Damselfishes alleviate the impacts of sediments on host corals

Mutualisms play a critical role in ecological communities; however, the importance and prevalence of mutualistic associations can be modified by external stressors. On coral reefs, elevated sediment deposition can be a major stressor reducing the health of corals and reef resilience. Here, we investigated the influence of severe sedimentation on the mutualistic relationship between small damselfishes (Pomacentrus moluccensis and Dascyllus aruanus) and their coral host (Pocillopora damicornis). In an aquarium experiment, corals were exposed to sedimentation rates of approximately 100 mg cm−2 d−1, with and without fishes present, to test whether: (i) fishes influence the accumulation of sediments on coral hosts, and (ii) fishes moderate partial colony mortality and/or coral tissue condition. Colonies with fishes accumulated much less sediment compared with colonies without fishes, and this effect was strongest for colonies with D. aruanus (fivefold less sediment than controls) as opposed to P. moluccensis (twofold less sediment than controls). Colonies with symbiont fishes also had up to 10-fold less sediment-induced partial mortality, as well as higher chlorophyll and protein concentrations. These results demonstrate that fish mutualisms vary in the strength of their benefits, and indicate that some mutualistic or facilitative interactions might become more important for species health and resilience at high-stress levels.

[1]  M. Hoogenboom,et al.  Supplementary material from "Damselfishes alleviate the impacts of sediments on host corals" , 2020 .

[2]  M. Hoogenboom,et al.  Behavioral trade-offs and habitat associations of coraldwelling damselfishes (family Pomacentridae) , 2020 .

[3]  D. Bellwood,et al.  Algal turf sediments on coral reefs: what's known and what's next. , 2019, Marine pollution bulletin.

[4]  Ross Jones,et al.  Sediment deposition and coral smothering , 2019, PloS one.

[5]  D. Bellwood,et al.  Quantifying sediment dynamics on an inshore coral reef: Putting algal turfs in perspective. , 2019, Marine pollution bulletin.

[6]  P. Buston,et al.  Comparison of efficiency of direct observations by scuba diver and indirect observations via video camera for measuring reef-fish behaviour. , 2019, Journal of fish biology.

[7]  M. Emslie,et al.  The Distribution of Planktivorous Damselfishes (Pomacentridae) on the Great Barrier Reef and the Relative Influences of Habitat and Predation , 2019, Diversity.

[8]  G. Russ,et al.  Cross-Shelf Differences in the Response of Herbivorous Fish Assemblages to Severe Environmental Disturbances , 2019, Diversity.

[9]  R. Evans,et al.  Cross-shelf Heterogeneity of Coral Assemblages in Northwest Australia , 2019, Diversity.

[10]  M. Hoogenboom,et al.  Coral-dwelling fish moderate bleaching susceptibility of coral hosts , 2018, PloS one.

[11]  D. Bellwood,et al.  Algal turf sediments across the Great Barrier Reef: Putting coastal reefs in perspective. , 2018, Marine pollution bulletin.

[12]  Passang Dorji,et al.  The effects of suspended sediment on coral reef fish assemblages and feeding guilds of north-west Australia , 2018 .

[13]  J. Reimer,et al.  Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts , 2018, Current Biology.

[14]  Christina C. Hicks,et al.  The future of hyperdiverse tropical ecosystems , 2018, Nature.

[15]  Ross Jones,et al.  Coral morphology and sedimentation. , 2017, Marine pollution bulletin.

[16]  M. Hoogenboom,et al.  Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme Thermal Anomaly , 2017, Front. Mar. Sci..

[17]  Benjamin J. Saunders,et al.  A critical analysis of the direct effects of dredging on fish , 2017 .

[18]  P. Ridd,et al.  Continuous in situ monitoring of sediment deposition in shallow benthic environments , 2017, Coral Reefs.

[19]  A. Kunzmann,et al.  Mutualistic damselfish induce higher photosynthetic rates in their host coral , 2017, Journal of Experimental Biology.

[20]  D. Wardle,et al.  The Overlooked Role of Facilitation in Biodiversity Experiments. , 2017, Trends in ecology & evolution.

[21]  Will F. Figueira,et al.  Global warming and recurrent mass bleaching of corals , 2017, Nature.

[22]  D. Bellwood,et al.  Algal Turf Sediments and Sediment Production by Parrotfishes across the Continental Shelf of the Northern Great Barrier Reef , 2017, PloS one.

[23]  D. Bellwood,et al.  The Effects of Algal Turf Sediments and Organic Loads on Feeding by Coral Reef Surgeonfishes , 2017, PloS one.

[24]  G. Jones,et al.  Life on the edge: Coral reef fishes exhibit strong responses to a habitat boundary , 2016 .

[25]  M. Brown,et al.  Coral Responses to Anthropogenic Stress in the Twenty- First Century: An Ecophysiological Perspective , 2016 .

[26]  D. Bellwood,et al.  Composition and temporal stability of turf sediments on inner-shelf coral reefs. , 2016, Marine pollution bulletin.

[27]  P. Clode,et al.  Mucous Secretion and Cilia Beating Defend Developing Coral Larvae from Suspended Sediments , 2016, PloS one.

[28]  D. Bellwood,et al.  Sediments and herbivory as sensitive indicators of coral reef degradation , 2016 .

[29]  Russell V. Lenth,et al.  Least-Squares Means: The R Package lsmeans , 2016 .

[30]  Wojciech M. Klonowski,et al.  Assessing the impacts of sediments from dredging on corals. , 2016, Marine pollution bulletin.

[31]  P. Clode,et al.  Suspended sediments limit coral sperm availability , 2015, Scientific Reports.

[32]  Mark C Ladd,et al.  Fish-derived nutrient hotspots shape coral reef benthic communities. , 2015, Ecological applications : a publication of the Ecological Society of America.

[33]  G. Ricardo,et al.  Effects of sediments on the reproductive cycle of corals. , 2015, Marine pollution bulletin.

[34]  J. Steffensen,et al.  Winter temperatures decrease swimming performance and limit distributions of tropical damselfishes , 2015, Conservation physiology.

[35]  A. Wenger,et al.  Exposure of clownfish larvae to suspended sediment levels found on the Great Barrier Reef: Impacts on gill structure and microbiome , 2015, Scientific Reports.

[36]  B. B. M. Wong,et al.  Behavioral responses to changing environments , 2015 .

[37]  M. Medina,et al.  Microbes in the coral holobiont: partners through evolution, development, and ecological interactions , 2015, Front. Cell. Infect. Microbiol..

[38]  M. Hoogenboom,et al.  Small-scale environmental variation influences whether coral-dwelling fish promote or impede coral growth , 2014, Oecologia.

[39]  S. Field,et al.  Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs , 2014, PloS one.

[40]  Scarla J. Weeks,et al.  The effects of river run-off on water clarity across the central Great Barrier Reef. , 2014, Marine pollution bulletin.

[41]  S. Wilson,et al.  Importance of live coral habitat for reef fishes , 2014, Reviews in Fish Biology and Fisheries.

[42]  A. Stier,et al.  Predators alter community organization of coral reef cryptofauna and reduce abundance of coral mutualists , 2014, Coral Reefs.

[43]  S. Holbrook,et al.  Determinants of the onset and strength of mutualistic interactions between branching corals and associate crabs , 2013 .

[44]  A. Wenger,et al.  Determining trigger values of suspended sediment for behavioral changes in a coral reef fish. , 2013, Marine pollution bulletin.

[45]  Qiang He,et al.  Global shifts towards positive species interactions with increasing environmental stress. , 2013, Ecology letters.

[46]  B. Willis,et al.  Cymo melanodactylus crabs slow progression of white syndrome lesions on corals , 2013, Coral Reefs.

[47]  C. Storlazzi,et al.  SedPods: a low-cost coral proxy for measuring net sedimentation , 2013, Coral Reefs.

[48]  M. Hay,et al.  Corals Chemically Cue Mutualistic Fishes to Remove Competing Seaweeds , 2012, Science.

[49]  A. Wenger,et al.  Increasing suspended sediment reduces foraging, growth and condition of a planktivorous damselfish , 2012 .

[50]  Peter A Todd,et al.  Environmental impacts of dredging and other sediment disturbances on corals: a review. , 2012, Marine pollution bulletin.

[51]  P. Munday,et al.  Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss , 2012, Ecology and evolution.

[52]  Hamed Nekoubin,et al.  Effect of anaesthesia with clove oil in fish (review) , 2012, Fish Physiology and Biochemistry.

[53]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[54]  D. Bellwood,et al.  The effect of coral morphology on shelter selection by coral reef fishes , 2012, Coral Reefs.

[55]  T. Cooper,et al.  Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts , 2012, PloS one.

[56]  T. Ferdelman,et al.  Mechanisms of damage to corals exposed to sedimentation , 2012, Proceedings of the National Academy of Sciences.

[57]  S. Mills,et al.  Housekeeping Mutualisms: Do More Symbionts Facilitate Host Performance? , 2012, PloS one.

[58]  I. Miller,et al.  The distribution of herbivorous fishes on the Great Barrier Reef , 2012 .

[59]  M. McFall-Ngai,et al.  Metaorganisms as the new frontier. , 2011, Zoology.

[60]  B. Willis,et al.  Selective feeding by coral reef fishes on coral lesions associated with brown band and black band disease , 2011, Coral Reefs.

[61]  C. Storlazzi,et al.  The use (and misuse) of sediment traps in coral reef environments: theory, observations, and suggested protocols , 2011, Coral Reefs.

[62]  S. Holbrook,et al.  Indirect effects of species interactions on habitat provisioning , 2011, Oecologia.

[63]  Judith L Bronstein,et al.  Mutualisms in a changing world: an evolutionary perspective. , 2010, Ecology letters.

[64]  M. Pratchett,et al.  Variation in the structure of epifaunal invertebrate assemblages among coral hosts , 2010, Coral Reefs.

[65]  A. Zeileis,et al.  Beta Regression in R , 2010 .

[66]  D. Gilliam,et al.  Elevated sedimentation on coral reefs adjacent to a beach nourishment project. , 2010, Marine pollution bulletin.

[67]  E. Wolanski,et al.  Quantifying the impact of watershed urbanization on a coral reef: Maunalua Bay, Hawaii , 2009 .

[68]  C. Osenberg,et al.  Effects of the fish anesthetic, clove oil (eugenol), on coral health and growth. , 2009 .

[69]  S. Holbrook,et al.  Effects of sheltering fish on growth of their host corals , 2008 .

[70]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[71]  D. Bellwood,et al.  Coral reef fishes exploit flow refuges in high-flow habitats , 2008 .

[72]  D. Bellwood,et al.  Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef , 2008, Coral Reefs.

[73]  C. Storlazzi,et al.  Quantity, composition, and source of sediment collected in sediment traps along the fringing coral reef off Molokai, Hawaii. , 2006, Marine pollution bulletin.

[74]  S. Holbrook,et al.  Symbiotic crabs maintain coral health by clearing sediments , 2006, Coral Reefs.

[75]  K. Fabricius Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. , 2005, Marine pollution bulletin.

[76]  R. Holzman,et al.  Aeration of corals by sleep‐swimming fish , 2004 .

[77]  A. Ogston,et al.  Wave- and tidally-driven flow and sediment flux across a fringing coral reef: Southern Molokai, Hawaii , 2004 .

[78]  A. Ogston,et al.  Sediment resuspension and transport patterns on a fringing reef flat, Molokai, Hawaii , 2004, Coral Reefs.

[79]  S. Holbrook,et al.  Mutualism can mediate competition and promote coexistence , 2003 .

[80]  Miles Furnas,et al.  Catchments and Corals: Terrestrial Runoff to the Great Barrier Reef , 2003 .

[81]  J. Bruno,et al.  Inclusion of facilitation into ecological theory , 2003 .

[82]  K. Fabricius,et al.  Photophysiological stress in scleractinian corals in response to short-term sedimentation , 2003 .

[83]  Malcolm McCulloch,et al.  Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement , 2003, Nature.

[84]  C. Lortie,et al.  Positive interactions among alpine plants increase with stress , 2002, Nature.

[85]  D. Doak,et al.  Physical stress and diversity-productivity relationships: The role of positive interactions , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[86]  J. Stachowicz Mutualism, Facilitation, and the Structure of Ecological Communities , 2001 .

[87]  G. Esslemont Heavy metals in seawater, marine sediments and corals from the Townsville section, Great Barrier Reef Marine Park, Queensland , 2000 .

[88]  M. Pratchett,et al.  Coral crbas influence the feeding patterns of crown-of-thorns starfish , 2000, Coral Reefs.

[89]  O. Hoegh‐Guldberg,et al.  Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event , 2000 .

[90]  J. B. Jones,et al.  Treatments for ectoparasites and diseases in captive Western Australian dhufish , 2000, Aquaculture International.

[91]  Graham E. Forrester,et al.  Spatial patterns in abundance of a damselfish reflect availability of suitable habitat , 2000, Oecologia.

[92]  Y. Achituv,et al.  Relationship between the coral pit crab Cryptochirus coralliodytes Heller and its host coral , 1997 .

[93]  Y. Loya,et al.  Effects on growth and reproduction of the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus , 1995 .

[94]  N. Shashar,et al.  Extreme Diel Fluctuations of Oxygen in Diffusive Boundary Layers Surrounding Stony Corals. , 1993, The Biological bulletin.

[95]  R. Richmond Coral Reefs: Present Problems and Future Concerns Resulting from Anthropogenic Disturbance , 1993 .

[96]  D. Bellwood,et al.  A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications , 1990, Environmental Biology of Fishes.

[97]  C. Rogers,et al.  Sublethal and lethal effects of sediments applied to common Caribbean Reef corals in the field , 1983 .

[98]  J. Meyer,et al.  Fish Schools: An Asset to Corals , 1983, Science.

[99]  R. Dodge,et al.  Coral Growth Related to Resuspension of Bottom Sediments , 1974, Nature.

[100]  C. Wentworth A Scale of Grade and Class Terms for Clastic Sediments , 1922, The Journal of Geology.

[101]  T. Walshe,et al.  Accounting for environmental uncertainty in the management of dredging impacts using probabilistic dose-response relationships and thresholds , 2018 .

[102]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[103]  S. Pelini,et al.  Insect mutualisms buffer warming effects on multiple trophic levels. , 2014, Ecology.

[104]  Eric Wolanski,et al.  Fine sediment and nutrient dynamics related to particle size and floc formation in a Burdekin River flood plume, Australia. , 2012, Marine pollution bulletin.

[105]  I. Bohnet,et al.  Terrestrial pollutant runoff to the Great Barrier Reef: An update of issues, priorities and management responses. , 2012, Marine pollution bulletin.

[106]  T. Done,et al.  Patterns in the distribution of coral communities across the central Great Barrier Reef , 2004, Coral Reefs.

[107]  Bellwood Carbonate transport and within-reef patterns of bioerosion and sediment release by parrotfishes (family Scaridae) on the Great Barrier Reef , 1995 .

[108]  R. Ormond,et al.  Sediment-rejection mechanisms of 42 species of Australian Scleractinian corals , 1992 .

[109]  C. Rogers Responses of coral reefs and reef organisms to sedimentation , 1990 .

[110]  Michael A. Borowitzka,et al.  Diurnal lipid and mucus production in the staghorn coral Acropora acuminata , 1980 .

[111]  B. Lassig Communication and coexistence in a coral community , 1977 .

[112]  R. Dodge,et al.  Coral Populations and Growth Patterns: Responses to Sedimentation and Turbidity Associated with Dredging , 1977 .