Using fin ray chemistry to discriminate hatchery reared juvenile age-0 Persian sturgeons by their origin in the Southern Caspian Sea region using split stream ICP-MS/MC ICP-MS

Highlights

• Fin ray chemistry applied for identifying the source of hatchery Persian sturgeon.

• Laser ablation split stream ICP-MS/MC ICP-MS applied for the first time to fin rays.

• Results contribute to an improved management of Persian sturgeon populations.

• Methodological improvements allow for a detailed life-time analysis of sturgeons.

Abstract

Trace elements integrated into fish fin rays from the ambient environment may represent a permanent record of the environmental conditions that an individual has experienced throughout its lifetime. Fish from hatcheries used for stocking may therefore carry a natural intrinsic tag of their origin, which can be then later used for assessing the efficiency of stocking measures. This study investigated the potential of the elemental and strontium isotope (n(⁸⁷Sr)/n(⁸⁶Sr)) composition of fin rays of juvenile Persian sturgeons (Acipenser persicus) to determine their origin. Water and pectoral fin ray samples of twenty age-0 juvenile Persian sturgeons were collected from the largest hatcheries in the east and west of the Southern Caspian Sea region. The elemental content and the Sr isotope ratio in water were determined by (multi collector) inductively coupled plasma mass spectrometry ((MC) ICP-MS), while the elemental content in fin rays (Ba, K, Mg, Mn, Na, Sr) together with the Sr isotope ratio were determined using laser ablation split stream ICP-MS/MC ICP-MS. The elemental composition of Al, B, Ba, Ca, Cu, Fe, Ga, Li, Mg, Mn, Mo, Na, Pb, Rb, Sr, Tl, U and Zn and the Sr isotope ratio of water differed between the investigated hatcheries from the east and west of the Southern Caspian Sea region. Fin rays reflected the elemental (Sr, Ba and Mn) and the Sr isotope composition of pool water of their hatchery of origin. A factor analysis yielded one main factor (high in Sr content and in the n(⁸⁷Sr)/n(⁸⁶Sr) ratio and low in Ba and Mn content) discriminating fin ray samples between sites explaining 86 % of the variation. A discrimination analysis by cross-validated classification yielded 100 % correct assignments of fin ray samples to the hatchery sites using all different parameter combinations. These results suggested that the Sr, Ba Mn elemental and Sr isotope composition of fin rays can be used for the determination of the source hatchery of stocked fish. This represents a valuable tool for evaluation restocking measures of Persian sturgeons in the Southern Caspian Sea region.

Introduction

The chemical composition of fish calcified structures is considered as a natural marker capable of recognizing fish from different habitats. The successful application of this method to fish stocks depends on the geographic variation of water chemistry and other factors such as temperature, which influence the chemical composition of calcified structures in fish (Campana et al., 2000; Elsdon et al., 2008). This natural chemical information can be used as an alternative to artificially induced markers to answer relevant fishery management questions, such as characterization and discrimination of hatchery-reared fish, evaluation of the introduction of non-native fish before their release to the sea, fish dispersal and migration patterns in natural systems, and to monitor the success of restocking programs (Rooker et al., 2016; Zitek et al., 2010). The strontium (Sr) isotope composition, more specifically the isotope amount ratio n(⁸⁷Sr)/n(⁸⁶Sr) (hereafter written as ⁸⁷Sr/⁸⁶Sr (isotope) ratio or Sr isotope ratio), varies in aquatic habitats as a result of variations in Sr sources and is incorporated without significant fractionation into the hard parts of aquatic organisms (Outridge et al., 2002). Further, the ⁸⁷Sr/⁸⁶Sr isotope ratio is not significantly affected by temperature, salinity or biological factors (Gillanders, 2005; Kennedy et al., 2000).

Thus, natural chemical tags recorded in calcified structures of fish like pectoral fin rays have clear advantages over artificial tags because all fish are naturally marked from early life, marks are cost free, and they are usually permanent compared to artificial ones (Elsdon et al., 2008).

Environmental conditions experienced by fish are reflected in all calcified tissues to some degree, thus fin rays are considered to be useful to reconstruct environmental life histories (Allen et al., 2009; Avigliano et al., 2020; Rude et al., 2014; Smith and Whitledge, 2010; Thorrold et al., 2001; Veinott and Porter, 2005; Veinott and Evans, 1999; Zitek et al., 2010). Applications of fin ray microchemistry in sturgeons in the past have aimed mainly at determining periods of marine and freshwater occupation for anadromous species (Allen et al., 2009; Arai et al., 2002; Balazik et al., 2012; Lowe, 2020; Nelson et al., 2013; Phelps et al., 2017; Sellheim et al., 2017; Tzadik et al., 2017a, 2017b; Veinott et al., 1999). Pectoral fin ray trace element composition analyses may also enable determination of freshwater natal environments such as large river and hatchery systems (Loeppky et al., 2020). Pectoral fin ray Sr isotope ratios (⁸⁷Sr/⁸⁶Sr) have been used to reconstruct origin of sturgeon fish (Allen et al., 2009; Arai et al., 2002; Balazik et al., 2012; Jarić et al., 2011; Nelson et al., 2013; Phelps et al., 2012; Sellheim et al., 2017; Veinott et al., 1999; Willmes et al., 2016) and as an artificial tag to evaluate retention rate of the enriched isotope marks (Smith and Whitledge, 2020). However, natural chemical elemental signatures in pectoral fin rays of juvenile age-0 hatchery Persian sturgeons have not yet been evaluated in combination with the natural ⁸⁷Sr/⁸⁶Sr isotope ratio as markers to determine their origin.

An advanced method to retrieve elemental and ⁸⁷Sr/⁸⁶Sr isotope ratio information simultaneously from the same sampling spots on solid biological materials like otoliths and fin rays significantly improves this type of analyses now (Prohaska et al., 2016). Important advantages to use pectoral fin rays for this kind of studies are, that they can be sampled without the necessity to kill the fish, and that they are also the preferred structure to assess aging in sturgeons (Jackson et al., 2007), as compared to their irregular otoliths (Arai and Miyazaki, 2002; Stevenson and Secor, 2000) making otolith annuli difficult to distinguish (Stevenson and Secor, 2000). Growth rates can thereby be analyzed in association with chemical patterns and critical processes occurring during early life (Sponaugle, 2009). These arguments are particularly relevant for imperiled sturgeon populations (Billard and Lecointre, 2000; Pikitch et al., 2005). However, another important factor to use elemental and Sr isotopic tags in fin rays of age-0 sturgeons is the consideration of the onset of the calcification process (Sweeney et al., 2020).

All five Caspian Sea sturgeons including great sturgeon (Huso huso), ship sturgeon (Acipenser nudiventris), starry sturgeon (A. stellatus), Russian sturgeon (A. gueldenstaedtii) and Persian sturgeons (A. persicus) are long lived, mature late, have intervals between their reproduction, slow growing with small population size which is under pressure (Bakhshalizadeh et al., 2011, 2012; 2013, 2015; Bakhshalizadeh et al., 2017; Pikitch et al., 2005). All of these long-lived anadromous species are listed as threatened species in the International Union for Conservation of Nature (IUCN) and were severely affected by long-term anthropogenic effects, which have virtually destroyed their natural survival ability, with being the Persian sturgeon populations in the Southern Caspian Sea most affected (Pourkazemi, 2006). Therefore, the vast majority of the current Persian sturgeon stock is currently supposed to have originated from hatcheries. That is why the investigation of chemical tags as natural markers for hatchery-reared Persian sturgeon juveniles represents an important step towards an improved management and conservation of Persian sturgeon populations in the Southern Caspian Sea.

Consequently, in this pilot study the potential usefulness of the trace element composition and the strontium isotope ratio (⁸⁷Sr/⁸⁶Sr) in pectoral fin rays as natural tags to differentiate hatchery-born Persian sturgeons collected from eastern and western hatchery sites in the Southern Caspian Sea region is assessed. Thus, the objectives of this study were to (i) investigate potential differences in water chemistry between eastern and western hatcheries (ii) evaluate the relationship between water and trace element and strontium isotope ratio (⁸⁷Sr/⁸⁶Sr) composition in fin rays and (iii) and identify potential chemical markers in fin rays for determining the source of age-0 Persian sturgeons. Demonstrating the potential to identify natal hatchery source for age-0 Persian sturgeons using fin ray microchemistry provides the basis for future studies on the stocking success of juvenile fish from different hatchery sources for this imperiled species, even including the potential to identify possible natural reproduction.