Insects associated to ephemeral pools in Huentelauquén (29ºS Coquimbo Region, Chile)

Insetos associados a lagoas temporárias em Huentelauquén (29ºS Região de Coquimbo, Chile)

J. Pizarro-Araya F.M. Alfaro P. De Los Ríos-Escalante About the authors

Abstract

In northern central Chile, ephemeral pools constitute shallow isolated water bodies with a favourable habitat for fauna adapted to seasonal changes. Based on the limited knowledge about the fauna—particularly insects—associated to these ecosystems, the objective of this study was to characterize the richness, composition, structure and similarity of the insect communities associated with ephemeral pools in Huentelauquén (29º S, Coquimbo Region, Chile). By using pitfall traps, 10,762 individuals were captured, represented by 7 orders, 27 families, and 51 species. Coleoptera and Hymenoptera were the best represented orders, with Neuroptera, Orthoptera and Plecoptera being poorly represented groups. The non-parametric estimators evaluated showed wealth values above those observed for all the studied pools, and their accumulation curves suggest the existence of an incomplete species inventory in the studied community. Additionally, the hierarchical and ordering analysis showed groupings of pools located in the northwest and southeast of Huentelauquén. Preliminarily we found a negative correlation between the area of the pools and the richness (species) and abundance of insects. Additional studies (on other arthropod groups and other seasons of the year) could provide a better understanding of the local processes of extinction and colonization of the species inhabiting these fragile coastal environments.

Keywords:
arid zones; coastal desert; coastal wetlands; insect communities; species richness

Resumo

No norte central do Chile, lagoas efêmeras constituem corpos de água isolados e pouco profundos, com um habitat favorável para a fauna adaptada as mudanças sazonais que as zonas úmidas estão sujeitas. Com relação a estes ecossistemas, sabe-se pouco sobre sua fauna, principalmente a de insetos. O objetivo do presente estudo foi caracterizar a riqueza, composição, estrutura e similaridade das comunidades de insetos que habitam as lagoas temporárias de Huentelauquén (29º S, Região de Coquimbo, Chile). Usando armadilhas de interceptação, se capturou um total de 10.762 indivíduos, pertencentes a 7 ordens, 27 famílias e 51 espécies. Coleoptera e Hymenoptera foram as ordens mais representativas, enquanto Neuroptera, Orthoptera e Plecoptera foram grupos pouco representativos. Os estimadores não paramétricos avaliados mostraram valores de riqueza superiores ao observados para todas as lagoas estudadas, e suas curvas de acumulação parecem indicar que o inventario da comunidade estudada está incompleto. A análise hierárquica e de ordenamento revelou agrupamentos de lagoas correspondentes a zona nordeste e sudeste de Huentelauquén. Preliminarmente encontramos uma correlação negativa entre a área de lagoas efêmeras e a riqueza (espécies) e abundância de insetos. É necessário realizar estudos adicionais (sobre outros grupos de artrópodes e em outras estações do ano) para melhor compreensão dos processos locais de extinção e colonização das espécies que habitam estes frágeis ambientes costeiros estudados.

Palavras-chave:
zonas áridas; deserto costeiro; zonas úmidas costeiras; comunidades de insetos; riqueza de espécies

1. Introduction

The coastal areas of northern Chile have different ecological and geomorphological zones (Abreu and Bannon, 1993ABREU, M.L. and BANNON, P.R., 1993. Dynamics of the South American coastal desert. Journal of the Atmospheric Sciences, vol. 50, no. 17, pp. 2952-2964. http://dx.doi.org/10.1175/1520-0469(1993)050<2952:DOTSAC>2.0.CO;2.
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; Villagrán, 2001VILLAGRÁN, C., 2001. Un modelo de la historia de la vegetación de la Cordillera de la Costa de Chile central-sur: la hipótesis glacial de Darwin. Revista Chilena de Historia Natural, vol. 74, no. 4, pp. 793-803. http://dx.doi.org/10.4067/S0716-078X2001000400007.
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; Smith-Ramírez et al., 2005SMITH-RAMÍREZ, C., ARMESTO, J.J. and VALDOVINOS, C., 2005. Historia, biodiversidad y ecología de los bosques costeros de Chile. Santiago: Editorial Universitaria, 708 p.) that support a wide variety of habitats conditioned by the maritime influence and aridity (Ormazábal, 1993ORMAZÁBAL, C.S., 1993. The conservation of biodiversity in Chile. Revista Chilena de Historia Natural, vol. 66, pp. 383-402.; Gajardo, 1993GAJARDO, R., 1993. La vegetación natural de Chile. Clasificación y distribución geográfica. Santiago: Editorial Universitaria, 165 p.). In these areas there have been relict zones with biotic components from the Tertiary period, which have affected species distribution and favoured the emergence of endemic species (Jerez, 2005JEREZ, V., 2005. Patrones de diversidad de Chrysomelidae (Insecta- Coleoptera) en la Cordillera de la Costa de Chile central y sur. In: C. SMITH-RAMÍREZ, J.J. ARMESTO and C.C. VALDOVINOS, eds. Historia, biodiversidad y ecología de los bosques costeros de Chile. Santiago: Editorial Universitaria, pp. 340-351.; Villagrán and Armesto, 2005VILLAGRÁN, C. and ARMESTO, J.J., 2005. Fitogeografía histórica de la Cordillera de la Costa de Chile. In: C. SMITH-RAMÍREZ, J.J. ARMESTO and C. VALDOVINOS, eds. Biodiversidad y ecología de los bosques costeros de Chile. Santiago: Editorial Universitaria, pp. 99-116.; Smith-Ramírez et al., 2005SMITH-RAMÍREZ, C., ARMESTO, J.J. and VALDOVINOS, C., 2005. Historia, biodiversidad y ecología de los bosques costeros de Chile. Santiago: Editorial Universitaria, 708 p.; Arroyo et al., 2006ARROYO, M.T.K., MARQUET, P.A., MARTICORENA, C., SIMONETTI, J.A., CAVIERES, L.A., SQUEO, F.A., ROZZI, R. and MASSARDO, F., 2006. El hotspot chileno, prioridad mundial para la conservación. Diversidad de ecosistemas, ecosistemas terrestres. In: Comisión Nacional del Medio Ambiente (CHILE), org. Diversidad de Chile: patrimonios y desafíos. Santiago: Comisión Nacional del Medio Ambiente, pp. 94-97.).

These coastal zones are considered important due to their diversity and endemism and, consequently, for biological conservation (Smith-Ramírez et al., 2005SMITH-RAMÍREZ, C., ARMESTO, J.J. and VALDOVINOS, C., 2005. Historia, biodiversidad y ecología de los bosques costeros de Chile. Santiago: Editorial Universitaria, 708 p.), and are included in an important hotspot for Chile (Cowling et al., 1996COWLING, R.M., RUNDEL, P.W., LAMONT, B.B., ARROYO, M.T.K. and ARIANOUTSOU, M., 1996. Plant diversity in Mediterranean-climate regions. Trends in Ecology & Evolution, vol. 11, no. 9, pp. 362- 366. http://dx.doi.org/10.1016/0169-5347(96)10044-6. PMid:21237880.
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; Gaston, 2000GASTON, K.J., 2000. Global patterns in biodiversity. Nature, vol. 405, no. 6783, pp. 220-227. http://dx.doi.org/10.1038/35012228. PMid:10821282.
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; Lamoreux et al., 2006LAMOREUX, J.F., MORRISON, J.C., RICKETTS, T.H., OLSON, D.M., DINERSTEIN, E., MCKNIGHT, M.W. and SHUGART, H.H., 2006. Global tests of biodiversity concordance and the importance of endemism. Nature, vol. 440, no. 7081, pp. 212-214. http://dx.doi.org/10.1038/nature04291. PMid:16382239.
http://dx.doi.org/10.1038/nature04291...
). In addition, as a result of its latitudinal position, the coastal area of Central Chile is affected by the ENSO phenomenon (El Niño Southern Oscillation) (Romero and Garrido, 1985ROMERO, H. and GARRIDO, A.M., 1985. Influencias genéticas del fenómeno El Niño sobre los patrones climáticos de Chile. Investigación Pesquera Chile, vol. 32, pp. 19-35.; Cepeda-Pizarro et al., 2005aCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005a. Composición y abundancia de artrópodos epígeos del Parque Nacional Llanos de Challe: impactos del ENOS de 1997 y efectos del hábitat pedológico. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 635-650. http://dx.doi.org/10.4067/S0716-078X2005000400004.
http://dx.doi.org/10.4067/S0716-078X2005...
, bCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005b. Variación en la abundancia de Arthropoda en un transecto latitudinal del desierto costero transicional de Chile, con énfasis en los tenebriónidos epígeos. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 651-663. http://dx.doi.org/10.4067/S0716-078X2005000400005.
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), as well as by the potential effects of global climate change (Schlesinger and Mitchell, 1987SCHLESINGER, M.E. and MITCHELL, J.B.F., 1987. Climatic model simulations of the equilibrium climatic response to increased carbon dioxide. Reviews of Geophysics, vol. 25, no. 4, pp. 760-798. http://dx.doi.org/10.1029/RG025i004p00760.
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; Mooney et al., 2001MOONEY, H.A., ARROYO, M.T.K., BOND, W.J., HOBBS, R.J., LAVOREL, S. and NEILSON, R.P., 2001. Mediterranean ecosystems. In: O. SALA and F.S. CHAPIN, eds. Global change scenarios. New York: Springer-Verlag, pp. 157-198.).

The first reports of aquatic insects inhabiting ephemeral pools in Chile in terms of structure and function were documented in Andean pools of Tambo-Puquios (29°45’ S; Cepeda-Pizarro and Pola, 2013CEPEDA-PIZARRO, J. and POLA, M., 2013. Relaciones de abundancia de órdenes de hexápodos terrestres en vegas altoandinas del desierto-transicional de Chile. Idesia, vol. 31, no. 2, pp. 31-39. http://dx.doi.org/10.4067/S0718-34292013000200005.
http://dx.doi.org/10.4067/S0718-34292013...
; Cepeda-Pizarro et al., 2006aCEPEDA-PIZARRO, J., SQUEO, F.A., CORTÉS, M., OYARZÚN, J. and ZAVALA, H., 2006a. La biota del humedal Tambo-Puquíos. In: J. CEPEDA-PIZARRO, ed. Geoecología de los Andes desérticos. La alta montaña del Valle del Elqui. La Serena: Ediciones Universidad de La Serena, pp. 243-283.; Cepeda-Pizarro et al., 2006bCEPEDA-PIZARRO, J., POLA, M., ZULETA, C. and GONZÁLEZ, C.R. 2006b. Relaciones de abundancia y diversidad de la entomofauna del humedal Tambo-Puquíos. In: J. CEPEDA-PIZARRO, ed. Geoecología de los Andes desérticos. La alta montaña del Valle del Elqui. La Serena: Ediciones Universidad de La Serena, pp. 475-521.; Cepeda-Pizarro et al., 2013CEPEDA-PIZARRO, J., GONZÁLEZ, C.R., ZULETA, C. and PIZARRO-ARAYA, J., 2013. Comparación de la eficiencia de trampas Barber y Malaise para el estudio de la biodiversidad de Hexapoda de vegas altoandinas. Idesia, vol. 31, no. 4, pp. 103-109. http://dx.doi.org/10.4067/S0718-34292013000400014.
http://dx.doi.org/10.4067/S0718-34292013...
; Cepeda-Pizarro et al., 2015aCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and MORALES, M.C., 2015a. Invertebrates inhabiting temporary ponds found in the Tambo-Puquíos wet pasture (Andes of north-central Chile), and the physicochemical characteristics of their habitat. Idesia, vol. 33, no. 4, pp. 55-64. http://dx.doi.org/10.4067/S0718-34292015000400008.
http://dx.doi.org/10.4067/S0718-34292015...
, bCEPEDA-PIZARRO, J., POLA, M. and GONZÁLEZ, C.R., 2015b. Efecto de la fase fenológica de verano sobre algunas características del ensamble de Diptera registrado en una vega altoandina del desierto transicional de Chile. Idesia, vol. 33, no. 1, pp. 49-58. http://dx.doi.org/10.4067/S0718-34292015000100006.
http://dx.doi.org/10.4067/S0718-34292015...
; Cepeda-Pizarro et al., 2016CEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and GONZÁLEZ, C.R., 2016. Efecto de la condición hídrica de vegas altoandinas del desierto transicional de Chile sobre algunas características comunitarias de su Dipterofauna. Idesia, vol. 34, no. 1, pp. 7-18. http://dx.doi.org/10.4067/S0718-34292016000100002.
http://dx.doi.org/10.4067/S0718-34292016...
), where 14 insects orders were reported in addition to other taxa, such as cladocerans, copepods, and ostracods. In these pools marked seasonal and spatial variation were reported (Cepeda-Pizarro et al., 2016CEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and GONZÁLEZ, C.R., 2016. Efecto de la condición hídrica de vegas altoandinas del desierto transicional de Chile sobre algunas características comunitarias de su Dipterofauna. Idesia, vol. 34, no. 1, pp. 7-18. http://dx.doi.org/10.4067/S0718-34292016000100002.
http://dx.doi.org/10.4067/S0718-34292016...
). Currently, there are no studies accounting for the diversity and structure of the arthropod assemblages of ephemeral pools in the coastal desert of Chile. Therefore, the aim of this study is to conduct a first characterization of the insects communities in ephemeral pools of northern Chile, more specifically in the plains of Huentelauquén (29° S, Coquimbo region), originating from the southern autumn and winter rains (Zuleta and Piñones, 2014ZULETA, C. and PIÑONES, C., 2014. Diagnóstico de Conservación y Valoración de Macrohábitats del Secano Costero de Huentelauquén (Canela, región de Coquimbo, Chile). La Serena: Informe Técnico Final. Universidad de La Serena-Ministerio de Medio Ambiente.; Zuleta and Piñones, 2015ZULETA, C. and PIÑONES, C. 2015. Secano costero de Huentelauquén. Paisajes y presencia humana. La Serena: Ediciones Universidad de La Serena, 177 p.; De Los Ríos-Escalante et al., 2019DE LOS RÍOS-ESCALANTE, P., PIZARRO-ARAYA, J., ALFARO, F.M. and ZULETA, C., 2019. First descriptions of aquatic crustaceans in coastal plains in northern Chile (Huentelauquén, 31°S, Coquimbo region, Chile. Crustaceana, vol. 92, no. 1, pp. 73-81. http://dx.doi.org/10.1163/15685403-00003825.
http://dx.doi.org/10.1163/15685403-00003...
; Sigvardt et al., 2019SIGVARDT, Z.M.S., ROGERS, D.C., DE LOS RÍOS-ESCALANTE, P., PALERO, F. and OLESEN, J., 2019. First molecular phylogeny of Laevicaudata (Crustacea, Branchipoda) with description of a new species of Lynceus from Chile and an updated key to species in the Americas. Invertebrate Systematics, vol. 33, no. 4, pp. 597-617. http://dx.doi.org/10.1071/IS18073.
http://dx.doi.org/10.1071/IS18073...
; Zuleta et al., 2019ZULETA, C., CEA, A., BRAVO-NARANJO, V., CASTILLO, R., ROBLES, M., PIZARRO-ARAYA, J., ALFARO, F.M., PIÑONES, C., DE LOS RÍOS-ESCALANTE, P. and MUÑOZ, G., 2019. Charcas temporales del secano costero de Huentelauquén. In: C. ZULETA and M. CONTRERAS-LÓPEZ, eds. Humedales costeros de la región de Coquimbo: biodiversidad, vulnerabilidades y conservación. La Serena: Editorial Universidad de La Serena, pp. 144-184.).

2. Material and Methods

2.1. Study area

The study site encompassed the locality of Huentelauquén in the Coquimbo region, Chile, located in the Choapa river basin, a zone under marine and fluvial influence (Castillo and Robles, 2012CASTILLO, R. and ROBLES, M., 2012. Geomorfología costera de Huentelauquén y ecotopos adyacentes. La Serena: Universidad de La Serena.). The study was conducted in the semiarid plains of a Ramsar site called “Las Salinas de Huentelauquén”, located 40 km north of the town of Los Vilos (Figure 1) and in coastal terrace/plains located near 5 km SE (around of 31°35'45"S, 71°30'30"W) . The weather is Mediterranean, with a nine-month dry season with many cloudy days, and an annual average precipitation of 130 mm (Novoa and Villaseca, 1989NOVOA, R. and VILLASECA, S., 1989. Mapa agroclimático de Chile. Santiago: Instituto de Investigaciones Agropecuarias (INIA), 221 p.). This site is inserted in a transition area between steppe shrubs and shrubs and trees (Chang et al., 1989CHANG, A., DROULLY, P., PALMA, S., RODRÍGUEZ, M. and VILINA, Y., 1989. Prospección de Áreas de Concentración de Fauna entre la I a VII Región. Santiago: FAO-CHI.; Gajardo, 1993GAJARDO, R., 1993. La vegetación natural de Chile. Clasificación y distribución geográfica. Santiago: Editorial Universitaria, 165 p.; Cepeda-Pizarro et al., 2000CEPEDA-PIZARRO, J., ZULETA, C. and OSORIO, R. 2000. Región de Coquimbo: biodiversidad y ecosistemas terrestres. La Serena: Ediciones Universidad de La Serena.). The flora species that have been reported for this area include Echinopsis skottsbergii (Backb.) H. Friedrich and G.D. Rowley, Heliotropium stenophyllum Hook. et Arn., Senna cumingii (Hook. et Arn.) Irwing et Barneby, Chuquiraga ulicina (Hook. et Arn.), Frankenia chilensis K. Presl., Baccharis macraei (Hook. et Arn.), Bahia ambrosioides Lag., Haplopappus foliosus DC., and Margyricarpus pinnatus (Lam.) Kuntze (Cea and Zuleta, 2016CEA, A. and ZULETA, C., 2016. Componente vegetal de las lagunas temporales en Huentelauquén (Canela-Choapa, Región de Coquimbo). La Serena: Universidad de La Serena.; Cea et al., 2019CEA, A., MARTÍNEZ-TILLERÍA, K.P., PASTÉN, V. and OSORIO, R., 2019. Flora y vegetación de los humedales costeros de Coquimbo. In: C. ZULETA and M. CONTRERAS-LÓPEZ, ed. Humedales costeros de la Región de Coquimbo: Biodiversidad, Vulnerabilidades and Conservación. La Serena: Editorial Universidad de La Serena, pp. 80-98.). The aquatic flora is characterized by the presence of Poaceae (Cea and Zuleta, 2016CEA, A. and ZULETA, C., 2016. Componente vegetal de las lagunas temporales en Huentelauquén (Canela-Choapa, Región de Coquimbo). La Serena: Universidad de La Serena.), a frequent family in ephemeral pools (Bliss et al., 1998BLISS, S.A., ZEDLER, P.H., KEELEY, J.E. and ARROYO, M.T.K., 1998. A floristic survey of the temporary wetlands in the mediterranean-climate region of Chile. In: A.J. MCCOMB and J.A. DAVIS, ed. Wetlands for the future. Adelaide: Gleneagles Publishing, pp. 219-228.; Álvarez et al., 2012ÁLVAREZ, M., SAN MARTÍN, J. and DEIL, U., 2012. Nanism and ephemerism as reason for a hidden abundance in vernal pool plants: the example of Lepuropetalon spathulatum in Chile. Feddes Repertorium, vol. 123, no. 1, pp. 55-66. http://dx.doi.org/10.1002/fedr.201200016.
http://dx.doi.org/10.1002/fedr.201200016...
). In this site, we studied a series of ephemeral pools with shallow and variable water levels subject to the rainfall conditions (Table 1, Figure 2). All the studied water pools were georeferenced using a satellite navigator (e-Trex 30, Personal Navigator, Garmin). The data were captured in decimal degrees using DATUM WGS84 and downloaded using MapSource 3.0. Based on this information, a grid was prepared using ArcGIS 9.3 with Add XY Data and projected to UTM 19S DATUM WGS84.

Figure 1
Map showing the geographic location of the ephemeral pools studied in Huentelauquén (Coquimbo Region, Chile).The numbers represent the pools as in Table 1.
Table 1
Geographical location and physical characteristics of the ephemeral pools studied in Huentelauquén (Coquimbo Region, Chile).
Figure 2
Panoramic views of the Huentelauquén ephemeral pools (Coquimbo Region, Chile). (A) pool 3 located in the north of Huentelauquén; (B) installation of pitfall traps in pool 5; (C) pool 6 in a coastal dune; (D) pool 7 located in the southeast of Huentelauquén; (E) pool 8 located in the southeast of Huentelauquén; (F) pool 9 located in the southeast of Huentelauquén.

2.2. Data collection, sample processing and identification of insects

The specimens were collected using pitfalls traps following Cepeda-Pizarro et al. (2005aCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005a. Composición y abundancia de artrópodos epígeos del Parque Nacional Llanos de Challe: impactos del ENOS de 1997 y efectos del hábitat pedológico. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 635-650. http://dx.doi.org/10.4067/S0716-078X2005000400004.
http://dx.doi.org/10.4067/S0716-078X2005...
, bCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005b. Variación en la abundancia de Arthropoda en un transecto latitudinal del desierto costero transicional de Chile, con énfasis en los tenebriónidos epígeos. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 651-663. http://dx.doi.org/10.4067/S0716-078X2005000400005.
http://dx.doi.org/10.4067/S0716-078X2005...
). For each site, a grid was installed consisting of 4 x 5 m sites with 20 traps each. The traps were installed between October 15 and October 18, 2015. The captured material was removed, cleaned and preserved in alcohol (70%) until the moment of processing. For the taxonomic identification at a generic and specific level, specialized literature was used. The collected specimens were deposited in the entomological collection of the Ecological Entomology Laboratory of the University of La Serena (LEULS, La Serena, Chile).

2.3. Statistical analysis

To estimate species richness, the smoothed richness accumulation curves for the non-parametric estimators ACE, Chao 1, Jackknife first order (Jack 1) and Bootstrap were analysed. (Colwell, 2013COLWELL, R.K., 2013. EstimateS. Version 9.1.0. Storrs: Department of Ecology and Evolutionary Biology, University of Connecticut.). ACE is based on the abundances of species with ten or less individuals in the sample, whereas Chao 1 is based on rare species found in the sample. Jack 1 is based on the number of species present in one sampling unit, whereas the bootstrap estimator is based on the proportion of sampling units containing each species. The non-parametric estimators do not require special assumptions as parametric estimators do—calculation is easy and effective (Escalante, 2003ESCALANTE, T., 2003. ¿Cuántas especies hay?: los estimadores no paramétricos de Chao. Elementos, vol. 52, pp. 53-56.). These estimators are universally valid for any species abundance distribution and more robust than parametric estimators based on species abundance (Chao and Chiu, 2016CHAO, A. and CHIU, C.H., 2016. Nonparametric estimation and comparison of species richness. Els, pp. 1-11. http://dx.doi.org/10.1002/9780470015902.a0026329.
http://dx.doi.org/10.1002/9780470015902....
). All of these estimators were calculated using EstimateS version 9.10 (Colwell, 2013COLWELL, R.K., 2013. EstimateS. Version 9.1.0. Storrs: Department of Ecology and Evolutionary Biology, University of Connecticut.). To calculate the structuration grade for each habitat (pool), a similarity join analysis or cluster analysis was done based on the Bray-Curtis index. To analyse the structure of the insect communities associated with the pools, a non-metric multidimensional scaling analysis (NMDS) was done using the similarity Bray-Curtis index. Finally, a correlation matrix was developed using Spearman’s rank correlation coefficient (r) to compare the richness and abundance of insects with some physical characteristics of pools (area, altitude, max deep). The similitude, ordering and correlation analysis were performed using RStudio 1.2.5033 (RStudio Team, 2021RSTUDIO TEAM, 2021. [viewed 21 December 2021] RStudio: Integrated Development for R. RStudio [online]. Boston: RStudio. Available from: http://www.rstudio.com/.
http://www.rstudio.com/...
).

A species absence/presence matrix was constructed, with the species in rows and the sites in columns. We calculated the Checkerboard score (“C-score”), which is a quantitative index of occurrence that measures the extent to which species co-occur less frequently than what is expected by chance (Gotelli, 2000GOTELLI, N.J., 2000. Null model analysis of species co-occurrence patterns. Ecology, vol. 81, no. 9, pp. 2606-2621. http://dx.doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2000...
). A community is structured by competition when the C-score is significantly larger than the value expected by chance (Gotelli, 2000GOTELLI, N.J., 2000. Null model analysis of species co-occurrence patterns. Ecology, vol. 81, no. 9, pp. 2606-2621. http://dx.doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2000...
; Tondoh, 2006TONDOH, J.E., 2006. Seasonal changes in earthworm diversity and community structure in Central Côte d’Ivoire. European Journal of Soil Biology, vol. 42, pp. s334-s340. http://dx.doi.org/10.1016/j.ejsobi.2006.09.003.
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; Tiho and Josens, 2007TIHO, S. and JOSENS, G., 2007. Co-occurrence of earth worms in urban surroundings: a null model analysis of community structure. European Journal of Soil Biology, vol. 43, no. 2, pp. 84-90. http://dx.doi.org/10.1016/j.ejsobi.2006.10.004.
http://dx.doi.org/10.1016/j.ejsobi.2006....
). In addition, we compared co-occurrence patterns with null expectations via simulation. Gotelli and Ellison (2013)GOTELLI, N.J. and ELLISON, A.M., 2013 [viewed 21 December 2021] EcoSimR 1.00. 2013 [online]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html
http://www.uvm.edu/~ngotelli/EcoSim/EcoS...
proposed the fixed-effects model as a statistical null model. In this model, the sums of the rows and columns of the matrix are preserved such that each random community contains the same number of species as the original community (fixed column) and each species occurs with the same frequency as in the original community (fixed row).

Niche overlap and separation in the insect communities were analyzed using a null model based on Pianka’s overlap index with retained niche breadth and reshuffled zero states. The null model analyses were performed using RStudio 1.2.5033 (RStudio Team, 2021RSTUDIO TEAM, 2021. [viewed 21 December 2021] RStudio: Integrated Development for R. RStudio [online]. Boston: RStudio. Available from: http://www.rstudio.com/.
http://www.rstudio.com/...
) and the package EcosimR version 7.0 (Gotelli and Ellison, 2013GOTELLI, N.J. and ELLISON, A.M., 2013 [viewed 21 December 2021] EcoSimR 1.00. 2013 [online]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html
http://www.uvm.edu/~ngotelli/EcoSim/EcoS...
; Carvajal-Quintero et al., 2015CARVAJAL-QUINTERO, J.D., ESCOBAR, F., ALVARADO, F., VILLA-NAVARRO, F.A., JARAMILLO-VILLA, Ú. and MALDONADO-OCAMPO, J.A., 2015. Variation in freshwater fish assemblages along a regional elevation gradient in the northern Andes, Colombia. Ecology and Evolution, vol. 5, no. 13, pp. 2608-2620. http://dx.doi.org/10.1002/ece3.1539. PMid:26257874.
http://dx.doi.org/10.1002/ece3.1539...
). The EcosimR program also determines whether the measured overlap values differ from what would be expected in a random sampling of the species data. EcosimR performs Monte Carlo randomisations to create pseudo-communities and then statistically compares the patterns of these randomised communities with those in the real data matrix (Gotelli and Ellison, 2013GOTELLI, N.J. and ELLISON, A.M., 2013 [viewed 21 December 2021] EcoSimR 1.00. 2013 [online]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html
http://www.uvm.edu/~ngotelli/EcoSim/EcoS...
). In our analysis, all the values in the general matrix were randomised 1,000 times and the niche breadth was retained for each species; in this way, the algorithm retained the total amount of specialization for each species (Gotelli and Ellison, 2013GOTELLI, N.J. and ELLISON, A.M., 2013 [viewed 21 December 2021] EcoSimR 1.00. 2013 [online]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html
http://www.uvm.edu/~ngotelli/EcoSim/EcoS...
; Carvajal-Quintero et al., 2015CARVAJAL-QUINTERO, J.D., ESCOBAR, F., ALVARADO, F., VILLA-NAVARRO, F.A., JARAMILLO-VILLA, Ú. and MALDONADO-OCAMPO, J.A., 2015. Variation in freshwater fish assemblages along a regional elevation gradient in the northern Andes, Colombia. Ecology and Evolution, vol. 5, no. 13, pp. 2608-2620. http://dx.doi.org/10.1002/ece3.1539. PMid:26257874.
http://dx.doi.org/10.1002/ece3.1539...
). Finally, an analysis was conducted based on the unified neutral theory of biodiversity (Hubbell, 2001HUBBELL, S.P. 2001. The unified theory of biodiversity and biogeography. Princeton: Princeton University Press. 375 p.) using the R package UNTB (Hankin, 2018HANKIN, R.K.S., 2018 [viewed 21 December 2021] Package “untb” [online]. Available from: https://cran.r-project.org/web/packages/untb/untb.pdf
https://cran.r-project.org/web/packages/...
). For this analysis, we used the θ estimator and conducted a Preston analysis.

3. Results

A total of 10,762 individuals were captured, belonging to 7 orders, 26 families, and 51 species (Table 2). The highest species richness was found in the two and seven pool, both with 24 species, whereas the lowest value was observed in the fifth pool, with 13 species (Figure 3). The exclusive species number was different for each ephemeral pool studied and three species (i.e., Bembidion (Notaphus) sp., Pachymorphus sp. and Plecoptera sp. larva) were present at all sites (Table 2)

Table 2
Taxonomic composition and abundance (n) of Insecta for the ephemeral pools studied in Huentelauquén (Coquimbo Region, Chile).
Figure 3
Number of species, families and orders of insects associated with ephemeral pools in Huentelauquén (Coquimbo Region, Chile).

Among the insect groups, the orders with the highest number of taxa were Coleoptera (17 families, 37 genus, and 39 species) and Hymenoptera (2 families, 4 genus, and 4 species), whereas those with the lowest were Neuroptera, Orthoptera, and Plecoptera (Table 2). Within Coleoptera, the families with the highest number of species were, in decreasing order, Tenebrionidae, Carabidae, and Curculionidae. Families with only one species included Anthicidae, Coccinellidae, Cryptophagidae, Dytiscidae, Erotylidae, Heteroceridae, Hidrophylidae, Hydraenidae, Latridiidae, Scarabaeidae, and Trogossitidae (Table 2).

The non-parametric estimators produced estimated total richness values higher than the values observed (Figure 4). For example, the estimator Chao 1 estimated a high number of rare species (singletons and doubletons) for the set of pools under study (see Figure 4); these species belonged mainly to Coleoptera (see Table 2).

Figure 4
Smoothed richness accumulation curves for the non-parametric estimators ACE, Chao 1, Jack 1, and Bootstrap, for insects associated with ephemeral pools in Huentelauquén.

The most abundant species were Collembolla sp. 1 (26.2% of total captured), Plecoptera sp. (larvae) (16.2%), and Arthrobrachus limbatus Solier, 1849 (15.7%) (Table 2). Overall, the highest relative abundances occurred in the second (20.5% of total captured), the seventh (17.3%), the third pool (13.8%), and the eight pool (13.6%) (Table 2). Although the second pool does not have a large surface area, it shows a high richness and abundance in comparison to the ninth pool, which has the largest surface area (see Table 1).

The cluster analysis showed high similarity between the first and fourth pools, and the seventh to ninth pools (more than 60% similarity) (Figure 5). The first group is located in the north of Huentelauquén and was characterized by the dominance of A. limbatus and Collembola sp. 2, whereas the second group is located in the south-east of this locality and was characterized by the almost exclusive dominance of Collembola sp. 1 (see Table 2). The non-metric multidimensional scaling analysis showed relative correspondence between the similarities identified in the cluster analysis. Nevertheless, the most notable similarity was observed in pools located southeast of Huentelauquén (seventh to ninth pool) (Figure 6), which are the habitats with the largest surface area included in the present study (see Figure 1).

Figure 5
Dendrogram of cluster analysis based on Bray-Curtis similarity for the ephemeral pools of Huentelauquén.
Figure 6
Non-metric multidimensional scaling analysis (NMDS) using the similarity Bray-Curtis index for the ephemeral pools of Huentelauquén.

Only richness (species) (r = -0.66, p = 0.02) and abundance (r = -0.44, p = 0.02) were negatively correlated with the area of the pools. No significant correlations were observed when analyzing the altitude and maximum depth of the pools (Figure 7).

Figure 7
Spearman's correlation matrix. Values (r) show the positive or negative correlation between richness (species and families) and abundance of insects and some physical characteristics of pools (area, altitude, maximum depth). *Significant at 0.05.

The co-occurrence species and niche-sharing analysis revealed that the species associations reported were not structured, which means the absence of patterns between species associations and niche overlapping (Table 3). The results of the analyses based on unified neutral theory of biodiversity revealed low species number, with an optimal θ of 6.581, respectively, and a singletons number of 16.

Table 3
Results of the null model of species co-occurrence and niche sharing for the species and sites included in the present study.

4. Discussion

The insect assemblage associated to ephemeral pools included native species that are widely distributed in the Chilean coastal desert, such as Camponotus morosus (Formicidae), a native species with wide distribution in sclerophyllous shrubs in central Chile and generalist feeding behaviour (Snelling and Hunt, 1975SNELLING, R.R. and HUNT, J.H., 1975. The ants of Chile (Hymenoptera: formicidae). Revista Chilena de Entomologia, vol. 9, pp. 63-129.; Grez et al., 1986GREZ, A.A., SIMONETTI, J.A. and IPINZA-REGLA, J.H., 1986. Hábitos alimenticios de Camponotus morosus (Smith, 1858) (Hymenoptera: Formicidae) en Chile central. Revista Chilena de Entomologia, vol. 13, pp. 51-54.); and Gyriosomus foveopunctatus (Tenebrionidae), a darkling beetle typical from inner steppe shrubs (Pizarro-Araya and Jerez, 2004PIZARRO-ARAYA, J. and JEREZ, V., 2004. Distribución geográfica del género Gyriosomus Guérin-Méneville, 1834 (Coleoptera: Tenebrionidae): una aproximación biogeográfica. Revista Chilena de Historia Natural, vol. 77, no. 3, pp. 491-500. http://dx.doi.org/10.4067/S0716-078X2004000300008.
http://dx.doi.org/10.4067/S0716-078X2004...
). The shared species of Carabidae (see Table 2) have a wide distribution in continental Chile (Roig-Juñent and Domínguez, 2001ROIG-JUÑENT, S. and DOMÍNGUEZ, M.C., 2001. Diversidad de la familia Carabidae (Coleoptera) en Chile. Revista Chilena de Historia Natural, vol. 74, no. 3, pp. 549-571. http://dx.doi.org/10.4067/S0716-078X2001000300006.
http://dx.doi.org/10.4067/S0716-078X2001...
).

Even though several insect groups characteristic of the coastal scrub were recorded, the species accumulation curves did not reach a defined asymptote, which suggests that the species inventory of the studied communities is incomplete (Escalante, 2003ESCALANTE, T., 2003. ¿Cuántas especies hay?: los estimadores no paramétricos de Chao. Elementos, vol. 52, pp. 53-56.; Alfaro and Pizarro-Araya, 2017ALFARO, F.M. and PIZARRO-ARAYA, J., 2017. Estimación de la riqueza de coleópteros epigeos de la Reserva Nacional Pingüino de Humboldt (Regiones de Atacama y Coquimbo, Chile). Gayana, vol. 81, no. 2, pp. 39-51. http://dx.doi.org/10.4067/S0717-65382017000200039.
http://dx.doi.org/10.4067/S0717-65382017...
).

Preliminarily we found a negative correlation between the area of the pools and the richness (species) and abundance of insects. These observations are in stark contrast with the increase in the number of species resulting from increased habitat size, a very common phenomenon observed in ecology (Rosenzweig, 1995ROSENZWEIG, M., 1995. Species diversity in space and time. New York: Cambridge University Press. 436 p. http://dx.doi.org/10.1017/CBO9780511623387.
http://dx.doi.org/10.1017/CBO97805116233...
). Even though coastal shrub-type vegetation dominates all the studied sites, it is likely that the presence of insect species is conditioned by the characteristics of the microhabitat around the area of the pools. Nevertheless, additional samplings in other seasons are necessary to test these ecological hypotheses at a local level, as well as it is also necessary to evaluate how the structure of the habitat, floristic richness and the connectivity between pools could explain the structure of the insect community in these environments (Tornero et al., 2016TORNERO, I., SALA, J., GASCÓN, S., ÀVILA, N., QUINTANA, X.D. and BOIX, D., 2016. Pond size effect on macrofauna community structure in a highly connected pond network. Limnetica, vol. 35, no. 2, pp. 337-354. http://dx.doi.org/10.23818/limn.35.27.
http://dx.doi.org/10.23818/limn.35.27...
; Heino et al., 2017HEINO, J., BINI, L.M., ANDERSSON, J., BERGSTEN, J., BJELKE, U. and JOHANSSON, F., 2017. Unravelling the correlates of species richness and ecological uniqueness in a metacommunity of urban pond insects. Ecological Indicators, vol. 73, pp. 422-431. http://dx.doi.org/10.1016/j.ecolind.2016.10.006.
http://dx.doi.org/10.1016/j.ecolind.2016...
).

Some groups, such as Collembola (see Table 2), require wet edaphic conditions to complete their biological cycles (Cepeda-Pizarro and Pola, 2013CEPEDA-PIZARRO, J. and POLA, M., 2013. Relaciones de abundancia de órdenes de hexápodos terrestres en vegas altoandinas del desierto-transicional de Chile. Idesia, vol. 31, no. 2, pp. 31-39. http://dx.doi.org/10.4067/S0718-34292013000200005.
http://dx.doi.org/10.4067/S0718-34292013...
), and their diversity and abundance patterns in arid environments may be determined by soil humidity (Cepeda-Pizarro and Whitford, 1989CEPEDA-PIZARRO, J. and WHITFORD, W.G., 1989. The relationships between abiotic factors and the abundance patterns of soil microarthropods on a desert watershed. Pedobiologia, vol. 33, pp. 76-86.). The dominance of some Collembola species in these pools could be explained by the higher humidity conditions observed in the surrounding microhabitat of these water bodies, however it was not a general pattern for all the pools studied (see Table 2). Although pitfall traps are directed to walking insects (Cepeda-Pizarro et al., 2005aCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005a. Composición y abundancia de artrópodos epígeos del Parque Nacional Llanos de Challe: impactos del ENOS de 1997 y efectos del hábitat pedológico. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 635-650. http://dx.doi.org/10.4067/S0716-078X2005000400004.
http://dx.doi.org/10.4067/S0716-078X2005...
, bCEPEDA-PIZARRO, J., PIZARRO-ARAYA, J. and VÁSQUEZ, H., 2005b. Variación en la abundancia de Arthropoda en un transecto latitudinal del desierto costero transicional de Chile, con énfasis en los tenebriónidos epígeos. Revista Chilena de Historia Natural, vol. 78, no. 4, pp. 651-663. http://dx.doi.org/10.4067/S0716-078X2005000400005.
http://dx.doi.org/10.4067/S0716-078X2005...
), and these have been used for studying tenebrionids (Coleoptera) in arid zones (Cepeda-Pizarro, 1989CEPEDA-PIZARRO, J., 1989. Actividad temporal de tenebriónidos epígeos (Coleoptera) y su relación con la vegetación arbustiva en un ecosistema árido de Chile. Revista Chilena de Historia Natural, vol. 62, pp. 115-125.; Alfaro et al., 2009ALFARO, F.M., PIZARRO-ARAYA, J. and FLORES, G.E., 2009. Epigean tenebrionids (Coleoptera: Tenebrionidae) from the Choros Archipelago (Coquimbo Region, Chile). Entomological News, vol. 120, no. 2, pp. 125-130. http://dx.doi.org/10.3157/021.120.0201.
http://dx.doi.org/10.3157/021.120.0201...
, 2016ALFARO, F.M., PIZARRO-ARAYA, J. and FLORES, G.E., 2016. Composición y estructura del ensamble de tenebriónidos epigeos (Coleoptera: Tenebrionidae) de ecosistemas continentales e insulares del desierto costero transicional de Chile. Revista Mexicana de Biodiversidad, vol. 87, no. 4, pp. 1283-1291. http://dx.doi.org/10.1016/j.rmb.2016.09.001.
http://dx.doi.org/10.1016/j.rmb.2016.09....
), they can also be used to capture flying and phytophage insects (Pietruszka, 1980PIETRUSZKA, R.D., 1980. Observations on seasonal variation in desert arthropods in central Nevada. The Great Basin Naturalist, vol. 40, no. 3, pp. 292-297.). In all studied pools a high number of Plecoptera (stoneflies) with this sampling method was observed. Although little is known about the biology of these groups in Chile, the aquatic nymphs of these species are dominant components in trophic networks of temperate freshwater ecosystems (Stewart, 2009STEWART, K.W., 2009. Plecoptera: Stoneflies. In: V.H. RESH and R.T. CARDE, eds. Encyclopedia of insects. Cambridge: Academic Press, pp. 810-813. http://dx.doi.org/10.1016/B978-0-12-374144-8.00214-9.
http://dx.doi.org/10.1016/B978-0-12-3741...
) and in some cases both their larvae and eggs can survive desiccation as survival strategy in habitats with intermittent conditions (McRoberts and Grubbs, 2021MCROBERTS, T.C. and GRUBBS, S., 2021. Effects of stream permanence on stonefly (Insecta, Plecoptera) community structure at Mammoth Cave National Park, Kentucky, USA. Biodiversity Data Journal, vol. 9, pp. e62242. http://dx.doi.org/10.3897/BDJ.9.e62242. PMid:33746535.
http://dx.doi.org/10.3897/BDJ.9.e62242...
).

In spite of the differences in the number of species reported, the random associations found between species is a result of the presence of many repeated species in the studied sites (Tondoh, 2006TONDOH, J.E., 2006. Seasonal changes in earthworm diversity and community structure in Central Côte d’Ivoire. European Journal of Soil Biology, vol. 42, pp. s334-s340. http://dx.doi.org/10.1016/j.ejsobi.2006.09.003.
http://dx.doi.org/10.1016/j.ejsobi.2006....
; Tiho and Josens, 2007TIHO, S. and JOSENS, G., 2007. Co-occurrence of earth worms in urban surroundings: a null model analysis of community structure. European Journal of Soil Biology, vol. 43, no. 2, pp. 84-90. http://dx.doi.org/10.1016/j.ejsobi.2006.10.004.
http://dx.doi.org/10.1016/j.ejsobi.2006....
), which is a very frequent phenomenon in the analysis of inland water communities in Chile. The present study is relevant because it is the first to include terrestrial insects, additional to a previous study on aquatic crustaceans (De Los Ríos-Escalante et al., 2019DE LOS RÍOS-ESCALANTE, P., PIZARRO-ARAYA, J., ALFARO, F.M. and ZULETA, C., 2019. First descriptions of aquatic crustaceans in coastal plains in northern Chile (Huentelauquén, 31°S, Coquimbo region, Chile. Crustaceana, vol. 92, no. 1, pp. 73-81. http://dx.doi.org/10.1163/15685403-00003825.
http://dx.doi.org/10.1163/15685403-00003...
), because both groups probably would have potential interactions that would regulate the presence and absence of the species in each habitat (Vega et al., 2020VEGA, R., DE LOS RÍOS-ESCALANTE, P., ENCINA, F., NORAMBUENA, J.A., BARILE, J. and MARDONES, A., 2020. First report of inventory and role of macroinvertebrate and fish in Cautin river (38º S, Araucania region, Chile). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 80, no. 1, pp. 215-228. http://dx.doi.org/10.1590/1519-6984.203511. PMid:31066767.
http://dx.doi.org/10.1590/1519-6984.2035...
). However, more detailed studies would be necessary to assess trophic interactions and interspecific competition in these coastal ecosystems.

The analysis based on unified neutral theory of biodiversity showed a number of species so high that each species would virtually be represented by a single individual (Hubbell, 2001HUBBELL, S.P. 2001. The unified theory of biodiversity and biogeography. Princeton: Princeton University Press. 375 p.; Hankin, 2018HANKIN, R.K.S., 2018 [viewed 21 December 2021] Package “untb” [online]. Available from: https://cran.r-project.org/web/packages/untb/untb.pdf
https://cran.r-project.org/web/packages/...
). The trend observed in the results is similar to that observed in zooplankton metacommunities in shallow water bodies (Sokol et al., 2015SOKOL, E.R., BROWN, B.L., CAREY, C.C., TORNWALL, B.M., SWAN, C.M. and BARRETT, J.E., 2015. Linking management to biodiversity in built ponds using metacommunity similations. Ecological Modelling, vol. 296, pp. 36-45. http://dx.doi.org/10.1016/j.ecolmodel.2014.10.022.
http://dx.doi.org/10.1016/j.ecolmodel.20...
), and to the existence of many repeated species in the studied sites (Rosindell et al., 2015ROSINDELL, J., HARMON, L.J. and ETIENNE, R.S., 2015. Unifying ecology and macroevolution with individual-based theory. Ecology Letters, vol. 18, no. 5, pp. 472-482. http://dx.doi.org/10.1111/ele.12430. PMid:25818618.
http://dx.doi.org/10.1111/ele.12430...
; Overcast et al., 2019OVERCAST, I., EMERSON, B.C. and HICKERSON, M.J., 2019. An integrated model of population genetics and community ecology. Journal of Biogeography, vol. 46, no. 4, pp. 816-829. http://dx.doi.org/10.1111/jbi.13541.
http://dx.doi.org/10.1111/jbi.13541...
).

In conclusion, the results suggest the existence of habitats with high species richness at the contour of ephemeral pools, where the studied pools represent metacommunities with their respective metapopulations. Considering the seasonality of these habitats, the presence and abundance of species is likely determined by colonization and microhabitat structure around the pools. To better understand the processes and factors influencing on the species inhabiting the studied sites, additional studies including absolute abundances of other invertebrates, such as crustaceans, as well as seasonal studies in other years are needed.

Acknowledgements

The authors would like to thank the community of Huentelauquén, mainly Gabriela Muñoz and Luis Guerra, for providing facilities to conduct field work, as well as Alberto Castex for its photography assistance (fundacion-indomita.org/) and Rodrigo Muñoz for their assistance in field work. This study was funded by projects FPA-NAC-I-032-2015 (FPA, MMA, Carlos Zuleta) and DIDULS PR2121210 (Universidad de La Serena, JPA), and MECESUP UCT 0804 (Universidad Católica de Temuco, PDE). PDE would like to thank M.I. and S.M.A for their valuable suggestions for improving the manuscript.

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Publication Dates

  • Publication in this collection
    10 Jan 2022
  • Date of issue
    2024

History

  • Received
    09 July 2021
  • Accepted
    04 Oct 2021
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