MOLLUSCAN ASSEMBLAGES IN ROCK POOLS ON SANDSTONE REEFS: LOCAL AND BETWEEN POOLS VARIABILITY.
Rocky pools are eroded depressions that occur in different types of rock and are frequent in sandstone, limestone, and granite (Ganning 1971. Brendonck et al. 2016). In intertidal zones, rocky pools retain seawater at low tide and are home to marine organism communities (Legrand et al. 2018), acting as a microcosm of marine life in this region (Matthews-Cascon & Lotufo 2006). Although the communities of rock pools are less studied than those of the emergent substrata of rocky intertidal environments, there has been growing interest in determining the biotic and abiotic factors which structure them (Metaxas & Scheibling 1993, Araujo et al. 2006, Brendonck et al. 2015, Bezerra et al. 2017). Despite this, most studies are on ichthyofauna (Davis 2000, Meager et al. 2005, Cunha et al. 2008, Godinho & Lotufo 2010, Chargulaf et al. 2011, Machado et al. 2015, Lobato et al. 2016, Bezerra et al. 2017). with few publications on the molluscan assemblages that occur there (Underwood 1976. Breves & Moraes 2014).
Organisms that live at the boundary between land and sea are exposed to consecutive periods of emersion and immersion (Stephenson & Stephenson 1949, Coutinho et al. 2016). During low tides, although rock pool organisms do not face emersion, they are subjected to varying environmental parameters such as temperature, salinity, oxygen, carbon dioxide, and pH (Ganning 1971, Metaxas & Scheibling 1993, Legrand et al. 2018). Pools farther from the ocean are exposed to longer periods of emersion and, therefore, experience greater variability in environmental conditions (Huggett & Griffiths 1986, Martins et al. 2007). Also, smaller pools experience more extreme environmental conditions because a smaller volume of water is more susceptible to such fluctuations (Bennett & Griffiths 1984, Martins et al. 2007). Thus, the distance between the pool and the ocean and pool size influence its biological composition (Martins et al. 2007).
In addition to effects of pool size on environmental fluctuations, there is the general principle that the number of species increases continuously as the area increases (Arrhenius 1921). This principle is often attributed to the explanation that larger areas contain more individuals, increasing the probability of finding greater species richness (Coleman 1981, Palmer & White 1994, Lomolino 2000, Matias et al. 2010). Moreover, larger areas have a greater diversity of ecological niches and contribute to the variation of species richness (Ricklefs & Lovette 1999). Patch size may also affect colonization patterns (Dye 1993), recruitment (Dudgeon & Petraitis 2001), and the intensity of biological interactions (Keough 1984). Hence, size of rock pools may influence community structure, with effects on the number of species present (Underwood & Skilleter 1996, Martins et al. 2007).
Studies on molluscs in rock pools have evaluated grazing intensity (Noel et al. 2009), nutrient and sediment effects (Atalah & Crowe 2010), and trophic relationships (Masterson et al. 2008, Breves & Moraes 2014). Therefore, there is no evidence that the distribution of molluscan assemblages of rock pools is influenced by the pool size.
The aim of this study was to analyze the molluscan assemblages on sandstone reefs at three different beaches in Ceara State in northeast Brazil, investigating their variation among sites and the sizes of the rock pools. The sampling design allowed for the testing of differences in the ecological descriptors and abundance of individual taxa between sites and between pools.
MATERIALS AND METHODS
Field collections were conducted on sandstone reefs at three different beaches on the northwest coast of Ceara in northeast Brazil (Fig. 1).
Common coastal features are the sandstone reefs with flat surfaces that are tilted slightly seaward (Morais 1967). These reefs differ from a typical rocky shore mainly in their gentle slope and sandstone composition (Rabelo et al. 2015). The reefs of Pedra Rachada (3[degrees] 23' S, 39[degrees] 00' O), Pacheco (3[degrees] 41' S, 38[degrees] 38' W), and Dois Coqueiros (3[degrees] 41' S, 38[degrees] 36' W) were chosen because of the abundance of rock pools of varying sizes and accessibility by land. The rocky beds of these reefs consist mainly of sandstone, calcium carbonate, and iron oxide (Godinho & Lotufo 2010).
Tides are semidiurnal with a maximum tidal amplitude of about 3.5 m and a minimum of -0.1 m. During spring low tides, the intertidal zone is exposed for about 3 h. Samplings were carried out during low tide, when the pools were completely isolated from the ocean and from each other. The tide pools analyzed in this study were generally characterized by rock bottom, presence of sand, small boulders, and walls partially covered by macroalgae. The 30 pools studied were randomly selected at low tide.
The following abiotic variables were measured: surface area, average depth, and volume of pools and pool--ocean distance. Hereafter, surface area, average depth, and volume of pools will be referred as size parameters. The molluscan assemblages were characterized by ecological descriptors. Therefore, the biotic variables were abundance, species richness, Shannon--Wiener diversity, and Pielou's evenness index.
A prospection was carried out to identify the presence and location of rock pools in each reef. Only pools with well-defined limits were registered, with no direct connection to other pools or to the ocean during low tide. Ten pools were randomly selected in each reef for this study.
Size parameters were measured to determine their effect on the structure of molluscan assemblages. Pool size was measured using a ruler. Length was measured at the greatest extent of the pool and the width was measured perpendicular to the midpoint of length axis. Length and width were used to calculate the surface area assuming an elliptical shape (Castellanos-Galindo et al. 2005). The mean depth was estimated from three measurements taken at points equidistant along the length axis (Cunha et al. 2008). Volume was estimated by multiplying the surface area by the mean depth (Castellanos-Galindo et al. 2005, Cunha et al. 2008). The lowest pool--ocean distance was calculated (Netto et al. 2003, Madeira & Joyeux 2011. White et al. 2015) using the geographic coordinates of each pool in Google Earth software.
The malacofauna present in the pool were manually removed using forceps and spatula and washed in a 0.5-mm mesh sieve. Infaunal molluscs were not considered in this study. Loose blocks (pebbles and stones) were turned over to ensure the removal of all organisms. Larger animals, such as octopuses and sea slugs (Aplysia spp.), were photographed but were not collected. The malacofauna were packed in plastic bags for transport to the laboratory where they were refrigerated for 24 h and then fixed in 70% ethanol. The molluscs were examined under a stereoscopic microscope and identified to the lowest possible taxonomic level.
The size parameters of the pools and the ecological descriptors of the molluscan assemblages were characterized by descriptive statistics (median, mean, and SD).
Analyses of variance (ANOVAs) were performed to test size parameter variation and assemblage descriptors between sites. Each was based on a one-way model. When significance was identified, a Tukey test was used to evaluate differences between pairs of means. The assumptions of normality and homogeneity of variance were tested before all analyses using Shapiro--Wilk and Levene tests, respectively. When necessary, data were log (x + 1) transformed to remove heterogeneous variances. In cases where homogeneity was not achieved, the tests were run on the raw data using a conservative significance level (P < 0.01) (Underwood 1997, Borthagaray & Carranza 2007, Scrosati et al. 2011, Bertocci et al. 2012).
Pools showed continuous variation in size parameters. Hence, rather than a factorial design using distinct size categories, a regression approach was adopted using continuous variations of these variables (Martins et al. 2007, Gotelli & Ellison 2011).
A linear regression analysis was used to evaluate the effect of the size parameters of the pools on molluscan assemblage descriptors. This analysis was performed independently for surface, depth, volume, and pool--ocean distance (Martins et al. 2007). The effects of the size parameters on the abundance of the most relevant species were also analyzed through regressions. Normality and multicollinearity assumptions were tested before using the Shapiro--Wilk test and variance inflation factors, respectively (Fox & Monette 1992, Fox & Weisberg 2018).
The SIMPER (SIMilarity PERcentage) procedure (Clarke 1993) was used to identify the per cent contribution (%) of each taxon to the measures of Bray-Curtis dissimilarity between groups. A taxon was considered important if its contribution to the total dissimilarity percentage was greater than or equal to 3% (Bertocci et al. 2012). A species with a consistently high contribution to dissimilarity between groups is a good species for discriminating patterns (Clarke & Warwick 2001). The abundances of relevant taxa (according to SIMPER results) were examined using a regression analysis (between pools) and an ANOVA (between sites), according to the same models mentioned previously.
All statistical tests were performed with software R version 1.1.453 (R Development Core Team, Boston, MA) (RStudio Team 2016).
The 30 rock pools studied at Pedra Rachada (P1PR, P2PR, P3PR, P4PR, P5PR, P6PR, P7PR, P8PR, P9PR, and P10PR), Pacheco (P1PA, P2PA, P3PA, P4PA, P5PA, P6PA, P7PA, P8PA, P9PA, and P10PA), and Dois Coqueiros (P1DC, P2DC, P3DC, P4DC, P5DC, P6DC, P7DC, P8DC, P9DC, and P10DC) had different amplitudes for all size parameters (Fig. 2A-D). By contrast, the differences in depth ([F.sub.2,27] = 2.392, P = 0.110), surface ([F.sub.2,27] = 1.474, P = 0.247), volume ([F.sub.2,27] = 1-756, P = 0,191), and pool-ocean distance ([F.sub.2,27] = 2.620, P = 0.091) were not significant in comparisons between sites.
Molluscan assemblages' Compositions
A total of 1,126 molluscs were recorded at the three study sites. Three classes of Mollusca were found: Bivalvia, Gastropoda, and Polyplacophora, comprising 26 families, 38 genera, and 42 species. The Bivalvia class represented 19.05% of the species found, Gastropoda represented 76.19%, and Polyplacophora represented 4.76%. Columbellidae was the most representative family in terms of species number (6), followed by Pyramidellidae (4), Fissurellidae (3), and Muricidae (3).
Considering all of the rock pools studied, 17 species were found at Pedra Rachada, 24 at Pacheco, and 23 at Dois Coqueiros. The number of specimens was higher at Dois Coqueiros, with 586 individuals collected. A total of 355 and 185 individuals were collected at Pedra Rachada and Pacheco, respectively.
Comparison between Sites--Assemblages
Consistent effects of local variation on ecological descriptors of molluscan assemblages were identified in the pools studied. The ANOVA indicated that there were significant differences in species richness ([F.sub.2,27] = 5.390, P = 0.010) and Shannon diversity ([F.sub.2,27] = 9.560, P < 0.001) of pools when comparing different sites. The greatest and the lowest mean values of species richness were observed in the pools of Dois Coqueiros and Pedra Rachada (Fig. 3A), which were significantly different from each other (Tukey's test: P < 0.001).
The mean value of diversity was significantly lower in the pools of Pedra Rachada (Fig. 3B) (Tukey's test: P < 0.001). No significant difference in the Pielou's evenness ([F.sub.2,27] = 2.060, P = 0.147) was found in comparisons between sites (Fig. 3C).
Relationship between Pool Size Parameters and Assemblages
There were no consistent effects of the pool size parameters on the ecological descriptors of molluscan assemblages. Although there were significant differences due to pool--ocean distance, no consistent patterns were associated with other variables. In addition, none of these conditions were repeated in more than one location. Of the 27 analyses examining the effects of the size parameters on descriptors of assemblages, only two showed significant interactions. A positive relationship between pool--ocean distance and richness at Pacheco (linear regression, [r.sup.2] = 0.619, P = 0.004) was identified. At Dois Coqueiros, there was a significant relationship between pools' surface areas and richness (linear regression, [r.sup.2] = 0.389, P = 0.031). There was no significant relationship between the other size parameters and the assemblage descriptors analyzed.
Comparison between Sites--Individual Taxa
The SIMPER analysis (Table 1) identified four species as more relevant (contributing [greater than or equal to]3% of percentage dissimilarity) for discriminating between sites. Collectively, these species [Eulithidium affine (C. B. Adams, 1850), Cerithium atratum (Born, 1778), Tegula viridula (Gmelin, 1791), and Ischnochiton striolatus (Gray, 1828)] contributed more than 75% of the total dissimilarity. The average abundances of E. affine ([F.sub.2,27] = 3.550, P = 0.042), C. atratum ([F.sub.2,27] = 10.110, P< 0.001), 77. viridula ([F.sub.2,27] = 27.610, P < 0.001), and I. striolatus ([F.sub.2,27] = 11.690, P < 0.001) were compared between sites to reveal significant interactions. The species E. affine was the most abundant in the three sites (Fig. 4) (Tukey's test: P < 0.001). The abundance of C. atratum was significantly higher at Dois Coqueiros (Tukey's test: P < 0.001) and no individual was recorded at Pacheco (Fig. 4).
Relationship between Pool Size Parameters and Individual Taxa
There was a significant positive relationship between the pool-ocean distance and the abundance of Cerithium atratum (linear regression, [r.sup.2] = 0.480, P = 0.015). There was no significant relationship between the abundance of other species and the size parameters evaluated.
This study documented the variation in the structure of molluscan assemblages in rocky pools on sandstone reefs depending on the location and pool size. Consistent effects of variation between sites in the assemblage structure were identified. Nevertheless, there were few indications that the evaluated size parameters and the pool--ocean distance influence this structure.
Molluscan assemblage compositions in rock pools were similar to those already observed in emergent substrata of the same geographical area (Veras et al. 2013). The Gastropoda class was the most abundant, as has been demonstrated in other studies carried out in northeast Brazil (Martinez et al. 2012, Barros & Rocha-Barreira 2013, Veras et al. 2013).
Differences in species richness and diversity were identified between sites. The greatest richness and diversity were found in rock pools at Dois Coqueiros and the least richness at Pedra Rachada. This result is not related to the pool size parameters because the variation of these parameters was similar at all of the sites. The variation of ecological descriptors between different sites may be due to the location of reefs in relation to adjacent estuaries. The pools with the greatest species richness occurred at Dois Coqueiros, which is approximately 2 km from the mouth of the Ceara River. By contrast, the pools with lower richness occurred at Pedra Rachada, which is about 6 km away from the Curu River. Pools at Pacheco had intermediate richness and diversity, and their distance to the nearest estuary was also intermediate between the other two sites (<5 km). Estuaries are transition zones, creating some of the most complex and biologically productive areas on Earth (Kennish 2002). This complexity occurs because two dynamic systems, rivers and coastal oceans, shape the estuarine basin through the processes of erosion and deposition, resulting in a heterogeneous landscape (Moyle et al. 2010). Environmental complexity promoted by estuarine systems has effects on the macrofauna diversity associated with them (Barroso & Matthews-Cascon 2009, Ourives et al. 2011) and possibly on adjacent areas.
Site differences were mainly driven by the gastropod Eulithidium affine, which was the most abundant species at the three beaches studied. The species E. affine is distributed in Brazil and Central America (Marcus & Marcus 1960, Rios 2009). This species inhabits sandstone and coral reefs (Matthews-Cascon & Lotufo 2006) and occurs from the intertidal zone up to 50 m deep (Rios 2009). Although it has already been found in estuarine sediments (Ourives et al. 2011), E. affine has been described as the dominant gastropod in macroalgal communities (Tanaka & Leite 2003, Pereira et al. 2010, Zamprogno et al. 2013) and seagrass meadows (Barros & Rocha-Barreira 2013). These animals feed on the periphyton on the surface of algae covered by debris (Marcus & Marcus 1960) and use algae as a refuge (Avila 2003). The tide pools investigated in this study were characterized by walls covered by macroalgae, constituting a favorable habitat for the establishment of populations of E. affine.
The gastropod Cerithium atratum also contributed to variation among the pools of the different sites. This species occurs from the archipelago of the Florida Keys to the West Indies and South America and is present at all Brazilian coasts (Marcus & Marcus 1964, Rios 2009). The species C. atratum feeds on debris (Meirelles & Matthews-Cascon 2003), occupies consolidated and nonconsolidated substrata, and is usually associated with vegetation (Houbrick 1974) or under graves in rock pools (Matthews-Cascon et al. 1986). Thus, the environments investigated in this work represent a suitable niche for the establishment of C. atratum. Nevertheless, an inconsistency was identified in the results on the distribution of this species at the studied sites. Although C. atratum was recorded in high densities in pools at Dois Coqueiros, no individuals were recorded at Pacheco. These beaches are less than 3 km apart and, therefore, some similarity in the occurrence of species at these sites was expected. In addition, C. atratum was previously recorded on rocky substrata in Pacheco (Veras et al. 2013). Therefore, studies on the population dynamics of C. atratum should be performed in this geographic region to clarify the possible causes of this variation.
Although they were less abundant, the gastropod Tegula viridula and the polyplacophoran Ischnochiton striolatus were also indicated as relevant for discriminating between sites. The species T. viridula is distributed on the coasts of Panama, Venezuela, Suriname, and Brazil (Rios 2009). This gastropod is a sedentary consumer, and the distribution pattern of this functional group is driven by bottom-up processes (Christofoletti et al. 2011). Therefore, it is considered that the balance of abundances is regulated predominantly by the availability of nutrients (Heath et al. 2014). The species T. viridula feeds by scraping algae, especially diatoms (Moreira Filho 1960). Diatoms grow attached to substrata such as macroalgae, rocks, sand grains, floating debris, and even other animals (Winter & Duthie 2000). Thus, the variation of the abundances of T. viridula in pools of different sites should be due to the characteristics of the substrata found in these environments. The polyplacophoran I. striolatus is a common species in intertidal zones along the Brazilian coast and North Carolina (Rios 2009). Most polyplacophorans are herbivorous and feed by scraping the thin layer of algae covering the rocks (Arey & Crozier 1919). The species I. striolatus, as a grazer, is dependent on algal communities for food (Rodrigues & Absalao 2005). Species of the genus Ischnochiton usually occur under or on pebbles on emergent rocky substrata or in rock pools (Chapman 2005, Jorger et al. 2008). Its abundance can be influenced by the diversity of algae (Jorger et al. 2008) and by pebble size (Vasconcelos 2011). Therefore, the substratum of the pools appears to play a greater role in the distribution of I. striolatus than the pool size. These considerations confirm the inherent relationship of the species T. viridula and I. striolatus to the substratum on which they live. Thus, studies that evaluate the response of these species to the substratum pool are necessary to understand their distribution in these habitats.
The absence of consistently significant effects of pool size parameters on molluscan assemblages was unexpected. The species-area relationship is often referred to as the closest thing to a rule in ecology (Lawton 1999, Franzen et al. 2012). Several articles have emphasized the role of fragment size on the biological structure in other systems (Keough 1984, Bowden et al. 2001, Martins et al. 2007, Matias et al. 2010). These works illustrate different interactions in the species-area relationship and their subsequent effects on the structure of communities occupying the fragments. Like other fragments in nature, tide pools can be described according to their area and shape as well as depth, which are an exclusive descriptor for pools (Martins et al. 2007). The relationship between pool size, species richness, and abundance was previously demonstrated (Meager et al. 2005, Martins et al. 2007, Godinho & Lotufo 2010, Firth et al. 2014, Bezerra et al. 2017). Nevertheless, those studies validated this relationship for fish (Meager et al. 2005, Godinho & Lotufo 2010, Bezerra et al. 2017) and macroalgae (Martins et al. 2007). Although Firth et al. (2014) included molluscs in their investigations, the analysis of community structure considered functional groups. Thus, although the influence of pool size on the assemblage structure has already been proven for other groups, this pattern has not been identified for molluscs. The structure of molluscan assemblages in rock pools might be driven by the interaction of these and other physical and biological factors.
The lack of a relationship between pool size and distribution of the organisms shown in the present study is consistent with the work of Underwood and Skilleter (1996). These authors found little evidence that pool diameter leads to differences in the abundance of most taxa. In general, larger areas are associated with a greater complexity of environments, and species tend to respond to this condition (Taniguchi et al. 2003, Graham & Nash 2013). Nevertheless, the components of environmental complexity and area have independent effects on biological structure (Matias et al. 2010). In addition to affecting the distribution of organisms, the size of a fragment also acts on the processes that determine it (Pacheco et al. 2012). Martins et al. (2007) could only confirm the hypothesis that pool size influences the community structure in pools that were in a late successional stage. The result shows that in addition to an effect of covering of the pool surface on the structure of the assemblages, this process occurs as a function of pool size.
In summary, this study showed that for molluscan assemblages, rock pools vary between sites and the pool size cannot explain the variation among pools within a site. Considering the inherent relationship between molluscs and substrate and that the substrate influences environmental complexity, it is possible that the association between these components explains the distribution of the assemblages. Although the effect of pool size as the primary source of variability in the structure of these assemblages remains misunderstood, it must to influence the processes that determine it. The probable explanation is that pool size influences the structural complexity of this environment, which in turn affects the biological structure. This condition supports the general idea that rock pools are complex habitats driven by the interaction of many physical and biological factors. In addition, macroscale components, such as the estuarine plume discharge, can also influence distribution patterns in these systems. Thus, larger scale studies with a multivariate approach can help clarify the structuring processes of molluscan assemblages in rock pools.
This study was financed in part by the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior - Brasil (CAPES) - Finance Code 001 (CAPES 1599287). We especially thank Laboratorio de Invertebrados Marinhos do Ceara -LIMCE team for technical support.
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SHAYANNA M. A. R. SOUZA (*) AND HELENA MATTHEWS-CASCON
Laboratorio de Invertebrados Marinhos Departamento de Biologia, Centre de Ciencias, Universidade Federal do Ceara, Av. Humberto Monte s/n, Campus do Pici - Bloco 909 - 60455-760, Fortaleza, CE, Brazil
(*) Corresponding author. E-mail: firstname.lastname@example.org
TABLE 1. Summary of SIMPER results: average abundance of species per site, their contribution (%) to the within-group similarity, and cumulative total (%) of contributions. Average abundance Taxon Pedra Pacheco Dois Contribution Cumulative Rachada Coqueiros (%) (%) Eulithidium 28.8 9.4 23.9 41.96 41.96 affine Cerithium alralum 3.2 0 17 16.25 58.22 Tegula viridula 0.1 4.3 3.2 10.23 68.44 Ischnochiton 0.2 0.9 5.3 6.86 75.31 striolatus Parvanachis obesa 0.2 0.1 0.9 2.62 77.93 Fissurella rosea 0.2 0.2 2.3 2.42 80.34 Anachis lyrata 0.1 0.6 0.3 2.24 82.58 Stramonita 0 0.2 0.4 1.82 84.40 brasiliensis Ischnoplax 0 0.3 0.6 1.47 85.88 pectinata Fissurella 0.2 0 1.3 1.21 87.09 clenchi Anachis catenata 0 0.4 0 1.11 88.20 Sphenia fragiiis 0 0 0.3 0.93 89.13 Pisania pusio 0 0.2 0.2 0.91 90.04 Leiosolenus 0 0 0.4 0.87 90.91 bisulcatus Anachis isabellei 0.7 0.1 0 0.78 91.69 Brachidontes 0 0 0.3 0.68 92.37 exustus Neritina virginea 0.1 0 0.5 0.61 92.98 Columbella 0 0.3 0 0.58 93.56 mercatoria Schwartziella 0.8 0 0.1 0.45 94.01 catesbyana Echinolillorina 0 0.1 0.1 0.42 94.43 lineolata Pilsbryspira 0 0.2 0 0.39 94.82 nodata Natica sp. 0 0 0.4 0.39 95.21 Leucozonia nassa 0 0.2 0 0.36 95.57 Engina turbinella 0 0.2 0 0.36 95.93 Arcopsis adamsi 0 0.1 0 0.34 96.27 Boonea jadisi 0.2 0 0.5 0.34 96.61 Juliacorbula 0.2 0 0 0.31 96.92 aequivahis Turbonilla sp. 0 0 0.2 0.31 97.22 Area imbricate 0 0.1 0 0.27 97.49 Anachis helenae 0 0.1 0 0.27 97.76 Siphonuria sp. 0 0.1 0 0.27 98.03 Isognomon bicolor 0 0 0.1 0.27 98.30 Melanella polila 0.1 0 0 0.23 98.52 Diodora 0 0.1 0 0.21 98.74 cayenensis Olivella minuta 0 0.1 0 0.21 98.95 Lithopoma 0.1 0 0 0.19 99.14 phoebium Pinctadu 0.1 0 0 0.19 99.33 imbricala Aspclla morchi 0 0 0.2 0.18 99.51 Iolaea robertsoni 0 0.1 0 0.18 99.69 Favartia alveata 0 0.1 0 0.13 99.82 Bittiolum varium 0.2 0 0 0.09 99.91 Odostomia 0 0 0.1 0.09 100 unidentata
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|Author:||Souza, Shayanna M.A.R.; Matthews-Cascon, Helena|
|Publication:||Journal of Shellfish Research|
|Date:||Apr 1, 2019|
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