DNA metabarcoding reveals fine scale geographical differences of consumed algae in the Galápagos marine iguanas (Amblyrhynchus cristatus)

Galápagos marine iguanas are primarily associated with the marine environment and show special nutritional adaptations. They are the only lizards worldwide that forage on marine macroalgae. Until now, consumed algae have been identified by direct observations during their feeding activities and microscopic identification in faeces samples. In this study, we use a novel DNA metabarcoding approach to identify consumed algal species from the faeces of marine iguanas. We developed primers for the ribulose-bisphosphate carboxylase (rbcL) gene and applied a metabarcoding approach to 25 individual faeces samples collected in four representative sites of two subspecies (Amblyrhynchus cristatus mertensi and A. c. godzilla), found in the San Cristóbal Island. We detected 18 consistently occurring macroalgal operational taxonomic units (OTUs). Most of the OTUs were assigned to Rhodophyta (red algae) and only one OTU to Chlorophyta (green algae). Despite the number of consumed algal species did not differ between two subspecies (OTU richness; P = 0.383), diet overlap level between A. c. mertensi and A. c. godzilla was low (Schoener index = 0.345), suggesting that both subspecies consumed different algal species in their natural environment. Further studies are needed to understand whether the difference of consumed algae reflects disparities in the abundance of algal species between sites, or whether iguanas of the two genetically differentiated subspecies prefer distinct algal species.

Exuberant Life

Why is Galápagos so endlessly fascinating, whether to read about, to visit, or both? Reasons include its menagerie of truly unusual organisms (like tree daisies, marine iguanas, and flightless cormorants), its relatively low human impact (most of its endemic biodiversity is still extant), and its unrivalled role in the history of science ever since Charles Darwin. Exuberant Life offers a contemporary synthesis of what is known about the evolution of the curiously wonderful organisms of Galápagos, of how they are faring in the tumultuous world of human-induced change, and how evolution can guide efforts today for their conservation. In eight case-study chapters, the book looks at each organism’s ancestry, at how and when it came to Galápagos, and how and why it changed since its arrival, all with an eye to its conservation today. Such analysis often provides surprises and suggestions not previously considered, like the potential benefits to joint conservation efforts with tree daisies and tree finches, for example, or ways that a new explanation for peculiar behaviors in Nazca and blue-footed boobies can benefit both species today. In each chapter, a social-ecological systems framework is used, because human influence is always present, and because it allows an explicit link to evolution. We see how the evolutionary fitnesses of Galápagos organisms are now a product of both ecological conditions and human impact, including climate change. Historically, Galápagos has played a central role in the understanding of evolution; what it now offers to teach us about conservation may well prove indispensable for the future of the planet.

Beautiful on the Inside

Marine iguanas stand in stark contrast to the Galápagos rails. They vary enormously in space by size and color, supporting classification into 11 subspecies (whereas rails are monotypic). And they vary in time, especially males, which change to bright colors in the mating season—some to the point of being bright red and green “Christmas iguanas.” They vary over time in an additional special way: iguanas shrink up to 20% (or 2.7 inches) during the food scarcity of El Niño events. They have evolved the capacity to shut down their normal stress response when the ocean gets warm, thus becoming quiescent and riding out the storm. The larger the iguanas, the more they shrink and the longer they survive. Furthermore, nearly all marine iguana subspecies have increased in size since 1905, while, at the same time, climate change has made El Niño events stronger and longer. Could climate change be driving the evolution of larger marine iguanas? Will iguanas be able to keep up as El Niño worsens?

Out of the Ordinary

Galápagos stands out for its vast collection of extreme life: the world’s only tropical albatross, its only flightless cormorants, and its marine iguanas; three colorful species of boobies; and 15 species of giant tortoises, one on each major volcano, except for one especially large volcano that has two. Each of these organisms has evolved adaptations to the unique rigors of life in an isolated archipelago on the equator. As Galápagos has recently grown ever more connected to the world system, many species’ adaptations have become vulnerabilities in the face of human-induced change. Fortunately, long before people arrived, evolution also endowed native species with forms of resilience to local perturbations like El Niño events and periodic droughts. The eight case studies in this book highlight these vulnerabilities and resiliences and argue that the mismatch between them, stemming from human impact, is the core conservation challenge today.

No impact of a short-term climatic “El Niño” fluctuation on gut microbial diversity in populations of the Galápagos marine iguana (Amblyrhynchus cristatus)

Gut microorganisms are crucial for many biological functions playing a pivotal role in the host’s well-being. We studied gut bacterial community structure of marine iguana populations across the Galápagos archipelago. Marine iguanas depend heavily on their specialized gut microbiome for the digestion of dietary algae, a resource whose growth was strongly reduced by severe “El Niño”-related climatic fluctuations in 2015/2016. As a consequence, marine iguana populations showed signs of starvation as expressed by a poor body condition. Body condition indices (BCI) varied between island populations indicating that food resources (i.e., algae) are affected differently across the archipelago during ‘El Niño’ events. Though this event impacted food availability for marine iguanas, we found that reductions in body condition due to “El Niño”-related starvation did not result in differences in bacterial gut community structure. Species richness of gut microorganisms was instead correlated with levels of neutral genetic diversity in the distinct host populations. Our data suggest that marine iguana populations with a higher level of gene diversity and allelic richness may harbor a more diverse gut microbiome than those populations with lower genetic diversity. Since low values of these diversity parameters usually correlate with small census and effective population sizes, we use our results to propose a novel hypothesis according to which small and genetically less diverse host populations might be characterized by less diverse microbiomes. Whether such genetically depauperate populations may experience additional threats from reduced dietary flexibility due to a limited intestinal microbiome is currently unclear and calls for further investigation.

Trophic niche differentiation mirrors intra-island population structure of Galápagos marine iguanas (Amblyrhynchus cristatus)

Background: Differences in the trophic niche often underlie ecological specialization of individuals and can promote ecological speciation of populations, but studies showing a link between differences in the trophic niche and genetic differentiation of populations are rare. On the island of San Cristóbal (Galapágos archipelago), a strong genetic differentiation between two relatively proximate populations (subspecies; Amblyrhynchus cristatus mertensi and A. c. godzilla) of marine iguanas along the coastline has been observed. Here, we explore whether this genetic differentiation is mirrored in the iguanas’ trophic niche. Results: Although, no significant difference in the number of consumed algal taxa between subspecies were detected, the Schoener index exhibited low diet overlap between A. c. mertensi and A. c. godzilla. The latter was also demonstrated by the PERMANOVA analysis with significantly different diet OTU composition from the fecal samples between subspecies. Stable isotope analysis revealed that subspecies identity was overall more important than site for the iguanas’ resource use. Conclusions: By applying a metabarcoding approach on feces samples in combination with stable isotope analysis of skin sheds, we found that A. c. mertensi and A. c. godzilla differ in their ecological niches. Moreover, stable isotope analysis indicated that marine iguana populations have low spatial foraging distances, which, together with the diet partitioning patterns, might explain, at least partially, the lack of gene flow between these geographically proximate marine iguana populations. Key words: diet analysis, trophic niche, metabarcoding, stable isotopes, marine iguanas, Amblyrhynchus cristatus

Pronocephaloid cercariae (Platyhelminthes: Trematoda) from gastropods of the Queensland coast, Australia

The superfamily Pronocephaloidea Looss, 1899 comprises digeneans occurring in the gut and respiratory organs of fishes, turtles, marine iguanas, birds and mammals. Although many life cycles are known for species of the Notocotylidae Lühe, 1909 maturing in birds and mammals, relatively few are known for the remaining pronocephaloid lineages. We report the cercariae of five pronocephaloid species from marine gastropods of the Queensland coast, Australia. From Lizard Island, northern Great Barrier Reef, we report three cercariae, two from Rhinoclavis vertagus (Cerithiidae) and one from Nassarius coronatus (Nassariidae). From Moreton Bay, southern Queensland, an additional two cercariae are reported from two genotypes of the gastropod worm shell Thylacodes sp. (Vermetidae). Phylogenetic analysis using 28S rRNA gene sequences shows all five species are nested within the Pronocephaloidea, but not matching or particularly close to any previously sequenced taxon. In combination, phylogenetic and ecological evidence suggests that most of these species will prove to be pronocephalids parasitic in marine turtles. The Vermetidae is a new host family for the Pronocephaloidea.