Project number: 2016-068
Project Status:
Completed
Budget expenditure: $421,129.00
Principal Investigator: Jeremy Lyle
Organisation: University of Tasmania (UTAS)
Project start/end date: 31 Mar 2017 - 30 Jul 2020
Contact:
FRDC
SPECIES

Need

The physio-chemical conditions in Macquarie Harbour have changed markedly since European settlement and the general decline in DO since 2009, which occurred at the same time as the rapid expansion of marine farming operations, is likely to have had a significant impact on many resident species, including the endangered Maugean Skate. Given the species poor ability to cope with low DO, any reductions in bottom DO concentrations are expected to directly influence the distribution of the skate, highlighting the need to better understand the oxygen demands of the species. Current generation acoustic tags capable of measuring DO and activity in the field, which when combined with laboratory studies, represent methods to examine tolerance and responses to varying levels of DO. Bottom DO also has implications for the development and survival of skate eggs. Limited information suggests that eggs are deposited at depths of > 20 m where they are likely to be increasingly exposed to low DO concentrations. An understanding of the relationships between environmental conditions and the development and survival of embryos, coupled with the depths in which eggs are deposited, has particular relevance to assessing the implications of changing environmental conditions on future recruitment and productivity of the Maugean Skate population.

Furthermore, the ability to monitor the status of this population, especially given the rate and extent of recent environmental changes in Macquarie Harbour is critical to assess its future viability. Tracking size composition, including data from previous studies, has the potential to provide a baseline against which reduced recruitment (if linked to the changed environmental conditions) could be detected.

The maintenance of best environmental practices by the aquaculture industry supported by effective monitoring and environmental management policies represent essential requirements if industry and Maugean Skate populations are to coexist.

Objectives

1. Determine the distribution of Maugean skate eggs within Macquarie Harbour, with particular reference to depth and bottom DO.
2. Examine the relationship between environmental conditions and survival and viability of Maugean skate eggs.
3. Determine what DO levels Maugean skate experience in Macquarie Harbour, particularly when in deeper waters.
4. Determine the physiological costs of the DO levels Maugean skate are exposed to in Macquarie Harbour.
5. Assess the potential of using the size composition of Maugean Skate catches as an indicator of population change, in particular recruitment variability
6. Assess the implications of declining DO concentrations in Macquarie Harbour on the future viability of the Maugean Skate population.

Final report

ISBN: 978-1-922352-39-2
Authors: David Moreno Jeremy Lyle Jayson Semmens Andrea Morash Kilian Stehfest Jaime McAllister Bailee Bowen and Neville Barrett
Final Report • 2020-10-01 • 3.41 MB
2016-068-DLD.pdf

Summary

Maugean Skate (Zearaja maugeana) are only known from two isolated estuarine systems located on the west coast of Tasmania, representing one of most restricted distributions of any elasmobranch. There is, however, uncertainty about the continued persistence of the species in one of these estuaries (Bathurst Harbour), suggesting that Macquarie Harbour may now represent the sole remaining habitat for the species.  The species is listed as Endangered under the Threatened Species Protection Act (Tas) and the Environmental Protection and Biodiversity Conservation Act (Comm) and, apart from protected status, is without a recovery plan or management strategy. 
The physicochemical conditions in Macquarie Harbour have changed markedly since European settlement, influenced by anthropogenic activities in and around the estuary (e.g. mining, forestry, hydro-electricity generation, and marine farming operations) as well as the more general effects of climate change.  Of recent concern, has been a marked decline in dissolved oxygen (DO) conditions in Macquarie Harbour which are likely to have a significant impact on many resident species, including the Maugean Skate.  In the absence of population dispersal or mixing outside of Macquarie Harbour, any longer-term changes to DO conditions in the harbour are likely to result in changes to ecological assemblages inhabiting this unique estuarine system. The current study describes the vulnerability of the Maugean Skate, across all its life history stages, to a range of environmental stressors. The ability to monitor population status and population responses of the Maugean Skate to any changes in environmental conditions will be critical in assessing the need for further conservation management action. 
Objectives
The primary aim of this study is to establish the mechanistic links between the environmental conditions experienced by the Maugean Skate across multiple life stages and the implications of the changing environment in Macquarie Harbour.  Specific objectives include:
  1. Determine the distribution of Maugean Skate eggs within Macquarie Harbour, with particular reference to depth and bottom DO.
  2. Examine the relationship between environmental conditions and survival and viability of Maugean Skate eggs. 
  3. Determine what DO levels Maugean Skate experience in Macquarie Harbour, particularly when in deeper waters.
  4. Determine the physiological costs of the DO levels Maugean Skate are exposed to in Macquarie Harbour.
  5. Assess the potential of using the size composition of Maugean Skate catches as an indicator of population change, in particular recruitment variability
  6. Assess the implications of declining DO concentrations in Macquarie Harbour on the future viability of the Maugean Skate population.
Methodology
The study comprised five main components: (1) systematic field surveys of skate egg distribution, (2) laboratory study of embryo development; (3) field assessment of skate behaviour in relation to environmental conditions; (4) laboratory assessment of physiological responses to conditions experienced in the wild; and (5) fishery-independent surveys to examine the potential to inform on changes to population status.

A combination of beam trawl and dive surveys was employed to sample for Maugean Skate egg cases in areas of known high skate abundance.  Egg capsules collected in the field were reared in the laboratory to describe embryonic development and gestation period.  Acoustic telemetry was used to examine links between environmental conditions (i.e. dissolved oxygen and temperature) and the distribution, movement and habitat use of the Maugean Skate within Macquarie Harbour. An acoustic array comprising 52 acoustic receivers was deployed in the Table Head/Liberty Point region of Macquarie Harbour and 25 adult Maugean Skate were externally tagged with multi-sensor acoustic tags capable of continuously transmitting information on the depth, temperature and dissolved oxygen concentrations experienced by the individuals over a 12-month period. Physiological trials were conducted in a purpose-designed field laboratory to examine physiological responses to low DO and low salinity exposure, replicating environmental conditions experienced by the skate in Macquarie Harbour.  Gillnet surveys were undertaken to extend the time series of Maugean Skate size composition data and evaluate its potential as an indicator of changing population status.  

Key findings
Maugean Skate eggs were found across a wide range of depths (2.5 - 33 m) but appear to be most abundant in relatively shallow sites (< 10 m). Based on an analysis of the condition of egg-capsules, hatching success was estimated to be about 40%, which is comparable to success rates reported for other temperate skate species.  An egg reared under laboratory conditions hatched 31 weeks (~ seven months) after oviposition.  Respiratory channels opened after 15 weeks, exposing the embryo to external environmental conditions for over half of the gestation period.  These findings indicate that, depending on the depths at which eggs are deposited in the wild, embryos will experience a range of dissolved oxygen, salinity and temperature conditions, reflective of localised fluctuations in environmental conditions.  The implications of these varying conditions for development and survival are unknown.

This study represents the first use of animal-borne acoustic sensors to monitor long-term dissolved oxygen conditions experienced by a coastal elasmobranch and the links with behaviour. The results showed that skate are subject to wide ranging fluctuations in water chemistry. For instance oxygen levels experienced ranged from normoxic (50-100%), hypoxic (20-50%) and to near anoxic (~0-20%), with individuals often experiencing substantial variation (as high as > 90%) in the range of DO levels within the same day.
Adult Maugean Skate exhibited a high level of site selectivity and site fidelity across a relatively small spatial extent and with a strong preference to depths between 7.5 and 12.5 m. Despite individual variation in long-term residency, noting that several individuals appeared to permanently exit the study area, the tagged skate showed a clear preference towards the Table Head and Liberty Point areas. Furthermore, home ranges calculated using continuous time movement models showed a high degree of spatial overlap in the core home ranges (50% utilisation distribution, UD) of each of the individuals.  Their extended activity areas (95% UD) did, however, change throughout the year corresponding to variation in environmental conditions.  For instance, a sharp increase in surface water temperature and declines in mid- and deep water dissolved oxygen levels during summer resulted in all detected individuals spending time at shallow depths before returning to their preferred depths. While the shallow sites provided access to improved oxygen conditions, higher temperatures and exposure to hyposaline conditions will place an increased metabolic demand on individuals, potentially driving them to continuously move back into deeper waters where temperature and salinity conditions are more stable.  A large storm surge and subsequent oxygen recharge in March/April 2019 resulted in all tracked individuals expanding their extended activity areas considerably, including movement into deeper waters, while still maintaining a strong attachment to their core areas.
The present study shows that there is an intricate link between movement of the Maugean Skate and environmental conditions in Macquarie Harbour. The species appear to behaviourally modulate environmental stressors through movement, likely balancing optimal habitat requirements against the energetic cost of chronic hypoxia in deeper waters and increased thermal and osmoregulatory stress at shallow sites. Such behavioural plasticity may constitute a key adaptation that to date has enabled the species to tolerate such a challenging environment that Macquarie Harbour represents.  However, since individuals continued to utilise the same core UD and preferential depth range, despite these areas being subject to the largest daily fluctuations in water chemistry conditions experienced by the skate, this behavioural plasticity appears to be limited to their extended use areas. Therefore, the site attached behaviour of the skate suggest that these core sites likely provide an advantage that outweighs the cost of exposure to unfavourable environmental conditions, such as access to prey that may not be as readily available elsewhere within the estuary. 
Physiological experiments demonstrated that adult Maugean Skate are quite capable of surviving chronic exposure to hypoxic conditions (< 20% DO) by using metabolic depression as a survival strategy. Metabolic depression does, however, occur at the cost of other energy intensive life history processes, such as growth, foraging and reproduction.  As such, metabolic depression cannot be sustained long-term, and as a result skate may seek oxygen in the shallower waters of the harbour where they will encounter hyposaline conditions.  Maugean Skate are unusual in that they are the only known species of skate to live exclusively in a euryhaline environment (areas with a wide range of salinities) and, based on the range of depths utilised, are constantly exposed to a wide range of salinities.  Routine metabolic rate appeared to be higher following acclimation to hyposaline conditions, although the corresponding statistical test only showed near-significance.  Since individuals appear to utilise shallow areas as a DO refuge during the summer months, they will also be exposed to higher temperatures which in turn will result in further metabolic stress. 
Physiological data based on a single individual suggests that neonates are oxyconformers (rate of oxygen consumption dependent on environmental DO), implying that even at an early age, Maugean Skate may be able to tolerate short-term hypoxic events through an increased reliance on anaerobic metabolism. The point below which oxygen uptake became negligible in the neonate was higher (~ 66% DO) compared with adults (10-25% DO), implying a lower tolerance threshold which could have important implications for survivorship of early life stages, especially in relation to the range of environmental conditions experienced in Macquarie Harbour.
During this study, an unexpectedly high proportion of tagged individuals died.  Although causality cannot be established, the timing of these events suggest that the mortalities were unlikely to have been a direct consequence of tagging.  Most mortalities (8 out of 11) were clustered in two discrete periods that corresponded with marked changes in environmental conditions within the core habitat used by the skate. In addition, behavioural changes (based on change point analysis) were observed at the same time in virtually all surviving individuals.  It is feasible, therefore, that the deaths may have been related to stress caused (directly or indirectly) by the significant changes in the environmental conditions of the harbour. If this is the case, then recent changes in the environmental health of the harbour (especially dissolved oxygen levels), coupled with the consequences of climate change (including occurrence of extreme weather events), may already be challenging the skate’s capacity to cope with the environmental conditions in Macquarie Harbour.
Deriving an estimate of the effective population size of the Maugean Skate in Macquarie Harbour has proven challenging and there is a high degree of uncertainty associated with current estimates that limit their applicability in monitoring the continuing status of the population. An analysis of research gillnet data collected since 2012 suggests a reduction in the relative abundance of juvenile and sub-adult individuals and as well as an increase in the size of the larger individuals (adults) in the catches through time.  Despite uncertainty as to the significance of the size composition data in terms of representing trends in population status, a recent decline in recruitment, possibly due lower hatching success or juvenile survival, coupled with adult growth represent plausible scenarios that could produce the changes observed.  
Implications
This study provides a greater understanding of the ecology and life history of the Maugean Skate and describes for the first time some of the behavioural and physiological adaptations that have enabled the species to survive in such a unique and challenging environment as Macquarie Harbour. Our results suggest that the species can mitigate some environment variability by a combination of behavioural (movement) responses and physiological capability.  However, the vulnerability of early life stages to the changing environmental conditions, long-term changes in the size structure of the population, and the mortality of some tagged individuals following significant environmental events collectively highlight the vulnerability of the Maugean Skate in Macquarie Harbour and the need to consider further conservation action to support the persistence of this unique micro-endemic skate. 
In addition to addressing uncertainties around the apparent changes in the size (and age) structure of the population through further research fishing, there is an urgent need to investigate cost-effective and non-invasive approaches to estimate population size and mortality rates, which can be applied to track population status and health over time.  Importantly, managing the known anthropogenic impacts on the environmental health of Macquarie Harbour, both in terms water column and benthic conditions, will ultimately prove crucial to the success of any conservation strategy for the Maugean Skate. A multi-stakeholder and holistic environmental management approach for Macquarie Harbour should be considered as part of this strategy.

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