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Incorporating rainy season and reproductive phenology into the survival and transition rates of the invasive species Sambucus nigra: an approximation with multistate models

Published online by Cambridge University Press:  23 December 2021

Leticia Bonilla-Valencia Open the ORCID record for Leticia Bonilla-Valencia [Opens in a new window] ,
Mariana Hernández-Apolinar Open the ORCID record for Mariana Hernández-Apolinar [Opens in a new window] ,
J. Jaime Zúñiga-Vega Open the ORCID record for J. Jaime Zúñiga-Vega [Opens in a new window] ,
Francisco J. Espinosa-García Open the ORCID record for Francisco J. Espinosa-García [Opens in a new window] ,
Yuriana Martínez-Orea Open the ORCID record for Yuriana Martínez-Orea [Opens in a new window]  and
Silvia Castillo-Argüero Open the ORCID record for Silvia Castillo-Argüero [Opens in a new window]
Leticia Bonilla-Valencia
Affiliation:
PhD Student, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad DE México, Mexico
Mariana Hernández-Apolinar
Affiliation:
Professor, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad DE México, Mexico
J. Jaime Zúñiga-Vega
Affiliation:
Professor, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad DE México, Mexico
Francisco J. Espinosa-García
Affiliation:
Professor, Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Yuriana Martínez-Orea
Affiliation:
Professor, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad DE México, Mexico
Silvia Castillo-Argüero*
Affiliation:
Professor, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad DE México, Mexico
*
Author for correspondence: Silvia Castillo-Argüero, Departamento DE Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, C.P. 04510, Ciudad DE México, México. (Email: silcas@ciencias.unam.mx)
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Abstract

Although it has been demonstrated that environmental changes within a year can affect the reproduction, survival, and growth of invasive species, these factors have rarely been incorporated into demographic analyses. Therefore, we applied multistate demographic models (based on capture–recapture animal methods accounting for imperfect detectability of individuals in natural conditions) to evaluate the effects of reproductive phenology and rainy season on the survival and transition/retrogression rates among stage categories of black elderberry (Sambucus nigra L.)—an invasive tree species widely distributed in temperate forests of Europe and America. In the Abies religiosa temperate forest, Mexico City, a multistate demographic model of S. nigra was built using bimonthly censuses during a year. We selected the best-fitting model according to Akaike’s information criterion adjusted for small sample sizes (AICc). We determined the response of reproductive phenology of S. nigra to the rainy season for 2 yr through repeatability and phenotypic plasticity indexes. Our results showed that the reproductive phenology of S. nigra has a low repeatability index and a high phenotypic plasticity index. We demonstrated that additive and interactive effects of reproductive phenology and rainy season promote changes in survival and transition/retrogression rates among stage categories. During the rainy season, the survival probability of seedlings and transition probability toward the adult category increased. Therefore, our study represents a significant contribution to the knowledge of the demographic dynamics of invasive species on an intra-annual scale.

Keywords

Phenotypic plasticityreproductive phenologysurvival ratetemperate foresttransition rate
Type
Research Article
Information
Invasive Plant Science and Management , Volume 15 , Issue 1 , March 2022 , pp. 16 - 24
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Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Weed Science Society of America

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Footnotes

Associate Editor: Songlin Fei, Purdue University

References

Adams, SN, Jennings, S, Warnock, N (2020) Plant invasion depresses native species richness, but control of invasive species does little to restore it. Plant Ecol Divers 13:257–266 CrossRefGoogle Scholar
Alexander, HM, Slade, NA, Kettle, WD, Pittman, GL, Reed, AW (2009) Detection, survival rates and dynamics of a cryptic plant, Asclepias meadii: applications of mark-recapture models to long-term monitoring studies. J Ecol 97:267–276 CrossRefGoogle Scholar
Ali, A (2019) Forest stand structure and functioning: current knowledge and future challenges. Ecol Indic 98:665–677 CrossRefGoogle Scholar
Allaie, RR, Reshi, Z, Wafai, BA (2005) Demographic plasticity in relation to growth and resource allocation pattern in Anthemis cotula—an alien invasive species in Kashmir Himalaya. India Appl Ecol Environ Res 4:63–74 CrossRefGoogle Scholar
Arreguín-Sánchez, ML (2001) Sambucus nigra L. Page 738 in Calderón de Rzedowski G, Rzedowski, J, eds. Flora Fanerogámica del Valle de México. 2nd ed. Michoacán, Mexico: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad Google Scholar
Atkinson, MD, Atkinson, E (2002) Sambucus nigra L. J. Ecol. 90:895–923 CrossRefGoogle Scholar
Atlan, A, Hornoy, B, Delerue, F, Gonzalez, M, Pierre, JS, Tarayre, M (2015) Phenotypic plasticity in reproductive traits of the perennial shrub Ulex europaeus in response to shading: a multi-year monitoring of cultivated clones. PLoS ONE 10(9):e0137500 CrossRefGoogle ScholarPubMed
Averill, KM, DiTommaso, A, Mohler, CL, Milbrath, LR (2011) Survival, growth, and fecundity of the invasive swallowworts (Vincetoxicum rossicum and V. nigrum) in New York State. Invasive Plant Sci Manag 4:198–206 CrossRefGoogle Scholar
Baker, HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24 CrossRefGoogle Scholar
Bonilla-Valencia, L, Castillo-Argüero, S, Martínez-Orea, Y (2017a) Reproductive phenology of Sambucus nigra subsp. canadensis in the Abies religiosa temperate forest of the Magdalena river basin, Mexico City. Bot Sci 95:23–35 CrossRefGoogle Scholar
Bonilla-Valencia, L, Espinosa-García, FJ, González, EJ, Lindig-Cisneros, R, Martínez-Orea, Y, Vega-Peña, EV, Castillo-Argüero, S (2020) Functional indicators to explain the anthropic effects on community plant composition changes: the case of a temperate forest in Mexico. Ecol Indic 116:106515 CrossRefGoogle Scholar
Bonilla-Valencia, L, Martínez-OreaY, Castillo-Argüero Barajas-Guzmán, S Romero-Romero, G Díaz-López, MA ET (2017b) Reproductive phenology of understory species in an Abies religiosa (Pinaceae) forest in the Magdalena River Basin, Mexico City. J Torrey Bot Soc 144:313–327 CrossRefGoogle Scholar
Brownie, C, Hines, JE, Nichols, JD, Pollock, KH, Hestbeck, JB (1993) Capture-recapture studies for multiple strata including non-Markovian transitions. Biometrics 49:1173–1187 CrossRefGoogle Scholar
Burnham, KP, Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information–Theoretic Approach. 2nd ed. New York: Springer–Verlag. 488 p Google Scholar
Caswell, H. 2000. Matrix Population Models. Vol. 1. Sunderland, MA: Sinauer. 722 p Google Scholar
[CABI] Centre for Agriculture and Bioscience International (2020) Invasive Species Compendium. http://www.cabi.org. Accessed: December 16, 2020Google Scholar
Challenger, A (2003) Conceptos Generales de los ecosistemas de montaña en México. Pages 14–44 in Sánchez Ó, Vega, E, Peters, E, y Monroy-Vilchis, O, eds. Conservación de ecosistemas templados de montaña en México. Ciudad de México, Mexico: Instituto Nacional de Ecología, INE, SEMARNATGoogle Scholar
Christy, MT, Yackel Adams, AA, Rodda, GH, Savidge, JA, Tyrrell, CL (2010) Modelling detection probabilities to evaluate management and control tools for an invasive species. J Appl Ecol 47:106–113 CrossRefGoogle Scholar
Colautti, RI, Ågren J, Anderson, JT (2017) Phenological shifts of native and invasive species under climate change: insights from the Boechera–Lythrum model. Philos Trans R Soc Lond B Biol Sci 372:20160032 CrossRefGoogle Scholar
Cornelissen, P, Gresnigt, M, Vermeulen, RA, Bokdam, J, Smit, R (2014) Transition of a Sambucus nigra L. dominated woody vegetation into grassland by a multi-species herbivore assemblage. J Nat Conserv 22:84–92 CrossRefGoogle Scholar
Debussche, M, Isenmann, P (1994) Bird-dispersed seed rain and seedling establishment in patchy Mediterranean vegetation. Oikos 69:414–426 CrossRefGoogle Scholar
DeWalt, SJ (2006) Population dynamics and potential for biological control of an exotic invasive shrub in Hawaiian rainforests. Biol Invasions 8:1145–1158 CrossRefGoogle Scholar
Dobler-Morales, E (2010) Caracterización del clima y su relación con la distribución de la vegetación en el suroeste del D.F., México. Ciudad de México, Mexico: Tesis de Licenciatura, Facultad de Ciencias, Universidad Nacional Autónoma de México. 50 p Google Scholar
Drenovsky, RE, Grewell, BJ, D’Antonio, CM, Funk, JL, James, JJ, Molinari, N, Parker, IM, Richards, C (2012) A functional trait perspective on plant invasion. Ann Bot 110:141–153 CrossRefGoogle ScholarPubMed
El-Barougy, RF, Cadotte, MW, Khedr, AHA, Nada, RM, Maclvor, JS (2017) Heterogeneity in patterns of survival of the invasive species Ipomoea carnea in urban habitats along the Egyptian Nile Delta. NeoBiota 33:1–17 CrossRefGoogle Scholar
Fernandez, RD, Ceballos, SJ, Aragón, R, Malizia, A, Montti, L, Whitworth-Hulse, JI, Grau, HR (2020) A global review of Ligustrum lucidum (OLEACEAE) invasion. Bot Rev 86:1–26 CrossRefGoogle ScholarPubMed
Franco, M, Silvertown, J (2004) A comparative demography of plants based upon elasticities of vital rates. Ecology 85:531–538 CrossRefGoogle Scholar
García, de Miranda E (1973) Modificaciones al sistema de clasificación climática de Köppen. 2nd ed. Ciudad de México, Mexico: Universidad Nacional Autónoma de México. 246 p Google Scholar
Goodall, J, Braack, M (2019) Screening herbicides for the control of the wetland invader, Sambucus nigra L., in South Africa. Afr J Aquat Sci 44:295–299 CrossRefGoogle Scholar
Hernández-Santin, C, Cuautle, M, de las, N Barranco-León García-Guzmán Jl, M, Badano, E, Luna-Castellanos, F (2019) Eucalyptus edge effect on Quercus-herbivore interactions in a neotropical temperate forest. Neotrop Entomol 48:764–771 CrossRefGoogle Scholar
Hidayati, SN, Baskin, JM, Baskin, CC (2000) Morphophysiological dormancy in seeds of two North American and one Eurasian species of Sambucus (Caprifoliaceae) with underdeveloped spatulate embryos. Am J Bot 87:1669–1678 CrossRefGoogle ScholarPubMed
Hidayati, SN, Walck, JL, Taylor, J (2010) Seed germination ecophysiology of two western North American species of Sambucus (Caprifoliaceae sensu lato), and comparisons with eastern North American and European congeners. Plant Species Biol 25:203–213 CrossRefGoogle Scholar
Jelbert, K, Buss, D, McDonald, Townley Franco, S Scott, M Jones, I Salguero-Gómez, O Buckley, R Knight, Y Silk, T Sargent, M Rolph, F Wilson, S Hodgson, P D (2019) Demographic amplification is a predictor of invasiveness among plants. Nat Commun 10:1–6 CrossRefGoogle ScholarPubMed
Jelbert, K, Stott, I, McDonald, RA, Hodgson, D (2015) Invasiveness of plants is predicted by size and fecundity in the native range. Ecol Evol 5:1933–1943 CrossRefGoogle ScholarPubMed
Jongejans, E, Shea, K, Skarpaas, O, Kelly, D, Ellner, SP (2011) Importance of individual and environmental variation for invasive species spread: a spatial integral projection model. Ecology 92:86–97 CrossRefGoogle ScholarPubMed
Kabuce, N, Priede, N (2006) Invasive alien species fact sheet: Sambucus nigra . Database of the European Network on Invasive Alien Species (NOBANIS). http://www.nobanis.org/files/factsheets/Sambucus%20nigra.pdf. Accessed: December 19, 2014Google Scholar
Kéry, M, Gregg, KB (2003) Effects of life—state on detectability in a demographic study of the terrestrial orchid Cleistes bifaria . J Ecol 91:265–273 CrossRefGoogle Scholar
Kéry, M, Gregg, KB (2004) Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae . J Ecol 92:686–695 CrossRefGoogle Scholar
Kéry, M, Gregg, KB, Schaub, M (2005) Demographic estimation methods for plants with unobservable life-states. Oikos 108:307–320 CrossRefGoogle Scholar
Madsen, JD, Marko, Wersal RM. MD (2016) Distribution and biomass allocation in relation to depth of flowering rush (Butomus umbellatus) in the Detroit Lakes. Minnesota Invasive Plant Sci Manag 9:161–170 CrossRefGoogle Scholar
Miller-Rushing, AJ, Høye, TT, Inouye, DW, Post, E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc Lond B Biol Sci 365:3177–3186 CrossRefGoogle ScholarPubMed
Möllerová, J (2005) Notes on invasive and expansive trees and shrubs. J For Sci 51:19–23 CrossRefGoogle Scholar
Moustakas, A, Evans, MR (2015) Effects of growth rate, size, and light availability on tree survival across life stages: a demographic analysis accounting for missing values and small sample sizes. BMC Ecol 15:6 CrossRefGoogle ScholarPubMed
Munguía-Rosas, MA, Parra-Tabla, V, Montiel, S (2013) Extreme variation in the reproductive phenology of the weed Ruellia nudiflora . Weed Res 53:328–336 CrossRefGoogle Scholar
Nakagawa, S, Schielzeth, H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc 85:935–956 Google ScholarPubMed
Nichols, JD, Kendall, WL (1995) The use of multi-state capture-recapture models to address questions in evolutionary ecology. J Appl Stat 22:835–846 CrossRefGoogle Scholar
Perkins, SR, Owens, MK (2003) Growth and biomass allocation of shrub and grass seedlings in response to predicted changes in precipitation seasonality. Plant Ecol 168:107–120 CrossRefGoogle Scholar
Pineda-Romero, C (2016) Fenología y producción de terpenos de Sambucus nigra, en la Cuenca del río Magdalen. Tesis de Licenciatura. Ciudad de México, Mexico: Facultad de Ciencias, Universidad Nacional Autónoma de México. 66 p Google Scholar
Prevéy, JS, Seastedt, TR (2014) Seasonality of precipitation interacts with exotic species to alter composition and phenology of a semiarid grassland. J Ecol 102:1549–1561 CrossRefGoogle Scholar
Ramula, S, Knight, TM, Burns, JH, Buckley, YM (2008) General guidelines for invasive plant management based on comparative demography of invasive and native plant populations. J Appl Ecol 45:1124–1133.CrossRefGoogle Scholar
R Development Core Team (2019) A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing Google Scholar
Richardson, DM, Pyšek, P, Rejmánek, M, Barbour, G, Panetta, D, West, CL (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107 CrossRefGoogle Scholar
Saenz-Pedroza, I, Feldman, R, Reyes-García, C, Meave, JA, Calvo-Irabien, LM, May-Pat, F, Dupuy, JM (2020) Seasonal and successional dynamics of size-dependent plant demographic rates in a tropical dry forest. PeerJ 8:e9636 CrossRefGoogle Scholar
Sandercock, BK (2006) Estimation of demographic parameters from live-encounter data: a summary review. J Wildl Manage 70:1504–1520 CrossRefGoogle Scholar
Santibáñez-Andrade, G, Castillo-Argüero, S, Zavala-Hurtado, Vega-Peña EV. (2015) Structural equation modeling as a tool to develop conservation strategies using environmental indicators: the case of the forests of the Magdalena river basin in Mexico City. Ecol Indic 54:124–136 CrossRefGoogle Scholar
Sass, GG, Cook, TR, Irons, KS, McClelland, MA, Michaels, NN, O’Hara, TM, Stroub, MR (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12:433–436 CrossRefGoogle Scholar
Schantz, MC, Sheley, RL, James, JJ (2019) Propagule pressure and priority seeding effects on the demography of invasive annual and native perennial grass species. Plant Ecol Divers 12:139–150 CrossRefGoogle Scholar
Sebert-Cuvillier, E, Paccaut, F, Chabrerie, O, Endels, P, Goubet, O, Decocq, G (2007) Local population dynamics of an invasive tree species with a complex life-history cycle: a stochastic matrix model. Ecol Model 201:127–143 CrossRefGoogle Scholar
Shea, K, Sheppard, A, Woodburn, T (2006) Seasonal life-history models for the integrated management of the invasive weed nodding thistle Carduus nutans in Australia. J Appl Ecol 43:517–526 CrossRefGoogle Scholar
Shefferson, RP, Sandercock, BK, Proper, J, Beissinger, SR (2001) Estimating dormancy and survival of a rare herbaceous perennial using mark-recapture models. Ecology 82:145–156 Google Scholar
Shriver, RK (2016) Quantifying how short-term environmental variation leads to long-term demographic responses to climate change. J Ecol 104:65–78 CrossRefGoogle Scholar
[SMN] Sistema Meteorológico Nacional México ( 2018) https://www.gob.mx/smn. Accessed: December 18, 2018Google Scholar
Stanley, TR, Burnham, KP (1998) Information-theoretic model selection and model averaging for closed population capture-recapture studies. Biom J 40:475–494 3.0.CO;2-#>CrossRefGoogle Scholar
Stoffel, MA, Nakagawa, S, Schielzeth, H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644 CrossRefGoogle Scholar
Van Der Maarel, E, De Cock, N, De Wildt, E (1985) Population dynamics of some major woody species in relation to long-term succession on the dunes of Voorne. Vegetation 61:209–219 CrossRefGoogle Scholar
Vargas-García, S, Argaez, V, Solano-Zavaleta, I, Zúñiga-Vega, JJ (2019) Population dynamics of three lizard species from the genus Sceloporus: short-term changes in demographic parameters. Integr Zool 14:542–560 CrossRefGoogle ScholarPubMed
Vibrans, H (2019) Malezas de México. Mexico City, Mexico: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). http://www.conabio.gob.mx/malezasdemexico/2inicio/home-malezas-mexico.htm. Accessed: December 12, 2019Google Scholar
Wainwright, CE, Wolkovich, EM, Cleland, EE (2012) Seasonal priority effects: implications for invasion and restoration in a semi-arid system. J Appl Ecol 49:234–241 CrossRefGoogle Scholar
White, GC, Burnham, KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(S1):S120–S139 CrossRefGoogle Scholar
White, GC, Kendall, WL, Barker, RJ (2006) Multistate survival models and their extensions in Program MARK. J Wildl Manage 70:1521–1529 CrossRefGoogle Scholar
Wolkovich, EM, Cleland, EE (2011) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294 CrossRefGoogle Scholar
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