Abstract
Seasonality is one of the main characteristics of a tropical dry forest that affects the structure of ecological communities. In this context, we evaluated the seasonal diversity of ferns and insects in the tropical dry forest of Morelos, Mexico, to determine whether a relationship exists between the presence of each of these two groups. Hill’s numbers indicated differences in the diversity of both groups according to season. In the rainy season, we recorded the highest diversity of ferns, with 6,471 individuals. In contrast, in the dry season, we recorded only 293 individuals. Regarding the insects, we collected 723 individuals in the rainy season and 171 individuals in the dry season. The order Orthoptera was the most abundant (50%). The best-represented functional group according to feeding guild was that of chewing herbivores. Correlation analysis revealed a positive relationship between insect and fern abundances since, for both groups, the minimum abundance was presented in the dry season and the maximum abundance in the rainy season. We recorded 12 orders of insects associated with eight ferns in the rainy season. Seasonal studies that consider different biological groups are necessary to understand how changes in resource availability shape temporal patterns of species diversity.
Key words:
alpha diversity; functional groups; herbivorous insects; tropical forest
Resumen
La estacionalidad es una de las principales características de los bosques tropicales secos que afectan la estructura de las comunidades ecológicas. En este contexto, evaluamos la diversidad estacional de helechos e insectos en el bosque tropical seco de Morelos, México, para determinar si existe una relación entre la presencia de estos dos grupos. Los números de Hill indicaron diferencias en la diversidad de ambos grupos según la temporada. En la época de lluvias registramos la mayor diversidad de helechos, con 6,471 individuos. En contraste, en la estación seca registramos solo 293 individuos. Con respecto a los insectos, colectamos 723 individuos en la época de lluvias y 171 individuos en la época seca. El orden Orthoptera fue el más abundante (50%). El grupo funcional mejor representado según el gremio alimenticio fue el de los herbívoros masticadores. El análisis de correlación reveló una relación positiva entre las abundancias de insectos y helechos ya que, para ambos grupos, la menor abundancia se presentó en la época seca y la abundancia mayor en la época lluviosa. Registramos 12 órdenes de insectos asociados a ocho helechos en la temporada de lluvias. Se necesitan estudios estacionales que consideren diferentes grupos biológicos para comprender cómo los cambios en la disponibilidad de recursos dan forma a los patrones temporales de la diversidad de especies.
Palabras clave:
diversidad alfa; grupos funcionales; insectos herbívoros; bosque tropical
Introduction
Seasonality is one of the main characteristics of a tropical dry forest (TDF) and it affects the structure of ecological communities through changes in different abiotic resources, such as water, temperature, and photoperiod (García & Cabrera-Reyes 2008García A & Cabrera-Reyes A (2008) Estacionalidad y estructura de la vegetación en la comunidad de anfibios y reptiles de Chamela, Jalisco, México. Acta zoológica mexicana 24: 91-115.; van Schaik et al. 1993van Schaik CP, Terborgh JW & Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.). Mexican TDF presents a marked seasonality, with only four months of rain and five to eight months of drought per year (Rzedowski 2006Rzedowski J (2006) Vegetación de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México. 504p.; Lopezaraiza-Mikel et al. 2014Lopezaraiza-Mikel M, Quesada M, Álvarez-Añorve M, Ávila-Cabadilla L, Martén-Rodríguez S, Calvo-Alvarado J, Espírito-Santo MM, Fernandes GW, Sanchez-Azofeifa A, Aguilar-Aguilar MJ, Balvino-Olvera F, Brandão D, Contreras-Sánchez JM, Correa-Santos J, Cristobal-Perez J, Fernandez P, Hilje B, Jacobi C, Fonseca-Pezzini F, Rosas F, Rosas-Guerrero V, Sánchez-Montoya G, Sáyago R & Vázquez-Ramírez A (2014) Phenological patterns of tropical dry forest along latitudinal and successional gradients in the Neotropics. In: Sánchez-Azofeifa A, Powers J, Fernandes GW & Quesada M (eds.) Tropical dry forests in the Americas: ecology, conservation and management. CRC Press, New York. Pp. 101-128.). This causes plant growth, reproduction, and establishment to be largely limited by the particular climatic conditions of the site (Murphy & Lugo 1986Murphy PG & Lugo A (1986) Ecology of tropical dry forest. Annual Review Ecology and Systematics 17: 67-88.; Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.). In addition, TDF is a highly diverse ecosystem comprising vertebrates, insects, and plants (Janzen 1987Janzen DH (1987) Insect diversity of a Costa Rican dry forest: why keep it, and how? Biological Journal of Linnean Society 30: 343-356.; Ceballos & Valenzuela 2010Ceballos G & Valenzuela D (2010) Diversidad, Ecología y Conservación de los Mamíferos de Latinoamérica. In: Ceballos G, García A, Martínez L, Espinoza E, Bezaury Creel J & Dirzo R (eds.) Diversidad, amenazas y áreas prioritarias para la conservación de las selvas secas del oeste de México. Ed. CONABIO/UNAM, México D.F.. Pp. 93-118.; Aguilar-Pérez et al. 2019Aguilar-Pérez JG, Pinedo-Escatel JA & Váldez-Quezada BC (2019) Three new Mexican species of the endemic Athysanini leafhopper genus Devolana DeLong (Hemiptera: Cicadellidae) from the tropical dry forest. Journal of Natural History 53: 2039-205.), mainly as a result of its structure and the physiological properties of the individuals that are determined by seasonality. In plants, for example, the dry season can trigger flowering (van Schaik et al. 1993van Schaik CP, Terborgh JW & Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.; Lopezaraiza-Mikel et al. 2014Lopezaraiza-Mikel M, Quesada M, Álvarez-Añorve M, Ávila-Cabadilla L, Martén-Rodríguez S, Calvo-Alvarado J, Espírito-Santo MM, Fernandes GW, Sanchez-Azofeifa A, Aguilar-Aguilar MJ, Balvino-Olvera F, Brandão D, Contreras-Sánchez JM, Correa-Santos J, Cristobal-Perez J, Fernandez P, Hilje B, Jacobi C, Fonseca-Pezzini F, Rosas F, Rosas-Guerrero V, Sánchez-Montoya G, Sáyago R & Vázquez-Ramírez A (2014) Phenological patterns of tropical dry forest along latitudinal and successional gradients in the Neotropics. In: Sánchez-Azofeifa A, Powers J, Fernandes GW & Quesada M (eds.) Tropical dry forests in the Americas: ecology, conservation and management. CRC Press, New York. Pp. 101-128.) or may accelerate leaf loss as a mechanism to resist drought, whereas the rainy season favors the production of new leaves (Sánchez-Azofeifa et al. 2013Sánchez-Azofeifa A, Kalacska ME, Quesada M, Stoner KE, Lobo JA & Arroyo-Mora P (2013) Tropical dry climates. In: Schwartz MD (ed.) Phenology: an integrative environmental Science. Springer, New York. Pp. 121-137.; Lopezaraiza-Mikel et al. 2014Lopezaraiza-Mikel M, Quesada M, Álvarez-Añorve M, Ávila-Cabadilla L, Martén-Rodríguez S, Calvo-Alvarado J, Espírito-Santo MM, Fernandes GW, Sanchez-Azofeifa A, Aguilar-Aguilar MJ, Balvino-Olvera F, Brandão D, Contreras-Sánchez JM, Correa-Santos J, Cristobal-Perez J, Fernandez P, Hilje B, Jacobi C, Fonseca-Pezzini F, Rosas F, Rosas-Guerrero V, Sánchez-Montoya G, Sáyago R & Vázquez-Ramírez A (2014) Phenological patterns of tropical dry forest along latitudinal and successional gradients in the Neotropics. In: Sánchez-Azofeifa A, Powers J, Fernandes GW & Quesada M (eds.) Tropical dry forests in the Americas: ecology, conservation and management. CRC Press, New York. Pp. 101-128.).
The main abiotic factors that affect the population dynamics of ferns are rainfall and temperature. These factors trigger the production of new and fertile leaves, as well as the release of spores (Mehltreter & García-Franco 2008Mehltreter K & García-Franco JG (2008) Leaf phenology and trunk growth of the deciduous tree fern Alsophila firma (Baker) D.S. Conant in a lower montane Mexican forest. American Fern Journal 98: 1-13.; Lee et al. 2018Lee PH, Huang YM & Chiou WL (2018) Fern Phenology. In: Fernández H (ed.) Current advances in fern research. Springer, Cham. Pp. 381-399.; Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.) since this season presents favorable conditions for their germination and establishment (Sharpe & Mehltreter 2010Sharpe JM & Mehltreter K (2010) Ecological insights from fern population dynamics. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 61-110.). Temporal dynamics such as seasonality can therefore affect species abundance (López-Carretero et al. 2015). For example, in the seasonal ecosystems of Mexico, Bolivia, and Costa Rica, higher abundance and diversity of vascular plants are reported in the rainy season (Acebey et al. 2003Acebey A, Gradstein SR & Krömer T (2003) Species richness and habitat diversification of bryophytes in submontane rain forest and fallows of Bolivia. Journal of Tropical Ecology 19: 9-18.; Gradstein et al. 2003Gradstein SR, Nadkarni NM, Krömer T, Holz I & Nöske N (2003) A protocol for rapid and representative sampling of vascular and non-vascular epiphyte diversity of tropical rain forests. Selbyana 24: 105-111.; Cardelús et al. 2006Cardelús CL, Colwell RK & Watkins JEJr (2006) Vascular epiphyte distribution patterns: explaining the mid-elevation richness peak. Journal of Ecology 94: 144-156.) because of the generalized influence of humidity and precipitation that to a large extent dictates the richness and abundance of vascular plants (Kessler et al. 2011Kessler M, Kluge J, Hemp A & Ohlemüller R (2011) A global comparative analysis of elevational species richness patterns of ferns. Global Ecology and Biogeography 20: 868-880.).
The same is true for the insect group, which varies seasonally according to changes in climatic conditions and food resource availability that act to favor the development and reproduction of these organisms (Wolda 1988Wolda H (1988) Insect seasonality: why? Annual review of evolution and systematic 19: 1-18.; Danks 2007Danks HV (2007) The elements of seasonal adaptations in insects. The Canadian Entomologist 139: 1-44.; Kishimoto-Yamada K & Itioka 2015). Seasonal patterns become more evident when comparing insect abundance and diversity between wet and dry seasons in ecosystems such as the TDF (Kishimoto-Yamada & Itioka 2015Kishimoto-Yamada K & Itioka T (2015) How much have we learned about seasonality in tropical insect abundance since Wolda (1988). Entomological Science 18: 407-419.). The dry season brings a reduction in insect diversity and abundance, which is largely due to the duration of the phenological leafing events that regulate plant-insect interactions (Janzen 1973Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54: 687-708.; van Schaik et al. 1993van Schaik CP, Terborgh JW & Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.; Borchert 1994Borchert R (1994) Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75: 1437-1449.). In this sense, insects of the chewing and sap-sucking food guild present reduced abundance and diversity in the dry season (Janzen 1973Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54: 687-708.; Creão-Duarte et al. 2016Creão-Duarte A, Hernández M, Rothéa R & Santos W (2016) Temporal variation of Membracidae (Hemiptera: Auchenorrhyncha) composition in areas of caatinga with different vegetation structures. Sociobiology 63: 826-830.), mainly as a result of habitat restriction, food shortage, or the presence of unsuitable conditions for their development (Pinheiro et al. 2002Pinheiro F, Diniz IR, Coelho D & Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136.).
The interaction between insects and ferns has been widely studied (Balick et al. 1978Balick MJ, Furth DG & Cooper- Driver G (1978) Biochemical and evolutionary aspects of arthropod predation on ferns. Oecologia 35: 55-89.; Auerbach & Hendrix 1980Auberbach MJ & Hendrix SD (1980) Insect-fern interactions: macrolepidopteran utilization and species-area association. Ecological Entomology 5: 99-104.; Mehltreter & Tolome 2003Mehltreter K & Tolome J (2003) Herbivory on three tropical fern species of a Mexican cloud forest. In: Chandra S & Srivastava M (eds.) Pteridology in the New Millennium. Springer, Dordrecht. Pp. 375-381.; Chaves & de Gois 2006Chaves OM & de Gois F (2006) Análisis comparativo de la folivoría en helechos y angiospermas en un bosque tropical húmedo de Costa Rica. Revista Pensamiento Actual 6: 7-13.; Mehltreter et al. 2006Mehltreter K, Hülber K & Hietz P (2006) Herbivory on epiphytic ferns of a Mexican cloud forest. Fern Gazette 17: 303-309.; Mehltreter 2010Mehltreter K (2010) Interactions of ferns with fungi and animals. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 221-254.; Fuentes-Jacques et al. 2022aFuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717., bFuentes-Jacques LJ, Hanson-Snortum P, Hernández-Ortiz V, Díaz-Castelazo C & Mehltreter K (2022b) A global review and network analysis of phytophagous insect interactions with ferns and lycophytes. Plant Ecology 223: 27-40.). Studies of ferns have reported foliar herbivory damage of between 5-15% (Auerbach & Hendrix 1980Auberbach MJ & Hendrix SD (1980) Insect-fern interactions: macrolepidopteran utilization and species-area association. Ecological Entomology 5: 99-104.; Mehltreter & Tolome 2003Mehltreter K & Tolome J (2003) Herbivory on three tropical fern species of a Mexican cloud forest. In: Chandra S & Srivastava M (eds.) Pteridology in the New Millennium. Springer, Dordrecht. Pp. 375-381.; Chaves & de Gois 2006Chaves OM & de Gois F (2006) Análisis comparativo de la folivoría en helechos y angiospermas en un bosque tropical húmedo de Costa Rica. Revista Pensamiento Actual 6: 7-13.; Mehltreter et al. 2006Mehltreter K, Hülber K & Hietz P (2006) Herbivory on epiphytic ferns of a Mexican cloud forest. Fern Gazette 17: 303-309.), with similar values reported in herbivory studies in angiosperms (Dirzo & Domínguez 1995Dirzo R & Domínguez CA (1995) Plant-herbivore interactions in Mesoamerican tropical dry forest. In: Bullock SH, Medina E & Mooney HA (eds.) Seasonally Dry Tropical Forest. Cambridge University Press, New York. Pp. 304-325.; Williams-Linera & Baltazar 2001Williams-Linera G & Baltazar A (2001) Herbivory on young and mature leaves of one temperate deciduous and two tropical evergreen trees in the understory and canopy of Mexican cloud forest. Selbyana 22: 213-218.). It should be noted that, although the study of interactions such as herbivory in ferns has received increasing attention, the existing information is focused mainly on studies in ecosystems with low seasonality (Fuentes-Jacques et al. 2022aFuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717., bFuentes-Jacques LJ, Hanson-Snortum P, Hernández-Ortiz V, Díaz-Castelazo C & Mehltreter K (2022b) A global review and network analysis of phytophagous insect interactions with ferns and lycophytes. Plant Ecology 223: 27-40.). In this sense, Mehltreter (2010)Mehltreter K (2010) Interactions of ferns with fungi and animals. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 221-254. suggests that the proportion of 98 herbivorous insects could be 3 to 7 times lower than in seed plants and that there could be between 1,500 and 3,500 species of insects that feed on the ferns.
It is therefore necessary to determine how the temporal seasonality of tropical dry forests affects the presence and/or absence of different groups of species. In this regard, the fern group can indicate changes in precipitation and temperature patterns since these plants are susceptible to environmental change. Consequently, they can be considered bioindicators (Zotz & Bader 2009Zotz G & Bader MY (2009) Epiphytes in a changing world: global change effects on vascular and non-vascular epiphytes. Progress in Botany 70: 47-70.; Pouteau et al. 2016Pouteau R, Meyer JY, Blanchard P, Nitta JH, Terorotua M & Taputuarai R (2016) Fern species richness and abundance are indicators of climate change on high-elevation islands: evidence from an elevational gradient on Tahiti (French Polynesia). Climatic Change 138: 143-156.). The objectives of the present study were 1) to determine the diversity of ferns and insects in the rainy and dry seasons; 2) to determine the richness of the functional groups of insects associated with ferns, considering their feeding guild; 3) to analyze the relationship between the diversities of ferns and insects.
We hypothesized that 1) there will be a greater diversity of ferns during the rainy season because of the high precipitation, and the insect diversity will increase due to the availability of a greater quantity of resources (e.g., food and shelter); and 2) the chewing herbivores functional groups will be the best represented.
Material and Methods
Study area
This study was conducted in a tropical dry forest (TDF) established on lava fields near the community of San Andres de la Cal, Tepoztlan, in Morelos, Mexico (18°57’22.2’’N, 99°06’50.2’’W). The local climate is semi-warm (A) C (w2) (w) ig, with rainfall during summer and winter (May to October). The average annual precipitation is approximately 1,200 mm and the average annual temperature is around 20 °C (Ruíz-Rivera 2001). The maximum and minimum temperatures are around 32 °C in April and 11 °C in January. The highest rainfall occurs from June to October, ranging from 113 to 242.3 mm per month (CONAGUA 2016CONAGUA - Comisión Nacional Del Agua (2016) Estaciones Meteorológicas Automáticas (EMA’s). Sistema de Información y Visualización de Estaciones Automatica: Tepoztlán. Available at <https://smn.conagua.gob.mx/es/observando-el-tiempo/estaciones-meteorologicas-automaticas-ema-s>. Access on 11 December 2023.
https://smn.conagua.gob.mx/es/observando...
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In Morelos, the TDF harbors about 39 species of woody plants, including Sapium macrocarpum Müll. Arg. (Euphorbiaceae), Ipomoea pauciflora M. Martens and Galeotti (Convolvulaceae), and Quercus obtusata Humb. & Bonpl. (Fagaceae) (Cortés-Anzúres 2015Cortés-Anzúres BO (2015) Mecanismos de establecimiento de Prosthechea citrina (La Llave & Lex.) W. E. Higgins. Tesis de Doctorado. Universidad Autónoma del Estado de Morelos, Cuernavaca. 57p.). In the case of the Pteridoflora, 22 species have been reported, the most abundant of which are Cheilanthes kaulfussii Kunze, Bommeria elegans (Davenp.) Ranker and Haufler, B. pedata (Sw.) Fourn, Dryopteris maxonii Underw. & C. Chr., Notholaena candida (M. Martens & Galeotti) Hook., and Pleopeltis polypodioides (L.) E.G. Andrews & Windham. Likewise, lycophytes such as Selaginella lepidophylla (Hook. & Grev.) Spring and S. pallescens (C. Presl) Spring (Selaginellaceae) have been reported (Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.).
Sampling
To determine the diversity of ferns and insects of the TDF, observations were made during 2019 and 2020 in the dry and rainy seasons (from 26 field samples). A total of 17 quadrats of 2.5 × 2.5 m were randomly established at a distance of 50 m apart. Sampling was conducted every 15 days from 9:00 am to 5:00 pm (eight hours per day). Each quadrat was checked for the presence of insects associated with ferns, through an active search for each individual of each fern species conducted for approximately 30 minutes, the time of the insect-fern sample effort was 3,536 hours in total.
In addition, in each quadrat, insects associated with the ferns were collected directly by sweeping the plants with an entomological net and then quantified. The collected insects were taken to the laboratory where the insects were identified to morphospecies level with the help of a specialist (Dr. Armando Burgos) in the plant parasitology laboratory of the Center for Biological Research of the Autonomous University of the State of Morelos and using specialized identification guides (Triplehorn & Johnson 2005Triplehorn CA & Johnson NF (2005) Borror and DeLong’s introduction to the study of insects. 7th ed. Thompson Brooks/Cole, Belmont. 864p.; Fontana & Buztetti 2007Fontana P & Buztetti FM (2007) New or little known Mexican Melanoplinae (Orthoptera: Acrididae). Atti della Accademia Roveretana degli Agiati 7: 73-130.; Fontana et al. 2008Fontana P, Buztetti FM & Mariño-Pérez R (2008) Chapulines, langostas, grillos y esperanzas de México. Guía fotográfica. WBA Handbooks, Verona. 272p.). The collected insects were deposited in the Morelos University Entomological Collection (CEUM) of the Center for Biological Research of the Autonomous University of the State of Morelos, Mexico (CIB-UAEM). The species were identified using floral listings, keys, and descriptions (Mickel & Smith 2004Mickel JT & Smith AR (2004) The pteridophytes of Mexico. Memoirs of the New York. Botanical Garden Press, New York. 1063p.), while the taxonomic classification was conducted according to the PPG I (2016)Pteridophyte Phylogeny Group - PPG I (2016) A community-derived classification for extant lycophytes and ferns. Journal and Systematic Evolution 54: 563-603.. The collected fern specimens were deposited in the herbarium (HUMO) of the Center for Biodiversity and Conservation Research of the Autonomous University of the State of Mexico (CIByC-UAEM).
The collected insects were classified according to the functional group (FG) to which they belong according to feeding guild (McGavin 2000McGavin GC (2000) Manual de identificación de insectos, arañas y otros artrópodos terrestres. Ed. Omega, Barcelona. Pp. 6-256.): 1) chewing herbivores; 2) sucking herbivores; 3) predators; 4) decomposers and 5) xylophages.
Data analysis
We obtained the average number of individuals per month for each fern species to calculate the abundance. We then determined the proportion in percentage as a proxy for the relative abundance of each species. To determine the sampling effort, rarefaction and extrapolation curves were generated, which allowed us to estimate the number of species based on the number of samples (Chao et al. 2014Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK & Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45-67.). To determine whether there were differences in the diversity of both groups according to season, Hill numbers, or the effective number of species, were used where the estimates of each order and their confidence intervals are shown. The order q = 0 refers to the richness or number of species and does not consider the abundance of species; order q = 1 indicates the effective number of equally frequent (or common) species, in which all species are included with a weight proportional to their abundance (exponential of the Shannon index) and its calculation is not biased by the presence of rare or abundant species in the sample; and order q = 2 indicates the effective number of very abundant or dominant species, the inverse of Simpson’s index (Moreno et al. 2011Moreno CE, Barragán F, Pineda E & Pavón NP (2011) Reanálisis de la diversidad alfa: alternativas para interpretar y comparar información sobre comunidades ecológicas. Revista mexicana de biodiversidad 82: 1249-1261.). These analyses were performed using the iNEXT package (Hsieh et al. 2016Hsieh TC, Ma KH & Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7: 1451-1456.). In addition, to define the relationship between fern and insect abundance, a Spearman correlation analysis was performed to determine the degree of correlation of different variables. All analyses were performed in R software (R Development Core Team 2017R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at <https://www.r-project.org>.
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Results
Diversity of ferns
A total of 6,764 individual ferns belonging to two orders, five families, and 13 species were recorded (Tab. 1). Regarding the seasons, the highest abundance was recorded in the rainy season, with a total of 6,471 individual ferns. The most abundant species were Bommeria pedata (24%; Fig. 1a), Bommeria elegans (22%; Fig. 1b), and Asplenium pumilum (17%; Fig. 1c) (Tab. 1). In contrast, in the dry season, a total of 293 individuals were recorded and the most abundant species were Bommeria pedata (28%) and Notholaena candida (16%) (Tab. 1).
a. Bommeria pedata. b. Bommeria elegans. c. Asplenium pumilum. Photos by David Tenango and Clara Hernández.
The sample coverage values for ferns during the rainy and dry seasons were 95% and 99%, respectively. Regarding fern diversity, it was found that the fern richness (q0) was significantly higher in the rainy season. In contrast, the common species (q1) were significantly lower in the rainy season, and the dominant species (q2) did not differ between seasons (Fig. 2a).
a. Alpha diversity of ferns (q0, q1, and q2) during the two seasons of the year in the tropical dry forest of Morelos, Mexico. Solid lines indicate individual rarefaction; dashed lines indicate extrapolation to the sample size of 6,764 individuals; shading denotes 95% confidence intervals. b. Alpha diversity of insects (q0, q1, and q2) during the two seasons of the year in the tropical dry forest of Morelos. Solid lines indicate individual rarefaction; dashed lines indicate extrapolation to the sample size of 899 individuals; shading denotes 97% confidence intervals.
Diversity of insects
A total of 899 insect individuals, belonging to ten orders, 17 families, and 75 morphospecies, were recorded (Tab. 2). The highest abundance was found in the rainy season, with 723 individual insects and 71 morphospecies belonging to 17 families and 10 orders. The families with the highest number of individuals were Acrididae (50%; Fig. 3a-f, dorsal and side) and Pentatomidae (10%). In contrast, in the dry season, 176 individual insects and 18 morphospecies belonging to eight families and ten orders were recorded. The families with the highest number of individuals were Acrididae (46%) and Lygaeidae (10%) (Tab. 2).
Taxonomic determination at morphospecies and functional group level of the insects collected in the tropical dry forest of Morelos.
a-f. Specimens of the order Orthoptera of the Tettigoniidae family in different stages - Nymph, habitus, lateral a) and dorsal view b); Female, habitus, lateral c) and dorsal view d); Male, habitus, lateral e) and dorsal view f) associated with ferns in the tropical dry forest of Morelos, Mexico. Scale bar = 10 mm.
The sample coverage for insects was 97% in both the rainy and dry seasons. Regarding diversity, we found the same pattern as in the ferns where the observed richness of insects (q0) and common species (q1) was significantly lower in the dry season; however, the dominant species (q2) did not present significant differences between seasons (Fig. 2b).
Functional groups of insects
In general, five functional groups according to feeding guild were found in both seasons. In the rainy season, a total of 480 chewing herbivores, 162 predators, 38 decomposers, 15 sucking herbivores, seven xylophages, and 21 unidentified individuals were recorded. During the dry season, 88 chewing herbivores, 51 sucking herbivores, 22 predators, 14 decomposers, one xylophage, and one unidentified individual were collected (Fig. 4).
Abundance of insect functional groups according to feeding guild in a tropical dry forest of Morelos, Mexico. Green and yellow colors indicate the rainy and dry seasons, respectively.
Seasonal relationship between abundances of ferns and insects
Correlation analysis showed a positive relationship between insect and fern abundances (r = 0.85; P = 0.007) since the minimum abundance was presented in the dry season and the maximum abundance in the rainy season for both groups.
Diversity of insects associated with ferns
We found 12 insect orders associated with eight fern species in the rainy season. The most associated species of ferns were Bommeria elegans, Dryopteris karwinskyana and B. pedata. The insect orders with the most associations were Hemiptera (9/9) followed by Orthoptera (6/9) (Fig. 5).
Diversity of insects associated with ferns in the rainy season in a tropical dry forest of Morelos, Mexico. Sankey diagram created using the open-source, online tool SankeyMATIC (sankeymatic.com).
Discussion
This study is the first to provide information about seasonal patterns among ferns and their associated insects in tropical dry forests. The hypotheses proposed were fulfilled since we found that both ferns and insects showed greater diversity in the rainy season. Regarding the functional group, herbivorous insects were the most commonly represented in this study, while we evidenced a positive correlation between the abundance of ferns and insects.
Effect of seasonality on fern diversity
Temporal habitat dynamics, such as seasonality, can affect species abundance (López-Carretero et al. 2015). In the present study, we found a greater diversity of ferns in the rainy season. This coincides with other studies in seasonal ecosystems in Mexico, Bolivia, and Costa Rica that also report the highest diversity of vascular plants in this season (Acebey et al. 2003Acebey A, Gradstein SR & Krömer T (2003) Species richness and habitat diversification of bryophytes in submontane rain forest and fallows of Bolivia. Journal of Tropical Ecology 19: 9-18.; Gradstein et al. 2003Gradstein SR, Nadkarni NM, Krömer T, Holz I & Nöske N (2003) A protocol for rapid and representative sampling of vascular and non-vascular epiphyte diversity of tropical rain forests. Selbyana 24: 105-111.; Cardelús et al. 2006Cardelús CL, Colwell RK & Watkins JEJr (2006) Vascular epiphyte distribution patterns: explaining the mid-elevation richness peak. Journal of Ecology 94: 144-156.; Jiménez-López et al. 2020Jiménez-López DA, Martínez-Camilo R, Martínez-Meléndez N & Kessler M (2020) Diversity of epiphyte ferns along an elevational gradient in El Triunfo Biosphere Reserve, southern Mexico. Plant Ecology and Evolution 153: 12-21.; Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.). This is likely to be because the rainy season presents optimal microenvironmental conditions of precipitation and humidity for the establishment and development of these plants (Kessler et al. 2011Kessler M, Kluge J, Hemp A & Ohlemüller R (2011) A global comparative analysis of elevational species richness patterns of ferns. Global Ecology and Biogeography 20: 868-880.; Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.).
The Pteridaceae family was the best represented, with Bommeria pedata and B. elegans contributing most to the abundance. These species have been reported to be associated with a wide variety of habitats, including those with xeric conditions (Mickel & Smith 2004Mickel JT & Smith AR (2004) The pteridophytes of Mexico. Memoirs of the New York. Botanical Garden Press, New York. 1063p.; Schuettpelz et al. 2007Schuettpelz E, Chen C-W, Kessler M, Pinson JB, Johnson G, Davila A, Cochran AT, Huiet L & Pryer KM (2007) A revised generic classification of vittarioid ferns (Pteridaceae) based on molecular, micromorphological, and geographic data. Taxon 65: 708-722.). In this sense, the TDF of our study site is characterized by a mainly rocky soil type. In addition, some species of this family present unique adaptations that enable them to establish under contrasting environmental conditions due to the presence of indumentum, leaf rolling, and deciduous leaves (Schuettpelz et al. 2007Schuettpelz E, Chen C-W, Kessler M, Pinson JB, Johnson G, Davila A, Cochran AT, Huiet L & Pryer KM (2007) A revised generic classification of vittarioid ferns (Pteridaceae) based on molecular, micromorphological, and geographic data. Taxon 65: 708-722.; Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.), which generally allow them to cope with adverse microenvironmental conditions (Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.).
It has been shown, mainly through changes in the availability of different abiotic resources such as water and temperature, that the structure of ecological communities can affect the diversity of species (García & Cabrera-Reyes 2008García A & Cabrera-Reyes A (2008) Estacionalidad y estructura de la vegetación en la comunidad de anfibios y reptiles de Chamela, Jalisco, México. Acta zoológica mexicana 24: 91-115.; Lopezaraiza-Mikel et al. 2014Lopezaraiza-Mikel M, Quesada M, Álvarez-Añorve M, Ávila-Cabadilla L, Martén-Rodríguez S, Calvo-Alvarado J, Espírito-Santo MM, Fernandes GW, Sanchez-Azofeifa A, Aguilar-Aguilar MJ, Balvino-Olvera F, Brandão D, Contreras-Sánchez JM, Correa-Santos J, Cristobal-Perez J, Fernandez P, Hilje B, Jacobi C, Fonseca-Pezzini F, Rosas F, Rosas-Guerrero V, Sánchez-Montoya G, Sáyago R & Vázquez-Ramírez A (2014) Phenological patterns of tropical dry forest along latitudinal and successional gradients in the Neotropics. In: Sánchez-Azofeifa A, Powers J, Fernandes GW & Quesada M (eds.) Tropical dry forests in the Americas: ecology, conservation and management. CRC Press, New York. Pp. 101-128.), limiting their growth, reproduction, and establishment (Murphy & Lugo 1986Murphy PG & Lugo A (1986) Ecology of tropical dry forest. Annual Review Ecology and Systematics 17: 67-88.). In this sense, in some fern species, the presence or absence of water provokes leaf loss by causing them to dry up and fall, with new leaves produced when conditions are optimal (van Shaik et al. 1993; Castrejón-Alfaro et al. 2022Castrejón-Alfaro EB, Ramos-Robles MI & Aguilar-Dorantes KM (2022) Phenology of the terrestrial fern community in a tropical dry forest of Morelos, Mexico. American Fern Journal 112: 269-284.).
This difference in seasonal patterns of fern diversity could be explained as a synchronization that reflects a direct influence of climate. Ferns have low control of evaporative potential during most of their life cycle and are thus dependent on water availability and relative humidity (Page 2002Page CN (2002) Ecological strategies in fern evolution: a neopteridological overview. Review of Palaeobotany and Palynology 119: 1-33.; Hietz 2010Hietz P (2010) Fern adaptations to xeric environments. In: Mehltreter K, Walker LR & Sharpe JM (eds.) Fern ecology. Cambridge University Press, Cambridge. Pp. 140-176.). Moreover, our study site presents low ambient humidity values of around 20% (CONAGUA 2016CONAGUA - Comisión Nacional Del Agua (2016) Estaciones Meteorológicas Automáticas (EMA’s). Sistema de Información y Visualización de Estaciones Automatica: Tepoztlán. Available at <https://smn.conagua.gob.mx/es/observando-el-tiempo/estaciones-meteorologicas-automaticas-ema-s>. Access on 11 December 2023.
https://smn.conagua.gob.mx/es/observando...
), which could be related to changes in the diversity and abundance of the group. Likewise, the relative homogeneity of microenvironments and low availability of suitable niches for ferns in tropical forests could be another limiting factor for the occurrence of greater fern richness (Kluge & Kessler 2011Kluge J & Kessler M (2011) Influence of niche characteristics and forest type on fern species richness, abundance and plant size along an elevational gradient in Costa Rica. Plant Ecology 212: 1109-1121.).
Effect of seasonality on insect diversity
In the insect group, we found the same pattern as in the ferns, since the insects presented greater diversity and abundance in the rainy season. A strong reduction in the abundance of insects has been documented during the dry season, which may be due to habitat restriction, food shortage, or the presence of unsuitable conditions for development (Pinheiro et al. 2002Pinheiro F, Diniz IR, Coelho D & Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136.). This could indicate that the insect diapause (i.e., the mechanism through which the annual life history rhythm is manifested) is synchronized with the presence of appropriate seasonal conditions (Janzen 1973Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54: 687-708.; van Schaik et al. 1993van Schaik CP, Terborgh JW & Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.; Rodríguez-Porras 2012Rodríguez-Porras R (2012) Influencia de la fenología de árboles del dosel en la diversidad y estacionalidad de Curculionidae (Coleoptera) en la Isla Barro Colorado, Panamá. Tesis Doctoral. Universidad de Panamá, Panama. 96p.).
The most abundant family in both seasons was Acrididae (locusts, grasshoppers). Another study conducted in a tropical dry forest in Mexico reports this as the most abundant and dominant family that contributes greatly to the biomass of herbivorous insects (Arya et al. 2015Arya MK, Joshi PC & Vinod PB (2015) Species composition, abundance, density and diversity of grasshoppers (Insecta: Orthroptera) in a protected forest ecosystem in the western Himalaya. Journal of Fauna and Biological studies 2: 42-46.). This group of generalist herbivores is characterized by folivores and has a wide distribution ranging from sea level to high elevations and including different habitat types from scrubland to temperate forest. They also possess a great capacity for migration and can infest economically important crops (Rusconi 2017Rusconi JM (2017) Diversidad de entomonemátodos asociados a insectos ortópteros plaga del suelo (Gryllidae y Gryllotalpide) en el Gran La Plata Tesis doctoral. Universidad Nacional de La Plata, Buenos Aires. 149p.). The family includes the order Orthoptera, which was the most abundant in this study, contrasting thus with findings from other tropical regions, which show a high abundance of the order Coleoptera during the rainy season (Tanaka & Tanaka 1982Tanaka L & Tanaka S (1982) Rainfall and seasonal changes in Arthropod abundance on a Tropical Oceanic lsland. Biotropica 14: 114-123.; Boinski & Fowler 1989Boinski S & Fowler NL (1989) Seasonal patterns in a Tropical Lowland Forest. Biotropica 21: 223-233.; Smythe 1990Smythe N (1990) Abundancia estacional de insectos nocturnos en un bosque neotropical. In: Rand AS, Windsor DM & Leigh EG Jr. (eds.) Ecología de un bosque tropical: ciclos estacionales y cambios a largo plazo. Smithsonian Tropical Research Institute, Balboa. Pp. 393-402.; Pinheiro et al. 2002Pinheiro F, Diniz IR, Coelho D & Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136.; Andresen 2005Andresen A (2005) Dung beetle assemblages in primary forest and disturbed habitats in a tropical dry forest landscape in western Mexico. Journal of Insect Conservation 12: 639-650.; Nyeko 2009Nyeko P (2009) Dung beetle assemblages and seasonality in primary forest and forest fragments on agricultural landscapes in Budongo, Uganda. Biotropica 41: 476-484.; Rodríguez-Porras 2012Rodríguez-Porras R (2012) Influencia de la fenología de árboles del dosel en la diversidad y estacionalidad de Curculionidae (Coleoptera) en la Isla Barro Colorado, Panamá. Tesis Doctoral. Universidad de Panamá, Panama. 96p.). This could be because this order contains 22,400 phytophagous species, but only 1.1% of all fern-insect interactions and 1.5% of all fern-feeding insect species (Fuentes-Jacques et al. 2022aFuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717.).
In contrast, the order Hemiptera (cicadas, aphids, or woodlice) was the least abundant, probably because this group presents very varied forms, including sessile organisms that are difficult to recognize as insects, for which reason we consider that this group may have been under-represented in this study. This result contrasts with Wolda (1996)Wolda H (1996) Seasonality of Homoptera on Barro Colorado Island. In: Leigh Jr EG, Rand AS & Windsor DM (eds.) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution Press, New York. Pp. 319-330., who reports that the order Hemiptera is the most abundant at the beginning of the rainy season in a tropical forest in Panama, while Pinheiro et al. (2002)Pinheiro F, Diniz IR, Coelho D & Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136. documents that the orders Hemiptera, Lepidoptera, and Orthoptera present a clustered distribution, with greater abundance during the transition from the end of the dry season to the beginning of the rainy season.
It is therefore possible that the difference in order is due to the vegetation type and the stable climatic conditions, which could mean that many tropical insects may have their greatest diversity in this type of ecosystem (Pinheiro et al. 2002Pinheiro F, Diniz IR, Coelho D & Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136.). It is possible that ferns provide microhabitats for other groups such as insects and that this acts to promote their abundance and diversity. However, the facilitation effect that ferns may have on insects or other groups in TDF remains to be studied, in addition to considering temporal habitat dynamics such as seasonality and resource abundance (López-Carretero et al. 2015).
Functional groups of insects
In this study, we found five functional groups, the most abundant feeding guild being chewing herbivores, followed by predators and, in lower proportion, by sucking and xylophagous herbivores. However, this pattern may vary among insect guilds, which depend mainly on the abiotic conditions of the site (Novais et al. 2018Novais S, Macedo-Reis LE, Cristobal-Peréz EJ, Sánchez-Montoya G, Janda M, Neves F & Quesada M (2018) Positive effects of the catastrophic Hurricane Patricia on insect communities. Scientific Reports 8-15042.). This result supports that reported by Fuentes-Jacques et al. (2022a)Fuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717., who state that the most common feeding guild is that of the leaf chewers and it usually comes from generalist insect groups. In this sense, it was the order Orthoptera that contributed the largest number of species for this feeding guild. This order has a worldwide distribution, with a preference for warm and temperate regions (Aguirre-Segura & Barranco 2015Aguirre-Segura A & Barranco VP (2015) Orden Orthoptera. Ibero Diversidad Entomológica 46: 1-13.) and with a very varied feeding regime, from omnivorous, phytophagous species to those that feed on material of animal origin (McGavin 2000McGavin GC (2000) Manual de identificación de insectos, arañas y otros artrópodos terrestres. Ed. Omega, Barcelona. Pp. 6-256.). However, it should be noted that the order Orthoptera could be overrepresented in this study since only 1.1% of all the species in this order interact with any fern species (Fuentes-Jacques et al. 2022aFuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717.).
The second most common feeding guild found was that of predators, where the order Hemiptera, specifically the reduvids and pentatomids, contributed 131 individuals to the guild. This order is among the most abundant insect groups in tropical forests, comprising more than 23,500 known species, many of which are highly specialized to particular host plants or habitats (Hamilton & Whitcomb 2010Hamilton KA & Whitcomb RF (2010) Leafhoppers (Homoptera: Cicadellidae): a major family adapted to grassland habitats. In: Shorthouse JD & Floate KD (eds.) Arthropods of Canadian grasslands. Vol. 1. Biological Survey of Canada, Alberta. Pp. 169-197.). In the same sense, Fuentes-Jacques et al. (2022a)Fuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717. state that the order Hemiptera is overrepresented for ferns since they found that this group accounted for 36.6% of all interactions between ferns and insects.
In contrast, the feeding guild with the lowest number of morphospecies (15) was that of the sap-sucking herbivores, belonging to the order Hemiptera. This finding was surprising because the guild of the sap-sucking herbivores is the most abundant in seasonal ecosystems (Novais et al. 2018Novais S, Macedo-Reis LE, Cristobal-Peréz EJ, Sánchez-Montoya G, Janda M, Neves F & Quesada M (2018) Positive effects of the catastrophic Hurricane Patricia on insect communities. Scientific Reports 8-15042.; Fuentes-Jacques et al. 2022aFuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717.).
It is worth mentioning that, in the case of the xylophagous feeding guild, we found the presence of five morphospecies that belong to the cerambycid family. In this sense, it could be that the ferns are providing oviposition sites for this group of insects, as suggested by Vargas-Cardoso et al. (2018)Vargas-Cardoso OR, Corona-López AM, López-Martínez V, Flores-Palacios A, Figueroa-Brito R & Toledo-Hernández VH (2018) New host records of Cerambycidae (Coleoptera) from central Mexico. The Pan-Pacific Entomologist 94: 91-102. since they mention that cerambycids have specific relationships with certain plant taxa, such that the time of emergence of these individuals could be dictated by the phenology of the host plants. Moreover, it has been reported that xylophagous beetles show greater activity in the transition between the rainy and dry seasons (Macedo-Reis 2016Macedo-Reis LE (2016) Spatio-temporal distribution of bark and ambrosia beetles in a Brazilian Tropical Dry Forest. Journal Insect of Science 16: 48.; Martínez-Hernández et al. 2019Martínez-Hernández JG, Corona AM, Flores-Palacios A, Rös M & Toledo-Hérnandez V (2019) Seasonal diversity of Cerambycidae (Coleoptera) is more complex than thought: evidence from a tropical dry forest of Mexico. Peer J 7:e7866.). The temporal patterns of the insect feeding guilds present a wide range (Fuentes-Jacques et al. (2022a)Fuentes-Jacques LJ, Hanson-Snortum P, Mehltreter K, Díaz-Castelazo C & Hernández-Ortiz V (2022a) Effects of experimental host-plant switching on the life cycle of a fern spore feeding micromoth of the genus Stathmopoda. Entomologia Experimentalis et Applicata 170: 708-717. but they are often unknown in tropical dry forests.
This type of approach can help to understand the effect of seasonality and how it affects the associations between ferns and insects. It also facilitates the identification of groups that are vulnerable to the effects of global climate change, due to the possible decoupling between the two groups. In this sense, it has been suggested that ferns will present modifications to their distribution range as a result of changes in weather patterns (Reyes-Chávez et al. 2021Reyes-Chávez J, Quail M, Tarvin S, Kessler M & Batke SP (2021) Nowhere to escape - diversity and community composition of ferns and lycophytes on the highest mountain in Honduras. Journal of Tropical Ecology 37: 72-81.; Pie et al. 2022Pie MR, Batke SP, Reyes-Chávez J & Dallimore T (2022) Fern and lycophyte niche displacement under predicted climate change in Honduras. Plant Ecology 223: 613-625.). This could affect the species that are related to the presence of ferns (Pie et al. 2022Pie MR, Batke SP, Reyes-Chávez J & Dallimore T (2022) Fern and lycophyte niche displacement under predicted climate change in Honduras. Plant Ecology 223: 613-625.), such as the different groups of insects (12 orders in this study) that we found associated with this group and which could be affected by the changes in distribution or the extinction of certain fern species that cannot adapt to the new climatic conditions. However, these studies have been conducted in various vegetation types, finding general patterns (Pie et al. 2022Pie MR, Batke SP, Reyes-Chávez J & Dallimore T (2022) Fern and lycophyte niche displacement under predicted climate change in Honduras. Plant Ecology 223: 613-625.; Murakami et al. 2023Murakami M, Batke S, Pie MR & Ramos F (2023) Climate change might lead to substantial niche displacement in one of the most biodiverse regions in the world. Plant Ecology 224: 403-415.) and have not explored highly seasonal tropical forests such as the TDF, which could yield different results from those previously reported. These studies can provide the basis for proposing strategies for the conservation and appropriate management of the TDF, which faces significant anthropic pressure.
Acknowledgements
Thanks to the Commissary of San Andrés de la Cal, Mtro. Elfego Miranda Desaida for granting authorization to carry out this research. Thanks to Magali Silvestre for her support in the field. We wish to thank Clara Hernández and David Tenango for the images of the fern species. We want to thank Dr. Ma. Ventura Rosas-Echeverria and Dr. Antonio López-Carretero for their comments on the manuscript. We thank two anonymous reviewers for their constructive comments that improved the manuscript.
Data availability statement
In accordance with Open Science communication practices, the authors inform that all data are available within the manuscript.
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Publication Dates
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Publication in this collection
01 Dec 2023 -
Date of issue
2023
History
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Received
20 Mar 2023 -
Accepted
22 July 2023