Simon J. Brandl

Fifty million years of herbivory on coral reefs: fossils, fish and functional innovations

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene–Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.

Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use.

Patterns of ecological specialization offer invaluable information about ecosystems. Yet, specialization is rarely quantified across several ecological niche axes and variables beyond the link between morphological and dietary specialization have received little attention. Here, we provide a quantitative evaluation of ecological specialization in a coral reef fish assemblage (f. Acanthuridae) along one fundamental and two realized niche axes. Specifically, we examined ecological specialization in 10 surgeonfish species with regards to morphology and two realized niche axes associated with diet and foraging microhabitat utilization using a recently developed multidimensional framework. We then investigated the potential relationships between morphological and behavioural specialization. These relationships differed markedly from the traditional ecomorphological paradigm. While morphological specialization showed no relationship with dietary specialization, it exhibited a strong relationship with foraging microhabitat specialization. However, this relationship was inverted: species with specialized morphologies were microhabitat generalists, whereas generalized morphotypes were microhabitat specialists. Interestingly, this mirrors relationships found in plant–pollinator communities and may also be applicable to other ecosystems, highlighting the potential importance of including niche axes beyond dietary specialization into ecomorphological frameworks. On coral reefs, it appears that morphotypes commonly perceived as most generalized may, in fact, be specialized in exploiting flat and easily accessible microhabitats.

Coordinated vigilance provides evidence for direct reciprocity in coral reef fishes

Reciprocity is frequently assumed to require complex cognitive abilities. Therefore, it has been argued that reciprocity may be restricted to animals that can meet these demands. Here, we provide evidence for the potential presence of direct reciprocity in teleost fishes. We demonstrate that in pairs of coral reef rabbitfishes (f. Siganidae), one fish frequently assumes an upright vigilance position in the water column, while the partner forages in small crevices in the reef substratum. Both behaviours are strongly coordinated and partners regularly alternate their positions, resulting in a balanced distribution of foraging activity. Compared to solitary individuals, fishes in pairs exhibit longer vigilance bouts, suggesting that the help provided to the partner is costly. In turn, fishes in pairs take more consecutive bites and penetrate deeper into crevices than solitary individuals, suggesting that the safety provided by a vigilant partner may outweigh initial costs by increasing foraging efficiency. Thus, the described system appears to meet all of the requirements for direct reciprocity. We argue that the nature of rabbitfish pairs provides favourable conditions for the establishment of direct reciprocity, as continuous interaction with the same partner, simultaneous needs, interdependence, and communication relax the cognitive demands of reciprocal cooperation.

Pair formation in the herbivorous rabbitfish Siganus doliatus

This study investigated the basis of pair formation in the abundant herbivorous rabbitfish Siganus doliatus on Orpheus Island, Great Barrier Reef. Pair formation was the most common social system in S. doliatus, with 67.4% of all individuals occurring in pairs. Pairs were stable (i.e. individuals remained with the same partner throughout the study) and pair members were found within 5 m of each other 82.9% of the time. Of the examined pairs, 25% were homosexual resulting in a proportion of heterosexual pairs (75%) that was significantly lower than expected if pairs were formed solely for reproductive reasons. Therefore, although reproduction appears to be the main driver of pair formation in S. doliatus, other factors are likely to influence this behaviour. The high density of individuals on the reef crest (5.7 ± 0 .9 individuals 200 m(-2); mean ± s.e.) and extensively overlapping home ranges of pairs indicated that the defence of territories plays no role in pair formation. Instead, it appears that pair formation in S. doliatus is driven, in part, by other, non-reproductive, ecological factors. It is suggested that pair formation allows for increased vigilance against predation and enables S. doliatus to execute a novel feeding behaviour.

Microtopographic refuges shape consumer‑producer dynamics by mediating consumer functional diversity

Consumer-producer dynamics are critical for ecosystem functioning. In marine environments, primary production is often subject to strong consumer control, and on coral reefs, the grazing pressure exerted by herbivorous fishes has been identified as a major determinant of benthic community structure. Using experimental surfaces, we demonstrate that on coral reefs, microtopographic refuges decrease the overall grazing pressure by more than one order of magnitude. Furthermore, by functionally characterizing consumer communities, we show that refuges also restrict grazer communities to only one functional group, algal croppers, which selectively remove the apical parts of algae. In contrast, detritivorous fishes, which intensively graze flat and exposed microhabitats and can remove both particulate matter and entire stands of algal filaments, are almost entirely excluded. This preclusion of an entire ecosystem process (the removal of particulates) results in two distinct coexisting benthic regimes: communities within refuges are diverse and characterized by numerous algal types and juvenile scleractinian corals, while communities outside refuges support only low-diversity assemblages dominated by simple, unbranched filamentous turf algal mats. Although limited to the scale of a few centimeters, microtopographic refuges can, therefore, mediate the biotic control of community development by affecting both overall grazing rates and the functional diversity of consumer communities. We suggest that the coexistence of two distinct benthic regimes at a small spatial scale may be an important factor for ecosystem functioning and highlight the need to consider the ecological complexity of consumer-producer dynamics when assessing the status of coral reef ecosystems.

Local extinction of a coral reef fish explained by inflexible prey choice

While global extinctions of marine species are infrequent, local extinctions are becoming common. However, the role of habitat degradation and resource specialisation in explaining local extinction is unknown. On coral reefs, coral bleaching is an increasingly frequent cause of coral mortality that can result in dramatic changes to coral community composition. Coral-associated fishes are often specialised on a limited suite of coral species and are therefore sensitive to these changes. This study documents the local extinction of a corallivorous reef fish, Oxymonacanthus longirostris, following a mass bleaching event that altered the species composition of associated coral communities. Local extinction only occurred on reefs that also completely lost a key prey species, Acropora millepora, even though coral cover remained high. In an experimental test, fish continued to select bleached A. millepora over the healthy, but less-preferred prey species that resisted bleaching. These results suggest that behavioural inflexibility may limit the ability of specialists to cope with even subtle changes to resource availability.

A test of trophic cascade theory: fish and benthic assemblages across a predator density gradient on coral reefs

Removal of predators is often hypothesized to alter community structure through trophic cascades. However, despite recent advances in our understanding of trophic cascades, evidence is often circumstantial on coral reefs because fishing pressure frequently co-varies with other anthropogenic effects, such as fishing for herbivorous fishes and changes in water quality due to pollution. Australia’s outer Great Barrier Reef (GBR) has experienced fishing-induced declines of apex predators and mesopredators, but pollution and targeting of herbivorous fishes are minimal. Here, we quantify fish and benthic assemblages across a fishing-induced predator density gradient on the outer GBR, including apex predators and mesopredators to herbivores and benthic assemblages, to test for evidence of trophic cascades and alternative hypotheses to trophic cascade theory. Using structural equation models, we found no cascading effects from apex predators to lower trophic levels: a loss of apex predators did not lead to higher levels of mesopredators, and this did not suppress mobile herbivores and drive algal proliferation. Likewise, we found no effects of mesopredators on lower trophic levels: a decline of mesopredators was not associated with higher abundances of algae-farming damselfishes and algae-dominated reefs. These findings indicate that top-down forces on coral reefs are weak, at least on the outer GBR. We conclude that predator-mediated trophic cascades are probably the exception rather than the rule in complex ecosystems such as the outer GBR.

Extending Rapid Ecosystem Function Assessments to Marine Ecosystems: A Reply to Meyer

Meyer et al. [1] propose a series of assays constituting their rapid ecosystem function assessment (REFA) to quickly and inexpensively survey terrestrial ecosystem processes. In this reply we extend their framework to estuarine and coastal marine ecosystems, which provide invaluable services to humanity. We propose an analogous suite of assays that are equally simple and easily deployed by a variety of end users, including scientists, managers, and citizens. We aim to facilitate cross-system comparisons, test ecological theory, engage society, and provide rigorous quantitative data on the consequences of global change and biodiversity loss for the worlds oceans.

Cryptic effects of habitat declines: coral-associated fishes avoid coral-seaweed interactions due to visual and chemical cues

Seaweed-dominated coral reefs are becoming increasingly common as environmental conditions shift away from those required by corals and toward those ideal for rampant seaweed growth. How coral-associated organisms respond to seaweed will not only impact their fate following environmental change but potentially also the trajectories of the coral communities on which they rely. However, behavioral responses by coral-associated organisms to seaweeds are poorly understood. This study examined interactions between a guild of obligate and opportunistic coral-feeding butterflyfishes (Chaetodontidae) and scleractinian corals to determine whether fishes continue to interact with corals in contact with seaweed or if they are avoided. Under natural conditions, all species interacted almost exclusively with seaweed-free corals. In a controlled patch reef experiment, fishes avoided corals in physical contact with seaweed, irrespective of dietary preferences. When visual seaweed cues were removed, butterflyfish continued to avoid corals that had been in contact with the allelopathic Galaxaura filamentosa, suggesting that chemical cues produced by coral-seaweed interactions are repellent. These findings suggest that, due to deleterious visual and chemical cues produced by coral-seaweed interactions, coral-associated organisms may struggle to locate resources as seaweed-free corals decline in abundance.

Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions

Abstract Anthropogenic habitats are increasingly prevalent in coastal marine environments. Previous research on sessile epifauna suggests that artificial habitats act as a refuge for nonindigenous species, which results in highly homogenous communities across locations. However, vertebrate assemblages that live in association with artificial habitats are poorly understood. Here, we quantify the biodiversity of small, cryptic (henceforth “cryptobenthic”) fishes from marine dock pilings across six locations over 35° of latitude from Maine to Panama. We also compare assemblages from dock pilings to natural habitats in the two southernmost locations (Panama and Belize). Our results suggest that the biodiversity patterns of cryptobenthic fishes from dock pilings follow a Latitudinal Diversity Gradient (LDG), with average local and regional diversity declining sharply with increasing latitude. Furthermore, a strong correlation between community composition and spatial distance suggests distinct regional assemblages of cryptobenthic fishes. Cryptobenthic fish assemblages from dock pilings in Belize and Panama were less diverse and had lower densities than nearby reef habitats. However, dock pilings harbored almost exclusively native species, including two species of conservation concern absent from nearby natural habitats. Our results suggest that, in contrast to sessile epifaunal assemblages on artificial substrates, artificial marine habitats can harbor diverse, regionally characteristic assemblages of vertebrates that follow macroecological patterns that are well documented for natural habitats. We therefore posit that, although dock pilings cannot function as a replacement for natural habitats, dock pilings may provide cost‐effective means to preserve native vertebrate biodiversity, and provide a habitat that can be relatively easily monitored to track the status and trends of fish biodiversity in highly urbanized coastal marine environments.