Toward a Solution of the “Peruvian Puzzle”: Pelagic Food-Web Structure and Trophic Interactions in the Northern Humboldt Current Upwelling System Off Peru

The northern Humboldt Current upwelling system (HCS) belongs to the most productive marine ecosystems, providing five to eight times higher fisheries landings per unit area than other coastal upwelling systems. To solve this “Peruvian puzzle”, to elucidate the pelagic food-web structure and to better understand trophic interactions in the HCS, a combined stable isotope and fatty acid trophic biomarker approach was adopted for key zooplankton taxa and higher trophic positions with an extensive spatial coverage from 8.5 to 16°S and a vertical range down to 1,000 m depth. A pronounced regional shift by up to ∼5‰ in the δ15N baseline of the food web occurred from North to South. Besides regional shifts, δ15N ratios of particulate organic matter (POM) also tended to increase with depth, with differences of up to 3.8‰ between surface waters and the oxygen minimum zone. In consequence, suspension-feeding zooplankton permanently residing at depth had up to ∼6‰ higher δ15N signals than surface-living species or diel vertical migrants. The comprehensive data set covered over 20 zooplankton taxa and indicated that three crustacean species usually are key in the zooplankton community, i.e., the copepods Calanus chilensis at the surface and Eucalanus inermis in the pronounced OMZ and the krill Euphausia mucronata, resulting in an overall low number of major trophic pathways toward anchovies. In addition, the semi-pelagic squat lobster Pleuroncodes monodon appears to play a key role in the benthic-pelagic coupling, as indicated by highest δ13C’ ratios of −14.7‰. If feeding on benthic resources and by diel vertical migration, they provide a unique pathway for returning carbon and energy from the seafloor to the epipelagic layer, increasing the food supply for pelagic fish. Overall, these mechanisms result in a very efficient food chain, channeling energy toward higher trophic positions and partially explaining the “Peruvian puzzle” of enormous fish production in the HCS.

The importance of direct and indirect trophic interactions in determining the presence of a locally rare day-flying moth

Ecosystem engineers affect other organisms by creating, maintaining or modifying habitats, potentially supporting species of conservation concern. However, it is important to consider these interactions alongside non-engineering trophic pathways. We investigated the relative importance of trophic and non-trophic effects of an ecosystem engineer, red deer, on a locally rare moth, the transparent burnet (Zygaena purpuralis). This species requires specific microhabitat conditions, including the foodplant, thyme, and bare soil for egg-laying. The relative importance of grazing (i.e., trophic effect of modifying microhabitat) and trampling (i.e., non-trophic effect of exposing bare soil) by red deer on transparent burnet abundance is unknown. We tested for these effects using a novel method of placing pheromone-baited funnel traps in the field. Imago abundance throughout the flight season was related to plant composition, diversity and structure at various scales around each trap. Indirect effects of red deer activity were accounted for by testing red deer pellet and trail presence against imago abundance. Imago abundance was positively associated with thyme and plant diversity, whilst negatively associated with velvet grass and heather species cover. The presence of red deer pellets and trails were positively associated with imago abundance. The use of these sites by red deer aids the transparent burnet population via appropriate levels of grazing and the provision of a key habitat condition, bare soil, in the form of deer trails. This study shows that understanding how both trophic and non-trophic interactions affect the abundance of a species provides valuable insights regarding conservation objectives.

The Combined Effects of Warming and Body Size on the Stability of Predator-Prey Interactions

Environmental temperature and body size are two prominent drivers of predation. Despite the ample evidence of their independent effects, the combined impact of temperature and predator-prey body size ratio on the strength and stability of trophic interactions is not fully understood. We experimentally tested how water temperature alters the functional response and population stability of dragonfly nymphs (Cordulegaster boltonii) feeding on freshwater amphipods (Gammarus pulex) across a gradient of their body size ratios. Attack coefficients were highest for small predators feeding on small prey at low temperatures, but shifted toward the largest predators feeding on larger prey in warmer environments. Handling time appeared to decrease with increasing predator and prey body size in the cold environment, but increase at higher temperatures. These findings indicate interactive effects of temperature and body size on functional responses. There was also a negative effect of warming on the stability of predator and prey populations, but this was counteracted by a larger predator-prey body size ratio at higher temperatures. Here, a greater Hill exponent reduced feeding at low prey densities when predators were much larger than their prey, enhancing the persistence of both predator and prey populations in the warmer environment. These experimental findings provide new mechanistic insights into the destabilizing effect of warming on trophic interactions and the key role of predator-prey body size ratios in mitigating these effects.

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>