An exotic chemical weapon explains low herbivore damage in an invasive alga

Abstract

Invasion success of introduced species is often attributed to a lack of natural enemies as stated by the enemy release hypothesis (ERH). The ERH intuitively makes sense for specialized enemies, but it is less evident why invaders in their new area escape attacks by generalist enemies. A recent hypothesis explains low herbivore damage on invasive plants with plant defense chemicals that are evolutionarily novel to native herbivores. Support for this novel weapon hypothesis (NWH) is so far based on circumstantial evidence. To corroborate the NWH, there is a need for direct evidence through explicit characterizations of the novel chemicals and their effects on native consumers. This study evaluated the NWH using the highly invasive red alga Bonnemaisonia hamifera. In pairwise feeding experiments, preferences between B. hamifera and native competitors were assessed for four common generalist herbivores in the invaded area. Through a bioassay-guided fractionation, we identified the deterrent compound and verified its effect in an experiment with the synthesized compound at natural concentrations. The results showed that native herbivores strongly preferred native algae to B. hamifera. The resistance against herbivores could be tracked down to the algal metabolite 1,1,3,3-tetrabromo-2-heptanone, a compound not known from native algae in the invaded area. The importance of the chemical defense was further underlined by the feeding preference of herbivores for individuals with a depleted content of 1,1,3,3-tetrabromo-2-heptanone. This study thus provides the first conclusive example of a highly successful invader where low consumption in the new range can be directly attributed to a specific chemical defense against evolutionarily naive native generalists. In conclusion, our results support the notion that novel chemical weapons against naive herbivores can provide a mechanistic explanation for plant invasion success.

Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed

“…Thus, Galaxaura produces different chemical defences to combat competitors versus herbivores. Some seaweeds and sponges produce a single molecule or suite of molecules that serve as a broad-spectrum defence [7,8,16], and this defence strategy has allowed certain seaweeds to invade new ecosystems because a single defence makes them both competitively superior and resistant to herbivores [46,47]. However, Galaxaura produces different compounds to combat different types of natural enemies, a phenomenon better described among terrestrial plants (e.g.…”

Reconstructing a herbivore’s diet using a novel rbcL DNA mini-barcode for plants

“…There are multiple hypotheses for invasive species success that rely on preferential consumption of native plant species. For example, the enemy-release hypothesis (Keane and Crawley, 2002) proposes that native species have the full complement of natural enemies (herbivores), but invasive species do not; likewise the novel defense hypothesis postulates exotic plants offer novel, and therefore more effective, plant defenses against herbivores (Enge et al 2012; Macel et al 2014). Deer are known to feed selectively on forest plants (Rooney 2001), but direct observation of deer behaviour is difficult and recent experiments have instead used a common garden approach to determine preference (Averill et al 2016).…”

Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatibility

“…It seems likely that these or other substances also act as feeding deterrents against L. brevicula and L. littorea. In a study with the invasive red alga Bonnemaisonia hamifera, Enge et al (2012) were able to show that low consumption in the new range of the seaweed can be directly attributed to a specific chemical defense against native generalists that did not encounter this type of chemical defense before. They conclude that novel chemical weapons against naive herbivores might provide a mechanistic explanation for algal invasion success.…”