On predicting particle capture rates in aquatic ecosystems

Recent advances in understanding the capture of moving suspended particles in aquatic ecosystems have opened up new possibilities for predicting rates of suspension feeding, larval settlement, seagrass pollination and sediment removal. Drawing on results from both highly-resolved computational fluid dynamics (CFD) simulations and existing experimental data, we quantify the controlling influence of flow velocity, particle size and collector size on rates of contact between suspended particles and biological collectors over the parameter space characterising a diverse range of aquatic ecosystems. As distinct from assumptions in previous modeling studies, the functional relationships describing capture are highly variable. Contact rates can vary in opposing directions in response to changes in collector size, an organism’s size, the size of particles being intercepted (related to diet in the case of suspension feeders), and the flow strength. Contact rates shift from decreasing to increasing with collector diameter when particles become relatively large and there is vortex shedding in the collector wake. And in some ranges of the ecologically relevant parameter space, contact rates do not increase strongly with velocity or particle size. The understanding of these complex dependencies allows us to reformulate some hypotheses of selection pressure on the physiology and ecology of aquatic organisms. We discuss the benefits and limitations of CFD tools in predicting rates of particle capture in aquatic ecosystems. Finally, across the complete parameter space relevant to real aquatic ecosystems, all quantitative estimates of particle capture from our model are provided here.

Recruitment, settlement and ontogeny of the serpulid 'Spirobranchus cariniferus' (Gray, 1843)

<p>Serpulids are a globally represented group of polychaetes and can be found in many habitats from the intertidal fringe to the subtidal environment and even in deep-sea ecosystems. These tube-dwelling worms are often described as pioneer species in new or disturbed habitats. Serpulids secrete a calcareous tube and often occur in aggregations. These patches can range from several centimetres to several metres in diameter and may even form reef systems. Accumulations of tube-dwelling worms provide a new habitat for other species and, therefore, serpulids are considered bioengineers. Serpulid aggregations are known to enhance biodiversity and species abundance and may increase water quality through their filter activity. Despite their ecological importance, their ecology and ontogeny have received little attention. Spirobranchus cariniferus, a New Zealand endemic intertidal serpulid, is a substantial contributor to intertidal ecosystems. For this and other Serpulidae, the link between larval development and larval settlement is missing. However, this connection is essential to understand recruitment and ecology of tube-dwelling worms. Therefore, in this thesis, I describe the ontogeny of S. cariniferus from larval development to recruitment and reproduction. In the first data chapter, I present my findings on the recruitment of S. cariniferus in the field. This serpulid settles aggregatively in the field but not necessarily in response to the presence of adult conspecifics, as has been previously reported. Abiotic factors such as sunlight or wave disturbance have a more substantial effect on recruitment rather than the occurrence of adult individuals of the same or a competing species. Additionally, this chapter provides support for the hypothesis that larvae of S. cariniferus may accumulate near the substrate before settlement. Many sessile marine invertebrate taxa occur in either aggregations or as solitary individuals, with potential benefits and disadvantages associated with each configuration. For S. cariniferus, solitary and aggregative individuals can be found in the same habitat. Therefore, the second data chapter compares growth and mortality for individuals living alone or in aggregation. While solitary and aggregative individuals elongate their tubes at a similar rate, further correlations of body to tube sizes lead to the conclusion that solitary worms focus more of their energy on tube length growth rather than body size increment compared to aggregative conspecifics. Mortality is highly variable but does not differ between both configurations. However, individuals living in a patch have a better ability to recover from damage to their tubes. In the last two decades, the idea that gonochorism is the general reproductive pattern for Serpulidae has been challenged, and instead it has been suggested by some that protandry is the more common trait. Therefore, with my third data chapter, I explore maturation and sex ratio of S. cariniferus and whether it changes for individuals living alone vs. in aggregation or based on size. While maturation depends on size, sex does not, and neither maturation nor sex ratio are dependent on whether individuals live in aggregation or not. Further, the ratio of females to males did not favour either sex consistently. For the first time in this species I found evidence of possible hermaphroditism. Through spawning trials and histological sections, I identified nine individuals which simultaneously contained oocytes and sperm cells. I suggest therefore, that S. cariniferus has alternating sexes rather than protandry as a reproductive strategy. In the fourth and final data chapter, I describe the metamorphosis and settlement behaviour of S. cariniferus larvae. For this serpulid species, settlement and metamorphosis are separate and distinct steps that involve both behavioural and morphological changes to the larvae. Further, this entire process can be quite prolonged (i.e. over several days), and at some points can be reversed. It is therefore very important that observations last longer than 24–48 hours, when studying serpulid settlement. As far as I am aware, this is the first study on a serpulid species to examine aggregative settlement in the field in relation to the presence of adult conspecifics and abiotic factors, and also to explicitly test for consequences of solitary vs. group living on growth and mortality. It is also the first to show evidence of hermaphroditism in this species. I hope my research and this thesis stimulates a more inclusive and holistic investigation of serpulids in the future. Larval development, settlement patterns and ontogeny need to be studied in detail if we want to understand the evolution, ecology, impacts and benefits of these and other sessile marine invertebrates.</p>

Recruitment, settlement and ontogeny of the serpulid 'Spirobranchus cariniferus' (Gray, 1843)

<p>Serpulids are a globally represented group of polychaetes and can be found in many habitats from the intertidal fringe to the subtidal environment and even in deep-sea ecosystems. These tube-dwelling worms are often described as pioneer species in new or disturbed habitats. Serpulids secrete a calcareous tube and often occur in aggregations. These patches can range from several centimetres to several metres in diameter and may even form reef systems. Accumulations of tube-dwelling worms provide a new habitat for other species and, therefore, serpulids are considered bioengineers. Serpulid aggregations are known to enhance biodiversity and species abundance and may increase water quality through their filter activity. Despite their ecological importance, their ecology and ontogeny have received little attention. Spirobranchus cariniferus, a New Zealand endemic intertidal serpulid, is a substantial contributor to intertidal ecosystems. For this and other Serpulidae, the link between larval development and larval settlement is missing. However, this connection is essential to understand recruitment and ecology of tube-dwelling worms. Therefore, in this thesis, I describe the ontogeny of S. cariniferus from larval development to recruitment and reproduction. In the first data chapter, I present my findings on the recruitment of S. cariniferus in the field. This serpulid settles aggregatively in the field but not necessarily in response to the presence of adult conspecifics, as has been previously reported. Abiotic factors such as sunlight or wave disturbance have a more substantial effect on recruitment rather than the occurrence of adult individuals of the same or a competing species. Additionally, this chapter provides support for the hypothesis that larvae of S. cariniferus may accumulate near the substrate before settlement. Many sessile marine invertebrate taxa occur in either aggregations or as solitary individuals, with potential benefits and disadvantages associated with each configuration. For S. cariniferus, solitary and aggregative individuals can be found in the same habitat. Therefore, the second data chapter compares growth and mortality for individuals living alone or in aggregation. While solitary and aggregative individuals elongate their tubes at a similar rate, further correlations of body to tube sizes lead to the conclusion that solitary worms focus more of their energy on tube length growth rather than body size increment compared to aggregative conspecifics. Mortality is highly variable but does not differ between both configurations. However, individuals living in a patch have a better ability to recover from damage to their tubes. In the last two decades, the idea that gonochorism is the general reproductive pattern for Serpulidae has been challenged, and instead it has been suggested by some that protandry is the more common trait. Therefore, with my third data chapter, I explore maturation and sex ratio of S. cariniferus and whether it changes for individuals living alone vs. in aggregation or based on size. While maturation depends on size, sex does not, and neither maturation nor sex ratio are dependent on whether individuals live in aggregation or not. Further, the ratio of females to males did not favour either sex consistently. For the first time in this species I found evidence of possible hermaphroditism. Through spawning trials and histological sections, I identified nine individuals which simultaneously contained oocytes and sperm cells. I suggest therefore, that S. cariniferus has alternating sexes rather than protandry as a reproductive strategy. In the fourth and final data chapter, I describe the metamorphosis and settlement behaviour of S. cariniferus larvae. For this serpulid species, settlement and metamorphosis are separate and distinct steps that involve both behavioural and morphological changes to the larvae. Further, this entire process can be quite prolonged (i.e. over several days), and at some points can be reversed. It is therefore very important that observations last longer than 24–48 hours, when studying serpulid settlement. As far as I am aware, this is the first study on a serpulid species to examine aggregative settlement in the field in relation to the presence of adult conspecifics and abiotic factors, and also to explicitly test for consequences of solitary vs. group living on growth and mortality. It is also the first to show evidence of hermaphroditism in this species. I hope my research and this thesis stimulates a more inclusive and holistic investigation of serpulids in the future. Larval development, settlement patterns and ontogeny need to be studied in detail if we want to understand the evolution, ecology, impacts and benefits of these and other sessile marine invertebrates.</p>

Increased Coral Larval Supply Enhances Recruitment for Coral and Fish Habitat Restoration

Loss of foundation reef-corals is eroding the viability of reef communities and ecosystem function in many regions globally. Coral populations are naturally resilient but when breeding corals decline, larval supply becomes limiting and natural recruitment is insufficient for maintaining or restoring depleted populations. Passive management approaches are important but in some regions they are proving inadequate for protecting reefs, therefore active additional intervention and effective coral restoration techniques are needed. Coral spawning events produce trillions of embryos that can be used for mass larval rearing and settlement on degraded but recoverable reef areas. We supplied 4.6 million Acropora tenuis larvae contained in fine mesh enclosures in situ on three degraded reef plots in the northwestern Philippines during a five day settlement period to initiate restoration. Initial mean larval settlement was very high (210.2 ± 86.4 spat per tile) on natural coral skeleton settlement tiles in the larval-enhanced plots, whereas no larvae settled on tiles in control plots. High mortality occurred during early post-settlement life stages as expected, however, juvenile coral survivorship stabilised once colonies had grown into visible-sized recruits on the reef by 10 months. Most recruits survived and grew rapidly, resulting in significantly increased rates of coral recruitment and density in larval-enhanced plots. After two years growth, mean colony size reached 11.1 ± 0.61 cm mean diameter, and colonies larger than 13 cm mean diameter were gravid and spawned, the fastest growth to reproductive size recorded for broadcast spawning corals. After three years, mean colony size reached 17 ± 1.7 cm mean diameter, with a mean density of 5.7 ± 1.25 colonies per m–2, and most colonies were sexually reproductive. Coral cover increased significantly in larval plots compared with control plots, primarily from A. tenuis recruitment and growth. Total production cost for each of the 220 colonies within the restored breeding population after three years was United States $17.80 per colony. A small but significant increase in fish abundance occurred in larval plots in 2018, with higher abundance of pomacentrids and corallivore chaetodontids coinciding with growth of A. tenuis colonies. In addition, innovative techniques for capturing coral spawn slicks and larval culture in pools in situ were successfully developed that can be scaled-up for mass production of larvae on reefs in future. These results confirm that enhancing larval supply significantly increases settlement and coral recruitment on reefs, enabling rapid re-establishment of breeding coral populations and enhancing fish abundance, even on degraded reef areas.

Larval culture and settlement of the intertidal gastropod Siphonaria australis

<p>Laboratory rearing studies on the larvae of benthic marine invertebrates are important in providing information on the development of marine species, particularly those with complex life history cycles. Intertidal gastropods of the genus Siphonaria have been well studied in aspects of their physiology, behaviour, ecology, and reproduction. However, to our current knowledge, there are no cases on the successful laboratory rearing, from hatching through to metamorphosis, of larvae within this genus. Siphonariids are a primitive family of basommatophoran limpets in which the majority produce encapsulated embryos that hatch into feeding, planktonic veliger larvae. For such larvae, the quality and quantity of phytoplankton food can strongly affect larval growth, survival, and the ability to settle and metamorphose successfully. The primary aim of this study was to identify the optimal algal feeding diet for culturing the larvae of Siphonaria australis to competence in laboratory conditions, with a focus on algal composition and quantity. Once having defined the preferred feeding conditions, a secondary aim was to successfully culture larvae through to metamorphosis, by identifying the required settlement cue(s). First, I exposed newly hatched larvae to diets of three different algal compositions (all at a high concentration of 20,000 cells/mL): two unialgal diets of Isochrysis galbana and Pavlova lutheri, and a mixed diet consisting of a 1:1 ratio of both species. The results revealed that, although they grew in all diets, S. australis larvae exhibited highest growth and survival when fed the unialgal I.galbana diet. In a second experiment, I exposed newly hatched larvae to three different food concentrations of the unialgal I. galbana diet; low (1,000 cells/mL), medium (10,000 cells/mL) and high (20,000 cells/mL). Larval growth and survival were highest when fed a high food concentration, with development and survival severely reduced in low food treatments. At the end of this experiment it was discovered that once larvae grew to ~350µm in length, at an age of approximately one month post-hatching, they began to demonstrate signs of competence and growth rates plateaued. Finally, I exposed newly hatched larvae to optimum feeding conditions in an attempt to achieve larval settlement using different potential cues. Once larvae began to show signs of competence, they were exposed to five settlement cues: (1) live adults in filtered seawater (FSW), (2) adult-conditioned FSW, (3) rocks in adult-conditioned FSW, (4) rocks in regular FSW, and (5) crustose coralline algae-covered rocks in FSW. Larvae only successfully metamorphosed (i.e. exhibited loss of the larval velum) in treatments containing live adults. In total, my results provide a successful method in culturing Siphonaria australis larvae in laboratory conditions, as well as determines the cue required to induce settlement and metamorphosis. Not only can this method aid in providing more information on the development of this species, but it may also be applied to other members in this genus as well, and further our knowledge on the overall biology of Siphonariid limpets.</p>

Larval culture and settlement of the intertidal gastropod Siphonaria australis

<p>Laboratory rearing studies on the larvae of benthic marine invertebrates are important in providing information on the development of marine species, particularly those with complex life history cycles. Intertidal gastropods of the genus Siphonaria have been well studied in aspects of their physiology, behaviour, ecology, and reproduction. However, to our current knowledge, there are no cases on the successful laboratory rearing, from hatching through to metamorphosis, of larvae within this genus. Siphonariids are a primitive family of basommatophoran limpets in which the majority produce encapsulated embryos that hatch into feeding, planktonic veliger larvae. For such larvae, the quality and quantity of phytoplankton food can strongly affect larval growth, survival, and the ability to settle and metamorphose successfully. The primary aim of this study was to identify the optimal algal feeding diet for culturing the larvae of Siphonaria australis to competence in laboratory conditions, with a focus on algal composition and quantity. Once having defined the preferred feeding conditions, a secondary aim was to successfully culture larvae through to metamorphosis, by identifying the required settlement cue(s). First, I exposed newly hatched larvae to diets of three different algal compositions (all at a high concentration of 20,000 cells/mL): two unialgal diets of Isochrysis galbana and Pavlova lutheri, and a mixed diet consisting of a 1:1 ratio of both species. The results revealed that, although they grew in all diets, S. australis larvae exhibited highest growth and survival when fed the unialgal I.galbana diet. In a second experiment, I exposed newly hatched larvae to three different food concentrations of the unialgal I. galbana diet; low (1,000 cells/mL), medium (10,000 cells/mL) and high (20,000 cells/mL). Larval growth and survival were highest when fed a high food concentration, with development and survival severely reduced in low food treatments. At the end of this experiment it was discovered that once larvae grew to ~350µm in length, at an age of approximately one month post-hatching, they began to demonstrate signs of competence and growth rates plateaued. Finally, I exposed newly hatched larvae to optimum feeding conditions in an attempt to achieve larval settlement using different potential cues. Once larvae began to show signs of competence, they were exposed to five settlement cues: (1) live adults in filtered seawater (FSW), (2) adult-conditioned FSW, (3) rocks in adult-conditioned FSW, (4) rocks in regular FSW, and (5) crustose coralline algae-covered rocks in FSW. Larvae only successfully metamorphosed (i.e. exhibited loss of the larval velum) in treatments containing live adults. In total, my results provide a successful method in culturing Siphonaria australis larvae in laboratory conditions, as well as determines the cue required to induce settlement and metamorphosis. Not only can this method aid in providing more information on the development of this species, but it may also be applied to other members in this genus as well, and further our knowledge on the overall biology of Siphonariid limpets.</p>

From Natural Xanthones to Synthetic C-1 Aminated 3,4-Dioxygenated Xanthones as Optimized Antifouling Agents

Biofouling, which occurs when certain marine species attach and accumulate in artificial submerged structures, represents a serious economic and environmental issue worldwide. The discovery of new non-toxic and eco-friendly antifouling systems to control or prevent biofouling is, therefore, a practical and urgent need. In this work, the antifouling activity of a series of 24 xanthones, with chemical similarities to natural products, was exploited. Nine (1, 2, 4, 6, 8, 16, 19, 21, and 23) of the tested xanthones presented highly significant anti-settlement responses at 50 μM against the settlement of mussel Mytilus galloprovincialis larvae and low toxicity to this macrofouling species. Xanthones 21 and 23 emerged as the most effective larval settlement inhibitors (EC50 = 7.28 and 3.57 µM, respectively). Additionally, xanthone 23 exhibited a therapeutic ratio (LC50/EC50) > 15, as required by the US Navy program attesting its suitability as natural antifouling agents. From the nine tested xanthones, none of the compounds were found to significantly inhibit the growth of the marine biofilm-forming bacterial strains tested. Xanthones 4, 6, 8, 16, 19, 21, and 23 were found to be non-toxic to the marine non-target species Artemia salina (<10% mortality at 50 μM). Insights on the antifouling mode of action of the hit xanthones 21 and 23 suggest that these two compounds affected similar molecular targets and cellular processes in mussel larvae, including that related to mussel adhesion capacity. This work exposes for the first time the relevance of C-1 aminated xanthones with a 3,4-dioxygenated pattern of substitution as new non-toxic products to prevent marine biofouling.

Life in the Fast Lane: Modeling the Fate of Glass Sponge Larvae in the Gulf Stream

Effective conservation management of deep-sea sponges, including design of appropriate marine protected areas, requires an understanding of the connectivity between populations throughout a species’ distribution. We provide the first consideration of larval connectivity among deep-sea sponge populations along the southeastern coast of North America, illustrate the influence of the Gulf Stream on dispersal, and complement published distribution models by evaluating colonization potential. Connectivity among known populations of the hexactinellid sponge Vazella pourtalesii was simulated using a 3-D biophysical dispersal model throughout its distribution from Florida, United States to Nova Scotia, Canada. We found no exchange with an estimated pelagic larval duration of 2 weeks between populations north and south of Cape Hatteras, North Carolina at surface, mid-water and seabed release depths, irrespective of month of release or application of a horizontal diffusion constant specific to cross-Gulf Stream diffusivity. The population north of Cape Hatteras and south of Cape Cod was isolated. There was some evidence that Gulf Stream eddies formed near Cape Hatteras could travel to the northwest, connecting the populations in the two sub-regions, however that would require a much longer pelagic duration than what is currently known. More likely almost all larval settlement will be in the immediate area of the adults. At sub-regional scales, connectivity was found from the Strait of Florida through to the Blake Plateau, southeastern United States, with the latter area showing potential for recruitment from more than one source population. The influence of the Charleston Bump, a shallow feature rising from the Blake Plateau, was substantial. Particles seeded just north of the Bump were transported greater distances than those seeded to the south, some of which were caught in an associated gyre, promoting retention at the seabed. To the north on the Scotian Shelf, despite weaker currents and greater distances between known occurrences, unidirectional transport was detected from Emerald Basin to the Northeast Channel between Georges and Browns Banks. These major conclusions remained consistent through simulations run with different averaging periods for the currents (decades to daily) and using two ocean model products (BNAM and GLORYS12V1).