Gene expression profiles during short‐term heat stress in the red sea coral Stylophora pistillata

During the past several decades, corals worldwide have been affected by severe bleaching events leading to wide‐spread coral mortality triggered by global warming. The symbiotic Red Sea coral Stylophora pistillata from the Gulf of Eilat is considered an opportunistic ‘r’ strategist. It can thrive in relatively unstable environments and is considered a stress‐tolerant species. Here, we used a S. pistillata custom microarray to examine gene expression patterns and cellular pathways during short‐term (13‐day) heat stress. The results allowed us to identify a two‐step reaction to heat stress, which intensified significantly as the temperature was raised to a 32 °C threshold, beyond which, coping strategies failed at 34 °C. We identified potential ‘early warning genes’ and ‘severe heat‐related genes’. Our findings suggest that during short‐term heat stress, S. pistillata may divert cellular energy into mechanisms such as the ER‐unfolded protein response (UPR) and ER‐associated degradation (ERAD) at the expense of growth and biomineralization processes in an effort to survive and subsequently recover from the stress. We suggest a mechanistic theory for the heat stress responses that may explain the success of some species which can thrive under a wider range of temperatures relative to others.     

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Ocean acidification is the increase in seawater pCO₂ due to the uptake of atmospheric anthropogenic CO₂, with the largest changes predicted to occur in the Arctic seas. For some marine organisms, this change in pCO₂, and associated decrease in pH, represents a climate change‐related stressor. In this study, we investigated the gene expression patterns of nauplii of the Arctic copepod Calanus glacialis cultured at low pH levels. We have previously shown that organismal‐level performance (development, growth, respiration) of C. glacialis nauplii is unaffected by low pH. Here, we investigated the molecular‐level response to lowered pH in order to elucidate the physiological processes involved in this tolerance. Nauplii from wild‐caught C. glacialis were cultured at four pH levels (8.05, 7.9, 7.7, 7.5). At stage N6, mRNA was extracted and sequenced using RNA‐seq. The physiological functionality of the proteins identified was categorized using Gene Ontology and KEGG pathways. We found that the expression of 151 contigs varied significantly with pH on a continuous scale (93% downregulated with decreasing pH). Gene set enrichment analysis revealed that, of the processes downregulated, many were components of the universal cellular stress response, including DNA repair, redox regulation, protein folding, and proteolysis. Sodium:proton antiporters were among the processes significantly upregulated, indicating that these ion pumps were involved in maintaining cellular pH homeostasis. C. glacialis significantly alters its gene expression at low pH, although they maintain normal larval development. Understanding what confers tolerance to some species will support our ability to predict the effects of future ocean acidification on marine organisms.     

Macroalgae reduces survival of nursery‐reared Acropora corals in the Florida reef tract

Recent declines in coral populations along the Florida reef tract have prompted the establishment of coral restoration programs which raise coral species, such as the threatened Acropora cervicornis, in nurseries ready for outplanting. Large numbers of nursery‐reared coral colonies have been outplanted along the Florida reef tract in recent years, yet few studies have characterized benthic habitats that are considered optimal for colony survival. In 2016, we surveyed 23 A. cervicornis restoration sites, located at six different reefs in the upper Florida Keys. We examined the condition of the outplanted corals and quantified the benthic assemblages adjacent to the outplanted coral colonies. We found that where A. cervicornis survived for more than 1 year, the substrate significantly supported less brown macroalgae of the genus Dictyota than at sites where A. cervicornis had died. Coral survival was highest at sites with less than 15% Dictyota cover. These results suggest that the habitat conditions that supported Dictyota spp. were not conducive to A. cervicornis growth and survival. Restoration practitioners should avoid attaching nursery‐raised corals to substrate with Dictyota spp. cover greater than 15%.     

Differential survival of nursery‐reared Acropora cervicornis outplants along the Florida reef tract

In recent decades, the Florida reef tract has lost over 95% of its coral cover. Although isolated coral assemblages persist, coral restoration programs are attempting to recover local coral populations. Listed as threatened under the Endangered Species Act, Acropora cervicornis is the most widely targeted coral species for restoration in Florida. Yet strategies are still maturing to enhance the survival of nursery‐reared outplants of A. cervicornis colonies on natural reefs. This study examined the survival of 22,634 A. cervicornis colonies raised in nurseries along the Florida reef tract and outplanted to six reef habitats in seven geographical subregions between 2012 and 2018. A Cox proportional hazards regression was used within a Bayesian framework to examine the effects of seven variables: (1) coral‐colony size at outplanting, (2) coral‐colony attachment method, (3) genotypic diversity of outplanted A. cervicornis clusters, (4) reef habitat, (5) geographical subregion, (6) latitude, and (7) the year of monitoring. The best models included coral‐colony size at outplanting, reef habitat, geographical subregion, and the year of monitoring. Survival was highest when colonies were larger than 15 cm (total linear extension), when outplanted to back‐reef and fore‐reef habitats, and when outplanted in Biscayne Bay and Broward–Miami subregions, in the higher latitudes of the Florida reef tract. This study points to several variables that influence the survival of outplanted A. cervicornis colonies and highlights a need to refine restoration strategies to help restore their population along the Florida reef tract.     

Coralclip®: a low‐cost solution for rapid and targeted out‐planting of coral at scale

Re‐attaching or out‐planting coral as fragments, colonies, and on larval settlement devices to substrates is a major bottleneck limiting scalabilty and viability of reef restoration practices. Many attachment approaches are in use, but none that are low‐cost, opportunistic, rapid but effective, for integration into existing tour operations on the Great Barrier Reef (GBR) where staff and boat time is a major cost and chemical fixatives cannot be easily used. We describe a novel attachment device—Coralclip®—developed to meet this need and so aid maintenance and restoration of GBR tourism sites. Coralclip® is a stainless steel springclip attached by a nail integrated through the spring coil, and can be deployed with a coral fragment in as fast as 15 seconds. Initial laboratory tests demonstrated that Coralclip® secured coral fragments or larval settlement tiles under dynamic flow regimes characteristic of exposed reefs. Coral out‐planting from fragments of opportunity and from nurseries (n = 4,580; 0.3–1.9 coral/minute; US$0.6–3.0/coral deployed) or larval settlement tiles (n = 400; 2.5 tiles/minute; US$0.5 tile deployed^?1) when deployed by divers from routine boat operations at Opal Reef confirmed highly effective attachment, with ≤15% failure of clips found after 3–7 months. We discuss how Coralclip® is a cost‐effective means to support reef maintenance and restoration practices.     

Genome‐wide regulatory deterioration impedes adaptive responses to stress in inbred populations of Drosophila melanogaster*

Inbreeding depression is often intensified under environmental stress (i.e., inbreeding–stress interaction). Although the fitness consequences of this phenomenon are well‐described, underlying mechanisms such as an increased expression of deleterious alleles under stress, or a lower capacity for adaptive responses to stress with inbreeding, have rarely been investigated. We investigated a fitness component (egg‐to‐adult viability) and gene‐expression patterns using RNA‐seq analyses in noninbred control lines and in inbred lines of Drosophila melanogaster exposed to benign temperature or heat stress. We find little support for an increase in the cumulative expression of deleterious alleles under stress. Instead, inbred individuals had a reduced ability to induce an adaptive gene regulatory stress response compared to controls. The decrease in egg‐to‐adult viability due to stress was most pronounced in the lines with the largest deviation in the adaptive stress response (R² = 0.48). Thus, we find strong evidence for a lower capacity of inbred individuals to respond by gene regulation to stress and that this is the main driver of inbreeding‐stress interactions. In comparison, the altered gene expression due to inbreeding at benign temperature showed no correlation with fitness and was pronounced in genomic regions experiencing the highest increase in homozygosity.     

Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe low‐temperature stress

Coral reefs of the Florida Keys typically experience seasonal temperatures of 20–31 °C. Deviation outside this range causes physiological impairment of reef‐building corals, potentially leading to coral colony death. In January and February 2010, two closely spaced cold fronts, possibly driven by an unusually extreme Arctic Oscillation, caused sudden and severe seawater temperature declines in the Florida Keys. Inshore coral reefs [e.g., Admiral Reef (ADM)] experienced lower sustained temperatures (i.e., < 12 °C) than those further offshore [e.g., Little Grecian Reef (LG), minimum temperature = 17.2 °C]. During February and March 2010, we surveyed ADM and observed a mass die‐off of reef‐building corals, whereas 12 km away LG did not exhibit coral mortality. We subsequently measured the physiological effects of low‐temperature stress on three common reef‐building corals (i.e., Montastraea faveolata, Porites astreoides, and Siderastrea siderea) over a range of temperatures that replicated the inshore cold‐water anomaly (i.e., from 20 to 16 to 12 °C and back to 20 °C). Throughout the temperature modulations, coral respiration as well as endosymbiont gross photosynthesis and maximum quantum efficiency of photosystem II were measured. In addition, Symbiodinium genotypic identity, cell densities, and chlorophyll a content were determined at the beginning and conclusion of the experiment. All corals were significantly affected at 12 °C, but species‐specific physiological responses were found indicating different coral and/or Symbiodinium cold tolerances. Montastraea faveolata and P. astreoides appeared to be most negatively impacted because, upon return to 20 °C, significant reductions in gross photosynthesis and dark respiration persisted. Siderastrea siderea, however, readily recovered to pre‐treatment rates of dark respiration and gross photosynthesis. Visual surveys of inshore reefs corroborated these results, with S. siderea being minimally affected by the cold‐water anomaly, whereas M. faveolata and P. astreoides exhibited nearly 100% mortality. This study highlights the importance of understanding the physiological attributes of genotypically distinct coral‐Symbiodinium symbioses that contribute to tolerance, recovery, and consequences to an environmental perturbation. These data also document effects of a rarely studied environmental stressor, possibly initiated by remote global climate events, on coral‐Symbiodinium symbioses and coral reef communities.     

Evolution of heat‐shock protein expression underlying adaptive responses to environmental stress

Heat‐shock proteins (Hsps) and their cognates are primary mitigators of cell stress. With increasingly severe impacts of climate change and other human modifications of the biosphere, the ability of the heat‐shock system to affect evolutionary fitness in environments outside the laboratory and to evolve in response is topic of growing importance. Since the last major reviews, several advances have occurred. First, demonstrations of the heat‐shock response outside the laboratory now include many additional taxa and environments. Many of these demonstrations are only correlative, however. More importantly, technical advances in “omic” quantification of nucleic acids and proteins, genomewide association analysis, and manipulation of genes and their expression have enabled the field to move beyond correlation. Several consequent advances are already evident: The pathway from heat‐shock gene expression to stress tolerance in nature can be extremely complex, mediated through multiple biological processes and systems, and even multiple species. The underlying genes are more numerous, diverse and variable than previously appreciated, especially with respect to their regulatory variation and epigenetic changes. The impacts and limitations (e.g., due to trade‐offs) of natural selection on these genes have become more obvious and better established. At last, as evolutionary capacitors, Hsps may have distinctive impacts on the evolution of other genes and ecological consequences.     

Effects of coral restoration on fish communities: snapshots of long‐term,multiregional responses and implications for practice

Coral restoration is widely used around the world to address dramatic declines in coral cover; however, very few studies have looked specifically at the temporal response of fish assemblages (i.e. abundance and diversity) to coral restoration. Several critical reef functions and processes are driven by fishes, thereby making their recovery and responses around restoration structures key indicators of success. This study evaluates fish abundance and community composition on restoration plots following 8–12 years of restoration activity, in four locations (two Caribbean and two Indo‐Pacific). Responses were very complex with region‐, site‐, and body size‐specific patterns. Overall, fish abundance only increased in Indo‐Pacific sites where damselfish responded positively to increased coral cover and topographic complexity. Restoration effects on other fish families and particularly on larger bodied reef fish were negative or neutral at all locations. If restoration initiatives are going to substantively improve the condition and recovery of degraded reef fish communities, restoration efforts need to be planned, designed, and monitored based on fish‐specific habitat requirements and locally specific community dynamics.