Downstream spawning migration by the amphidromous ... - CiteSeerX

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Marine and Freshwater Research, 2013, 64, 31–41 http://dx.doi.org/10.1071/MF12196

Downstream spawning migration by the amphidromous Australian grayling (Prototroctes maraena) in a coastal river in south-eastern Australia W. M. Koster A,B,D, D. R. Dawson A and D. A. Crook A,C A

Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment, 123 Brown Street, Heidelberg, Vic. 3084, Australia. B School of Life and Environmental Sciences, Deakin University, Warrnambool, Vic. 3280, Australia. C Present address: Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia. D Corresponding author. Email: [email protected]

Abstract. Understanding the reasons and cues for migration is crucial for developing effective conservation and management strategies of diadromous fishes. Spawning and movement patterns of the threatened diadromous Australian grayling (Prototroctes maraena) were investigated in the Bunyip River, Victoria, using drift sampling (2008–2011) and acoustic telemetry (2009–2010) during the autumn–winter spawning period of each year. Fifty-five adult fish (2009: n ¼ 21; 2010: n ¼ 34) were tagged and released in February ,15–30 km upstream of the Bunyip River estuary. Thirteen fish (2009: n ¼ 7; 2010: n ¼ 6) undertook rapid downstream migrations from March to April to reaches immediately upstream of the estuary. Drifting eggs were detected at multiple sites between April and July; however, the majority (78.8%) were collected in the lower reaches within ,0.5 km of the estuary in early–mid-May. Tagged adult fish arrived in this area 1–4 weeks before eggs were detected and usually moved back upstream within 2 weeks following the peak egg abundance. Downstream migration and peak egg abundance were associated with increased river flows. Although the proportion of fish that undertook migrations was low, low rates of tag retention in this species likely account for the failure to detect migration by many of the tagged individuals. Additional keywords: amphidromy, environmental flows, reproduction, Retropinnidae, telemetry. Received 20 July 2012, accepted 6 November 2012, published online 6 February 2013

Introduction Migration between habitats is an important, and often complex, component of the life histories of freshwater fish (Eiler 2000; Lucas and Baras 2001). For many fish species, migration occurs for the purposes of reproduction, sometimes to specific breeding grounds and over long distances, and is often associated with the onset of particular environmental conditions (e.g. changes in flow, temperature, photoperiod) (McKeown 1984; Jonsson and Jonsson 2009; Crook et al. 2010). Understanding the reasons and cues for migration is critical to the development of targeted strategies for fish conservation and management. For example, confirming a relationship between flow events and spawning migrations provides the basis for scientifically defensible decisions relating to the provision of environmental flows (e.g. autumn–winter flow pulses or ‘freshes’ to trigger migration) (Crook et al. 2010; Reinfelds et al. 2011), whilst identification of key spawning grounds allows for management actions (e.g. planning controls and conditions) to protect these areas (Hicks et al. 2010). Journal compilation Ó CSIRO 2013

The Australian grayling (Prototroctes maraena) (Gu¨nther, 1864; Retropinnidae) is a migratory fish found in coastal rivers and streams in south-eastern Australia. The species is amphidromous (McDowall 2007), with adult fish spawning in freshwater and larvae drifting downstream to the sea, where they spend 4–6 months before migrating back into freshwater as juveniles (Berra 1982; Crook et al. 2006). Males may spawn in their first year but females do not spawn until their second year (Berra 1984). Australian grayling grows up to ,300-mm total length and was reported in the late 1880s to early 1900s to be a popular angling species (Saville-Kent 1886a; Stead 1903; McDowall 1996). The species has declined dramatically since European settlement and is currently listed as threatened under State and Federal legislation (Backhouse et al. 2008a). Altered flow regimes, barriers to movement, habitat degradation and alien species are considered to be likely contributors to the decline (Backhouse et al. 2008b). The only other member of the genus, the New Zealand grayling (Prototroctes oxyrhynchus), was last recorded in 1923 and appears to be extinct (McDowall 1976). www.publish.csiro.au/journals/mfr

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Marine and Freshwater Research

Although various aspects of the biology of Australian grayling have been studied over many years (Allport 1870; Saville-Kent 1885, 1886a, 1886b; Stead 1903; Lord and Scott 1924; Bishop and Bell 1978; Berra 1982, 1984; 1987; Bacher and O’Brien 1989; Hall and Harrington 1989; O’Connor and Mahoney 2004; Crook et al. 2006; Schmidt et al. 2011), substantial gaps remain in our knowledge of the movement and spawning behaviours of adults. Previous studies have suggested that spawning takes place from February to May, on the basis of examination of fish gonads and observations of newly spent fish, although eggs and larvae were not collected, nor have spawning locations been determined (Bishop and Bell 1978; Berra 1982; Hall and Harrington 1989). It has been proposed that mature fish rely on increases in river flow to initiate spawning and may undergo ovarian involution in the absence of appropriate flow cues (O’Connor and Mahoney 2004). Spawning has also been reported to coincide with decreases in water temperature to ,12–138C (Berra 1982; Hall and Harrington 1989). It has been suggested that adult fish migrate downstream before spawning (Saville-Kent 1886a; Stead 1903; Lord and Scott 1924), although the evidence for this is equivocal. Saville-Kent (1886a) observed fish spawning in the lower reaches of the Derwent River, Tasmania, and Stead (1903) and Lord and Scott (1924) suggested that spawning may take place in brackish water. It has since been shown that artificially fertilised eggs developed normally only in water of salinity ,5 g L1 (Bacher and O’Brien 1989). Berra (1982) collected large numbers of recently spent fish in the freshwater mid-reaches of the Tambo River, Victoria, and suggested that spawning most likely occurs in the freshwater mid-reaches of the river. The aims of the current study were to use telemetry techniques to determine whether adult Australian grayling undertakes downstream migrations to the lower reaches of rivers during the spawning period, and confirm the timing, location and spatial extent of spawning by sampling eggs and larvae. The migratory and spawning behaviours of Australian grayling are discussed with regards to previous work on diadromous fish, and the implications for management of this threatened species. Materials and methods Study site The study was conducted in the mid- to lower Bunyip River (mean stream width 6–8 m), a coastal stream that flows into Westernport Bay, 90 km east of Melbourne, Victoria, Australia (Fig. 1). The length of the Bunyip River is ,65 km, with a catchment area of 979 km2 (Earth Tech 2006). The main tributary of the Bunyip River is the Tarago River, which experiences flow regulation as a result of the operation of Tarago Reservoir. The upper reaches of the catchment are forested and the lower reaches consist predominantly of cleared agricultural land and small urban areas. The Bunyip River estuary is relatively small, with saline water penetrating the lower reaches only during high tides. A weir ,4 km from the Bunyip River mouth at Koo Wee Rup defines the maximum upstream limit of tidal influence, although during surveys of the tidal range of the estuary, tidal influence was not detected further than 3.3 km from the mouth (Earth Tech 2006). A rock-ramp fishway was constructed on the

W. M. Koster et al.

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Fig. 1. Map showing location of the study site. White triangles represent the locations of each of the listening stations in the Bunyip River. Black circles represent the locations of each of the drift sampling sites.

weir in 1998 to facilitate fish passage. The lower catchment once comprised a large wetland complex of 30 000 ha known as the Koo Wee Rup Swamp, into which the Bunyip River flowed (Yugovic and Mitchell 2006). Extensive drainage activities and land clearing since the 1870s have vastly altered the Koo Wee Rup landscape and the lower Bunyip River now consists of a highly modified and straightened channel (Yugovic and Mitchell 2006). Despite its degraded state, the lower Bunyip River supports a diverse native fish fauna and a relatively abundant Australian grayling population (Hortle and Lake 1983; W. M. Koster, unpubl. data). Fish movement Acoustic telemetry Australian grayling (mean s.e. fork length (FL) 210 1.9 mm, range 175–240 mm) was collected from a range of sites in the Bunyip River between 15 and 30 km upstream of the estuary, by using a back-pack electro-fishing unit. Fish were tagged with acoustic transmitters in February 2009 (n ¼ 21) and February 2010 (n ¼ 34). Fish were occasionally encountered in small schools, but only one individual was collected per school to minimise holding time, eliminate crowding and associated

Migration and spawning of Australian grayling

stress (Bridger and Booth 2003) and minimise the potential for bias caused by multiple tagged fish from a school moving nonindependently. The timing of tagging was chosen to avoid the onset of gonad development (mid-March) (Berra 1982, 1987). On capture, fish were immediately transferred from the stream into an aerated, circular 50-L holding container and individually anaesthetised (0.03 mL AQUI-S per litre water) (AQUI-S, Lower Hutt, New Zealand). The transmitters (model V7-4L, Vemco, Nova Scotia, Canada; frequency 69 kHz; dimensions: 22 7 mm; weight 1.8 g in air; average delay between transmissions 60 s; estimated battery life 150–170 days) were implanted into the peritoneal cavity through an incision of 8–10 mm, on the ventral surface between the pelvic and anal fins, slightly towards the lateral side of the body wall. The transmitters were gently pushed away from the incision towards the anterior. To minimise handling and surgery time, the incision was not closed with sutures (see Koster and Crook 2008). We considered this important because observations in the field and aquaria showed that Australian grayling is an extremely delicate species that does not tolerate handling well. Only fish .170-mm FL were tagged to ensure that the transmitter : fish weight ratios remained below ,2% (Winter 1996). On the basis of length–age relationships for the species, these fish are likely to be 2þ years old and therefore capable of spawning (Berra and Cadwallader 1983; Berra 1984). Each fish was placed into a recovery net positioned in the stream channel. Once the fish were observed to maintain their balance and freely swim throughout the holding net, they were released near their point of capture (i.e. within 5 m). Twenty-five acoustic listening stations (Model VR2W, Vemco) were deployed in February 2009, between the township of Bunyip and Westernport Bay (a distance of ,40 km) (Fig. 1). The listening stations were deployed using a length of plasticcoated stainless-steel cable attached to metal pickets as anchor points. Range tests showed that the listening stations had detection ranges of ,60–80 m, depending on the physical attributes of the site (e.g. depth, turbulence). Data were downloaded from the listening stations bi-monthly for the duration of the study. After 2009, the placement of listening stations was refined. Ten of the listening stations were re-positioned in February 2010 to the lower reaches near Koo Wee Rup because the results obtained in 2009 indicated that the downstream migration of fish was directed to these reaches (Fig. 1). The relocation of listening stations provided more precise information on fish locations within these reaches, in particular on whether individual fish migrate to the same areas of river to spawn. Radio-telemetry Radio-telemetry was used in 2010 to investigate potential reasons for the apparently restricted movement of many fish tagged with acoustic transmitters in 2009. Unlike fixed-array acoustic telemetry, which provides only coarse-scale spatial information, radio-telemetry allows locations of fish to be determined with a very high spatial resolution (e.g. ,2 m) (David and Closs 2002). Twenty Australian grayling individuals (mean s.e. FL 210 3.8 mm, range 170–240 mm) were collected near Cora Lynn, 10–15 km upstream of the estuary, by using a back-pack electro-fishing unit, between late February and early March 2010. Radio-transmitters with an internal coil


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antenna (Model 1010, Advanced Telemetry Systems (ATS), Isanti, USA; frequency 150 MHz; dimensions 20 9 mm; weight 1.4 g in air; estimated battery life 34 days) were implanted into the peritoneal cavity by using the method described above and released at the point of capture. The radio-transmitters had dimensions very similar to those of acoustic transmitters. Radio-tracking began 3–6 days after transmitter implantation. Fish movements were recorded during daylight on two occasions per week, from late February to late March 2010. Fish were located by triangulation from the bank and within the stream with a hand-held, three-element Yagi antenna and an ATS receiver (R4100). Markers were placed at 5-m intervals on the bank to assist with locating of fish. The radio-transmitter trial revealed high rates (85%) of transmitter expulsion. Radio-transmitters from 17 of the 20 tagged Australian grayling were located in the same position on consecutive occasions 6–9 days after tagging. We conducted searches for the transmitters and retrieved eight transmitters from the streambed. The small size of transmitters, variable flow and substrate complexity made locating of the transmitters difficult, and nine transmitters could not be retrieved. These transmitters remained in the same position following three 20-s back-pack electro-fishing passes in the immediate area and, therefore, we concluded that they had been expelled. Two tagged fish which had expelled their transmitters (identified by a small incision and absence of tag) were recaptured by electro-fishing. The body condition of these fish was normal and there were no signs of infection or poor health. Extensive visual searches were also undertaken by wading the stream between the most upstream release location and ,2 km below the most downstream release location, on three occasions between early and late March 2010. No dead fish were found during the visual searches. Only three Australian grayling individuals retained their radio-transmitters for the duration of the tracking period, as evidenced by shifts in their positions over distances of tens of metres or more throughout this period. These three fish were located and visually observed to be swimming freely, feeding and interacting with other conspecifics. Spawning Fish eggs and larvae were collected at three sites in the freshwater reaches of the Bunyip River, using two drift nets set at each site in 2008, 2009 and 2010 (Fig. 1). Eggs and larvae were also collected in 2011, although sampling was restricted to the most downstream site (Koo Wee Rup) where most eggs and larvae were collected in the previous 3 years. Sampling was conducted every 1–2 weeks from March to July in each year. Drift nets were 1.5 m long, with a 0.5-m-diameter mouth opening, consisted of 500-mm mesh, and had flow meters fitted to the mouth of the net to measure the volume of water filtered. The nets were set in late afternoon (1500–1700 hours) and retrieved the following morning (0800–1000 hours) (approximate soak time 17–18 h). Samples were immersed into a solution of overdosed anaesthetic (4 mL Alfaxan per litre water) (Jurox, Rutherford, NSW, Australia) for 10 min to euthanase any fish, and then preserved in 70% ethanol and sorted in the laboratory under a dissecting microscope. Because no egg or larval identification keys were

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available for Australian grayling, genetic analysis was undertaken by staff at Griffith University, Brisbane, Queensland, to identify a subsample of 613 specimens. Specimens were selected to include a range of sizes, as well as a range of sampling trips and sites. DNA was extracted using either a modified CTAB procedure (Doyle and Doyle 1987) or a modified salt-extraction method (Aljanabi and Martinez 1997). Polymerase chain reactions (PCRs) were performed to amplify 658 bp of the mitochondrial ATPase gene by using the primers ATP 82 L8331 and COIII 2H9236 (S. McCafferty, unpubl. data; http://stri.si.edu/sites/bermingham/research/primers/index.html). PCR products were purified using exonuclease I and shrimp alkaline phosphate and sequenced on a 3130 Genetic Analyser (Applied Biosystems, Foster City, CA) using Big Dye Terminator mix v3.1 (Applied Biosystems). Sequences were manually aligned, edited and compared with known ATPase genes from autumn–winter-spawning species recorded in coastal Victorian streams using Sequencher 4.9 (Genecodes, Ann Arbor, MI, USA). The species compositions of the samples that were not identified using genetic techniques were estimated on the basis of ratios of genetic identities confirmed at each site for each week of sampling. Environmental variables Daily discharge records were obtained from a gauging station at Iona (Fig. 1). Water temperature and electrical conductivity were measured using a data recorder (Odyssey, Dataflow Systems, Christchurch, New Zealand) at Cora Lynn and using a hand-held water-quality meter (90FL-T, TPS, Brisbane, Australia) at each of the drift sampling times on each sampling trip. During the years when fish were tagged (2009 and 2010), water temperature and electrical conductivity were also measured using data recorders at Koo Wee Rup at two sites downstream of the weir between March and July, to determine the upstream extent of saltwater ingress, although no data were obtained for 2009 because the recorders were lost following high flows. Data analysis Generalised linear models were used to examine relationships between the number of acoustically tagged fish moving downstream each day (using a poisson error term) and the mean daily flow and water temperature during the downstream migration period, separately for 2009 and 2010, using R 2.14.0 (R Development Core Team 2012, The R Foundation, Vienna). The downstream-migration period was defined as from midMarch until early May. Mid-March was chosen as the starting date for the downstream-migration period, because gonadal development begins around this time (Berra 1982, 1987). Early May was chosen as the end date, because all migrating fish had arrived at the lower reaches (i.e. 2–6 km upstream of where the Bunyip River enters Westernport Bay) by this time. Although Australian grayling may exhibit schooling behaviour at times, each tagged fish was considered to represent an independent observation, as described above. Linear models were used to examine relationships between egg density (number of eggs per 1000 m3) and the mean weekly flow before each sampling collection date from mid-March to

W. M. Koster et al.

the end of July, using R 2.14.0. This analysis included only data from the Koo Wee Rup site because insufficient eggs were collected at the other sites for analysis. The four years of data were combined to provide enough replicates for the models. A weekly period was chosen to represent flow conditions because the exact age of eggs was unknown; however, most eggs were likely to be less than about 7 days old because they were at early development stages (i.e. eyes not yet developed) (Allport 1870; Saville-Kent 1885; Bacher and O’Brien 1989). To account for inter-annual variation in egg density and flows, egg density and flow was standardised across years. Egg density was converted for each sampling date to a percentage of the total number of eggs for that year, whereas flow for each sampling date was converted to a percentage of the maximum weekly flow during the spawning period for that year. Data were split into two periods, the first being sampling dates up to and including the first major spawning event and the second being dates after this event in each year, so as to assess the influence of flow on initial peak spawning and subsequent spawning. Generalised least-squares (gls, Zuur et al. 2009) were used instead of ordinary least-squares (ols) because variance in standardised egg density increased with increasing flows for the first period. Temperature was not included in this analysis because of the difficulty in standardising temperatures across years and the small sample size. Results Acoustic tracking Of the 55 Australian grayling individuals tagged across 2 years, 47 (2009: n ¼ 21 (100% of tagged fish); 2010: n ¼ 26 (76% of tagged fish)) were detected by the listening stations. The decrease in the percentage of fish detected in 2010 compared with 2009 is partly attributable to the re-positioning of many of the listening stations to the lower reaches, further away from the area where fish were released. Twenty-two of the fish were recorded for only a short period after release (,30 days) on a single station closest to their release point or multiple stations near (,0.5 km) their release point. Twelve of the fish were recorded for an extended period (i.e. several months), but only on single stations after ,30 days. The radio-tracking trial (see above) showed that many (85%) of the tagged fish had expelled their transmitters, which likely accounts for the failure to detect movement by many of the fish tagged with acoustic transmitters. The remaining 13 fish (2009: n ¼ 7; 2010: n ¼ 6) (mean s.e. FL 205 3.8 mm, range 180–220 mm) were detected moving downstream to the lower reaches of the river (Fig. 2). Similar movement patterns were observed each year, with tagged adults undertaking rapid downstream migrations from late March to late April over distances between 15 and 30 km, to reaches immediately upstream of the estuary. Once fish were first detected moving, they continued moving downstream over 1–4 days. Five of these individuals arrived at the lower reaches of the river during this period, some moving over 15–18 km (e.g. Fig. 2e–g). The other eight fish temporarily ceased migrating between ,4 and 14 km downstream of their release points (e.g. Fig. 2c, j, k). These fish then recommenced downstream movement ,1–3 weeks later, moving a further 3–18 km over 1–4 days, to the lower reaches of the river. The


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Fig. 2. Movement patterns of all Australian grayling tagged with acoustic transmitters that migrated downstream in the Bunyip River in (a–g) 2009 and (h–m) 2010. White triangles on the y-axis represent the locations of each of the listening stations. Black circles show the date and location of tagging and grey circles show detections of tagged fish on the listening stations. The broken line joins consecutive detections for clarity, but does not necessarily represent the timing of movements between listening stations. Red dashed line represents instantaneous temperature (30-min intervals) and the blue line represents daily mean discharge in the Bunyip River at Cora Lynn and Iona, respectively.

downstream migrations corresponded with the timing of spawning (see below). All 13 of the fish detected moving downstream halted their migration at locations 2–6 km upstream of where the Bunyip River enters Westernport Bay. Six of these fish were detected by a listening station located 3.5 km upstream of the mouth (i.e. potentially within the 3.3-km upstream tidal limit of the estuary (Earth Tech 2006), given the next downstream listening station was 0.5 km further downstream), although only for short periods (,1–3 days). Measurements of electrical conductivity

3.9 and 3.3 km upstream from the mouth between March and July 2010 reached a maximum of 500 and 1200 mS cm1, respectively, indicating a lack of saltwater ingress at these locations. Two fish were detected 2 km upstream of the mouth (i.e. within the upstream tidal limit) during the spawning period, for short periods (,1 day); electrical conductivity at this location during these times is unknown. Five of the 13 fish spent 1–6 days and seven fish spent between 18 and 35 days in the lower reaches of the river throughout April–May, before rapidly moving back upstream



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Fig. 3. Initiation of downstream movement of Australian grayling tagged with acoustic transmitters in the Bunyip River in (a) 2009 and (b) 2010. The arrows indicate the dates when downstream movement was first detected. Letters in italics refer to individual fish and correspond to the same letters as in Fig. 2. Red dashed line represents instantaneous temperature (30-min intervals) and the blue line represents daily mean discharge in the Bunyip River at Cora Lynn and Iona, respectively. 6

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Discharge (ML day⫺1) Fig. 4. Scatterplot showing the relationship between the daily numbers of Australian grayling tagged with acoustic transmitters moving downstream and daily mean discharge in the Bunyip River in (a) 2009 and (b) 2010 during the downstream migration period (defined as the period from mid-March until all tagged migrating fish reached the lower reaches, i.e. early May).

in early to late May. Another fish spent 52 days in the lower reaches between April and June, before moving ,5 km upstream in mid-June, where it was last detected (Fig. 2i). Following spawning, seven of the fish returned to within 1–2 km of their original release point (e.g. Fig. 2a, b, e). One of these fish moved downstream again in mid-May and made a range of upstream and downstream movements before moving back upstream to near its pre-movement location (Fig. 2a). One of the fish moved downstream again in mid-June, to ,8 km upstream of the river mouth, where it was last detected (Fig. 2j). Times when fish were first detected moving downstream coincided with increases in flow (e.g. from 28.7 to 68.7 ML day1 in early April 2009, 38.2 to 158.3 ML day1 in late April 2009, 48.0 to 77.8 ML day1 in mid April 2010, 47.9 to 122.5 ML day1 in late April 2010) on a rising limb or near the peak of the hydrograph (Figs 2, 3). Water temperature during times when downstream movement was first detected also decreased (e.g. from 19.48C to 15.88C in early April 2009, from 14.78C to 11.08C in late April 2009, from 17.68C to 14.98C in mid-April 2010, from 18.38C to 16.88C in late April 2010) (Fig. 2). Once fish were first detected moving downstream, they continued

moving downstream during the flow peak or as water levels dropped. Cessation of downstream movement by migrating fish typically coincided with 1–3 days of decreasing flows following a flow peak. Downstream movement recommenced when flow again increased. On the basis of poisson regression models, there were significant positive relationships between the number of fish moving each day and mean daily flow (ML day1) in 2009 (z1,45 ¼ 3.68, P , 0.001) (Fig. 4a) and 2010 (z1,46 ¼ 6.57, P , 0.001) (Fig. 4b). Spawning In total, 9085 eggs and 491 larvae of Australian grayling were collected in the drift sampling (Table 1). Eggs and larvae were collected in all 4 years; however, their abundance varied among years, and also among the three sites in the first 3 years of sampling. A high percentage (95.8%) of eggs and larvae was collected from the most downstream site (Koo Wee Rup) during the first 3 years. Eggs and larvae were collected from May to July in 2008 and 2009, from April to July in 2010, and from March to June in 2011 (Fig. 5). The abundance of eggs and larvae was highest in 2010 and lowest in 2008 (Table 1). In the



Table 1. Total number of Australian grayling eggs and larvae collected during the 2008, 2009, 2010 and 2011 sampling events at the three collection sites in the Bunyip River Cl, Cora Lynn; Knth, Koo Wee Rup North; Kwr, Koo Wee Rup Stage

2008

2009

2010

2011

Cl Knth Kwr

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Cl Knth Kwr

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201 11

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1575 124

Egg 32 Larvae 9

37 8

91 81

(a) 2008

0 5

788 164

20 0

Koo Wee Rup

6336 89

tagged fish moved downstream. Water temperature during these times also decreased (i.e. from 12.68C to 9.58C in mid–late May 2008, from 14.78C to 10.08C in late April–early May 2009, and from 13.58C to 11.98C in mid-May 2010) (Fig. 5). In 2011, peak egg abundances were also collected immediately following an increase in flow (i.e. from 284.7 to 1699.6 ML day1 in midApril 2011) (Fig. 5). Large numbers of eggs were also collected in early May 2011 after this flow peak subsided but when there was another smaller increase in flow (i.e. from 330.2 to 357.1 ML day1) (Fig. 5). In contrast to the first 3 years, water temperature during this period was higher and relatively stable (i.e. ,14.9–15.58C) (Fig. 5). There was a significant positive relationship between standardised egg density and mean weekly flow for the period up to and including the first major spawning event (t1,15 ¼ 3.14, P ¼ 0.007). In contrast, there was no relationship in the second period (t1,33 ¼ 0.84, P ¼ 0.409). Measurements of water temperature and electrical conductivity

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first 3 years, peak egg abundances were collected immediately following increases in flow (i.e. from ,47.5 to 68.3 ML day1 in mid–late May 2008, from 38.2 to 158.3 ML day1 in late April 2009, from 74.5 to 136.7 ML day1 in mid-May 2010) (Fig. 5) and in 2009 and 2010 occurred shortly after the period when

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Jul

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Fig. 5. Adjusted total density of Australian grayling eggs (grey bar) and larvae (black bar) per 1000 m3 collected in drift nets in the Bunyip River. Solid triangles on x-axis indicate sampling events. Red dashed line represents instantaneous water temperature (30-min intervals) and the blue line represents daily mean discharge in the Bunyip River at Cora Lynn and Iona, respectively.

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were similar at each drift-net site and ranged from 78C to 198C and from 200 mS cm1 to 500 mS cm1. Discussion Downstream spawning migrations The present study has confirmed that reproduction of Australian grayling in the Bunyip River takes place in freshwater reaches, predominantly just above the estuary, and that spawning occurs following the downstream migration of adults to this area. The timing of downstream migration by Australian grayling was consistent, with all fish migrating downstream between late March and late April in each year. All downstream-migrating fish moved to the same reach of river upstream of the estuary mouth in each year, regardless of where they were tagged (i.e. 20 km or 35 km upstream of the river mouth), and most returned back upstream to areas near their original capture location after spawning. The proportion of tagged fish that undertook migrations was low; however, as the radio-tracking trial revealed, a high rate of transmitter rejection likely accounted for the failure to detect migration by many of the tagged individuals. Although transmitter rejections were high and limited the data collected, observations of the behaviour and condition of fish that had both retained and lost transmitters suggested that the tagging procedure is unlikely to have caused high rates of mortality. The results of other studies also have suggested that high rates of transmitter rejection do not necessarily result in high mortality of tagged fish (Summerfelt and Mosier 1984; Chisholm and Hubert 1985). It appears likely that loss of transmitters occurred through the non-sutured incision site. Although incisions are usually closed with sutures, previous studies have shown that non-closure can be effective for delicate species that are prone to handling stress and fungal infection (Baras and Jeandrain 1998; Jepsen et al. 2002; Koster and Crook 2008). The approach we used for tagging Australian grayling with telemetric transmitters conforms closely with the scheme outlined for developing tagging methods for threatened species by Ebner et al. (2009). Prior to the study, we had successfully applied the transmitter-insertion technique on a non-threatened, surrogate species (river blackfish, (Gadopsis marmoratus), Koster and Crook 2008) and determined, on the basis of observations of a relatively large total population size, that a sample of Australian grayling could be tagged without causing a major risk to the Bunyip River population. Because of their sensitivity to handling, we considered the risks of transmitterinsertion trials (e.g. Broadhurst et al. 2009) in captivity excessive. The acoustic- and radio-tagging were therefore used as a field-based trial of the transmitter-insertion method, as well comprising part of our main study. Although the outcomes clearly demonstrated a need for further refinement of the transmitter-insertion technique, the results obtained for the fish that retained transmitters, nonetheless, provided critical information on the migratory characteristics of the species. The finding that adult Australian grayling undertakes downstream spawning migrations to the lower reaches of the Bunyip River during March and April supports suggestions by Stead (1903) and Lord and Scott (1924) that Australian grayling moves downstream in autumn to spawn. Downstream spawning

W. M. Koster et al.

migrations have been reported for many other diadromous fish species, although typically they involve migrations of adult fish to estuarine or marine waters to spawn (i.e. catadromy) (e.g. Harris 1986; Boube´e et al. 2001; Crook et al. 2010). Although there are other examples of amphidromous fish species that undertake downstream spawning migrations to lower river reaches (e.g. red-tailed goby (Sicyopterus extraneus) (Herre 1960), ayu sweetfish (Plecoglossus altivelis) (Iguchi et al. 1998), ‘o’opu-nakea (Awaous stamineus) (Kido and Heacock 1991)), it appears to be a relatively rare strategy among the amphidromous fishes (McDowall 2010). A possible benefit of a downstream spawning migration to lower river reaches may be to facilitate successful transport of gametes to the sea, which is an obligatory component of the life cycle of Australian grayling (Crook et al. 2006). The downstream spawning migration by Australian grayling in the present study, to just upstream of the estuary, is not dissimilar to that undertaken by the sympatric common galaxias (Galaxias maculatus), a species considered ‘marginally catadromous’ (McDowall 1988). Common galaxias undertake a downstream spawning migration from the lower freshwater reaches to river estuaries, with spawning reported to occur in freshwater, just upstream of the salt wedge among tidally flooded vegetation (Benzie 1968; Mitchell 1994; Taylor 1996; Richardson and Taylor 2002). Hicks et al. (2010) suggested that the adult common galaxias may locate spawning habitat by migrating downstream until they reach saltwater, indicating they have reached the estuary and a tidally influenced habitat, and then select areas of low salinity to spawn. Whether the downstream extent of spawning migrations by the tagged Australian grayling was similarly linked to salinity is unclear; two tagged fish were detected within the upstream tidal limit of the estuary, six of the fish were potentially within the upstream tidal limit, whereas the other five fish that migrated downstream were detected only upstream of the tidal limit. Location and timing of spawning Eggs and larvae of Australian grayling were collected at multiple sites in the Bunyip River; however, most were collected at the most downstream site in the lower reaches near Koo Wee Rup. During the spawning period, electrical conductivity reached a maximum of 500 mS cm1 at this site, indicating that Australian grayling spawns in freshwater in the Bunyip River, with spawning activity concentrated in the lower freshwater reaches of the river. The finding that spawning activity was concentrated in the lower freshwater reaches of the Bunyip River contrasts with the suggestion by Berra (1982) that spawning occurs in the midreaches of the Tambo River. Our findings are consistent, however, with observations by Saville-Kent (1886a, 1886b) of Australian grayling spawning in the Derwent River close to the falls above New Norfolk in Tasmania; this section of the Derwent River represents the lower fresh water reaches of the river. Berra (1982) did not observe spawning, but inferred its occurrence from examination of fish gonads and observations of newly spent fish. The rapid, long-distance movements (i.e. up to 30 km) observed during the spawning period of the current study suggest that spent fish collected in one area (i.e. mid-reaches)


could have spawned elsewhere (i.e. lower reaches) and then returned upstream. This could potentially explain the difference between the observations of the current study and those of Berra (1982). The collection of small numbers of Australian grayling eggs and larvae further upstream in the Bunyip River indicates some flexibility in the spawning locality. Whether some Australian grayling also spawn in brackish waters as suggested by Lord and Scott (1924) cannot be confirmed by the current study because drift sampling was not conducted in brackish waters. However, some tagged fish were detected within the upstream tidal limit of the estuary during the spawning period, but only for short periods (i.e. ,1–3 days). Peaks in egg abundance from mid-April to mid-May are consistent with the suggestion by Berra (1984, 1987) that spawning peaks in late April to early May. The spawning period of Australian grayling has been described as short (about 2 weeks) and synchronised (Berra 1982, 1984). The downstream migrations of fish to the lower reaches of the Bunyip River and subsequent upstream migrations in the current study were synchronous, although most of the fish spent longer than 2 weeks in the lower reaches and eggs and larvae were also collected over a more extensive period. The timing of spawning in the current study also contrasts with suggestions that spawning takes place in February to April in Tasmania (Saville-Kent 1886b) and early February to early March in the Shoalhaven River in New South Wales (Bishop and Bell 1978). It is possible that the timing and duration of spawning varies depending on environmental conditions (e.g. river flow), as well as geographic (e.g. latitudinal differences in photoperiod) and physiological (e.g. fish condition) factors. In the current study, for instance, the timing of peak egg abundance in 2011 was mid–late April. This was ,2–3 weeks earlier than the previous years, which coincided with a large increase in flow earlier in the season (i.e. mid-April) compared with the previous 3 years (i.e. late April to mid-May). Australian grayling eggs are demersal and are thought to settle in the interstices of gravel, whereas the larvae are buoyant, positively phototropic and actively swim towards the water surface (Berra 1982; Bacher and O’Brien 1989). Bacher and O’Brien (1989) found that artificially fertilised Australian grayling eggs failed to develop normally in salinities .5 g L1 when transferred directly from freshwater. The collection of large numbers of eggs, rather than larvae, only a short distance from the sea in the current study was therefore unexpected. It is possible that high flows resulted in the downstream displacement of eggs. The majority of eggs were collected in early stages of development (i.e. eyes not yet developed) and it appears unlikely that all would have hatched before drifting into saline water downstream. Artificial breeding experiments have indicated that Australian grayling eggs take about 7 days to reach eye development and a further 14 days to hatch (Saville-Kent 1885), although faster hatch times (i.e. 8–12 days) have been reported (Allport 1870; Bacher and O’Brien 1989). Whether eggs could develop successfully in saltwater is unclear. Although Bacher and O’Brien (1989) found that eggs directly transferred among salinity treatments did not develop normally at high salinities, it is possible that the salinity tolerance of eggs differs in a natural environment where the exposure to salinity may be more gradual than direct transfer.


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Environmental correlations There was a clear association between increased flows and the commencement of downstream migration by Australian grayling, with all tagged individuals commencing migration during increases in flow between late March and late April. Fish did not commence migration during earlier increases in flow (e.g. early to mid-March), presumably because gonadal development does not commence until mid-March (Berra 1982, 1987). Water temperature during the times when fish commenced migration generally decreased by several degrees, although within a broad range. For fish that commenced migration earlier (e.g. early to mid-April), water temperature typically decreased from ,17–198C to 15–168C, whereas for fish that commenced migration later (e.g. late April), water temperature typically decreased from ,14–158C to 11–128C. Once downstream migration commenced, fish continued moving downstream on the rising and falling limb of the hydrograph, over a broad range of flows (50–160 ML day1). Fish that had not arrived at the lower reaches during high flows, however, ceased their migrations temporarily, and then recommenced migration on the next flow event. There was also an association between increased flows and spawning by Australian grayling, with peak egg abundances being collected in the Bunyip River shortly after increases in flow between mid-April and mid-May. Between 2008 and 2010, water temperatures during this period also decreased by several degrees, from ,15–188C to 10–138C. However, in 2011, water temperatures during the same period were higher and relatively stable (i.e. ,15–168C). This finding supports previous suggestions that spawning of Australian grayling is associated with increasing flows (Hall and Harrington 1989; O’Connor and Mahoney 2004) and suggests that a decrease in water temperature to ,12–138C (Berra 1982; Hall and Harrington 1989) is not crucial to spawning. The links between spawning migrations and flows have important implications for the development of environmentalflow recommendations aimed at restoring suitable flow patterns for Australian grayling in coastal rivers across south-eastern Australia. Environmental-flow recommendations for Australian grayling have focussed primarily on providing short-lived flow events to trigger spawning (SKM 2005; Earth Tech 2006), but not specifically for adult migration to spawning areas. The large distances often travelled (i.e. ,30 km) and the tendency of Australian grayling to cease downstream migration when discharge declines, suggest a need to provide flow events of sufficient magnitude and duration to allow adults to reach spawning areas. Non-migratory movements Australian grayling displayed little or no detectable movement before migrating downstream, and following downstream migration, most individuals returned upstream to the area they previously occupied, suggesting attachment to a precise locality during the non-migratory phase and homing behaviour. Restricted movement for extended periods before migration has been reported for other diadromous fish species (Baras et al. 1998; David and Closs 2002; Jellyman and Sykes 2003). Return movements to original locations following migration are widespread among freshwater fish species (Parkinson et al.

40


1999; Koehn et al. 2009), although documented examples among diadromous species appear uncommon (but see David and Closs 2002). Evidence of attachment to precise localities suggests that local-scale habitat modifications could lead to significant changes in the quality and availability of preferred habitats for Australian grayling, and homing behaviour highlights the importance of maintaining connectivity of habitats to allow fish to return to home areas. Conclusion The present study has provided significant new information about the movements and spawning of Australian grayling that is directly relevant to development of conservation strategies for the species. In particular, the study has demonstrated the existence of a downstream spawning migration and the importance of increased river flow as a migration cue. These findings highlight the potential impacts of in-stream barriers and altered flow regimes resulting from water-resource development and predicted climate change (Morrongiello et al. 2011) on Australian grayling reproduction in south-eastern Australia. Given the spatial and temporal patchiness in the occurrence and abundance of this rare and threatened species (Backhouse et al. 2008b), it is critical that amelioration of threats to the spawning migrations of the species is addressed over a broad spatial extent to ensure the long-term viability of the species. Acknowledgements Melbourne Water and the Department of Sustainability and Environment (DSE) funded this study. The assistance of D. Borg, R. Coleman, A. Lucas, L. Rose, E. Tsyrlin and J. Frame from Melbourne Water and P. Mitchell and S. Nicol from DSE is gratefully acknowledged. J. Macdonald, D. O’Mahony, F. Amtstaetter and L. Dodd assisted with the fieldwork. T. Raadik and J. O’Connor shared information through valuable discussions about the ecology of Australian grayling. Thanks go to J. O’Connor, J. Kearns, G. Quinn, R. Lester, T. Matthews, B. Ebner and an anonymous reviewer for constructive comments on earlier versions of the manuscript. Thanks go to J. Hughes and K. Real for coordinating and conducting the genetic analyses of eggs and larvae. This study was conducted under Victorian Flora and Fauna Guarantee Permit 10004353, Fisheries Victoria Research Permit RP-827 and ethics permit 07/20 and 08/04 (ARI Animal Ethics Committee).

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