Spatial distribution of Echinolitorina peruviana (Lamarck, 1882) for intertidal rocky shore in Antofagasta (23° S, Chile).

Distribuição espacial de Echinolitorina peruviana (Lamarck, 1882) para costa rochosa entremarés em Antofagasta (23 ° S, Chile)

P. De Los Ríos-Escalante C. Esse C. Stella P. Adikesavan O. Zúñiga About the authors

Abstract

The intertidal rocky shores in continental Chile have high species diversity mainly in northern Chile (18-27° S), and one of the most widespread species is the gastropod Echinolittorina peruviana (Lamarck, 1822). The aim of the present study is do a first characterization of spatial distribution of E. peruviana in along rocky shore in Antofagasta town in northern Chile. Individuals were counted in nine different sites that also were determined their spectral properties using remote sensing techniques (LANDSAT ETM+). The results revealed that sites without marked human intervention have more abundant in comparison to sites located in the town, also in all studied sites was found an aggregated pattern, and in six of these sites were found a negative binomial distribution. The low density related to sites with human intervention is supported when spectral properties for sites were included. These results would agree with other similar results for rocky shore in northern and southern Chile.

Keywords:
Echinolittorina peruviana; rocky shore; intertidal environment; spectral properties; negative binomial distribution

Resumo

As costas rochosas entremarés no Chile continental apresentam alta diversidade de espécies, principalmente no norte do país (18-27 ° S), e uma das espécies mais difundidas é o gastrópode Echinolittorina peruviana (Lamarck, 1822). O objetivo do presente estudo é fazer uma primeira caracterização da distribuição espacial de E. peruviana no costão rochoso da cidade de Antofagasta no norte do Chile. Os indivíduos foram contados em nove locais diferentes onde também foram determinadas suas propriedades espectrais usando técnicas de sensoriamento remoto (LANDSAT ETM +). Os resultados revelaram que os locais sem intervenção humana marcada apresentam maior abundância em comparação aos locais localizados no município. Também em todos os locais estudados foi encontrado um padrão agregado, sendo que em seis desses locais foi encontrada uma distribuição binomial negativa. A baixa densidade relacionada a sites com intervenção humana é suportada quando as propriedades espectrais para sites foram incluídas. Esses resultados concordariam com outros resultados semelhantes para costões rochosos no norte e no sul do Chile.

Palavras-chave:
Echinolittorina peruviana; costão rochoso; ambiente intertidal; propriedades espectrais; distribuição binomial negativa

1. Introduction

The rocky intertidal environments in Chilean coast is characterized by the high species diversity, including molluscs, that has a marked geographic distribution pattern (Santelices, 1992SANTELICES, B., 1992. Algas marinas de Chile. Distribución, ecología, utilización y diversidad. Santiago: Ediciones Pontificia Universidad Católica de Chile.; Broitman et al., 2001BROITMAN, B.R., NAVARRETE, S.A., SMITH, F. and GAINES, S.D., 2001. Geographic variation of southeastern Pacific intertidal communities. Marine Ecology Progress Series, vol. 224, pp. 21-34. http://dx.doi.org/10.3354/meps224021.
http://dx.doi.org/10.3354/meps224021...
; Lee et al., 2008LEE, M.R., CASTILLA, J.C., FERNÁNDEZ, M., CLARKE, M., GONZÁLEZ, C., HERMOSILLA, C., PRADO, L., ROZBACZYLO, N. and VALDOVINOS, C., 2008. Free-living benthic marine invertebrates in Chile. Revista Chilena de Historia Natural, vol. 81, no. 1, pp. 51-67. http://dx.doi.org/10.4067/S0716-078X2008000100005.
http://dx.doi.org/10.4067/S0716-078X2008...
). The rocky shore is markedly exposed to waves among a wide latitudinal gradient in Chile (17-41°S), whereas in extreme southern Chile the coast is characterized by the presence of islands and inner seas with different patterns in species reported (Santelices, 1992SANTELICES, B., 1992. Algas marinas de Chile. Distribución, ecología, utilización y diversidad. Santiago: Ediciones Pontificia Universidad Católica de Chile.; Camus et al., 2013CAMUS, P.A., ARANCIBIA, P.A. and AVILA-THIEME, M.I., 2013. A trophic characterization of intertidal consummers on Chilean rocky shores. Revista de Biología Marina y Oceanografía, vol. 48, no. 3, pp. 431-450. http://dx.doi.org/10.4067/S0718-19572013000300003.
http://dx.doi.org/10.4067/S0718-19572013...
; Velásquez et al., 2016VELÁSQUEZ, C., JARAMILLO, E., CAMUS, P.A., MANZANO, M. and SÁNCHEZ, R., 2016. Biota del intermareal rocoso expuesto de la Isla Grande de Chiloé, Archipiélago de Chiloé, Chile: patrones de diversidad e implicancias ecológicas y biogeográficas. Revista de Biología Marina y Oceanografía, vol. 51, no. 1, pp. 33-50. http://dx.doi.org/10.4067/S0718-19572016000100004.
http://dx.doi.org/10.4067/S0718-19572016...
).

The literature about intertidal invertebrates revealed that these species can have a gregarious behaviour, as protection against drying during low tide, or for efficient use of food resources (Rojas et al., 2000ROJAS, J. M., FARIÑA, J. M., SOTO, R.E. and BOZINOVIC, F., 2000. Variabilidad geográfica en la tolerancia térmica y economía hídrica del gastrópodo intermareal Nodilittorina peruviana (Gastropoda: Littorinidae, Lamarck, 1822). Revista de Chilena de Historia Natural, vol. 73, no. 3, pp. 543-552. http://dx.doi.org/10.4067/S0716-078X2000000300018.
http://dx.doi.org/10.4067/S0716-078X2000...
), many of these species inhabits in rocky cracks or under rocks, or macroalgae basal disks. (Santelices, 1980SANTELICES, B., 1980. Quantitative sampling of intertidal communities in central Chile. Archivos de Biologia y Medicina Experimentales, vol. 13, no. 4, pp. 413-424. PMid:7185325.; Camus and Andrade, 1999CAMUS, P.A. and ANDRADE, Y.N., 1999. Diversidad de comunidades intermareales rocosas del norte de Chile y el efecto potencial de la surgencia costera. Revista Chilena de Historia Natural, vol. 72, no. 3, pp. 389-410.; Cerda and Castilla, 2001CERDA, M.A. and CASTILLA, J.C., 2001. Diversidad y biomasa de macroinvertebrados en matrices intermareales del tunicado Pyura praeputialis (Heller, 1878) en la bahía de Antofagasta, Chile. Revista Chilena de Historia Natural, vol. 74, no. 4, pp. 841-853. http://dx.doi.org/10.4067/S0716-078X2001000400011.
http://dx.doi.org/10.4067/S0716-078X2001...
). Also, the distribution patterns can be affected due the topography of rocky shores, involving recruitment patterns of small gastropods (Underwood, 2004UNDERWOOD, A.J., 2004. Landing on one’s foot: small-scale topographic features of habitat and the dispersion of juvenile intertidal gastropods. Marine Ecology Progress Series, vol. 268, pp. 173-182. http://dx.doi.org/10.3354/meps268173.
http://dx.doi.org/10.3354/meps268173...
). Considering these antecedents, there are interspecific competence between intertidal gastropods and monoplacophora due shelter availabilities (Aguilera and Navarrete, 2011AGUILERA, M.A. and NAVARRETE, S.A., 2011. Distribution and activity patterns in an intertidal grazer assemblage: influence of temporal and spatial organization on interspecific associations. Marine Ecology Progress Series, vol. 431, pp. 119-136. http://dx.doi.org/10.3354/meps09100.
http://dx.doi.org/10.3354/meps09100...
; 2012AGUILERA, M.A. and NAVARRETE, S.A., 2012. Interspecific competition for shelters in territorial and gregarious intertidal grazers: consequences for individual behaviour. PLoS One, vol. 7, no. 9, pp. e46205. http://dx.doi.org/10.1371/journal.pone.0046205. PMid:23049980.
http://dx.doi.org/10.1371/journal.pone.0...
), that can generate that some species can have diurnal or nocturnal activity (Aguilera and Navarrete, 2011AGUILERA, M.A. and NAVARRETE, S.A., 2011. Distribution and activity patterns in an intertidal grazer assemblage: influence of temporal and spatial organization on interspecific associations. Marine Ecology Progress Series, vol. 431, pp. 119-136. http://dx.doi.org/10.3354/meps09100.
http://dx.doi.org/10.3354/meps09100...
).

The northern Chile (18-27° S), is a zone with high species diversity due high productivity of these coasts (Santelices, 1992SANTELICES, B., 1992. Algas marinas de Chile. Distribución, ecología, utilización y diversidad. Santiago: Ediciones Pontificia Universidad Católica de Chile., Camus and Andrade, 1999CAMUS, P.A. and ANDRADE, Y.N., 1999. Diversidad de comunidades intermareales rocosas del norte de Chile y el efecto potencial de la surgencia costera. Revista Chilena de Historia Natural, vol. 72, no. 3, pp. 389-410.), that would have complex trophic interactions between involved species (Camus and Andrade, 1999CAMUS, P.A. and ANDRADE, Y.N., 1999. Diversidad de comunidades intermareales rocosas del norte de Chile y el efecto potencial de la surgencia costera. Revista Chilena de Historia Natural, vol. 72, no. 3, pp. 389-410.), one of the most widespread species is the gastropod Echinolittorina peruviana that inhabits among rocky shores along Chilean territory (Santelices, 1992SANTELICES, B., 1992. Algas marinas de Chile. Distribución, ecología, utilización y diversidad. Santiago: Ediciones Pontificia Universidad Católica de Chile.; Lee et al., 2008LEE, M.R., CASTILLA, J.C., FERNÁNDEZ, M., CLARKE, M., GONZÁLEZ, C., HERMOSILLA, C., PRADO, L., ROZBACZYLO, N. and VALDOVINOS, C., 2008. Free-living benthic marine invertebrates in Chile. Revista Chilena de Historia Natural, vol. 81, no. 1, pp. 51-67. http://dx.doi.org/10.4067/S0716-078X2008000100005.
http://dx.doi.org/10.4067/S0716-078X2008...
), specifically in upper levels (Castillo and Brown, 2010CASTILLO, V.M. and BROWN, D.I., 2010. Echinolittorina peruviana (Lamarck, 1822): antecedentes de la especie. Amici Molluscarum, vol. 18, pp. 39-42.) and southern Perú (Paredes, 1974PAREDES, C., 1974. El modelo de zonación en la orilla rocosa del departamento de Lima. Revista Peruana de Biología, vol. 1, pp. 168-191.; Tejada-Perez et al., 2018TEJADA-PÉREZ, C.A., VILLASANTE, F., LUQUE-FERNÁNDEZ, C. and TEJADA-BEGAZO, C.L., 2018. Mollusk richness and vertical distribution along the rocky shore of Islay, Arequipa, Southern Peru. Journal of Marine and Coastal Sciences, vol. 10, no. 1, pp. 47-66. http://dx.doi.org/10.15359/revmar10-1.4.
http://dx.doi.org/10.15359/revmar10-1.4...
). The aim of the present study is do a first descriptive analysis of E. peruviana adults (10-15 mm total length) in different rocky intertidal environments in Antofagasta town, northern Chile, with the aim of determine the presence of defined spatial distribution patterns.

2. Material and Methods

Field works and study site: the ten sites are located in the coastal town of Antofagasta, northern Chile, six sites are located within town, whereas as external group, was included a four sites in a rocky shore located at 20 km of the town, with low or practically null human intervention (Figure 1, Table 1). The studied sites were visited in summer 2019, for each site, was thrown out random (Ríos and Arancibia, 2018; Ríos and Carreño, 2020), 10 * 10 cm quadrants (n = 40 for each site), considering the relative small size of considered species (Underwood, 2004UNDERWOOD, A.J., 2004. Landing on one’s foot: small-scale topographic features of habitat and the dispersion of juvenile intertidal gastropods. Marine Ecology Progress Series, vol. 268, pp. 173-182. http://dx.doi.org/10.3354/meps268173.
http://dx.doi.org/10.3354/meps268173...
; Underwood and Chapman, 2005UNDERWOOD, A.J. and CHAPMAN, M.G., 2005. Design and analysis in benthic surveys in environmental sampling. In: A. Eleftheriou and A. Mcintyre, eds. Methods for the study of marine benthos. Oxford: Blackwell Science, pp. 1-42.; Ahmad et al., 2011AHMAD, O., FANG, T.P. and YAHYA, K., 2011. Distribution of intertidal organisms in the shores of Teluk Aling, Pulau Pinang, Malaysia. Publications of the Seto Marine Biological Laboratory, vol. 41, pp. 51-61. http://dx.doi.org/10.5134/159483.
http://dx.doi.org/10.5134/159483...
; Ríos and Carreño, 2020).

Table 1
Geographical location, abundance (ind/quadrant; 1 quadrant = 10 x 10 cm), (mean, variance, and mean variance ratio), and reflectance (B1, B2, B3, B4, B5, B6, B7 bands ETM+) values for studied sites.

Spectral properties: Satellite data was obtained from LANDSAT/ETM+ image obtained dated from January 2018 (Table 1) provided by the Land Processes Distributed Active Archive Center (LP DAAC), U.S. Geological Survey (http://LPDAAC.usgs.gov). The bands of visible, near, and mid-infrarred were calibrated radiometrically to spectral irradiance and then to reflectance with atmospheric correction being applied (Table 1).

Data analysis: in a first step, it was compared the E. peruviana abundances for each site, and for two groups of sites, homocedasticity and normality were determined for data, and due the absence of both conditions it was done a non-parametric tests (Zar, 1999ZAR, J., 1999. Biostatistical analysis. New Jersey: Prentice Hall) using software R (R Development Core Team, 2009R DEVELOPMENT CORE TEAM, 2009. R: A language and environment for statistical computing. Version 2.1 [software]. Vienna: R Foundation for Statistical Computing.), Wilcoxon for compare sites with presence or absence of human intervention, and a Kruskall-Wallis for comparison among sites using the PGIRMESS R package (Giraoudoux et al., 2018GIRAOUDOUX, P., ANTONIETTI, J.-P., BEALE, C., PLEYDELL, D. and TREGLIA, M., 2018 [viewed 2 May 2020]. Package: “pgirmess” [online]. Available from https://cran.r-project.org/web/packages/pgirmess/pgirmess.pdf
https://cran.r-project.org/web/packages/...
). For these analyses one site that has E. peruviana absence has not considered.

To each specie counting data, was obtained in first instance a variance mean ratio, first for determine if the specie has random if the value is 1, uniform if the value is lower than 1, or aggregated distribution, if the value is upper than 1, (Brower et al., 1998BROWER, J.E., ZAR, J.H. and VON ENDE, C.N., 1998. Field and laboratory methods for general ecology. 4th ed. Dubuque: WCB McGraw Hill.; Zar, 1999ZAR, J., 1999. Biostatistical analysis. New Jersey: Prentice Hall; Fernandes et al., 2003FERNANDES, M.G., BUSOLI, A.C. and BARBOSA, J.C., 2003. Distribucao espacial de Alabama argillacea (Hubner) (Lepidoptera: Noctuidae) em algodoeiro. Neotropical Entomology, vol. 32, no. 1, pp. 107-115. http://dx.doi.org/10.1590/S1519-566X2003000100016.
http://dx.doi.org/10.1590/S1519-566X2003...
; De Los Ríos Escalante, 2017DE LOS RÍOS ESCALANTE, P., 2017. Non randomness in spatial distribution in two inland water species malacostracans. Journal of King Saud University - Sciences, vol. 29, no. 2, pp. 260-262. http://dx.doi.org/10.1016/j.jksus.2016.12.002.
http://dx.doi.org/10.1016/j.jksus.2016.1...
; De Los Ríos Escalante and Mansilla, 2017DE LOS RÍOS ESCALANTE, P. and MANSILLA, A., 2017. Spatial patterns of Pisidium chilense (Mollusca Bivalvia) and Hyalella patagonica (Crustacea, Amphipoda) in an unpolluted stream in Navarino Island (54° S; Cape Horn Biosphere Reserve). Journal of King Saud University - Sciences, vol. 29, no. 1, pp. 28-31. http://dx.doi.org/10.1016/j.jksus.2016.07.003.
http://dx.doi.org/10.1016/j.jksus.2016.0...
; Ríos and Arancibia, 2018). Once determined the spatial pattern, random, uniform or aggregated, it determined if the species have Poisson, binomial or negative binomial distribution respectively, the analysis was done manually using Excel software and literature descriptions (Zar, 1999ZAR, J., 1999. Biostatistical analysis. New Jersey: Prentice Hall; Fernandes et al., 2003FERNANDES, M.G., BUSOLI, A.C. and BARBOSA, J.C., 2003. Distribucao espacial de Alabama argillacea (Hubner) (Lepidoptera: Noctuidae) em algodoeiro. Neotropical Entomology, vol. 32, no. 1, pp. 107-115. http://dx.doi.org/10.1590/S1519-566X2003000100016.
http://dx.doi.org/10.1590/S1519-566X2003...
; De Los Ríos Escalante, 2017DE LOS RÍOS ESCALANTE, P., 2017. Non randomness in spatial distribution in two inland water species malacostracans. Journal of King Saud University - Sciences, vol. 29, no. 2, pp. 260-262. http://dx.doi.org/10.1016/j.jksus.2016.12.002.
http://dx.doi.org/10.1016/j.jksus.2016.1...
; De Los Ríos Escalante and Mansilla, 2017DE LOS RÍOS ESCALANTE, P. and MANSILLA, A., 2017. Spatial patterns of Pisidium chilense (Mollusca Bivalvia) and Hyalella patagonica (Crustacea, Amphipoda) in an unpolluted stream in Navarino Island (54° S; Cape Horn Biosphere Reserve). Journal of King Saud University - Sciences, vol. 29, no. 1, pp. 28-31. http://dx.doi.org/10.1016/j.jksus.2016.07.003.
http://dx.doi.org/10.1016/j.jksus.2016.0...
; Ríos and Arancibia, 2018). For these analyses one site that has E. peruviana absence has not considered.

Finally, for spectral properties data and E. peruviana abundance mean, a principal component analysis was done using the Factoextra R package (Kassambara and Mundt, 2017KASSAMBARA, A. and MUNDT, F., 2017. [viewed 2 May 2020]. Package “factoextra” [online]. Available from https://cran.r-project.org/web/packages/factoextra/factoextra.pdf
https://cran.r-project.org/web/packages/...
) with the aim of determine potential grouping patterns in studied sites.

3. Results

The obtained results revealed that the sites without human intervention have marked high abundances in comparison to sites located in the town, and the results of spatial distribution, revealed the presence of aggregated pattern for eight sites, and one site with uniform distribution (Barrio Histórico) (Table 1). The results revealed that seven sites has negative binomial distribution, and only two sites (Caleta Coloso and El Lenguado 1) have not negative binomial distribution (Figure 2).

Figure 2
Graphs of distributional patterns for E. peruviana included in the present study.

The results of correlation matrix only show significant correlations between abundances with B2, B3, B4 and B5 reflectances, B1 with B3, B4 with B2, B4 with B3, B5 with B3, B5 with B4, B6 with B4, B6 with B5, B7 with B4, B7 with B5, and B7 with B6 (Table 2). The results of PCA revealed that abundances are the main factor is abundances (Table 3), and for axis 1 the main factors are all reflectance values, whereas for the axis 2 the main factor is the abundance of E. peruviana (Figure 3). Finally, the PCA results revealed the existence of two main groups, the first group corresponded to sites with high reflectance and low abundances (El Lenguado 1, El Lenguado 2, El Lenguado 3), and one site with relative low abundance (El Lenguado 4)(Figure 3). The second group joined sites with low reflectance, corresponded to sites with marked human intervention and low abundances (Trocadero 2, Carboncillo, Barrio Histórico, Las Garumas, Coloso), and one site with high abundance (Trocadero 1)(Figure 3).

Table 2
Correlation matrix for variables included in the present study, “p” values lower than 0.05 denotes significant associations.
Table 3
Eigenvalue for considered sites in the present study.
Figure 3
PCA results for spectral properties and E. peruviana abundances in sites included in the present study.

The heat map obtained from PCA, revealed two main groups, one that has sites Trocadero 1, Coloso (with human intervention), Lenguado 1, Lenguado 2 and Lenguado 3 (these three without human intervention). The second group has one main sub-group with human intervention (Trocadero 2, Carboncillo, Barrio Histórico), one without human intervention (El Lenguado 4), and finally one with human intervention (Las Garumas)(Figure 4).

Figure 4
Heat map of PCA for spectral properties and E. peruviana abundances in sites included in the present study.

4. Discussion

The results of abundances, would indicate that many of the studied sites with high E. peruviana abundances corresponded to low or null human intervention, that is associated to low reflectance (El Lenguado 1, El Lenguado 2, El Lenguado 3 and El Lenguado 4) whereas sites located in the town at north, have high reflectance and low E. peruviana abundances (Trocadero 1, Trocadero 2, El Carboncillo, Barrio Histórico), finally an intermediate situation would occur in sites with human intervention with high reflectance and low E. peruviana abundance (Coloso) and absence (Las Garumas). The marked differences between sites with different kind of human intervention, in studied sites probably is due to the presence of Pyura praeputialis that is a kind of key species that regulate the species composition in rocky shores in northern Chile (Castilla et al., 2004CASTILLA, J.C., LAGOS, N.A. and CERDA, M., 2004. Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Marine Ecology Progress Series, vol. 268, pp. 119-130. http://dx.doi.org/10.3354/meps268119.
http://dx.doi.org/10.3354/meps268119...
), in this context, in the present study the human altered sites have not P. praeputialis. Also, the low abundances in sites with marked human intervention agree with results for central Chilean rocky shore (Durán and Castilla, 1989DURAN, L.R. and CASTILLA, J.C., 1989. Variation and persistence of the middle rocky intertidal community of central Chile, with and without human harvesting. Marine Biology, vol. 103, pp. 555-562. http://dx.doi.org/10.1007/BF00399588.
http://dx.doi.org/10.1007/BF00399588...
) that is similar to the observations for European rocky shore (Stevčić et al., 2018STEVČIĆ, C., PEREZ-MIGUEL, M., DRAKE, P., TOVAR-SANCHEZ, A. and CUESTA, J.A., 2018. Macroinvertebrate communities on rocky shores: impact due to human visitors. Estuarine, Coastal and Shelf Science, vol. 211, pp. 127-136. http://dx.doi.org/10.1016/j.ecss.2017.11.026.
http://dx.doi.org/10.1016/j.ecss.2017.11...
) and Arabian Sea in India (Pandey et al., 2018PANDEY, V., THIRUCHITRAMBALAM, G. and SATYAM, K., 2018. Habitat heterogeneity determines structural properties of intertidal gastropod assemblages in a pristine tropical island ecosystem. Indian Journal of Geo-Marine Sciences, vol. 47, no. 4, pp. 846-853.; Savurirajan et al., 2018SAVURIRAJAN, M., EQUBAL, J., LAKRA, R.K., SATYAM, K. and THIRUCHITRAMBALAM, G., 2018. Species diversity and distribution of seagrasses from the South Andaman, Andaman and Nicobar Islands, India. Botanica Marina, vol. 61, no. 3, pp. 225-234. http://dx.doi.org/10.1515/bot-2017-0109.
http://dx.doi.org/10.1515/bot-2017-0109...
)

The results about negative binomial distribution agree with similar observations for inland water benthic invertebrates (Gray, 2005GRAY, B.R., 2005. Selecting a distributional assumption for modeling relative densities of benthic macroinvertebrates. Ecological Modelling, vol. 185, no. 1, pp. 1-12. http://dx.doi.org/10.1016/j.ecolmodel.2004.11.006.
http://dx.doi.org/10.1016/j.ecolmodel.20...
; De Los Ríos Escalante, 2017DE LOS RÍOS ESCALANTE, P., 2017. Non randomness in spatial distribution in two inland water species malacostracans. Journal of King Saud University - Sciences, vol. 29, no. 2, pp. 260-262. http://dx.doi.org/10.1016/j.jksus.2016.12.002.
http://dx.doi.org/10.1016/j.jksus.2016.1...
; De Los Ríos Escalante and Mansilla, 2017DE LOS RÍOS ESCALANTE, P. and MANSILLA, A., 2017. Spatial patterns of Pisidium chilense (Mollusca Bivalvia) and Hyalella patagonica (Crustacea, Amphipoda) in an unpolluted stream in Navarino Island (54° S; Cape Horn Biosphere Reserve). Journal of King Saud University - Sciences, vol. 29, no. 1, pp. 28-31. http://dx.doi.org/10.1016/j.jksus.2016.07.003.
http://dx.doi.org/10.1016/j.jksus.2016.0...
; Ríos and Arancibia, 2018). Also, in recent studies, it has described the use of negative binomial distribution for intertidal environments, specifically in middle intertidal zone, in rocky shores without seaweeds, similar to sites in the present study (Philippe et al., 2016PHILIPPE, A.S., PINAUD, D., CAYATTE, M.-L., GOULEVANT, C., LACHAUSSÉE, N., PINEAU, P., KARPYTCHEV, M. and BOCHER, P., 2016. Influence of environmental gradients on the distribution of benthic resources available for shorebirds on intertidal mudflats of Yves Bay, France. Estuarine, Coastal and Shelf Science, vol. 174, pp. 71-81. http://dx.doi.org/10.1016/j.ecss.2016.03.013.
http://dx.doi.org/10.1016/j.ecss.2016.03...
; Checon et al., 2017CHECON, H.H., CORTE, G.N., SILVA, C.F., SCHAEFFER-NOVELLI, Y. and AMARAL, A.C.Z., 2017. Mangrove vegetation decreases density but does not affect species richness and trophic structure of intertidal polychaete assemblages. Hydrobiologia, vol. 795, no. 1, pp. 169-179. http://dx.doi.org/10.1007/s10750-017-3128-0.
http://dx.doi.org/10.1007/s10750-017-312...
; Sibaja-Cordero, 2018SIBAJA-CORDERO, J.A., 2018. Spatial distribution of macrofauna within a sandy beach on the Caribbean coast of Costa Rica. Revista de Biología Tropical, vol. 66, no. 1-1, pp. S176-S186.; Ríos and Arancibia, 2018). In this context Rojas et al. (2000)ROJAS, J. M., FARIÑA, J. M., SOTO, R.E. and BOZINOVIC, F., 2000. Variabilidad geográfica en la tolerancia térmica y economía hídrica del gastrópodo intermareal Nodilittorina peruviana (Gastropoda: Littorinidae, Lamarck, 1822). Revista de Chilena de Historia Natural, vol. 73, no. 3, pp. 543-552. http://dx.doi.org/10.4067/S0716-078X2000000300018.
http://dx.doi.org/10.4067/S0716-078X2000...
studied the aggregated pattern of intertidal gastropod Nodolittorina peruviana, nevertheless they did not focus in interpretative equations for explain its absolute abundance, but they remark the role of aggregation behaviour for avoid dehydration during low tide. Similar description was done in the first studies on intertidal decapods (Bahamonde and López, 1969BAHAMONDE, N. and LÓPEZ, M.T., 1969. Cyclograpsus cinereus Dana, en biocenosis supramareales de Chile. Boletin Mensual del Museo Nacional de Historia Natural. Santiago: Museo Nacional de Historia Natural.). The literature for other similar ecosystems proposed as survival strategy the joining of groups for avoid dehydration due temperature increase at low tide (Atta et al., 2014ATTA, M.H., MUJAHID, A., and CHAGHTAI, F., 2014. Population density of Cellana and Acmea (Mollusca: Gastropoda) at various tidal zones on the rocky coast of Manora, Karachi, Pakistan. International Journal of Biological Research, vol. 2, no. 2, pp. 143-146.; Shanks et al., 2014SHANKS, A.L., WALSER, A. and SHANKS, L., 2014. Population structure, northern range limit, and recruitment variation in the intertidal limpet Lottia scabra. Marine Biology, vol. 161, no. 5, pp. 1073-1086. http://dx.doi.org/10.1007/s00227-014-2400-3.
http://dx.doi.org/10.1007/s00227-014-240...
; Mortensen and Dunphy, 2016MORTENSEN, B.J.D. and DUNPHY, B.J., 2016. Effect of tidal regime on the thermal tolerance of the marine gastropod Lunella smaragda (Gmelin, 1791). Journal of Thermal Biology, vol. 60, pp. 186-194. http://dx.doi.org/10.1016/j.jtherbio.2016.07.009. PMid:27503732.
http://dx.doi.org/10.1016/j.jtherbio.201...
). About the absence of negative binomial distribution observed in sites such as Caleta Coloso and El Lenguado 1 would be probably to interspecific behaviour mediated probably by topographic differences (Underwood, 2004UNDERWOOD, A.J., 2004. Landing on one’s foot: small-scale topographic features of habitat and the dispersion of juvenile intertidal gastropods. Marine Ecology Progress Series, vol. 268, pp. 173-182. http://dx.doi.org/10.3354/meps268173.
http://dx.doi.org/10.3354/meps268173...
), that would provide shelters for optimizate the use of trophic resources (Hidalgo et al., 2008HIDALGO, F.J., FIRSTATER, F.N., FANJUL, E., BAZTERRICA, M.C., LOMOVASKY, B.J., TARAZONA, J. and IRIBARNE, O.O., 2008. Grazing effects of periwinkle Echinolittorina peruviana at a central Peruvian high rocky intertidal. Helgoland Marine Research, vol. 62, pp. 73-83. http://dx.doi.org/10.1007/s10152-007-0086-3.
http://dx.doi.org/10.1007/s10152-007-008...
; Aguilera and Navarrete, 2011AGUILERA, M.A. and NAVARRETE, S.A., 2011. Distribution and activity patterns in an intertidal grazer assemblage: influence of temporal and spatial organization on interspecific associations. Marine Ecology Progress Series, vol. 431, pp. 119-136. http://dx.doi.org/10.3354/meps09100.
http://dx.doi.org/10.3354/meps09100...
, 2012AGUILERA, M.A. and NAVARRETE, S.A., 2012. Interspecific competition for shelters in territorial and gregarious intertidal grazers: consequences for individual behaviour. PLoS One, vol. 7, no. 9, pp. e46205. http://dx.doi.org/10.1371/journal.pone.0046205. PMid:23049980.
http://dx.doi.org/10.1371/journal.pone.0...
).

Other important factor that would explain differences in aggregated pattern probably would be the insolation exposure that would generate dehydration stress, this condition was studied for other gastropods of the Littorinidae family (Erlandsson et al., 1999ERLANDSSON, J., KOSTYLEV, V. and ROLÁN-ALVAREZ, E., 1999. Mate search and aggregation behaviour in the Galician hybrid zone of Littorina saxatilis. Journal of Evolutionary Biology, vol. 12, no. 5, pp. 891-896. http://dx.doi.org/10.1046/j.1420-9101.1999.00087.x.
http://dx.doi.org/10.1046/j.1420-9101.19...
; Lauzon-Guay and Scheibling, 2009LAUZON-GUAY, J.-S. and SCHEIBLING, R.E., 2009. Food dependent movement of periwinkles (Littorina littorea) associated with feeding fronts. Journal of Shellfish Research, vol. 28, no. 3, pp. 581-587. http://dx.doi.org/10.2983/035.028.0322.
http://dx.doi.org/10.2983/035.028.0322...
; Miller and Denny, 2011MILLER, L.P. and DENNY, M.W., 2011. Importance of behaviour and morphological traits for controlling body temperature in littorinid snails. The Biological Bulletin, vol. 220, no. 3, pp. 209-223. http://dx.doi.org/10.1086/BBLv220n3p209. PMid:21712229.
http://dx.doi.org/10.1086/BBLv220n3p209...
; Rickards and Boulding, 2015RICKARDS, K.J.C. and BOULDING, E.G., 2015. Effects of temperature and humidity on activity and microhabitat selection by Littorina subrotundata. Marine Ecology Progress Series, vol. 537, pp. 163-173. http://dx.doi.org/10.3354/meps11427.
http://dx.doi.org/10.3354/meps11427...
), including E. peruviana (Muñoz et al., 2008MUÑOZ, J.L.P., CAMUS, P.A., LABRA, F.A., FINKE, G.R. and BOZINOVIC, F., 2008. Thermal constraints on daily patterns of aggregation and density along an intertidal gradient in the periwinkle Echinolittorina peruviana. Journal of Thermal Biology, vol. 33, no. 3, pp. 149-156. http://dx.doi.org/10.1016/j.jtherbio.2007.10.002.
http://dx.doi.org/10.1016/j.jtherbio.200...
). Also, the topographical differences in rocky shores, can generate sites with different insolation or wave gradient exposure that would regulate the aggregated pattern of the individuals (Lauzon-Guay and Scheibling, 2009LAUZON-GUAY, J.-S. and SCHEIBLING, R.E., 2009. Food dependent movement of periwinkles (Littorina littorea) associated with feeding fronts. Journal of Shellfish Research, vol. 28, no. 3, pp. 581-587. http://dx.doi.org/10.2983/035.028.0322.
http://dx.doi.org/10.2983/035.028.0322...
). If it integrated these antecedents, the study site is characterized by irregularities in topography in rocky shores, and wave exposure that would generate a complex scenario that would have consequences in aggregation patterns in intertidal marine invertebrates (Guiller, 1959GUILLER, E.R., 1959. Intertidal belt-forming species on the rocky coast of northern Chile. Papers and Proceedings of the Royal Society of Tasmania, vol. 93, pp. 33-58.; Pacheco and Castilla, 2000PACHECO, C.J. and CASTILLA, J.C., 2000. Ecología trófica de los ostreros Haematopus palliatus pitanay (Murphy 1925) and Haematopus ater (Vieillot et Oudart 1825) en mantos del tunicado Pyura praeputialis (Heller 1878) en la Bahía de Antofagasta, Chile. Revista Chilena de Historia Natural, vol. 73, no. 3, pp. 533-541. http://dx.doi.org/10.4067/S0716-078X2000000300017.
http://dx.doi.org/10.4067/S0716-078X2000...
).

As conclusion it suggests do more ecological studies considering the importance of the marine invertebrates in these ecosystems as important preys for littoral fishes and/or marine birds, that would understand the ecological community structure and process in Chilean rocky shores.

Acknowledgements

The present study was founded by projects Tides Grant Foundation TRF13-03011 MECESUP UCT 0804, Technical Faculty, and the Research Direction of the Catholic University of Temuco. M.I. and S.M.A. are acknowledged for her valuable comments that helped improve the manuscript.

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Publication Dates

  • Publication in this collection
    20 Aug 2021
  • Date of issue
    2023

History

  • Received
    22 Dec 2020
  • Accepted
    10 Feb 2021
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