Does life history mediate discharge as a driver of multi-decadal changes in populations of freshwater fish?

Understanding how and why the size of populations varies is critical knowledge for conservation and management. While considerable work has explored how different demographic parameters affect population growth, less is known the drivers of variability in these parameters. Long-term time series tracking population size that are coupled with empirical data to examine the relative importance of different drivers are rare, especially in freshwater systems. Even rarer are studies that collect this information concurrently from multiple species with contrasting life history strategies in the same system to assess whether population size and the relative importance of drivers also vary. We studied changes in the abundance and size structure of four native freshwater fish species in the Murray River, southeastern Australia, over a continuous 19-yr period. Two species with traits typical of "equilibrium" species (Murray cod Maccullochella peelii and trout cod Maccullochella macquariensis) and two with traits of "periodic" species (golden perch Macquaria ambigua and silver perch Bidyanus bidyanus) were sampled annually and capture-mark-recapture modeling was used to ask (1) how did population size change during this period, (2) how were changes in population size related to variability in hydrology, and (3) how were changes in population size driven by different processes (local recruitment or migration events)? Populations of all four species varied throughout the study, and our results are consistent with the notion that local recruitment is an important driver of this variability for Murray cod and trout cod, whereas immigration is more important for the two other species. Increases in spring river discharge strongly influenced these responses for trout cod and golden perch. Our study provides fundamental insights into the population dynamics of these valued species, and how management strategies might differ based on their life histories. Management should focus on allowing connectivity for golden and silver perch, and on promoting local scale recruitment and survival for Murray cod and trout cod. More generally, our study highlights the importance of understanding the processes underpinning population persistence, how these processes may vary for different species, and ultimately how this knowledge can inform targeted management actions.

Increased population size of fish in a lowland river following restoration of structural habitat.

Most assessments of the effectiveness of river restoration are done at small spatial scales (<10 km) over short time frames (less than three years), potentially failing to capture large-scale mechanisms such as completion of life-history processes, changes to system productivity, or time lags of ecosystem responses. To test the hypothesis that populations of two species of large-bodied, piscivorous, native fishes would increase in response to large-scale structural habitat restoration (reintroduction of 4,450 pieces of coarse woody habitat into a 110-km reach of the Murray River, southeastern Australia), we collected annual catch, effort, length, and tagging data over seven years for Murray cod (Maccullochella peelii) and golden perch (Macquaria ambigua) in a restored "intervention" reach and three neighboring "control" reaches. We supplemented mark-recapture data with telemetry and angler phone-in data to assess the potentially confounding influences of movement among sampled populations, heterogeneous detection rates, and population vital rates. We applied a Bayesian hierarchical model to estimate changes in population parameters including immigration, emigration, and mortality rates. For Murray cod, we observed a threefold increase in abundance in the population within the intervention reach, while populations declined or fluctuated within the control reaches. Golden perch densities also increased twofold in the intervention reach. Our results indicate that restoring habitat heterogeneity by adding coarse woody habitats can increase the abundance of fish at a population scale in a large, lowland river. Successful restoration of poor-quality "sink" habitats for target species relies on connectivity with high-quality "source" habitats. We recommend that the analysis of restoration success across appropriately large spatial and temporal scales can help identify mechanisms and success rates of other restoration strategies such as restoring fish passage or delivering water for environmental outcomes.

Spawning-stock characteristics and migration of a lake-bound population of the endangered Macquarie perch Macquaria australasica.

The intrapopulation variability in the size and age structure of the spawning stock and migration of the threatened Macquarie perch Macquaria australasica in Lake Dartmouth was investigated between 2008 and 2016. Sampling centred on the core reproductive period (October-December) when mature fish migrate from the lake into riverine habitat to spawn. Spawning fish were predominantly large, spanning a broad age structure, with a high proportion of fish (25%) aged 15-30 years. The overall median size of spawning fish did not change for males or females during the 9 year study period. The size of the smaller mature male fish did change in some years suggesting a small proportion of male M. australasica matured at age 1+ and 2+. Acoustic telemetry employed over 3 years showed that M. australasica were most likely to be in the spawning reach from October to mid-December, migrated to this reach annually and moved large distances throughout the lake all year, with no evidence for any spatial structuring. Mature fish sometimes occupied the spawning reach for several months after the core reproductive period, which increased their vulnerability to recreational fishing. Males tagged in the lake were seldom recorded in the spawning reach, presumably because a high proportion had not yet entered the spawning stock despite their size suggesting maturity. Maintaining a broad age and size-structure of the spawning stock of long-lived iteroparous fish species is crucial for recruitment stability and population persistence. Overexploitation of the spawning stock has probably contributed to previous population declines in the lake as well as the collapse of other M. australasica populations in south-eastern Australia.

Signatures of polygenic adaptation associated with climate across the range of a threatened fish species with high genetic connectivity.

Adaptive differences across species' ranges can have important implications for population persistence and conservation management decisions. Despite advances in genomic technologies, detecting adaptive variation in natural populations remains challenging. Key challenges in gene-environment association studies involve distinguishing the effects of drift from those of selection and identifying subtle signatures of polygenic adaptation. We used paired-end restriction site-associated DNA sequencing data (6,605 biallelic single nucleotide polymorphisms; SNPs) to examine population structure and test for signatures of adaptation across the geographic range of an iconic Australian endemic freshwater fish species, the Murray cod Maccullochella peelii. Two univariate gene-association methods identified 61 genomic regions associated with climate variation. We also tested for subtle signatures of polygenic adaptation using a multivariate method (redundancy analysis; RDA). The RDA analysis suggested that climate (temperature- and precipitation-related variables) and geography had similar magnitudes of effect in shaping the distribution of SNP genotypes across the sampled range of Murray cod. Although there was poor agreement among the candidate SNPs identified by the univariate methods, the top 5% of SNPs contributing to significant RDA axes included 67% of the SNPs identified by univariate methods. We discuss the potential implications of our findings for the management of Murray cod and other species generally, particularly in relation to informing conservation actions such as translocations to improve evolutionary resilience of natural populations. Our results highlight the value of using a combination of different approaches, including polygenic methods, when testing for signatures of adaptation in landscape genomic studies.

A novel approach to spatially assessing instream woody habitat densities across large areas.

Fish habitat restoration efforts frequently involve the reintroduction of instream woody habitat (IWH) in areas where large scale removal has taken place over time. Identifying areas of low IWH density for reintroduction requires a 'current state' spatial representation of the IWH densities that is traditionally a labour intensive and costly exercise. We present a meso-macro scale assessment procedure that incorporates a rapid on-ground field survey method with a novel analytical approach to map IWH densities. In situ IWH locations with categorical values for size and complexity were obtained along the lower Ovens River in South Eastern Australia. Despite relatively high densities of IWH and limited access, 120 km of river was able to be investigated. A bound kernel density estimate (BKDE) analysis was performed using the IWH point locations, weighted by an average volume inferred from the point size and complexity values. A fine scale map is obtained providing a continuous representation of IWH densities (m(3) m(-2)) indicating a high degree of IWH density variability along the river. The relative high resolution map is produced for habitat restoration managers to assess river sections generally less than 1 km long for IWH reintroduction.

First tracking of the oceanic spawning migrations of Australasian short-finned eels (Anguilla australis).

Anguillid eel populations have declined dramatically over the last 50 years in many regions of the world, and numerous species are now under threat. A critical life-history phase is migration from freshwater to distant oceans, culminating in a single life-time spawning event. For many anguillids, especially those in the southern hemisphere, mystery still shrouds their oceanic spawning migrations. We investigated the oceanic spawning migrations of the Australasian short-finned eel (Anguilla australis) using pop-up satellite archival tags. Eels were collected from river estuaries (38° S, 142° E) in south-eastern temperate Australia. In 2019, 16 eels were tracked for up to about 5 months, ~ 2620 km from release, and as far north as the tropical Coral Sea (22° S, 155° E) off the north-east coast of Australia. Eels from southern Australia appeared to access deep water off the Australian coast via two main routes: (i) directly east via Bass Strait, or (ii) south-east around Tasmania, which is the shortest route to deep water. Tagged eels exhibited strong diel vertical migrations, alternating between the warm euphotic zone (~ 100-300 m, 15-20 °C) at night and the mesopelagic zone (~ 700-900 m, 6-8 °C) during the day. Marine predators, probably lamnid sharks, tuna, or marine mammals, ended many eel migrations (at least ~ 30%), largely before the eels had left the Australian continental shelf. The long and risky marine migrations of Australasian eels highlight the need for better information on the processes contributing to eel mortality throughout the life cycle, including the impacts of future changes to oceanic currents, predator abundance and direct anthropogenic disturbances.

Using multiple sources during reintroduction of a locally extinct population benefits survival and reproduction of an endangered freshwater fish.

Through using different sources, population reintroductions can create genetically diverse populations at low risk of harmful inbreeding and well equipped for adaptation to future environments. Genetic variation from one source can mask locally nonoptimal alleles from another, thereby enhancing adaptive potential and population persistence. We assessed the outcomes in survival, growth and reproduction of using two differentiated sources (genetically diverse Yarra and moderately diverse Dartmouth) for translocations and stocking to reintroduce the endangered Australian freshwater Macquarie perch Macquaria australasica into the Ovens River. For stocking, same- and different-population parents ("cross-types") were used during hatchery production. Genetic samples and data on individual fish were collected over three years of monitoring the Ovens. We genetically assigned Ovens fish to their broodstock parents and tested whether cross-type and genetic dissimilarity between parents are associated with offspring survival, and whether cross-type and parental dissimilarity or individual genetic diversity are associated with somatic growth rates of stocked fish. We genetically identified translocated fish and assessed local recruit ancestry. Of 296 Ovens fish, 31.1% were inferred to be stocked, 1.3% translocated and 67.6% locally born. Cross-type strongly predicted survival of stocked offspring: those with two Yarra parents had the highest survival, followed by offspring with two-population, then Dartmouth, ancestry. Of the Ovens recruits, 59.5% had Yarra, 33.5% two-population and 7.0% Dartmouth ancestry, despite 67% of stocked and 98% of translocated fish originating from Dartmouth. Offspring with two Yarra parents grew faster than offspring of Dartmouth or two-population ancestry. Although Dartmouth fish appear to be less fit in the Ovens compared to Yarra fish, possibly due to deleterious variation or genetic or plastic maladaptation, they contribute to the reintroduced population through local interbreeding with Yarra fish and relatively high survival of stocked offspring of two-population ancestry. Thus, combining compatible stocks is likely to benefit restoration of other wildlife populations.

Linking flow attributes to recruitment to inform water management for an Australian freshwater fish with an equilibrium life-history strategy.

Recognition that many species share key life-history strategies has enabled predictions of responses to habitat degradation or rehabilitation by these species groups. While such responses have been well documented for freshwater fish that exhibit 'periodic' and 'opportunistic' life-history strategies, this is rare for 'equilibrium' life-history, due largely to their longevity and by comparison, more regular and stable levels of recruitment. Unfortunately, this limits the confidence in using life-history strategies to refine water management interventions to rectify the negative impacts of river regulation for these species. We addressed this knowledge gap for Murray cod Maccullochella peelii, a high-profile, long-lived recreationally popular equilibrium species in south-eastern Australia. We used monitoring data collected across a gradient of hydrologically altered rivers over two decades, to test various hypotheses linking recruitment strength with key attributes of the flow regime. Although Murray cod recruited in most years, as expected for an equilibrium species, responses to flow varied among and within rivers among years. We found links between recruitment strength and the magnitude and variation in discharge during the spring spawning period, as well as flows experienced by juvenile fish during summer and winter - the hydrological components most affected by river regulation. However, the specific slopes and directions of some of these links varied idiosyncratically across rivers. Our results emphasise the importance of accounting for flows that influence each of the key life stages during the recruitment process and lend support for managing rivers in accordance with the natural flow regime. It also shows the need for waterway-specific studies and further refinement of existing flow metrics to allow more credible transferability of results. The approach used in this study can also be applied to other species sharing life-history strategies for which long-term monitoring data has been compiled and length-at-age relationships established.

Combining capture-recapture data and known ages allows estimation of age-dependent survival rates.

In many animal populations, demographic parameters such as survival and recruitment vary markedly with age, as do parameters related to sampling, such as capture probability. Failing to account for such variation can result in biased estimates of population-level rates. However, estimating age-dependent survival rates can be challenging because ages of individuals are rarely known unless tagging is done at birth. For many species, it is possible to infer age based on size. In capture-recapture studies of such species, it is possible to use a growth model to infer the age at first capture of individuals. We show how to build estimates of age-dependent survival into a capture-mark-recapture model based on data obtained in a capture-recapture study. We first show how estimates of age based on length increments closely match those based on definitive aging methods. In simulated analyses, we show that both individual ages and age-dependent survival rates estimated from simulated data closely match true values. With our approach, we are able to estimate the age-specific apparent survival rates of Murray and trout cod in the Murray River, Australia. Our model structure provides a flexible framework within which to investigate various aspects of how survival varies with age and will have extensions within a wide range of ecological studies of animals where age can be estimated based on size.

Severe consequences of habitat fragmentation on genetic diversity of an endangered Australian freshwater fish: A call for assisted gene flow.

Genetic diversity underpins the ability of populations to persist and adapt to environmental changes. Substantial empirical data show that genetic diversity rapidly deteriorates in small and isolated populations due to genetic drift, leading to reduction in adaptive potential and fitness and increase in inbreeding. Assisted gene flow (e.g. via translocations) can reverse these trends, but lack of data on fitness loss and fear of impairing population "uniqueness" often prevents managers from acting. Here, we use population genetic and riverscape genetic analyses and simulations to explore the consequences of extensive habitat loss and fragmentation on population genetic diversity and future population trajectories of an endangered Australian freshwater fish, Macquarie perch Macquaria australasica. Using guidelines to assess the risk of outbreeding depression under admixture, we develop recommendations for population management, identify populations requiring genetic rescue and/or genetic restoration and potential donor sources. We found that most remaining populations of Macquarie perch have low genetic diversity, and effective population sizes below the threshold required to retain adaptive potential. Our simulations showed that under management inaction, smaller populations of Macquarie perch will face inbreeding depression within a few decades, but regular small-scale translocations will rapidly rescue populations from inbreeding depression and increase adaptive potential through genetic restoration. Despite the lack of data on fitness loss, based on our genetic data for Macquarie perch populations, simulations and empirical results from other systems, we recommend regular and frequent translocations among remnant populations within catchments. These translocations will emulate the effect of historical gene flow and improve population persistence through decrease in demographic and genetic stochasticity. Increasing population genetic connectivity within each catchment will help to maintain large effective population sizes and maximize species adaptive potential. The approach proposed here could be readily applicable to genetic management of other threatened species to improve their adaptive potential.