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Intertidal Vermetid Reef As a Shelter for Invasive Bivalves in a Tropical Bay A

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Intertidal Vermetid Reef As a Shelter for Invasive Bivalves in a Tropical Bay A Intertidal vermetid reef as a shelter for invasive bivalves in a tropical bay A. Breves* and A. O. R. Junqueira Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Av. Pedro Calmon, 550 – Cidade Universitaria, Rio de Janeiro – RJ, 21941-901, Brazil *Corresponding author: [email protected] Vermetid reef building species play an important role as ecosystem engineers modifying the physical environment, creating microhabitats and affecting local hydro-sedimentary patterns. We explore the association of native vermetid reefs (Petaloconchus varians) with the invasive bivalves Isognomon bicolor and Leiosolenus aristatus. We also examined the different utilization of the reef habitat, since L. aristatus is a boring species, comparing their population structure on sheltered and exposed rocky shores. Ten sites (five sheltered, five exposed) were sampled at Ilha Grande Bay (Rio de Janeiro, Brazil). I. bicolor and L. aristatus were the most frequent with mean densities of 20,000 (§3400) and 2100 (§600) ind.m2, respectively. There were no significant differences (t D 1.41; p D 0.17) between sheltered and exposed sites in relation to the densities of I. bicolor. However, there were significant differences (t D 3.14; p D 0.03) in relation to the densities of L. aristatus, with higher values at exposed sites. Mean size of both species was significantly (p < 0.01) higher in sheltered areas where the vermetid weight was significantly higher (t D 2.36; p D 0.02). Although native vermetid reefs act as a shelter for both invasive bivalves on sheltered and exposed rocky shores, they prevent the growth of I. bicolor which reaches smaller sizes in relation to populations outside of the reefs. Our results indicate that the two invasive bivalves might be differently affected by hydrodynamic processes. Keywords: ecosystem engineer, Isognomon bicolor, Leiosolenus aristatus, Petaloconchus varians, Vermetidae Introduction the local hydro-sedimentary patterns and creating microhabitats which offer numerous niches for a The Vermetidae is a family of sessile marine large and often unique and diverse group of associ- gastropods with spiral irregular shells usually liv- ated species (Colombo et al., 2013). ing on hard substrata of warm-temperate to tropi- Petaloconchus varians (d’Orbigny, 1841) is a cal seas (Keen, 1961). One of the most interesting native vermetid from Rio de Janeiro (Brazil) and and significant aspects of the vermetids is related is currently a dominant species on intertidal rocky to their role as reef-builders, and they are among shores at Ilha Grande Bay (Moyses, 2007; Breves- the most important bioconstructors in the marine Ramos et al., 2010a,b; Ignacio et al., 2010). Indi- environment (Vescogni et al., 2008; Chemello and viduals of P. varians build a tridimensional reef Silenzi, 2011). Bioengineer reef building species where different organisms live, including are known to increase spatial complexity, affecting the invasive bivalves Isognomon bicolor (C. B. 384 Aquatic Ecosystem Health & Management, 20(4):384–392, 2017. Copyright Ó 2017 AEHMS. ISSN: 1463-4988 print / 1539-4077 online DOI: 10.1080/14634988.2017.1401416 Downloaded from http://read.dukeupress.edu/aehm/article-pdf/20/4/384/889310/384breves.pdf by guest on 25 September 2021 Breves and Junqueira/Aquatic Ecosystem Health and Management 20 (2017) 384–392 385 Adams, 1845) and Leiosolenus aristatus (Dillwyn, five sites on sheltered and five on exposed rocky 1817) (Breves-Ramos et al., 2010a,b). shores (Figure 1). Ilha Grande Bay, with an area These bivalves are native to the Caribbean Sea. of around 3,100 km2, has many inlets and 365 Isognomon bicolor was first recorded in Brazil by islands of varying sizes. The local climate is tropi- Domaneschi and Martins (2002) and the expansion cal wet (Silva et al., 1989) and surface seawater of this species along the coast occurred during the temperature is frequently warm, ranging from 24.4 early 1980s (Breves et al. 2014). Leiosolenus aris- to 28.4C (Creed et al., 2007). Surface salinity tatus was first recorded on the Brazilian coast by varies between 27 and 37% (Creed et al., 2007). Simone and Goncalves¸ (2006) in Ubatuba (S~ao At each sampling site, during low tides, a line Paulo) and Arraial do Cabo (Rio de Janeiro). This of 15 meters long was laid over the vermetid species was previously known as Lithophoga aris- band, parallel to the waterline. Five quadrats of tata (Dillwyn, 1817) and was called Myoforceps 100 cm2 were randomly positioned along the line aristatus in several references (Simone & Gon- and the area inside the quadrats was cut out to col- calves 2006; Breves-Ramos et al. 2010b; Ignacio lect the organisms inside the reef (Figure 1). The et al. 2012; Gomes et al. 2014). It is now included material within each quadrat was placed in plastic in the synonymy of Leiosolenus aristatus (Huber, bags, fixed in 70% ethanol and transported to the 2012). laboratory. Understanding the ecological processes under- Five reef blocks from each site were air-dried lying bioinvasion, such as facilitation, increase our for about 1 hour and weighed on a digital scale in chance to predict where and when invasion is order to estimate the weight of P. varians reefs, as likely to happen (Sueiro et al., 2013). Suitable a measure of structural complexity. Then, each hard substrates are limiting resources for non- reef block was broken into small pieces, washed in native species and one of the key factors affecting running tap water, sieved through a 1 mm mesh, their establishment and subsequent population and the malacofauna was sorted. The invasive growth (Heiman et al., 2008). The impact that bivalves were deposited in the Malacological Col- native species have on the survival, persistence lection of the Museu Nacional, UFRJ (MNRJ18 and/or range-expansion of invasive species is 651-18 674 [L. aristatus] and MNRJ18 907–18 receiving attention from ecologists (Sueiro et al., 931 [I. bicolor]). 2013). Studies that show how a native ecosystem The frequency of occurrence of the invasive engineer can enhance the success of invasive bivalves was calculated through the relationship of species and facilitate their local spread are very the number of blocks in which the species were necessary (Sueiro et al., 2013). Concerning man- present and the total number of samples at each agement strategies for the marine environment, site. Low frequency species occurred between the use of ecosystem engineers in restoration prac- 0.01 and 0.2; Frequent between 0.2 and 0.59; High tices could enhance overall biodiversity but at frequent between 0.6 and 1.0. the same time create opportunities for invaders The population structure of I. bicolor and L. (Bulleri et al, 2008). aristatus was assessed by their mean total den- The present study aimed to explore the associa- sity (live and dead individuals) and size. The tion of the invasive bivalves I. bicolor and L. aris- mean number of individuals was obtained for tatus with native reefs of P. varians. We also each site. For all living individuals, length of examined the different utilization of the reef habi- the shell was measured with a caliper with a tat by these invasive species, comparing their pop- 0.05 mm precision. ulation structure on sheltered and exposed rocky Spearman correlation analyses were performed shores. using the software GraphPad Prism 5.0. It was used to assess the relationship of the weight of the reef of P. varians with the densities of I. bicolor Methodology and L. aristatus. Correlation analysis was also con- ducted to test the relationship between the densi- This study was carried out in Ilha Grande Bay ties of L. aristatus and I. bicolor. A t-test (Student (latitude 23150S; longitude 44300W), in the test) was performed in order to compare the weight southern region of Rio de Janeiro State (Figure 1). of P. varians reefs between sheltered and exposed In 2008, we surveyed ten sites in Ilha Grande Bay: sites. It was also used to compare the densities and Downloaded from http://read.dukeupress.edu/aehm/article-pdf/20/4/384/889310/384breves.pdf by guest on 25 September 2021 386 Breves and Junqueira/Aquatic Ecosystem Health and Management 20 (2017) 384–392 Figure 1. Map of Ilha Grande Bay (Rio de Janeiro, Brazil) indicating the sampling sites (sheltered D black circles; exposed D white circles). Photograph of the reefs of Petaloconchus varians on mid intertidal rocky shores (black bar) in: (a) Coqueiros Beach (site 6) and (b) Cunhambebe Island (site 1). (c) Photograph of one quadrat cut out and the organisms inside the reefs scraped (scale bar D 5 cm). size of I. bicolor and L. aristatus between shel- of living individuals (Table 1). The mean density tered and exposed sites. of L. aristatus was 2118 (§1989) ind.m2 with a low number of dead individuals (Table 1). There was no significant correlation between the Results densities of L. aristatus and I. bicolor (n D 50; r D¡0.16; p > 0.05). Petaloconchus varians was present in high There were no significant differences (t D abundance on intertidal rocky shores in Ilha 1.41; p D 0.17) between sheltered and exposed Grande Bay. The mean weight of the reefs of P. sites in relation to the densities of I. bicolor varians was significantly higher (t D 2.36; p D (Figure 3). However, there were significant dif- 0.02) at sheltered sites (76,692 § 26,920 g.m2) ferences (t D 3.14; p D 0.03) in relation to the than at exposed sites (53,839 § 27,345 g.m2). densities of L. aristatus, with higher values at Considering all studied sites, the invasive exposed sites (Figure 3). A positive and signifi- bivalves I.
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