**4. Two "special topics" in benthic BEF studies**

As mentioned in the former sections, most BEF studies assess ecosystem functioning in terms of biomass production, effects on community composition or element cycling. However, there are other possible effects with important implications for the whole ecosystem. We choose two examples to illustrate this: trophic cascades and invasion success. We chose these two special topics because the former shows that slightly different levels of intraguild diversity can lead to completely opposed effects, whereas the latter illustrates that although experimental approaches meet hypotheses based on theory, they sometimes do not reflect what is actually happening in nature.

## **4.1 Trophic cascades**

Trophic species-level cascades occur when a change in predator abundance induces changes in the biomass of primary producers, due to a control of the abundance of grazers, thereby releasing lower trophic levels from grazing pressure (Polis et al., 2000). Predator diversity may reduce trophic cascades and may therefore be important for the population development of lower trophic levels and primary production. The importance of such intraguild diversity was studied by manipulating predator species richness (1, 2 or 3 species). The predator species pool consisted of several invertebrates such as hunting and web-building spiders preying on an arthropod (planthopper) assemblage inhabiting *Spartina* cordgrass (Finke & Denno, 2005). The occurrence of trophic cascades was

Integrating Different Organizational Levels in Benthic

availability may be the underlying mechanism.

should be interpreted with caution.

**approach** 

Biodiversity – Ecosystem Functioning (BEF) Studies 101

processes. To investigate the relationship between native species diversity and invasion success of exotic species, experiments were conducted on marine sessile epibenthic invertebrates of the southern rocky coasts of New England, exposed to the invasion of the colonial ascidian *Botrylloides diegensis*, native of the Pacific Ocean (Stachowicz et al., 1999, 2002). Experimental communities were composed of zero to four native species. Species richness was manipulated by transplanting juveniles or by allowing larvae to settle on 2x2 cm tiles that were (after the successful colonization) combined in a 5x5 grid (i.e., a complete plate consisted of 25 interchangeable subunits). During the course of the experiment all but the five target species were removed regularly. As a result, survival of the invasive species decreased with higher species richness, and it was hypothesized that reduced resource

Contrary to the previous example, two observational studies on natural assemblages evidenced the opposite to what had been demonstrated in controlled experiments before. A long-term (11 months) survey of sessile invertebrates on a rocky jetty on the Tasmanian coast revealed a positive relationship between colonization rates of both native and introduced species and natural species richness (Dunstan & Johnson, 2004). Similarly, in a natural riparian assemblage, the most diverse assemblages were the most invaded by exotic plants; the same patterns were evidenced by an *in situ* experiment manipulating local diversity (Levine, 2000). A possible explanation therefore could be the different niche opportunities across varying environmental gradients (Shea & Chesson, 2002). Therefore at a larger observational scale, invasion success will be higher, given that more suitable niches are available, be it for native or exotic species, whereas invasion success would negatively relate to species richness at smaller, i.e. local scales (Shea & Chesson, 2002). On a more individual basis, the specific characteristics and functions of the resident species as well as the interactions among them and with the invasive species, rather than species richness *per se* may be the determinant for the invasion success (Dunstan & Johnson, 2004). These examples show that isolated experiments can sometimes be misleading in their outcomes. Therefore a combination of field observations, and field as well as laboratory experiments would certainly be the best approach to avoid such inherent biases. As this extensive approach is often not feasible, isolated laboratory experiments

**5. Integrating species and genetic diversity in one experiment: an alternative** 

The preceding sections provided an overview of benthic experimental studies that alter either species or genotypic diversity separately. It has been argued that genetic diversity is only important in ecosystems that rely on or are dominated by one or a few key or habitat providing species, such as *Zostera marina* ecosystems (Hughes et al., 2008). However, all living organisms are hierarchically organized: genes make up genotypes, genotypes define populations and populations collectively constitute a species (Reusch & Hughes, 2006). If there is variation and heritability, as well as selection in ecologically important traits such as, e.g., growth rate or resistance to parasites, diversity at any level can have important ecological effects (Hughes et al., 2008). Moreover, it has been shown in terrestrial plant communities that genetic diversity can have direct consequences on species diversity: in a long-term experiment, genetically diverse communities reduced the rate at which species diversity declined (Booth & Grime, 2003), and genetic and species diversity maintained each

dependent on predator species richness, however the magnitude of the effect depended on whether the predators were a mixture of strict predators only, or of strict and intraguild predators combined. Higher intraguild predator richness led to antagonistic interactions among predators and dampened trophic cascades. As a consequence, it diminished herbivore suppression and therefore reduced primary productivity, indicating that predator diversity indirectly affects primary biomass production via trophic topdown control (Finke & Denno, 2005).

A similar outcome resulted from an experiment containing five species of predators, namely four carnivores (crabs, shrimp, blennies and killifish) and one omnivore (pinfish), preying on a herbivore assemblage dominated by amphipods and isopods, which in turn grazed on five species of macroalgae (Bruno & O'Connor, 2005). In an outdoor experiment, one, three or five predators were randomly assigned to mesocosms containing algae and herbivores. Predator diversity and identity had strong effects on the strength of the trophic cascade: when a generalist carnivore was present, grazers were significantly limited and algal biomass increased, whereas algal biomass decreased with increasing predator diversity, especially when the omnivorous fish was included.

Analogous to the previous examples, field observations in kelp forest ecosystems have revealed that predator diversity is negatively correlated with herbivore abundance and positively correlated with kelp density (Byrnes et al., 2006). To confirm the causality of this observation, predator richness was manipulated experimentally in kelp mesocosms. Accordingly, decreasing predator richness stimulated herbivore grazing leading to a decrease in giant kelp biomass. The underlying mechanism was not antagonistic behaviour among multiple predator species as observed in Finke & Denno (2005); instead, the herbivores changed their behaviour towards the different predators and therefore spent less time grazing.

Duffy et al. (2005) tested the effect of food chain length and trophic cascades on biomass of primary producers and consumers. In outdoor mesocosm tanks, experimental eelgrass communities were assembled in treatments of two (plants, grazers) and three (plants, grazers and predator) trophic levels. Grazer diversity was altered in the different treatments, and one omnivore predator (blue crab) was in- or excluded in order to modify the length of the trophic chain (Duffy et al., 2005). Results showed that the crabs had a strong effect on the grazers, resulting in higher algal biomass.

The results of these studies show that slight changes in predator diversity (e.g., one *versus* two species) can cascade to lower trophic levels. However, the exact outcome depends on the intraguild interactions at the predator's trophic level on one hand, and on the predatorprey response on the other. This implies that the loss of certain species at the top of the food chain can have unprecedented effects inducing fundamental changes to the whole system. In the case of seagrass and macroalgal systems, the loss of predators may induce the loss of key habitat-providing species with harmful consequences for the whole community (e.g. Estes et al., 1998).

#### **4.2 Invasion success**

Marine biological invasions are a major issue at regional and global scales. One of the major causes is the large number of transport vectors, like cargo vessels, but it has also been hypothesized that a depauperate native flora and fauna may facilitate the invasion success of exotic species (Elton, 1958). Non-native species can be a threat to regional biota due to competitive advantage, with uncontrollable consequences for the functioning of ecological

dependent on predator species richness, however the magnitude of the effect depended on whether the predators were a mixture of strict predators only, or of strict and intraguild predators combined. Higher intraguild predator richness led to antagonistic interactions among predators and dampened trophic cascades. As a consequence, it diminished herbivore suppression and therefore reduced primary productivity, indicating that predator diversity indirectly affects primary biomass production via trophic top-

A similar outcome resulted from an experiment containing five species of predators, namely four carnivores (crabs, shrimp, blennies and killifish) and one omnivore (pinfish), preying on a herbivore assemblage dominated by amphipods and isopods, which in turn grazed on five species of macroalgae (Bruno & O'Connor, 2005). In an outdoor experiment, one, three or five predators were randomly assigned to mesocosms containing algae and herbivores. Predator diversity and identity had strong effects on the strength of the trophic cascade: when a generalist carnivore was present, grazers were significantly limited and algal biomass increased, whereas algal biomass decreased with increasing predator diversity,

Analogous to the previous examples, field observations in kelp forest ecosystems have revealed that predator diversity is negatively correlated with herbivore abundance and positively correlated with kelp density (Byrnes et al., 2006). To confirm the causality of this observation, predator richness was manipulated experimentally in kelp mesocosms. Accordingly, decreasing predator richness stimulated herbivore grazing leading to a decrease in giant kelp biomass. The underlying mechanism was not antagonistic behaviour among multiple predator species as observed in Finke & Denno (2005); instead, the herbivores changed their behaviour towards the different predators and therefore

Duffy et al. (2005) tested the effect of food chain length and trophic cascades on biomass of primary producers and consumers. In outdoor mesocosm tanks, experimental eelgrass communities were assembled in treatments of two (plants, grazers) and three (plants, grazers and predator) trophic levels. Grazer diversity was altered in the different treatments, and one omnivore predator (blue crab) was in- or excluded in order to modify the length of the trophic chain (Duffy et al., 2005). Results showed that the crabs had a

The results of these studies show that slight changes in predator diversity (e.g., one *versus* two species) can cascade to lower trophic levels. However, the exact outcome depends on the intraguild interactions at the predator's trophic level on one hand, and on the predatorprey response on the other. This implies that the loss of certain species at the top of the food chain can have unprecedented effects inducing fundamental changes to the whole system. In the case of seagrass and macroalgal systems, the loss of predators may induce the loss of key habitat-providing species with harmful consequences for the whole community (e.g.

Marine biological invasions are a major issue at regional and global scales. One of the major causes is the large number of transport vectors, like cargo vessels, but it has also been hypothesized that a depauperate native flora and fauna may facilitate the invasion success of exotic species (Elton, 1958). Non-native species can be a threat to regional biota due to competitive advantage, with uncontrollable consequences for the functioning of ecological

down control (Finke & Denno, 2005).

spent less time grazing.

Estes et al., 1998).

**4.2 Invasion success** 

especially when the omnivorous fish was included.

strong effect on the grazers, resulting in higher algal biomass.

processes. To investigate the relationship between native species diversity and invasion success of exotic species, experiments were conducted on marine sessile epibenthic invertebrates of the southern rocky coasts of New England, exposed to the invasion of the colonial ascidian *Botrylloides diegensis*, native of the Pacific Ocean (Stachowicz et al., 1999, 2002). Experimental communities were composed of zero to four native species. Species richness was manipulated by transplanting juveniles or by allowing larvae to settle on 2x2 cm tiles that were (after the successful colonization) combined in a 5x5 grid (i.e., a complete plate consisted of 25 interchangeable subunits). During the course of the experiment all but the five target species were removed regularly. As a result, survival of the invasive species decreased with higher species richness, and it was hypothesized that reduced resource availability may be the underlying mechanism.

Contrary to the previous example, two observational studies on natural assemblages evidenced the opposite to what had been demonstrated in controlled experiments before. A long-term (11 months) survey of sessile invertebrates on a rocky jetty on the Tasmanian coast revealed a positive relationship between colonization rates of both native and introduced species and natural species richness (Dunstan & Johnson, 2004). Similarly, in a natural riparian assemblage, the most diverse assemblages were the most invaded by exotic plants; the same patterns were evidenced by an *in situ* experiment manipulating local diversity (Levine, 2000). A possible explanation therefore could be the different niche opportunities across varying environmental gradients (Shea & Chesson, 2002). Therefore at a larger observational scale, invasion success will be higher, given that more suitable niches are available, be it for native or exotic species, whereas invasion success would negatively relate to species richness at smaller, i.e. local scales (Shea & Chesson, 2002). On a more individual basis, the specific characteristics and functions of the resident species as well as the interactions among them and with the invasive species, rather than species richness *per se* may be the determinant for the invasion success (Dunstan & Johnson, 2004). These examples show that isolated experiments can sometimes be misleading in their outcomes. Therefore a combination of field observations, and field as well as laboratory experiments would certainly be the best approach to avoid such inherent biases. As this extensive approach is often not feasible, isolated laboratory experiments should be interpreted with caution.
