Fluctuating Asymmetry in the Size of the Otolith of Engraulis Australis

Marine Pollution Bulletin 168 (2021) 112391

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Marine Pollution Bulletin

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Baseline Fluctuating asymmetry in the size of the otolith of Engraulis australis (Shaw, 1790) recovered from the food of the Australasian gannet, Morus serrator, Hauraki Gulf, New Zealand

Laith A. Jawad a,b,*, Nigel J. Adams b a Pokeno, Auckland 2417, New Zealand b School of Environmental and Animal Sciences, Unitec Institute of Technology, Auckland, New Zealand

ARTICLE INFO ABSTRACT

Keywords: The fluctuating asymmetry values of the two otolith parameters: length and width of Engraulis australis, recov Bilateral asymmetry ered from the food of gannet, which inhabit colonies in islands at Hauraki Gulf, New Zealand was calculated in Otolith length this study. The dissimilarity value of the otolith width was higher than that of the otolith length. An inclination of Otolith width upsurge in the dissimilarity values with the fish length was noted for the otolith sizes studied. The dissimilarity Pollution value in the two otolith sizes was the lowest for fishhaving total length of 115–154 mm, and the highest for fish Morphometry with length of 151–160 mm. The conceivable reason of the dissimilarity obtained could be related to diverse contaminants and their presence in the study location.

Somarakis et al. (1997) have proposed that the measurements of the at two gannet colonies located within the Hauraki Gulf, off the north fluctuating asymmetry will be useful as an indicator of the fish condi eastern side of the North Island of New Zealand on two occasions, tion, because it has been revealed that this condition is a subtle indicator January 2018 and 2019. We sampled gannets in December and January of stress (Clark, 1992). Consistent with this, the fluctuating asymmetry when the adult birds were attending numerous chicks and making reg has served as a bio index to check the health status of different organ ular trips to coastal waters to collect food to feed their chicks. isms present (Somarakis et al., 1997) or to check the impact of pollution Adult gannets were caught at their breeding colony immediately on (Hardersen, 2000) on fishpopulations. The use of asymmetry in otoliths their arrival to feed the chicks. Such birds showed frequent and spon as an indicator of historically stressful environmental factors is helped taneous regurgitation of food when caught. In general, the prey in the by the fact that otolith characters examined by Somarakis et al. (1997) stomach of near-shore feeding gannets is often intact such that the fish did not exhibit any relation to size or age. can be separated and otoliths can be extracted from the skull. After Fluctuating asymmetry studies on the otolith sizes of the Australian collection, food samples were placed in plastic bags and kept chilled in anchovy E. australis from the New Zealand waters are not available. an insulated container with freezer blocks. Eventually, the samples were Consequently, the aim of the present study is to determine the amount of frozen for preservation. Once back at the laboratory, the samples were bilateral dissimilarity in both otolith sizes of E. australis, which is a defrosted for analysis and removal of the otoliths. common fishconsumed by gannets (Robertson, 1992). Accordingly, we A total of 55 whole, intact fish specimens were obtained from the collected sample anchovies from regurgitations of the gannets returning gannet’s food samples. The whole fish specimens were selected; thus, to their colonies from Hauraki Gulf, New Zealand. Although the fish their sizes are known. The specimens were washed with water to remove specimens were obtained from the food of these piscivorous birds, the any adhering food remains. Total length (LTL) was measured to the asymmetry study results from this study are of importance and can be nearest 1 mm from the anterior point of the snout to the back point of the used for comparative studies of the specimens from the wild, in the tail fin. Otoliths (sagittae) were extracted from both sides of the fish future. head by an incision in the skull to uncover the otolith, and then washed The fish analysed for this study were recovered from regurgitations and kept dry in plastic containers. The otoliths of specimens having wide of the Australasian gannet (Morus serrator). Collections were conducted range of length were collected from the food of gannets to ensure that

* Corresponding author at: Pokeno, Auckland 2417, New Zealand. E-mail address: [email protected] (L.A. Jawad). https://doi.org/10.1016/j.marpolbul.2021.112391 Received 19 December 2020; Received in revised form 23 March 2021; Accepted 4 April 2021 0025-326X/© 2021 Elsevier Ltd. All rights reserved. L.A. Jawad and N.J. Adams Marine Pollution Bulletin 168 (2021) 112391 the obtained sample is more represented and the evaluated factors are Table 2 more forceful. Each otolith was positioned under a dissecting micro Squared coefficientof asymmetry and character means by size class of Engarulis scope to locate sulcus acusticus upward; thus, their length was measured australis retrieved from food of gannet inhabiting islands in Hauraki Gulf, New on the axis between the rostrum and post rostrum axis. Zealand. 2 Statistical calculations were built on the squared coefficient of Character CV a N Character mean (mm) % of individuals with 2 ± dissimilarity variation (CV a) for the two otolith sizes conferring to SD asymmetry Valentine et al. (1973): Otolith length 110–120 19.1 6 7.31 ± 1.1 90 2 2 CV a = (S r l X 100/X r + l) 121–130 19.9 10 7.29 ± 2.3 89 131–140 20.2 9 6.82 ± 2.3 69 where S r-l is the standard deviation of signed variances and X r + l is the 141–150 21.7 20 7.33 ± 1.2 98 – ± mean of the feature, which is considered by adding the absolute counts 151 160 22.3 10 7.54 1.5 89 for two sides of the fish head and dividing by the number of fish in Otolith width dividuals studied. Individual errors in recording sizes can mask the re 110–120 27.6 6 3.64 ± 1.3 99 – ± sults of dissimilarity calculations that make it useless (Palmer, 1994). 121 130 34.9 10 3.56 2.4 100 131–140 36.3 9 3.49 ± 2.6 79 Thus, in the present study, sizes were recorded by using a single reader 141–150 38.7 20 3.62 ± 1.4 99 to elude any unsolicited fault (Lee and Lysak, 1990), and were per 151–160 40.9 10 3.59 ± 1.7 100 formed two times. This analysis used average measurement. Coefficients of dissimilarity were evaluated between the various length groups using ANOVA test. suggested that there is an obvious link between habitat impact owing to The outcome of dissimilarity data calculation of the otolith sizes of contamination and dissymmetry in this species. These habitat influences E. australis are presented in Table 1. The value of dissimilarity of the are found in the waters of New Zealand. In contrast, it can be interpreted otolith width was greater than that of the length. Also, the value of that the small dissymmetry in the otolith length is less liable to habitat dissimilarity was at its lowermost and uppermost levels for specimens impact (Jawad et al., 2012a). Jawad (2003) suggested that the lower having size between 115–154 mm and 151–160 mm, respectively. dissymmetry value reached for otolith length may be described based on The percentage of fishspecimens showing dissimilarity in the otolith the growth time of these features, as they might not coincide with the width character was higher than those having asymmetry in otolith existence of opposing habitat features. length (Table 1). Specimens of E. australis were categorized according to There is no exact measurement to gauge the level of the fluctuating their length (Table 2). A trend of increase in the dissimilarity values with asymmetry to know whether the value is more or less (Valentine et al., the upsurge of the fish length was noted in both otolith characters 1973).But, to evaluate the result of the obtained dissymmetry, samples studied. of fishes are usually compared with other samples obtained from a The use of gannets as a sampling tool for fish and their otoliths is recognized, contaminated locality. Because there is no fluctuating feasible, as gannets are coastal feeders rather than pelagic, during nest asymmetry values available for E. australis in the Pacific region, the attendance. Consequently, regurgitations often contain intact fish from other possible choice is to relate the present dissymmetry obtained with which, otoliths can be recovered before gastric secretions begin to digest those attained for other species, reported from other parts of the world. the fish tissue and cranium that causes the release and erosion of In the present study, E. australis was studied from only one locality, otoliths. whereas no previous study has been conducted on its fluctuating Digestion by gastric and enzyme secretions is the major challenge asymmetry to enable comparison and to assess the level of fluctuating when stomach contents are used to describe the diet of many species of asymmetry. However, the present data will be a foundation for more piscivorous birds and the characteristics of ingested fish. Some birds research on dissymmetry in fishes in the Pacific region, and it will be a produce regurgitation pellets that contain the remains of the hard parts reference record for comparison. of digestive resistant prey, including otoliths. These parts will often be To evaluate the dissymmetry values obtained for both otolith sizes of eroded to different extents that make them unsuitable for both prey E. australis, an appraisal was conducted between the present study and species identification of fish, and reconstruction of the size to obtain the dissymmetric values of similar sizes obtained from various fish other biological information (Johnstone et al., 1990). species from other parts of the world (Table 3). Dissymmetry estimates There are few variations in the dissymmetry levels between the two of the otolith length in the related species has a range of 2.1 in Sardinella otolith traits of E. australis. It is problematic to evaluate the dissymmetry sindensis that Jawad et al. (2012c) obtained from the Arabian Gulf and values of such features and to determine whether they are greater or lesser than the usual asymmetry level. This is because of the missing Table 3 2 information related to the usual dissymmetry in New Zealand species. Comparison of the Coefficient of asymmetry (CV a) of otolith sizes of Engraulis Nonetheless, features such as otolith width exhibited greater dissym australis examined in the present study with those of other fishspecies collected metry level than the otolith length trait. The high dissymmetry value in from other localities around the world. this case could specify the vulnerability of this feature to the direct Species Coefficient of Reference 2 variations in the environment. Earlier investigations in this field asymmetry (CV a) OL OW

Beryx splendens 41.87 87.30 Albusaidi et al. (2010) Table 1 Engraulis australis 43.55 86.56 Present study 2 Squared coefficient of asymmetry (CV a) value and character means (Xr+l) of Carangoides caeruleopinnatus 28.43 54.05 Jawad et al. (2012a) Engraulis australis recovered from the food of gannets inhabiting colonies in Chlorurus sordidus 14.05 10.44 El-Regal et al. (2016) Hipposcarus harid 15.19 11.90 El-Regal et al. (2016) Hauraki Gulf, New Zealand. Liza Kluzingeri 4.23 14.06 Sadighzadeh et al. (2011) 2 Character CV a N Character mean % of individuals with Lutjanus bengalensis 5.06 10.29 Jawad et al. (2012a) (mm) ± SD asymmetry Merlangius merlangus 4.710 4.772 Kontas¸ et al. (2018) Rastrelliger kanagurta 88.71 41.75 Al-Mamry et al. (2011) Otolith 43.55 55 7.32 ± 3.1 75 Rhynchorhamphus georgi 66.70 117.60 Al-Rasady et al. (2010) length Sargocentron spiniferum 2.34 4.59 El-Mahdy et al. (2019) Otolith 86.56 55 3.63 ± 2.3 95 Sardinella sindensis 2.10 9.00 Jawad et al. (2012b) width Sillago sihama 2.9 21.6 Jawad et al. (2012c)

2 L.A. Jawad and N.J. Adams Marine Pollution Bulletin 168 (2021) 112391

88.71 in Rastrelliger kanagurta (Cuvier, 1816) gathered from the Omani analysis in this study showed that large-size specimens of E. australis had waters (Al-Mamry et al., 2011). In contrast, dissymmetry in the otolith higher dissymmetry value than younger individuals (P < 0.001). It was width differs in value from 4.59 in Sargocentron spiniferum from the clear that the extent of fluctuatingasymmetry of the length and width of Egyptian waters of the Red Sea obtained by El-Mahdy et al. (2019) to the otolith increased with the fishsize (Table 2). Analogous results were 117.60 in Rhynchorhamphus georgii (Valenciennes, 1847) obtained from obtained by Valentine et al. (1973) in chosen fishspecies collected from the Omani waters (Al-Rasady et al., 2010). When the otolith length is California, U.S.A. They recommended two likely theories that might be considered, the amount of dissymmetry of the otolith of E. australis falls liable for such an approach; ontogenetic disparities related to a surge in just below the midpoint to the maximum amount of 88.71 attained for dissymmetry with size (age), and possible historical occasions which Rastrelliger kanagurta from the Omani waters (Al-Mamry et al. (2011) resulted in an increase in dissymmetry. Otherwise, Thiam (2004) com (Table 3). The amount of dissymmetry in the otolith width is 86.56. This mended that a growing tendency in dissymmetry value with fish size level falls closer to the highest dissymmetry value (117.60) given for could be because of the exposure of grown-up species to unfavourable Rhynchorhamphus georgi gathered from the Omani waters. The outcome environment for a longer period. of this assessment reveals that the amount of dissymmetry in both Fish growth abnormalities may result from chemical and organic otolith sizes of E. australis studied are high, but that of the otolith width pollution (Elie and Girard, 2014). In the waters of New Zealand, fish is higher. Even though the species of fishobtained from various localities anomalies stated have been associated with heavy loads of metal and incorporated in this evaluation are not the same, they display similar organic pollution (Diggles, 2003; Jawad, 2004; Jawad et al., 2006; amount of effect of the habitat on the otolith features, i.e., traits of the Jawad and Hosie, 2007; Davie et al., 2018). otolith: either they are susceptible or resistant to the hostile settings of the habitat (Fey and Hare, 2008). CRediT authorship contribution statement The extent of asymmetry in fishotoliths may be related to a range of factors, which include genetic and environmental factors. Numerous Both authors have read and approved the manuscript. LAJ contrib reasons, one of which is genetic issue could be accountable for the uted to ideas, data generation, data analysis, and manuscript prepara dissymmetry in these two features. But this factor could not be tested at tion. NJD performed field trips to collect and sort food samples of this step owing to the unavailability of genetic data on the Australian gannet, editing, and commenting on the manuscript before submission. anchovy in New Zealand. The other probable reason is the habitat in fluence that exhibits an increased dissymmetric value, but it can also Declaration of competing interest exhibit less dissymmetric value before initiating wide spread death (Bengtsson and Hindberg, 1985). Nigel Adams and Laith Jawad declare no conflict of interest. Pollution of sea water and sediments by various contaminants are deliberated to be the principal foundation of many adverse impacts in Acknowledgements the aquatic habitat. This type of contamination was accustomed to the waters of New Zealand, where varied contaminants had been noted to The study was funded in part by Birds NZ and Unitec Strategic intrude for the past twenty years (Smith and McVeagh, 1991; Abrahim Research Fund. and Parker, 2008; Marx et al., 2014). Pollution can affect living creatures in water in various ways Ethical statement (Newman and Clements, 2007). If accumulated in body parts of the fish, heavy metals or other contaminants can impact metabolism and growth The gannets, from which regurgitations were collected, were of the fish (Sindermann, 1979; Heath, 1995; Newman and Clements, sampled under the Department of Conservation Wildlife Authority 2007). Implicitly, contaminants can also have an impact on the feeding (38016-FAU) and the University of Auckland Animal Ethics Committee of fish, thus disturbing its growth (Newman and Clements, 2007). For approval notice (001797). example, heavy metals and organic contents cause noteworthy de viations in macrobenthic groups in rivers around Sydney (Stark, 1998; References Wright and Burgin, 2009), and therefore, might affect fish food; benthos-feeding fishin particular. Food is a vital component that has an Abrahim, G.M.S., Parker, R.J., 2008. Assessment of heavy metal enrichment factors and impact on the growth of fish, which includes the growth of skeletal the degree of contamination in marine sediments from Tamaki Estuary, Auckland, – ø New Zealand. Environ. Mont. Asses. 136, 227 238. materials and shaping of bones (Tacon, 1992; Waagb et al., 2005). Albusaidi, H.K., Jawad, L.A., Al-Mamry, J.M., Al-Marzouqi, M.S., 2010. 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