Diving into the deep-end: investigating tropical deep-reef fish assemblages

Increasing demand paired with declining catch rates from traditional fisheries has caused fishers from across the tropical Indian and Pacific Oceans to shift their focus towards deep-reef species. This trend is also seen in Australia; however, little is known about the local biology and ecology of these newly targeted species. Therefore, my objective was to combine multiple techniques, including underwater video, multibeam analysis of habitat, and otolith microchemistry, to examine the distribution, abundance, and species composition of a commercially important assemblage of deep-reef fishes. The information gathered from this project will assist in the resource management of these unique fish assemblages. In this project I examined the biodiversity and ecology of deep-reef fishes at multiple spatial scales. I considered large depth gradients along the continental shelf-break to look at shifts in assemblage structure, but also broad geographic scales extending thousands of kilometres that had the potential to encapsulate multiple stocks. My specific aims were: (1) to describe deep-reef fish assemblages and examine fish-habitat associations for shelf-break environments in the Great Barrier Reef (GBR), Chapters 2 through 5; (2) to determine the utility of otolith microchemistry to identify regional stock structure, and then to apply the technique to fish populations across the Indian Ocean to the Central Pacific (Chapters 6 and 7). In Chapter 2, I demonstrated that depth was a strong predictor of the distribution of fishes. Individual species had different depth distributions and few fish species overlapped between adjacent depth strata, indicating that these are unique assemblages that change with respect to depth. In general, species richness and abundance decreased with increasing depth. New species location records were found for Chromis circumaurea, Chromis okamurai, Chromis mirationis, Hoplolatilus marcosi and Bodianus bennetti in the GBR at lower mesophotic depths. After consulting various fish experts, three potentially new species from the genera Selenanthias, Chromis, and Bodianus species were detected. This was the first research project to use underwater video stations at multiple reefs down to 260 m depths in the GBR and in doing so this research has re-defined depth distributions of some fish assemblages and increased maximum depth records for a number of species. Habitat was also important in predicting where deep-reef fish occur and there was high variation within depth strata (Chapter 3). Although species were often only found within a certain depth range, species' distribution and abundance was determined by localized habitat features. Furthermore, species distribution was dependent on the trophic group and degree of habitat specialization. Shelf-break slope environments had decreasing structural complexity with depth, such as greater proportion of plants and calcified reefs at shallower and middle depths and more mud, sand and rubble at the deepest depths. Depth, relative steepness, topographical relief and hardness of substrate differentiated where these species were distributed. Epibenthic cover and substrate were important factors in influencing fish distributions and the presence of encrusting organisms and calcified reef translated to higher abundance and diversity (Chapter 4). Deeper fishes had varying degrees of habitat specialization and these habitat preferences can have important management implications (Chapter 5). Closely related species (in the same genus) had varying levels of habitat association; these differences likely reflected their species-specific ecology and behaviour (i.e. what they eat, degree of movement). Species with stronger associations may be more easily targeted and directly or indirectly impacted by environmental changes. I hypothesized that environmental variation among species would be reflected in the hard structures of the fish themselves and give some insight to population structure at multiple spatial scales. I investigated otolith elemental composition for commercially-valuable deep-reef fishes of the Pacific: Etelis coruscans (flame snapper) and Etelis sp. (ruby snapper, recently distinguished from the pygmy ruby snapper) to determine the most robust approach to elemental chemistry that would assist in revealing population structure (Chapter 6). Overlapping and non-overlapping elemental fingerprints clarified where deepwater fish resources should be considered a continuous stock or separate stocks between locations. I compared the two major methods of otolith chemistry; laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) had better discriminatory accuracy than solution-based inductively coupled plasma mass spectrometry. Using a smaller ablation spot size had greater temporal resolution when I used a transect of the cross-section of the otolith, from the core to the edge to represent the timeline, or life history, of the fish. Using specific locations of the otolith transect also increased the spatial discrimination of the elemental fingerprints. It was concluded that the spatial separation of the otolith edge was better for stock discrimination. Fishery management decisions rely on accurate information of where natural boundaries in fish populations occur (i.e. stock structure), and it was predicted that the chemistry of otoliths could help in discriminating distinct groups or management units. Based on the outcomes of Chapter 6, I then extended LA-ICP-MS chemical analyses to assess fish populations from otolith samples collected by fisheries researchers from the Pacific Community (New Caledonia) and Fisheries Western Australia. Otoliths were from three broad regions (Indian Ocean, West Pacific and Central Pacific) and included multiple Pacific Island nations: New Caledonia, Tonga, Vanuatu, Samoa, Fiji, Papua New Guinea, Wallis and Futuna, and Monowai Seamount (international waters). Combined with samples I collected from the Indonesia, the GBR and Coral Sea (Australia), this sampling design included ten international Exclusive Economic Zones (EEZ), and three fishery management zones in Australia (Kimberley, Pilbara/Gascoyne and GBR/Coral Sea). This is the first project that applied otolith chemical analyses of multiple deep-reef species (E. coruscans, E. sp. and Etelis carbunculus, the pygmy ruby snapper) across a broad area (most of their distribution), for which identifying stock structure could assist management decisions and promote cooperation between adjoining nations. The potentially robust stocks identified were smaller than previously suggested, which is cause for concern. Smaller stocks may be more vulnerable to fishing pressure and local extirpation. For these locations precautionary management measures should be put in place that recognises these biological units until further evidence suggests otherwise. My PhD research suggests that due to narrow depth distributions, deep-reef assemblages of fishes are vulnerable to overexploitation. Further, deep-reef fish depend on certain habitats and this can add an extra level of vulnerability if these depths and preferred habitat are isolated or uncommon. Deep reefs are critical ecological habitats and unique from shallower environments. Deep-reef ecosystems are still poorly understood, but they are an increasingly threatened component of the GBR and mesophotic reefs worldwide. Tropical deep-reef fish stocks are at risk of over-exploitation in the Indo-Pacific without sufficient information for fisheries management. Sensible protection of deeper areas will be critical if stocks are to be sustainably managed before they are lost. Deep-reef fisheries have been managed by EEZ rather than biological stocks. Here, I used elemental chemistry to identify biological units that could be useful for management strategies. Greater resolution of stock identity and pathways of connectivity in large biological stocks, is required to conserve the unique resources and unappreciated biodiversity of deep-reef fishes

High-resolution otolith elemental signatures in eteline snappers from valuable deepwater tropical fisheries

Marine resources are often shared among countries, with some fish stocks straddling multiple Exclusive Economic Zones, therefore understanding the structure of populations is important for the effective management of fish stocks. Otolith chemical analyses could discriminate among populations based on differences in the chemical composition of otoliths. We used otoliths from two deepwater snappers (flame snapper Etelis coruscans and ruby snapper Etelis boweni) to examine the evidence for population structure across six Pacific Island countries using solution-based inductively coupled plasma mass spectrometry (ICP-MS) for otolith core and whole otolith samples and laser ablation ICP-MS (LA-ICP-MS) for core and edge areas of a cross-sectioned otolith. The inter-species comparison of these methods is important as the two species are often managed under the same regulations. For both species, the two methods demonstrated separation among the locations sampled with high classification accuracy. Smaller laser ablation spot size gave greater temporal resolution over the life-history transect. Comparing the early life-history section of the otoliths (i.e., the core), one interpretation is that young fish experienced more uniform environments in the open ocean as larvae than adults, as the elemental fingerprints had greater overlap among multiple locations. LA-ICP-MS methods had some advantages over solution-based ICP-MS and generally better discrimination for the trace elements investigated. There were substantial differences between species, but both methods suggested nonmixing populations at the regional scale. Otolith chemistry can be an effective tool in discriminating variation for deepwater marine species in multispecies fisheries, and edge measurements from LA-ICP-MS provided the greatest resolution. Although caution should be taken in interpreting the results from relatively small samples sizes, otolith chemical analyses could be useful at these spatial scales to investigate population structure. This information on separate or overlapping populations could be used in future regional fishery management plans

Deep-reef fish communities of the Great Barrier Reef shelf-break: trophic structure and habitat associations

The ecology of habitats along the Great Barrier Reef (GBR) shelf-break has rarely been investigated. Thus, there is little understanding of how associated fishes interact with deeper environments. We examined relationships between deep-reef fish communities and benthic habitat structure. We sampled 48 sites over a large depth gradient (54–260 m) in the central GBR using Baited Remote Underwater Video Stations and multibeam sonar. Fish community composition differed both among multiple shelf-break reefs and habitats within reefs. Epibenthic cover decreased with depth. Deep epibenthic cover included sponges, corals, and macro-algae, with macro-algae present to 194 m. Structural complexity decreased with depth, with more calcified reef, boulders, and bedrock in shallower depths. Deeper sites were flatter and more homogeneous with softer substratum. Habitats were variable within depth strata and were reflected in different fish assemblages among sites and among locations. Overall, fish trophic groups changed with depth and included generalist and benthic carnivores, piscivores, and planktivores while herbivores were rare below 50 m. While depth influenced where trophic groups occurred, site orientation and habitat morphology determined the composition of trophic groups within depths. Future conservation strategies will need to consider the vulnerability of taxa with narrow distributions and habitat requirements in unique shelf-break environments

Domestication via the commensal pathway in a fish-invertebrate mutualism.

Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world's landscapes and biodiversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish (Stegastes diencaeus) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps (Mysidium integrum). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domestication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved

Near-reef elemental signals in the otoliths of settling Pomacentrus amboinensis (Pomacentridae)

Settlement is a key life history transition for coral reef fishes, and how long a fish spends close to a reef prior to settlement is poorly understood. We used laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) and otolith microstructure analysis (daily increments and settlement marks) to determine the length of time larval fish spend near a reef prior to settlement. The otoliths of Pomacentrus amboinensis collected from four neighbouring reefs in the southern Great Barrier Reef showed clear and consistent differences in their elemental signatures prior to and following settlement. Elevated Ba:Ca near settlement and post-settlement was found in fish from all four reefs. However, there was individual variation in elemental profiles, with an increased otolith Ba-to-Ca ratio (near-reef signature) at settlement in 33 % of fish, and up to 8 d prior to settlement in others. Increment widths, often used as a proxy for growth, decreased approaching the settlement mark for all fish, providing further evidence for a "search phase" in larvae. We demonstrated experimentally that otoliths of fish kept in reefal or inter-reefal waters had different elemental chemistry. There were differences in the elemental composition of water samples within the study area, but no consistent trends with distance from reefs. There was poor discrimination of multi-element signatures among fish from different reefs during their pre-settlement phases. However, discrimination improved in the settlement and post-settlement phases of otoliths, indicating that reef waters and perhaps stage of ontogeny affected otolith chemistry. This study demonstrated clear near-reef elemental signatures in fish around settlement. We suggest these differences are due to a combination of water chemistry and physiological influences (e.g., growth). Combining LA-ICP-MS with otolith microstructure analysis can provide high-resolution information on the early life history of reef fishes. Further, a near-reef "search phase" prior to settlement may be common in reef fishes

Deep-reef fish assemblages of the Great Barrier Reef shelf-break (Australia)

Abstract Tropical mesophotic and sub-mesophotic fish ecology is poorly understood despite increasing vulnerability of deeper fish assemblages. Worldwide there is greater fishing pressure on continental shelf-breaks and the effects of disturbances on deeper fish species have not yet been assessed. Difficult to access, deeper reefs host undocumented fish diversity and abundance. Baited Remote Underwater Video Stations (BRUVS) with lights were used to sample deeper habitats (54–260 m), in the Great Barrier Reef (GBR), Australia. Here we describe fish biodiversity, relative abundance and richness, assessing the prediction that depth would drive assemblage structure in the GBR. Distinct groups of fishes were found with depth whilst overall richness and abundance decreased steeply between 100 and 260 m. Commercially-valuable Lutjanidae species from Pristipomoides and Etelis genera, were absent from shallower depths. Few fish species overlapped between adjacent depth strata, indicating unique assemblages with depth. We also detected new location records and potential new species records. The high biodiversity of fish found in shelf-break environments is poorly appreciated and depth is a strong predictor of assemblage composition. This may pose a challenge for managers of commercial fisheries as distinct depth ranges of taxa may translate to more readily targeted habitats, and therefore, an inherent vulnerability to exploitation

Contact with seaweed alters prey selectivity in a coral-feeding reef fish

Human-driven disturbance is fundamentally altering the composition of benthic marine communities. For instance, many coral reefs are experiencing declining coral cover alongside increased macroalgae (seaweed) abundance. While the responses of herbivorous fishes to sea-weeds are comparatively well understood, little is known regarding the responses of other important trophic guilds that interact with the benthic community, such as corallivores. To this end, we investigated how 2 species of seaweed (Galaxaura filamentosa and Sargassum polycystum) affected foraging in an obligate corallivorous fish, Oxymonacanthus longirostris. Corals with no seaweed contact were preferred over corals in contact with seaweed, regardless of the seaweed species. However, following seaweed removal, fish associated with, and fed on, all corals equally, suggesting that corals in contact with these seaweeds do not produce repellant chemical cues. This second finding contrasts with patterns seen in other corallivores, indicating that, while seaweeds may be generally repellent, sensory cues used to make foraging decisions may vary. Regardless, these findings provide further evidence that seaweeds negatively affect foraging in non-herbivorous fishes, which could have far-reaching impacts as habitat quality declines

Warming-induced shifts in amphibian phenology and behavior lead to altered predator-prey dynamics

Climate change induced phenological variation in amphibians can disrupt time-sensitive processes such as breeding, hatching, and metamorphosis, and can consequently alter size-dependent interactions such as predation. Temperature can further alter size-dependent, predator-prey relationships through changes in species' behavior. We thus hypothesized that phenological shifts due to climate warming would alter the predator-prey dynamic in a larval amphibian community through changes in body size and behavior of both the predator and prey. We utilized an amphibian predator-prey system common to the montane wetlands of the U.S. Pacific Northwest: the long-toed salamander (Ambystoma macrodactylum) and its anuran prey, the Pacific chorus frog (Pseudacris regilla). We conducted predation trials to test if changes in predator phenology and environmental temperature influence predation success. We simulated predator phenological shifts by using different size classes of the long-toed salamander representing an earlier onset of breeding, while using spring temperatures corresponding to early- and mid-season larval rearing conditions. Our results indicated that the predator-prey dynamic was highly dependent upon predator phenology and temperature, and both acted synergistically. Increased size asymmetry resulted in higher tadpole predation rates and tadpole tail damage. Both predators and prey altered activity and locomotor performance in warmer treatments. Consequently, behavioral modifications resulted in decreased survival rates of tadpoles in the presence of large salamander larvae. If predators shift to breed disproportionately earlier than prey due to climate warming, this has the potential to negatively impact tadpole populations in high-elevation amphibian assemblages through changes in predation rates mediated by behavior.Fil: Jara, Fabian Gaston. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Thurman, Lindsey. United States Geological Survey; Estados UnidosFil: Montiglio, Piere. University of California at Davis; Estados Unidos. McGill University; CanadáFil: Sih, Andrew. University of California at Davis; Estados UnidosFil: Garcia, Tiffany. State University of Oregon; Estados Unido

Domestication via the commensal pathway in a fish-invertebrate mutualism.

Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world's landscapes and biodiversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish (Stegastes diencaeus) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps (Mysidium integrum). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domestication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved