Fluctuating asymmetry as a pollution monitor: The Australian estuarine smooth toadfish Tetractenos glaber (Teleostei: Tetraodontidae)
Graphical abstract
Introduction
Estuarine environments adjacent to large cities are subjected to a wide range of anthropogenic activities. Organisms living in these areas are exposed to alterations resulting from agricultural, industrial and engineering projects, overfishing and other human-related activities associated with urbanization and industrialization (Haedrich, 1983). One of the most serious anthropogenic stresses in estuaries is associated with increased concentration of pollutants of various types (Long and MacDonald, 1998). Knowing the biological effect of pollution is important for predicting the future status of biological systems, at the level of organisms, populations and communities, and to predict their responses to changes in the environment. There are a number of approaches to assess such effects, depending on the type of biological system and parameter, and on the focus of the particular research (Newman, 2014).
One approach uses developmental instability, which reflects the ability of an organism to follow a developmental trajectory defined for a given genotype and environment (Zakharov, 1989). The most common measure of developmental instability is fluctuating asymmetry (FA), which is a departure from perfect morphological symmetry. This index has attracted increasing attention as a surrogate of fitness and therefore a measure of the effect of various environmental stressors since the late 1980s–early 1990s (Palmer and Strobeck, 1986, Zakharov, 1989, Parsons, 1990, Graham et al., 1993). After a decade of intensive use of the technique, some studies yield results that were far from researcher's expectation and disagreed with other fitness indicators, which initiated hot debates about the utility of FA as an indicator of stress and fitness (for instance, Bjorksten et al., 2000a and the following discussion: Møller, 2000, Van Dongen and Lens, 2000, Bjorksten et al., 2000b).
Empirical research showed that heritability of FA is usually low, but not zero, and in some studies approaches statistical significance (Leamy and Klingenberg, 2005, Johnson et al., 2008, Loehr et al., 2012). Modelling confirms the necessity of large samples to obtain significant results on heritability because of high sampling error associated with FA measurement (Fuller and Houle, 2003, Van Dongen, 2007). Theoretical analyses reveal that stress reduces energy available for growth and reproduction (Parsons, 1990, Parsons, 2005, Hoffmann and Parsons, 1991, Graham et al., 2010), and, because control over growth processes is also energetically costly (Koehn and Bayne, 1989, Sommer, 1996), reduces energy allocated for developmental control, which may lead to increase of developmental instability under stress (Lajus, 2014). Therefore, an absence of a detectable response of stressed populations in terms of FA in empirical studies is probably due to a high sampling error or to methodological problems.
The effects of pollution on fish stress, resulting in increased FA, has been shown in many instances: higher levels of FA were observed in the California grunion Leuresthes tenius affected by industrial pollution (Valentine and Soule, 1973, Valentine et al., 1973); in three-spined stickleback Gasterosteus aculeatus from industrially polluted waters (Zakharov, 1981); in roach Rutilus rutilus from water bodies receiving warmed industrial effluents of a nuclear station (Zakharov and Ruban, 1985); in bluegill Lepomis macrochirus, exposed to mercury contamination (Ames et al., 1979); in Crucian carp Carassius auratus from locations in Chernobyl area with different level of radioactivity (Zakharov et al., 1996) and varying in industrial pollution (Romanov and Kovalev, 2004); in channel catfish Ictalurus punctatus reared in sublethal concentrations of isopropyl methylphosphonic acid (Green and Lochman, 2006), and in dolly varden Salvelinus malma affected by contamination caused by active volcanism in Kamchatka (Esin, 2015). In several other studies relationship between FA and contamination was not found or was found for only some characters (Østbye et al., 1997, Chebotarev and Iziumov, 2001, Kenney and von Hippel, 2014, Lajus et al., 2014). In general, in fish FA is now routinely used for assessment of stress and fitness (Allenbach, 2011).
To effectively use FA to monitor effects of pollution in the marine environment, the species under study should exist under a wide gradient of pollution, to be locally resident, and preferably feed on bottom fauna to allow direct access to sediment pollution. Also, it should have a sufficient number of convenient morphological structures for accurate analysis of FA. The smooth or common toadfish Tetractenos glaber (Tetraodontidae) meets these requirements. This species is widely distributed in south eastern Australia (Kuiter, 1993, Booth and Schultz, 1999), is reasonably abundant and plays a significant role in communities (e.g. Thresher, 1984). Resident populations prey on local benthic invertebrates and it represents a convenient bioindicator species (Booth and Schultz, 1999, Alquezar et al., 2006a, Alquezar et al., 2006b). Recruitment occurs in late spring to sites along an entire estuary form full salinity to almost freshwater (Booth and Schultz, 1999). Moreover, bony fishes allow analysis of FA of a large number of bilateral characters with a reasonable measurement error (ME) (Lajus, 2001, Lajus et al., 2003a, Yurtseva et al., 2010). Concentrations of heavy metals in toadfish tissues are higher in more polluted locations of estuaries in the Sydney region than in cleaner areas (Alquezar et al., 2006a) and such differences are associated with variations in lipid and protein concentrations in fish tissues, suggesting that heavy metals may influence life history parameters of the toadfish (Alquezar et al., 2006b). Sydney Harbour estuary has been intensively studied in terms of toxic effect on biota (Birch and Taylor, 2002a, Birch and Taylor, 2002b, Birch and Taylor, 2002c, Birch et al., 2008). Metals (Cu, Pb and Zn) are of particular concern in Sydney Harbour estuary because they bioaccumulate in tissue of local filter-feeding animals (mussels and oysters) (Scanes and Roach, 1999, Birch and Apostolatos, 2013, Birch et al., 2014), and in prawns (Lewtas et al., 2014) and fish (Chvojka, 1998, Alquezar et al., 2006a, Alquezar et al., 2006b). In all cases, metal tissue concentrations are higher in locations with elevated sediment metals.
The objective of this study was to use FA techniques to study effects of sediment pollution on smooth toadfish at different locations in Sydney area and to consider it as a potential predictor of environmental pollution status in fishes. To inform interpretation of FA asymmetry patterns, we studied variation of mean values characterizing bone shape.
Section snippets
Sites and species
The samples were collected in 1995–2001 from ten locations in the Sydney region, New South Wales, Australia (Fig. 1, Table 1) by beach seines and hook and line. In total, 188 specimens were analysed, from 10 to 38 per sample. Samples were collected in two estuaries — Hawkesbury River (five samples, 116 individuals) and Sydney Harbour (five samples, 72 individuals), which are about 30 km apart. Individuals were sexed and total length was measured. Geographical distances for all pairs of sites
Pollution patterns
Sediment pollution in Sydney Harbour estuary was considerably higher than in the Hawkesbury River estuary (Table 2). Average MERMQ levels in Sydney estuary exceeded Hawkesbury levels 2.3-fold in heavy metals, and 4.4-fold in organic pesticides. Higher average pollution was observed in all individual pollutants except ligands, which were absent. The use of MERMQ techniques shows that heavy metals have a low risk of toxicity in all but two sites situated in Sydney estuary (Table 2). Risk of
Discussion
We have shown that organic pollution in the Sydney area is linked to increased developmental instability for fish from the most polluted sites, with pollution characterized by the MERMQ approach (Long et al., 2006). Pollution can influence aquatic organisms on different levels (Newman and Clements, 2007). If accumulated in fish body tissue, heavy metals or other pollutants can directly influence metabolism and development of fish (Sindermann, 1979, Heath, 1995, Newman and Clements, 2007).
Conclusion
In our study FA approached statistically significant association with pollution level, but quantitatively this association is not very strong — only about 5% of total variance in FA on an individual fish level was associated with organic pollution. On a sample level percentage of variance explained by organic pollution was higher — about 35%, but statistical significance was lower. Our toadfish study confirms the suggestion that absence of association between FA and environmental stress quite
Acknowledgements
The study was supported by visiting researcher grants from University of Technology, Sydney Vice Chancellors Travel Fund, to D.L. in 2001 and 2003 and to D.B. in 2002. Data analyses were done with support of the Russian Scientific Fund, grant 14-14-00284. Thanks to John Lee for assistance in drafting. Thanks to Ralph Alquezar for fish collections and processing.
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