Abstract
In semi-arid environments, the marked contrast in temperature and precipitation over the year strongly shapes ecological communities. The composition of species and their ecological interactions within a community may vary greatly over time. Although intra-annual variations are often studied, empirical information on how plant–bird relationships are structured within and among years, and how their drivers may change over time are still limited. In this study, we analyzed the temporal dynamics of the structure of plant–hummingbird interaction networks by evaluating changes in species richness, diversity of interactions, modularity, network specialization, nestedness, and β-diversity of interactions throughout four years in a Mexican xeric shrubland landscape. We also evaluated if the relative importance of abundance, phenology, morphology, and nectar sugar content consistently explains the frequency of pairwise interactions between plants and hummingbirds across different years. We found that species richness, diversity of interactions, nestedness, and network specialization did vary within and among years. We also observed that the β-diversity of interactions was high among years and was mostly associated with species turnover (i.e., changes in species composition), with a minor contribution of interaction rewiring (i.e., shifting partner species at different times). Finally, the temporal co-occurrence of hummingbird and plant species among months was the best predictor of the frequency of pairwise interactions, and this pattern was consistent within and among years. Our study underscores the importance of considering the temporal scale to understand how changes in species phenologies, and the resulting temporal co-occurrences influence the structure of interaction networks.
Similar content being viewed by others
Data availability statement
All response and predictor variables presented in the Supporting Information. Plant–hummingbird interactions are available at: https://doi.org/10.6084/m9.figshare.10050035.
References
Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117:1796–1807. https://doi.org/10.1111/j.0030-1299.2008.16987.x
Araujo AC, Martín González AM, Sandel B, Maruyama PK, Fischer E, Vizentin-Bugoni J, Las-Casas FMG et al (2018) Spatial distance and climate determine modularity in a cross-biomes plant–hummingbird interaction network in Brazil. J Biogeogr 45:1846–1858. https://doi.org/10.1111/jbi.13367
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. PNAS USA 100:9383–9387. https://doi.org/10.1073/pnas.1633576100
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. https://doi.org/10.1126/science.1123412
Blake JG, Hanowski JM, Niemi GJ, Collins PT (1994) Annual variation in bird populations of mixed conifer-northern hardwood forests. Condor 96:381–399. https://doi.org/10.2307/1369322
Berns CM, Adams DC (2010) Bill shape and sexual shape dimorphism between two species of temperate hummingbirds: Black-Chinned hummingbird (Archilochus alexandri) and Ruby-Throated hummingbird (A. colubris). Auk 127:626–635. https://doi.org/10.1525/auk.2010.09213
Burkle L, Irwin R (2009) The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks. Oikos 118:1816–1829. https://doi.org/10.1111/j.1600-0706.2009.17740.x
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. https://doi.org/10.1126/science.1232728
Canard E, Mouquet N, Marescot L, Gaston KJ, Gravel D, Mouillot D (2012) Emergence of structural patterns in neutral trophic networks. PLoS ONE 7:e38295. https://doi.org/10.1371/journal.pone.0038295
Canard EF, Mouquet N, Mouillot D, Stanko M, Miklisova D, Gravel D (2014) Empirical evaluation of neutral interactions in host-parasite networks. Am Nat 183:468–479
CaraDonna PJ, Petry WK, Brennan RM, Cunningham JL, Bronstein JL, Waser NM, Sanders NJ (2017) Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol Lett 20:385–394. https://doi.org/10.1111/ele.12740
Chacoff NP, Resasco J, Vázquez DP (2018) Interaction frequency, network position, and the temporal persistence of interactions in a plant–pollinator network. Ecology 99:21–28. https://doi.org/10.1002/ecy.2063
Chacoff NP, Vázquez DP, Lomáscolo SB, Stevani EL, Dorado J, Padrón B (2012) Evaluating sampling completeness in a desert plant–pollinator network. J Anim Ecol 81:190–200. https://doi.org/10.1111/j.1365-2656.2011.01883.x
Correa-Lima APA, Varassin IG, Barve N, Zwiener VP (2019) Spatio-temporal effects of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants. Ann Bot 124:389–398. https://doi.org/10.1093/aob/mcz079
Dalsgaard B, Magård E, Fjeldså J, González AMM, Rahbek C, Olesen JM, Lara C et al (2011) Specialization in plant–hummingbird networks is associated with species richness, contemporary precipitation and quaternary climate-change velocity. PLoS ONE 6:e25891. https://doi.org/10.1371/journal.pone.0025891
Dáttilo W, Marquitti FM, Guimarães PR Jr, Izzo TJ (2014) The structure of ant–plant ecological networks: Is abundance enough? Ecology 95:475–485. https://doi.org/10.1890/12-1647.1
Dáttilo W, Rico-Gray V (2018) Ecological networks in the tropics. Springer, New York
Dáttilo W, Vasconcelos HL (2019) Macroecological patterns and correlates of ant–tree interaction networks in Neotropical savannas. Glob Ecol Biog 28:1283–1294. https://doi.org/10.1111/geb.12932
Díaz-Valenzuela R (2008) Análisis descriptivo del sistema colibrí-planta en tres escalas de las escalas espacial, temporal y en la jerarquía ecológica en un paisaje mexicano. Master thesis, Centro Iberoamericano de la Biodiversidad, Alicante, España
Dormann CF, Fründ J, Schaefer HM (2017) Identifying causes of patterns in ecological networks: opportunities and limitations. Annu Rev Ecol Evol Syst 48:559–584. https://doi.org/10.1146/annurev-ecolsys-110316-022928
Dupont YL, Olesen JM (2012) Stability of modular structure in temporal cumulative plant-flower-visitor networks. Ecol Complex 11:84–90. https://doi.org/10.1016/j.ecocom.2012.03.004
Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269. https://doi.org/10.1111/j.1600-0706.2009.17594.x
Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15:198–208. https://doi.org/10.1111/j.1461-0248.2011.01726.x
Falcão JC, Dáttilo W, Rico-Gray V (2016) Sampling effort differences can lead to biased conclusions on the architecture of ant–plant interaction networks. Ecol Complex 25:44–52. https://doi.org/10.1016/j.ecocom.2016.01.001
Fontaine C, Guimarães PR Jr, Kéfi S, Loeuille N, Memmott J, van Der Putten WH, Thébault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181. https://doi.org/10.1111/j.1461-0248.2011.01688.x
Fründ J, McCann KS, Williams NM (2016) Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model. Oikos 125:502–513. https://doi.org/10.1111/oik.02256
Galetto L, Bernardello G (2005) Rewards in flower/Nectar. In: Dafni P, Kevan G, Husband BC (eds) Practical pollination biology. England, Cambridge, pp 261–313
Gonzalez O, Loiselle BA (2016) Species interactions in an Andean bird–flowering plant network: phenology is more important than abundance or morphology. PeerJ 4:e2789. https://doi.org/10.7717/peerj.2789
Gotelli NJ, McGill BJ (2006) Null versus neutral models: what's the difference? Ecography 29:793–800. https://doi.org/10.1111/j.2006.0906-7590.04714.x
Graham CH, Weinstein BG (2018) Towards a predictive model of species interaction beta diversity. Ecol Lett 21:1299–1310. https://doi.org/10.1111/ele.13084
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
INEGI (2016) Anuario estadístico y geográfico de Hidalgo 2016. Instituto Nacional de Estadística, Geografía e Informática, Aguascalientes, Mexico
INEGI (2017) Guía para la interpretación de cartografía: uso de suelo y vegetación: escala 1:250,000: serie VI. Instituto Nacional de Estadística, Geografía e Informática, Aguascalientes, Mexico
Jordano P (2016) Sampling networks of ecological interactions. Funct Ecol 30:1883–1893. https://doi.org/10.1111/1365-2435.12763
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. https://doi.org/10.1101/gr.092759.109
Lange D (2013) Influence of extrafloral nectary phenology on ant–plant mutualistic networks in a neotropical savanna. Ecol Entomol 38:463–469. https://doi.org/10.1111/een.12036
Lara C (2006) Temporal dynamics of flower use by hummingbirds in a highland temperate forest in Mexico. Ecoscience 13:23–29. https://doi.org/10.2980/1195-6860(2006)13[23:TDOFUB]2.0.CO;2
Lara-Rodríguez NZ, Díaz-Valenzuela R, Martínez-García V, Mauricio-López E, Díaz SA, Valle OI, Fisher AD, Lara C, Ortiz-Pulido R (2012) Redes de interacción planta-colibrí del centro-este de México. Rev Mex Biodivers 83:569–577
Lindenmayer DB, Likens GE, Andersen A, Bowman D, Bull CM, Burns E, Lowe AJ (2012) Value of long-term ecological studies. Austr Ecol 37:745–775. https://doi.org/10.1111/j.1442-9993.2011.02351.x
Luna P, Peñaloza-Arellanes Y, Castillo-Meza AL, García-Chávez JH, Dáttilo W (2018) Beta diversity of ant-plant interactions over day-night periods and plant physiognomies in a semiarid environment. J Arid Environ 156:69–76. https://doi.org/10.1016/j.jaridenv.2018.04.00
Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M (2014) Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics. Ecology 95:3325–3334. https://doi.org/10.1890/13-2261.1
Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M (2015) Functional structure and specialization in three tropical plant–hummingbird interaction networks across an elevational gradient in Costa Rica. Ecography 38:1119–1128. https://doi.org/10.1111/ecog.01538
Maron M, Lill A, Watson DM, Nally RM (2005) Temporal variation in bird assemblages: How representative is a one-year snapshot? Aust Ecol 30:383–439. https://doi.org/10.1111/j.1442-9993.2005.01480.x
Martín González AM, Dalsgaard B, Nogués-Bravo D, Graham CH, Schleuning M, Maruyama PK, de Azevedo Jr SM et al (2015) The macroecology of phylogenetically structured hummingbird–plant networks. Global Ecol Biogeogr 24:1212–1224. https://doi.org/10.1111/geb.12355
Martínez GAL (2008) Disponibilidad floral de plantas ornitofílicas en cuatro tipos de vegetación del centro-sur de Hidalgo, México. Bachelor thesis, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Hidalgo, Mexico
Martínez-García V, Ortiz-Pulido R (2014) Redes mutualistas colibrí-planta: comparación en dos escalas espaciales. Ornitol Neotrop 25:273–289
Maruyama PK, Oliveira GM, Ferreira C, Dalsgaard B, Oliveira PE (2013) Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds. Naturwissenschaften 100:1061–1068. https://doi.org/10.1007/s00114-013-1111-9
Maruyama PK, Sonne J, Vizentin-Bugoni J, Martín-González AM, Zanata TB, Abrahamczyk S, Chávez-González E et al (2018) Functional diversity mediates macroecological variation in plant–hummingbird interaction networks. Global Ecol Biogeogr 27:1186–1199. https://doi.org/10.1111/geb.1277
Maruyama PK, Vizentin-Bugoni J, Oliveira GM, Oliveira PE, Dalsgaard B (2014) Morphological and spatio-temporal mismatches shape a neotropical savanna plant–hummingbird network. Biotropica 46:740–747. https://doi.org/10.1111/btp.12170
Mauricio-López E (2005) Interacción colibrí-planta: variación espacial en un matorral xerófilo de Hidalgo, México. Bachelor thesis, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo. Hidalgo, Mexico
Meserve PL, Kelt DA, Milstead WB, Gutiérrez JR (2003) Thirteen years of shifting top-down and bottom-up control. Bioscience 53:633–646. https://doi.org/10.1641/0006-3568(2003)053[0633:TYOSTA]2.0.CO;2
Morente-López J, Lara-Romero C, Ornosa C, Iriondo JM (2018) Phenology drives species interactions and modularity in a plant-flower visitor network. Sci Rep 8:9386. https://doi.org/10.1038/s41598-018-27725-2
Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. https://doi.org/10.1890/07-0451.1
Olesen JM, Bascompte J, Dupont YL, Elberling H, Rasmussen C, Jordano P (2011a) Missing and forbidden links in mutualistic networks. Proc R Soc B 278:725–732. https://doi.org/10.1098/rspb.2010.1371
Olesen JM, Stefanescu C, Traveset A (2011b) Strong, long-term temporal dynamics of an ecological network. PLoS ONE 6:e2455. https://doi.org/10.1371/journal.pone.0026455
Olito C, Fox JW (2015) Species traits and abundances predict metrics of plant–pollinator network structure, but not pairwise interactions. Oikos 124:428–436. https://doi.org/10.1111/oik.01439
Ortiz-Pulido R, Rico-Gray V (2000) The effect of spatio-temporal variation in understanding the fruit crop size hypothesis. Oikos 93:523–528. https://doi.org/10.1034/j.1600-0706.2000.910314.x
Ortiz-Pulido R, Vargas-Licona G (2008) Explorando la relación entre registros de colibríes y abundancia de flores con escalamiento espacio-temporal. Ornitol Neotrop 19:473–483
Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11:564–575. https://doi.org/10.1111/j.1461-0248.2008.01170.x
Poisot T, Canard E, Mouillot D, Mouquet N, Gravel D (2012) The dissimilarity of species interaction networks. Ecol Lett 15:1353–1361. https://doi.org/10.1111/ele.12002
Poisot T, Stouffer DB, Gravel D (2015) Beyond species: why ecological interaction networks vary through space and time. Oikos 124:243–251. https://doi.org/10.1111/oik.01719
Ponisio LC, Gaiarsa MP, Kremen C (2017) Opportunistic attachment assembles plant–pollinator networks. Ecol Lett 20:1261–1272. https://doi.org/10.1111/ele.12821
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed 3 Aug 2018
Ralph CJ, Droege S, Sauer JR (1995) Managing and monitoring birds using point counts: standards and applications. In: Ralph CJ, Sauer JR, Droege S (eds) Monitoring bird populations by point counts. USDA Forest Service, Pacific Southwest Research Station, General Technical Report PSW-GTR, pp 161–168
Ralph JC, Geupel GR, Pyle P, Martin TE, DeSante DF, Milá B (1996) Manual de métodos de campo para el monitoreo de aves terrestres. Gen Tech Rep PSW-GTR159 Albany, CA: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture
Ramos-Robles M, Andresen E, Díaz-Castelazo C (2016) Temporal changes in the structure of a plant-frugivore network are influenced by bird migration and fruit availability. PeerJ 4:e2048. https://doi.org/10.7717/peerj.2048
Rzedowski J (2006) Vegetación de México. 1ra. Edición digital, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Stiles FG (1985) Seasonal patterns and coevolution in the hummingbird-flower community of a Costa Rican subtropical forest. Ornithol Monogr 36:757–787
Sonne J, Martín González AM, Maruyama PK, Sandel B, Vizentin-Bugoni J, Schleuning M et al (2016) High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas. Proc Royal Soc B 283:20152512
Sonne J, Vizentin-Bugoni J, Maruyama PK, Araujo AC, Chávez-González E, Coelho AG et al (2020) Ecological mechanisms explaining interactions within plant–hummingbird networks: morphological matching increases towards lower latitudes. Proc R Royal Soc B 287:20192873
Tanaka LK, Tanaka SK (1982) Rainfall and seasonal changes in arthropod abundance on a tropical oceanic island. Biotropica 14:114–123. https://doi.org/10.2307/2387740
Thompson JN (2006) Mutualistic webs of species. Science 312:372–373. https://doi.org/10.1126/science.1126904
Trøjelsgaard K, Jordano P, Carstensen DW, Olesen JM (2015) Geographical variation in mutualistic networks: similarity, turnover and partner fidelity. Proc R Soc B 282:20142925. https://doi.org/10.1098/rspb.2014.2925
Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst 48:25–48. https://doi.org/10.1146/annurev-ecolsys-110316-022821
Vázquez DP, Aizen MA (2003) Null model analyses of specialization in plant–pollinator interactions. Ecology 84:2493–2501. https://doi.org/10.1890/02-0587
Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009a) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457. https://doi.org/10.1093/aob/mcp057
Vázquez DP, Chacoff NP, Cagnolo L (2009b) Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90:2039–2046. https://doi.org/10.1890/08-1837.1
Vázquez DP, Melián CJ, Williams NM, Blüthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127. https://doi.org/10.1111/j.0030-1299.2007.15828.x
Verdú M, Valiente-Banuet A (2011) The relative contribution of abundance and phylogeny to the structure of plant facilitation networks. Oikos 120:1351–1356. https://doi.org/10.1111/j.1600-0706.2011.19477.x
Verner J, Ritter LV (1988) A comparison of transects and spot mapping in oak-pine woodlands of California. Condor 90:401–419. https://doi.org/10.2307/1368569
Vizentin-Bugoni J, Maruyama PK, Debastiani VJ, Duarte LDS, Dalsgaard B, Sazima M (2016) Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant–hummingbird network. J Animal Ecol 85:262–272. https://doi.org/10.1111/1365-2656.12459
Vizentin-Bugoni J, Maruyama PK, Sazima M (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird–plant network. Proc R Soc B 281:20132397. https://doi.org/10.1098/rspb.2013.2397
Vizentin-Bugoni J, Maruyama PK, Souza CS, Ollerton J, Rech R, Sazima M (2018) Plant-pollinator networks in the tropics: a review. In: Dáttilo W, Rico-Gray V (eds) Ecological networks in the tropics: an integrative overview of species interactions from some of the most species-rich habitats on earth. Springer, New York, pp 73–91
Weinstein BG, Graham CH (2017a) On comparing traits and abundance for predicting species interactions with imperfect detection. Food Webs 11:17–25. https://doi.org/10.1016/j.fooweb.2017.05.002
Weinstein BG, Graham CH (2017b) Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbird-plant interactions. Ecol Lett 20:326–335. https://doi.org/10.1111/ele.12730
Acknowledgements
We thank Román Díaz-Valenzuela, Vanesa Martínez-García, Ubaldo Márquez-Luna, and Erika Guzmán-Arias for their valuable assistance during the fieldwork and Juan Francisco Ornelas, Carlos Lara, and Jose G. García-Franco for their valuable comments and suggestions to the early versions of this paper. Financial support was provided by CONACYT (Consejo Nacional de Ciencia y Tecnología) through the project 258364 and an MSc scholarship to ECG (609146). We also thank Museo de Zoología de la Facultad de Ciencias, UNAM and Herbarium XAL, Instituto de Ecología A.C. for facilitating the use of hummingbirds and plants specimens, respectively. DPV was supported by an FONCYT grant (PICT-2014-3168).
Author information
Authors and Affiliations
Contributions
ECG, WD, and ROP conceived the study, ECG and ROP collected the data, ECG and WD analysed the data, JVB, DV, and IMF advertised on the analyses. ECG, JVB, WD, and ROP led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Statement of human and animal rights
“This article does not contain any studies with human participants or animals performed by any of the authors.”
Additional information
Communicated by David M Watson.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chávez-González, E., Vizentin-Bugoni, J., Vázquez, D.P. et al. Drivers of the structure of plant–hummingbird interaction networks at multiple temporal scales. Oecologia 193, 913–924 (2020). https://doi.org/10.1007/s00442-020-04727-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04727-4