies complementarity effects (Cardinale et al. 2007). Specifically, the role of phenology has not been thoroughly assessed in primary productivity studies, although variables such as standing biomass of the species, its functioning (e.g., the outcome of carbon assimilation, nutrient uptake), and phenology have been suggested to influence net primary productivity (Lavorel and Garnier 2002). The majority of biodiversity research manipulates species richness with few studies manipulating or measuring species evenness, i.e., the relative contribution of each species to the total biomass or number of individuals (but see Wilsey and Potvin 2000, Altieri et al. 2009, Arenas et al. 2009). Contrasting with previous results in both marine and terrestrial systems (Wilsey and Potvin 2000, Altieri et al. 2009), this study showed no positive effects of evenness on ecosystem functioning in native assemblages. Most importantly, evidence suggests that different mechanisms seem to be operating in November and May.
The productivity of macroalgal assemblages was measured as O2 production, contrasting with general production studies which usually focus on carbon or biomass accumulation (e.g., Bruno et al. 2005, Cardinale et al. 2006, Reynolds and Bruno 2012). Results from the regression models indicated an overall negative effect of evenness on the performance of macroalgal assemblages in November. Negative relationships have been observed as a result of the dominance of species with greater biomass per unit area (Mulder et al. 2004), reducing evenness and increasing productivity (Nijs and Roy 2000). In our assemblages, we observed that the species used in monocultures, such as Corallina spp. and Chrondrus crispus, remained dominant throughout the experimental period (“sampling effect” of Huston 1997), which could explain the negative relationship described in our results. No significant differences were observed between native and invaded assemblages, as the biomass of the invader was scarce. In May, however, assemblages invaded by S. muticum were characterized by greater rates of respiration and light-use efficiency. The patterns observed on respiration response function, a light autonomous process, were, however, not very clear. The amount of variance explained by species evenness in native assemblages was very low at 9%. Thus, the proportion of the response variable variability left unexplained was very high. On the other hand, no relationship has been registered between respiration and species evenness in invaded assemblages. Species interactions drive biodiversity effects (Hillebrand et al. 2008) and thus, identity effects may explain our results. According to Hillebrand et al. (2008), an increase in the ecosystem process is expected if the dominant species performs better than the mean of the community, whereas the opposite should be observed if the dominant performs below average. In particular, dominance may intensify intraspecific interactions for the dominant species, negatively influencing S. muticum performance at low evenness.
It has been suggested that the magnitude of energy transferred to seaweed from a moving water mass depends on its size and shape (Norton 1991). Accordingly, after taking into consideration the biomass of the invader, the overall results were different, revealing biomass dependent effects (Emmerson and Raffaelli 2000, Tait and Schiel 2011). After normalizing by biomass, the efficiency of macroalgal assemblages was associated with effects of species richness and evenness on light-use efficiency, suggesting that at higher diversity, species may be more effective at using resources. These results are consistent with complementarity as a mechanism linking diversity and function. Recent findings comparing productivity of subtidal turf and foliose algal assemblages describe foliose assemblages to be more productive due to their greater biomass per unit area and not because of greater production per unit biomass (Miller et al. 2009). The same trend can be described for S. muticum. Due to its longer canopy height, S. muticum is more productive on a per-area basis than on a biomass-specific basis.
Finally, in agreement with the similarity hypothesis (Yachi and Loreau 1999), the increase in species richness in native macroalgal assemblages increased the predictability of primary production across space. Contrasting results were, however, obtained for invaded assemblages, where the presence of S. muticum removed the positive relationship between species richness and ecosystem function predictability. These results suggest that invaded assemblages' dynamics are less predictable than native dynamics. Further interactions between habitat-modifying species can decrease predictability of community-level effects of an invasion, particularly if invasive species show extremely variable cycles over time (Ward and Ricciardi 2010). The consequences of invasion for the invaded communities, especially with regard to their functioning, have been rarely considered (Pfisterer et al. 2004). However, the identity of the species being added or removed and its similarity to other species are often of critical importance in determining overall effects (Mooney et al. 1995). In native assemblages, the dominant species were perennial algae such as C. crispus or Corallina spp., while the dominance of the invader varied drastically between seasons. Previous studies have demonstrated a high variability in S. muticum productivity and reproductive development between habitats (Baer and Stengel 2010) and grazing pressure (Plouguerné et al. 2006). Thus, the reduced predictability of highly diverse communities when invaded suggested by our results might be related to the very large local variability of the invader.
In conclusion, our results highlight the fact that ecosystem functioning is a function of the biotic ecosystem components (Schläpfer and Schmid 1999), which vary in different ecological contexts such as seasons. Moreover, results showed that different components of diversity, beyond species richness, may also shape the relationship between diversity and ecosystem function. In agreement with previous studies, our results also suggest that richness and evenness may not be correlated positively (Buzas and Hayek 1996, Stirling and Wilsey 2001). Specifically, the impact of S. muticum was related to its greater biomass in the invaded assemblages, although species interactions and season influenced the magnitude of the impact.