Abstract
Context
The metacommunity concept helps to understand how local and regional processes regulate species distributions in landscapes. Metacommunity structure is often assumed as static, but may be rather dynamic, following temporal changes along environmental gradients.
Objectives
We present an empirical test of the temporal dynamics of metacommunity structure, using small mammals in an Atlantic Forest landscape as a model system.
Methods
We analyzed incidence matrices using the Elements of Metacommunity Structure framework and evaluated whether local, landscape, and spatial factors structured the metacommunity during different climatic seasons (HS = humid; SHS = super-humid) and time periods (1 = 1999–2001; 2 = 2005–2009). We compared HS-1 and SHS-1 to evaluate if metacommunity structure varies between seasons, and HS-1 and HS-2 to evaluate if it varies between time periods.
Results
Metacommunity structure changed from Clementsian (HS-1) to random (SHS-1), but during HS-2 it was Clementsian again. This suggests that groups of species are responding similarly to the major gradient of variation during the HS only. Patch size structured the metacommunity during both humid periods, and local habitat structure only during HS-1. We suggest that during the SHS these gradients are lost due to increased matrix permeability to movement, which homogenizes local communities resulting in a random structure.
Conclusions
Species habitat requirements and specializations determined metacommunity structure, but only during the HS. The Clementsian structure indicates that forest disturbances may result in the loss of whole groups of species during the HS. Alternating patterns of metacommunity structure may be associated to changes on matrix suitability between seasons.
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Data accessibility
Data are presented in ESM 1–2.
References
Altermatt F, Pajunen VI, Ebert D (2009) Desiccation of rock pool habitats and its influence on population persistence in a Daphnia metacommunity. PLoS ONE 4(3):e4703
Bloch CP, Higgins CL, Willig MR (2007) Effects of large scale disturbance on metacommunity structure of terrestrial gastropods: temporal trends in nestedness. Oikos 116(3):395–406
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer Science & Business Media, New York
Brady MJ, McAlpine CA, Possingham HP, Miller CJ, Baxter GS (2011) Matrix is important for mammals in landscapes with small amounts of native forest habitat. Landscape Ecol 26(5):617–628
Braga CAC, Prevedello JA, Pires MRS (2015) Effects of cornfields on small mammal communities: a test in the Atlantic Forest hotspot. J Mamm 96(5):938–945
Briani DC, Vieira EM, Vieira MV (2001) Nests and nesting sites of Brazilian forest rodents (Nectomys squamipes and Oryzomys intermedius) as revealed by a spool-and-line device. Acta Theriol 46(3):331–334
Castello ACD, Coelho S, Cardoso-Leite E (2017) Lianas, tree ferns and understory species: indicators of conservation status in the Brazilian Atlantic Rainforest remnants, southeastern Brazil. Braz J Biol 77(2):213–226
Catzeflis F, Patton J, Percequillo A, Weksler M (2016) Euryzygomatomys spinosus. The IUCN Red List of Threatened Species 2016: e.T8418A22205855. http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T8418A22205855.en
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(2):373–385
Clements FE (1916) Plant Succession: an analysis of community functions, vol 242. Carnigie Institution Washington Publications, Washington DC
Coleman BD, Mares MA, Willig MR, Hsieh YH (1982) Randomness, area, and species richness. Ecology 63:1121–1133
Crouzeilles R, Prevedello JA, Figueiredo MSL, Lorini ML, Grelle CEV (2014) The effects of the number, size and isolation of patches along a gradient of native vegetation cover: how can we increment habitat availability? Landscape Ecol 29:479–489
Datry T, Bonada N, Heino J (2016) Towards understanding the organization of metacommunities in highly dynamic ecological systems. Oikos 125(2):149–159
Davis ED (1945) The annual cycle of plants, mosquitoes, birds, and mammals in two Brazilian forests. Ecol Monogr 15(3):243–295
de la Sancha NU, Higgins CL, Presley SJ, Strauss RE (2014) Metacommunity structure in a highly fragmented forest: has deforestation in the Atlantic Forest altered historic biogeographic patterns? Divers Dist 20(9):1058–1070
Delciellos AC, Vieira MV (2006) Arboreal walking performance in seven didelphid marsupials as an aspect of their fundamental niche. Austral Ecol 31(4):449–457
Delciellos AC, Vieira MV, Grelle CEV, Cobra P, Cerqueira R (2016) Habitat quality versus spatial variables as determinants of small mammal assemblages in Atlantic Forest fragments. J Mamm 97(1):253–265
Develey PF, Peres CA (2000) Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic forest of southeastern Brazil. J Trop Ecol 16(01):33–53
Diamond JM (1975) Assembly of species communities. Ecol Evol Communities 342:444
Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196(3):483–493
Driscoll DA, Banks SC, Barton PS, Lindenmayer DB, Smith AL (2013) Conceptual domain of the matrix in fragmented landscapes. Trends Ecol Evol 28:605–613
Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65(1):169–175
ESRI (2008) ARCGIS, V-late tool. Environmental System Research Institute Inc, Redlands
Ewers RM, Didham RK (2007) The effect of fragment shape and species sensitivity to habitat edges on animal population size. Conserv Biol 21:926–936
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(5):464–475
Ferreira MS, Vieira MV, Cerqueira R, Dickman CR (2016) Seasonal dynamics with compensatory effects regulate populations of tropical forest marsupials: a 16-year study. Oecologia 182(4):1095–1106
Finotti R, Kurtz BC, Cerqueira R, Garay IG (2012) Variação na estrutura diamétrica, composição florística e características sucessionais de fragmentos florestais da bacia do rio Guapiaçu (Guapimirim/Cachoeiras de Macacu, RJ, Brasil). Acta Bot Bras 26:464–475
Freitas SR, Mello MC, Cruz CB (2005) Relationships between forest structure and vegetation indices in Atlantic Rainforest. For Ecol Manage 218(1):353–362
Gentile R, Finotti R, Rademaker V, Cerqueira R (2004) Population dynamics of four marsupials and its relation to resource production in the Atlantic Forest in southeastern Brazil. Mammalia 68(2):5–15
Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25(6):325–331
Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53(1):7–26
Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution, Washington, DC
Haynes KJ, Cronin JT (2006) Interpatch movement and edge effects: the role of behavioral responses to the landscape matrix. Oikos 113(1):43–54
Hylander K, Nilsson C, Jonsson BG, Göthner T (2005) Differences in habitat quality explain nestedness in a land snail meta community. Oikos 108(2):351–361
IBGE (2012) Manual Técnico da Vegetação Brasileira. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro
Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: elements of metacommunity structure. Oikos 97(2):237–250
Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7(7):601–613
Machado ELM, Oliveira-Filho ATD (2010) Spatial patterns of tree community dynamics are detectable in a small (4 ha) and disturbed fragment of the Brazilian Atlantic forest. Acta Bot Bras 24(1):250–261
Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB (2000) Phenology of Atlantic rain forest trees: a comparative study 1. Biotropica 32(4):811–823
Naxara L, Pinotti BT, Pardini R (2009) Seasonal microhabitat selection by terrestrial rodents in an old-growth Atlantic Forest. J Mamm 90(2):404–415
Nimer E (1989) Climatologia no Brasil, 2nd edn. Fundação IBGE, Rio de Janeiro
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Wagner H (2017) Package ‘vegan’—community ecology package: ordination, diversity and dissimilarities. v.2.4-2. L. http://cran.r-project.org/, http://r-forge.r-project.org/projects/vegan/
Oliveira-Filho AT, Carvalho DA, Vilela EA, Curi N, Fontes MAL (2004) Diversity and structure of the tree community of a fragment of tropical secondary forest of the Brazilian Atlantic Forest domain 15 and 40 years after logging. Rev Bras Bot 27(4):685–701
Patterson BD, Atmar W (1986) Nested subsets and the structure of insular mammalian faunas and archipelagos. Biol J Linn Soc 28:65–82
Pires AS, Lira PK, Fernandez FAS, Schittini GM, Oliveira LC (2002) Frequency of movements of small mammals among Atlantic Coastal Forest fragments in Brazil. Biodivers Conserv 108(2):229–237
Presley SJ, Higgins CL, López-González C, Stevens RD (2009) Elements of metacommunity structure of Paraguayan bats: multiple gradients require analysis of multiple ordination axes. Oecologia 160(4):781–793
Presley SJ, Higgins CL, Willig MR (2010) A comprehensive framework for the evaluation of metacommunity structure. Oikos 119(6):908–917
Prevedello JA, Vieira MV (2010) Does the type of matrix matter? A quantitative review of the evidence. Biodivers Conserv 19(5):1205–1223
Püttker T, Pardini R, Meyer-Lucht Y, Sommer S (2008) Responses of five small mammal species to micro-scale variations in vegetation structure in secondary Atlantic Forest remnants, Brazil. BMC Ecol 8(1):9
Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235(4785):167–171
Ruhí A, Dtary T, Sabo JL (2017) Interpreting beta-diversity components over time to conserve metacommunities in highly dynamic ecosystems. Conserv Biol 31(6):1459–1468
Sarremejane R, Cañedo-Argüelles M, Prat N, Mykrä H, Muotka T, Bonada N (2017) Do metacommunities vary through time? Intermittent rivers as model systems. J Biogeogr 44(12):2752–2763
Sikes RS, ACAUC of the AS of Mammalogists (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mamm 97:663–688
Silva JMC, Uhl C, Murray G (1996) Plant succession, landscape management, and the ecology of frugivorous birds in abandoned Amazonian pastures. Conserv Biol 10(2):491–503
SOS Mata Atlântica, INPE (2005) Atlas dos remanescentes florestais da Mata Atlântica. Fundação SOS Mata Atlântica and Instituto Nacional de Pesquisas Espaciais, São Paulo
Summerville KS, Crist TO (2004) Contrasting effects of habitat quantity and quality on moth communities in fragmented landscapes. Ecography 27(1):3–12
Tilman D (1982) Resource competition and community structure. Princeton University Press, New Jersey
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes-eight hypotheses. BiolRev 87(3):661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x
Uezu A, Metzger JP (2011) Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers Conserv 20(14):3627–3643
Umetsu F, Metzger JP, Pardini R (2008) Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic forest small mammals. Ecography 31(3):359–370
Uzêda MC, Fidalgo ECC, Iguatemy MA, Alves RC, Rouws JRC (2011) Explorando as relações entre estrutura da paisagem e atributos de qualidade de fragmentos em região de Mata Atlântica no Estado do Rio de Janeiro. Bol Pesqui Desenvolv 136:1–31
Vandermeer J, Carvajal R (2001) Metapopulation dynamics and the quality of the matrix. Am Nat 158(3):211–220
Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85(2):183–206
Vieira MV, Olifiers N, Delciellos AC, Antunes VZ, Bernardo LR, Grelle CEV, Cerqueira R (2009) Land use vs. fragment size and isolation as determinants of small mammal composition and richness in Atlantic Forest remnants. Biol Conserv 142:1191–1200
Wojciechowski J, Heino J, Bini LM, Padial AA (2017) Temporal variation in phytoplankton beta diversity patterns and metacommunity structure across subtropical reservoirs. Freshwater Biol 62:751–766
Acknowledgements
We thank the students and staff of the Laboratório de Vertebrados (Universidade Federal do Rio de Janeiro), particularly Angela Marcondes, Maycon Belarmino, Natalie Olifiers, and Nélio Barros. We also thank Carlos Grelle for comments on previous statistical analyses, and Renato Crouzeilles for providing the measures of forest fragments isolation and habitat amount. Two anonymous reviewers provided valuable suggestions to the manuscript. Landowners of the study sites at the Macacu River basin that allowed access to their lands for scientific research. Financial support was provided by grants from Projetos Demonstrativos/Ministério do Meio Ambiente, Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; to JAP, MVV, and RC), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; to JAP, MVV, and RC), PPBIO/CNPq/Rede Bio.Ma, PROBIO I/MMA/GEF, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). ACD has a postdoctoral scholarship from CAPES/FAPERJ (PAPD- E-26/202.144/2015); VNTBJ from CNPq/PDJ (157750-9) and CNPq/CAPES/PELD (88887.137536/2017-00); and CB from CNPq/CAPES/FAPs/PELD (88887.140649/2017-00). SER has a doctoral fellowship from CAPES/PROEX (1343229). Permissions to handle animals were given by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis/Ministério do Meio Ambiente (Authorization numbers 87/05-RJ, 099/06-RJ, 13861-1, 13861-2, and 16703).
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Delciellos, A.C., Borges-Júnior, V.N.T., Prevedello, J.A. et al. Seasonality in metacommunity structure: an empirical test in the Atlantic Forest. Landscape Ecol 33, 1769–1783 (2018). https://doi.org/10.1007/s10980-018-0701-5
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DOI: https://doi.org/10.1007/s10980-018-0701-5