Crawford Drury

Growth dynamics of the threatened caribbean staghorn coral acropora cervicornis: Influence of host genotype, symbiont identity, colony size, and environmental setting

Background The drastic decline in the abundance of Caribbean acroporid corals (Acropora cervicornis, A. palmata) has prompted the listing of this genus as threatened as well as the development of a regional propagation and restoration program. Using in situ underwater nurseries, we documented the influence of coral genotype and symbiont identity, colony size, and propagation method on the growth and branching patterns of staghorn corals in Florida and the Dominican Republic. Methodology/Principal Findings Individual tracking of> 1700 nursery-grown staghorn fragments and colonies from 37 distinct genotypes (identified using microsatellites) in Florida and the Dominican Republic revealed a significant positive relationship between size and growth, but a decreasing rate of productivity with increasing size. Pruning vigor (enhanced growth after fragmentation) was documented even in colonies that lost 95% of their coral tissue/skeleton, indicating that high productivity can be maintained within nurseries by sequentially fragmenting corals. A significant effect of coral genotype was documented for corals grown in a common-garden setting, with fast-growing genotypes growing up to an order of magnitude faster than slow-growing genotypes. Algal-symbiont identity established using qPCR techniques showed that clade A (likely Symbiodinium A3) was the dominant symbiont type for all coral genotypes, except for one coral genotype in the DR and two in Florida that were dominated by clade C, with A- and C-dominated genotypes having similar growth rates. Conclusion/Significance The threatened Caribbean staghorn coral is capable of extremely fast growth, with annual productivity rates exceeding 5 cm of new coral produced for every cm of existing coral. This species benefits from high fragment survivorship coupled by the pruning vigor experienced by the parent colonies after fragmentation. These life-history characteristics make A. cervicornis a successful candidate nursery species and provide optimism for the potential role that active propagation can play in the recovery of this keystone species.

Genotype and local environment dynamically influence growth, disturbance response and survivorship in the threatened coral, Acropora cervicornis.

The relationship between the coral genotype and the environment is an important area of research in degraded coral reef ecosystems. We used a reciprocal outplanting experiment with 930 corals representing ten genotypes on each of eight reefs to investigate the influence of genotype and the environment on growth and survivorship in the threatened Caribbean staghorn coral, Acropora cervicornis. Coral genotype and site were strong drivers of coral growth and individual genotypes exhibited flexible, non-conserved reaction norms, complemented by ten-fold differences in growth between specific G-E combinations. Growth plasticity may diminish the influence of local adaptation, where foreign corals grew faster than native corals at their home sites. Novel combinations of environment and genotype also significantly affected disturbance response during and after the 2015 bleaching event, where these factors acted synergistically to drive variation in bleaching and recovery. Importantly, small differences in temperature stress elicit variable patterns of survivorship based on genotype and illustrate the importance of novel combinations of coral genetics and small differences between sites representing habitat refugia. In this context, acclimatization and flexibility is especially important given the long lifespan of corals coping with complex environmental change. The combined influence of site and genotype creates short-term differences in growth and survivorship, contributing to the standing genetic variation needed for adaptation to occur over longer timescales and the recovery of degraded reefs through natural mechanisms.

Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity

Abstract Threatened Caribbean coral communities can benefit from high‐resolution genetic data used to inform management and conservation action. We use Genotyping by Sequencing (GBS) to investigate genetic patterns in the threatened coral, Acropora cervicornis, across the Florida Reef Tract (FRT) and the western Caribbean. Results show extensive population structure at regional scales and resolve previously unknown structure within the FRT. Different regions also exhibit up to threefold differences in genetic diversity (He), suggesting targeted management based on the goals and resources of each population is needed. Patterns of genetic diversity have a strong spatial component, and our results show Broward and the Lower Keys are among the most diverse populations in Florida. The genetic diversity of Caribbean staghorn coral is concentrated within populations and within individual reefs (AMOVA), highlighting the complex mosaic of population structure. This variance structure is similar over regional and local scales, which suggests that in situ nurseries are adequately capturing natural patterns of diversity, representing a resource that can replicate the average diversity of wild assemblages, serving to increase intraspecific diversity and potentially leading to improved biodiversity and ecosystem function. Results presented here can be translated into specific goals for the recovery of A. cervicornis, including active focus on low diversity areas, protection of high diversity and connectivity, and practical thresholds for responsible restoration.

Making biodiversity work for coral reef restoration

Coral reefs, and the important ecosystem services they provide, are uniquely threatened by global climate change factors that include a combination of sea level rise, temperature extremes and ocean acidification (Hoegh-Guldberg et al. 2007). Reefs also face pressure from multiple local sources of disturbance such as overfishing, eutrophication and habitat degradation due to their proximity to, and importance for, growing human populations (Pandolfi et al. 2003). In coastal areas, biodiversity is a valuable resource that may facilitate resistance and resilience, but could also be a key for improving the effectiveness of protection and restoration of corals and coral reef ecosystems. Biodiversity exists on several scales, from species diversity to the genomes of individual organisms within a species (Hughes et al. 2008), with important functional roles at varying levels of this hierarchy. Communities with more diverse assemblages have functional redundancy, which is uniquely important during and after stress and may produce widely different resistant and resilience outcomes. Within stressed communities, the genetic diversity of keystone or foundation taxa like stony corals or seagrasses can be especially important, influencing stress responses at both the species and community levels (Barbour et al. 2009; Jahnke, Olsen, and Procaccini 2015). Moreover, increased disease resistance (Zhu et al. 2000), structuring of associated biota (Booth and Grime 2003; Crutsinger et al. 2006) and increased resistance and resilience to thermal stress (Hughes and Stachowicz 2004; Reusch et al. 2005) attributed to higher genetic diversity can have cascading impacts on ecosystem services (Forsman and Wennersten 2015). Thus, biodiversity can and should be a focal point for targeted management, conservation and active restoration because more diverse systems are more likely to survive, prosper and provide the adaptive capacity needed to persist under future disturbance scenarios like those facing coral reefs (Jump, Marchant, and Peñuelas 2009). Approaching biodiversity as a functional tool is relevant for coral and coral reef restoration, especially in the context of intraspecific diversity. Recent coral restoration focuses primarily on branching corals, which grow quickly and reproduce asexually effectively through fragmentation (Young, Schopmeyer, and Lirman 2012). Corals are now propagated worldwide within in situ and ex situ nurseries as steps in the coral gardening method that produces a sustainable source of corals for restoration and minimises impacts on wild ‘donor’ colonies (Lirman and Schopmeyer 2016; Rinkevich 2005). As restoration technology and efforts have matured, work with massive coral species has also increased (Forsman et al. 2015), now providing the opportunity to conduct restoration projects with a wide range of taxa. Under this framework, creating or supplementing communities with the highest interspecific and intraspecific diversity is compulsory. Conducting coral reef restoration activities considering both species and genetic diversity provides several major benefits: taking advantage of environmental differences that may promote various physiological disturbance responses (Drury, Manzello, and Lirman 2017), fostering successful sexual reproduction and preventing ‘selfing’ and inbreeding of closely related individuals (Baums 2008) and maintaining genetic diversity, the raw material for adaptation (Oliver et al. 2015; Sgrò, Lowe, and Hoffmann 2011). Recent work with the staghorn coral Acropora cervicornis in Florida illustrates the importance of intraspecific genetic diversity of a foundation coral species during and after disturbance (Drury, Manzello, and Lirman 2017). In this study, reciprocal transplanting of corals originally propagated in nurseries was used to create genotype × environment (G × E) combinations that yielded a wide range of differences in bleaching susceptibility and survivorship despite similar symbiont communities in all coral genotypes (Figure 1). This work, which occurred during the high-temperature anomaly of 2015, showed

Dispersal capacity and genetic relatedness in Acropora cervicornis on the Florida Reef Tract

Sexual reproduction in scleractinian corals is a critical component of species recovery, fostering population connectivity and enhancing genetic diveristy. The relative contribution of sexual reproduction to both connectivity and diversity in Acropora cervicornis may be variable due to this species’ capacity to reproduce effectively by fragmentation. Using a biophysical model and genomic data in this threatened species, we construct potential connectivity pathways on the Florida Reef Tract (FRT) and compare them to inferred migration rates derived from next-generation sequencing, using a link and node-based approach. Larval connectivity on the FRT can be divided into two zones: the northern region, where most transport is unidirectional to the north with the Florida Current, and the southern region that is more dynamic and exhibits complex spatial patterns. These biophysical linkages are poorly correlated with genetic connectivity patterns, which resolve many reciprocal connections and suggest a less sparse network. These results are difficult to reconcile with genetic data which indicate that individual reefs are diverse, suggesting important contributions of sexual reproduction and recruitment. Larval connectivity models highlight potential resources for recovery, such as areas with high larval export like the Lower Keys, or areas that are well connected to most other regions on the FRT, such as the Dry Tortugas.