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Assessing the Continuous Impact of Tributyltin from Antifouling Paints In Hindawi Publishing Corporation International Journal of Oceanography Volume 2013, Article ID 769415, 8 pages http://dx.doi.org/10.1155/2013/769415 Research Article Assessing the Continuous Impact of Tributyltin from Antifouling Paints in a Brazilian Mangrove Area Using Intersex in Littoraria angulifera (Lamarck, 1822) as Biomarker M. B. Costa,1,2 G. C. Zamprogno,1,2 F. C. Pedruzzi,1,3 G. B. Dalbem,1 andM.M.P.Tognella2 1 Biological Sciences Department, Federal University of Espirito Santo, Vitoria,´ ES, Brazil 2 Center for Human and Natural Sciences, Postgraduate Program in Environmental Oceanography, Federal University of Espirito Santo, Vitoria,´ ES, Brazil 3 Institute of Oceanography, Postgraduate Program in Coastal Management, Federal University of Rio Grande, Rio Grande, RS, Brazil Correspondence should be addressed to M. B. Costa; [email protected] Received 1 October 2013; Accepted 4 November 2013 Academic Editor: Heinrich Huhnerfuss¨ Copyright © 2013 M. B. Costa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Intersex is a sensitive biomarker of TBT exposure and effects in littorinid gastropods and described for the mangrove periwinkle Littoraria angulifera for the first time in this study. The objective was to describe the occurrence of intersex in L. angulifera,to propose the species as a sentinel organism to assess TBT contamination, and to characterize the contamination in mangroves. The study was carried out in 2009 by sampling at 20 stations near harbors and marinas and at a reference station on the coast of Esp´ırito Santo Estate, Brazil. At the reference station, no intersex specimens were found, while at 20 sampling stations 51% of the females exhibited different degrees of intersex development, including the occurrence of functionally sterilized females. The highest incidence of intersex and greatest intersex intensities was found in areas close to marinas and shipyards indicating that vessel- related activities are still the main source of TBT contamination. L. angulifera collected from stations in areas with well-preserved mangroves was larger than specimens collected from other areas. These differences are attributed to environmental quality and not to occurrence of intersex. The results indicate that this region is still affected by TBT contamination andthat L. angulifera has the required sensitivity to be used as a bioindicator. 1. Introduction considered the most toxic xenobiotic substance deliberately introduced into the environment [4, 5]. Estuarine systems are highly complex and dynamic envi- TBT can cause various negative effects in multiple tax- ronments due to the spatiotemporal variability of their onomic groups, but mollusks are among the most sensitive physicochemical parameters and the influence of a variety of invertebrates to this substance [6]. To these species, TBT natural and anthropogenic stressors that may affect the health and stability of these ecosystems [1]. However, the effects of acts as an endocrine disrupter, affecting wild populations stressors and their interaction with individual components of of marine gastropods by means of the syndromes called an ecosystem remain unknown [1–3]. imposex and intersex [7–13]. Anthropogenic activities in ports, such as shipping and Imposex is defined as a process of masculinization char- vessel painting and repair, contaminate sediment and the acterized by development and superimposition of male sex- biota. Tributyltin (TBT), a biocide used in marine antifouling ual characteristics (penis and vas deferens) in females. This paints, contributes to this contamination. TBT exhibits the phenomenon is widely distributed, and currently, approxi- highest toxicity among organotin compounds (OT) and is mately 220 known species of neogastropods are affected14 [ ]. 2 International Journal of Oceanography Imposex is the most widely used biomarker for this type of TBT contamination using intersex as a biomarker in Victoria contamination [15]. Harbor and the Bay of Esp´ırito Santo, southeastern Brazil. Intersex, another important biomarker for TBT was first observedin1993,onthecoastofGermany,whenmalforma- 2. Materials and Methods tions observed in the pallial reproductive tract of the female gastropod Littorina littorea (Linnaeus, 1758) [9, 16]were 2.1. Study Area. Thisstudywasconductedin2009,around −1 related to TBT contamination at levels around 10 ng L Sn the city of Vitoria and at a reference site (RS) in the city [17]. This syndrome is characterized by a phenotypic disorder of Serra (Figure 2). The city of Vitoria is highly urbanized in the reproductive tract and the gradual transformation of and has several ports, including the Port of Tubarao˜ and the pallial female reproductive organs into male structures which Vitoria Port Complex. In addition to these ports, the region is classified by five morphological stages (Figure 1): Stage 0, includes several marinas that support fishing, recreation, normal female without evidence of intersexuality; Stage 1, the and small vessel maintenance. The reference site was char- female genital opening is enlarged and the proximal bursa acterized by the lack of apparent OT contamination because copulatrix is divided ventrally; Stage 2, division of the ventral all L. angulifera specimens collected in this area were free portion of the pallial oviduct, which exposes the inner lobes; of intersex and all specimens of Leucozonia nassa collected Stage3,theglandsofthepallialoviductarepartiallyor between 2006 and 2012 in this area did not exhibit imposex completely supplanted by a prostate gland; Stage 4, finally, the (Costa et al., accepted manuscript). penis and seminal groove are formed. The females in this state do not exhibit spermiogenesis. According to Bauer et al. [16], 2.2. Intersex Analysis. Forty L. angulifera individuals were in Stages 2–4, the morphological malformation of the oviduct collectedatthereferencesite(RS)andateachofthe20 inhibits the formation of capsules and the copulation, which sampling stations in the Vitoria Harbor and the Bay of the leads to sterilization of females. Espirito Santo region. All specimens measured above 10 mm After the initial reports on intersex a number of studies and were considered sexually mature. The sample size and were performed [7–9, 11, 12, 18–21], especially in locations sexual maturity were selected according to De Wolf et al. where TBT contamination levels are quite high and therefore [11]. The animals were transported to the laboratory, kept in neogastropod species are not found. The main parameter for tanks containing a 1 : 1 ratio of seawater to distilled water, and quantifying the intensity of intersex in populations is the were anesthetized in a 4% MgCl2 solution. Measurements index of intersex (ISI), calculated as the mean value of each ofshelllength(mm)weretakenwithaMytutoyocaliper. sampledintersexstageproposedbyBaueretal.[16]. The shells were broken and the snails analyzed under a Due to the toxic effects of TBT, antifouling paints con- stereomicroscope. The sex ratio (M : F) was determined taining this substance were banned in many countries, but according to Birchenough et al. [33] for all stations. Values its use persists in many regions of the world, especially in less than 1 indicate a shift of the sex ratio in favor of females, developing countries such as Brazil [22]. In these locations, values greater than 1 in favor of males. The percentage or organotin compounds such as tributyltin are currently being incidence of intersex was calculated by the proportion of produced and marketed [23]. Recent studies have indicated females with masculine features, and the intersex index (ISI) thatthesecompoundsarestillbeingusedinsomeareasand was determined according to [9, 16] considering the five high concentrations of this compound are still found in the stages proposed by these authors. environment [24]. Until now, contamination from OTs in Brazil has mainly 2.3. Littoraria angulifera. L. angulifera (Figure 3(a))isatrop- been studied using imposex in several species of Neogas- ical littorinid species found almost exclusively in mangroves. tropods, such as Stramonita haemastoma (Linnaeus, 1758) This species has separate sexes (Figures 3(b) and 3(c))andis [25–27], Thais rustica (Lamarck, 1822) [28], Thais deltoidea ovoviviparous with a planktotrophic larval stage [34]. Adults (Lamarck, 1822) [29], Leucozonia ocellata (Gmelin, 1791), are found on the upper shore zone on the trunks, roots, and Leucozonia nassa (Gmelin, 1791) (Costa et al., accepted leaves of mangrove trees. The species is also found on artificial manuscript), and Cymatium parthenopeum parthenopeum substrate or rocky shores, where they feed on fungi and algae. (von Salis, 1973) [30], of the order Caenogastropoda. The normal structure of the genital system in L. angulifera is Caenogastropods are recognized as being less sensitive documented in Merkt and Ellison [35]. to contamination by OTs [31, 32], but where neogastropods are not present, such as in mangrove areas, species of 2.4. Data Analysis. The Kruskal-Wallis test was used to Caenogastropods may present an option for monitoring the compare the values of the ISI at each sampling area. The presence of this contaminant. test of multiple comparisons was performed aposteriori. Studies investigating OT contamination using bioindica- Correlations between percentage of intersex
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