Caitlin R. Fong

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway

The evolutionary histories of complex traits are complicated because such traits are comprised of multiple integrated and interacting components, which may have different individual histories. Phylogenetic studies of complex trait evolution often do not take this into account, instead focusing only on the history of whole, integrated traits; for example, mapping eyes as simply present or absent through history. Using the biochemistry of animal vision as a model, we demonstrate how investigating the individual components of complex systems can aid in elucidating both the origins and diversification of such systems. Opsin-based phototransduction underlies all visual phenotypes in animals, using complex protein cascades that translate light information into changes in cyclic nucleotide gated (CNG) or canonical transient receptor potential (TRPC) ion-channel activity. Here we show that CNG ion channels play a role in cnidarian phototransduction. Transcripts of a CNG ion channel co-localize with opsin in specific cell types of the eyeless cnidarian Hydra magnipapillata. Further, the CNG inhibitor cis-diltiazem ablates a stereotypical photoresponse in the hydra. Our findings in the Cnidaria, the only non-bilaterian lineage to possess functional opsins, allow us to trace the history of CNG-based photosensitivity to the very origin of animal phototransduction. Our general analytical approach, based on explicit phylogenetic analysis of individual components, contrasts the deep evolutionary history of CNG-based phototransduction, today used in vertebrate vision, with the more recent assembly of TRPC-based systems that are common to protostome (e.g. fly and mollusc) vision.

Cnidocyte discharge is regulated by light and opsin-mediated phototransduction.

BackgroundCnidocytes, the eponymous cell type of the Cnidaria, facilitate both sensory and secretory functions and are among the most complex animal cell types known. In addition to their structural complexity, cnidocytes display complex sensory attributes, integrating both chemical and mechanical cues from the environment into their discharge behavior. Despite more than a century of work aimed at understanding the sensory biology of cnidocytes, the specific sensory receptor genes that regulate their function remain unknown.ResultsHere we report that light also regulates cnidocyte function. We show that non-cnidocyte neurons located in battery complexes of the freshwater polyp Hydra magnipapillata specifically express opsin, cyclic nucleotide gated (CNG) ion channel and arrestin, which are all known components of bilaterian phototransduction cascades. We infer from behavioral trials that different light intensities elicit significant effects on cnidocyte discharge propensity. Harpoon-like stenotele cnidocytes show a pronounced diminution of discharge behavior under bright light conditions as compared to dim light. Further, we show that suppression of firing by bright light is ablated by cis-diltiazem, a specific inhibitor of CNG ion channels.ConclusionsOur results implicate an ancient opsin-mediated phototransduction pathway and a previously unknown layer of sensory complexity in the control of cnidocyte discharge. These findings also suggest a molecular mechanism for the regulation of other cnidarian behaviors that involve both photosensitivity and cnidocyte function, including diurnal feeding repertoires and/or substrate-based locomotion. More broadly, our findings highlight one novel, non-visual function for opsin-mediated phototransduction in a cnidarian, the origins of which might have preceded the evolution of cnidarian eyes.

Bolstered physical defences under nutrient‐enriched conditions may facilitate a secondary foundational algal species in the South Pacific

Summary 1.Humans have a long history of changing species’ ranges and habitat distributions, making studies of the ecological processes that may facilitate these changes of key importance, particularly in cases where a primary foundation species is replaced by another, less desirable species. 2.We investigated the impact of nutrients and herbivory on Turbinaria ornata, a secondary foundational macroalga that depends on and likely competes with coral, the primary foundational community. T. ornata is also rapidly expanding in range and habitat across the South Pacific. We conducted: 1) a mesocosm experiment assessing relative nutrient limitation, 2) a field experiment comparing importance of nutrients (+/-) and herbivory (+/-) to biomass accumulation, and 3) an herbivory assay and toughness test comparing enriched and ambient thalli to assess changes to anti-herbivory defences. 3.We found no evidence of growth being nutrient limited in T. ornata; rather than stimulating growth, nutrient addition deterred herbivores. However, when physical toughness was removed, enriched algae were preferred, with consumption rates 25-fold those of unenriched algae. Additionally, enriched thalli were tougher than ambient thalli, suggesting physical defences were bolstered by nutrient enrichment. 4.Synthesis. We found a unique interaction where nutrients inhibit herbivory and facilitate Turbinaria ornata biomass accumulation. While concern is often placed on degradation of foundation species via anthropogenic change, instead here we show that anthropogenic change can facilitate secondary foundation species. This facilitation may allow a secondary foundation species to better compete with primary foundation species. This article is protected by copyright. All rights reserved.

Sediments influence accumulation of two macroalgal species through novel but differing interactions with nutrients and herbivory

Despite increasing concern that sediment loads from disturbed watersheds facilitate algal dominance on tropical reefs, little is known of how sediments interact with two primary drivers of algal communities, nutrients and herbivory. We examined the effects of sediment loads on the thalli of two increasingly abundant genera of macroalgae, Galaxaura and Padina, in a bay subject to terrestrial sediment influx in Mo’orea, French Polynesia. Field experiments examining (1) overall effects of ambient sediments and (2) interacting effects of sediments (ambient/removal) and herbivores (caged/uncaged) demonstrated that sediments had strong but opposite effects on both species’ biomass accumulation. Sediment removal increased accumulation of Padina boryana Thivy 50% in the initial field experiment but had no effect in the second; rather, in a novel interaction, herbivores overcompensated for increases in tissue nutrient stores that occurred with sediments loads, likely by preferential consumption of nutrient-rich meristematic tissues. Despite negative effects of sediments on biomass, Padina maintained rapid growth across treatments in both experiments. In contrast, positive growth in Galaxaura divaricata Kjellman only occurred with ambient sediment loads. In mesocosm experiments testing interactions of added nutrients and sediments on growth, Galaxaura grew at equivalent rates with sediments (collected from thalli on the reef) as with additions of nitrate and phosphate, suggesting sediments provide a nutrient subsidy. For Padina, however, the only effect was a 50% reduction in growth with sediment. Overall, retention of thallus sediments creates a positive feedback that Galaxaura appears to require to sustain net growth, while Padina merely tolerates sediments. These results indicate that sediments can modify nutrient and herbivore control of algae in ways that differ among species, with the potential for strong and unexpected effects on the abundance and composition of tropical reef macroalgae.

High density and strong aggregation do not increase prevalence of the isopod Hemioniscus balani (Buchholz, 1866), a parasite of the acorn barnacle Chthamalus fissus (Darwin, 1854) in California

Parasitism is a common life history strategy among animals and has been the topic of empirical and theoretical study for decades. Many classic mathematical models assume increased spatial aggregation and density increase prevalence in a host population. Parasites can nevertheless take on a diversity of life history strategies that could result in deviations from these assumptions. I investigated the importance of density and aggregation of hosts on the prevalence, or percent of hosts infected by a parasitic castrator with a complex life cycle. An isopod parasite, Hemioniscus balani (Buchholz, 1866), infects an intertidal barnacle, Chthamalus fissus (Darwin, 1854), and renders the barnacle unable to produce eggs. To test the assumptions that density and aggregation increase parasitism, I conducted a survey of density, aggregation, and parasitism in the rocky intertidal zone in Santa Barbara County, CA, USA. I found spatial patterns of host density and aggregation did not lead to increases in parasitism. Furthermore, there was no evidence of a selfish herd effect, whereby the per capita risk of infection decreases with population size. Understanding patterns and drivers of infection is particularly important in marine systems, which are understudied compared to terrestrial diseases, and work done in terrestrial systems could not correspond to patterns and processes in marine systems.

A Rapidly Expanding Macroalga Acts as a Foundational Species Providing Trophic Support and Habitat in the South Pacific

Foundation species facilitate associated communities and provide key ecosystem functions, making anthropogenically driven phase-shifts involving these species critically important. One well-documented such phase-shift has been from coral to algal domination on tropical reefs. On South Pacific coral reefs, the macroalga Turbinaria ornata has expanded its range and habitat but, unlike algae that often dominate after phase-shifts, T. ornata is structurally complex and generally unpalatable to herbivores. Therefore, it may serve a foundational role on coral reefs, such as providing habitat structure to more palatable primary producers and corresponding trophic support to fishes. We predicted increasing T. ornata density would facilitate growth of associated algae, resulting in a positive trophic cascade to herbivorous fish. An experiment manipulating T. ornata densities showed a unimodal relationship between T. ornata and growth of understory algae, with optimal growth occurring at the most frequent natural density. Epiphyte cover also increased with density until the same optimum, but remained high with greater T. ornata densities. Foraging by herbivorous fishes increased linearly with T. ornata density. An herbivore exclusion experiment confirmed T. ornata facilitated epiphytes, but resource use of epiphytes by herbivores, though significant, was not affected by T. ornata density. Therefore, T. ornata performs foundational roles because it provides novel habitat to understory and epiphytic macroalgae and trophic support to consumers, though likely this function is at the expense of the original foundational corals.

Nutrient Fluctuations in Marine Systems: Press Versus Pulse Nutrient Subsidies Affect Producer Competition and Diversity in Estuaries and Coral Reefs

Resource subsidy regimes, which range from presses to pulses, are common structuring forces in communities, yet research contrasting their effects is lacking. Many coastal marine ecosystems, including estuaries and coral reefs, have experienced increased nutrient subsidies while concurrently shifting to macroalgal dominance; however, the role of subsidy regime in transitions remains unknown. We created concentration–frequency distributions of nutrients in Cook’s Bay, Moorea, French Polynesia, and Carpinteria Salt Marsh Reserve, CA, USA. Both showed relatively high pulses interspersed by press concentrations. We grew dominant macroalgae alone and together in microcosms approximating these subsidy regimes to quantify individual performance and competitive outcomes. Subsidy regime changed growth and competitive abilities of macroalgae from both ecosystems but with divergent effects. In nutrient-limited reefs, different species were favoured under each enrichment regime, suggesting a fluctuating nutrient environment enhances diversity. In contrast, in eutrophic estuaries, enrichment of both regimes facilitated a single competitive dominant, suppressing diversity. Functional form groups did not predict responses to subsidy regime, likely because classifications ignore temporal variability in resource supplies. Because climate change will alter rainfall patterns globally, further accelerating nutrient subsidies from land to sea, understanding species’ responses to nutrient subsidy regimes is key to predicting the fate of coastal communities.

Epibionts on Turbinaria ornata, a secondary foundational macroalga on coral reefs, provide diverse trophic support to fishes

Worldwide, many coral reef ecosystems have shifted from coral to algal dominance, yet the ecological function of these emergent communities remains relatively unknown. Turbinaria ornata, a macroalga with a rapidly expanding range in the South Pacific, forms dense stands on hard substrate, likely providing ecological services unique from corals. While generally unpalatable, T. ornata can function as a secondary foundation species and hosts an epibiont community that may provide overlooked trophic resources in phase shifted reef ecosystems. Results from video recorded field experiments designed to quantify consumer pressure on T. ornata epibionts showed that both consumer pressure and epibiont cover increased with thallus size. Additionally, most fish species, including herbivores, omnivores, and detritivores, exhibited higher bite rates on thalli with epibionts compared to thali with epibionts experimentally removed. Juvenile parrotfishes were responsible for 50% of total bites recorded and also had the highest bite rates. Results indicate that epibionts, particularly on large T. ornata, are a food resource for a diversity of fishes, representing a previously undescribed function of this macroalga in coral reef ecosystems. Exploring the functions of macroalgal dominated reef communities will be increasingly important as reefs continue to phase shift toward macroalgal dominance in the Anthropocene.

Empirical data demonstrates risk-tradeoffs between landscapes for herbivorous fish may promote reef resilience

Herbivores balance resource requirements with predation risk, which can differ among landscapes; hence, landscape can shape these trade-offs, influencing herbivore distribution and behavior. While this paradigm has been well established on coral-dominated reefs, tropical reefs worldwide are shifting to algal dominance. If herbivores avoid algae due to higher risk and forage in coral, these algal states may be stabilized. However, if herbivores forage more in resource-rich algal states, this may promote coral recovery. We assessed the distribution and behavior of herbivorous fishes in Moorea, French Polynesia in coral and algal turf-dominated fringing reef sites. Acanthuridae were more abundant in coral states and Labridae, tribe Scarinae, in algal turf states, though total fish abundances were equivalent in the two states. Fish in both families spent more time feeding in algal states and hiding/swimming in coral states. Thus, behavior reflects the trade-off between resource acquisition and refuge in these two landscapes and may promote recovery to coral.