River Streamflow, Remotely Sensed Water Quality, and Benthic Composition of Previously Undescribed Nearshore Coral Reefs in Northern Puerto Rico

Land-based sediment stress represents a threat to many coral reefs in Puerto Rico primarily as a result of unrestricted land cover/land use changes and poor best management practices. The effects of such stresses have been documented along most coasts around the island. However, little attention has been paid to reefs located on the north coast, and very little is known about their composition and current state. Here, we present a study characterizing riverine inputs, water quality conditions, and benthic composition of two previously undescribed coral reefs (Tómbolo and Machuca reefs) located just eastward of the Río Grande de Manatí outlet in north-central Puerto Rico. This study utilizes a time series of remotely sensed ocean color products [diffuse vertical attenuation coefficient at 490 nm (Kd490) and chlorophyll-a concentration (Chl-a) estimated with data from the Visible Infrared Imaging Radiometer Suite (VIIRS)] to characterize water quality in this coastal region. In general, the months with relatively high mean daily river streamflow also coincide with months having the highest proportion of eastward wave direction, which can promote the eastward influence of river waters toward the two coral reefs sites. Kd490 and Chl-a showed a higher riverine influence closer to the watershed outlet. Kd490 and Chl-a monthly peaks also coincide with river streamflow highs, particularly at those pixels closer to shore. Tómbolo Reef, located farther eastward of the river outlet, shows a well-developed primary reef framework mainly composed of threatened reef-building species (Acropora palmata, Pseudodiploria) and high coral cover (19–51%). The benthos of Machuca Reef, located closer to the river outlet, is dominated by macroalgae with a significantly lower coral cover (0.2–2.7%) mainly composed of “weedy” coral species (Porites astreoides and Siderastrea radians). Cover of major benthic components correlates with distance from the river outlet, and with gradients in Kd490 and Chl-a, with higher coral cover and lower macroalgal cover farther from the river outlet. Coral cover at Tómbolo Reef is higher than what has been reported for similar sites around Puerto Rico and other Caribbean islands showing its ecological importance, and as up until now, an unrecognized potential refuge of reef-building threatened coral species.

Assisted gene flow using cryopreserved sperm in critically endangered coral

Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao–Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.

Differential Effects of Substrate Type and Genet on Growth of Microfragments of Acropora palmata

Global decline of coral reefs has led to a widespread adoption of asexual propagation techniques for coral restoration, whereby coral colonies are fragmented and allowed to re-grow before being returned to the reef. While this approach has become increasingly popular and successful, many questions remain regarding best practices to maximize restoration speed, efficiency, and survival. Two variables that may influence growth and survival of asexually fragmented colonies include coral genet and growth substrate. Here, we evaluate the effects of genet and substrate (commercially available ceramic vs. in-house made cement) on the survival and growth of 221 microfragments of elkhorn coral Acropora palmata over 193 days. All corals survived the experimental period, and doubled their initial size in 45 days, with an average growth of 545% over the study duration. Growth was generally linear, though the growth of some corals more closely matched logistic, logarithmic, or exponential curves. Both genet and substrate had significant effects on coral growth, though the two factors did not interact. Genet had a stronger influence on coral growth than substrate, with the fastest genet growing at 216% the rate of the slowest genet. Corals on cement substrate grew at 111.9% the rate of those grown on ceramic. This represents both a significant cost savings and elimination of logistical challenges to restoration practitioners, as the cement substrate ingredients are cheap and globally available. Our work shows that both genet and substrate should be considered when undertaking asexual restoration of Acropora palmata to maximize restoration speed and efficiency.

Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals

Coral reef health depends on an intricate relationship among the coral animal, photosynthetic algae, and a complex microbial community. The holobiont can impact the nutrient balance of their hosts amid an otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Here we use 15N-tracer experiments to produce the first simultaneous measurements of ammonium oxidation, nitrate reduction, and nitrous oxide (N2O) production among five iconic species of reef-building corals (Acropora palmata, Diploria labyrinthiformis, Orbicella faveolata, Porites astreoides, and Porites porites) in the highly protected Jardines de la Reina reefs of Cuba. Nitrate reduction is present in most species, but ammonium oxidation is low potentially due to photoinhibition and assimilatory competition. Coral-associated rates of N2O production indicate a widespread potential for denitrification, especially among D. labyrinthiformis, at rates of ~1 nmol cm−2 d−1. In contrast, A. palmata displays minimal active nitrogen metabolism. Enhanced rates of nitrate reduction and N2O production are observed coincident with dark net respiration periods. Genomes of bacterial cultures isolated from multiple coral species confirm that microorganisms with the ability to respire nitrate anaerobically to either dinitrogen gas or ammonium exist within the holobiont. This confirmation of anaerobic nitrogen metabolisms by coral-associated microorganisms sheds new light on coral and reef productivity.

Reestablishing a stepping-stone population of the threatened elkhorn coral Acropora palmata to aid regional recovery

Recovery of the elkhorn coral Acropora palmata is critical to reversing coral reef ecosystem collapse in the western Atlantic, but the species is severely threatened. To gauge potential for the species’ restoration in Florida, USA, we conducted an assisted migration experiment where 50 coral fragments of 5 nursery-raised genetic strains (genets) from the upper Florida Keys were moved to 5 sites across 350 km of the offshore reef. Additionally, 4 fragments from the 1 remaining colony of A. palmata in Dry Tortugas National Park (DRTO) were added to the 2 DRTO experimental sites to test for local adaptation. To measure coral performance, we tracked coral survival, calcification, growth, and condition from May 2018 to October 2019. All 24 corals relocated to the DRTO sites survived and calcified ~85% faster than the fewer surviving corals transplanted to the 2 upper Keys sites. While coral survival across the entire experiment did not depend on genet, there was a weak but statistically significant genetic effect on calcification rate among the corals relocated to DRTO. The DRTO native genet was among the fastest growing genets, but it was not the fastest, suggesting a lack of local adaptation at this scale. Our results indicate that DRTO, a remote reef system inhabited by the species during the Holocene and located at the nexus of major ocean currents, may be a prime location for reestablishing A. palmata. Assisted migration of A. palmata to DRTO could restore a sexually reproducing population in <10 yr, thereby promoting the species’ regional recovery.

Valoración actual de las poblaciones de Acropora palmata y Acropora cervicornis en el Parque Nacional Natural Tayrona, Caribe colombiano

La última valoración sobre la extensión, estado y cobertura viva (%) de las formaciones de Acropora palmata (29) y A. cervicornis (12) en el Parque Nacional Natural Tayrona fue realizada en 2001 y publicada en 2004. Estas mismas formaciones, incluyendo una adicional en isla Aguja, fueron evaluadas de nuevo entre 2016 y 2018 teniendo en cuenta las mismas variables, y adicionalmente el registro de condición de las colonias. Para A. palmata se encontraron 24 formaciones con una reducción en área de 28,9 %. La cobertura promedio aumentó cerca de 2,0 %, y se observó una amplia distribución de frecuencia de tallas y una proporción importante de colonias con territorios de peces damisela (Stegastes). El área de las formaciones de A. cervicornis se redujo 99,3 % y solo se encontró una formación en Nenguange, aunque se registran dos nuevas y pequeñas en Cinto y otra en Chengue. La cobertura promedio fue de 8,0 %, en su mayoría constituida por colonias de talla pequeña y principalmente afectadas por blanqueamiento, macroalgas, enfermedades y depredadores. Claramente el estatus de las dos especies es diferente por lo que requieren esfuerzos diferentes para su manejo y conservación. Las formaciones de A. palmata han persistido, pero es necesario realizar estudios continuos que permitan detectar cambios temporales, con evaluaciones de aspectos ecológicos como las afectaciones por los peces damisela. El estado de A. cerviconis es crítico, por lo que demanda acciones urgentes de restauración y otras medidas de manejo para mitigar la tendencia a su desaparición en el área.

Juvenile corals inherit mutations acquired during the parent’s lifespan

Abstract128 years ago, August Weismann proposed that the only source of inherited genetic variation in animals is the germline1. Julian Huxley reasoned that if this were true, it would falsify Jean-Baptiste Lamarck’s theory that acquired characteristics are heritable2. Since then, scientists have discovered that not all animals segregate germline cells from somatic cells permanently and early in development3. In fact, throughout their lives, Cnidaria4–6 and Porifera7 maintain primordial stem cells that continuously give rise to both germline and somatic cells. The fate of mutations generated in this primordial stem cell line during adulthood remains an open question. It was unknown whether post-embryonic mutations could be heritable in animals8–10—until now. Here we use two independent genetic marker analyses to show that post-embryonic mutations are inherited in the coral Acropora palmata (Cnidaria, Anthozoa). This discovery upends the long-held supposition that post-embryonic genetic mutations acquired over an animal’s lifetime in non-germline tissues are not heritable2. Over the centuries-long lifespan of a coral, the inheritance of post-embryonic mutations may not only change allele frequencies in the local larval pool but may also spread novel alleles across great distances via larval dispersal. Thus, corals may have the potential to adapt to changing environments via heritable somatic mutations10. This mechanism challenges our understanding of animal adaptation and prompts a deeper examination of both the process of germline determination in Cnidaria and the role of post-embryonic genetic mutations in adaptation and epigenetics of modular animals. Understanding the role of post-embryonic mutations in animal adaptation will be crucial as ecological change accelerates in the Anthropocene.

Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

Mutualisms where hosts are coupled metabolically to their symbionts often exhibit high partner fidelity. Most reef-building corals form obligate symbioses with specific species of photosymbionts, dinoflagellates in the family Symbiodiniaceae, despite needing to acquire symbionts early in their development from environmental sources. Three Caribbean acroporids (Acropora palmata, A. cervicornis, and their hybrid A. prolifera) are geographically sympatric across much of their range in the greater Caribbean, but often occupy different depth and light habitats. Both species and their hybrid associate with Symbiodinium ‘fitti’, a genetically diverse species of symbiont that is specific to these hosts. Since the physiology of the dinoflagellate partner is strongly influenced by light (and therefore depth), we investigated whether S. ‘fitti’ populations from each host source were differentiated genetically. We generated shallow genome sequences of acroporid colonies sampled from across the Caribbean. Single Nucleotide Polymorphisms (SNPs) among S. ‘fitti’ strains were identified by aligning sequences to a ~600 Mb draft assembly of the S. ‘fitti’ genome, assembled from an A. cervicornis metagenome. Phylogenomic and multivariate analyses revealed that allelic variation among S. ‘fitti’ partitioned to each host species, as well as their hybrid, rather than by biogeographic origin. This is particularly noteworthy because the hybrid, A. prolifera, has a sparse fossil record and may be of relatively recent origin. Many of the SNPs putatively under selection were non-synonymous mutations predicted to alter protein efficiency. Differences in allele frequency among S. ‘fitti’ populations from each host taxon may correspond to distinct phenotypes that thrive in the different cellular environments found in each acroporid. The non-random sorting among genetically diverse strains, or genotypes, to different hosts could be the basis for lineage diversification via disruptive selection, leading to ecological specialization and ultimately speciation.