Response of fishes to algae reduction on Glovers Reef, Belize

PLoS One, 2010

Background: Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.

Turf algae are multispecies communities of small marine macrophytes that are becoming a dominant component of coral reef communities around the world. To assess the impact of turf algae on corals, we investigated the effects of increased nutrients (eutrophication) on the interaction between the Caribbean coral Montastraea annularis and turf algae at their growth boundary. We also assessed whether herbivores are capable of reducing the abundance of turf algae at coral-algae boundaries. We found that turf algae cause visible (overgrowth) and invisible negative effects (reduced fitness) on neighbouring corals. Corals can overgrow neighbouring turf algae very slowly (at a rate of 0.12 mm 3 wk 21 ) at ambient nutrient concentrations, but turf algae overgrew corals (at a rate of 0.34 mm 3 wk 21 ) when nutrients were experimentally increased. Exclusion of herbivores had no measurable effect on the rate turf algae overgrew corals. We also used PAM fluorometry (a common approach for measuring of a colony's ''fitness'') to detect the effects of turf algae on the photophysiology of neighboring corals. Turf algae always reduced the effective photochemical efficiency of neighbouring corals, regardless of nutrient and/or herbivore conditions. The findings that herbivores are not capable of controlling the abundance of turf algae and that nutrient enrichment gives turf algae an overall competitive advantage over corals together have serious implications for the health of Caribbean coral reef systems. At ambient nutrient levels, traditional conservation measures aimed at reversing coral-to-algae phase shifts by reducing algal abundance (i.e., increasing herbivore populations by establishing Marine Protected Areas or tightening fishing regulations) will not necessarily reduce the negative impact of turf algae on local coral communities. Because turf algae have become the most abundant benthic group on Curaçao (and likely elsewhere in the Caribbean), new conservation strategies are required to mitigate their negative impact on coral communities. Citation: Vermeij MJA, van Moorselaar I, Engelhard S, Hö rnlein C, Vonk SM, et al. (2010) The Effects of Nutrient Enrichment and Herbivore Abundance on the Ability of Turf Algae to Overgrow Coral in the Caribbean. PLoS ONE 5(12): e14312.

Blooms of alien invasive marine algae have become common, greatly altering the health and stability of nearshore marine ecosystems. Concurrently, herbivorous fishes have been severely overfished in many locations worldwide, contributing to increases in macroalgal cover. We used a multi-pronged, interdisciplinary approach to test if higher biomass of herbivorous fishes inside a no-take marine reserve makes this area more resistant to invasive algal overgrowth. Over a two year time period, we (1) compared fish biomass and algal cover between two fished and one unfished patch reef in Hawai'i, (2) used acoustic telemetry to determine fidelity of herbivorous fishes to the unfished reef, and (3) used metabarcoding and next-generation sequencing to determine diet composition of herbivorous fishes. Herbivore fish biomass was significantly higher in the marine reserve compared to adjacent fished reefs, whereas invasive algal cover differed by species. Herbivorous fish movements were largely confined to the unfished patch reef where they were captured. Diet analysis indicated that the consumption of invasive algae varied among fish species, with a high prevalence of comparatively rare native algal species. Together these findings demonstrate that the contribution of herbivores to coral reef resilience, via resistance to invasive algae invasion, is complex and species-specific. Herbivorous fishes and sea urchins are primarily responsible for the high grazing intensity found in healthy coral reef ecosystems 1–3. This intense grazing pressure has a large influence on the distribution of algae on coral reefs, with macroalgae generally rare in reef zones with the highest grazing pressure 2,4,5. Although there has been some debate regarding the mechanisms and causality of competition between algae and corals 6 high algal biomass has been shown to have a negative effect on coral health 7–9. Based on their role in algal removal, herbivorous fishes are considered to promote reef resilience and assist in reef recovery to coral dominated states after a disturbance 10–12. Over the past several decades, blooms of both indigenous and introduced marine algae have become common on coral reefs, greatly altering the health and stability of nearshore ecosystems 10,13. On reefs subjected to anthropogenic disturbances such as increased terrestrial nutrient inputs or the removal of grazers by overfishing, algal growth rates may exceed grazing rates, resulting in overgrowth of hard corals and other non-mobile ben-thic invertebrates, and suppression of coral recruitment 14–16. Herbivorous fishes, particularly large parrotfishes and surgeonfishes, have been severely overfished in many locations/regions and reduction in these grazers has been thought to contribute to increases in macroalgae and subsequent decreases in coral cover 17–19. Introduced species of macroalgae are often not subject to ecological controls that normally limit abundance in their native range, such as high grazing pressure from native herbivores, allowing them to become invasive 20,21 and accelerate coral-algal phase shifts on coral reefs. Herbivorous fishes play an important role in promoting resilience and supporting coral recovery, and tend to have small home ranges, suggesting that relatively small-scale (1–10 s km) variation in their abundance will contribute to local changes in rates of reef recovery 22,23. Therefore, local-scale management measures that decrease fishing mortality and increase the abundance and size of herbivorous fishes, such as marine reserves, are expected to play a significant role in supporting recovery and resilience of coral reef ecosystems 24,25. The extent to which different species of herbivorous fishes control macroalgae and promote coral recovery will also depend on their functional role and the algae upon which they graze 26. Herbivorous fish species tend to be selective in their

Coral Reefs, 2001

Since the 1970s, macroalgae have become considerably more abundant on many Caribbean reefs and over®shing of grazing ®shes has been implicated as a contributory factor. We explored relationships between algal cover and grazers (biomass of herbivorous ®shes and abundance of the sea-urchin Diadema antillarum) on mid-depth reefs (12±15 m) in 19 areas at seven locations in Jamaica, Barbados, Belize, Grand Cayman and Cuba, between April 1997 and April 1998. Diadema antillarum density was never >0.01 m ±2 , while herbivorous ®sh biomass (acanthurids and scarids ³12 cm total length) varied from 2±5 g m ±2 in Jamaica to 17.1 g m ±2 in Barbados, and was strongly correlated, negatively with macroalgal cover and positively with `cropped' substratum (sum of `bare', turf and crustose-coralline substrata) cover. However, over®shing of herbivorous ®shes alone cannot explain the widespread abundance of macroalgae, as even on lightly ®shed reefs, macroalgal cover was mostly >20%. Herbivorous ®sh populations on those reefs were apparently only able to maintain approximately 40±60% of reef substratum in cropped states, but due to low space-occupation by coral and other invertebrates, 70±90% of substratum was available to algae. The abundance of macroalgae on lightly ®shed reefs may therefore be a symptom of low coral cover in combination with the continuing absence of Diadema antillarum.

Marine Ecology Progress Series, 2009

Coral reefs are in global decline, with seaweeds replacing corals as spatial dominants. Overfishing of herbivores, anthropogenic eutrophication, and interactions between these factors have been postulated as causes, but long-term tests of these factors are uncommon. We factorially manipulated herbivorous fishes and nutrients at a depth of 16 to 18 m for 7 to 10 mo in 2 experiments over 2 yr. Herbivore exclusion increased algal cover by about 4 to 10 ×, algal biomass by 4 to 6 ×, and suppressed cover of crustose coralline algae by 80 to 100%. Nutrient enrichment had no effect on the cover or mass of upright algae, but altered species composition by suppressing cyanobacteria and facilitating red macroalgae in the absence of herbivores. Nutrient addition increased macroalgal species richness in the absence, but not the presence of herbivores. Feeding by herbivorous fishes increased by 3 to 13 × on nutrient-enriched vs. control plots. This herbivory facilitated cover of crustose coralline algae, demonstrated that herbivores selectively target more nutritional prey, and suggested that herbivores could suppress macrophyte accumulation at sites with increased nutrient availability. Effects of fishes and nutrients on corals varied as a function of coral species. For the branching coral Porites porites, 56% of individuals exposed to fishes were completely consumed; however, individuals that survived grew 60 to 80% more in the presence of fishes. For Porites astreoides, exposure to fishes did not affect mortality, but increased net growth by 3 to 4 times. For this coral, nutrient addition decreased growth when exposed to fishes but not when protected from fishes, suggesting that fishes may have fed more on nutrient-enriched corals.

Ecology, 2013

Indirect biotic interactions play a crucial role in structuring ecological communities, but many of these interactions have not been explored. Algal competition and corallivory are two major stressors contributing to the decline of coral reefs. Here, we provide the first evidence of algal-induced corallivory and synergistic effects between the two stressors on corals. When corals (Montastraea faveolata) were placed in contact with algae (Halimeda opuntia) together with corallivorous fireworms (Hermodice carunculata) in aquaria, corals suffered high tissue mortality. This mortality was reduced in the presence of algae only, and no mortality occurred in the presence of fireworms only or when excluding both algae and fireworms. These findings were supported by field observations showing a predominance of fireworms inside algae contacting live corals, and by an in situ experiment demonstrating higher coral mortality in contact with algae left undisturbed than with algae from which all mobile epifauna were periodically removed. Among the main contributing mechanisms, we suggest that algal contact produces decaying coral tissue that attracts the corallivore and enhances its aggregation behavior. Our study demonstrates an indirect effect pathway by which algae can impact corals, which shares similarities with the classic models of apparent competition and habitat facilitation.

Coral reefs can exist as coral-and macroalgae-dominated habitats often separated by only a few hundred metres. While herbivorous fish are known to depress the abundance of algae and help maintain the function of coral-dominated habitats, less is known about their influence in algae-dominated habitats. Here, we quantified herbivorous fish and benthic algal communities over a 6 mo period in coral-dominated (back-reef) and algal-dominated (lagoon) habitats in a relatively undisturbed fringing coral reef (Ningaloo, Western Australia). Simultaneously, we tested the effects of herbivorous fish on algal recruitment in both habitats using recruitment tiles and fish exclusion cages. The composition of established algal communities differed consistently between habitats, with the back-reef hosting a more diverse community than the Sargassum-dominated lagoon. However, total algal biomass and cover only differed between habitats in autumn, coinciding with maximum Sargassum biomass. The back-reef hosted high coral cover and a diverse herbivorous fish community, with herbivore biomass an order of magnitude greater than the lagoon. Despite these differences in herbivore composition, exclusion of large herbivores had a similar positive effect to foliose macroalgae recruitment on experimental tiles in both back-reef and lagoon habitats. Additionally, territorial damselfish found in the backreef increased turf algae cover and decreased crustose coralline algae cover on recruitment tiles. Collectively, our results show that disparate herbivorous fish communities in coral-and algaedominated habitats are similarly able to limit the recruitment of foliose macroalgae, but suggest that when herbivorous fish biomass and diversity are relatively low, macroalgal communities are able to escape herbivore control through increased growth.

Oecologia, 2012

Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9–46 times, upright macroalgal biomass by 23–84 times, and cyanobacteria cover by 0–27 times, but decreased cover of encrusting coralline algae by 46–100% and short turf algae by 14–39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33–42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30–35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.

Long-term phase shifts from coral to macroalgal dominated reef systems are well documented in the Caribbean. Although the impact of coral diseases, climate change and other factors is acknowledged, major herbivore loss through disease and overfishing is often assigned a primary role. However, direct evidence for the link between herbivore abundance, macroalgal and coral cover is sparse, particularly over broad spatial scales. In this study we use a database of coral reef surveys performed at 85 sites along the Mesoamerican Reef of Mexico, Belize, Guatemala and Honduras, to examine potential ecological links by tracking site trajectories over the period 2005–2014. Despite the long-term reduction of herbivory capacity reported across the Caribbean, the Mesoamerican Reef region displayed relatively low macroalgal cover at the onset of the study. Subsequently, increasing fleshy macroalgal cover was pervasive. Herbivorous fish populations were not responsible for this trend as fleshy macroalgal cover change was not correlated with initial herbivorous fish biomass or change, and the majority of sites experienced increases in macroalgae browser biomass. This contrasts the coral reef top-down herbivore control paradigm and suggests the role of external factors in making environmental conditions more favourable for algae. Increasing macroalgal cover typically suppresses ecosystem services and leads to degraded reef systems. Consequently, policy makers and local coral reef managers should reassess the focus on herbivorous fish protection and consider complementary measures such as watershed management in order to arrest this trend.

Journal of Applied Phycology, 2019