Abstract
Cryptic species that are morphologically similar co-occur because either the rate of competitive exclusion is very slow, or because they are not, in fact, ecologically similar. The processes that maintain cryptic local diversity may, therefore, be particularly subtle and difficult to identify. Here, we uncover differences among several cryptic species in their relative abundance across a depth gradient within a dominant and ecologically important genus of hard coral, Pocillopora. From extensive sampling unbiased toward morphological characters, at multiple depths on the fore reef around the island of Mo’orea, French Polynesia, we genetically identified 673 colonies in the Pocillopora species complex. We identified 14 mitochondrial Open Reading Frame haplotypes (mtORFs, a well-studied and informative species marker used for pocilloporids), which included at least six nominal species, and uncovered differences among haplotypes in their relative abundance at 5, 10, and 20 m at four sites around the island. Differences in relative haplotype abundance across depths were greater than differences among sites separated by several kilometers. The four most abundant species are often visibly indistinguishable at the gross colony level, yet they exhibited stark differences in their associations with light irradiance and daily water temperature variance. The pattern of community composition was associated with frequent cooling in deeper versus shallower water more than warmer temperatures in shallow water. Our results indicate that these cryptic species are not all ecologically similar. The differential abundance of Pocillopora cryptic species across depth should promote their coexistence at the reef scale, as well as promote resilience through response diversity.
Data availability
R scripts and data used to perform analyses and prepare figures are available at Dryad (https://doi.org/10.5061/dryad.kwh70rz3p)
References
Adam TC, Schmitt RJ, Holbrook SJ, Brooks AJ, Edmunds PJ, Carpenter RC, Bernardi G (2011) Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation. PLoS One 6:e23717
Baird AH, Babcock RC, Mundy CP (2003) Habitat selection by larvae influences the depth distribution of six common coral species. Mar Ecol Prog Ser 252:289–293
Banguera-Hinestroza E, Ferrada E, Sawall Y, Flot JF (2019) Computational characterization of the mtORF of Pocilloporid Corals: Insights into protein structure and function in Stylophora lineages from contrasting Environments. Genes 10(324):1–30
Baskett ML, Fabina NS, Gross K (2014) Response diversity can increase ecological resilience to disturbance in coral reefs. Am Nat 184:E16–E31
Baums IB, Devlin-Durante M, Laing BAA, Feingold J, Smith T, Bruckner A, Monteiro J (2014) Marginal coral populations: the densest known aggregation of Pocillopora in the Galapagos Archipelago is of asexual origin. Front Mar Sci 1:1–11
Berkley HA, Kendall BE, Mitarai S, Siegel DA (2010) Turbulent dispersal promotes species coexistence. Ecol Lett 13:360–371
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155
Blanchet FG, Cazelles K, Gravel D (2020) Co-occurrence is not evidence of ecological interactions. Ecol Lett 23:1050–1063
Bode M, Bode L, Armsworth PR (2011) Different dispersal abilities allow reef fish to coexist. Proc Natl Acad Sci U S A 108:16317–16321
Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871
Bongaerts P, Frade PR, Ogier JJ, Hay KB, Van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of Agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205
Bongaerts P, Cooke IR, Ying H, Wels D, Haan den S, Hernandez-Agreda A, Brunner CA, Dove S, Englebert N, Eyal G, Forêt S, Grinblat M, Hay KB, Harii S, Hayward DC, Lin Y, Mihaljević M, Moya A, Muir P, Sinniger F, Smallhorn-West P, Torda G, Ragan MA, van Oppen MJH, Hoegh-Guldberg O (2021) Morphological stasis masks ecologically divergent coral species on tropical reefs. Curr Biol. https://doi.org/10.1016/j.cub.2021.03.028
Boulay JN, Hellberg ME, Cortés J, Baums IB (2014) Unrecognized coral species diversity masks differences in functional ecology. Proc Biol Sci 281:20131580
Bouwmeester J, Berumen ML, Baird AH (2011) Daytime broadcast spawning of Pocillopora verrucosa on coral reefs of the central Red Sea Galaxea,. J Coral Reef Stud 13:23–24
Brener-Raffalli K, Clerissi C, Vidal-Dupiol J, Adjeroud M, Bonhomme F, Pratlong M, Aurelle D, Mitta G, Toulza E (2018) Thermal regime and host clade, rather than geography, drive Symbiodinium and bacterial assemblages in the scleractinian coral Pocillopora damicornis sensu lato. Microbiome 6(39):1–13
Burgess SC, Johnston EC, Wyatt ASJ, Leichter JJ, Edmunds PJ (2021) Response diversity in corals: hidden differences in bleaching mortality among cryptic Pocillopora species. Ecology: e03324. https://doi.org/10.1002/ecy.3324
Carlon DB, Budd AF (2002) Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56:2227–2242
Chapin FS, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366
Combosch DJ & Vollmer SV (2013) Mixed asexual and sexual reproduction in the Indo-Pacific reef coral Pocillopora damicornis. Ecol Evol 3(10):3379–3387. https://doi.org/10.1002/ece3.721
Cunning R, Glynn PW, Baker AC (2013) Flexible associations between Pocillopora corals and Symbiodinium limit utility of symbiosis ecology in defining species. Coral Reefs 32:795–801
Daly AJ, De Meester N, Baetens JM, Moens T, De Baets B (2021) Untangling the mechanisms of cryptic species coexistence in a nematode community through individual-based modelling. Oikos 130:587–600
Darling ES, McClanahan TR, Côté IM (2013) Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol 19:1930–1940
Edmunds PJ, Leichter JJ, Johnston EC, Tong EJ, Toonen RJ (2016) Ecological and genetic variation in reef-building corals on four Society Islands. Limnol Oceanogr 61:543–557
Edmunds P, Adam T, Baker A, Doo S, Glynn P, Manzello D, Silbiger N, Smith T, Fong P (2019) Why more comparative approaches are required in time-series analyses of coral reef ecosystems. Mar Ecol Prog Ser 608:297–306
Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494
Flot JF, Tillier S (2007) The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: the putative D-loop and a novel ORF of unknown function. Gene 401:80–87
Flot JF, Magalon H, Cruaud C, Couloux A, Tillier S (2008) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus - Biol 331:239–247
Forsman ZH, Johnston EC, Brooks AJ, Adam TC, Toonen RJ (2013) Genetic evidence for regional isolation of Pocillopora corals from Moorea. Oceanography 26:153–155
Frouin R, Franz BA, Werdell product PJTSP (2003) The seawifs PAR product. In: Hooker SB, Firestone ER (eds) Algorithm Updates for the Fourth SeaWiFS Data Reprocessing: NASA Technical Memo 2003–206892. NASA Goddard Space Flight Center, Greenbelt, Maryland, pp 46–50
Gaither MR, Szabó Z, Crepeau MW, Bird CE, Toonen RJ (2011) Preservation of corals in salt-saturated DMSO buffer is superior to ethanol for PCR experiments. Coral Reefs 30:329–333
Gélin P, Postaire B, Fauvelot C, Magalon H (2017) Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites. Mol Phylogenet Evol 109:430–446
Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama and Galápagos Islands (Ecuador). Part I Pocilloporidae Mar Biol 109:355–368
Gómez-Corrales M, Prada C (2020) Cryptic lineages respond differently to coral bleaching. Mol Ecol 29:4265–4274
González AM, Prada CA, Ávila V, Medina M (2018) Ecological speciation in corals. In: Oleksiak M, Rajora O (eds) Population genomics: Marine organisms. Population genomics, Cham
Hirose M, Kinzie RA, Hidaka M (2000) Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol Bull 199:68–75
Holbrook SJ, Adam TC, Edmunds PJ, Schmitt RJ, Carpenter RC, Brooks AJ, Lenihan HS, Briggs CJ (2018) Recruitment drives spatial variation in recovery rates of resilient coral reefs. Sci Rep 8:7338
Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301
Johnston EC, Forsman ZH, Flot J, Schmidt-Roach S, Pinzón J, Knapp ISS, Toonen RJ (2017) A genomic glance through the fog of plasticity and diversification in Pocillopora. Sci Rep 7:5991
Johnston EC, Forsman ZH, Toonen RJ (2018) A simple molecular technique for distinguishing species reveals frequent misidentification of Hawaiian corals in the genus Pocillopora. PeerJ 6:e4355
Johnston EC, Counsell CW, Sale TL, Burgess SC, Toonen RJ (2020) The legacy of stress: Coral bleaching impacts reproduction years later. Funct Ecol 34:2315–2325
Kayal M, Lenihan HS, Brooks AJ, Holbrook SJ, Schmitt RJ, Kendall BE (2018) Predicting coral community recovery using multi-species population dynamics models. Ecol Lett 22:605–615
Knowlton N, Weil E, Weigt LA, Guzmán HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330–333
Legendre P, Andersson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Levin SA, Lubchenco J (2008) Resilience, robustness, and marine ecosystem-based management. Bioscience 58:27–32
Levitan DR (2004) Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. Am Nat 164:298–309
Levitan DR, Fogarty ND, Jara J, Lotterhos KE, Knowlton N (2011) Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65:1254–1270
Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868
Marti-Puig P, Forsman ZH, Haverkort-yeh RD, Knapp ISS, Maragos JE, Toonen RJ (2014) Extreme phenotypic polymorphism in the coral genus Pocillopora; micro-morphology corresponds to mitochondrial groups, while colony morphology does not. Bull Mar Sci 90:1–22
Massé LM, Séré MG, Smit AJ, Schleyer MH (2013) Sexual reproduction in Pocillopora damicornis at high latitude off South Africa. West Indian Ocean J Mar Sci 11:55–65
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093
Mayfield AB, Bruckner AW, Chen C, Chen C (2015) A survey of pocilloporid corals and their endosymbiotic dinoflagellate communities in the Austral and Cook Islands of the South Pacific. Platax 12:1–17
McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7
McPeek MA, Gomulkiewicz R (2005) Assembling and depleting species richness in metacommunities: insights from ecology, population genetics and macroevolution. In: Holyoak M et al (eds) Metacommunities: Spatial Dynamics and Ecological Communities. University of Chicago, Chicago (IL), pp 355–373
De Meester N, Derycke S, Bonte D, Moens T (2011) Salinity effects on the coexistence of cryptic species: a case study on marine nematodes. Mar Biol 158:2717–2726
Miller DJ, Ball EE (2000) The coral Acropora: what it can contribute to our knowledge of metazoan evolution and the evolution of developmental processes. BioEssays 22:291–296
Montero-Pau J, Ramos-Rodríguez E, Serra M, Gómez A (2011) Long-term coexistence of rotifer cryptic species. PLoS One 6:e21530
Morel A, Huot Y, Gentili B, Werdell PJ, Hooker SB, Franz BA (2007) Examining the consistency of products derived from various ocean color sensors in open ocean (Case 1) waters in the perspective of a multi-sensor approach. Remote Sens Environ 111:69–88
Mundy CN, Babcock RC (1998) Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement? J Exp Mar Bio Ecol 223:235–255
Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens M, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2.5–6. https://cran.r-project.org/web/packages/vegan/index.html
De Palmas S, Soto D, Denis V, Ho M-J, Chen CA (2018) Molecular assessment of Pocillopora verrucosa (Scleractinia; Pocilloporidae) distribution along a depth gradient in Ludao. Taiwan. PeerJ 6:e5797
Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420
Paz-García DA, Hellberg ME, García-de-León FJ, Balart EF (2015a) Switch between morphospecies of Pocillopora corals. Am Nat 186:434–440
Paz-García DA, Aldana-Moreno A, Cabral-Tena RA, García-De-León FJ, Hellberg ME, Balart EF (2015b) Morphological variation and different branch modularity across contrasting flow conditions in dominant Pocillopora reef-building corals. Oecologia 178:207–218
Penin L, Michonneau F, Baird A, Connolly S, Pratchett M, Kayal M, Adjeroud M (2010) Early post-settlement mortality and the structure of coral assemblages. Mar Ecol Prog Ser 408:55–64
Pinzón JH, Reyes-Bonilla H, Baums IB, LaJeunesse TC (2012) Contrasting clonal structure among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California. Coral Reefs 31:765–777
Pinzón JH, Sampayo E, Cox E, Chauka LJ, Chen CA, Voolstra CR, LaJeunesse TC (2013) Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). J Biogeogr 40:1595–1608
Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci U S A 110:3961–3966
Prada C, Hellberg ME (2021) Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation? J Evol Biol 34:128–137
Pratchett MS, McCowan D, Maynard JA, Heron SF (2013) Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea. French Polynesia. PLoS One 8:e70443
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Richards ZT, Berry O, van Oppen MJH (2016) Cryptic genetic divergence within threatened species of Acropora coral from the Indian and Pacific Oceans. Conserv Genet 17:577–591
Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc B Biol Sci 272:573–579
Rouzé H, Lecellier G, Pochon X, Torda G, Berteaux-Lecellier V (2019) Unique quantitative Symbiodiniaceae signature of coral colonies revealed through spatio-temporal survey in Moorea. Sci Rep 9:7921
Sawall Y, Al-Sofyani A, Hohn S, Banguera-Hinestroza E, Voolstra CR, Wahl M (2015) Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci Rep 5:8940
Schmidt-Roach S, Miller KJ, Woolsey E, Gerlach G, Baird AH (2012) Broadcast spawning by Pocillopora species on the Great Barrier Reef. PLoS One 7:e50847
Schmidt-Roach S, Lundgren P, Miller KJ, Gerlach G, Noreen AME, Andreakis N (2013) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32:161–172
Schmidt-Roach S, Miller KJ, Lundgren P, Andreakis N (2014) With eyes wide open: a revision of species within and closely related to the Pocillopora damicornis species complex (Scleractinia; Pocilloporidae) using morphology and genetics. Zool J Linn Soc 170:1–33
Snyder RE, Chesson P (2004) How the spatial scales of dispersal, competition, and environmental heterogeneity interact to affect coexistence. Am Nat 164:633–650
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
Torda G, Lundgren P, Willis BL, van Oppen MJH (2013) Genetic assignment of recruits reveals short- and long-distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef. Mol Ecol 22:5821–5834
Tsounis G & Edmunds PJ (2016) The potential for self-seeding by the coral Pocillopora spp. in Moorea, French Polynesia. PeerJ 4:e2544
Warner PA, Van Oppen MJH, Willis BL (2015) Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial-genetic patterns of connectivity. Mol Ecol 24:2993–3008
Whitney JL, Bowen BW, Karl SA (2018) Flickers of speciation: sympatric colour morphs of the arc-eye hawkfish, Paracirrhites arcatus, reveal key elements of divergence with gene flow. Mol Ecol 27:1479–1493
Wyatt ASJ, Leichter JJ, Toth LT, Miyajima T, Aronson RB, Nagata T (2020) Heat accumulation on coral reefs mitigated by internal waves. Nat Geosci 13:28–34
Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96:1463–1468
Zhang DY, Lin K, Hanski I (2004) Coexistence of cryptic species. Ecol Lett 7:165–169
Acknowledgements
This work was funded by a National Science Foundation (NSF) grant to S. C. Burgess (OCE 18-29867). We thank J. Powell and C. Peters for invaluable assistance in the field, C. Peters and the Florida State University Dive Program for facilitating field work on SCUBA, the staff of the UC Berkeley Richard B. Gump South Pacific Research Station for facilitating our research, and M. Hay for logistical support. Research was completed under permits issued by the French Polynesian Government (Délégation à la Recherche), the Haut-Commissariat de la République en Polynésie Française (DTRT) (Protocole d’Accueil 2019), and the U.S. Fish and Wildlife. A. S. J. Wyatt was supported by funding from the Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (SMSEGL20SC01) and the Research Grants Council (RGC) of Hong Kong (RGC Project No. 26100120).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Topic Editor James Davis Reimer
Rights and permissions
About this article
Cite this article
Johnston, E.C., Wyatt, A.S.J., Leichter, J.J. et al. Niche differences in co-occurring cryptic coral species (Pocillopora spp.). Coral Reefs 41, 767–778 (2022). https://doi.org/10.1007/s00338-021-02107-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-021-02107-9