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.

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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

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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

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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. bicolor and L. aristatus were the most cant correlation was found between the reef frequent mollusk species other than P. varians in weight and the density of I. bicolor (n D 50; the reefs, occurring in 100% of the sampling r D 0.74; p < 0.05). This correlation was how- blocks. ever negative and not significant for L. aristatus Since the reef presented different layers, living (n D 50; r D¡0.17; p > 0.05). individuals of I. bicolor were recorded on the sur- The mean, minimum and maximum length of I. face (Figure 2). On the other hand, we observed bicolor and L. aristatus are presented in Table 2. most of the dead individuals of I. bicolor in the The size of both I. bicolor and L. aristatus was sig- internal layers of the reef, including the lower nificantly higher (respectively, t D 4.59; t D 11.52; layer attached to the substrate (Figure 2). Living p < 0.01) at protected sites. Size of the individuals and dead individuals of L. aristatus were found in of I. bicolor was between the classes 2 to 14 mm, internal layers of the reef forming tunnels with modes in classes 4 to 6 mm at most of the (Figure 2). studied sites. A few individuals of larger sizes The mean density of I. bicolor was 20 008 were observed on the surface of P. varians reefs. (§10,794) ind.m2. Densities of dead individuals of In the present study we registered large size ranges I. bicolor were, in general, much higher than those for L. aristatus, reaching about 40 mm.

Figure 2. Photographs of Petaloconchus varians (scale bar D 10 mm): (a) Lateral view of the reef with erect and irregular shells; (b) the reef surface with living individuals of Isognomon bicolor (black arrows); (c) lower layer of the reef with dead individuals of I. bicolor (grey arrows); (d) specimen of the boring Leiosolenus aristatus (white arrow).

Discussion exposed sites. This was ﬁve times lower than values observed by Breves-Ramos et al. (2010a) Petaloconchus varians was abundant and domi- 15 years before the present study, at Brand~ao nant on the mid intertidal of sheltered and exposed Island, in the same bay. This decrease in the den- rocky shores in Ilha Grande Bay. The weight of P. sity of I. bicolor had already been observed in varians reefs was signiﬁcantly higher at sheltered other regions on the coast of Rio de Janeiro State sites, according to Laborel (1977), who suggested (Breves-Ramos et al., 2009; Lopez et al., 2010). this species prefers relatively calm waters. The number of dead individuals was higher com- According to Barash and Zenziper (1985), life in pared to living ones at most of the studied sites. dense aggregations is at an advantage due to the Breves-Ramos et al. (2010a) suggested that the competitive superiority by the monopolization of high mortality of I. bicolor occurs because the space. individuals were found imbedded in the reef struc- Isognomon bicolor, although not a dominant ture, compared to other areas without reefs where species as observed elsewhere (Breves-Ramos the broken shells were loosened among the rocks. et al., 2010a), was found at all sampling sites in Furthermore, according to these authors the high Ilha Grande Bay. Oliveira and Creed (2008) also mortality of I. bicolor can also occur because the registered this species in 31 sites in this bay, reef apparently is an environment with a high although in the sublitoral zone. This species has amount of organic matter, a low internal water cir- well established populations on the coast of Rio de culation and also with greater competition and pre- Janeiro State, with local variations in its density dation. However, other studies focusing on the and individual size (Breves-Ramos et al, 2010a). trophic ecology in the reefs of P. varians are nec- Furthermore, it has been found in many locations essary to verify the exact effects of the ecological along the Brazilian coast (Breves-Ramos et al., relationships. 2010a; Lopez et al., 2010; Zamprogno et al., Most individuals of I. bicolor were of a smaller 2010). size compared to populations outside the reefs in The mean total density of I. bicolor was 20,008 other locations of Rio de Janeiro State, mainly in ind.m2 with no differences between sheltered and eutrophic regions with more nutrients in the water

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Table 1. Mean densities (§standard deviation) of the invasives Isognomon bicolor and Leiosolenus aristatus in sheltered (S) and exposed (E) rocky shores in Ilha Grande Bay.

I. bicolor L. aristatus S Live Dead Total Live Dead Total 1 3400 (§2100) 22,700 (§31,500) 26,000 (§33,500) 400 (§200) 100 (§100) 500 (§300) 2 3000 (§1500) 10,000 (§3900) 13,100 (§4900) 800 (§400) 100 (§100) 900 (§400) 3 1900 (§700) 6700 (§2300) 8600 (§2800) 1500 (§200) 100 (§100) 1600 (§200) 4 3900 (§1600) 25,600 (§17,100) 29,500 (§18,200) 1300 (§600) 100 (§100) 1400 (§600) 5 5700 (§1600) 35,300 (§25,700) 41,000 (§27,200) 800 (§600) 100 (§100) 900 (§600) E 6 2200 (§2500) 19,300 (§5500) 21,500 (§7600) 800 (§1700) 400 (§200) 1200 (§1700) 7 4500 (§2500) 20,200 (§9600) 24,700 (§8900) 1800 (§600) 2400 (§1100) 4200 (§1600) 8 2500 (§600) 14,000 (§8700) 16,600 (§8900) 800 (§600) 0 (§0) 800 (§600) 9 4000 (§2000) 10,500 (§19,800) 14,500 (§18,900) 6600 (§5600) 100 (§100) 6700 (§5500) 10 3500 (§500) 1000 (§1000) 4600 (§700) 2800 (§1500) 300 (§200) 3200 (§1600) Breves and Junqueira/Aquatic Ecosystem Health and Management 20 (2017) 384–392 389

Figure 3. Mean densities of Isognomon bicolor and Leiosolenus aristatus in the reefs of Petaloconchus varians on sheltered (black bar) and exposed (white bar) rocky shores in Ilha Grande Bay.

(Breves-Ramos et al., 2010a; Zamprogno et al., Ignacio et al., 2012). In Ilha Grande bay, P. varians 2010). The highest frequency of small individuals is an important substrate for the population of L. in Ilha Grande Bay was probably because the reefs aristatus. The mean density of L. aristatus inside of P. varians are a physical barrier for the growth the reefs was much higher than that found by Igna- of I. bicolor. The great adaptive capacity, as well cio et al. (2012) on shallow rocky shores as the variation in morphological characteristics of (0.5 meters deep) without reefs of P. varians in I. bicolor, such as its quite irregular shell, allows Gipoia and Itanhanga islands (12–15 ind.m2), both the specimens to live in small crevices and cavities in Ilha Grande Bay. The densities found in our (Domaneschi and Martins, 2002; Moyses et al., study were also higher than that found by Gomes 2007) or in reefs as is the case in this study. et al. (2014) on intertidal rocky shores in There were differences in the size of I. bicolor Marataızes and Piuma (300–500 ind.m2), on the in relation to the wave exposure. The size of I. coast of Espırito Santo State. In other regions of bicolor was larger in protected sites where P. var- Rio de Janeiro State, such as in Rio das Ostras at ians was more abundant. This study did not cor- 23 meters deep (1600 ind.m2) (Gomes et al., roborate previous studies which found larger sizes 2014); in the municipality of Arraial do Cabo (385 out of reefs in more exposed sites (Lopez, 2008). § 140 ind.m2) in the infralittoral fringe (Ignacio Leiosolenus aristatus is a boring species which et al., 2012); and in Sepetiba Bay (143 § 26 ind. recently expanded its distribution rapidly along the m2) on subtidal artiﬁcial substrate (Ignacio et al., Brazilian coast (Simone and Goncalves,¸ 2006; 2012). Breves-Ramos et al. 2010b; Agudo-Padron, 2011; According to Gomes et al. (2014), the differen- Gomes et al., 2014) and in other countries of the ces in densities suggest that local conditions might Eastern Atlantic Ocean (Lopes, 2011). This species be the key to the invase success of L. aristatus, has a potential to cause economic and environmen- since types of substrate, depth and wave exposure tal problems (Valentich-Scott and Dinesen, 2004; did not indicate a clear association with species

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Table 2. Mean size and range of the length (mm) of the shells of Isognomon bicolor and Leiosolenus aristatus in in sheltered and exposed rocky shores in Ilha Grande Bay. n D number of individuals measured.

I. bicolor L. aristatus Sites n Mean/Min.-Max. n Mean/Min.-Max. Sheltered 1 131 5.18/2.13–12.92 16 16.61/2.33–28.12 2 145 5.58/1.46–13.18 35 18.97/3.67–36.4 3 90 7.44/4.28–17.88 59 17.99/2.18–27.07 4 140 7.22/1.75–15.82 38 17.86/7.2–28.59 5 150 9.26/1.12–20.54 30 25.80/9.60–38.43 Exposed 6 96 5.83/1.81–12.28 22 19.50/10.3–24.81 7 123 4.36/1.33–11.74 63 12.61/2.99–28.39 8 106 6.14/2.00–15.23 36 14.46/2.17–26.25 9 154 8.85/2.09–20.96 227 13.44/3.57–27.64 10 152 4.98/1.36–15.33 99 11.78/3.54–21.52

density. On the other hand, we found significant knowledge of a native engineer species which pro- differences between sheltered and exposed sites in vides habitat for non-native species and their eco- relation to the densities of L. aristatus, with higher logical interrelationships. values at exposed sites. Previous studies (Santos and Creed, 2011) indicated an interaction between L. aristatus and the invasive coral Tubastrea spp., Conclusions which provides substrate for the bivalves in Petaloconchus varians reefs act as a shelter for exposed areas at Ilha Grande Island. the invasive bivalves I. bicolor and L. aristatus. Unlike what occurs to I. bicolor, the reefs of P. The reefs of P. varians prevent the growth of I. varians do not seem to be inhospitable or a physi- bicolor, except for a few individuals on the reef cal barrier for the growth of L. aristatus. Instead, surface. In contrast, they were not a physical bar- since L. aristatus is a boring species in shells of rier for the growth of L. aristatus. Our results sug- other mollusks (Valentich-Scott and Dinesen, gest that I. bicolor is more affected by the 2004; Owada, 2007), the reefs of P. varians on structural complexity of the reefs while L. arista- intertidal rocky shores facilitated their occurrence. tus seems to be more affected by hydrodynamic Moreover, mean size of this species was higher in processes. sheltered sites where the weight of P. varians was significantly higher. The complexity of habitats created by hard-shelled organisms of the recipient Acknowledgements community seems to be essential to the successful colonization of new environments by this species We thank the staff of Setor de Malacologia/ (Ignacio et al., 2012). MN, Laboratorio de Benthos/UFRJ and Labo- The two mentioned invasive species have differ- ratorio Integrado de Ficologia/UFRJ for helping in ent interactions with the reefs. While I. bicolor is field work and Thomas Sprengers for the English more affected by the reef or by the increase in revision. structural complexity of its surface, L. aristatus is more affected by hydrodynamic processes. It is Funding known that the same organisms that are affected by bioengineers can also be affected by physical char- We would like to thank Conselho Nacional de acteristics of the habitat (Lenihan, 1999; Schwindt, Desenvolvimento Cientıfico e Tecnologico (CNPq) et al., 2001). This manuscript contributed to the for the PhD scholarship granted to the first author;

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