Native generalist herbivores promote invasion of a chemically defended seaweed via refuge‐mediated apparent competition

Enge, Swantje; Nylund, Göran M.; Pavia, Henrik

doi:10.1111/ele.12072

Cited by 36 publications

(38 citation statements)

References 52 publications

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“…As predicted by theory (Holt and Lawton 1993), apparent competition between native and invasive taxa mediated by herbivores appears to be a common phenomenon in natural ecosystems (e.g., Orrock et al 2008, Enge et al 2013. A search of Web of Science using "apparent," "competition," "inva*" or "exotic," and "plant" as keywords yielded 20 publications that evaluated the indirect effects of invasive plants on co-occurring native plants through apparent competition (Appendix S2: Table S1).…”

Section: Discussionmentioning

confidence: 94%

“…Both theory (Holt 1977, Holt andLawton 1993) and empirical data provide compelling evidence that apparent competition is as important as resource-based competition in structuring ecological communities (e.g., Bonsall and Hassell 1997, Chaneton and Bonsall 2000, Morris et al 2004). Apparent competition is an underappreciated but likely important mechanism that may facilitate species invasions (White et al 2006, Borer et al 2007, Enge et al 2013. For example, apparent competition mediated by viral pathogens has been suggested to drive the invasion of California grasslands by competitively inferior introduced annual grasses (Borer et al 2007).…”

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confidence: 99%

“…For example, apparent competition mediated by viral pathogens has been suggested to drive the invasion of California grasslands by competitively inferior introduced annual grasses (Borer et al 2007). Refuge-mediated apparent competition has recently been proposed as one of the mechanisms for plant invasions (Orrock et al 2010, Enge et al 2013. The taller and denser structures of invasive plants are hypothesized to increase the abundance of natural enemies by providing refuge that ultimately causes greater negative impacts on the fitness of neighboring native plants.…”

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confidence: 99%

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Geographic variation in apparent competition between native and invasive Phragmites australis

Bhattarai

Meyerson

Cronin

2017

Ecology

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Apparent competition, the negative interaction between species mediated by shared natural enemies, is thought to play an important role in shaping the structure and dynamics of natural communities. However, its importance in driving species invasions, and whether the strength of this indirect interaction varies across the latitudinal range of the invasion, has not been fully explored. We performed replicated field experiments at four sites spanning 900 km along the Atlantic Coast of the United States to assess the presence and strength of apparent competition between sympatric native and invasive lineages of Phragmites australis. Four herbivore guilds were considered: stem-feeders, leaf-miners, leaf-chewers and aphids. We also tested the hypothesis that the strength of this interaction declines with increasing latitude. Within each site, native and invasive plants of P. australis were cross-transplanted between co-occurring native and invasive patches in the same marsh habitat and herbivore damage was evaluated at the end of the growing season. Apparent competition was evident for both lineages and involved all but the leaf-chewer guild. For native plants, total aphids per plant was 296% higher and the incidence of stem-feeding and leaf-mining herbivores was 34% and 221% higher, respectively, when transplanted into invasive than native patches. These data suggest that invasive P. australis has a negative effect on native P. australis via apparent competition. Averaged among herbivore types, the indirect effects of the invasive lineage on the native lineage was 57% higher than the reverse situation, suggesting that apparent competition was asymmetric. We also found that the strength of apparent competition acting against the native lineage was comparable to the benefits to the invasive lineage from enemy release (i.e., proportionately lower mean herbivory of the invasive relative to the native taxa). Finally, we found the first evidence that the strength of apparent competition acting against the native lineage (from stem-feeders only) decreased with increasing latitude. These results suggest that not only could apparent competition be of tantamount importance to enemy release in enhancing the establishment and spread of invasive taxa, but also that these indirect and direct herbivore effects could vary over the invasion range.

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Section: Discussionmentioning

confidence: 94%

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confidence: 99%

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confidence: 99%

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Geographic variation in apparent competition between native and invasive Phragmites australis

Bhattarai

Meyerson

Cronin

2017

Ecology

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“…). They are important members of seaweed assemblages as they can affect ecological processes such as recruitment potential, biofouling, and fish behaviour (Enge, Nylund & Pavia ; Wright et al . ).…”

Section: Discussionmentioning

confidence: 99%

Invasive seaweeds transform habitat structure and increase biodiversity of associated species

et al. 2017

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Summary The visual landscape of marine and terrestrial systems is changing as a result of anthropogenic factors. Often these shifts involve introduced species that are morphologically dissimilar to native species, creating a unique biogenic structure and habitat for associated species within the landscape. While community‐level changes as a result of introduced species have been documented in both terrestrial and marine systems, it is still unclear how long‐term shifts in species composition will affect habitat complexity or its potential to influence the biodiversity of species that occur at the base of the food web. We analysed quadrat photos collected at several subtidal sites in the Gulf of Maine over a 30+ year period, and collected individual seaweed species to determine their complexity and the biodiversity of meso‐invertebrates associated with each species. By coupling the relationship of 30+ years of shifts in seaweed assemblages, morphological structure of the seaweed assemblage, and their meso‐invertebrates, we determined introduced seaweeds have increased by up to 90%, corresponding to a rise in two‐dimensional (2D) structure, and a decline in canopy height of subtidal rocky habitats. The highly complex two‐dimensional habitat provided by introduced filamentous red seaweeds supports two to three times more meso‐invertebrate individuals and species that form the base of the food web than simpler forms of morphological habitat. Synthesis. The present study demonstrates a long‐term shift in foundation species towards a dominance of invasive seaweeds that directly reduce canopy height and increase the 2D biogenic structure of the habitat. These introduced seaweeds harbour greater biodiversity of species found at the base of the food web than seaweeds with simpler forms such as the native kelp species. Such shifts in habitat structure will propagate to food webs by influencing the structure of lower trophic‐level meso‐invertebrates and indirectly upper trophic‐level species that feed on these invertebrates and use the seaweed structure as refuge.

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“…The success of the invasive red seaweed Bonnemaisonia hamifera has been attributed to the presence of a defence metabolite that is evolutionarily new to the local generalist herbivores (Enge et al . ) and to refuge‐mediated apparent competition (Enge, Nylund & Pavia ). G. vermiculophylla is known to defend itself against feeding via the up‐regulation of defence metabolites (Nylund et al .…”

Section: Discussionmentioning

confidence: 99%

Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed

et al. 2016

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Summary Rapid adaptation to novel biotic interactions and abiotic factors in introduced ranges can be critical to invasion success of both exotic terrestrial and aquatic plants. Seaweeds are extremely successful biological invaders in marine environments. Along with herbivores, foulers − ubiquitous enemies in the marine environment − have the potential to determine the success or failure of invasive seaweeds. However, research on the topic of rapid adaptation of seaweeds to biotic challenges is still in its nascent stages and rapid adaptation of seaweeds to fouling is unexplored. We tested whether the impressive invasion success of the red macroalga Gracilaria vermiculophylla may be enhanced by the rapid adaptation of chemical control (defence) of new bacterial epibionts in the invaded range. The native and invasive G. vermiculophylla populations investigated were equally well defended against currently co‐occurring bacterial epibionts isolated from their respective ranges. In contrast, the native populations were weakly defended against bacterial epibionts from the invaded range, whereas the invasive populations were weakly defended against bacterial epibionts from their native range. Apparently during the invasion process, invasive populations have adapted their control capacity to cope with the new epibionts but have lost the capacity to fend off old epibionts. Synthesis. These results provide the first evidence that a change in habitat and, thus, confrontation by new enemies, may trigger rapid defence adaptation of seaweeds, which could be necessary for invasiveness. Such adaptation dynamics as found in the current study could be also applicable to other types of host plant – enemy interaction e.g. plant root – microbe interactions, freshwater plant – fouler interactions in general and for cases of shifting plant – enemy interactions in course of climate change.

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Native generalist herbivores promote invasion of a chemically defended seaweed via refuge‐mediated apparent competition

Cited by 36 publications

References 52 publications

Geographic variation in apparent competition between native and invasive Phragmites australis

Geographic variation in apparent competition between native and invasive Phragmites australis

Invasive seaweeds transform habitat structure and increase biodiversity of associated species

Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed

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