Journal of Experimental Marine Biology and Ecology
Otolith microchemistry of two amphidromous galaxiids across an experimental salinity gradient: A multi-element approach for tracking diadromous migrations
Introduction
Methodologies for characterising age-specific migration patterns are necessary to identify essential fish habitat at different life stages, as well as determining whether connectivity between different habitats is important for completion of typical life cycles (Elsdon et al., 2008). Being able to track individual migration patterns also allows an understanding of intergenerational exchange that can occur among spatially separated populations (as in a meta-population, Thorrold et al., 2007). Diadromous migrations are an extreme form of large scale movement and differential habitat utilisation, and diadromous species comprise important fisheries worldwide (McDowall, 1990). It has been difficult to track diadromous migrations due to the large distances these fishes can travel, the low recapture rates of tagged individuals, and the inability to physically tag small individuals with traditional methods, which limit the feasibility of mark/recapture studies (Secor et al., 1995). The development of otolith microchemical techniques, whereby chronologically deposited and metabolically inert geochemical information can be used to reconstruct the environmental history of a fish, has allowed diadromous migrations to be more efficiently reconstructed (Secor et al., 1995).
Otolith microchemistry has revealed a diverse range of life history strategies and habitat utilisation in a range of diadromous fish species (Secor et al., 1995). ‘Facultative diadromy’, whereby not all individuals in a presumed diadromous population actually make a migration between the river and the sea, has been identified in numerous species and populations (e.g.,: Herring, Alosa aestivalis, Limburg, 1998; Smelt, Hypomesus nipponensis, Katayama et al., 2000; Sturgeon, Acipenser guldenstadti, Arai and Miyazaki, 2001; Stickleback, Gasterosteus aculeatus, Arai et al., 2003; Striped bass, Morone saxatilis Zlokovitz et al., 2003; Shirauo, Salangichthys microdon, Yamaguchi et al., 2004; Smelt, Retropinna semoni, Crook et al., 2008). Facultative diadromy extends to all three forms of diadromy (as defined by McDowall, 1992). For example, facultative catadromy in Anguillids (Arai et al., 2004), whereby some eels complete their life entirely within the marine environment; facultative anadromy in brown trout (Arai et al., 2002), whereby some individuals are freshwater resident; and facultative amphidromy in bullies and galaxiids, whereby larvae develop in freshwater lake systems despite having open access to the ocean (Closs et al., 2003, David et al., 2004). In all cases, otolith microchemistry has been used to distinguish whether individuals have utilised marine and/or freshwater habitat during different stages of their lives.
Strontium, and to a lesser extent barium, are the two elements commonly used to distinguish residency in waters of different salinity (Elsdon et al., 2008). There is usually a much higher and lower abundance of strontium and barium, respectively, in saltwater compared with freshwater (Elsdon et al., 2008). Often, scientists are interested in distinguishing estuarine versus freshwater or marine habitat use (e.g., Arai et al., 2004), or even utilisation of different parts of an estuary (e.g., Kafemann et al., 2000). Distinguishing between freshwater and saltwater residency has usually been straightforward in previous validation experiments (e.g., Farrell & Campana, 1996, Tzeng, 1996, Kraus & Secor, 2003, Secor et al., 1995), but there has been mixed success in discriminating habitat utilisation over finer salinity scales. For example, Kraus and Secor (2003) suggested otolith Sr:Ca ratios could be used to determine residency in completely fresh, estuarine or open ocean water, but not over finer salinity scales. Importantly, the non-linear relationship between salinity and ambient element:Ca ratios would make it difficult to discriminate between medium to high salinity habitat utilisation (most variation occurs below 8 ppt — Kraus & Secor, 2003, Lowe et al., 2009), if ambient element:Ca ratio rather than ambient absolute concentrations dictate the rate of element uptake into otoliths.
The patterns of strontium and barium uptake can be both species and age dependent. Validation studies performed on one species will not necessarily extend to others (Zimmerman, 2005). Similarly, validation studies performed on adult fish will not necessarily extend to larvae. Hence, laboratory validation studies should be undertaken on the species and age group of interest before trying to infer patterns of diadromy or habitat utilisation, particularly if the goal is to reconstruct movements across finer salinity scales (Kraus & Secor, 2004, Elsdon et al., 2008).
Amphidromy is a distinct form of diadromy with adults living in freshwater where most growth and reproduction takes place, but a short larval phase is expected to take place in the ocean (McDowall, 2007). Amphidromous galaxiids are a dominant freshwater fish fauna in New Zealand, Australia and South America (McDowall, 1990). Amphidromous galaxiid species typically spend a 3–6 month larval period in the ocean, before the transparent juveniles return to rivers where they are targeted as the basis of whitebait fisheries (McDowall, 1990). Genetic homogeneity at a continental scale suggests considerable larval dispersal occurs during the marine phase (Waters et al., 2001). Landlocked populations exist in large inland lake systems that have open access to the sea (McDowall, 1990), which suggests larvae are not actively dispersing (out of the lake system). There is also evidence for larval retention in galaxiids inhabiting coastal lake systems with open access to the sea (David et al., 2004). The presence of one and three endemic migratory galaxiid species in Australia and New Zealand and nearby islands, respectively, suggests colonisation abilities may differ among galaxiids despite all species having a pelagic larval period (McDowall, 1990). Being able to track a large number of individual larvae is thus necessary to determine the scale of movement of most individuals and effective population connectivity. This is difficult when trying to track movement through a comparatively homogeneous ocean, but determining retention in lakes or estuaries should be more straightforward. Determining the salinity history of larvae, and whether patterns of larval retention in lakes and estuaries are consistent among species, will thus help explore the magnitude of self-recruitment in galaxiid species.
Before relating otolith microchemistry of wild-caught fish to their salinity history, we needed to determine the degree to which movements across salinity gradients could be confidently inferred. We thus reared larvae of two migratory galaxiid species, Galaxias maculatus and G. argenteus, in salinities of 2, 5, 10, 20 and 34 to determine whether otolith trace element signatures could be related to a range of freshwater, estuarine and saltwater conditions. We primarily wanted to ensure we could identify individuals that had not spent time in a marine environment (i.e., were non-diadromous). We also wanted to explore whether there was potential to identify movements across finer salinity scales. To advance a more general understanding of factors regulating otolith microchemistry, we also explore whether otolith element:Ca is best predicted by the salinity, ambient element:Ca or ambient element concentrations in our experimental treatments.
Section snippets
Methods
Fish were reared in a constant temperature controlled room maintained at an average of 14.2 °C (range 13.5 °C–15.1 °C) and operating under a 12 h day/ 12 h night cycle. Eggs of both Galaxias argenteus and G. maculatus were obtained from a commercial breeding and culturing facility run by Charles Mitchell on the North Island of New Zealand. Eggs hatched between the 25/8/06–2/9/06 and larvae were transferred into several holding tanks of salinity approximately 17 and fed freshly hatched Artemia. A
Results
Otolith Li:Ca and Sr:Ca increased linearly with salinity for both species (Fig. 1, elements with R-squared values were significant at 0.05 level). Adjusted R squared values were above 0.85 for all Li:Ca and Sr:Ca regressions. Positive relationships between otolith B:Ca, Al:Ca, P:Ca, Cu:Ca and salinity were detected for G. argenteus, as well as negative relationships for S:Ca, Mn:Ca, Rb:Ca and Ba:Ca. Of these latter 8 elements, adjusted R squared values were above 0.85 for Rb:Ca and Cu:Ca only (
Discussion
Exposure to different salinity treatments imparted distinct signatures in the otoliths of both G. maculatus and G. argenteus. As in numerous other studies, high otolith Sr:Ca resulted from exposure to saltwater (reviewed in Elsdon et al., 2008). Validation studies are system specific, and the high variability in chemistry among water catchments means patterns of otolith microchemistry observed in one body of freshwater will not be indicative of all freshwater systems (Elsdon et al., 2008). The
Conclusions
This experiment is a first step towards validating the use of otolith microchemistry to track movements of Galaxias species across salinity gradients. Discrimination between saltwater and freshwater was straightforward in this study, and we are confident that an otolith Sr:Ca of less than 4 mmol/mol relates to non-diadromous recruitment in this species (i.e., no marine phase). Freshwater Sr is not always low, however, and so otolith Li:Ca above 4 mmol/mol may result from development in saltwater
Acknowledgements
We thank Charles Mitchell for the advice on rearing larval galaxiids, Kim Garrett for technical support with animal husbandry and two anonymous referees for positive and constructive feedback. Hicks was supported by an Otago University Postgraduate Scholarship. Funding from the University of Otago Zoology Department and the Australian Society for Fish Biology (Barry Jonassen award) covered microchemical costs. [ST]
References (62)
- et al.
Comparison of digestion methods for ICP-MS determination of trace elements in fish tissues
Anal. Chim. Acta
(2009) - et al.
Strontium and barium uptake in aragonitic otoliths of marine fish
Geochim. Cosmochim. Acta
(2000) - et al.
Li, Sr, Mg, and Na in foraminiferal calcite shells from laboratory culture, sediment traps, and sediment cores
Geochim. Cosmochim. Acta
(1985) - et al.
The composition of peridotites and their minerals: a laser-ablation ICP-MS study
Earth Planet. Sci. Lett.
(1998) - et al.
Regulation of calcium and strontium deposition on the otoliths of juvenile tilapia, Oreochromis niloticus
Comp. Biochem. Physiol.
(1996) - et al.
Li/Ca in multiple species of benthic and planktonic foraminifera: thermocline, latitudinal, and glacial-interglacial variation
Geochim. Cosmochim. Acta
(2004) - et al.
Lithium and its isotopes in major world rivers: implications for weathering and the oceanic budget
Geochim. Cosmochim. Acta
(1998) - et al.
Variation in otolith strontium and calcium ratios as an indicator of life-history strategies of freshwater fish species within a brackish water system
Fish. Res.
(2000) Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition
J. Exp. Mar. Biol. Ecol.
(1989)- et al.
Incorporation of strontium into otoliths of an estuarine fish
J. Exp. Mar. Biol. Ecol.
(2004)
Sources and uptake of trace metals in otoliths of juvenile barramundi (Lates calcarifer)
J. Exp. Mar. Biol. Ecol.
Can otolith microchemistry chart patterns of migration and habitat utilization in anadromous fishes?
J. Exp. Mar. Biol. Ecol.
Simultaneous use of strontium:calcium and barium:calcium ratios in otoliths as markers of habitat application to the European eel (Anguilla anguilla) in the Adour basin, South West France
Mar. Environ. Res.
Effects of salinity and ontogenetic movements on strontium:calcium ratios in the otoliths of the Japanese eel, Anguilla japonica Temminck and Schlegel
J. Exp. Mar. Biol. Ecol.
Patterns of migration in Hudson River striped bass as determined by otolith microchemistry
Fish. Res.
Use of otolith microchemistry to estimate the migratory history of the Russian sturgeon, Acipenser guldenstadti
J. Mar. Bio. Assoc. UK
Identifying sea-run brown trout, Salmo trutta, using Sr:Ca ratios of otolith
Ichthyol. Res.
Use of otolith microchemistry to estimate the migratory history of the threespine stickleback, Gasteroseus aculeatus
J. Mar. Bio. Assoc. UK
Evidence of different habitat use by New Zealand freshwater eels Anguilla australis and A. dieffenbachia, as revealed by otolith microchemistry
Mar. Ecol. Prog. Ser.
Characterizing natal source population signatures in the diadromous fish, Galaxias maculatus, using embryonic otolith chemistry
Mar. Ecol. Prog. Ser.
The inclusion of sub-detection limit LA-ICPMS data, in the analysis of otolith microchemistry, by use of a palindrome sequence analysis (PaSA)
Limnol. Oceanogr. Methods
Effect of diet on otolith composition in Pomatomus saltatrix, an estuarine piscivore
J. Fish. Biol.
Chemistry and composition of fish otoliths: pathways, mechanisms and applications
Mar. Ecol. Prog. Ser.
Using otolith microchemistry of Haemulon flavolineatum (French Grunt) to characterize mangroves and coral reefs throughout Turneffe Atoll, Belize: difficulties at small spatial scales
Estuaries
Non diadromous recruitments in coastal populations of common bully (Gobiomorphus cotidianus)
N.Z. J. Mar. Fresh. Res.
Evidence of diadromous movements in a coastal population of southern smelts (Retropinninae: Retropinna) from Victoria, Australia
Mar. Fresh. Res.
Evidence of flexible recruitment strategies in coastal populations of giant kokopu (Galaxias argenteus)
Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri
Mar. Ecol. Prog. Ser.
Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency
Can. J. Fish. Aquat. Sci.
Otolith microchemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences
Oceanogr. Mar. Biol.
Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys
Am. J. Physiol.-Reg. I
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2022, Estuarine, Coastal and Shelf ScienceCitation Excerpt :This protein is likely to be found in the primordium of otoliths, explaining the higher natal signatures observed (Thomas et al., 2020). Li incorporation into the otolith is also influenced by salinity, and it seems to occur by direct substitution of Ca, which means that biological influence should be minimum (Marriot et al., 2004; Hicks et al., 2010). This suggests that the oscillations observed among locations may be directly related to the environmental concentration of this element (Thomas et al., 2020).