Karen E. Arthur

Chemical Defenses: From Compounds to Communities

Marine natural products play critical roles in the chemical defense of many marine organisms and in some cases can influence the community structure of entire ecosystems. Although many marine natural products have been studied for biomedical activity, yielding important information about their biochemical effects and mechanisms of action, much less is known about ecological functions. The way in which marine consumers perceive chemical defenses can influence their health and survival and determine whether some natural products persist through a food chain. This article focuses on selected marine natural products, including okadaic acid, brevetoxins, lyngbyatoxin A, caulerpenyne, bryostatins, and isocyano terpenes, and examines their biosynthesis (sometimes by symbiotic microorganisms), mechanisms of action, and biological and ecological activity. We selected these compounds because their impacts on marine organisms and communities are some of the best-studied among marine natural products. We discuss the effects of these compounds on consumer behavior and physiology, with an emphasis on neuroecology. In addition to mediating a variety of trophic interactions, these compounds may be responsible for community-scale ecological impacts of chemically defended organisms, such as shifts in benthic and pelagic community composition. Our examples include harmful algal blooms; the invasion of the Mediterranean by Caulerpa taxifolia; overgrowth of coral reefs by chemically rich macroalgae and cyanobacteria; and invertebrate chemical defenses, including the role of microbial symbionts in compound production.

Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids.

Effective conservation strategies for highly migratory species must incorporate information about long-distance movements and locations of high-use foraging areas. However, the inherent challenges of directly monitoring these factors call for creative research approaches and innovative application of existing tools. Highly migratory marine species, such as marine turtles, regularly travel hundreds or thousands of kilometers between breeding and feeding areas, but identification of migratory routes and habitat use patterns remains elusive. Here we use satellite telemetry in combination with compound-specific isotope analysis of amino acids to confirm that insights from bulk tissue stable isotope analysis can reveal divergent migratory strategies and within-population segregation of foraging groups of critically endangered leatherback sea turtles (Dermochelys coriacea) across the Pacific Ocean. Among the 78 turtles studied, we found a distinct dichotomy in δ15N values of bulk skin, with distinct “low δ15N” and “high δ15N” groups. δ15N analysis of amino acids confirmed that this disparity resulted from isotopic differences at the base of the food chain and not from differences in trophic position between the two groups. Satellite tracking of 13 individuals indicated that their bulk skin δ15N value was linked to the particular foraging region of each turtle. These findings confirm that prevailing marine isoscapes of foraging areas can be reflected in the isotopic compositions of marine turtle body tissues sampled at nesting beaches. We use a Bayesian mixture model to show that between 82 and 100% of the 78 skin-sampled turtles could be assigned with confidence to either the eastern Pacific or western Pacific, with 33 to 66% of all turtles foraging in the eastern Pacific. Our forensic approach validates the use of stable isotopes to depict leatherback turtle movements over broad spatial ranges and is timely for establishing wise conservation efforts in light of this species’ imminent risk of extinction in the Pacific.

A comparison of immature green turtles (Chelonia mydas) diets among seven sites in the main Hawaiian islands

ABSTRACT Understanding resource acquisition and feeding ecology of threatened species is integral to their conservation because diet is intimately linked with growth rate and reproductive output. We examined diets of immature green sea turtles, Chelonia mydas (L.), from seven sites on the islands of Hawai‘i, O‘ahu, Moloka‘i, and Lāna‘i in January and August 2003. Diet analysis was based on 191 samples collected from 181 live green turtles by stomach lavage. These samples were identified and quantified using dissection microscopy and the principles of microstereology. Diet of green turtles in the Main Hawaiian Islands was dominated by red algae, and diet items most commonly encountered were Acanthophora spicifera (an introduced species), Hypnea sp., Pterocladiella sp., and Cladophora sp. Sea grasses (Halophila hawaiiana and H. decipiens) were an important component of diet in turtles from Kāne‘ohe Bay. Content of green turtle diets differed among foraging grounds, and these differences may provide an insight into previously documented differences in turtle growth rates among sites.

Phylogenetic and Chemical Diversity of Three Chemotypes of Bloom-Forming Lyngbya Species (Cyanobacteria: Oscillatoriales) from Reefs of Southeastern Florida

ABSTRACT The cyanobacterial genus Lyngbya includes free-living, benthic, filamentous cyanobacteria that form periodic nuisance blooms in lagoons, reefs, and estuaries. Lyngbya spp. are prolific producers of biologically active compounds that deter grazers and help blooms persist in the marine environment. Here, our investigations reveal the presence of three distinct Lyngbya species on nearshore reefs in Broward County, FL, sampled in 2006 and 2007. With a combination of morphological measurements, molecular biology techniques, and natural products chemistry, we associated these three Lyngbya species with three distinct Lyngbya chemotypes. One species, identified as Lyngbya cf. confervoides via morphological measurements and 16S rRNA gene sequencing, produces a diverse array of bioactive peptides and depsipeptides. Our results indicate that the other two Lyngbya species produce either microcolins A and B or curacin D and dragonamides C and D. Results from screening for the biosynthetic capacity for curacin production among the three Lyngbya chemotypes in this study correlated that capacity with the presence of curacin D. Our work on these bloom-forming Lyngbya species emphasizes the significant phylogenetic and chemical diversity of the marine cyanobacteria on southern Florida reefs and identifies some of the genetic components of those differences.

A review of the potential role of tumour-promoting compounds produced by Lyngbya majuscula in marine turtle fibropapillomatosis

Harmful algal blooms (HABs) have increased in abundance and severity in recent decades. Whereas the implications for human impacts and intoxication resulting from blooms have been extensively studied, the ecological implications of these microalgae are less well understood. Many HAB species produce biologically active, secondary metabolites and the fate of these toxins through the foodweb is generally not well understood unless it culminates in extensive fish mortalities or human poisonings. This review focusses on one HAB species, the cyanobacterium Lyngbya majuscula, and presents a hypothetical role for its involvement in fibropapillomatosis (FP), a neoplastic disease of marine turtles. FP is expressed as benign tumours that grow both internally and externally on marine turtles, preventing vision, movement and organ function. The aetiology of FP is currently not conclusively understood, but virus material has been associated with tumours and previous studies have suggested a role for naturally produced tumour promoters. In this review, we present a hypothesis regarding the involvement of L. majuscula in FP, either through direct intoxication and action of tumour-promoting compounds or indirectly by causing seagrass loss and compromised immune function, thus leaving the turtles more susceptible to disease.

Baseline blood biochemistry of Australian green turtles (Chelonia mydas) and effects of exposure to the toxic cyanobacterium Lyngbya majuscula

Quantifying health in wild marine turtles is challenging because reptiles have characteristically wide-ranging normal reference values for many indicators of health and because of the shortage of population-specific baseline data for wild animals. We measured blood biochemistry profiles (calcium, magnesium, sodium, lactate dehydrogenase (LDH), urea, cholesterol, triglycerides, and glucose) of green turtles (Chelonia mydas) in Moreton and Shoalwater Bays, Australia, and compared them in relation to capture site, age, sex and exposure to harmful algal blooms of the toxic cyanobacteria Lyngbya majuscula. Turtles were considered to be clinically healthy when no external injuries or lesions were observed and there was no evidence of disease or emaciation. Differences in blood profiles were detected between sites, but not between age groups or sexes. Turtles that were exposed to L. majuscula generally had lower plasma glucose concentrations and decreased LDH activity, which may represent a metabolic downregulation resulting from food limitation. This study provides the first blood biochemistry reference values for green turtles in Queensland, Australia, that can be used in future assessments of green turtles in these foraging habitats.

Opportunism on the High Seas: Foraging Ecology of Olive Ridley Turtles in the Eastern Pacific Ocean

Stable isotopic compositions in animal tissues have been widely used to gain insight into trophic dynamics, especially of mobile aquatic predators whose behavior and dietary preferences are difficult to directly measure. Olive ridley sea turtles (Lepidochelys olivacea) range across >3 million km2 of the tropical and subtropical eastern Pacific Ocean and their trophic ecology in open ocean areas has not yet been adequately described. Individuals feed within biogeographic regions where varying nutrient cycling regimes result in phytoplankton with distinct δ13C and δ15N values that are assimilated by the turtles. We sampled 346 turtles at-sea between 2003 and 2009 and used bulk tissue (n = 346) and amino acid compound specific isotope analysis (AA-CSIA, n = 31) to empirically support the conventional understanding that olive ridleys are omnivores. Bulk δ15N values did not significantly vary with carapace length, a proxy for age, or with putative sex of adults. We therefore hypothesize that trophic position (TP) does not vary across age or sex. In line with other isotopic studies of this biogeographic scale in the same region, we observed a trend of bulk tissue 15N enrichment with increasing latitude. Using AA-CSIA to account for δ15N baseline shifts among food webs (space), we estimated the TP of adult foragers using two methods. We found that across their eastern Pacific range, olive ridley δ13C and δ15N niche area varied, but median TP of adults remained constant (~3.1). Using the simpler, two-amino acid TP estimation method, we detected a small but notable elevation of TP for olive ridleys on the Costa Rica Dome. This study underscores the value of large-scale in-water olive ridley sea turtle research across oceanic foraging habitats to confirm or challenge anecdotal understanding of trophic roles, susceptibility to environmental change, and critical habitats. Further, it improves our understanding of why this species is now abundant in the eastern Pacific Ocean. A prey generalist with plenty of suitable foraging habitat can recover from the brink of extinction despite the presence of major threats. However, such foraging characteristics may require dynamic open ocean management approaches to meet conservation objectives if threats persist and/or increase.