Trophic interactions of marine sponges

<p>Marine communities in the Anthropocene are changing rapidly with potentially severe consequences for ecosystem functioning. Recently, there has been increased interest in the ecological role of sponges, particularly on coral reefs, driven by evidence that sponges may be less affected by this period of environmental change than other benthic organisms. The Sampela reef system in the Wakatobi Marine National Park, Indonesia, is an example of a reef that has shifted to sponge dominance following a decline in hard corals and an increase in sponge density. Previous research suggests that the Sampela reef system may support a greater abundance of spongivorous fishes relative to surrounding reefs, however, uncertainties remain regarding spongivore identity and predated sponges. In addition, little is known about how shifts towards sponge dominance affect the trophic structure of reefs. The primary aim of my thesis was to investigate sponge trophic interactions to gain insight into the way sponge-dominated reefs of the future might function. This information is essential to predict the broader functional consequences of increasing sponge dominance on reefs in the Anthropocene. In my first data chapter, I measured the functional impact of spongivorous fishes by quantifying sponge biomass consumption on Wakatobi reefs. Video analysis identified 33 species from 10 families of reef fish grazing on Xestospongia spp., although 95% of bites were taken by only 11 species. Gut content analysis indicated that Pygoplites diacanthus and Pomacanthus imperator were obligate spongivores and Pomacanthus xanthometopon, Zanclus cornutus and Siganus punctatus regularly consumed sponges. In situ feeding observations revealed that sponges from the family Petrosiidae are preferred by P. diacanthus and Z. cornutus. Spongivores were estimated to consume 46.6 ± 18.3 g sponge 1000 m- 2 of reef day-1 and P. diacanthus had the greatest predatory impact on sponges. While estimates provided here are conservative and likely underestimate the true magnitude of spongivory on Indo-Pacific coral reefs, this chapter provides the first known estimate of reef wide sponge biomass consumption. Comparisons with published data estimating coral consumption by Chaetodontids in the Pacific suggests that biomass transferred through both pathways is similar in magnitude. Hence spongivory is an important, yet overlooked, trophic pathway on Indo-Pacific reefs. In my second data chapter, I developed genetic methods to identify sponges from the stomach contents of spongivorous angelfishes sampled in my first chapter. A range of primers and associated predator-blocking primers targeting the 18S rDNA gene were designed and tested on extracts of sponge and spongivore DNA. Sequences were successfully amplified from 14 sponges spanning 6 orders of Porifera, with the majority of samples identified belonging to the order Haplosclerida. This study is the first to successfully sequence sponges from the gut contents of spongivorous fishes. Sequence data indicated that Pygoplites diacanthus consumed sponges with considerable chemical defences and exhibited significant dietary plasticity within the Porifera phylum, similar to observations of angelfishes in the Caribbean and the eastern Pacific. In my third data chapter, I used stable isotope analysis to investigate differences in consumer niche widths and trophic diversity on the sponge-dominated Sampela reef system in comparison to an adjacent, higher quality reef. I measured the stable isotope ratios of coral reef fish representing different functional feeding groups, prey items and basal carbon sources at both sites. I used isotope data to calculate the trophic position and isotopic niches of each species and performed interspecific and inter-site comparisons. The fish assemblage had a significantly lower mean trophic position at the sponge-dominated site and the majority of species had wider isotopic niches, in accordance with optimal foraging theory which supports expansion in niche widths when per capita prey is low. The fish assemblage sampled at the sponge-dominated site used a significantly lower range of resources, had lower trophic diversity and obtained more carbon from benthic production than fish from the higher quality reef site. Results indicate a simpler trophic structure at the sponge-dominated site characterised by fish with more similar diets. Whilst trophic niche expansion may facilitate population survival in the short term, it can be expected to lead to intensified competition for increasingly scarce resources. In my final data chapter, I investigated niche partitioning and organic matter contributions to co-occurring temperate sponges. I sampled the stable isotope ratios of five abundant sponge species at 10 m and 30 m at two sites at opposing ends of Doubtful Sound, Fiordland. I also used an ROV to opportunistically sample sponges at depths >50 m and measured stable isotope ratios of picoplankton (</p>

Trophic interactions of marine sponges

<p>Marine communities in the Anthropocene are changing rapidly with potentially severe consequences for ecosystem functioning. Recently, there has been increased interest in the ecological role of sponges, particularly on coral reefs, driven by evidence that sponges may be less affected by this period of environmental change than other benthic organisms. The Sampela reef system in the Wakatobi Marine National Park, Indonesia, is an example of a reef that has shifted to sponge dominance following a decline in hard corals and an increase in sponge density. Previous research suggests that the Sampela reef system may support a greater abundance of spongivorous fishes relative to surrounding reefs, however, uncertainties remain regarding spongivore identity and predated sponges. In addition, little is known about how shifts towards sponge dominance affect the trophic structure of reefs. The primary aim of my thesis was to investigate sponge trophic interactions to gain insight into the way sponge-dominated reefs of the future might function. This information is essential to predict the broader functional consequences of increasing sponge dominance on reefs in the Anthropocene. In my first data chapter, I measured the functional impact of spongivorous fishes by quantifying sponge biomass consumption on Wakatobi reefs. Video analysis identified 33 species from 10 families of reef fish grazing on Xestospongia spp., although 95% of bites were taken by only 11 species. Gut content analysis indicated that Pygoplites diacanthus and Pomacanthus imperator were obligate spongivores and Pomacanthus xanthometopon, Zanclus cornutus and Siganus punctatus regularly consumed sponges. In situ feeding observations revealed that sponges from the family Petrosiidae are preferred by P. diacanthus and Z. cornutus. Spongivores were estimated to consume 46.6 ± 18.3 g sponge 1000 m- 2 of reef day-1 and P. diacanthus had the greatest predatory impact on sponges. While estimates provided here are conservative and likely underestimate the true magnitude of spongivory on Indo-Pacific coral reefs, this chapter provides the first known estimate of reef wide sponge biomass consumption. Comparisons with published data estimating coral consumption by Chaetodontids in the Pacific suggests that biomass transferred through both pathways is similar in magnitude. Hence spongivory is an important, yet overlooked, trophic pathway on Indo-Pacific reefs. In my second data chapter, I developed genetic methods to identify sponges from the stomach contents of spongivorous angelfishes sampled in my first chapter. A range of primers and associated predator-blocking primers targeting the 18S rDNA gene were designed and tested on extracts of sponge and spongivore DNA. Sequences were successfully amplified from 14 sponges spanning 6 orders of Porifera, with the majority of samples identified belonging to the order Haplosclerida. This study is the first to successfully sequence sponges from the gut contents of spongivorous fishes. Sequence data indicated that Pygoplites diacanthus consumed sponges with considerable chemical defences and exhibited significant dietary plasticity within the Porifera phylum, similar to observations of angelfishes in the Caribbean and the eastern Pacific. In my third data chapter, I used stable isotope analysis to investigate differences in consumer niche widths and trophic diversity on the sponge-dominated Sampela reef system in comparison to an adjacent, higher quality reef. I measured the stable isotope ratios of coral reef fish representing different functional feeding groups, prey items and basal carbon sources at both sites. I used isotope data to calculate the trophic position and isotopic niches of each species and performed interspecific and inter-site comparisons. The fish assemblage had a significantly lower mean trophic position at the sponge-dominated site and the majority of species had wider isotopic niches, in accordance with optimal foraging theory which supports expansion in niche widths when per capita prey is low. The fish assemblage sampled at the sponge-dominated site used a significantly lower range of resources, had lower trophic diversity and obtained more carbon from benthic production than fish from the higher quality reef site. Results indicate a simpler trophic structure at the sponge-dominated site characterised by fish with more similar diets. Whilst trophic niche expansion may facilitate population survival in the short term, it can be expected to lead to intensified competition for increasingly scarce resources. In my final data chapter, I investigated niche partitioning and organic matter contributions to co-occurring temperate sponges. I sampled the stable isotope ratios of five abundant sponge species at 10 m and 30 m at two sites at opposing ends of Doubtful Sound, Fiordland. I also used an ROV to opportunistically sample sponges at depths >50 m and measured stable isotope ratios of picoplankton (</p>

Stable Isotopes of Platinum: Measurement and Application to Constraining the Formation and Differentiation of Earth

<p>A wide range of novel, non-traditional, stable isotope systems have been developed over the last decade, largely as a result of the advent of multiple-collector inductively coupled plasma mass spectrometry (MC-ICPMS), and continue to provide valuable new insights in the earth, environmental and planetary sciences. The platinum (Pt) stable isotope system represents a potentially powerful but, as yet, unexplored addition to this suite of stable isotope tracers. Pt has six naturally occurring isotopes, and can exist in a range of oxidation states. The geochemical behaviour of Pt coupled with the relatively large mass difference (ca. 2%) between the abundant heavy and light isotopes and its variable oxidation states leads to potential applications in tracing a range of natural processes. In particular, the strong elemental partitioning of Pt between metals and silicates makes the Pt stable isotope system uniquely suited to tracing processes of Earth’s accretion and differentiation. This study aims to develop new techniques for measurement of Pt stable isotopes in geological samples, and to apply these to terrestrial and meteorite samples to attempt to resolve outstanding questions relating to Earth’s early evolution. A technique was developed for measurement of Pt stable isotope ratios using multiple collector inductively coupled plasma mass spectrometry (MCICPMS), employing a ¹⁹⁶Pt–¹⁹⁸Pt double-spike to correct for instrumental mass fractionation. Results are reported in terms of δ¹⁹⁸Pt, which represents the per mil difference in the ¹⁹⁸Pt/¹⁹⁴Pt ratio from the IRMM-010 Pt isotope standard. A range of analytical tests were conducted and show that this approach has a reproducibility of ca. ±0.04 %∘ on δ¹⁹⁸Pt (i.e., ±0.01%∘ amu⁻¹) for Pt solution standards, and is insensitive to minor amounts of matrix that may be retained after chemical purification of Pt. Measurements of Pt solution standards conducted using two different MC-ICPMS instruments showed resolvable variations, which suggest that natural fractionations exist that exceed the reproducibility of the technique. Techniques were also developed for dissolution of natural samples and chemical separation of Pt. Geological standards were digested using a nickel sulphide fire assay technique, which pre-concentrates the highly siderophile elements in a NiS bead that is readily dissolved in acid. This was followed by chemical separation of Pt from digested samples using anion exchange chemical techniques. Elution curves were constructed for a range of synthetic rock matrices. These tests show that Pt separation is achieved with >90% Pt yield and ca. 95% purity. Analytical tests show that this level of Pt separation is sufficient for accurate determination of Pt stable isotope ratios by double-spike MC-ICPMS. These techniques were then applied to 11 international geological standard reference materials representing mantle peridotites, igneous samples, and Pt ore materials. The reproducibility in natural samples was determined by processing multiple replicate digestions of a standard reference material, and was shown to be ca. ±0.08%∘ (2 sd). Pt stable isotope data for the full set of reference materials have a range of δ¹⁹⁸Pt values with offsets of up to 0.40%∘ from the IRMM-010 standard, which are readily resolved with this technique. Mantle samples yielded the lightest (most negative) isotopic compositions of the terrestrial standards, with igneous and Pt ore samples defining a continuous trend towards zero, which is consistent with the IRMM-010 standard being derived from a Pt ore. These results demonstrate the potential of the Pt isotope system as a tracer in geochemical systems. The techniques developed above were then applied to investigate an outstanding problem relating to Earth’s accretion and differentiation. Highly siderophile elements (HSE) are strongly partitioned into the cores of terrestrial planets during core formation, and the abundances of HSE in Earth’s mantle compared with primitive meteorites have provided key constraints on models of Earth’s early evolution. Two leading models to explain the HSE abundances in the silicate Earth involve either a late-veneer of chondritic material that was added after core formation or core formation in a deep magma ocean. The platinum (Pt) stable isotope system represents a novel tool for investigating these processes. Using the techniques developed above, Pt stable isotope ratios were measured in a range of meteorite samples, including enstatite, ordinary and carbonaceous chondrites, primitive achondrites, achondrites and iron meteorites, as well as additional terrestrial mantle xenolith samples. Our data set reveals that the Pt stable isotopic composition of Earth’s mantle overlaps with all of the chondrite groups. Primitive achondrite and ureilite samples revealed the heaviest compositions of all meteorite groups. These data suggest that metal–silicate differentiation produces an isotopic fractionation for Pt, with heavy isotopes being preferentially retained in the silicate phase. Thus, Earth’s mantle is expected to have been significantly enriched in the heavy isotopes of Pt during core formation, even if metal–silicate differentiation took place in a magma ocean. The absence of a large fractionation between chondrites, representing the composition of the undifferentiated Earth, and the mantle suggests that the signature of core formation in the mantle has been subsequently overprinted. Considering the overlap between the Pt stable isotopic compositions of the mantle and chondrites, the most likely means for overprinting the composition of the mantle is by addition of a chondritic late-veneer. Mixing calculations show that addition of 0.5% of Earth’s mass by a late-veneer of chondritic material would be sufficient to overprint highly fractionated Pt stable isotope signatures resulting from core-formation.</p>

Stable Isotopes of Platinum: Measurement and Application to Constraining the Formation and Differentiation of Earth

<p>A wide range of novel, non-traditional, stable isotope systems have been developed over the last decade, largely as a result of the advent of multiple-collector inductively coupled plasma mass spectrometry (MC-ICPMS), and continue to provide valuable new insights in the earth, environmental and planetary sciences. The platinum (Pt) stable isotope system represents a potentially powerful but, as yet, unexplored addition to this suite of stable isotope tracers. Pt has six naturally occurring isotopes, and can exist in a range of oxidation states. The geochemical behaviour of Pt coupled with the relatively large mass difference (ca. 2%) between the abundant heavy and light isotopes and its variable oxidation states leads to potential applications in tracing a range of natural processes. In particular, the strong elemental partitioning of Pt between metals and silicates makes the Pt stable isotope system uniquely suited to tracing processes of Earth’s accretion and differentiation. This study aims to develop new techniques for measurement of Pt stable isotopes in geological samples, and to apply these to terrestrial and meteorite samples to attempt to resolve outstanding questions relating to Earth’s early evolution. A technique was developed for measurement of Pt stable isotope ratios using multiple collector inductively coupled plasma mass spectrometry (MCICPMS), employing a ¹⁹⁶Pt–¹⁹⁸Pt double-spike to correct for instrumental mass fractionation. Results are reported in terms of δ¹⁹⁸Pt, which represents the per mil difference in the ¹⁹⁸Pt/¹⁹⁴Pt ratio from the IRMM-010 Pt isotope standard. A range of analytical tests were conducted and show that this approach has a reproducibility of ca. ±0.04 %∘ on δ¹⁹⁸Pt (i.e., ±0.01%∘ amu⁻¹) for Pt solution standards, and is insensitive to minor amounts of matrix that may be retained after chemical purification of Pt. Measurements of Pt solution standards conducted using two different MC-ICPMS instruments showed resolvable variations, which suggest that natural fractionations exist that exceed the reproducibility of the technique. Techniques were also developed for dissolution of natural samples and chemical separation of Pt. Geological standards were digested using a nickel sulphide fire assay technique, which pre-concentrates the highly siderophile elements in a NiS bead that is readily dissolved in acid. This was followed by chemical separation of Pt from digested samples using anion exchange chemical techniques. Elution curves were constructed for a range of synthetic rock matrices. These tests show that Pt separation is achieved with >90% Pt yield and ca. 95% purity. Analytical tests show that this level of Pt separation is sufficient for accurate determination of Pt stable isotope ratios by double-spike MC-ICPMS. These techniques were then applied to 11 international geological standard reference materials representing mantle peridotites, igneous samples, and Pt ore materials. The reproducibility in natural samples was determined by processing multiple replicate digestions of a standard reference material, and was shown to be ca. ±0.08%∘ (2 sd). Pt stable isotope data for the full set of reference materials have a range of δ¹⁹⁸Pt values with offsets of up to 0.40%∘ from the IRMM-010 standard, which are readily resolved with this technique. Mantle samples yielded the lightest (most negative) isotopic compositions of the terrestrial standards, with igneous and Pt ore samples defining a continuous trend towards zero, which is consistent with the IRMM-010 standard being derived from a Pt ore. These results demonstrate the potential of the Pt isotope system as a tracer in geochemical systems. The techniques developed above were then applied to investigate an outstanding problem relating to Earth’s accretion and differentiation. Highly siderophile elements (HSE) are strongly partitioned into the cores of terrestrial planets during core formation, and the abundances of HSE in Earth’s mantle compared with primitive meteorites have provided key constraints on models of Earth’s early evolution. Two leading models to explain the HSE abundances in the silicate Earth involve either a late-veneer of chondritic material that was added after core formation or core formation in a deep magma ocean. The platinum (Pt) stable isotope system represents a novel tool for investigating these processes. Using the techniques developed above, Pt stable isotope ratios were measured in a range of meteorite samples, including enstatite, ordinary and carbonaceous chondrites, primitive achondrites, achondrites and iron meteorites, as well as additional terrestrial mantle xenolith samples. Our data set reveals that the Pt stable isotopic composition of Earth’s mantle overlaps with all of the chondrite groups. Primitive achondrite and ureilite samples revealed the heaviest compositions of all meteorite groups. These data suggest that metal–silicate differentiation produces an isotopic fractionation for Pt, with heavy isotopes being preferentially retained in the silicate phase. Thus, Earth’s mantle is expected to have been significantly enriched in the heavy isotopes of Pt during core formation, even if metal–silicate differentiation took place in a magma ocean. The absence of a large fractionation between chondrites, representing the composition of the undifferentiated Earth, and the mantle suggests that the signature of core formation in the mantle has been subsequently overprinted. Considering the overlap between the Pt stable isotopic compositions of the mantle and chondrites, the most likely means for overprinting the composition of the mantle is by addition of a chondritic late-veneer. Mixing calculations show that addition of 0.5% of Earth’s mass by a late-veneer of chondritic material would be sufficient to overprint highly fractionated Pt stable isotope signatures resulting from core-formation.</p>