Availability of food resources and habitat structure shape the individual-resource network of a Neotropical marsupial

. 2019 Apr ; 9 (7) : 3946-3957. [epub] 20190321

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31015979

Spatial and temporal variation in networks has been reported in different studies. However, the many effects of habitat structure and food resource availability variation on network structures have remained poorly investigated, especially in individual-based networks. This approach can shed light on individual specialization of resource use and how habitat variations shape trophic interactions.To test hypotheses related to habitat variability on trophic interactions, we investigated seasonal and spatial variation in network structure of four populations of the marsupial Gracilinanus agilis in the highly seasonal tropical savannas of the Brazilian Cerrado.We evaluated such variation with network nestedness and modularity considering both cool-dry and warm-wet seasons, and related such variations with food resource availability and habitat structure (considered in the present study as environmental variation) in four sites of savanna woodland forest.Network analyses showed that modularity (but not nestedness) was consistently lower during the cool-dry season in all G. agilis populations. Our results indicated that nestedness is related to habitat structure, showing that this metric increases in sites with thick and spaced trees. On the other hand, modularity was positively related to diversity of arthropods and abundance of fruits.We propose that the relationship between nestedness and habitat structure is an outcome of individual variation in the vertical space and food resource use by G. agilis in sites with thick and spaced trees. Moreover, individual specialization in resource-rich and population-dense periods possibly increased the network modularity of G. agilis. Therefore, our study reveals that environment variability considering spatial and temporal components is important for shaping network structure of populations.

Zobrazit více v PubMed

Ab'Sáber, A. (1977). Os domínios morfoclimáticos na América do Sul: Primeira aproximação. Geomorfologia, 52, 3946–21.

Aléssio, F. , Pontes, A. , & Silva, V. (2005). Feeding by Didelphis albiventrison tree gum in the northeastern Atlantic forest of Brazil. Mastozoología Neotropical, 12, 53–56.

Almeida‐Neto, M. , Guimarães, P. R. Jr , & Lewinsohn, T. M. (2007). On nestedness analyses: Rethinking matrix temperature and anti‐nestedness. Oikos, 116, 716–722. 10.1111/j.0030-1299.2007.15803.x DOI

Anthony, E. L. , & Kunz, T. H. (1977). Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology, 58, 775–786. 10.2307/1936213 DOI

Araújo, M. S. , Guimarães, P. R. , Svanbäck, R. , Pinheiro, A. , Guimarães, P. , Reis, S. F. D. , & Bolnick, D. I. (2008). Network analysis reveals contrasting effects of intraspecific competition on individual vs. population diets. Ecology, 89, 1981–1993. 10.1890/07-0630.1 PubMed DOI

Araújo, M. S. , Martins, E. G. , Cruz, L. D. , Fernandes, F. R. , Linhares, A. X. , Dos Reis, S. F. , & Guimarães, P. R. (2010). Nested diets: A novel pattern of individual‐level resource use. Oikos, 119, 81–88. 10.1111/j.1600-0706.2009.17624.x DOI

Bascompte, J. , & Jordano, P. (2007). Plant–animal mutualistic networks: The architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38, 567–593. 10.1146/annurev.ecolsys.38.091206.095818 DOI

Bollobás, B. (1998). Random graphs In Bollobás B. (Ed.), Modern graph theory (pp. 215–252). New York, NY: Springer.

Bolnick, D. I. , Ingram, T. , Stutz, W. E. , Snowberg, L. K. , Lau, O. L. , & Paull, J. S. (2010). Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proceedings of the Royal Society of London B: Biological Sciences, 277, 1789–1797. PubMed PMC

Bolnick, D. I. , Svanbäck, R. , Fordyce, J. A. , Yang, L. H. , Davis, J. M. , Hulsey, C. D. , & Forister, M. L. (2002). The ecology of individuals: Incidence and implications of individual specialization. The American Naturalist, 161, 3946–28. PubMed

Bolnick, D. I. , Yang, L. H. , Fordyce, J. A. , Davis, J. M. , & Svanbäck, R. (2002). Measuring individual‐level resource specialization. Ecology, 83, 2936–2941.

Camargo, A. C. L. , Barrio, R. O. L. , Camargo, N. F. , Mendonça, A. F. , Ribeiro, J. F. , Rodrigues, C. M. F. , & Vieira, E. M. (2018). Fire affects the occurrence of small mammals at distinct spatial scales in a neotropical savanna. European Journal of Wildlife Research, 64, 63 10.1007/s10344-018-1224-8 DOI

Camargo, N. F. , Ribeiro, J. F. , Camargo, A. J. , & Vieira, E. M. (2014a). Diet of the gracile mouse opossum Gracilinanus agilis(Didelphimorphia: Didelphidae) in a neotropical savanna: Intraspecific variation and resource selection. Acta Theriologica, 59, 183–191.

Camargo, N. F. , Ribeiro, J. F. , Camargo, A. J. , & Vieira, E. M. (2014b). Intra‐and inter‐individual variation show distinct trends as drivers of seasonal changes in the resource use of a neotropical marsupial. Biological Journal of the Linnean Society, 111, 737–747.

Cantor, M. , Pires, M. M. , Longo, G. O. , Guimarães, P. R. , & Setz, E. Z. F. (2013). Individual variation in resource use by opossums leading to nested fruit consumption. Oikos, 122, 1085–1093. 10.1111/j.1600-0706.2012.00070.x DOI

Cooper‐Ellis, S. , Foster, D. R. , Carlton, G. , & Lezberg, A. (1999). Forest response to catastrophic wind: Results from an experimental hurricane. Ecology, 80, 2683–2696. 10.1890/0012-9658(1999)080[2683:FRTCWR]2.0.CO;2 DOI

Csardi, G. , & Nepusz, T. (2006). The igraph software package for complex network research. InterJournal Complex Systems, 1695, 3946–9.

Dalsgaard, B. o. , Schleuning, M. , Maruyama, P. K. , Dehling, D. M. , Sonne, J. , Vizentin‐Bugoni, J. , … Rahbek, C. (2017). Opposed latitudinal patterns of network‐derived and dietary specialization in avian plant–frugivore interaction systems. Ecography, 40, 3946–7. 10.1111/ecog.02604 DOI

Devoto, M. , Medan, D. , & Montaldo, N. H. (2005). Patterns of interaction between plants and pollinators along an environmental gradient. Oikos, 109, 461–472. 10.1111/j.0030-1299.2005.13712.x DOI

Dormann, C. F. , Gruber, B. , & Fründ, J. (2008). Introducing the bipartite package: Analysing ecological networks. R News, 8, 8–11.

Dormann, C. F. , & Strauss, R. (2014). A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution, 5, 90–98. 10.1111/2041-210X.12139 DOI

Eiten, G. (1972). The cerrado vegetation of Brazil. The Botanical Review, 38, 201–341. 10.1007/BF02859158 DOI

Emmons, L. H. , & Feer, F. (1997). Neotropical rainforest mammals: A field guide. Chicago, IL: The University of Chicago Press.

Erdõs, P. , & Rényi, A. (1959). On random graphs, I. Publicationes Mathematicae (Debrecen), 6, 290–297.

Erwin, L. T. (1995). Measuring arthropod biodiversity in the Tropical forest canopy In Lowman M. D., & Nadkarni N. M. (Eds.), Forest canopies (pp. 109–127). San Diego, CA: Academic Press.

Felfili, J. M. (1995). Diversity, structure and dynamics of a gallery forest in central Brazil. Vegetatio, 117, 3946–15. 10.1007/BF00033255 DOI

Fortuna, M. A. , Stouffer, D. B. , Olesen, J. M. , Jordano, P. , Mouillot, D. , Krasnov, B. R. , … Bascompte, J. (2010). Nestedness versus modularity in ecological networks: Two sides of the same coin? Journal of Animal Ecology, 79, 811–817. PubMed

Freitas, S. , Cerqueira, R. , & Vieira, M. (2002). A device and standard variables to describe microhabitat structure of small mammals based on plant cover. Brazilian Journal of Biology, 62, 795–800. 10.1590/S1519-69842002000500008 PubMed DOI

Gilman, S. E. , Urban, M. C. , Tewksbury, J. , Gilchrist, G. W. , & Holt, R. D. (2010). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25, 325–331. 10.1016/j.tree.2010.03.002 PubMed DOI

Gouveia, G. P. , & Felfili, J. M. (1998). Fenologia de comunidades de cerrado e de mata de galeria no Brasil Central. Revista Árvore, 22, 443–450.

Guimerà, R. , Sales‐Pardo, M. , & Amaral, L. A. N. (2007). Module identification in bipartite and directed networks. Physical Review E, 76, 036102 10.1103/PhysRevE.76.036102 PubMed DOI PMC

Hammer, Ø. , Harper, D. , & Ryan, P. (2001). Paleontological statistics software: Package for education and data analysis. Palaeontologia Electronica, 4, 3946–9.

Hannibal, W. , & Caceres, N. C. (2010). Use of vertical space by small mammals in gallery forest and woodland savannah in south‐western Brazil. Mammalia, 74, 247–255. 10.1515/mamm.2010.007 DOI

Hitimana, J. , Kiyiapi, J. L. , & Njunge, J. T. (2004). Forest structure characteristics in disturbed and undisturbed sites of Mt. Elgon Moist Lower Montane Forest, western Kenya. Forest Ecology and Management, 194, 269–291. 10.1016/j.foreco.2004.02.025 DOI

Jordano, P. , Bascompte, J. , & Olesen, J. M. (2003). Invariant properties in coevolutionary networks of plant–animal interactions. Ecology Letters, 6, 69–81. 10.1046/j.1461-0248.2003.00403.x DOI

Jost, L. (2006). Entropy and diversity. Oikos, 113, 363–375.

Lemmon, P. E. (1956). A spherical densiometer for estimating forest overstory density. Forest Science, 2, 314–320.

Lemos‐Costa, P. , Pires, M. M. , Araújo, M. S. , Aguiar, M. A. , & Guimarães, P. R. (2016). Network analyses support the role of prey preferences in shaping resource use patterns within five animal populations. Oikos, 125, 492–501. 10.1111/oik.03006 DOI

Lessa, L. G. , & da Costa, F. N. (2010). Diet and seed dispersal by five marsupials (Didelphimorphia: Didelphidae) in a Brazilian cerrado reserve. Mammalian Biology, 1, 10–16. 10.1016/j.mambio.2008.11.002 DOI

Lewinsohn, T. M. , Prado, P. I. , Jordano, P. , Bascompte, J. , & Olesen, J. M. (2006). Structure in plant–animal interaction assemblages. Oikos, 113, 174–184. 10.1111/j.0030-1299.2006.14583.x DOI

López‐Carretero, A. , Díaz‐Castelazo, C. , Boege, K. , & Rico‐Gray, V. (2014). Evaluating the spatio‐temporal factors that structure network parameters of plant‐herbivore interactions. PLoS ONE, 9, e110430 10.1371/journal.pone.0110430 PubMed DOI PMC

Macfadyen, S. , Gibson, R. H. , Symondson, W. O. , & Memmott, J. (2011). Landscape structure influences modularity patterns in farm food webs: Consequences for pest control. Ecological Applications, 21, 516–524. 10.1890/09-2111.1 PubMed DOI PMC

Mallet‐Rodrigues, F. (2001). Foraging and diet composition of the Black‐capped Foliage‐gleaner (Philydor atricapillus). Ornitologia Neotropical, 12, 255–264.

Martins, E. G. , Bonato, V. , Da‐Silva, C. Q. , & Dos Reis, S. F. (2006). Seasonality in reproduction, age structure and density of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in a Brazilian cerrado. Journal of Tropical Ecology, 22, 461.

Martins, R. L. , & Gribel, R. (2007). Polinização de Caryocar villosum (Aubl.) Pers. (Caryocaraceae) uma árvore emergente da Amazônia Central. Revista Brasileira De Botanica, 30, 37–45. 10.1590/S0100-84042007000100005 DOI

May, R. M. (1972). Will a large complex system be stable? Nature, 238, 413–414. PubMed

McCann, K. S. (2000). The diversity‐stability debate. Nature, 405, 228 10.1038/35012234 PubMed DOI

Mendonça, A. F. , Armond, T. , Camargo, A. C. L. , Camargo, N. F. , Ribeiro, J. F. , Zangrandi, P. L. , & Vieira, E. M. (2015). Effects of an extensive fire on arboreal small mammal populations in a neotropical savanna woodland. Journal of Mammalogy, 96, 368–379. 10.1093/jmammal/gyv038 DOI

Miranda, A. , Miranda, H. , & Dias, I. (1993). Soil and air temperatures during provocated cerrado fires in central Brazil. Journal of Tropical Ecology, 9, 313–320.

Neutel, A. M. , Heesterbeek, J. A. , & de Ruiter, P. C. (2002). Stability in real food webs: Weak links in long loops. Science, 296, 1120–1123. 10.1126/science.1068326 PubMed DOI

Newman, M. E. , & Girvan, M. (2004). Finding and evaluating community structure in networks. Physical Review E, 69, 026113 10.1103/PhysRevE.69.026113 PubMed DOI

Nitikman, L. , & Mares, M. (1987). Ecology of small mammals in a gallery forest of central Brazil. Annals of Carnegie Museum, 56, 75–95.

Nuwagaba, S. (2015). The architecture of antagonistic networks: Node degree distribution, compartmentalization and nestedness. Computational Ecology and Software, 5, 317.

Olesen, J. M. , Bascompte, J. , Dupont, Y. L. , & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104, 19891–19896. 10.1073/pnas.0706375104 PubMed DOI PMC

Olesen, J. M. , & Jordano, P. (2002). Geographic patterns in plant–pollinator mutualistic networks. Ecology, 83, 2416–2424.

Pimm, S. L. , & Lawton, J. H. (1980). Are food webs divided into compartments? The Journal of Animal Ecology, 49, 879–898.

Pinheiro, F. , Diniz, I. , Coelho, D. , & Bandeira, M. (2002). Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology, 27, 132–136. 10.1046/j.1442-9993.2002.01165.x DOI

Pires, M. , Guimarães, P. , Araújo, M. , Giaretta, A. , Costa, J. , & Dos Reis, S. (2011). The nested assembly of individual‐resource networks. Journal of Animal Ecology, 80, 896–903. 10.1111/j.1365-2656.2011.01818.x PubMed DOI

Pires, M. M. , Martins, E. G. , Araujo, M. S. , & Reis, S. F. (2013). Between‐individual variation drives the seasonal dynamics in the trophic niche of a Neotropical marsupial. Austral Ecology, 38, 664–671. 10.1111/aec.12011 DOI

Pocock, M. J. , Evans, D. M. , & Memmott, J. (2012). The robustness and restoration of a network of ecological networks. Science, 335, 973–977. 10.1126/science.1214915 PubMed DOI

R Development Core Team (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rezende, E. L. , Albert, E. M. , Fortuna, M. A. , & Bascompte, J. (2009). Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecology Letters, 12, 779–788. 10.1111/j.1461-0248.2009.01327.x PubMed DOI

Rezende, E. L. , Lavabre, J. E. , Guimarães, P. R. , Jordano, P. , & Bascompte, J. (2007). Non‐random coextinctions in phylogenetically structured mutualistic networks. Nature, 448, 925–928. 10.1038/nature05956 PubMed DOI

Ribeiro, J. (2011). Avaliação do uso do espaço pelo marsupial Gracilinanus agilis em área de cerradao no Brasil Central. Brasília, Brazil: Universidade de Brasília.

Ribeiro, J. , & Walter, B. (1998). Fitofisionomias do Cerrado In Sano S., & Almeida S. (Eds.), Cerrado: Ambiente e flora (pp. 87–166). Planaltina, Brazil: EMBRAPA‐CPAC.

Robinson, K. M. , Hauzy, C. , Loeuille, N. , & Albrectsen, B. R. (2015). Relative impacts of environmental variation and evolutionary history on the nestedness and modularity of tree–herbivore networks. Ecology and Evolution, 5, 2898–2915. 10.1002/ece3.1559 PubMed DOI PMC

Rodríguez‐Gironés, M. A. , & Santamaría, L. (2006). A new algorithm to calculate the nestedness temperature of presence–absence matrices. Journal of Biogeography, 33, 924–935. 10.1111/j.1365-2699.2006.01444.x DOI

Schwieder, M. , Leitão, P. J. , da Cunha Bustamante, M. M. , Ferreira, L. G. , Rabe, A. , & Hostert, P. (2016). Mapping Brazilian savanna vegetation gradients with Landsat time series. International Journal of Applied Earth Observation and Geoinformation, 52, 361–370. 10.1016/j.jag.2016.06.019 DOI

Silva, N. A. P. , Frizzas, M. R. , & Oliveira, C. M. (2011). Seasonality in insect abundance in the “Cerrado” of Goiás State, Brazil. Revista Brasileira De Entomologia, 55, 79–87. 10.1590/S0085-56262011000100013 DOI

Svanbäck, R. , & Bolnick, D. I. (2005). Intraspecific competition affects the strength of individual specialization: An optimal diet theory method. Evolutionary Ecology Research, 7, 993–1012.

Svanbäck, R. , & Bolnick, D. I. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society of London B: Biological Sciences, 274, 839–844. PubMed PMC

Takemoto, K. , Kanamaru, S. , & Feng, W. (2014). Climatic seasonality may affect ecological network structure: Food webs and mutualistic networks. BioSystems, 121, 29–37. 10.1016/j.biosystems.2014.06.002 PubMed DOI

Thébault, E. , & Fontaine, C. (2010). Stability of ecological communities and the architecture of mutualistic and trophic networks. Science, 329, 853–856. 10.1126/science.1188321 PubMed DOI

Thompson, A. R. , Adam, T. C. , Hultgren, K. M. , & Thacker, C. E. (2013). Ecology and evolution affect network structure in an intimate marine mutualism. The American Naturalist, 182, E58–E72. 10.1086/670803 PubMed DOI

Trøjelsgaard, K. , & Olesen, J. M. (2013). Macroecology of pollination networks. Global Ecology and Biogeography, 22, 149–162. 10.1111/j.1466-8238.2012.00777.x DOI

Trøjelsgaard, K. , & Olesen, J. M. (2016). Ecological networks in motion: Micro‐and macroscopic variability across scales. Functional Ecology, 30, 1926–1935.

Tur, C. , Vigalondo, B. , Trøjelsgaard, K. , Olesen, J. M. , & Traveset, A. (2014). Downscaling pollen–transport networks to the level of individuals. Journal of Animal Ecology, 83, 306–317. 10.1111/1365-2656.12130 PubMed DOI

Tylianakis, J. M. , Laliberté, E. , Nielsen, A. , & Bascompte, J. (2010). Conservation of species interaction networks. Biological Conservation, 143, 2270–2279. 10.1016/j.biocon.2009.12.004 DOI

Valiente‐Banuet, A. , Aizen, M. A. , Alcántara, J. M. , Arroyo, J. , Cocucci, A. , Galetti, M. , … Zamora, R. (2015). Beyond species loss: The extinction of ecological interactions in a changing world. Functional Ecology, 29, 299–307. 10.1111/1365-2435.12356 DOI

van Veen, F. , Müller, C. , Pell, J. , & Godfray, H. (2008). Food web structure of three guilds of natural enemies: Predators, parasitoids and pathogens of aphids. Journal of Animal Ecology, 77, 191–200. 10.1111/j.1365-2656.2007.01325.x PubMed DOI

Vázquez, D. P. , Chacoff, N. P. , & Cagnolo, L. (2009). Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology, 90, 2039–2046. 10.1890/08-1837.1 PubMed DOI

Vieira, M. V. (2003). Seasonal niche dynamics in coexisting rodents of the Brazilian Cerrado. Studies on Neotropical Fauna and Environment, 38, 7–15. 10.1076/snfe.38.1.7.14034 DOI

Wade, M. J. (2007). The co‐evolutionary genetics of ecological communities. Nature Reviews Genetics, 8, 185–195. 10.1038/nrg2031 PubMed DOI

Wirta, H. K. , Weingartner, E. , Hambäck, P. A. , & Roslin, T. (2015). Extensive niche overlap among the dominant arthropod predators of the High Arctic. Basic and Applied Ecology, 16, 86–92. 10.1016/j.baae.2014.11.003 DOI

Zar, J. H. (1999). Biostatistical analysis, 4th ed. Upper Saddle River, NJ: Prentice Hall.

Zobrazit více v PubMed

Dryad
10.5061/dryad.c73p54m

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...