Skip to main content

Advertisement

SpringerLink
Log in

Partitioning resilience of a marine foundation species into resistance and recovery trajectories

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The resilience of an ecological unit encompasses resistance during adverse conditions and the capacity to recover. We adopted a ‘resistance-recovery’ framework to experimentally partition the resilience of a foundation species (the seagrass Cymodocea nodosa). The shoot abundances of nine seagrass meadows were followed before, during and after simulated light reduction conditions. We determined the significance of ecological, environmental and genetic drivers on seagrass resistance (% of shoots retained during the light deprivation treatments) and recovery (duration from the end of the perturbed state back to initial conditions). To identify whether seagrass recovery was linearly related to prior resistance, we then established the connection between trajectories of resistance and recovery. Finally, we assessed whether recovery patterns were affected by biological drivers (production of sexual products—seeds—and asexual propagation) at the meadow-scale. Resistance to shading significantly increased with the genetic diversity of the meadow and seagrass recovery was conditioned by initial resistance during shading. A threshold in resistance (here, at a ca. 70% of shoot abundances retained during the light deprivation treatments) denoted a critical point that considerably delays seagrass recovery if overpassed. Seed densities, but not rhizome elongation rates, were higher in meadows that exhibited large resistance and quick recovery, which correlated positively with meadow genetic diversity. Our results highlight the critical role of resistance to a disturbance for persistence of a marine foundation species. Estimation of critical trade-offs between seagrass resistance and recovery is a promising field of research to better manage impacts on seagrass meadows.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and material

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Alberto F, Correia L, Billot C, Duarte CM, Serrao E (2003) Isolation and characterization of microsatellite markers for the seagrass Cymodocea nodosa. Mol Ecol Notes 3:397–399

    CAS  Google Scholar 

  • Alberto F, Arnaud-Haond S, Duarte CM, Serrao EA (2006) Genetic diversity of a clonal angiosperm near its range limit: the case of Cymodocea nodosa at the Canary Islands. Mar Ecol Prog Ser 309:117–129

    CAS  Google Scholar 

  • Alberto F, Massa S, Manent P, Diaz-Almela E, Arnaud-Haond S, Duarte CM, Serrao EA (2008) Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean-Atlantic transition region. J Biogeogr 35:1279–1294

    Google Scholar 

  • Barry SC, Jacoby CA, Frazer TK (2018) Resilience to shading influenced by differential allocation of biomass in Thalassia testudinum. Limnol Oceanogr 63:1817–1831

    Google Scholar 

  • Bartoń K (2016) MuMIn: multi-model inference. R Package Version 1(15):6

    Google Scholar 

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press Princeton, USA

    Google Scholar 

  • Boschetti F, Prunera K, Vanderklift MA, Thomson DP, Babcock RC, Doropoulos C, Cresswell A, Lozano-Montes H (2019) Information-theoretic measures of ecosystem change, sustainability, and resilience. ICES J Mar Sci. https://doi.org/10.1093/icesjms/fsz105

    Article  Google Scholar 

  • Bulleri F, Eriksson BK, Queiros A, Airoldi L, Arenas F, Arvanitidis C, Bouma TJ, Crowe TP, Davoult D, Guizien K, Ivesa L, Jenkins SR, Michalet R, Olabarria C, Procaccini G, Serrao EA, Wahl M, Benedetti-Cecchi L (2018) Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversity. PLoS Biol 16(9):2006852

    Google Scholar 

  • Connell SD, Ghedini G (2015) Resisting regime-shifts: the stabilising effect of compensatory processes. Trends Ecol Evol 30:513–515

    PubMed  Google Scholar 

  • Connell SD, Nimmo SD, Ghedini G, Mac Nally R, Bennett AF (2016) Ecological resistance—why mechanisms matter: a reply to Sundstrom et al. Trends Ecol Evol 31:413–414

    PubMed  Google Scholar 

  • Connolly RM, Smith TM, Maxwell PS, Olds AD, Macreadie PI, Sherman CDH (2018) Highly disturbed populations of seagrass show increased resilience but lower genotypic diversity. Front Plant Sci 9:894

    PubMed  PubMed Central  Google Scholar 

  • El-Hacen EH, Bouma TJ, Fivash GS, Sall AA, Piersma T, Olff H, Govers LL (2018) Evidence for ‘critical slowing down’ in seagrass: a stress gradient experiment at the southern limit of its range. Sci Rep 8:17263

    PubMed  PubMed Central  Google Scholar 

  • Erftemeijer PL, Lewis R III, Roy R (2006) Environmental impacts of dredging on seagrasses: a review. Mar Pollut Bull 52:1553–1572

    CAS  PubMed  Google Scholar 

  • Evans SM, Sinclair EA, Poore AGB, Bain KF, Vergés A (2017) Genotypic diversity and short-term response to shading stress in a threatened seagrass: does low diversity mean low resilience? Front Plant Sci 8:1417

    PubMed  PubMed Central  Google Scholar 

  • Falk DA, Watts AC, Thode AE (2019) Scaling ecological resilience. Front Ecol Evol 7:275

    Google Scholar 

  • Fox J (2005) The R Commander: a basic statistics graphical user interface to R. J Stat Softw 14:1–42

    Google Scholar 

  • Gartner A, Tuya F, Lavery PS, McMahon K (2013) Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. J Exp Mar Biol Ecol 439:143–151

    Google Scholar 

  • Gunderson LH, Allen CR, Holling CS (2010) Foundations of ecological resilience. Island Press, Washington

    Google Scholar 

  • Harrison XA, Donaldson L, Correa-Cano ME, Evans J, Fisher DN, Goodwin CED, Robinson BS, Hodgson DJ, Inger R (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. Peer J 6:e4794

    PubMed  PubMed Central  Google Scholar 

  • Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Hodgson D, McDonald JL, Hosken DJ (2015) What do you mean, ‘resilient’? Trends Ecol Evol 30:503–506

    PubMed  Google Scholar 

  • Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 1:1–23

    Google Scholar 

  • Hoover DL, Knapp AK, Smith MD (2014) Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95:2646–2656

    Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ingrisch J, Bahn M (2018) Towards a comparable quantification of resilience. Trends Ecol Evol 33:251–259

    PubMed  Google Scholar 

  • Jahnke M, Pagès JF, Alcoverro T, Lavery PS, McMahon KM, Procaccini G (2015) Should we sync? Seascape-level genetic and ecological factors determine seagrass flowering patterns. J Ecol 103:1464–1474

    CAS  Google Scholar 

  • Kendrick G, Waycott M, Carruthers TJB, Cambridge ML, Hovey R, Krauss SL, Lavery PS, Les DH, Lowe RJ, Mascaró O, Ooi JLS, Orth RJ, Rivers DO, Ruiz-Montoya L, Sinclair EA, Statton J, Kornelis J, Verduin JJ (2012) The central role of dispersal in the maintenance and persistence of seagrass populations. Bioscience 62:56–65

    Google Scholar 

  • Kilminster K, McMahon K, Waycott M, Kendrick GA, Scanes P, McKenzie L, O’Brien KR, Lyons M, Ferguson A, Maxwell P, Glasby T, Udy J (2015) Unravelling complexity in seagrass systems for management: Australia as a microcosm. Sci Total Environ 534:97–109

    CAS  PubMed  Google Scholar 

  • Massa SI, Paulino CM, Serrão EA, Duarte CM, Arnaud-Haond S (2013) Entangled effects of allelic and clonal (genotypic) richness in the resistance and resilience of experimental populations of the seagrass Zostera noltii to diatom invasion. BMC Ecol 13:39

    PubMed  PubMed Central  Google Scholar 

  • Maxwell P, Eklof J, van Katwijk MM, O’Brien KR, de la Torre-Castro M, Boström C, Bouma TJ, Krause-Jensen D, Unsworth RKF, van Tussenbroek BI (2016) The fundamental role of ecological feedback mechanisms in seagrass ecosystems—a review. Biol Rev 92:1521–1538

    PubMed  Google Scholar 

  • Nimmo DG, Mac Nally R, Cunningham SC, Haslem A, Bennet AF (2015) Vive la résistance: reviving resistance for 21st century conservation. Trends Ecol Evol 30:516–523

    CAS  PubMed  Google Scholar 

  • Nyström M, Norström AV, Blenckner T, de la Torre-Castro M, Eklöf JS, Folke C, Österblom H, Steneck RS, Thyresson M, Troell M (2012) Confronting feedbacks of degraded marine ecosystems. Ecosystems 15:695–710

    Google Scholar 

  • O’Brien KR, Waycott M, Maxwell P, Kendrick GA, Udy JW, Ferguson AJP, Kilminster K, Scanes P, McKenzie LJ, McMahon K, Adams MP, Samper-Villarreal J, Collier C, Lyons M, Munby PJ, Radke L, Christianen MJA, William C, Dennison WC (2018) Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance. Mar Poll Bull 134:166–176

    CAS  Google Scholar 

  • Oliver TH, Heard MS, Isaac NJB, Roy DB, Procter D, Eigenbrod F, Freckleton R, Hector A, Orme CDL, Petchey OL, Proença V, Raffaelli D, Blake Suttle K, Mace GM, Martín-López B, Woodcock BA, Bullock JM (2016) A synthesis is emerging between biodiversity–ecosystem function and ecological resilience research: reply to Mori. Trends Ecol Evol 31:89–92

    PubMed  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Google Scholar 

  • Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol Biochem 36:1907–1912

    CAS  Google Scholar 

  • Paulo D, Diekmann O, Alexandre A, Alberto F, Serrão A (2019) Sexual reproduction vs. clonal propagation in the recovery of a seagrass meadow after an extreme weather event. Sci Mar 83:357–363

    Google Scholar 

  • Procaccini G, Olsen J, Reusch TBH (2007) Contribution of genetics and genomics to seagrass biology and conservation. J Exp Mar Biol Ecol 350:234–259

    CAS  Google Scholar 

  • Ralph PJ, Durako MJ, Enriquez S, Collier CJ, Doblin MA (2007) Impact of light limitation on seagrasses. J Exp Mar Biol Ecol 350:176–193

    Google Scholar 

  • Reyes J, Sansón M, Afonso-Carrillo J (1995) Distribution and reproductive phenology of the seagrass Cymodocea nodosa (Ucria) Ascherson in the Canary Islands. Aquat Bot 50:171–180

    Google Scholar 

  • Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021

    PubMed  PubMed Central  Google Scholar 

  • Roca G, Alcoverro T, Krause-Jensen D, Balsby TJS, van Katwijk MM, Marbà N, Santos R, Arthur R, Mascaró O, Fernández-Torquemada Y, Perez M, Duarte CM, Romero J (2016) Response of seagrass indicators to shifts in environmental stressors: a global review and management synthesis. Ecol Indic 63:310–323

    Google Scholar 

  • Ruggiero MV, Reusch TBH, Procaccini G (2005) Local genetic structure in a clonal dioecious angiosperm. Mol Ecol 14:957–967

    CAS  PubMed  Google Scholar 

  • Ruiz JM, Marín-Guirao L, García-Muñoz R, Ramos-Segura A, Bernardeau-Esteller J, Pérez M, Sanmartí N, Ontoria Y, Romero J, Arthur R, Alcoverro T, Procaccini G (2018) Experimental evidence of warming-induced flowering in the Mediterranean seagrass Posidonia oceanica. Mar Poll Bull 134(49):54

    Google Scholar 

  • Salo T, Reusch TBH, Boström C (2015) Genotype-specific responses to light stress in eelgrass Zostera marina, a marine foundation plant. Mar Ecol Prog Ser 519:129–140

    CAS  Google Scholar 

  • Selwood KE, Thomson JR, Clarke RH, McGeoch MA, Mac Nally R (2015) Resistance and resilience of terrestrial birds in drying climates: do floodplains provide drought refugia? Global Ecol Biogeogr 24:838–848

    Google Scholar 

  • Terrados J (1993) Sexual reproduction and seed banks of Cymodocea nodosa (Ucria) Ascherson meadows on the southeast Mediterranean coast of Spain. Aquat Bot 46:293–299

    Google Scholar 

  • Terrados J, Duarte CM, Kenworthy WJ (1997) Is the apical growth of Cymodocea nodosa dependent on clonal integration? Mar Ecol Prog Ser 148:263–268

    Google Scholar 

  • Tuya F, Martín JA, Luque A (2006) Seasonal cycle of a Cymodocea nodosa (Ucria) Ascherson seagrass meadow and associated ichthyofauna in Playa Dorada (Lanzarote Canary Islands eastern Atlantic). J Cienc Mar 32:695–704

    Google Scholar 

  • Tuya F, Viera-Rodríguez MA, Guedes R, Espino F, Haroun R, Terrados J (2013a) Seagrass responses to nutrient enrichment depend on clonal integration, but not flow-on effects on associated biota. Mar Ecol Prog Ser 490:23–35

    CAS  Google Scholar 

  • Tuya F, Espino F, Terrados J (2013b) Preservation of seagrass clonal integration buffers against burial stress. J Exp Mar Biol Ecol 439:42–46

    Google Scholar 

  • Tuya F, Ribeiro-Leite L, Arto-Cuesta N, Coca J, Haroun R, Espino F (2014) Decadal changes in the structure of Cymodocea nodosa seagrass meadows: natural vs. human influences. Estuar Coast Shelf Sci 137:41–49

    CAS  Google Scholar 

  • Tuya F, Fernández-Torquemada Y, Zarcero J, del Pilar RY, Csenteri I, Espino F, Manent P, Curbelo L, Antich A, de la Ossa JA, Royo L, Castejón I, Procaccini G, Terrados J, Tomas F (2019) Biogeography modulates seagrass resistance to small-scale perturbations. J Ecol 107:1263–1275

    Google Scholar 

  • Waycott M, Duarte C, Carruthers TRO, Dennison W, Olyarnik S, Fourqurean J, Heck K, Hughes AR, Kendrick GA, Kenworthy W, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei T, Simko V (2017) R package “corrplot”: visualization of a Correlation Matrix (Version 0.84)

  • Wernberg T, Coleman MA, Bennett S, Thomsen MS, Tuya F, Kelaher BP (2018) Genetic diversity and kelp forest vulnerability to climatic stress. Sci Rep 8:1851

    PubMed  PubMed Central  Google Scholar 

  • York PH, Smith TM, Coles RG, McKenna SA, Connolly RM, Irving AD, Jackson EL, McMahon K, Runcie JW, Sherman CDH, Sullivan BK, Trevathan-Tackett SM, Brodersen KE, Carter AB, Ewers CJ, Lavery PS, Roelfsema CM, Sinclair EA, Strydom S, Tanner JE, van Dijk KJ, Warry FY, Waycott M, Whitehead S (2017) Identifying knowledge gaps in seagrass research and management: an Australian perspective. Mar Environ Res 127:163–172

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge Paula Bonet, Nestor Bosch, Luis M. Ferrero-Vicente, Andrea García, Tony Sánchez, and José L. Sánchez-Lizaso for their help during fieldwork.

Funding

This work was funded by a project (RESIGRASS, CGL2014-58829) supported by the Secretaría de Estado de Investigación, Desarrollo e Innovación (MINECO, Government of Spain).

Author information

Authors and Affiliations

  1. Grupo en Biodiversidad y Conservación, IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, 35017, Las Palmas, Canary Islands, Spain

    Fernando Tuya, Fernando Espino, Pablo Manent, Leticia Curbelo & Francisco Otero-Ferrer

  2. Departamento de Ciencias del Mar y Biología Aplicada, Universidad de Alicante, Alicante, Spain

    Yolanda Fernández-Torquemada, Yoana del Pilar-Ruso & Jose A. de la Ossa

  3. Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB), C/ Miquel Marquès, 21, 07190, Esporles, Islas Baleares, Spain

    Laura Royo, Laura Antich, Inés Castejón, Julia Máñez-Crespo, Ángel Mateo-Ramírez, Jorge Terrados & Fiona Tomas

  4. Universidad de Los Lagos, 5480000, Puerto Montt, Chile

    Julia Máñez-Crespo

  5. GEMAR Group, Centro Oceanográfico de Málaga, Instituto Español de Oceanografía (IEO), Puerto Pesquero s/n, Apdo. 285, 29640, Fuengirola, Málaga, Spain

    Ángel Mateo-Ramírez

  6. Stazione Zoologica Anton Dohrn, 80121, Napoli, Italy

    Gabriele Procaccini

  7. CEAB (CSIC), C/ d’accés a la Cala St. Francesc, 14, Blanes, Girona, Spain

    Candela Marco-Méndez

Authors
  1. Fernando Tuya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yolanda Fernández-Torquemada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoana del Pilar-Ruso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Espino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pablo Manent
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leticia Curbelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Francisco Otero-Ferrer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jose A. de la Ossa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Laura Royo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Laura Antich
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Inés Castejón
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Julia Máñez-Crespo
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ángel Mateo-Ramírez
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Gabriele Procaccini
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Candela Marco-Méndez
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jorge Terrados
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Fiona Tomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F Tuya, F Tomas, YFT and JT conceived the ideas and designed the experiments. F Tuya, YFT, YPR, FE, PM, LC, FOT, JADO, LR, LA, IC, JMC, AMR, GP, CM, JT and F Tomas performed the experiments. F Tuya analysed the data. F Tuya wrote the manuscript; other authors provided editorial advice.

Corresponding author

Correspondence to Fernando Tuya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Ethics approval was not required for this study according to local legislation.

Additional information

Communicated by James Fourqurean.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1398 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tuya, F., Fernández-Torquemada, Y., del Pilar-Ruso, Y. et al. Partitioning resilience of a marine foundation species into resistance and recovery trajectories. Oecologia 196, 515–527 (2021). https://doi.org/10.1007/s00442-021-04945-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-04945-4

Keywords

Search

Navigation