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Taxonomic and functional diversity of mollusk assemblages in a tropical rocky intertidal zone

Diversidade taxonômica e funcional das assembleias de moluscos em uma zona entre marés rochosa tropical

ABSTRACT

We investigated the spatial variation of molluscan assemblages with different habitat-forming species and bare rock habitat in a rocky intertidal zone in northeastern Brazil. The high intertidal zone substrate was covered predominantly of barnacles [Chthamalus bisinuatus (Pilsbry, 1916)], the mid-intertidal of mussels [Brachidontes exustus (Linnaeus, 1758)] and the low intertidal of macroalgae chlorophytes [Gayralia oxysperma (Kützing) K. L. Vinogradova ex Scagel et al., 1989 and Ulva lactuca Linnaeus, 1753], phaeophytes [Sargassum vulgare C. Agardh] and rhodophytes [Palisada flagellifera (J.Agardh) K. W. Nam, 2007]. A total of 3,861 mollusks were recorded, belonging to the classes Gastropoda (9 species; 3,800 individuals), Bivalvia (3 spp.; 54 ind.), and Polyplacophora (1 sp.; 7 ind.). Functional diversity was accessed through the trophic structure, in which we identified food guilds: suspension feeders, grazers, herbivores, and carnivores. The analysis revealed significant differences in mollusk abundance, species richness, diversity indices, and trophic diversity among barnacle belts, mussel beds, algae habitat, and bare rock habitats. The highest species richness and trophic diversity were detected in algae habitat and mussel beds, which showed low abundance. In contrast, barnacle belts registered low species richness and trophic diversity and a high number of individuals. Bare rock recorded low values in all surveyed indices. This result points to the effect of environmental modification caused by habitat-forming species in this system. These species increase environmental complexity and enable the establishment of organisms through facilitation processes. The various food guilds found in this study reaffirm the role of habitat-forming species in providing niches that support different occupation patterns.

KEYWORDS
Trophic groups; benthic ecology; ecosystem engineers; biological substrate; southwestern Atlantic

RESUMO

Nós investigamos a variação espacial das assembleias de moluscos em função de diferentes habitats formados por fauna séssil e substrato rochoso em uma zona entre marés rochosa no nordeste do Brasil. O substrato da zona entre marés superior era predominantemente recoberto por cracas [Chthamalus bisinuatus (Pilsbry, 1916)], da zona entre marés média por mexilhões [Brachidontes exustus (Linnaeus, 1758)] e da zona entre marés inferior por macroalgas clorofíceas [Gayralia oxysperma (Kützing) K. L. Vinogradova ex Scagel et al., 1989 and Ulva lactuca Linnaeus, 1753], feofíceas [Sargassum vulgare C. Agardh, 1820] e rodofíceas [Palisada flagellifera (J. Agardh) K. W. Nam, 2007]. Foram registrados 3861 moluscos pertecentes às classes Gastropoda (9 espécies; 3800 indivíduos), Bivalvia (3 spp.; 54 ind.), e Polyplacophora (1 sp.; 7 ind.). A diversidade funcional foi analisada através da estrutura trófica, na qual identificamos as guildas alimentares: suspensívoros, raspadores, herbívoros e carnívoros. Abundância, riqueza de espécies, diversidade de Shannon, uniformidade de Pielou e diversidade trófica variaram em função dos habitats formados por cracas, mexilhões, algas e substrato rochoso. Habitats formados por algas e mexilhões apresentaram elevada riqueza de espécies e diversidade trófica, entretanto, apresentaram baixa abundância. Ao contrário, o habitat formado por cracas registrou baixa riqueza e diversidade trófica e elevado número de indivíduos. O substrato rochoso apresentou valores baixos em todos os índices investigados. Esse resultado mostra o efeito da modificação ambiental provocada pela fauna séssil nesse sistema. Esses organismos aumentam a complexidade ambiental e viabilizam o estabelecimento de organismos por meio de processos de facilitação. As diferentes guildas alimentares encontradas neste estudo reafirmam o papel dos substratos biológicos no fornecimento de nichos capazes de suportar diferentes padrões de ocupação.

PALAVRAS-CHAVE
Grupos tróficos; ecologia bentônica; engenheiros do ecossistema; substrato biológico; Atlântico sul ocidental

Biodiversity can be quantified at many levels of biological organization, from the molecular to the ecosystem (Feld et al., 2009Feld, C. K.; Silva, P. M.; Sousa, J. P.; Bello, F.; Bugter, R.; Grandin, U.; Hering, D.; Lavorel, S.; Mountford, O.; Pardo, I.; Pärtel, M.; Römbke, J.; Sandin, L.; Jones, K. B. & Harrison, P. 2009. Indicators of biodiversity and ecosystem services: a synthesis across ecosystems and spatialscales. Oikos 118(12):1862-1871.; Moreno et al., 2018Moreno, C. E.; Calderón-Patrón, J. M.; Martín-Regalado, N.; Martínez-Falcón, A. P.; Ortega-Martínez, I. J.; Rios-Díaz, C. L. & Rosas, F. 2018. Measuring species diversity in the tropics: a review of methodological approaches and framework for future studies. Biotropica 50(6):929-941.). Classically, biodiversity has been described through diversity indices based on species richness or evenness, with relative abundance (Villéger et al., 2010Villéger, S.; Miranda, J. R.; Hernández, D. F.& Mouillot, D. 2010. Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecological Applications 20(6):1512-1522. ; Moreno et al., 2018Moreno, C. E.; Calderón-Patrón, J. M.; Martín-Regalado, N.; Martínez-Falcón, A. P.; Ortega-Martínez, I. J.; Rios-Díaz, C. L. & Rosas, F. 2018. Measuring species diversity in the tropics: a review of methodological approaches and framework for future studies. Biotropica 50(6):929-941.). Although they provide meaningful information about the structure of biotic systems, they do not consider the functional identity of organisms (Orwin et al., 2014Orwin, K. H.;Ostle, N.; Wilby, A. & Bardgett, R. D. 2014. Effects of species evenness and dominant species identity on multiple ecosystem functions in model grassland communities. Oecologia 174(3):979-992. ). Functional diversity is the component of biodiversity that describes the functions performed by organisms in an assemblage, community, or ecosystem (Tilman, 2001Tilman, D. 2001. Functional diversity. In: Levin, S. A. ed. Encyclopedia of Biodiversity. San Diego, Academic Press, p. 109-120.). It can be quantified by the functional characteristics of the species, described as biological attributes that influence ecosystem organization (Mlambo, 2014Mlambo, M. C. 2014. Not all traits are ‘functional’: insights from taxonomy and biodiversity-ecosystem functioning research. Biodiversity and Conservation 23(3):781-790. ; Gusmão-Júnior et al., 2016Gusmão-Júnior, J. B.; Brauko, K. M.; Eriksson, B. K. & Lana, P. C. 2016. Functional diversity of macrobenthic assemblages decreases in response to sewage discharges. Ecological Indicators 66:65-75. ).

Among the methods for assessing functional diversity is the analysis of functional groups or trophic guilds (Gusmão-Júnior & Lana, 2015Gusmão-Júnior, J. B. L. & Lana, P. C. 2015. Spatial variability of the infauna adjacent to intertidal rocky shores in a subtropical estuary. Hydrobiologia 743(1):53-64. ; Donnaruma et al., 2018aDonnarumma, L.; Sandulli, R.; Appolloni, L. & Russo, G. F. 2018a. Assessing molluscs functional diversity within different coastal habitats of Mediterranean marine protected areas. Ecological Questions 29(3):35-51. ). According to the original definition, guilds are groupings of species that exploit the same class of environmental resources in a similar way (Root, 1967Root, R. B. 1967. The niche exploitation pattern of the blue-gray gnatcatcher. Ecological Monographs 37(4):317-350. ). In turn, feeding guild refers to the assemblage of species with similarities in the size and composition of food particles, the mechanism of ingestion, and the mobility patterns associated with feeding (Fauchald & Jumars, 1979Fauchald, K. & Jumars, P. A. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology: An Annual Review 17:193-284. ).

The feeding guild structure of intertidal benthic communities is affected by environmental heterogeneity (Gallucci et al., 2020Gallucci, F.; Christofoletti, R. A.; Fonseca, G. & Dias, G. M. 2020. The Effects of Habitat Heterogeneity at Distinct Spatial Scales on Hard-Bottom-Associated Communities. Diversity 12(1):1-13. ). In the rocky intertidal zone, sessile organisms, such as mussels and macroalgae, increase environmental heterogeneity, and host a diverse associated fauna (Borthagaray & Carranza, 2007Borthagaray, A. I. & Carranza, A. 2007. Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica 31(3):243-250.; Bellgrove et al., 2017Bellgrove, A.; McKenzie, P. F.; Cameron, H. & Pocklington, J. B. 2017. Restoring rocky intertidal communities: Lessons from a benthic macroalgal ecosystem engineer. Marine Pollution Bulletin 117(1-2):17-27.). Sessile biota provides other organisms with protection from physical stress (Scrosati et al., 2011Scrosati, R. A.; Van Genne, B.; Heaven, C. S. & Watt, C. A. 2011. Species richness and diversity in different functional groups across environmental stress gradients: a model for marine rocky shores. Ecography 34(1):151-161. ), food source (Gosselin & Chia, 1995Gosselin, L. A. & Chia, F. S. 1995. Distribution and dispersal of early juvenile snails: effectiveness of intertidal microhabitats as refuges and food sources. Marine Ecology Progress Series 128:213-223. ), and shelter from predation and desiccation (Gutiérrez et al., 2003Gutiérrez, J. L.; Jones, C. G.; Strayer, D. L. & Iribarne, O. O. 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101(1):79-90. ). Therefore, these organisms fulfill the role of habitat-forming species by creating and modifying the habitat in which they occur (Jones et al., 1994Jones, C. G.; Lawton, J. H. & Shachak, M. 1994. Organisms as ecosystem engineers. In: Samson, F. B. & Knopf, F. L. eds. Ecosystem management: selected readings. New York, Springer, p. 130-147. ). The habitat-forming species influence species richness, abundance, uniformity, and functional identity playing an important role in the organization and functioning of intertidal benthic communities (Lemieux & Cusson, 2014Lemieux, J. & Cusson, M. 2014. Effects of Habitat-Forming Species Richness, Evenness, Identity, and Abundance on Benthic Intertidal Community Establishment and Productivity. PLoS One 9(10):e109261. ).

Mollusks are among the more diverse and abundant groups of marine intertidal benthic communities, occupying a wide range of habitats and ecological niches (Zuschin et al., 2001Zuschin, M.; Hohenegger, J. & Steininger, F. 2001. Molluscan assemblages on coral reefs and associated hard substrata in the northern Red Sea. Coral Reefs 20(2):107-116. ; Ponder & Lindberg, 2008Ponder, W. & Lindberg, D. R. 2008. Molluscan evolution and phylogeny: an introduction. In: Ponder, W. & Lindberg, D. R. eds. Phylogeny and Evolution of the Mollusca. Berkeley, University of California Press, p. 1-17.). Functional diversity through the use of feeding guilds, in molluscan assemblages, has been investigated in submerged environments (Rueda et al., 2009Rueda, J. L.; Gofas, S.; Urra, J. & Salas, C. 2009. A highly diverse molluscan assemblage associated with eelgrass beds (Zostera marina L.) in the Alboran Sea: Micro-habitat preference, feeding guilds and biogeographical distribution. Scientia Marina 73(4):679-700. ; Donnaruma et al., 2018aDonnarumma, L.; Sandulli, R.; Appolloni, L. & Russo, G. F. 2018a. Assessing molluscs functional diversity within different coastal habitats of Mediterranean marine protected areas. Ecological Questions 29(3):35-51. ). In the intertidal zone, studies on mollusk feeding guilds have been carried out on sandy beaches (Arruda et al., 2003Arruda, E. P.; Domaneschi, O. & Amaral, A. C. Z. 2003. Mollusc feeding guilds on sandy beaches in São Paulo State, Brazil. Marine Biology143(4):691-701. ) and on vermetid bioconstructions (Donnaruma et al., 2018bDonnarumma, L.; Sandulli, R.; Appolloni, L.; Sánchez-Lizaso, J. L. & Russo, G. F. 2018b. Assessment of structural and functional diversity of mollusc assemblages within vermetid bioconstructions. Diversity 109(3):1-14.). A study on the rocky intertidal community with a biological substrate was developed for medium- and macrofauna, with a secondary emphasis on mollusks (Gallucci et al., 2020Gallucci, F.; Christofoletti, R. A.; Fonseca, G. & Dias, G. M. 2020. The Effects of Habitat Heterogeneity at Distinct Spatial Scales on Hard-Bottom-Associated Communities. Diversity 12(1):1-13. ). To our knowledge there is only one previous study assessed the trophic structure of molluscan assemblages inhabiting different habitat types in a tropical rocky intertidal zone (Olabarria et al., 2001Olabarria, C.; Carballo, J. L. & Vega, C. 2001. Spatio-temporal changes in the trophic structure of rocky intertidal mollusc assemblages on a tropical shore. Ciencias Marinas 27(2):235-254. ).

Therefore, the goal of this study was to investigate the structure and function (through the use of feeding guilds) of molluscan assemblages inhabiting different habitat types in a rocky intertidal zone. We analyzed the taxonomic and functional diversity of molluscan assemblages in a tropical urban area in Bahia state, in Brazilʼs Northeast Region, investigating their spatial variation among three habitats-forming species, and bare rock habitat. We have tested the hypothesis that different biological substrates harbor different associated assemblages. We admit that the variation in taxonomic and functional diversity will be explained by environmental heterogeneity (Hutchinson, 1959Hutchinson, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist 93(870):145-159.; Villéger et al., 2010Villéger, S.; Miranda, J. R.; Hernández, D. F.& Mouillot, D. 2010. Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecological Applications 20(6):1512-1522. ). We, therefore, expect mollusk assemblages to exhibit differences in composition between the different habitats investigated. In this investigation, we first characterized habitats and feeding guilds and subsequently compared synecological indices and functional diversity. Finally, we discuss the taxonomic structure and trophic relationships identified and their association with described habitats.

MATERIAL AND METHODS

Study area. The study was performed in the south-west Atlantic, in the Northeast Region Brazil, on a hill called Morro de Pernambuco (14°48ʼS, 39°01ʼW), located at the limits of a peninsula at the mouth of the Cachoeira River. It is inserted in the urban area of Ilhéus, Bahia state. The climate is tropical, with a mean temperature of 24.6°C and an annual precipitation of 2,000 mm irregularly distributed throughout the year (Alvares et al., 2013Alvares, C. A.; Stape, J. L.; Sentelhas, P. C.; Gonçalves, J. L. M. & Sparovek, G. 2013. Köppenʼs climate classification map for Brazil. Meteorologische Zeitschrift 22(6):711-728.). Recreation and tourism activities are carried out in this place, which suffers from environmental impact due to garbage deposition, erosive tendencies, and inadequate traffic of motor vehicles (Silva, 2015Silva, E. B. 2015. Caracterização do ambiente no município de Ilhéus (BA): O caso da baía do pontal. Boletim Goiano de Geografia 35(1):157-175. ). The site was selected because of land accessibility, and to provide a stable rocky substrate (no loose blocks). Morro de Pernambuco is formed by irregular rocky outcrops of volcanic origin (Oliveira et al., 1989Oliveira, M. F. T.; Bellieni, G.; Comin-Chiaramonti, P.; Melfi, A. J.; Piccirillo, E. M. & Moraes-Brito, C. 1989. Preliminary petrographic and geochemical considerations on the precambrian mafic dykes of the Ilhéus-Olivença area, Bahia. Boletim IG-USP Série Científica 20:5-19. ). The substrate of these outcrops stretch covered by sessile biota, including different species of invertebrates and macroalgae.

Data collection. Sampling was carried out in August 2012 on the rocky intertidal zone along the eastern side of Morro de Pernambuco, facing the Atlantic Ocean, at low spring tide. The molluscan assemblages were investigated in two rocky outcrops. In each of them, samples were obtained along three parallel transects measuring 1 by 30 m (30 m along-shore transects). The positioning of transects was chosen according to the intertidal zones. The upper boundary was determined using ecological indicators (barnacle zone). The intertidal range was then divided into three zones of equal vertical extent (high, mid, and low level) (Heaven & Scrosati, 2008Heaven, C. S. & Scrosati, R. A. 2008. Benthic community composition across gradients of intertidal elevation, wave exposure, and ice scour in Atlantic Canada. Marine Ecology Progress Series 369:13-23. ). Samples with five aleatory replicates at each intertidal zone in each of the rocky outcrops were collected by visual estimate of percentage cover, totaling 10 samples per level. The percentage cover of sessile organisms was estimated using quadrats (60 x 60 cm) with 100 subdivisions (Dethier et al., 1993Dethier, M. N.; Graham, E. S.; Cohen, S. & Tear, L. M. 1993. Visual versus random-point percent cover estimations: ʽobjectiveʼ is not always better. Marine Ecology Progress Series 96:93-100. ). Samples with five aleatory replicates at each intertidal zone in each of the rocky outcrops were collected by scraping the hard bottom, totaling 10 samples per level. The biological substrate was removed by scraping a quadrat (25 × 25 cm) and the malacofauna present in each sample were manually removed using forceps and spatula and washed in a 0.5-mm meshsieve. The organisms retained were packed in plastic bags for transport to the laboratory, where they were refrigerated for 24 h and then fixed in 70% ethanol. Infaunal mollusks were not considered in this study.

The mollusks were examined under a stereoscopic microscope and identified to the lowest possible taxonomic level. To each mollusk species, a feeding guild was assigned, according to Rios (2009Rios, E. C. 2009. Compendium of Brazilian Sea Shells. Rio de Janeiro, Editora Evangraf. 720p.) and Felder & Camp (2009Felder, D. L. & Camp, D. K. 2009. Gulf of Mexico origin, waters, and biota: biodiversity. College Station, Texas A&M University Press. 393p.). The following categories were considered: suspension feeders, grazers, herbivores, and carnivores (e.g., Barroso et al., 2018Barroso, C. X.; Rabay, S. G. & Matthews-Cascon, H. 2018. Mollusks on recruitment panels placed in an offshore harbor in Tropical Northeastern Brazil. Arquivos de Ciências do Mar 51(1):65-74. ).All collected material was incorporated into the Malacological Collection “Prof. Henry Ramos Matthews” - series B of the Universidade Federal do Ceará (CMPHRM-B/UFC).

Data analysis. The habitat-forming species were described through the average percentage cover per level sampled in the intertidal zone. Subsequently, they were classified into different habitats.

Mollusk assemblages were analyzed using synecological indices, such as the total abundance of individuals (N), species richness, the Shannon-Weaver species diversity (H’), and the Pielou’s Evenness (J). The quantitative and qualitative dominances (%DI and %DQ) and frequency (%F) were also calculated. The functional (trophic) diversity of the molluscan assemblages at each habitat was analyzed through the index of trophic diversity (ITD) (Heip et al., 1985Heip, C.;Vincx, M. & Vranken, G. 1985. The ecology of marine nematodes. Oceanography and Marine Biology 23:399-490.). The ITD ranges from 0 to 1 (high and low trophic diversity, respectively), and is calculated according to the following equation:

I T D = q i 2 (1)

where q i is the relative contribution of the number of individuals of each trophic group (i) to the total number of individuals. According to the modified version applied to mollusks (Antit et al., 2016Antit, M.; Daoulatli, A.; Urra, J.; Rueda, J. L.; Gofas, S. & Salas, C. 2016. Seasonality and trophic diversity in molluscan assemblages from the Bay of Tunis (southern Mediterranean Sea). Mediterranean Marine Science 17(3):692-707.), ITD was calculated as 1-ITD to have the highest trophic diversity with the greatest weight (Donnarumma et al., 2018aDonnarumma, L.; Sandulli, R.; Appolloni, L. & Russo, G. F. 2018a. Assessing molluscs functional diversity within different coastal habitats of Mediterranean marine protected areas. Ecological Questions 29(3):35-51. ).

Analyses of variance (ANOVAs) were performed to test abundance, species richness, Shannon-Weaver diversity, Pielou’s Evenness, and index of trophic diversity variation between habitat types. 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 (Zar, 1996Zar, J. H. 1996. Biostatistical analysis. Upper Saddle River, Prentice Hall. 944p.).

To assess the relationship between food guilds and habitat types we use redundancy analysis (RDA). The response matrix of presence-absence data was Hellinger transformed and the explanatory matrix was standardized to zero mean and unit variance (Legendre & Gallagher, 2001Legendre, P. & Gallagher, E. D. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129(2):271-280. ). Normality and multicollinearity assumptions were tested before using the Shapiro-Wilk test and variance inflation factors, respectively (Fox & Monette, 1992Fox, J. & Monette, G. 1992. Generalized collinearity diagnostics. Journal of the American Statistical Association 87(417):178-183.). All analyses were performed in R ver. 3.6.1 (R CoreTeam, 2019R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ).

RESULTS

Environmental characteristics. The high intertidal zone substrate was covered predominantly (68%) of barnacles [Chthamalus bisinuatus (Pilsbry, 1916)], and the mid-intertidal (52%) of mussels [Brachidontes exustus (Linnaeus, 1758)]. In the low intertidal there was a predominance (78%) of macroalgae chlorophytes [Gayralia oxysperma (Kützing) K. L. Vinogradova ex Scagel et al.,1989 and Ulva lactuca Linnaeus, 1753], phaeophytes [Sargassum vulgare C. Agardh] and rhodophytes [Palisada flagellifera (J. Agardh) K. W. Nam, 2007]. Substrate with no cover (bare rock) were identified at the high (31%), mid (4%), and low (5%) intertidal zones. Therefore, barnacles, mussels, and macroalgae were considered habitat-forming species, and the rocky substrate with no associated sessile biota were described as bare rock. For data analysis, each substrate (barnacle belt, mussel beds, algae habitat and bare rock) was treated as a habitat type (Fig. 1).

Fig. 1.
Substrate characterization of the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil. Intertidal zones (High, Mid and Low) and percent cover (mean) of algae habitat (ALG), bare rock (BAR), barnacle belt (BNC) and mussel beds (MUS).

Taxonomic composition. A total of 3,861 mollusks were recorded at the 30 sampled points. Overall, 13 species, belonging to the classes of Gastropoda (9 species; 3,800 individuals), Bivalvia (3 spp.; 54 ind.), and Polyplacophora (1 sp.; 7 ind.) were identified in the four habitat types (Tab. I). The bivalve Brachidontes exustus occurred in a high-density aggregate distribution, forming a continuous patch covering the substrate. This bivalve was described as habitat-forming species (MUS - mussel beds) and was not included in the composition of mollusk assemblages.

Tab. I.
Taxonomic list of mollusk species with their feeding guilds (suspension feeders, grazers, herbivores, and carnivores), abundance (N) and frequency (F%) for each habitat type (ALG, algae habitat; BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) recorded in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil. References: aRios, 2009Rios, E. C. 2009. Compendium of Brazilian Sea Shells. Rio de Janeiro, Editora Evangraf. 720p. and bFelder & Camp, 2009Felder, D. L. & Camp, D. K. 2009. Gulf of Mexico origin, waters, and biota: biodiversity. College Station, Texas A&M University Press. 393p..

Consistent effects of variation on sinecological indices of molluscan assemblages were identified in the habitat types studied. The ANOVA indicated that there were significant differences in abundance (F3, 26=53.22; p<0.001), species richness (F3,26=3.82; p=0.022), Shannon diversity (F3,26=8.59; p<0.001) and Pielou’s evenness (F3,26=10.43; p<0.001) when comparing different habitats.

Barnacle belt (BNC) recorded lower species richness and diversity indices than mussel beds (MUS) and algae habitat (ALG). However, BNC showed the highest total abundance among these habitats. Algae habitat showed higher diversity indices than BNC and bare rock habitat (BAR) (Fig. 2).

Fig. 2.
Mollusk assemblages: number of individuals (Abundance), number of species (Species richness) and diversity indices (Shannon-Weaver H' and Pielou’s evenness J) calculated (mean ± SE) measured for each habitat (ALG, algae habitat; BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil. Significant differences are indicated with different letters (Tukey’s test: p<0.05).

Gastropoda was dominant in all habitat types. Only gastropods occurred at BNC and BAR. Two species, Echinolittorina lineolata (dʼOrbigny, 1840) and Lottia subrugosa (dʼOrbigny, 1846), have been recorded in these habitats (Fig. 3).

Fig. 3.
Contribution of taxonomic groups (Gastropoda, Bivalvia, Polyplacophora) to quantitative (Abundance %DI) and qualitative (Species richness %DQ) dominances for each habitat (ALG, algae habitat;BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil.

In the MUS, gastropods were dominant both in abundance (DI 96.93%, 536 individuals) and species richness (DQ 60%, 3 species), followed by bivalves (DI 2.35%, 13 ind.; DQ 20%, 1 sp.) and polyplacophorans (DI 0.72%, 4 ind.; DQ 20%, 1 sp.) (Fig. 3). The most abundant and frequent species were E. lineolata and L. subrugosa (495 individuals; frequency: F 100% and 32 ind.; F 100%, respectively), followed by the bivalve Isognomon bicolor (C. B. Adams, 1845) (13 ind.; F 20%) (Tab. I).

In ALG, gastropods were also dominant both in abundance (DI 67.88%, 93 ind.) and species richness (DQ 69.23%, 9 spp.), followed by bivalves (DI 29.93%, 41 ind.; DQ 23.08%, 3 spp.) and polyplacophorans (DI 2.19%, 3 ind.; DQ 7.69%, 1 sp.) (Fig. 3). The most abundant and frequent species were the gastropods L. subrugosa and Eulithidium affine (C. B. Adams, 1850) (29 ind.; F 46.67% and 19 ind.; F 6.67%, respectively), followed by I. bicolor (17ind.; F 20%) (Tab. I).

Functional composition. Four feeding guilds were identified: suspension feeders, grazers, herbivores, and carnivores. The feeding guild grazers showed high dominance in BNC (DI 99.80%, 2515 ind.; DQ 50%, 1 sp.), BAR (DI 97.60%, 636 ind.; DQ 50%, 1 sp.) and MUS (DI 89.51%, 495 ind.; DQ 20%, 1 sp.). Suspension feeders occurred in greater quantitative abundance in ALG (DI 29.93%, 41 ind.; DQ 23.08%, 3 spp.), followed by herbivores (DI 27.74%, 38 ind.; DQ 23.08%, 3 spp.). The highest qualitative contribution in ALG was observed in carnivores. (DQ 38.46%, 5 spp.) (Fig. 4).

Fig. 4.
Contribution of feeding guilds (suspension feeders, grazers, herbivores, and carnivores) to quantitative (Abundance %DI) and qualitative (Species richness %DQ) dominances for each habitat (ALG, algae habitat; BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil.

The most abundant species in each feeding guilds were: the grazer E. lineolata (3,660 ind.), the herbivore L. subrugosa (81 ind.), the suspension feeder I. bicolor (30 ind.) and the carnivore gastropod Stramonita brasiliensis Claremont & D. Reid, 2011 (23 ind.) (Tab. I).

The index of trophic diversity (ITD) differed between habitats (F3, 26=8.68; p<0.001). In ALG, trophic diversity was higher than in BNC and BAR. The least ITD was recorded in BNC (Fig. 5).

Fig. 5.
Index of trophic diversity (ITD) calculated (mean ± SE, standard error) for each habitat (ALG, algae habitat; BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil. Significant differences are indicated with different letters (Tukey’s test: p<0.05).

Redundancy analysis (RDA) showed that the habitat variable explained 49.27% (ANOVA: F4, 25=5.80; p=0,001) of variability in the occurrence of feeding guilds. The first axis explained 37.89% variability and was positively related to variables ALG (0.86) and MUS (0.67) and negatively to variables BNC (-0.93) and BAR (-0.65). The tri-plot showed an association between carnivores and ALG and between grazers, BNC, and BAR. Herbivores were related to MUS. Guild suspension feeders had a low association with investigated habitats (Fig. 6).

Fig. 6.
Redundancy analysis (RDA) tri-plot on habitats types (ALG, algae habitat; BAR, bare rock; BNC, barnacle belt; MUS, mussel beds) and feeding guilds (suspension feeders, grazers, herbivores, and carnivores) in the rocky intertidal zone of Morro de Pernambuco, Ilhéus, Bahia, Brazil.

DISCUSSION

This study documented the spatial variation in taxonomic and functional diversity of mollusk assemblages in different types of habitat in a tropical rocky intertidal zone. Species of Gastropoda, Bivalvia, and Polyplacophora were identified and classified according to the feeding guilds suspension feeders, grazers, herbivores, and carnivores. Variations in the mollusk assemblage structure were identified between barnacle belt, mussel beds, algae habitat, and bare rock habitats.

Of the three taxonomic classes recorded, gastropods showed high abundance, species richness, and trophic diversity, having occurred in the four habitats investigated. This result is in line with that described for the rocky intertidal zone in other tropical regions (Flores-Rodríguezet al., 2012Flores-Rodríguez, P.; Flores-Garza, R.; García-Ibáñez, S.; Valdés-González, A.; Violante-González, J.; Cortés, E. S.; Galeana-Rebolledo, L. & Torreblanca-Ramírez, C. 2012. Mollusk species richness on the rocky shores of the state of Guerrero, Mexico, as affected by rains and their geographical distribution. Natural Resources 3(4):248-260. ; Martinez et al., 2012Martinez, A. S.; Mendes, L. F. & Leite, T. S. 2012. Spatial distribution of epibenthic molluscs on a sandstone reef in the Northeast of Brazil. Brazilian Journal of Biology 72(2):287-298. ), confirming gastropods affinity for these environments. The grazer Echinolittorina lineolata was the dominant species in this study. Species of Echinolittorina are described as dominant gastropods in the highest levels of intertidal rocky zones at tropical coasts (Reid, 2009Reid, D. G. 2009. The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean. Zootaxa 2184(1):1-103. ). The highest species richness among gastropods was detected in the carnivores feeding guild. Stramonita brasiliensis was the most abundant in this guild. All bivalve species recorded in this study, such as I. bicolor and Modiolus americanus (Leach, 1815), belong to feeding guild suspension feeders. The guild occurs only in mussel beds and algae habitats and is a significant trophic category of marine hard-bottom communities (Donnarumma et al., 2018bDonnarumma, L.; Sandulli, R.; Appolloni, L.; Sánchez-Lizaso, J. L. & Russo, G. F. 2018b. Assessment of structural and functional diversity of mollusc assemblages within vermetid bioconstructions. Diversity 109(3):1-14.). Polyplacophorans, in turn, were poorly represented both in the number of individuals and in species richness, with the herbivore Rhyssoplax janeirensis (Gray, 1828) being the only species recorded. Although polyplacophorans are common in rocky intertidal zones on the Brazilian coast (Rios, 2009Rios, E. C. 2009. Compendium of Brazilian Sea Shells. Rio de Janeiro, Editora Evangraf. 720p.), their occurrence is commonly associated with the presence of pebbles (Jörger et al., 2008Jörger, K. M.; Meyer, R. & Wehrtmann, I. S. 2008. Species composition and vertical distribution of chitons (Mollusca: Polyplacophora) in a rocky intertidal zone of the Pacific coast of Costa Rica. Journal of the Marine Biological Association of the United Kingdom 88(4):807-816. ) and the formation of rocky pools (Souza & Matthews-Cascon, 2019Souza, S. M. A. R. & Matthews-Cascon, H. 2019. Molluscan Assemblages in Rock Pools on Sandstone Reefs: Local and between Pools Variability. Journal of Shellfish Research 38(1):201-208. ). The system investigated in this study is characterized by the absence of loose blocks and continuous rocky substrate covered by sessile biota. This environment may not be conducive to the expressive establishment of polyplacophorans.

The barnacle belt habitat showed high abundance, however, with low species richness and diversity. Predators are less common in these regions, increasing competition for space and food. This condition can lead to competitive exclusion and consequent dominance of the system by a few species (Menge et al., 1987Menge, B. A. & Sutherland, J. P. 1987. Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. The American Naturalist 130(5):730-757.; Clarke 2004Clarke, P. J. 2004. Effects of experimental canopy gaps on mangrove recruitment: lack of habitat partitioning may explain stand dominance. Journal of Ecology 92:203-213. ). There was a predominance of gastropods in the barnacle belt, with the occurrence of two species, the grazer E. lineolata, and the herbivore L. subrugosa; these species were the most abundant in their respective feeding guilds. The high density of litorinids in the barnacle belt is characteristic in tropical rocky substrates (Apolinário et al., 1999Apolinário, M.; Coutinho, R. & Baeta-Neves, M. H. 1999. Periwinkle (Gastropoda: Littorinidae) habitat selection and its impact upon microalgal populations. Revista Brasileira de Biologia 59(2):211-218. ). Littorinid E. lineolata also occurred in high abundance in bare rock habitat. This result is in accordance with the habitat described for the distribution of this species (Reid, 2009Reid, D. G. 2009. The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean. Zootaxa 2184(1):1-103. ). In addition, rocky surfaces in the intertidal zone are primarily covered by periphyton (Aguilera et al., 2013Aguilera, M. A.; Navarrete, S. A. & Broitman, B. R. 2013. Differential effects of grazer species on periphyton of a temperate rocky shore. Marine Ecology Progress Series 484:63-78.), which is the main food source for benthic grazers (Liess et al.,2009Liess, A.; Lange, K.; Schulz, F.; Piggott, J. J.;Matthaei, C. D. & Townsend, C. R. 2009. Light, nutrients and grazing interact to determine diatom species richness via changes to productivity, nutrient state and grazer activity. Journal of Ecology 97(2):326-336. ). Grazers’ dominance in barnacle belt and bare rock explains the low trophic diversity in these habitats. This condition also clarifies the association between grazers and these habitats identified in redundancy analysis.

The highest species richness and trophic diversity were detected in algae habitat and mussel beds, which showed low abundance. In contrast, barnacle belts registered low species richness and trophic diversity, and a high number of individuals. The inverse relationship between species richness and abundance is common in ecological systems and has already been described for mollusk assemblages (Donnarumma et al., 2018aDonnarumma, L.; Sandulli, R.; Appolloni, L. & Russo, G. F. 2018a. Assessing molluscs functional diversity within different coastal habitats of Mediterranean marine protected areas. Ecological Questions 29(3):35-51. ). According to a hypothesis describing this pattern, the greater the number of species, the smaller the size of their populations due to the partitioning of resources (Griffin et al., 2008Griffin, J. N.; De La Haye, K. L.; Hawkins, S. J.; Thompson, R. C. & Jenkins, S. R. 2008. Predator diversity and ecosystem functioning: density modifies the effect of resource partitioning. Ecology 89(2):298-305. ;Donnarumma et al., 2018aDonnarumma, L.; Sandulli, R.; Appolloni, L. & Russo, G. F. 2018a. Assessing molluscs functional diversity within different coastal habitats of Mediterranean marine protected areas. Ecological Questions 29(3):35-51. ). This result also indicates competition in habitats with the highest diversity. Resource competition can lead to increased niche variation and drive diversity via changes in foraging behaviour (Svanbäck & Bolnick, 2007Svanbäck, R. & Bolnick, D. I. 2007. Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B: Biological Sciences 274(1611):839-844.).

Algae habitat and mussel beds hosted all feeding guilds identified in this study. In these habitats, grazers were mostly represented by E. affine, herbivores by L. subrugosa, carnivores by S. brasiliensis, and suspension feeders by I. bicolor. The co-occurrence of these guilds explains the high taxonomic diversity in such habitats due to environmental heterogeneity (Tews et al., 2004Tews, J.; Brose, U.; Grimm, V.; Tielbörger, K.; Wichmann, M. C.; Schwager, M. & Jeltsch, F. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31(1):79-92. ; Ortega et al., 2018Ortega, J. C.; Thomaz, S. M. & Bini, L. M. 2018. Experiments reveal that environmental heterogeneity increases species richness, but they are rarely designed to detect the underlying mechanisms. Oecologia 188(1):11-22.). The habitat-forming species increase structural complexity to support a diverse associated fauna (Lemieux & Cusson, 2014Lemieux, J. & Cusson, M. 2014. Effects of Habitat-Forming Species Richness, Evenness, Identity, and Abundance on Benthic Intertidal Community Establishment and Productivity. PLoS One 9(10):e109261. ; Gallucci et al., 2020Gallucci, F.; Christofoletti, R. A.; Fonseca, G. & Dias, G. M. 2020. The Effects of Habitat Heterogeneity at Distinct Spatial Scales on Hard-Bottom-Associated Communities. Diversity 12(1):1-13. ). Different types of macroalgae along with their complex architecture, promote diversity in mollusk assemblages (Chemello & Milazzo, 2002Chemello, R. & Milazzo, M. 2002. Effect of algal architecture on associated fauna: Some evidence from phytalmolluscs. Marine Biology 140(5):981-990.; Pitacco et al., 2014Pitacco, V.; Orlando-Bonaca, M.; Mavrič, B.; Popović, A. & Lipej, L. 2014. Mollusc fauna associated with the Cystoseira algal associations in the Gulf of Trieste (Northern Adriatic Sea). Mediterranean Marine Science 15(2):225-238. ). Mussel beds, in turn, increase complexity by aggregating living individuals, empty shells and byssal threads, providing shelter and reducing physiological and mechanical stress (Borthagaray & Carranza, 2007Borthagaray, A. I. & Carranza, A. 2007. Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica 31(3):243-250.; Arribas et al., 2014Arribas, L. P.; Donnarumma, L.; Palomo, M. G. & Scrosati, R. A. 2014. Intertidal mussels as ecosystem engineers: Their associated invertebrate biodiversity under contrasting wave exposures. Marine Biodiversity 44(2):203-211. ).

The algae habitat also registered a high qualitative contribution to carnivores. This accounts for the association found between this guild and algae habitat, as well as the high species richness in this habitat. Predator gastropods, such as S. brasiliensis, keep their prey below their carrying capacity, enabling the coexistence of a higher number of species (Paine, 1966Paine, R. T. 1966. Food web complexity and species diversity. The American Naturalist 100(910):65-75.). Predators modify their preyʼs population growth rates by direct consumption or by inducing behavioral and physiological changes (Preisser & Bolnick, 2008Preisser, E. L. & Bolnick, D. I. 2008. The Many Faces of Fear: Comparing the Pathways and Impacts of Nonconsumptive Predator Effects on Prey Populations. PLoSONE 3(6):e2465. ). In general, predation prevents a monopoly on food resources and reduces the intensity of competitive interactions between species at lower trophic levels (Paine, 1966; Griffin et al., 2008Griffin, J. N.; De La Haye, K. L.; Hawkins, S. J.; Thompson, R. C. & Jenkins, S. R. 2008. Predator diversity and ecosystem functioning: density modifies the effect of resource partitioning. Ecology 89(2):298-305. ). In addition to this top-down effect, the habitat algae discussed here comprises different macroalgae species, and may, therefore, hold diverse micro-habitats in them. Furthermore, macroalgae are primary producers in intertidal regions (Mann, 1973Mann, K. H. 1973. Seaweeds: their productivity and strategy for growth. Science 182(4116):975-981. ; Tait & Schiel, 2011Tait, L. W. & Schiel, D. R. 2011. Dynamics of productivity in naturally structured macroalgal assemblages: importance of canopy structure on light-use efficiency. Marine Ecology Progress Series 421:97-107. ), including resource availability and increasing species coexistence (Cardinale et al., 2009Cardinale, B. J.; Hillebrand, H.; Harpole, W. S.; Gross, K. & Ptacnik, R. 2009. Separating the influence of resource ‘availability’ from resource ‘imbalance’ on productivity-diversity relationships. Ecology Letters 12(6):475-487. ). Increased bottom-up resource base in the food chain leads to an increase in all trophic levels (Menge, 2000Menge, B. A. 2000. Top-down and bottom-up community regulation in marine rocky intertidal habitats. Journal of Experimental Marine Biology and Ecology 250(1-2):257-289. ).

A relative abundance of gastropod E. lineolata was detected in the mussel beds habitat. This periwinkle is normally distributed on bare rocks, between barnacles and mussels in upper and mid intertidal zones (Reid, 2009Reid, D. G. 2009. The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean. Zootaxa 2184(1):1-103. ). This occupation pattern is explained by group physiological characteristics (Garrity, 1984Garrity, S. D. 1984. Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 65(2):559-574. ), and predation pressure (Perez et al., 2009Perez, K. O.; Carlson, R. L.; Shulman, M. J. & Ellis, J. C. 2009. Why are intertidal snails rare in the subtidal? Predation, growth and the vertical distribution of Littorina littorea (L.) in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 369(2):79-86.) faced in the low intertidal zone. However, E. lineolata occurred at all sampled points in mussel beds habitat, including the low intertidal, characterized by frequent submersion. This result differs from traditional models (Stephenson & Stephenson, 1949Stephenson, T. A. & Stephenson, A. 1949. The universal features of zonation between tide-marks on rocky coasts. The Journal of Ecology 37:289-305. ) and from the one described for the Brazilian coast (Coutinho et al., 2016Coutinho, R.; Yaginuma, L. E.; Siviero, F.; Santos, J. C. Q. P.; López, M. S.; Christofoletti, R. A.; Berchez, F.; Ghilardi-Lopes, N. P.; Ferreira, C. E. L.; Gonçalves, J. E. A.; Masi, B. P.; Correia, M. D.; Sovierzoski, H. H.; Skinner, L. F. & Zalmon, I. R. 2016. Studies on benthic communities of rocky shores on the Brazilian coast and climate change monitoring: status of knowledge and challenges. Brazilian Journal of Oceanography 64(SPE2):27-36.). Although the environmental conditions in the low intertidal zone are not suitable to host litorinids, mussels can act as facilitators for these snails (Borthagaray & Carranza, 2007Borthagaray, A. I. & Carranza, A. 2007. Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica 31(3):243-250.; Cartwright & Williams, 2012Cartwright, S. R. & Williams, G. A. 2012. Seasonal variation in utilization of biogenic microhabitats by littorinid snails on tropical rocky shores. Marine Biology 159(10):2323-2332.), facilitating an increase in the spatial range of fundamental niche species by mitigating the effects of niche reduction factors (Bruno et al., 2003Bruno, J. F.; Stachowicz, J. J. & Bertness, M. D. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology &Evolution18(3):119-125.). Thus, the fundamental niche of E. lineolata may be increased by the facilitation provided by mussel beds. This habitat-forming species decreases the effect of factors that, in its absence, would limit the distribution of E. lineolata on barnacle belt and bare rock habitats.

The bivalve I. bicolor was detected at mussel beds and algae habitat. It was the suspension feeder species most abundant in these feeding guilds. The presence of this invasive species is well documented in Brazil (Dias et al., 2013Dias, T. L. P.; Mota, E.; Almeida, S.; Gondim, A. I.; Rabelo, E.; Oliveira, J. & Christoffersen, M. 2013. Isognomon bicolor (CB Adams, 1845) (Mollusca: Bivalvia): First record of this invasive species for the States of Paraíba and Alagoas and new records for other localities of Northeastern Brazil. Check List 9:157-161.; Barroso et al., 2018Barroso, C. X.; Rabay, S. G. & Matthews-Cascon, H. 2018. Mollusks on recruitment panels placed in an offshore harbor in Tropical Northeastern Brazil. Arquivos de Ciências do Mar 51(1):65-74. ). Isognomon bicolor is native to Jamaica and was originally distributed in the Caribbean region (Domaneschi & Martins,2002Domaneschi, O. & Martins, C. M. 2002. Isognomon bicolor (CB Adams) (Bivalvia, Isognomonidae): primeiro registro para o Brasil, redescrição da espécie e considerações sobre a ocorrência e distribuição de Isognomon na costa brasileira. Revista Brasileira de Zoologia 19(2):611-627.). This bivalve is an example of a successful invasion in Brazilian coastal areas (Dias et al., 2013Dias, T. L. P.; Mota, E.; Almeida, S.; Gondim, A. I.; Rabelo, E.; Oliveira, J. & Christoffersen, M. 2013. Isognomon bicolor (CB Adams, 1845) (Mollusca: Bivalvia): First record of this invasive species for the States of Paraíba and Alagoas and new records for other localities of Northeastern Brazil. Check List 9:157-161.), and has sufficient dispersion capacity to interfere with the survival of native species (Breves-Ramos et al., 2010Breves-Ramos, A.; Junqueira, A. O. R.; Lavrado, H. P.; Silva, S. H. G. & Ferreira-Silva, M. A. G. 2010. Population structure of the invasive bivalve Isognomon bicolor on rocks shores of Rio de Janeiro State (Brazil). Journal of the Marine Biological Association of the United Kingdom 90(3):453-459. ; Martinez, 2012Martinez, A. S. 2012. Spatial distribution of the invasive bivalve Isognomon bicolor on rocky shores of Arvoredo Island (Santa Catarina, Brazil). Journal of the Marine Biological Association of the United Kingdom 92(3):495-503. ). During fieldwork, we observed predation of I. bicolor by S. brasiliensis, in which this gastropod consumes the invasive bivalve instead of the native mussel Brachidontes exustus. Taking into account the dispersive capacity and the potential to modify systems where it occurs, I. bicolor and its interactions with native species need to be further studied.

Rocky surfaces with no associated biological substrate presented low values in all taxonomic and functional components investigated. This is attributed to the high desiccation stress experienced on bare areas in rock intertidal systems. Diversity in these environments can be maintained by positive interactions that ameliorate physical stress (Silliman et al., 2011Silliman, B. R.; Bertness, M. D.; Altieri, A. H.; Griffin, J. N.; Bazterrica, M. C.; Hidalgo, F. J.; Caitlin, M.; Crain, C. M. & Reyna, M. V. 2011. Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS One 6(10):e24502.). This result confirms the effect of environmental modification caused by the presence of habitat-forming species. Chthamalus bisinuatus, Brachidontes exustus, and the macroalgae group act as habitat-forming species in the system studied. By providing habitat and protection, habitat-forming species facilitate distributions of organisms by reducing desiccation stress (Silliman et al., 2011Silliman, B. R.; Bertness, M. D.; Altieri, A. H.; Griffin, J. N.; Bazterrica, M. C.; Hidalgo, F. J.; Caitlin, M.; Crain, C. M. & Reyna, M. V. 2011. Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS One 6(10):e24502.). Furthermore, such organisms modify the landscape, increasing heterogeneity and, consequently, affecting associated communities (Lemieux & Cusson, 2014Lemieux, J. & Cusson, M. 2014. Effects of Habitat-Forming Species Richness, Evenness, Identity, and Abundance on Benthic Intertidal Community Establishment and Productivity. PLoS One 9(10):e109261. ; Gallucci et al., 2020Gallucci, F.; Christofoletti, R. A.; Fonseca, G. & Dias, G. M. 2020. The Effects of Habitat Heterogeneity at Distinct Spatial Scales on Hard-Bottom-Associated Communities. Diversity 12(1):1-13. ). Thus, the habitat-forming species identified provide niches capable of supporting different occupation patterns and therefore affect taxonomic and functional diversity in mollusk assemblages.

In summary, our results showed that the taxonomic and functional structure of mollusk assemblages in the tropical rocky intertidal zone varies between different types of habitat investigated. The structure of mollusk assemblages is a result of the interplay of many different biotic and abiotic drivers, many of them not considered here. Intertidal elevation, wave exposure gradients, seasonality, bottom-up and top-down effects, for example, are some of these features. These are interconnected processes that have a strong influence on the structure of rocky intertidal communities. These processes and their relation to the taxonomic and functional diversity of mollusk assemblages will be analyzed and discussed elsewhere.

Acknowledgments

We are grateful to Dr. Poliana Salve Guizardi for her assistance with fieldwork and Laboratório de Ecologia Bêntica (LEB) team for technical support. We thank the Editing, Translation and Proofreading Laboratory (Letrare) for English language editing. We also thank anonymous reviewers whose comments greatly improved this manuscript. This work was supported in part by the grant of the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) (Grant #. BOL0537/2012 to SMARS).

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  • Data availability.

    The datasets generated and analysed during the current study was deposited in the Open Science Framework repository, https://osf.io/6fhjr/. The data are available from the corresponding author on reasonable request and will be publicly available as soon as the manuscript is accepted for publication.

Publication Dates

  • Publication in this collection
    25 Nov 2020
  • Date of issue
    2020

History

  • Received
    10 July 2020
  • Accepted
    26 Oct 2020
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