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A canonical metacommunity structure over 3 decades: ecologically consistent but spatially dynamic patterns in a hurricane-prone montane forest

  • Global change ecology – original research
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Abstract

The Anthropocene is a time of rapid change induced by human activities, including pulse and press disturbances that affect the species composition of local communities and connectivity among them, giving rise to spatiotemporal dynamics at multiple scales. We evaluate effects of global warming and repeated intense hurricanes on gastropod metacommunities in montane tropical rainforests of Puerto Rico for each of 28 consecutive years. Specifically, we quantified metacommunity structure each year; assessed effects of global warming, hurricane-induced disturbance, and secondary succession on interannual variation in metacommunity structure; and evaluated legacies of previous land use on metacommunity structure. Gastropods were sampled annually during a 28-year period characterized by disturbance and succession associated with 3 major hurricanes (Hurricanes Hugo, Georges, and Maria). For each year, we evaluated coherence (the extent to which the environmental distributions of species are uninterrupted along a common latent environmental gradient), species range turnover, and species range boundary clumping; and conducted co-occurrence analyses for each pair of species. We used generalized linear mixed-effects model to evaluate long-term responses of the metacommunity to aspects of global warming and disturbance. Metacommunity structure was remarkably stable, with consistent patterns of species co-occurrence. Disturbance, warming, and successional stage had little effect on metacommunity structure. Despite great temporal variation in environmental conditions, groups of species tracked their niche through space and time to maintain the same general structure. Consequently, metacommunity structure was highly resistant and resilient to multiple disturbances, even those that greatly altered forest structure.

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Data availability statement

Gastropod and temperature data are archived publicly and openly available in the Luquillo Long-Term Ecological Research data catalog: gastropod data (https://luq.lter.network/data/luqmetadata107 or https://portal.edirepository.org/nis/mapbrowse?packageid=knb-lter-luq.107.9996737), temperature data (https://luq.lter.network/data/luqmetadata16 or https://portal.edirepository.org/nis/mapbrowse?packageid=knb-lter-luq.16.538551).

References

  • Adams A (2001) Effects of a hurricane on two assemblages of coral reef fishes: multiple-year analysis reverses a false snapshot interpretation. Bull Mar Sci 69:341–356

    Google Scholar 

  • Amrhein V, Trafimow D, Greenland S (2019) Inferential statistics as descriptive statistics: there is no replication crisis if we don’t expect replication. Am Stat 73:262–270

    Article  Google Scholar 

  • Barbara A, Richardson Michael J, Richardson G, González Aaron B, Shiels Diane S, Srivastava (2010) A canopy trimming experiment in puerto rico: the response of litter invertebrate communities to canopy loss and debris deposition in a tropical forest subject to hurricanes. Ecosystems 13(2):286–301. https://doi.org/10.1007/s10021-010-9317-6

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B 57:289–300

    Google Scholar 

  • Bloch CP, Weiss L (2002) Distribution and abundance of the whipspider Phrynus longipes (Arachnida: Amblypygi) in the Luquillo Experimental Forest, Puerto Rico: Response to natural and anthropogenic disturbance. Caribb J Sci 38:260–262

    Google Scholar 

  • Bloch CP, Willig MR (2006) Context-dependence of long-term responses of terrestrial gastropod populations to large-scale disturbance. J Trop Ecol 22:111–122

    Article  Google Scholar 

  • Bloch CP, Higgins CL, Willig MR (2007) Effects of large-scale disturbance on metacommunity structure of terrestrial gastropods: temporal trends in nestedness. Oikos 116:395–406

    Article  Google Scholar 

  • Bonthoux S, Balent G (2015) Bird metacommunity processes remain constant after 25 years of landscape changes. Ecol Complex 21:39–43

    Article  Google Scholar 

  • Boose RR, Foster DR, Fluet M (1994) Hurricane impacts to tropical and temperate forest landscapes. Ecol Monogr 64:369–400

    Article  Google Scholar 

  • Brokaw N, Crowl TA, Lugo AE, McDowell WH, Scatena FN, Waide RB, Willig MR (eds) (2012) A Caribbean forest tapestry: the multidimensional nature of disturbance and response. Oxford University Press, New York

    Google Scholar 

  • Brown S, Lugo AE, Silander S, Liegel L (1983) Research history and opportunities in the Luquillo Experimental Forest. General Technical Report SO–44. U.S. Department of Agriculture, Forest Service, Southern Forest Experiment Station, New Orleans

  • Cisneros LM, Fagan ME, Willig MR (2015) Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats. J Anim Ecol 84:373–385

    Article  PubMed  Google Scholar 

  • Clements FE (1916) Plant succession: an analysis of the development of vegetation. Carnegie Institution of Washington, Washington, DC

    Book  Google Scholar 

  • Collins SL, Ladwig LM, Petrie MD, Jones SK, Mulhouse JM, Thibault JR, Pockman WT (2016) Press–pulse interactions: effects of warming, N deposition, altered winter precipitation, and fire on desert grassland community structure and dynamics. Glob Change Biol 23:1095–1108

    Article  Google Scholar 

  • Delciellos AC, Borges-Júnior VN, Prevedello JA, Ribeiro SE, Braga C, Vieira MV, Cerqueira R (2018) Seasonality in metacommunity structure: an empirical test in the Atlantic Forest. Landscape Ecol 33:1769–1783

    Article  Google Scholar 

  • Dewey M (2020) metap: meta-analysis of significance values. R package version 1.4

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139

    Article  CAS  PubMed  Google Scholar 

  • Ellison AM, Gotelli NJ, Inouye BD, Strong DR, Editors (2014) P values, hypothesis testing and model selection: it’s déjà vu all over again. Ecology 95:609‒653

  • Erős T, Sály P, Takács P, Higgins CL, Bíró P, Schmera D (2014) Quantifying temporal variability in the metacommunity structure of stream fishes: the influence of non-native species and environmental drivers. Hydrobiologia 722:31–43

    Article  Google Scholar 

  • Everham EM III, Brokaw NVL (1996) Forest damage and recovery from catastrophic wind. Bot Rev 62:113–185

    Article  Google Scholar 

  • Fernandes IM, Henriques-Silva R, Penha J, Zuanon J, Peres-Neto PR (2014) Spatiotemporal dynamics in a seasonal metacommunity structure is predictable: the case of floodplain-fish communities. Ecography 37:464–475

    Google Scholar 

  • Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage Publishers, Thousand Oaks

    Google Scholar 

  • Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53:7–26

    Article  Google Scholar 

  • Griffith DM, Veech JA, Marsh CJ (2016) cooccur: probabilistic species co-occurrence analysis in R. J Stat Softw 69:1–17

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363

    Article  Google Scholar 

  • Hurlbert SH (1990) Spatial distribution of the montane unicorn. Oikos 58:257–271

    Article  Google Scholar 

  • Jenkins DG (2006) In search of quorum effects in metacommunity structure: species co-occurrence analyses. Ecology 87:1523–1531

    Article  Google Scholar 

  • Jenkins DG, Buikema AL Jr (1998) Do similar communities develop in similar sites? A test with zooplankton structure and function. Ecol Monogr 68:421–443

    Article  Google Scholar 

  • Josefson AB, Loo L-O, Blomqvist M, Rolandsson J (2018) Substantial changes in the depth distributions of benthic invertebrates in the eastern Kattegat since the 1880s. Ecol Evol 8:9426–9438

    Article  PubMed  PubMed Central  Google Scholar 

  • Keith SA, Newton AC, Morecroft MD, Golicher DJ, Bullock JM (2011) Plant metacommunity structure remains unchanged during biodiversity loss in English woodlands. Oikos 120:300–310

    Article  Google Scholar 

  • Kueffer C (2015) Ecological novelty: towards an interdisciplinary understanding of ecological change in the Anthropocene. In: Greschke H, Tischler J (eds) Grounding global climate change. Springer, Dordrecht, pp 19–37

    Chapter  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • Leibold MA (2011) The metacommunity concept and its theoretical underpinnings. In: Scheiner SM, Willig MR (eds) The theory of ecology. University of Chicago Press, Chicago, pp 163–184

    Google Scholar 

  • Leibold MA, Chase JM (2018) Metacommunity ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: Elements of meta-community structure. Oikos 97:237–250

    Article  Google Scholar 

  • Leibold MA, Chase JM, Ernest SKM (2017) Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystem attributes. Ecology 98:909–919

    Article  PubMed  Google Scholar 

  • Lugo AE (2013) Novel tropical forests: nature’s response to global change. Trop Conserv Sci 6:325–337

    Article  Google Scholar 

  • Lugo AE, Carlo TA, Wunderle JM Jr (2012) Natural mixing of species: novel plant–animal communities on Caribbean Islands. Anim Conserv 15:233–241

    Article  Google Scholar 

  • McDowell WH, Estrada-Pinto A (1988) Rainfall at the El Verde Field Station, 1964–1986. Center for Energy and Environment Research Publication CEER T-228. University of Puerto Rico, San Juan, Puerto Rico

  • Mihaljevic JR, Joseph MB, Johnson PTJ (2015) Using multispecies occupancy models to improve the characterization and understanding of metacommunity structure. Ecology 96:1783–1792

    Article  PubMed  Google Scholar 

  • Monastersky R (2015) Anthropocene: the human age. Nature 519:144–147

    Article  CAS  PubMed  Google Scholar 

  • Newton AC, Walls RM, Golicher D, Keith SA, Diaz A, Bullock JM (2012) Structure, composition and dynamics of a calcareous grassland metacommunity over a 70-year interval. J Ecol 100:196–209

    Article  Google Scholar 

  • Nicolai A, Ansart A (2017) Conservation at a slow pace: terrestrial gastropods facing fast-changing climate. Conserv Physiol 5:cox007

    Article  PubMed  PubMed Central  Google Scholar 

  • Ochoa-Ochoa LM, Whittaker RJ (2014) Spatial and temporal variation in amphibian metacommunity structure in Chiapas, Mexico. J Trop Ecol 30:537–549

    Article  Google Scholar 

  • Ostertag R, Scatena FN, Silver WL (2003) Forest floor decomposition following hurricane litter inputs in several Puerto Rican forests. Ecosystems 6:261–273

    Article  CAS  Google Scholar 

  • Patterson BD, Atmar A (1986) Nested subsets and the structure of insular mammalian faunas and archipelagos. Biol J Linn Soc 28:65–82

    Article  Google Scholar 

  • Pedler RD, Brandle R, Reed JL, Southgate R, Bird P, Moseby KE (2016) Rabbit biocontrol and landscape-scale recovery of threatened desert mammals. Conserv Biol 30:774–782

    Article  PubMed  Google Scholar 

  • Peters DPC, Bestelmeyer BT, Turner MG (2007) Cross-scale interactions and changing pattern-process relationships: consequences for system dynamics. Ecosystems 10:790–796

    Article  Google Scholar 

  • Presley SJ (2020) On the detection of metacommunity structures. Community Ecol 21:103–106

    Article  Google Scholar 

  • Presley SJ, Willig MR (2010) Bat metacommunity structure on Caribbean islands and the role of endemics. Global Ecol Biogeogr 19:185–199

    Article  Google Scholar 

  • Presley SJ, Higgins CL, López-González C, Stevens RD (2009) Elements of metacommunity structure of Paraguayan bats: multiple gradients require analysis of multiple axes of variation. Oecologia 160:781–793

    Article  PubMed  Google Scholar 

  • Presley SJ, Higgins CL, Willig MR (2010) A comprehensive framework for the evaluation of metacommunity structure. Oikos 11:908–917

    Article  Google Scholar 

  • Presley SJ, Willig MR, Bloch CP, Castro-Arellano I, Higgins CL, Klingbeil BT (2011) A complex metacommunity structure for gastropods along an elevational gradient. Biotropica 43:480–488

    Article  Google Scholar 

  • Presley SJ, Mello JHF, Willig MR (2019) Checkerboard metacommunity structure: an incoherent concept. Oecologia 190:323–331

    Article  PubMed  Google Scholar 

  • Proença V, Martin LJ, Pereira HM, Fernandez M, McRae L, Belnap J, Böhm M, Brummitt N, García-Moreno J, Gregory RD, Pradinho Honrado J, Jürgens N, Opige M, Schmeller DS, Tiago P, van Swaay CAM (2017) Global biodiversity monitoring: from data sources to essential biodiversity variables. Biol Conserv 213:256–263

    Article  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 3 Mar 2020

  • Rice K, Brokaw N, Thompson J (2004) Liana abundance in a Puerto Rican forest. For Ecol Manag 190:33–41

    Article  Google Scholar 

  • Sasaki T, Furukawab T, Iwasaki Y, Seto M, Mori AS (2015) Perspectives for ecosystem management based on ecosystem resilience and ecological thresholds against multiple and stochastic disturbances. Ecol Indic 57:395–408

    Article  Google Scholar 

  • Scatena FN, Larsen MC (1991) Physical aspects of Hurricane Hugo in Puerto Rico. Biotropica 23:317–323

    Article  Google Scholar 

  • Schmera D, Podani J, Botta-Dukát Z, Erős T (2018) On the reliability of the elements of metacommunity structure framework for separating idealized metacommunity patterns. Ecol Indic 85:853–860

    Article  Google Scholar 

  • Schowalter T, Pandey M, Presley SJ, Willig MR, Zimmerman JK (2021) Arthropods are not declining but are responsive to disturbance in the Luquillo Experimental Forest, Puerto Rico. Proc Natl Acad Sci USA 118: e2002556117

  • Secrest MF, Willig MR, Peppers LL (1996) The legacy of disturbance on habitat associations of terrestrial snails in the Luquillo Experimental Forest, Puerto Rico. Biotropica 28:502–514

    Article  Google Scholar 

  • Thompson J, Brokaw N, Zimmerman JK, Waide RB, Everham EM III, Lodge DJ, Taylor CM, García-Montiel D, Fluet M (2002) Land use history, environment, and tree composition in a tropical forest. Ecol Appl 12:1344–1363

    Article  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton

    Google Scholar 

  • Ulrich W, Gotelli NJ (2012) Pattern detection in null model analysis. Oikos 122:2–18

    Article  Google Scholar 

  • Uriarte M, Thompson J, Zimmerman JK (2019) Hurricane Maria tripled stem breaks and double tree mortality relative to other major storms. Nat Commun 10:1362

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Veech JA (2013) A probabilistic model for analysing species co-occurrence. Global Ecol Biogeogr 22:252–260

    Article  Google Scholar 

  • Waide RB, Willig MR (2012) Conceptual overview: disturbance, gradients, and ecological response. In: Brokaw N, Crowl TA, Lugo AE, McDowell WH, Scatena FN, Waide RB, Willig MR (eds) A Caribbean forest tapestry: the multidimensional nature of disturbance and response. Oxford University Press, New York, pp 42–71

    Chapter  Google Scholar 

  • Walker LR (1991) Tree damage and recovery from Hurricane Hugo in the Luquillo Experimental Forest, Puerto Rico. Biotropica 23:379–385

    Article  Google Scholar 

  • Walker LR (ed) (1999) Ecosystems of disturbed ground. Elsevier Science, Amsterdam

    Google Scholar 

  • Whittaker RH (1975) Communities and ecosystems. The Macmillan Company, New York

    Google Scholar 

  • Willig MR, Walker LR (1999) Disturbance in terrestrial ecosystems: salient themes, synthesis, and future directions. In: Walker LR (ed) Ecosystems of disturbed ground. Elsevier Science, Amsterdam, pp 747–767

    Google Scholar 

  • Willig MR, Secrest MF, Cox SB, Camilo GR, Cary JF, Alvarez J, Gannon MR (1998) Long-term monitoring of snails in the Luquillo Experimental Forest of Puerto Rico: heterogeneity, scale, disturbance, and recovery. In: Dallmeier F, Comisky J (eds) Forest biodiversity in North, Central, and South America and the Caribbean: research and monitoring. Parthenon Press, Carnforth, pp 293–322

    Google Scholar 

  • Willig MR, Bloch CP, Brokaw N, Higgins CL, Thompson J, Zimmermann CR (2007) Cross-scale responses of biodiversity to hurricane and anthropogenic disturbance in a tropical forest. Ecosystems 10:824–838

    Article  Google Scholar 

  • Willig MR, Presley SJ, Bloch CP (2011) Long-term dynamics of tropical walking sticks in response to multiple large-scale and intense disturbances. Oecologia 165:357–368

    Article  PubMed  Google Scholar 

  • Willig MR, Bloch CP, Covich AP, Hall CAS, Lodge DJ, Lugo AE, Silver WL, Waide RB, Walker LR, Zimmerman JK (2012) Long-term research in the Luquillo Mountains: synthesis and foundations for the future. In: Brokaw N, Crowl TA, Lugo AE, McDowell WH, Scatena FN, Waide RB, Willig MR (eds) A Caribbean forest tapestry: the multidimensional nature of disturbance and response. Oxford University Press, New York, pp 361–441

    Chapter  Google Scholar 

  • Willig MR, Bloch CP, Presley SJ (2014) Experimental decoupling of canopy opening and debris addition on tropical gastropod populations and communities. For Ecol Manag 332:103–117

    Article  Google Scholar 

  • Willig MR, Woolbright L, Presley SJ, Schowalter TD, Waide RB, Heartsill Scalley T, Zimmerman JK, González G, Lugo AE (2019) Populations are not declining and food webs are not collapsing in the Luquillo Experimental Forest. Proc Natl Acad Sci USA 116:12143–12144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young KR (2014) Biogeography of the Anthropocene: novel species assemblages. Prog Phys Geogr 38:664–673

    Article  Google Scholar 

  • Zaykin DV (2011) Optimally weighted Z-test is a powerful method for combining probabilities in meta-analysis. J Evol Biol 24:1836–1841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was facilitated by Grants DEB-0218039, DEB-0620910, DEB-1239764, DEB-1546686, and DEB-1831952 from the National Science Foundation to the Institute of Tropical Ecosystem Studies, University of Puerto Rico, and the International Institute of Tropical Forestry as part of the Long-Term Ecological Research Program. Additional support was provided by the United States Forest Service and the University of Puerto Rico. Integration and synthesis were supported by an OPUS Grant from NSF (DEB-1950643) to MRW. A stipend to EIC was provided by a Research Experience for Undergraduate supplement to DEB-1546686. Support was also provided by the Center for Environmental Sciences and Engineering and Institute of the Environment at the University of Connecticut.

Funding

This work was supported by National Science Foundation (DEB-0218039, DEB-0620910, DEB-1239764, DEB-1546686, DEB-1831952, and DEB-1950643). Partial financial support was received from the United States Forest Service, the University of Puerto Rico, and from the Center for Environmental Sciences and Engineering and Institute of the Environment at the University of Connecticut.

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MRW conceived and managed all aspects of the project. MRW and SJP designed the analytical phases of the work, and SJP and EIC executed quantitative analyses. MRW, SJP, and EIC wrote the manuscript.

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Correspondence to Steven J. Presley.

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The authors have no relevant financial or non-financial interests to disclose.

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Communicated by Andreas Prinzing.

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Willig, M.R., Presley, S.J. & Cullerton, E.I. A canonical metacommunity structure over 3 decades: ecologically consistent but spatially dynamic patterns in a hurricane-prone montane forest. Oecologia 196, 919–933 (2021). https://doi.org/10.1007/s00442-021-04968-x

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