Effects of temperature on somatic growth, otolith growth, and uncoupling in the otolith to fish size relationship of larval northern pike, Esox lucius L
Introduction
Northern pike (Esox lucius) is a species of significant importance to both commercial and recreational fisheries that inhabits a wide range of environments where, during its early life stages, it encounters temperatures from 6 to above 20 °C (Craig, 2008). However, temperatures above 22 °C (the maximum value used in the present study) are very occasional. Unfortunately, this species is close to extirpation in many geographical areas including freshwater and coastal marine systems, for example the Baltic Sea (Skov and Nilsson, 2018). Although over-exploitation can explain this to some extent, the disappearance of suitable spawning grounds and low recruitment seem to be the main reasons for the decline of population size of this species (Nilsson et al., 2014; Larsson et al., 2015; Skov and Nilsson, 2018; Fey et al., 2019). Other factors related to human activities in coastal areas, such as wind farms and underwater cables, did not affect the growth or survival of the early life stages of northern pike (Fey et al., 2019) despite its demersal eggs and larvae attached to the substrate during the yolk-sac stage (Horbowa and Fey, 2013). The more endangered the northern pike populations are, the more urgent it is to better understand ecological relations during the early life period. This is especially true since the recruitment success and states of given fish populations are frequently determined during the larval and juvenile life stages (Houde, 1987) when a number of factors are responsible for mortality in given populations (Anderson, 1988).
The main source of information on the early life history of fish are otoliths – calcified structures used by fish for balance, hearing, and orientation (for reviews on otolith formation and daily increment deposition see Morales-Nin, 1992, 2000) – that can provide data on, inter alia, age, growth, condition, hatching dates, geographical area of origin, and mortality at individual and population levels in larvae (Campana and Nielson, 1985; Francis, 1990; Secor and Dean, 1992; Campana and Jones, 1992; Campana, 2005; Berg et al., 2017), specimens that are several months old (Fey and Linkowski, 2006), and even adults (Hussy et al., 2010). Bearing in mind all the advantages of otolith methods, one should also consider the complexity of processes affecting short- and long-term otolith growth and otolith microstructures (e.g., response time, differences in how body size changes are reflected in length and mass). This is especially well visualized in studies that assess the somatic growth of larval fish using several methods simultaneously such as RNA/DNA, condition factor K, and otolith increment widths (Peck et al., 2015), or, for example, RNA/DNA and marginal otolith increment widths (Do Souto, 2019a).
Before otolith methods can be applied to obtain biological data for ecological studies, it is important to evaluate several assumptions. First, when the first increment is formed and whether increments are deposited daily must be verified (Geffen, 1992; Campana, 2001). Some factors such as temperature and somatic growth should be considered as they affect increment formation and visibility under the microscope. Otolith increments can be too narrow to be distinguished under a light microscope if somatic growth is too slow, for example as a result of poor feeding conditions (Geffen, 1982; Folkvord et al., 2000; Fox et al., 2003) or low temperatures (Radtke and Fey, 1996; Fukuda et al., 2009). On the other hand, even if increments are formed daily and are above the resolution of light microscope, significant differences in their enumeration may occur among readers with different experience, resulting in substantial error in growth rate and hatch-dates of larval fish estimates (Spich and Fey, 2020). Moreover, it should be confirmed if the otolith size-fish size relationship is independent of somatic growth and temperature and if otolith growth follows somatic growth (Geffen, 1992) so that increment widths can be used as proxies for fish growth on given days. Results obtained for species other than northern pike indicate that slower growing specimens might have relatively (i.e., at the same fish size) larger otoliths (Mosegaard et al., 1988; Secor and Dean, 1989; Fey, 2001; 2006), and otolith growth can also be affected not only by, as expected, somatic growth but also independently by temperature itself (Mosegaard et al., 1988; Barber and Jennings, 2001; Fey, 2001, 2005, 2006; Fey and Hare, 2012). In such cases, when other factors control these two relationships, it can be concluded that uncoupling in otolith size-fish size relationship and/or fish growth-otolith growth occurred (Mosegaard et al., 1988).
The uncoupling in somatic growth-otolith growth and otolith size-fish size relationships can have particularly serious consequences for the accuracy of results obtained with methods based on increment width measurements, like growth back-calculation (Campana, 1990; Francis, 1990; Vigliola and Meekan, 2009; Ashworth et al., 2017; Morrison et al., 2019), marginal otolith increment width analysis (e.g., Sepúlveda, 1994; Fey, 2001, 2005; Do Souto et al., 2019a) or increment width trajectory analysis (e.g., Gultiérrez and Morales-Nin, 1986; Paperno et al., 1997; Do Souto et al., 2019b).
The assumption of the daily periodicity of increment formation in northern pike otoliths and the timing of the first increment formation were confirmed previously for the sagitta (Fey et al., 2018) and lapillus (Wang and Eckmann, 1992; Fey et al., 2018). However, there is still no data to support the assumption that otolith growth depends on somatic growth or that the fish size-otolith size relationship is independent of somatic growth. Confirmation of these assumptions is especially important for early life stages of species like northern pike that are characterized by fast growth and that possibly experience wide ranges of temperature (Skov and Nilsson, 2018).
The aim of the present study was to determine for larval and early juvenile northern pike (9−27 mm SL) the effect of somatic growth and temperature (10, 15, 22 °C) on the otolith growth (sagittae and lapilli). It was also verified whether the otolith size to fish size relationship was independent from the effects of somatic growth.
Section snippets
Experimental conditions
The experiments were performed in nine tanks with volumes of 55 L each that were divided into three freshwater recirculating aquaculture systems (RAS) at three temperatures (mean ± SD) of 10 ± 0.6 °C, 15 ± 0.4 °C, and 22 ± 0.5 °C. There were three replicates for each temperature (3 temperatures x 3 replicates). Each of the systems was equipped with UV sterilization and a filtering-deposit container with a volume of 70 L providing both mechanical and biological filtration. The volume of the
Temperature effect on somatic growth
The mean growth rate (slopes of the regression lines fitted to SL at age data) of larval northern pike depended significantly on rearing temperature (Fig. 1, Table 1), with the highest rate observed at 22 °C (0.83 mm·d−1), a lower rate at 15 °C (0.48 mm·d−1), and the lowest at 10 °C (0.25 mm·d−1). The described above among temperatures differences in slopes of the SL at age regressions (i.e., somatic growth) were statistically significant (GLM unequal slopes model, all P < 0.05, Table 2). The
Temperature effect on somatic growth
The growth rate of larval northern pike in the present study depended significantly on rearing temperature with the highest mean rate observed at 22 °C (0.83 mm·d−1), a lower rate at 15 °C (0.48 mm·d−1), and the lowest at 10 °C (0.25 mm·d−1). The mean life growth rates of individuals were even higher at up to 1.28 mm·d−1. These results were not surprising since the positive temperature effect on larval fish growth is a well-known phenomenon (Elliot, 1982).
The value obtained in the current study
CRediT authorship contribution statement
Dariusz P. Fey: Conceptualization, Formal analysis, Investigation, Writing - original draft, Writing - review & editing, Supervision, Project administration. Martyna Greszkiewicz: Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft, Visualization.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
This paper is a contribution to statutory project Dot19/PIKE conducted at the National Marine Fisheries Research Institute and financed by the Ministry of Science and Higher Education, Poland. We would like to thank Adam Lejk and Michał Zimak for their help with obtaining pike eggs and consultations on larvae rearing. We also thank Hanna Wróblewska for otolith extraction.
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