Peter D'Amato

Carnivory in plants as a beneficial trait in wetlands

The decline in herbivorous fishes is an important contributing factor to the degradation of coral reefs, because their reduction contributes to macro algae overgrowth, which can have harmful effects on corals. Herbivorous fish often form mixed-species groups to locate foraging sites and for defense. The movements and compositions of these groups are dependent on the relative numbers of different species present. Some species, such as the striped parrotfish (Scarus iserti) and ocean surgeonfish (Acanthurus bahianus), serve as core species that lead mixed-species groups. Others, such as the redband (Sparisoma aurofrenatum) and stoplight parrotfishes (Sparisoma viride), follow core species as their associates. Despite the potential importance and abundance of mixed-species groups on reefs, little attention has been given to their composition and movements. Our intent was to determine whether the social dynamics of mixed-species groups in Jamaica were similar to those of Grand Cayman. The overall sizes of mixed-species groups were smaller in Grand Cayman. Focal striped parrotfish in Grand Cayman formed smaller groups, changed composition less, and moved less frequently than in Jamaica. Although probably more abundant than striped parrotfish, the ocean surgeonfish in Grand Cayman did not function as a core species but rather attached themselves as associates to the smaller striped parrotfish groups. Redband parrotfish moved less often in Grand Cayman, and appeared to be more dependent on striped parrotfish groups than stoplight parrotfish. While previous studies on herbivorous reef fish have shown that changes in foraging patterns can change with location, perhaps related to structural heterogeneity and resource distribution, this study illustrates that social interactions between common members of mixed-species groups also change. We suggest that the intra and interspecific social interactions in Grand Cayman are less attuned to finding erratically located high quality resources than those in Jamaica. Other plausible explanations are also considered.

Herbivorous fishes can be sensitive to environmental fluctuations, which influence both availability of food resources and metabolic rate, and thus nutritional requirements. Impacts on herbivore nutritional ecology may result from seasonal variations in temperature and meteoceanographic shifts such as wind-induced upwelling events. We evaluated the effects of seasonal changes on the nutritional ecology of 3 nominally herbivorous fishes (Acanthurus chirurgus, Sparisoma axillare and Kyphosus vaigiensis) in a subtropical rocky reef on the southeastern Brazilian coast using a combination of gut content analysis (at 2 scales of magnification) and stable isotope analysis. Sampling of in situ water temperature covered both patterns of seasonal variation in sea surface temperature, and seasonal occurrence of upwelling. Local upwelling occurred throughout the year but less frequently in winter. Diet and isotopic niche displayed little seasonal variation. Species-specific patterns of seasonal variation indicated distinct responses to environmental fluctuations. Temperature alone cannot explain the locality-specific variation in the nutritional ecology of herbivorous reef fish, and contrary to predictions that digestion in herbivorous fishes is impaired by cooler temperatures, no significant shifts in species’ nutritional ecology were detected.

A form of active restoration for coral assemblages involves culturing coral nubbins at nursery sites before transplantation to recipient reefs. Incidental grazing and/or directed predation by local fish assemblages are major sources of dislodgement and mortality for coral nubbins in nurseries. However, the rate of coral nubbin detachment, how this varies across fish taxa, and whether nubbin size affects rates of detachment warrant further investigation. We used field and aquaria experiments to examine the effect of incidental grazing and predation on the detachment of Porites cylindrica nubbins of different sizes (0.5, 1, 2, 3, 4, and 5 cm height). Short‐term (6 hours) exposure of nubbins to local fish assemblages at Lucero Reef, northwestern Philippines, caused higher detachment (1.93% ± 0.53 SE) compared to caged controls (0.16% ± 0.16 SE), with no detectable effect of nubbin size. To identify the impact of individual fish species, nubbins were exposed to one of four locally abundant herbivorous and corallivorous fish species in aquaria for 8 hours. Nubbin detachment was greater when exposed to Chlorurus spilurus (1.20–36.2%) and Siganus fuscescens (0.00–15.0%) than Chaetodon lunulatus (0.00–4.00%) and Chaetodon kleinii (0.00–1.20%), with the smallest nubbins (0.5 cm) being the most vulnerable. Our results suggest that incidental grazing by herbivorous fishes, especially parrotfishes, may potentially be an important source of detachment and likely mortality of nubbins. Optimizing coral nursery protocols should consider potential trade‐offs between excluding grazing fishes and the accumulation of algal material on caging structures to minimize nubbin mortality and improve coral restoration success.

Potentially toxic metals and metalloids (PTMs) may become a concern to plant and animal health when soil concentrations exceed toxicity limits. These limits are often exceeded in polluted environments (anthropogenic sources) and may transfer through the trophic system, from contaminated soil to plants, and thereafter to herbivores and predators. The aim of this mini review was to consider trophic transfer of PTMs in terrestrial ecosystems, focusing on arthropods as the endpoint. ScienceDirect® was used as search engine with a set of keywords. The most assessed PTMs were Cd, Pb, and Zn, and 63% of all PTMs considered in research were attributed to anthropogenic sources. Industrial or mining sites were most frequently studied, and agricultural sites the least. Brassica was the most studied plant genus as the main extractor of PTMs from the soil as they are easy growing food plants known to take up PTMs. Research mostly focused on primary consumers, with Coleoptera being the most investigated arthropod order, probably because of the diversity of the order and its common occurrence worldwide. Most research was conducted in Europe, while South America and Africa only contributed 6.8% and 2.6%, respectively. The majority of the investigated articles (61%) assessed trophic transfer. From those, only 24% directly measured PTM transfer with experimental trials and included only one trophic level, that is, primary consumers, while 7% of research directly measured PTM transfer across multiple trophic levels (primary and secondary consumers).

One of the central goals in paleoecology is to understand the nature and consequences of biotic interactions. In marine systems, it has been argued that one of the major steps in the escalation of biotic interactions was marked by the origins of grazing fishes in the Cenozoic. Here I investigate the origins of herbivory and grazing in marine fishes using analyses of functional morphospace. Closing and opening lever ratios and relative length of the lower jaw are used to construct a plot of functional morphospace, a quantitative description of the potential feeding modes of fishes. Four fish faunas were examined, spanning the Mesozoic and Cenozoic (Triassic, Jurassic, Eocene and Recent). All three fossil faunas are from conservation Lagerstätten in the central Tethys, in the vicinity of coral reefs or coral-bearing hardgrounds. Changes in functional morphospace occupation reveal a marked shift in the Cenozoic, with the appearance of fishes with relatively small forceful jaws. In Recent faunas, this functional morphospace is occupied almost exclusively by grazing herbivores. This taxon-independent morphological signal of herbivory was lacking in the Mesozoic faunas, was first recorded in the Eocene, and persisted throughout the Cenozoic. This suggests that the Cenozoic did indeed witness the appearance and proliferation of herbivory and grazing by marine fishes. The arrival of these piscine herbivores had the potential to fundamentally alter the dynamics of benthic marine communities.

Distinct zonation of community assemblages among habitats is a ubiquitous feature of coral reefs. The distribution of roving herbivorous fishes (parrotfishes, surgeonfishes and rabbitfishes) is a particularly clear example, with the abundance of these fishes generally peaking in shallow-water, high-energy habitats, regardless of the biogeographic realm. Yet, our understanding of the factors which structure this habitat partitioning, especially with regards to different facets of structural complexity and nutritional resource availability, is limited. To address this issue, we used three-dimensional photogrammetry and structure-from-motion technologies to describe five components of structural complexity (rugosity, coral cover, verticality, refuge density and field-of-view) and nutritional resource availability (grazing surface area) among habitats and considered how these factors are related to herbivorous fish distributions. All complexity metrics (including coral cover) were highest on the slope and crest. Nutritional resource availability differed from this general pattern and peaked on the outer-flat. Unexpectedly, when compared to the distribution of herbivorous fishes, none of the complexity metrics had a marked influence in the models. However, grazing surface area was a strong predictor of both the abundance and biomass of herbivorous fishes. The strong relationship between grazing surface area and herbivorous fish distributions indicates that nutritional resource availability may be one of the primary factors driving the distribution of roving herbivorous fishes. The lack of a relationship between complexity and herbivorous fishes, and a strong affinity of herbivorous fishes for low-complexity, algal turf-dominated outer-flat habitats, offers some cautious optimism that herbivory may be sustained on future, low-complexity, algal turf-dominated reef configurations.

Unsustainable fishing has been identified as one of the most important direct drivers of the degradation of coral reef ecosystems. Herbivorous reef fish, which prevent excessive accumulation of coral-suffocating algae, are in a steady decline due to the presence of invasive predators together with overfishing in many coral reef systems. Here, a two-dimensional predator–prey model is proposed that enables exploration of intermittent harvesting policies, where a control function in the model is evoked that signals when harvesting should cease and commence to maintain a herbivorous fish density above a critical threshold necessary for population stability. We analyze the model by using Filippov’s regularization method, which is ideal for discontinuous dynamic systems, such as the system explored here with intermittent harvesting. We obtain the sliding segment of the Filippov’s system and its domains together with the conditions for the existence and stability of the regular, virtual and pseudo-equilibria. We show that regular equilibria and pseudo-equilibrium can coexist. Further, we show that intermittent harvesting, with time lags between fishery harvesting decisions and implementations considered, can lead to a bounded oscillation about pseudo-equilibria, or in other words, a sustainable herbivorous fishery. Finally, using a selective harvesting policy, where the invasive predator fish is targeted (here lionfish), we show that a longer herbivorous fish harvesting period can be achieved without changing the critical threshold for harvesting.

Coral reefs around the world are changing rapidly, with overfishing of herbivorous fishes and increased sediment inputs being two of the major local-scale stressors. We therefore assessed the effects of sediment loads and overfishing on the nutritional quality and yield to grazing fishes of algal turfs, within the epilithic algal matrix, on a coral reef at Lizard Island, Australia. Low, ambient and high sediment loads were maintained on turf-covered coral tiles, with and without grazer exclusion cages, for 1 month. Subsequently, algal turfs were removed and analysed for organic carbon and nitrogen content. Under grazer exclusion, sediment additions decreased algal turf biomass by approximately 63%, while algal turf biomass was the highest on tiles with sediments removed. In the presence of grazing fishes, algal turfs in all treatments were cropped by grazers to similar low biomass levels. Nitrogen content of algal turfs followed a similar trend. Effectively, added sediments decreased the potential yield of algal turf biomass and nitrogen to grazing fishes by an average of 2000 and 3300%, respectively. Sediments profoundly affect algal turf yield to grazing herbivorous fishes and, therefore, the productivity of algal turf-based food chains, potentially diminishing reef-based fisheries.

Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides. IMPORTANCE This work connects specific uncultured bacterial taxa with distinct polysaccharide digestion capabilities lacking in their marine vertebrate hosts, providing fresh insights into poorly understood processes for deconstructing complex sulfated polysaccharides and potential evolutionary mechanisms for microbial acquisition of expanded macroalgal utilization gene functions. Several thousand new marine-specific candidate enzyme sequences for polysaccharide utilization have been identified. These data provide foundational resources for future investigations into suppression of coral reef macroalgal overgrowth, fish host physiology, the use of macroalgal feedstocks in terrestrial and aquaculture animal feeds, and the bioconversion of macroalgae biomass into value-added commercial fuel and chemical products.

The Enenteridae Yamaguti, 1958 and Gyliauchenidae Fukui, 1929 exhibit an interesting pattern of host partitioning in herbivorous fishes of the Indo-West Pacific. Enenterids are known almost exclusively from fishes of the family Kyphosidae, a group of herbivorous marine fishes common on tropical and temperate reefs. In contrast, gyliauchenids are found in most of the remaining lineages of marine herbivorous fishes, but until the present study, had never been known from kyphosids. Here we report on the first species of gyliauchenid known from a kyphosid. Endochortophagus protoporus gen. nov., sp. nov. was recovered from the Western buffalo bream, Kyphosus cornelii (Whitley, 1944), collected off Western Australia. Kyphosus cornelii also hosts an enenterid, Koseiria allanwilliamsi Bray & Cribb, 2002, and is thus the first fish known in which enenterids and gyliauchenids co-occur. Molecular phylogenetic analyses place the new species close to those of Affecauda Hall & Chambers, 1999 and Flagellotrema Ozaki, 1936, but there is sufficient morphological evidence, combined with the unusual host, to consider it distinct from these genera. We discuss factors which may have contributed to the host partitioning pattern observed between enenterids and gyliauchenids.

Dynamics of fish communities on Reunion fringing reefs, Indian Ocean. I. Patterns of spatial distribution

Algae and detritus co-occur on reef substrata, but their relative importance to consumers, in terms of biomass and nutrient content, is poorly understood. Epilithic algae, sediment and detritus were sampled among four windward zones at Lizard Island, Australia, using a vacuum sampler. Total N, P and biomass (total organic C) were quantified for algae and detritus. Algal and detrital biomass varied among zones and both were positively correlated with sediment load. Algal biomass was approximately six times higher than detritus on the reef crest. In other zones, the two components were more similar in abundance. Particulates on the reef crest had the highest organic:inorganic ratios, a feature likely to be favoured by herbivorous and detritivorous fishes. C:N ratios of algae and detritus, while locally variable, were broadly comparable among zones. C:P ratios of both components decreased in leeward zones. Although locally variable, detritus had a higher content of both N and P. Overall, detritus is relatively abundant on windward reef substrata and of equal or greater nutritional quality than algae. It represents a potentially important resource for both detritivorous and herbivorous fishes.

Dionaea is a highly specialized carnivorous plant species with a unique mechanism for insect capture. The leaf is converted into an osmotically driven trap that closes when an insect triggers sensory trichomes. This study investigates the significance of insect capture for growth of Dionaea at different successional stages after a fire, under conditions where the prey is highly variable in its isotope signature. The contribution of insect-derived nitrogen (N) was estimated using the natural abundance of 15N. In contrast to previous 15N studies on carnivorous plants, the problem emerges that delta15N values of prey insects ranged between -4.47 per thousand (grasshoppers) and +7.21 per thousand (ants), a range that exceeds the delta15N values of non carnivorous reference plants (-4.2 per thousand) and soils (+3 per thousand). Thus, the isotope-mixing model used by Shearer and Kohl to estimate the amount of insect-derived N is not applicable. In a novel approach, the relationships of delta15N values of different organs with delta15N of trapping leaves were used to estimate N partitioning within the plant. It is estimated that soon after fire approximately 75% of the nitrogen is obtained from insects, regardless of plant size or developmental stage. The estimates are verified by calculating the average isotope signatures of insects from an isotope mass balance and comparing this with the average measured delta15N values of insects. It appears that for Dionaea to survive and reach the flowering stage, seedlings must first reach the 6th-leaf rosette stage, in which trap surface area nearly doubles and facilitates the capture of large insects. Large amounts of nitrogen thus made available to plants may facilitate an enhanced growth rate and the progressive production of additional large traps. Dionaea reaches a maximum abundance after fire when growth of the competing vegetation is suppressed. About 10 years after fire, when grasses and shrubs recover, Dionaea becomes overtopped by other species. This would not only reduce carbon assimilation but also the probability of catching larger prey. The amount of insect-derived nitrogen decreases to 46%, and Dionaea becomes increasingly dependent on N-supply from the soil. Competition for both light and N may cause the near disappearance of Dionaea in older stages of the fire succession.

The carnivorous pitcher plant genus Nepenthes grows in nutrient-deficient substrates and produce jug-shaped leaf organs (pitchers) that trap arthropods as a source of N and P. A number of Bornean Nepenthes demonstrate novel nutrient acquisition strategies. Notably, three giant montane species are engaged in a mutualistic association with the mountain treeshrew, Tupaia montana, in which the treeshrew defecates into the pitchers while visiting them to feed on nectar secretions on the pitchers' lids.Although the basis of this resource mutualism has been elucidated, many aspects are yet to be investigated. We sought to provide insights into the value of the mutualism to each participant. During initial observations we discovered that the summit rat, R. baluensis, also feeds on sugary exudates of N. rajah pitchers and defecates into them, and that this behavior appears to be habitual. The scope of the study was therefore expanded to assess to what degree N. rajah interacts with the small mammal community.We found that both T. montana and R. baluensis are engaged in a mutualistic interaction with N. rajah. T .montana visit pitchers more frequently than R. baluensis, but daily scat deposition rates within pitchers do not differ, suggesting that the mutualistic relationships are of a similar strength. This study is the first to demonstrate that a mutualism exists between a carnivorous plant species and multiple members of a small mammal community. Further, the newly discovered mutualism between R. baluensis and N. rajah represents only the second ever example of a multidirectional resource-based mutualism between a mammal and a carnivorous plant.