Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, August 13 until 12:00 AM ET on Friday, August 14 due to maintenance. We apologize for the inconvenience.


Title: Asynchronous effects of heat stress on growth rates of massive corals and damselfish in the Red Sea
Climate change is imposing multiple stressors on marine life, leading to a restructuring of ecological communities as species exhibit differential sensitivities to these stressors. With the ocean warming and wind patterns shifting, processes that drive thermal variations in coastal regions, such as marine heatwaves and upwelling events, can change in frequency, timing, duration, and severity. These changes in environmental parameters can physiologically impact organisms residing in these habitats. Here, we investigate the synchrony of coral and reef fish responses to environmental disturbance in the Red Sea, including an unprecedented combination of heat stress and upwelling that led to mass coral bleaching in 2015. We developed cross-dated growth chronologies from otoliths of 156 individuals of two planktivorous damselfish species,Pomacentrus sulfureusandAmblyglyphidodon flavilatus, and from skeletal cores of 48Poritesspp. coral colonies. During and immediately after the 2015 upwelling and bleaching event, damselfishes exhibited a positive growth anomaly but corals displayed reduced growth. Yet, after 2015–2016, these patterns were reversed with damselfishes showing a decline in growth and corals rebounding to pre-disturbance growth rates. Our results reveal an asynchronous response between corals and reef fish, with corals succumbing to the direct effects of heat stress, and then quickly recovering when the heat stress subsided—at least, for those corals that survived the bleaching event. Conversely, damselfish growth temporarily benefited from the events of 2015, potentially due to the increased metabolic demand from increased temperature and increased food supply from the upwelling event, before declining over four years, possibly related to indirect effects associated with habitat degradation following coral mortality. Overall, our study highlights the increasingly complex, often asynchronous, ecological ramifications of climate extremes on the diverse species assemblages of coral reefs.  more » « less
Award ID(s):
2444864
PAR ID:
10581072
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Mayfield, Anderson B
Publisher / Repository:
PLOS ONE
Date Published:
Journal Name:
PLOS ONE
Volume:
20
Issue:
1
ISSN:
1932-6203
Page Range / eLocation ID:
e0316247
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Marine heatwaves are starting to occur several times a decade, yet we do not understand the effect this has on corals across biological scales. This study combines tissue-, organism-, and community-level analyses to investigate the effects of a marine heatwave on reef-building corals. Adjacent conspecific pairs of coral colonies of Montipora capitata and Porites compressa that showed contrasting phenotypic responses (i.e., bleached vs. not bleached) were first identified during a marine heatwave that occurred in 2015 in Kāne’ohe Bay, Hawai‘ i. These conspecific pairs of bleaching-resistant and bleaching-susceptible colonies were sampled for histology and photographed before, during, and after a subsequent marine heatwave that occurred in 2019. Histology samples were quantified for: (i) abundance of mesenterial filaments, (ii) tissue structural integrity, (iii) clarity of epidermis, and (iv) cellular integrity (lack of necrosis/granulation) on a 1–5 scale and averaged for an overall tissue integrity score. Tissue integrity scores revealed a significant decline in overall tissue health during the 2019 heatwave relative to the months prior to the heatwave for individuals of both species, regardless of past bleaching history in 2015 or bleaching severity during the 2019 heatwave. Coral tissue integrity scores were then compared to concurrent colony bleaching severity, which revealed that tissue integrity was significantly correlated with colony bleaching severity and suggests that the stability of the symbiosis is related to host tissue health. Colony partial mortality was also quantified as the cumulative proportion of each colony that appeared dead 2.5 years following the 2019 bleaching event, and tissue integrity during the heatwave was found to be strongly predictive of the extent of partial mortality following the heatwave for M. capitata but not P. compressa, the latter of which suffered little to no mortality. Surprisingly, bleaching severity and partial mortality were not significantly correlated for either species, suggesting that tissue integrity was a better predictor of mortality than bleaching severity in M. capitata. Despite negative effects of heat stress at the tissue- and colony-level, no significant changes in coral cover were detected, indicating resilience at the community level. However, declines in tissue integrity in response to heat stress that are not accompanied by a visible bleaching response may still have long-term consequences for fitness, and this is an important area of future investigation as heat stress is commonly associated with long-term decreases in coral fecundity and growth. Our results suggest that histology is a valuable tool for revealing the harmful effects of marine heatwaves on corals before they are visually evident as bleaching, and may thus improve the predictability of ecosystem changes following climate change-driven heat stress by providing a more comprehensive assessment of coral health. 
    more » « less
  2. In 2023, a record-setting marine heat wave triggered the ninth mass coral bleaching event on Florida’s Coral Reef (FCR). We examined spatial patterns of heat exposure along the ~560-kilometer length of FCR and the mortality of two ecologically important, critically endangered reef-building corals. Sea surface temperatures were ≥31°C for an average of 40.7 days, leading to heat exposures 2.2- to fourfold higher than all prior years on record. In the Florida Keys and Dry Tortugas, 97.8 to 100% of theAcropora palmataandAcropora cervicorniscolonies died. Mortality was lower offshore southeast Florida (37.9%), reflecting cooler temperatures in this region. Since the late 1970s, multiple stressors had already reduced the ecological relevance ofAcroporain Florida, but the 2023 heat wave marks their functional extinction from FCR. 
    more » « less
  3. Ecosystem responses to disturbance depend on the nature of the perturbation and the ecological legacies left behind, making it critical to understand how climate‐driven changes in disturbance regimes modify resilience properties of ecosystems. For coral reefs, recent increases in severe marine heat waves now co‐occur with powerful storms, the historic agent of disturbance. While storms kill coral and remove their skeletons, heat waves bleach and kill corals but leave their skeletons intact. Here, we explored how the material legacy of dead coral skeletons modifies two key ecological processes that underpin coral reef resilience: the ability of herbivores to control macroalgae (spatial competitors of corals), and the replenishment of new coral colonies. Our findings, grounded by a major bleaching event at our long‐term study locale, revealed that the presence of structurally complex dead skeletons reduced grazing on turf algae by ~80%. For macroalgae, browsing was reduced by >40% on less preferred (unpalatable) taxa, but only by ~10% on more preferred taxa. This enabled unpalatable macroalgae to reach ~45% cover in 2 years. By contrast, herbivores prevented macroalgae from becoming established on adjacent reefs that lacked skeletons. Manipulation of unpalatable macroalgae revealed that the cover reached after 1 year (~20%) reduced recruitment of corals by 50%. The effect of skeletons on juvenile coral growth was contingent on the timing of settlement relative to the disturbance. If corals settled directly after bleaching (before macroalgae colonized), dead skeletons enhanced colony growth by 34%, but this benefit was lost if corals colonized dead skeletons a year after the disturbance once macroalgae had proliferated. These findings underscore how a material legacy from a changing disturbance regime can alter ecosystem resilience properties by disrupting key trophic and competitive interactions that shape post‐disturbance community dynamics. 
    more » « less
  4. The oceans are warming and coral reefs are bleaching with increased frequency and severity,fueling concerns for their survival through this century. Yet in the central equatorial Pacific,some of the world’s most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30%bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with ElNiño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015–16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world. 
    more » « less
  5. Abstract Cryptic species (evolutionarily distinct lineages that do not align with morphologically defined species) are being increasingly discovered but are poorly integrated into ecological theory. In particular, we still lack a useful understanding of if and how cryptic species differ in ways that affect community recovery from disturbances and responses to anthropogenic stressors, such as the removal of consumers and pollution from nutrients. On coral reefs, nutrient pollution increases the growth of macroalgae that displace corals. Reductions in herbivorous fishes reduce the suppression of macroalgae, while reductions in coralivorous fishes reduce predation on corals. An unresolved question is if and how cryptic coral species respond differently to these impacts, thereby differing in their ability to influence coral community dynamics and maintain coral dominance. Therefore, we assessed how the response of crypticPocilloporaspecies over a period of three years following a simulated disturbance from a cyclone depended on the experimental reduction of fish consumer pressure and nutrient addition. After three years, five morphologically cryptic, but genetically distinct,Pocilloporaspecies recruited to the reef. However, recruitment was dominated by two species:Pocillopora tuahiniensis(46%) andPocillopora meandrina(43%). Under ambient conditions, recruitment ofP. tuahiniensisandP. meandrinawas similar, but experimentally reducing consumer pressure increased recruitment ofP. tuahiniensisby up to 73% and reduced recruitment ofP. meandrinaby up to 49%. In both species, nutrient enrichment increased recruitment and colony growth rates equally, but colonies ofP. tuahiniensisgrew faster and were up to 25% larger after three years than those ofP. meandrina,and growth was unaffected by reduced consumer pressure. Predation by excavating corallivorous fish was higher forP. meandrinathan forP. tuahiniensis, especially under nutrient enrichment. In contrast, polyp extension (an indicator of elevated heterotrophic feeding as well as susceptibility and attractiveness to corallivores) was lower forP. meandrinathan forP. tuahiniensis, especially under low to medium consumer pressure. Overall, we uncovered ecological differences in the response of morphologically cryptic foundation species to two pervasive stressors on coral reefs. Our results demonstrate how cryptic species respond differently to key anthropogenic stressors, which may contribute to response diversity that can support ecological resilience or increase extinction risk. 
    more » « less