Sublethal effects of a rapidly spreading native alga on a key herbivore

Abstract

Multiple anthropogenic stressors are causing a global decline in foundation species, including macrophytes, often resulting in the expansion of functionally different, more stressor‐tolerant macrophytes. Previously subdominant species may experience further positive demographic feedback if they are exposed to weaker plant–herbivore interactions, possibly via decreased palatability or being structurally different from the species they are replacing. However, the consequences of the spread of opportunistic macrophytes for the local distribution and life history of herbivores are unknown. The green alga, Caulerpa filiformis, previously a subdominant macrophyte on low intertidal‐shallow subtidal rock shores, is becoming locally more abundant and has spread into warmer waters across the coast of New South Wales, Australia. In this study, we measured (a) the distribution and abundance of a key consumer, the sea urchin Heliocidaris erythrogramma, across a seascape at sites where C. filiformis has become dominant, (b) performed behavioral field experiments to test the role of habitat selection in determining the local distribution of H. erythrogramma, and (c) consumer experiments to test differential palatability between previously dominant higher quality species like Ecklonia radiata and Sargassum sp. and C. filiformis and the physiological consequences of consuming it. At all sites, urchin densities were positively correlated with distance away from C. filiformis beds, and they actively moved away from beds. Feeding experiments showed that, while urchins consumed C. filiformis, sometimes in equal amounts to higher quality algae, there were strong sublethal consequences associated with C. filiformis consumption, mainly on reproductive potential (gonad size). Specifically, the gonad size of urchins that fed on C. filiformis was equivalent to that in starved urchins. There was also a tendency for urchin mortality to be greater when fed C. filiformis. Overall, strong negative effects on herbivore life‐history traits and potentially their survivorship may establish further positive feedback on C. filiformis abundance that contributes to its spread and may mediate shifts from top‐down to bottom‐up control at locations where C. filiformis has become dominant.

Marine Autotroph-Herbivore Synergies: Unravelling the Roles of Macroalgae in Marine Ecosystem Dynamics

“…In marine communities, the preference and performance of the herbivores often relate directly to the nutritional value of algae or some other autotrophs, which is driven mostly by the protein and nitrogen content [ 151 , 152 , 153 , 154 , 155 ]. For example, several studies on the high-value marine abalone (Haliotis asinine) suggested that their diverse preferences are primarily influenced by the protein and nitrogen content of macroalgae [ 156 , 157 , 158 , 159 , 160 , 161 , 162 , 163 , 164 , 165 , 166 , 167 , 168 , 169 , 170 , 171 , 172 ]. Table 3 shows some examples of studies involving the interactions between marine autotrophs and herbivores based on the herbivore nutrient acquisition since the 2010s.…”

“…The lack of preference for protein-enriched algae (i.e., high-nutrient algae) can be explained by the compensatory feeding behaviour of some herbivore species. Previous studies reported the optimal growth rate and adequate intakes of limiting nutrients by testing the consumption rates of different herbivores on the low nutritional quality of algae foods [ 39 , 43 , 164 , 165 ]. According to Bradley et al (2021), herbivores may avoid species that are less palatable or have lower nutritional value, which may affect their distribution and abundance [ 164 ].…”

“…Previous studies reported the optimal growth rate and adequate intakes of limiting nutrients by testing the consumption rates of different herbivores on the low nutritional quality of algae foods [ 39 , 43 , 164 , 165 ]. According to Bradley et al (2021), herbivores may avoid species that are less palatable or have lower nutritional value, which may affect their distribution and abundance [ 164 ]. However, the distinct nutritional drivers underlying the feeding preferences of specific marine herbivores are still a frontier that needs to be further explored.…”