Available online at www.nznaturalsciences.org.nz

Influence of open and closed river systems on the migrations of two northern populations of banded kokopu ( fasciatus)

Raymond Tana1 and Brendan J. Hicks2

Centre for Biodiversity and Ecology Research, Department of Biological Sciences, Faculty of Science and Engineering, The University of Waikato, Hamilton 3240, New Zealand. Email addresses: [email protected], [email protected]

(Received 31 January 2012, revised and accepted 10 April 2012)

Abstract

Otolith microchemical analysis by laser ablation inductively coupled mass spectrometry (ICP-MS) was used to investigate the migratory life histories of banded kokopu (Galaxias fasciatus) in two streams on the North Island of New Zealand. Known differences in marine and freshwater chemistry were used as a premise to document the migratory life strategies of banded kokopu between these environments. More specifically, temporal trends in high and low strontium/calcium ratios (Sr/Ca) identified in fish otoliths were used to determine evidence of migration between fresh and saltwater environments. Trace element analysis of fish captured above the Whau Valley Reservoir reflected non-migratory life histories and exhibited consistently low Sr/Ca ratios across the entire otolith. However, one fish from above the reservoir indicated unusually high Sr/Ca ratios in early adulthood. These high Sr levels were attributed to localised inputs from mineral-rich seepages associated with past mining practices in the region and low calcium availability within the Pukenui Stream. Otoliths from banded kokopu collected from Komiti Stream were shown to be migratory with a marine larval stage (high Sr/Ca ratio levels at the otolith nucleus), followed by a freshwater adult phase (low Sr/Ca ratio levels towards the edge) indicating their amphidromous origins. The study provides further evidence of non-diadromous recruitment for banded kokopu as a consequence of a large in-stream barrier and will add to the known distribution of landlocked species in New Zealand.

Key words: Banded kokopu – Galaxias fasciatus – diadromy – otolith microchemistry – landlocked – laser ablation ICP-MS

Introduction followed by ten of New Zealand’s eighteen diadromous fish species (McDowall 1993; The amphidromous lifecycle of 1995). Typically, strategies involving fish banded kokopu (Galaxias fasciatus) is movement between fresh and saltwater representative of life history patterns environments are termed ‘diadromy’

New Zealand Natural Sciences (2012) 37: 25-36. © New Zealand Natural Sciences 26 New Zealand Natural Sciences 37 (2012)

(McDowall 1988; 1990; 1996). More ple forms of larval recruitment in giant specifically, an amphidromous life kokopu (Galaxias argenteus) collected strategy is characterised by spawning from the lower Taieri and Mataura River and egg development in freshwater catchments in Southland Otago. Aside followed by a marine growth phase (as from identifying typical diadromous hatchlings) returning several months movements in fish, their study indicated later as upstream migrant juveniles to that non-diadromous recruitment may mature in freshwater (McDowall 1995; also play an important role in sustaining 2007). For researchers, the task of coastal populations of in documenting movement patterns of this the region (David et al. 2004). Similarly, type can be difficult, particularly where otolith chemical analysis of common fish may range over large temporal and bully (Gobiomorphus cotidianus) by Closs spatial scales. Furthermore, such life et al. (2003) collected from the same strategies preclude conventional tagging general sample locations as David et al. methods due to size limitations in tagging (2004), provided further evidence of technology, costs and the inability to diadromous and non-diadromous recruit- effectively track larval fish throughout ment. This was later shown to be the case time and space (Thorrold. et al. 1998; for common bully in Lake Tarawera and Munro 2004). the Tarawera River on the North Island However, microchemical analysis of of New Zealand (Michel et al. 2008). In fish otoliths offers another approach as the present study, we set out to expand otoliths act as natural tags recording in the current information on the migratory chronological sequence daily growth life strategies of banded kokopu caught increments composed of trace elements within an open and closed river system present in the water throughout a fish’s using otolith microchemistry techniques. life (Campana 1999; Campana & Thor- More specifically, we compare 88Sr:43Ca rold 2001). Furthermore, once chemical ratios in otoliths of fish taken above a elements are deposited in the otolith they large 65 m high dam near Whangarei are neither resorbed nor re-metabolized, City (with no upstream access from the resulting in a permanent chemical record sea) with fish from a small stream in the of the fish’s life history (Campana 1999; Kaipara Harbour (with sea access) on the Campana & Thorrold 2001). For this North Island of New Zealand. reason, the ratio of Sr over Ca (Sr/Ca), can be used to describe fish movements Methods between fresh and saltwater environ- ments particularly as Sr concentrations Fishing sites are higher in seawater (0.088 ppm), than freshwater (0.00018 ppm), (Tzeng 1996; Banded kokopu were collected from the Tzeng et al. 2005). Pukenui Stream located above the Whau In New Zealand, a growing number Valley Reservoir near Whangarei on the of studies have used Sr/Ca ratios to elu- east coast and from Komiti Stream in cidate diadromous life histories for several the Kaipara Harbour on the west coast freshwater fish species. Davidet al. (2004) of northern New Zealand (Figure 1). used Sr/Ca ratios to identify the princi- The Whau Valley Reservoir (25 ha) Tana & Hicks: Open and closed populations of banded kokopu 27 was constructed in the early 1950s in labelled containers in 70% ethanol for by the Whangarei District Council as transport to the lab. the main water supply for Whangarei Otolith extraction and polishing residents. Three headwater streams feed into the Pukenui Stream before entering Sagittal otolith pairs were extracted the reservoir from the Pukenui Forest from fifteen banded kokopu (Table 1). Reserve (NZMS260 Topographic Map, The head of each fish was sectioned 1:50,000 Q07, Q08). From the reservoir with a scalpel along the midline dorsal outlet the Pukenui Stream descends 65 surface (from the head to the mouth), m into the Waiarohia Stream and the and separated to expose left and right Whangarei Harbour. Fish species above cranial cavities. Brain tissue was carefully the reservoir include banded kokopu flushed out with distilled water using a (Galaxias fasciatus), rainbow trout pipette, exposing the brain cavity and (Onchorynchus mykiss) and the longfin inner ear. Left and right otolith pairs eel (Anguilla dieffenbachii), (Manning were then removed from both cavities 1996). However, in the Waiarohia using fine-tip tweezers under a compound Stream immediately below the reservoir microscope. Excess tissue was removed banded kokopu are not present. Instead and otoliths were rinsed thoroughly in a population from Komiti Stream in the distilled water before being stored in Kaipara Harbour was sampled (Figure 1). labelled vials to air-dry for 24 h. Otoliths The surrounding catchment of Komiti were then embedded in thermosetting Stream is primarily pine forest (Pinus glue (Crystalbond, Aremco Products, radiata) with a small residential area Inc, USA) and mounted on glass slides leading to the river mouth. We selected (3 per slide), labelled by date and stream this stream because it had no in-stream site using a glass etching drill and left barriers (waterfalls or culverts and dams) overnight to dry. Otolith polishing was that would prevent fish passage from the carried out systematically using firstly sea. Eight fish from Pukenui Stream above 1200, 2000, and then 4000 grain wetted the reservoir and seven from Komiti carborundum sand paper to expose the Stream were collected on 1 July and 10 otolith nucleus (area representing the October 2006 (Table 1), using minnow larval growth phase in fish) for chemical traps (4 mm mesh), baited with Kraft analysis. Vegemite®, and by spotlighting. For each Laser ablation ICP-MS day of sampling, traps were set before sunset along the Pukenui Stream and in Chemical analysis of fish otoliths was the Komiti Stream. Within the first hour conducted at the University of Waikato’s after sunset, spotlighting was carried out Mass Spectroscopy Suite using a Perkin along shallow (< 600 mm depth) stream Elmer Elan SCIEX DRCII inductively reaches and banded kokopu identified coupled mass spectrometer (ICP-MS) by spotlight were carefully scooped up with a New Wave Research Nd: YAG by dip net (5 mm mesh). Fish captured 213 nm wave length laser. Only six (by both methods) were anaesthetised in otoliths from Komiti Stream and six benzocaine until dead, measured to the from Pukenui Stream were suitable for nearest mm total length (TL), and placed analysis after sustaining damage during 28 New Zealand Natural Sciences 37 (2012)

Figure 1. Location of banded kokopu fishing sites in the Pukenui Stream above Whau Valley Reservoir near Whangarei on the east coast and Komiti Stream in the Kaipara Harbour on the west coast of northern New Zealand. the polishing and ablation process. To standards, a single line of spots across minimise the need to repeatedly open the otolith growth axis starting from the the laser ablation chamber, three otoliths nucleus to the edge of the otolith was mounted on a single glass slide were ablated. The core was identified with loaded into the chamber and purged transmitted light through an ablation by an argon carrier gas for 15 minutes chamber viewing screen. Spot diameter to remove any residual material in the was 30 µm, and the laser was fired at a chamber, lines and ICP. Prior to and repetition rate of 20 Hz; grid spacing after sample analysis National Institute ranged between 50-75 µm because larger of Standards and Technology (NIST) and smaller otolith sizes influenced the 612 standard reference material (SRM) amount of spots which could be placed for which concentrations of 50 elements on the otolith. The laser was fired at are known, was ablated. In between 50% output power and a 10 s inter-site Tana & Hicks: Open and closed populations of banded kokopu 29

pause to allow for background noise from acid (HNO3) and shaken. Water samples the previous firing point to dissipate. collected from both fish sampling sites Similarly, prior to ablation of each were analysed using ICP-MS in aqueous sample, argon gas blanks were flushed mode. The water sample transport lines through the sample chamber alongside were rinsed before and after each sample normal purge procedures when starting with Type-1 water and HNO3 (2 %), a new sample. The mean counts of blanks to clean the lines for the next sample. were subtracted from the sample counts The ICP-MS was calibrated at two per second (cps) to determine if any levels of sensitivity using Merck XXI polyatomic interferences were present standards. A calibration blank was run in the carrier gas and to provide baseline for specified elements at low sensitivity measures to show where true laser data 50 ppb and compared with a separate were being recorded and completed. standard with known elements of 50 Although a broad range of elements ppb, to indicate how close the readings were measured only three isotopes 88Sr, were to the standards. The process was 43Ca, and 137Ba were of interest in this also repeated at high sensitivity 330 ppb, study based on the effectiveness of these to determine the level of calibration one isotopes in documenting diadromous to the standards. Mean differences (± migrations in New Zealand (Closs et SD), in stream water chemistry for 88Sr al. 2003; David et al. 2004; Hicks et al. and 43Ca between the ten fishing sites 2005) and overseas (Arai et al. 2006; were evaluated by small-sample t-tests Limburg 1995; Tzeng 1996; Tzeng et al. (unequal variances) and are presented as 2005). Elemental data for otoliths are elemental concentrations in ppb. presented as mean counts per second for each isotope (ratioed to calcium) as a con- Results sequence of the lack of matrix-matched standards (Morales-Nin et al. 2005). Otolith Sr/Ca ratios Water sample analyses Banded kokopu from both sample Ten water samples from each stream streams showed varying levels of Sr/Ca were collected at separate fishing sites and Ba /Ca ratios (cps) from the nucleus at the same time as fish were collected (larval growth zone) to the otolith edge using 15 mL acid-washed Falcon tubes. (maturing growth zone), (Figures 2 & 3). In the field, the sampling tubes were Otoliths extracted from fish in Komiti rinsed thoroughly in the stream then Stream all showed peak Sr/Ca ratios filled completely and sealed with the cap 14-19 at the otolith nucleus indicating while submerged. Samples were then a marine rearing growth phase (Figure stored in a chilled thermos at about 4ºC 2). Similarly, from the nucleus edge for transport to the laboratory. In the noticeable decreases in Sr/Ca ratios were laboratory, water samples were filtered shown for all fish otoliths from Komiti through disposable 0.45 μm millipore Stream and were generally the same as filters and transferred back into sterile low level Sr/Ca ratios from above the 15 mL falcon tubes at a set volume of 9.8 reservoir < 2-5 with the exception of mL then topped off with 0.2 mL nitric one individual fish (Figure 2A, Table 30 New Zealand Natural Sciences 37 (2012)

Table 1. Summary information of fish collection dates, identification codes and location of fishing sites Komiti Stream (KS) and Pukenui Stream (PS) along with fish size (TL, mm) and otolith condition (after polishing) for laser ablation ICP-MS analysis.

1) which showed a slight increase in Sr/ zones reflective of permanent freshwater Ca ratios at the edge of the otolith. In residency (Figure 3A-E). Trends in Ba/ addition, fish from Komiti Stream were Ca ratios were more variable and typi- smaller (81mm to 142mm) than fish cally ranged around 0.008-0.032 across from above the Whau Valley Reservoir otolith growth zones. However, a large (95-175 mm), suggesting there were a 175mm adult fish (Figure 3F) indicated number of recent recruits (Figure 2B-F), unusually high Sr/Ca ratios. Most nota- as well as a resident adult (Figure 2A). bly, these high Sr levels were not observed Ba/Ca ratios generally demonstrated an at the nucleus (larval growth zone) but inverse relationship to Sr/Ca with ratios midway between the otolith edge and being lower near the otolith nucleus and nucleus fringe existing over a relatively slightly higher towards the otolith edge large proportion of the otolith before (Figure 2). decreasing back to original nucleus Sr/ Otoliths of fish taken from the Puke- Ca ratio levels 4 (Figure 3F). In addition, nui Stream above the reservoir showed all fish taken from above the reservoir consistent trends in otolith chemistry were mature adults 95-175 mm (Table with only slight variations in Sr/Ca ratios 1; McDowall 1990). Concentrations of at distance from the nucleus. Gener- Ca in water samples from Komiti Stream ally, Sr/Ca ratios followed relatively low (30163 ± 11213; mean ± 1 SD ppb), were uniform trends across all otolith growth significantly higher P( < 0.001) than in Tana & Hicks: Open and closed populations of banded kokopu 31

Figure 2. Elemental ratios of Sr/Ca and Ba/Ca (cps) in sequence from the otolith nucleus (µm) to the otolith edge of banded kokopu collected from Komiti Stream in the Kaipara Harbour. the Pukenui Stream (6983 ± 2551; mean ± clear access to and from the sea, marine 1 SD ppb), small sample t-test, N =10 for phase life strategies for banded kokopu each stream. Similarly, elemental concen- in this site were expected. Similarly, all trations of Sr were also significantly higher developmental trends associated with (P < 0.001), in Komiti Stream (341 ± 139; the recruitment of juveniles from the sea mean ± 1 SD ppb), than in the Pukenui suggest maturation in freshwater habitats. Stream (101 ± 22; mean ± 1 SD ppb). Banded kokopu populations above the Whau Valley Reservoir appear to be non- Discussion migratory (Figure 3). Banded kokopu typically have a larval marine growth stage All banded kokopu collected from Komiti (Charteris et al. 2003, McDowall 1995), Stream were shown to have marine phase subsequently low Sr/Ca ratios in otoliths life histories as larvae (indicated by high Sr/ of fish collected from above the reservoir Ca ratios at the core). Probably the most suggests that the recruitment of fish within important determinator of these migrations this watershed occurred entirely within was the absence of large in-stream barriers freshwater. such as dams waterfalls or culverts. With The propensity of banded kokopu to 32 New Zealand Natural Sciences 37 (2012)

Figure 3. Elemental ratios of Sr/Ca and Ba/Ca (cps) in sequence from the otolith nucleus (µm) to the otolith edge of banded kokopu collected from Pukenui Stream above the Whau Valley Reservoir. NB: Plots F and G are left and right otolith analyses from the same fish. adopt non-diadromous recruitment strate- Lake Okataina in the Rotorua District gies as a consequence of impeded access to of northeastern New Zealand (Rowe the sea is widely recognised and has been & Graynoth 2002). Additionally, a shown to occur throughout much of New number of small reservoirs (Waitakere Zealand. Schipper (1979) was the first to and Hunua reservoirs near Auckland), document landlocked banded kokopu in are also known to contain landlocked Lake Ototoa on the westcoast of Northland banded kokopu (Rowe & Graynoth New Zealand. However, in more recent 2002). While much of the evidence years landlocked banded kokopu have been supporting landlocking has been based recorded in Lake Kaihoka northwest of on identifying major in-stream barriers Nelson, Lake Hochstetter in Westland, and to migration, in the present study we Tana & Hicks: Open and closed populations of banded kokopu 33 used an alternative line of evidence to in lake and freshwater catchments with address this question based on high or geothermal and spring fed groundwater low Sr/Ca ratios. inputs (Muller, 1969). For banded kokopu collected above This would seem a likely answer to in- the Whau Valley Reservoir, the Sr/Ca ra- creased Sr/Ca uptake although given this tios suggest that fish have not been to sea. particular fish was a large adult and the However, one banded kokopu (Figure 3F, proportion of high Sr/Ca relative to time 3G), had high Sr/Ca ratios in midlife 29 (approx, 280 µm growth), the high Sr/ which not only exceeded ratios of other Ca levels would have to be relatively con- fish from the same location 5 but also sur- stant at that level and time period to be passed the marine ratios reflected in fish incorporated. These high Sr counts may from Komiti Stream 19. This may be due therefore be compounded by fluctuations to several factors the most obvious being in available calcium within the stream that the fish was flushed over the reser- (McDonald et al. 1983), which would voir, down into a marine environment limit calcium’s uptake and therefore fa- as a juvenile where it spent a substantial cilitate Sr and Ba uptake in fish otoliths amount of time before returning back in the absence of calcium (De Vries et al. over the reservoir as a larger fish sometime 2005). Similarly, given that Ba forms a later. Although banded kokopu are widely carbonate structure that is isostructural recognised as being excellent climbers with aragonite, it like Sr can substitute as post larvae-juveniles, with increasing for calcium within the otolith crystalline size the climbing ability of larger adults matrix when calcium is in low abundance would have been greatly reduced (Boubée (Campana 1999; Munro 2004). This was et al. 2000; McDowall 2000), making indicated at least for the water samples this highly unlikely. For this reason we collected from the Pukenui Stream with processed the right sagittal otolith using calcium concentrations (6983 ± 2551 the same preparation methods and laser ppb), significantly lower P( < 0.001) than ablation settings, which resulted in the in Komiti Stream (30163 ± 11213 ppb). general ratios and trends (Figure 3G), Similarly, low calcium in fish may also be indicating that they were a true reflection the product of disease or injury resulting of the fish’s life history. We suggest the in calcium deficiencies (Kulczykowskaet reason for these high Sr/Ca ratios maybe al. 2004). However, in some cases fish due to localised variations within the res- may recover from deficiency problems ervoir and its draining catchment. In this when calcium once again becomes read- study, we observed the presence of several ily available in the system (McDonald iron-rich seepages scattered throughout et al. 1983). In this study low calcium the same sample catchment including a availability, coupled with the presence small tributary stream which was covered of iron-rich seepages within the Whau in iron flocculent. Similarly, there is a Valley Reservoir may explain why the prior history of mining in the general indifferent Sr/Ca ratio of the fish above area (Manning 1996). The high presence the reservoir fluctuated over time (Figure of dissolved ions as a result of iron-rich 2A) before returning to similar ratios as seepages may accompany elevated Sr was indicated in its early rearing stage. levels, which have been shown to occur Overall, this study illustrated that banded 34 New Zealand Natural Sciences 37 (2012) kokopu are flexible in their migratory life NIWA Client Report ARC. strategies regardless of in stream barriers, Campana, S.E. & Neilson, J.D. (1985). with fish collected from above the reser- Microstructure of fish otoliths. voir indicating permanent freshwater resi- Canadian Journal Fish Aquatic Science. dent life histories, while banded kokopu 42: 1014–1032. collected from Komiti Stream, exhibited Campana, S. E. (1999). Chemistry and early marine life histories indicative of composition of fish otoliths: pathways, their diadromous origins. The study pro- mechanisms and applications. Review. vides further evidence of non-diadromous Marine Ecology Progress Series 188: recruitment for banded kokopu as a 263-297. consequence of a large in-stream barrier Campana, S. E. & Thorold, S. R. (2001). and will add to the current information Otoliths, increments, and elements: on the known distribution of landlocked keys to a comprehensive understanding species. Future management and conser- of fish populations?Canadian Journal vation impetus will need to build on and Fish Aquatic Science 58: 30-38. include a broader understanding of the Charteris, S. C., Allibone, R. M., & extent of diadromy for a range of species Death, R. G. (2003). Spawning site throughout New Zealand. selection, egg development, and larval drift of Galaxias postvectis and G. fasciatus in a New Zealand stream. Acknowledgements Journal of Marine and Freshwater Research 37: 493-505. This research was carried out for a Special Closs, G.P., Smith, M., Barry, B., & Topic BIOL307 study and was funded by Markwitz, A. (2003). Non-diadromous the Department of Biological Sciences, recruitment in coastal populations University of Waikato. We are grateful of common bully Gobiomorphus for field assistance from Steve Pohe cotidianus. New Zealand Journal of and help from laser technician Steve Marine and Freshwater Research 37: Cameron of the Mass Spectrometry Suite, 301–313. Department of Chemistry, University David, B., Chadderton, L., Closs, G.P., of Waikato. Helpful comments on the & Markwitz, B. (2004) Evidence of manuscript were provided by two referees. flexible recruitment strategies in coastal populations of giant kokopu Galaxias References argenteus. DOC Science Internal Series 160, New Zealand Department of Arai, T., Yang, J., & Miyazaki, N. Conservation Wellington, pp.1-23. (2006). Migration flexibility between De Vries, M .C., Gillanders, B. M., freshwater and marine habitats of the & Elsdon, T. S. (2005) Facilitation pond smelt Hypomesus nipponensis. of barium uptake into fish otoliths: Journal of Fish Biology 68: 1388–1398. Influence of strontium concentration Boubée, J. A. T., Richardson, J., & and salinity. Ge o c h i m i c a e t Williams, E. (2000) Fish Passage: Cosmochimica Acta 69: 4061–4072. Review and Guidelines for the Hicks, A.S., Closs, G.P., & Swearer, S.E. Auckland Regional Council. Auckland, (2008). Otolith microchemistry of Tana & Hicks: Open and closed populations of banded kokopu 35

two amphidromous galaxiids across Journal of Experimental Biology 102: an experimental salinity gradient: A 141-155. multi-element approach for tracking McDowall, R. M. (1972). The species diadromous migrations. Journal of problem in freshwater fishes and Experimental Marine Biology and the of diadromous and Ecology 394: 85-97. lacustrine populations of Galaxias Hicks, B .J., West, D.W., Barry, B.J., maculatus (Jenyns). Journal of the Royal Markwitz, A., Baker, C.F, & Mitchell, Society of New Zealand 2: 325-367. C. P. (2005). Chronosequences of McDowall, R.M. (1988). Diadromy in strontium in the otoliths of two New fishes: migrations between freshwater and Zealand migratory freshwater fish, marine environments. Croom Helm, inanga Galaxias maculatus and koaro London. G. brevipinnus. International Journal of McDowall, R.M. (1990). New Zealand PIXE, 1-7. Freshwater Fishes: a Natural History and Kalish, J. M. (1990). Use of otolith Guide. Heinemann Reed, Auckland. microchemistry to distinguish the McDowall, R.M. (1993). Implications progeny of sympatric anadromous and of diadromy for the structuring and non- anadromous salmonids. Fishery modeling of riverine fish communities Bulletin (US) 88: 657-66. in New Zealand. New Zealand Journal Kulczykowska, E., Sokolowska, E., of Marine and Freshwater Research 27: Gozdowska, M., & Kalamarz, H. 453-462. (2004). Disruption of the melatonin McDowall, R.M. (1995). Seasonal rhythm in wild and farmed fish: a pulses in migrations of New Zealand consequence of prolonged thyroxine diadromous fish and the potential administration and calcium depletion. impacts of river mouth closure. Journal of Fish Biology 65: 331-332. New Zealand Journal of Marine and Limburg, K.E. (1995). Otolith strontium Freshwater Research 29: 517-526. traces environmental history of McDowall, R.M. (1996). Diadromy and sub-yearling American shad Alosa the assembly and restoration of riverine sapidissima. Marine Ecology Progress fish communities: a downstream Series 119: 25–35. view. Canadian Journal of Fisheries Manning, D. (1996). Natural areas and Aquatic Sciences, 53 (Suppl. 1): of Whangarei Ecological District, 219–236. Reconnaissance survey report for the McDowall, R. M. (2000). Hidden treasures Protected Natural Areas Programme. exposed: discovering our freshwater fish Published by the Department of fauna. Cawthron Institute Nelson New Conservation Northland Conservancy, Zealand, pp. 1-24. Whangarei New Zealand, pp.132-145. McDowall, R.M. (2007). On McDonald, D. G., Walker, R. L., amphidromy, a distinct form of & Wilkes, P. R. H. (1983). The diadromy in aquatic organisms. Fish interaction of environmental Calcium and Fisheries, 8: 1–13. and low pH on the physiology of the Michel C., Hicks, B.J., Stölting, K.N., Rainbow Trout, Salmo gairdneri: II. Clarke, A.C., Stevens, M.I., Tana, R., brachial ionoregulatory mechanisms. Meyer, A., & van den Heuvel, M. R. 36 New Zealand Natural Sciences 37 (2012)

(2008). Distinct migratory and non- 1835. migratory ecotypes of an endemic Tzeng, W. N. (1996). Effects of salinity New Zealand eleotrid (Gobiomorphus and ontogenetic movement on cotidianus) – implications for incipient strontium: calcium ratio in otolith speciation in island freshwater fish of the Japanese eel Anguilla japonica species. BMC Evolutionary Biology (Temminck and Schlegel). Journal 49: 1-14. Experimental Marine Biology and Morales-Nin, B., Swan, S. C., Gordon, Ecology 199: 111-122. J. D. M., Palmer, M., Geffen, A. J., Tzeng, W. N., Severin, K. P., Wang, Shimmield, T., & Sawyer, T. (2005). C. H., & Wickstrom, H. (2005). Age-related trends in otolith chemistry Elemental composition of otoliths as a of Merluccius merluccius from the discriminator of life stage and growth north-eastern Atlantic Ocean and the habitat of the European eel, Anguilla western Mediterranean Sea. Marine anguilla. Marine and Freshwater and Freshwater Research 56: 599-607. Research 56: 629-635. Muller, G. (1969). High strontium contents and Sr/Ca ratios in Lake Constants waters and carbonates and their sources in the drainage area of the Rhine River (Alpenrhein). Mineral Deposita 4: 75-84. Munro., A. R. (2004). Identification of life history variation in salmonids using otolith microchemistry and scale patterns implications for illegal introductions and for whirling disease in Missouri River rainbow trout. Fish and Wildlife Biology. Montana State University, pp. 1-218. Rowe, D.K. & Graynoth, E. (2002). Lake Managers’ Handbook; Fish in New Zealand Lakes. The Ministry for the Environment, Wellington, New Zealand. Schipper, C. M. (1979). Landlocked banded kokopu (Galaxias fasciatus) from Lake Ototoa. Fisheries Research Division, New Zealand Ministry of Agriculture and Fisheries, Rotorua. Thorrold, S. R., Jones, C. M., Campana, S. E., McLaren, J. W., & Lam. J. W. H. (1998). Trace element signatures in otoliths record natal river of juvenile American shad Alosa sapidissima. Limnology and Oceanography 43: 1826-