Abstract
Hypoxia is a widespread and increasing phenomenon in marine environments, including coral reefs. The bearded fireworm (Hermodice carunculata) is a large corallivorous amphinomid polychaete, with a high tolerance of environmental stress, including temperature, salinity, and dissolved oxygen (DO). Currently, little is known about the response of H. carunculata to chronic (≥ 18 h) hypoxia, although this knowledge is crucial to understand its impact on coral reef health under hypoxia scenarios. We tested the hypothesis that the number of branchial filaments (previously used as a diagnostic character for species identification) increases in response to chronic hypoxia. We subjected wild-caught fireworms to two levels of reduced DO (Mid: 4.5 ± 0.25 mg O2 L−1 and Low: 2.5 ± 0.25 mg O2 L−1) to explore their morphological and physiological responses to seven days of chronic hypoxia. Hypoxia exposure resulted in a higher number of branchial filaments (low = 57.2 ± 5.3, mid = 57.4 ± 6.1, and normal = 47.4 ± 11.2) after seven days. Fireworms exposed to hypoxia further reduced their rate of regeneration, but returned to normal regenerative rates after fifteen weeks under normoxic conditions. There was no difference in regeneration rates between low and mid DO groups. Our results demonstrate the importance of considering multiple physiological and morphological endpoints as well as phenotypic plasticity in species delimitations. Indeed, the results suggest that morphological variation can be indicative of environmental conditions.
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References
Ahrens JB, Borda E, Barroso R, Paiva PC, Campbell AM, Wolf A, Nugues MM, Rouse GW, Schulze A (2013) The curious case of Hermodice carunculata (Annelida: Amphinomidae): evidence for genetic homogeneity throughout the Atlantic Ocean and adjacent basins. Mol Ecol 22:2280–2291
Ahrens JB, Kudenov JD, Marshall CD, Schulze A (2014) Regeneration of Posterior Segments and Terminal Structures in the Bearded Fireworm, Hermodice carunculata (Annelida: Amphinomidae). J Morphol 275:1103–1112. https://doi.org/10.1002/jmor.20287
Altieri AH, Gedan KB (2015) Climate change and dead zones. Global Change Biology 21(4):1395–1406
Altieri AH, Diaz RJ (2019) Dead zones: oxygen depletion in coastal ecosystems world seas: an environmental evaluation. Elsevier, Amsterdam, pp 453–473
Altieri AH, Harrison SB, Seemann J, Collin R, Diaz RJ, Knowlton N (2017) Tropical dead zones and mass mortalities on coral reefs. Proc Natl Acad Sci 114:3660–3665
Andersen AC, Hamraoui L, Zaoui D (2001) The obturaculum of Riftia pachyptila (Annelida, Vestimentifera): ultrastructure and function of the obturacular muscles and extracellular matrix. Cah Biol Mar 42(3):219–238
Astall C, Anderson S, Taylor A, Atkinson R (1997) Comparative studies of the branchial morphology, gill area and gill ultrastructure of some thalassinidean mud-shrimps (Crustacea: Decapoda: Thalassinidea). J Zool 241:665–688
Barton K (2009) MuMIn: multi-model inference, R package version 0.12. 0. https://r-forge.r-project.org/projects/mumin/
Bayer C, Vaupel P (2012) Acute versus chronic hypoxia in tumors. Strahlenther Onkol 188:616–627
Borda E, Kudenov JD, Chevaldonné P, Blake JA, Desbruyeres D, Fabri M-C, Hourdez S, Pleijel F, Shank TM, Wilson NG (2013) Cryptic species of Archinome (Annelida: Amphinomida) from vents and seeps. Proc R Soc Lond B Biol Sci 280:20131876
Cardigos F, Colaço A, Dando P, Ávila S, Sarradin P-M, Tempera F, Conceição P, Pascoal A, Santos RS (2005) Shallow water hydrothermal vent field fluids and communities of the D. João de Castro Seamount (Azores). Chem Geol 224:153–168
Cosentino A, Giacobbe S (2011) The new potential invader Linopherus canariensis (Polychaeta: Amphinomidae) in a Mediterranean coastal lake: Colonization dynamics and morphological remarks. Mar Pollut Bull 62:236–245
Dasgupta N, Patel AM, Scott BA, Crowder CM (2007) Hypoxic preconditioning requires the apoptosis protein CED-4 in C. elegans. Curr Biol 17:1954–1959
David E, Tanguy A, Pichavant K, Moraga D (2005) Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. Febs J 272:5635–5652
Dean TL, Richardson J (1999) Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. N Z J Mar Fresh 33:99–106
Decelle J, Andersen AC, Hourdez S (2010) Morphological adaptations to chronic hypoxia in deep-sea decapod crustaceans from hydrothermal vents and cold seeps. Mar Biol 157(6):1259–1269
Dhillon RS, Yao L, Matey V, Chen B-J, Zhang A-J, Cao Z-D, Fu S-J, Brauner CJ, Wang YS, Richards JG (2013) Interspecific differences in hypoxia-induced gill remodeling in carp. Physiol Biochem Zool 86:727–739
Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol 33:245–203
Ferraris JD (1981) Oxygen uptake with acute variation in temperature and salinity in two coral reef polychaetes. Mar Ecol 2:159–168
Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S (2012) Package ‘car’. Vienna: R Foundation for Statistical Computing.
Garcia HE, Levitus S (2006) World Ocean Atlas 2005. Vol. 3, Dissolved oxygen, apparent oxygen utilization, and oxygen saturation. NOAA Institutional Repository. https://repository.library.noaa.gov/view/noaa/1128
Gillet P, Dauvin J-C (2003) Polychaetes from the Irving, Meteor and Plato seamounts, North Atlantic Ocean: origin and geographical relationships. J Mar Biol Assoc UK 83:49–53
Giraudoux P (2013) pgirmess: data analysis in ecology. R package version 1.5. 8. R Foundation for Statistical Computing Vienna, Austria. https://cran.r-project.org/web/packages/pgirmess/index.html
Grecay P, Stierhoff K (2002) A device for simultaneously controlling multiple treatment levels of dissolved oxygen in laboratory experiments. J Exp Mar Biol Ecol 280:53–62
Hayes DS, Branco P, Santos JM, Ferreira T (2019) Oxygen depletion affects kinematics and shoaling cohesion of cyprinid fish. Water 11(4):642
Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu Rev Physiol 58:539–563
Herreid CF II (1980) Hypoxia in invertebrates. Comp Biochem Phys A 67:311–320
Hoogewijs D, Terwilliger N, Webster KA, Powell-Coffman J, Tokishita S, Yamagata H, Hankeln T, Burmester T, Rytkönen K, Nikinmaa M (2007) From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia. Integr Comp Biol 47:552–577
Johnston MA, Nuttall MF, Eckert RJ, Blakeway RD, Sterne TK, Hickerson EL, Schmahl GP, Lee MT, MacMillan J, Embesi JA (2019) Localized coral reef mortality event at East Flower Garden Bank, Gulf of Mexico. Bull Mar Sci 95:239–250
Lamont PA, Gage JD (2000) Morphological responses of macrobenthic polychaetes to low oxygen on the Oman continental slope, NW Arabian Sea. Deep-Sea Res Part II 47:9–24
Landon MS, Stasiak RH (1983) Daphnia hemoglobin concentration as a function of depth and oxygen availability in Arco Lake, Minnesota 1. Limnol Oceanogr 28:731–737
Levin LA, Gage JD (1998) Relationships between oxygen, organic matter and the diversity of bathyal macrofauna. Deep-Sea Res Part II 45:129–163
Lucey NM, Collins M, Collin R (2019) Oxygen-mediated plasticity confers hypoxia tolerance in a corallivorous polychaete. Ecol Evol. https://doi.org/10.1002/ece3.5929
Matey V, Richards JG, Wang Y, Wood CM, Rogers J, Davies R, Murray BW, Chen X-Q, Du J, Brauner CJ (2008) The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. J Exp Biol 211:1063–1074
McMahon BR, Wilkens JL (1975) Respiratory and circulatory responses to hypoxia in the lobster Homarus americanus. J Exp Biol 62(3):637–655
Mills DB, Ward LM, Jones C, Sweeten B, Forth M, Treusch AH, Canfield DE (2014) Oxygen requirements of the earliest animals. Proc Natl Acad Sci 111:4168–4172
Nelson HR, Altieri AH (2019) Oxygen: the universal currency on coral reefs. Coral Reefs 38(2):177–198
Nicolet K, Chong-Seng K, Pratchett M, Willis B, Hoogenboom M (2018) Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease. Sci Rep 8:1–10
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Commun Ecol Packag 10:631–637
Pechenik JA, Chaparro OR, Pilnick A, Karp M, Acquafredda M, Burns R (2016) Effects of embryonic exposure to salinity stress or hypoxia on post-metamorphic growth and survival of the polychaete Capitella teleta. Biol Bull 231(2):103–112
Peruzza L, Gerdol M, Oliphant A, Wilcockson D, Pallavicini A, Hawkins L, Thatje S, Hauton C (2018) The consequences of daily cyclic hypoxia on a European grass shrimp: from short-term responses to long-term effects. Funct Ecol 32:2333–2344
Pires IM, Bencokova Z, Milani M, Folkes LK, Li J-L, Stratford MR, Harris AL, Hammond EM (2010) Effects of acute versus chronic hypoxia on DNA damage responses and genomic instability. Cancer Res 70:925–935
Pollock M, Clarke L, Dubé M (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ Rev 15:1–14
Reipschläger A, Pörtner H-O (1996) Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J Exp Biol 199:1801–1807
Rice MM, Ezzat L, Burkepile DE (2019) Corallivory in the anthropocene: interactive effects of anthropogenic stressors and corallivory on coral reefs. Front Mar Sci 5:525
Richardson J, Williams EK, Hickey CW (2001) Avoidance behaviour of freshwater fish and shrimp exposed to ammonia and low dissolved oxygen separately and in combination. N Z J Mar Fresh 35:625–633
Righi S, Maletti I, Maltagliati F, Castelli A, Barbieri M, Fai S, Prevedelli D, Simonini R (2019) Morphometric and molecular characterization of an expanding Ionian population of the fireworm Hermodice carunculata (Annelida). J Mar Biol Assoc UK 99:1569–1577
Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D, Ripley MB (2013) Package ‘mass’. Cran R. Jan 8: 538. https://cran.r-project.org/web/packages/MASS/index.html
Roever C, Raabe N, Luebke K, Ligges U, Szepannek G, Zentgraf M, Ligges MU, SVMlight S (2018) Package ‘klaR’. https://cran.r-project.org/web/packages/klaR/index.html
Schöttler U, Grieshaber M (1988) Adaptation of the polychaete worm Scoloplos armiger to hypoxic conditions. Mar Biol 99:215–222
Schulze A, Grimes CJ, Rudek TE (2017) Tough, armed and omnivorous: Hermodice carunculata (Annelida: Amphinomidae) is prepared for ecological challenges. J Mar Biol Assoc UK. https://doi.org/10.1017/S0025315417000091
Simonini R, Maletti I, Righi S, Fai S, Prevedelli D (2018) Laboratory observations on predator–prey interactions between the bearded fireworm (Hermodice carunculata) and Mediterranean benthic invertebrates. Mar Freshw Behav Phy 51:145–158
Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673
R Core Team (2018) R: A language and environment for statistical computing
Wannamaker CM, Rice JA (2000) Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J Exp Mar Biol Ecol 249:145–163
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, Berlin
Wolf AT, Nugues MM, Wild C (2014) Distribution, food preference, and trophic position of the corallivorous fireworm Hermodice carunculata in a Caribbean coral reef. Coral Reefs 33:1153–1163
Wren J, Morris S, Gassmann M, Gorr T (2008) Response to hypoxia and low temperature in ganglionic cells of the crayfish Orconectes limosus. In: Proceedings of the 4th CPB Meeting in Africa: Mara, pp. 19–25.
Wu RS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45
Yáñez-Rivera B, Salazar-Vallejo SI (2011) Revision of Hermodice Kinberg, 1857 (Polychaeta: Amphinomidae). Sci Mar 75(2):251–62
Acknowledgements
As this is a portion of CJG’s dissertation, we acknowledge her committee members, Drs. Jerry Kudenov and Maria Pia Miglietta, and the Marine Biology Department for additional funding. Two undergraduate interns, Kyle Donnelly and Crystal Capps, assisted with morphological data acquisition and aquarium maintenance. We’d also like to acknowledge the Miglietta Lab, Katie St. Claire, Sea Life Facility volunteers, TAMUG staff and Cory Ames for help with experimental tank set up, maintenance, and map creation. Organisms were collected under the Florida Fish and Wildlife Conservation Commission (FWC) Special Activity License (SAL-17–1946-SR). Finally, we’d like to thank the reviewers for their feedback and suggestions.
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This project was funded by the TAMU-CAPES Collaborative Grant Program (grant 2015-16). We declare no conflicts of interest.
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This study was conceived by CJG, PCP and AS. CJG, LHP and AS designed the experimental set-up. CJG was primarily responsible for performing the experiments, collecting and analyzing the data and writing the manuscript. The data were discussed among all authors and all authors contributed wording and edits to the final version of the manuscript.
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Grimes, C.J., Paiva, P.C., Petersen, L.H. et al. Rapid plastic responses to chronic hypoxia in the bearded fireworm, Hermodice carunculata (Annelida: Amphinomidae). Mar Biol 167, 140 (2020). https://doi.org/10.1007/s00227-020-03756-0
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DOI: https://doi.org/10.1007/s00227-020-03756-0