Abstract
Emerging evidence indicates that individual stressors can modify the coral microbiome; however, few studies have examined the impacts of multiple stressors through natural climatic events. During periods of low and high heat stress associated with the 2015–2016 El Niño, we tracked the microbiomes of two coral species (Porites lobata and Montipora aequituberculata) across sites on Kiritimati (Christmas) Island with different levels of local disturbance (i.e. subsistence fishing, pollution, dredging). At low heat stress, local disturbance was associated with increased microbial alpha diversity (i.e. number of microbial OTUs and their relative abundance) in both species and increased beta diversity (i.e. coral to coral variation in microbial community composition) in P. lobata. High levels of thermal stress subsequently elevated microbial beta diversity in both species at the low disturbance sites up to the level experienced at the high disturbance sites under low heat stress, illustrating that each stressor can destabilize the coral microbiome. However, with high heat stress microbial alpha diversity was no longer significantly different between disturbance levels for either species. Survival of P. lobata throughout the entire El Niño event was greater at low disturbance sites than high ones (40% vs. 15%), suggesting that protection from local stressors may enhance survival of stress-tolerant corals. However, no M. aequituberculata tracked in this study survived the thermal anomaly. Whether enhanced survivorship can be directly attributed to lower microbial diversity, however, remains to be tested. Overall, we found that, rather than acting synergistically, multiple stressors either acted antagonistically to one another (alpha diversity for both coral species, beta diversity for P. lobata) or exhibited dominance (beta diversity for M. aequituberculata), suggesting that multiple stressors cause various interaction outcomes on the coral microbiome and highlighting the need for future research to evaluate these interactions and their consequences for coral resilience.
Similar content being viewed by others
References
Ainsworth TD, Gates RD (2016) Ocean Biology. Corals’ microbial sentinels. Science 352:1518–1519
Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342
Ban SS, Graham NAJ, Connolly SR (2014) Evidence for multiple stressor interactions and effects on coral reefs. Glob Change Biol 20:681–697
Barton K (2016) MuMIn: Multi-model inference. R package version 1.15.6
Beijbom O, Edmunds PJ, Kline DI, Mitchell BG, Kriegman D (2012) Automated annotation of coral reef survey images. IEE Conference on Computer Vision and Pattern Recognition
Beijbom O, Edmunds PJ, Roelfsema C, Smith J, Kline DI, Neal BP, Dunlap MJ, Moriarty V, Fan T-Y, Tan C-J, Chan S, Treibitz T, Gamst A, Mitchell BG, Kriegman D (2015) Towards Automated Annotation of Benthic Survey Images: Variability of Human Experts and Operational Modes of Automation. PLoS ONE 10:e0130312–e0130322
Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55
Blackall LL, Wilson B, van Oppen MJH (2015) Coral-the world’s most diverse symbiotic ecosystem. Mol Ecol 24:5330–5347
Bourne D, Iida Y, Uthicke S, Smith-Keune C (2007) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7:335–336
Carilli JE, Norris RD, Black BA, Walsh SM, one MMP, 2009 Local stressors reduce coral resilience to bleaching. PLoS One https://doi.org/10.1371/journal.pone.0006324
Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563
Ceh J, Kilburn MR, Cliff JB, Raina J-B, van Keulen M, Bourne DG (2013) Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol 3:2393–2400
Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, Bushman FD, Collman RG (2012) Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med 186:536–545
Côté IM, Darling ES, Brown CJ (2016) Interactions among ecosystem stressors and their importance in conservation. Proc Biol, Sci, p 283
Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386
Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286
De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999
EMP (2016) DNA extraction protocol. Earth Microbiome Project http://www.earthmicrobiome.org/protocols-and-standards/dna-extraction-protocol/:
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146
Frias-Lopez J, Klaus JS, Bonheyo GT, Fouke BW (2004) Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70:5955–5962
Garren M, Raymundo L, Guest J, Harvell CD, Azam F (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS ONE 4:e7319–9
Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:1–13
Gove JM, McManus MA, Neuheimer AB, Polovina JJ, Drazen JC, Smith CR, Merrifield MA, Friedlander AM, Ehses JS, Young CW, Dillon AK, Williams GJ (2016) Near-island biological hotspots in barren ocean basins. Nat Comm 7:10581
Hester ER, Barott KL, Nulton J, Vermeij MJ, Rohwer FL (2016) Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J 10:1157–1169
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C-Y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Iacarella JC, Adamczyk E, Bowen D, Chalifour L, Eger A, Heath W, Helms S, Hessing-Lewis M, Hunt BPV, MacInnis A, O’Connor MI, Robinson CLK, Yakimishyn J, Baum JK (2018) Anthropogenic disturbance homogenizes seagrass fish communities. Glob Change Biol 24:1904–1918
Jessen C, Villa Lizcano JF, Bayer T, Roder C, Aranda M, Wild C, Voolstra CR (2013) In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS ONE 8:e62091–11
Kirchman D, Sigda J, Kapuscinski R, Mitchell R (1982) Statistical analysis of the direct count method for enumerating bacteria. Appl Environ Microbiol 44:376–382
Krediet CJ, Ritchie KB, Alagely A, Teplitski M (2012) Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J 7:980–990
Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Microbiol 51:1383–1388
Kushmaro A, Rosenberg E, Fine M, Ben-Haim Y, Loya Y (1998) Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 171:131–137
Kvennefors ECE, Sampayo E, Kerr C, Vieira G, Roff G, Barnes AC (2011) Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol 63:605–618
Lagkouvardos I, Fischer S, Kumar N, Clavel T (2017) Rhea: a transparent and modular R pipeline for microbial profiling based on 16S rRNA gene amplicons. PeerJ
Lee STM, Davy SK, Tang S-L, Kench PS (2016) Mucus sugar content shapes the bacterial community structure in thermally stressed Acropora muricata. Front Microbiol 7:3274–11
Lee Yang J, Bougouffa S, Wang Y, Batang Z, Tian R, Al-Suwailem A, Qian PY (2012) Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing. Appl Environ Microbiol 78:7173–7184
Lema KA, Willis BL, Bourne DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78:3136–3144
Lenth RV (2016) Least-squares means: the rpackage lsmeans. J Stat Soft 69:
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing Cyanobacteria in corals. Science 305:997–1000
Liu G, Rauenzahn J, Heron SF, Eakin CM, Skirving W, Christensen T, Strong A, Li J (2013) NOAA Coral Reef Watch 50 km satellite sea surface temperature-based decision support system for coral bleaching management
McDevitt-Irwin JM, Baum JK, Garren M, Thurber RV (2017) Responses of coral-associated bacterial communities to local and global stressors. Front Mar Sci 4:1–16
McKew BA, Dumbrell AJ, Daud SD, Hepburn L, Thorpe E, Mogensen L, Whitby C (2012) Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 78:5229–5237
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217
McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531
Meron D, Atias E, Iasur Kruh L, Elifantz H, Minz D, Fine M, Banin E (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5:51–60
Moeller AH, Shilts M, Li Y, Rudicell RS, Lonsdorf EV, Pusey AE, Wilson ML, Hahn BH, Ochman H (2013) SIV-induced instability of the chimpanzee gut microbiome. Cell Host Microbe 14:340–345
Morris EK, Caruso T, Buscot F, Fischer M, Hancock C, Maier TS, Meiners T, Müller C, Obermaier E, Prati D, Socher SA, Sonnemann I, Wäschke N, Wubet T, Wurst S, Rillig MC (2014) Choosing and using diversity indices: insights for ecological applications from the German Biodiversity Exploratories. Ecol Evol 4:3514–3524
Morrow KM, Bourne DG, Humphrey C, Botté ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE, Webster NS (2015) Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J 9:894–908
Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449
Mouchka ME, Hewson I, Harvell CD (2010) Coral-Associated Bacterial Assemblages: Current Knowledge and the Potential for Climate-Driven Impacts. Integr Comp Biol 50:662–674
National Statistics Office (2016) Kiribati 2015 population and housing census volume 1
Neave MJ, Michell CT, Apprill A, Voolstra CR (2017) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci Rep 7:40579
Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F, Carlson CA (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7:962–979
NOAA Coral Reef Watch (2013) NOAA Coral Reef Watch daily global 5-km satellite virtual station time series data for the Northern Line Islands. https://coralreefwatch.noaa.gov/vs/gauges/northern_line_islands.php
Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, OHara R, Simpson G, Solymos P, Stevens H, Szoecs E, Wagner H (2016) vegan: community ecology package
Olden JD, Rooney TP (2006) On defining and quantifying biotic homogenization. Global Ecol Biogeogr 15:113–120
Pantos O, Bongaerts P, Dennis PG, Tyson GW, Hoegh-Guldberg O (2015) Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9:1916–1927
Pinzón JH, Kamel B, Burge CA, Harvell CD, Medina M, Weil E, Mydlarz LD (2015) Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R Soc Open Sci 2:140214
Pratte ZA, Longo GO, Burns AS, Hay ME, Stewart FJ (2017) Contact with turf algae alters the coral microbiome: contact versus systemic impacts. Coral Reefs 37:1–13
Qian H, Ricklefs RE (2006) The role of exotic species in homogenizing the North American flora. Ecol Lett 9:1293–1298
Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501
Ritchie K (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser. 322:1–14
Roder C, Arif C, Bayer T, Aranda M, Daniels C, Shibl A, Chavanich S, Voolstra CR (2014) Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J 8:31–39
Roder C, Bayer T, Aranda M, Kruse M, Voolstra CR (2015) Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol 24:3501–3511
Röthig T, Ochsenkühn MA, Roik A, van der Merwe R, Voolstra CR (2016) Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25:1308–1323
Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39
Santos HF, Carmo FL, Duarte G, Dini-Andreote F, Castro CB, Rosado AS, van Elsas JD, Peixoto RS (2014) Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J 8:2272–2279
Schielzeth H, Nakagawa S (2013) Nested by design: model fitting and interpretation in a mixed model era. Methods Ecol Evo 4:14–24
Sharp KH, Distel D, Paul VJ (2012) Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J 6:790–801
Shnit-Orland M, Sivan A, Kushmaro A (2012) Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb Ecol 64:851–859
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3:512–521
Sutherland KP, Shaban S, Joyner JL, Porter JW, Lipp EK (2011) Human pathogen shown to cause disease in the threatened elkhorn coral Acropora palmata. PLoS ONE 6:e23468–7
Sweet MJ, Croquer A, Bythell JC (2010) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
Tout J, Siboni N, Messer LF, Garren M, Stocker R, Webster NS, Ralph PJ, Seymour JR (2015) Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Front Microbiol 6:403–412
Vega Thurber R, Burkepile DE, Correa AMS, Thurber AR, Shantz AA, Welsh R, Pritchard C, Rosales S (2012) Macroalgae decrease growth and alter microbial community structure of the reef-building coral, Porites astreoides. PLoS ONE 7:e44246–10
Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163
Vega Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR (2013) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Change Biol 20:544–554
Vidal-Dupiol J, Dheilly NM, Rondon R, Grunau C, Cosseau C, Smith KM, Freitag M, Adjeroud M, Mitta G (2014) Thermal stress triggers broad Pocillopora damicornis transcriptomic remodeling, while Vibrio coralliilyticus infection induces a more targeted immuno-suppression response. PLoS ONE 9:e107672–15
Walsh SM (2011) Ecosystem-scale effects of nutrients and fishing on coral reefs. J Mar Biol 2011:1–13
Wang L, Shantz AA, Payet JP, Sharpton TJ, Foster A, Burkepile DE, Vega Thurber R (2018) Corals and their microbiomes are differentially affected by exposure to elevated nutrients and a natural thermal anomaly. Front Mar Sci 5:36
Watson MS, Claar DC, Baum JK (2016) Subsistence in isolation: Fishing dependence and perceptions of change on Kiritimati, the world’s largest atoll. Ocean and Coastal Management 123:1–8
Wear SL, Thurber RV (2015) Sewage pollution: mitigation is key for coral reef stewardship. Ann NY Acad Sci n/a–n/a
Webster NS, Negri AP, Botté ES, Laffy PW, Flores F, Noonan S, Schmidt C, Uthicke S (2016) Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci Rep 1–9
Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719
Welsh RM, Rosales SM, Zaneveld J, Payet JP (2015) Alien vs. Predator: Pathogens open niche space for opportunists, unless controlled by predators. PeerJ
Welsh RM, Zaneveld JR, Rosales SM, Payet JP, Burkepile DE, Thurber RV (2016) Bacterial predation in a marine host-associated microbiome. ISME J 10:1540–1544
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70
Zaneveld JR, McMinds R, Vega Thurber R (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:17121
Zaneveld JR, Shantz AA, Pritchard CE, McMinds R, Payet JEROMP, Welsh R, Correa AMS, Lemoine NP, Rosales S, Fuchs C, Maynard JA, Burkepile DE, Thurber RV (2016) Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Comm 7:1–12
Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016a) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105:629–640
Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016b) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. 1–12
Acknowledgements
JMI acknowledges funding from a Natural Sciences and Engineering Research Council of Canada (NSERC) Canada Graduate Scholarship and Michael Smith Foreign Study Supplement, and from Sigma Xi, American Museum of Natural History, and the University of Victoria; JKB acknowledges support from NSF RAPID (OCE-1446402), the Packard Foundation, the Rufford Maurice Laing Foundation, an NSERC Discovery Grant, the Canadian Foundation for Innovation, the British Columbia Knowledge Development Fund, the University of Victoria and UVic’s Centre for Asia–Pacific Initiatives. This work was also supported by a NSF Dimensions of Biodiversity Grant to (DOB #1442306) RLVT. We thank Danielle Claar for all of her help with the sea surface temperature data. We also thank Danielle Claar, Kristina Tietjen, Lisa Szostek, and Kieran Cox for assistance collecting the data in the field, and the support of the Kiribati Government in conducting this research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states there is no conflict of interest.
Additional information
Topic Editor Morgan S. Pratchett
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
McDevitt-Irwin, J.M., Garren, M., McMinds, R. et al. Variable interaction outcomes of local disturbance and El Niño-induced heat stress on coral microbiome alpha and beta diversity. Coral Reefs 38, 331–345 (2019). https://doi.org/10.1007/s00338-019-01779-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01779-8