Range‐extending tropical herbivores increase diversity, intensity and extent of herbivory functions in temperate marine ecosystems

Abstract

Climate change is modifying species distributions around the world, forcing some species poleward, where they can alter trophic interactions. Many tropical herbivorous fishes have successfully expanded their ranges into temperate ecosystems, and while it is clear they drive increases in herbivory rates in specific localities, little is known about how they might affect the diversity of herbivory functions across large spatial scales, considering their interaction with assemblages of native herbivores in temperate habitats. We assessed the spatial overlap and habitat associations of native temperate and range‐expanding tropical herbivorous fishes in six subregions of south‐western Australia to determine how incursions of tropical species may have affected the diversity, redundancy (index of uniqueness) and the ‘spatial extent’ (addition of functions in new areas) and ‘intensity’ (increasing density of functional groups) of specific herbivory functions in recipient ecosystems. Tropical herbivores had high abundances in temperate ecosystems, forming schools from 40 (parrotfish) to 200 (rabbitfish) individuals strongly associated with seagrass meadows and reefs with high cover of turf algae. Overlap with temperate herbivores was highest in the northern subregions, forming unique assemblages, with no apparent species displacements. The addition of tropical species increased functional diversity and uniqueness (the complement of redundancy), introducing novel herbivory functions to many locations. Seagrass browsing increased in spatial extent (27%) and intensity (15×), while seaweed browsing and grazing increased in intensity by up to 2.5× in regions with high abundances of tropical herbivores. Our results suggest that the diversity, intensity and spatial extent of different herbivory functions can change as tropical species with different habitat affinities, behaviours and diets shift their distributions poleward. Changes in functional redundancy are likely to be heterogeneous in space and might not increase initially because the diversity of herbivory functions is relatively low in some temperate marine ecosystems. However, there is the potential for greater redundancy as further tropical species arrive, their abundances increase and the spatial and functional overlap of communities rises. A free Plain Language Summary can be found within the Supporting Information of this article.

A global meta‐analysis of temperature effects on marine fishes’ digestion across trophic groups

“…Our findings also have key implications concerning ongoing range expansions of herbivorous fishes, which can have transformative impacts on biogenic habitats such as kelp forests and seagrass meadows (Hyndes et al., 2016; Vergés et al., 2014, 2016, 2019; Zarco‐Perello et al., 2017, 2020). First, our results suggest that herbivorous fishes colonizing new habitats are not subject to unique thermal constraints as would be expected if low temperatures imposed a general disadvantage on plant digestion.…”

“…It has been proposed that thermal constraints drive global patterns of fish biodiversity based on the observation that the abundance and diversity of herbivorous fishes relative to all fishes decline with increasing latitude and decreasing temperature (Ferreira et al., 2004; Floeter et al., 2004, 2005; Gaines & Lubchenco, 1982; Meekan & Choat, 1997). This relationship between temperature and the distribution of herbivorous fishes is of critical interest because of herbivorous fishes’ potential to have profound impacts on community structure and ecosystem function, as shown by recent poleward expansions in the distribution of marine herbivorous fishes and the ‘tropicalization’ of marine ecosystems (Hyndes et al., 2016; Vergés et al., 2014, 2016, 2019; Zarco‐Perello et al, 2020, 2017). A commonly invoked explanation for the relative rarity of herbivorous fishes at high latitudes is the temperature constraint hypothesis, which proposes that herbivorous fishes have greater difficulty than carnivorous fishes meeting their nutritional requirements with decreasing temperature due to constraints on digestion (Ferreira et al., 2004; Floeter et al., 2004, 2005; Gaines & Lubchenco, 1982; Harmelin‐Vivien, 2002).…”

Persistence of tropical herbivores in temperate reefs constrains kelp resilience to cryptic habitats

“…A surveyor swam at a constant pace parallel to the reef crest for 15 min (~2,000 m 2 ) registering the abundance and the specific habitat where individuals of adult and juvenile herbivorous fish were encountered, completing two transects parallel to each other, ~20 m apart, per day. Fish abundance is reported as density (fish counts 2,000 m −2 ) and as the highest school sizes (MaxS; individuals per school, ind per school) found during surveys (Zarco‐Perello et al., 2020).…”

“…The abundance and diversity of herbivores in several temperate regions of the world are increasing due to the poleward range extension of tropical species as a result of the intensification of warm currents that transport tropical propagules to higher latitudes (Vergés et al., 2014). This has increased the intensity and the functional diversity of herbivory (Zarco‐Perello et al., 2020), accelerating the transformation of kelp and other macrophytes to detrital biomass (Zarco‐Perello et al., 2019). While there is no clear evidence at this point that range‐extending tropical herbivores have been the primary cause of shifts to canopy‐free states, there is clear evidence that they have increased kelp consumption, contributing to reduce kelp abundance (Bennett et al., 2015; Vergés et al., 2016; Zarco‐Perello et al., 2017) and maintenance of turf‐dominated states (Bennett et al., 2015) with predictions of further increases of consumption under future warmer conditions (Vergés et al., 2019; Zarco‐Perello et al., 2019).…”

Commentary on Osland et al.: Tropicalization of temperate ecosystems in North America: The northward range expansion of tropical organisms in response to warming winter temperatures

“…These studies would be especially key for vulnerable conservation areas, such as national parks and wildlife refuges (McClenachan et al 2020). An interesting ecosystem-level example by Zarco-Perello et al (2020) reported that tropicalization is occurring faster in marine systems than in terrestrial habitats.…”