Hamish A. Malcolm

Global warming and recurrent mass bleaching of corals

During 2015–2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp

Significance Most studies of the impact of global warming focus on the direct physiological impacts of climate change. However, global warming is shifting the distribution of many species and leading to novel interactions between previously separated species that have the potential to transform entire ecological communities. This study shows that an increase in the proportion of warmwater species (“tropicalization”) as oceans warm is increasing fish herbivory in kelp forests, contributing to their decline and subsequent persistence in alternate “kelp-free” states. These tropical and subtropical herbivores are increasingly impacting temperate algal communities worldwide, posing a significant threat to the long-term stability of these iconic ecosystems and the valuable services they provide. Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical–temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.

Connectivity within and among a Network of Temperate Marine Reserves

Networks of marine reserves are increasingly being promoted as a means of conserving marine biodiversity. One consideration in designing systems of marine reserves is the maintenance of connectivity to ensure the long-term persistence and resilience of populations. Knowledge of connectivity, however, is frequently lacking during marine reserve design and establishment. We characterise patterns of genetic connectivity of 3 key species of habitat-forming macroalgae across an established network of temperate marine reserves on the east coast of Australia and the implications for adaptive management and marine reserve design. Connectivity varied greatly among species. Connectivity was high for the subtidal macroalgae Ecklonia radiata and Phyllospora comosa and neither species showed any clear patterns of genetic structuring with geographic distance within or among marine parks. In contrast, connectivity was low for the intertidal, Hormosira banksii, and there was a strong pattern of isolation by distance. Coastal topography and latitude influenced small scale patterns of genetic structure. These results suggest that some species are well served by the current system of marine reserves in place along this temperate coast but it may be warranted to revisit protection of intertidal habitats to ensure the long-term persistence of important habitat-forming macroalgae. Adaptively managing marine reserve design to maintain connectivity may ensure the long-term persistence and resilience of marine habitats and the biodiversity they support.

Effects of reef proximity on the structure of fish assemblages of unconsolidated substrata.

Fish assemblages of unconsolidated sedimentary habitats on continental shelves are poorly described when compared to those of hard substrata. This lack of data restricts the objective management of these extensive benthic habitats. In the context of protecting representative areas of all community types, one important question is the nature of the transition from reefal to sedimentary fish assemblages. We addressed this question using Baited Remote Underwater Videos (BRUVs) to assess fish assemblages of sedimentary habitats at six distances from rocky reefs (0, 25, 50, 100, 200, and 400 m) at four sites in subtropical eastern Australia. Distance from reef was important in determining fish assemblage structure, and there was no overlap between reef sites and sedimentary sites 400 m from reef. While there was a gradient in assemblage structure at intermediate distances, this was not consistent across sites. All sites, however, supported a mixed ‘halo’ assemblage comprising both reef and sediment species at sampling stations close to reef. BRUVs used in conjunction with high-resolution bathymetric and backscatter spatial data can resolve differences in assemblage structure at small spatial scales (10s to 100s of metres), and has further application in unconsolidated habitats. Unless a ‘reef halo’ assemblage is being examined, a minimum of 200 m but preferably 400 m distance from any hard substrate is recommended when designing broader-scale assessments of fish assemblages of sedimentary habitats.

Habitat structural complexity metrics improve predictions of fish abundance and distribution

Habitat structural complexity influences biotic diversity and abundance, but its influence on marine ecosystems has not been widely addressed. Recent advances in computer vision and robotics allow quantification of structural complexity at higher-resolutions than previously achieved. This provides an important opportunity to determine the ecological role of habitat structural complexity in marine ecosystems. We used high-resolution three-dimensional (3D) maps to test multiple structural complexity metrics, depth and benthic biota as surrogates of fish assemblages across hundreds of meters on subtropical reefs. Non-parametric multivariate statistics were used to determine the relationship between these surrogates and the entire fish assemblage. Fish were divided into functional groups, which were used to further investigate the relationship between surrogates and fish abundance using generalized linear models. Fish community composition and abundance were strongly related to habitat complexity metrics, benthic biota and depth. Surface rugosity and its variance had a significant positive influence on the abundance of piscivores and sediment infauna predators, and a negative effect on the abundance of predators, herbivores, planktivores and cleaners. Final models for fish functional groups explained up to 68% of the variance. The best metrics to explain the variance in fish abundance were benthic biota (25 7.5% of variance explained, mean  SE) and complexity metrics (16 6.6%, mean  SE). Our results show that high-resolution 3D maps and derived metrics can predict a large percentage of variance in fish abundance and potentially serve as useful surrogates of fish abundance across all functional groups in spatially dynamic reefs.

Integrating Seafloor Habitat Mapping and Fish Assemblage Patterns Improves Spatial Management Planning in a Marine Park

ABSTRACT Malcolm, H.A., Jordan, A., Schultz, A.L., Smith, S.D.A., Ingleton, T., Foulsham, E., Linklater, M., Davies, P., Ferrari, R., Hill, N., and Lucieer, V., 2016. Integrating seafloor habitat mapping and fish assemblage patterns improves spatial management planning in a marine park. In: Vila-Concejo, A.; Bruce, E.; Kennedy, D.M., and McCarroll, R.J. (eds.), Proceedings of the 14th International Coastal Symposium (Sydney, Australia). Journal of Coastal Research, Special Issue, No. 75, pp. 1292 - 1296. Coconut Creek (Florida), ISSN 0749-0208. Marine Protected Areas (MPAs) are important spatial mechanisms for managing human activities, if effectively planned. The Solitary Islands Marine Park (SIMP), covering 720 km2 of coastal waters in New South Wales, Australia, includes reef and unconsolidated habitats up to 17 km from shore and 75 m depth. When established in 1991, there was limited knowledge of biotic patterns, seafloor habitats and habitat-biotic relationships in the multiple-use SIMP, which constrained effective conservation planning. Subsequent mapping of sub-tidal habitats from aerial photography and single-beam acoustics improved habitat representation following rezoning in 2002 using Comprehensive, Adequate, Representative (CAR) principles and assisted site selection for diver surveys of fishes, a key surrogate taxon. In 2006, a swath acoustic mapping program commenced, which mapped ~35% of the MPA. This has produced high-resolution data on seafloor habitats, including depths >50 m. Bathymetry and backscatter layers have facilitated targeted deployment of Baited Remote Underwater Video (BRUV) to test hypotheses about associations between fishes and physical habitat characteristics. Strong and persistent patterns in fish assemblage composition in relation to particular habitat characteristics provided the basis for a Habitat Classification Scheme (HCS) to be refined with the following categories: substratum (consolidated, unconsolidated), cross-shelf position (inshore, mid, offshore) and depth (shallow, intermediate, deep). Further refinement of unconsolidated substratum into gravel and sand habitats, which were mapped using backscatter layers, improves this classification. The HCS, which integrates habitat and biotic patterns, greatly increases the potential for effective spatial management planning in the SIMP when used with spatial planning tools (e.g. Marxan).

Surviving under pressure and protection: a review of the biology, ecology and population status of the highly vulnerable grouper Epinephelus daemelii

Epinephelus daemelii is a threatened serranid grouper species that is restricted to the south-western Pacific Ocean, ranging from eastern Australia to northern New Zealand and the Kermadec Islands. Declines in its abundance due to fishing pressure were reported as early as 1916. Aspects of this species’ biology and behaviour that make it vulnerable include its longevity, late age at maturity, protogynous hermaphroditism, territoriality and limited shallow reef habitat. Adults prefer complex habitat with caves and overhangs at depths of less than 50m, whereas juveniles live in rock pools, shallow intertidal reefs and estuaries. Epinephelus daemelii lives at least 65 years and reaches 170-cm total length. Individuals change sex from female to male at ~100–110cm and ~25 years. Absence of large (>100cm) fish across a large part of their range has implications for reproduction. Although nearly fully protected, incidental bycatch still occurs. A lack of long-term data hinders determination of population status, but abundance appears to be much lower than before, except in remote regions (Kermadec Islands, Elizabeth and Middleton reefs) with extensive no-fishing areas. Further prohibitions on fishing in key locations are likely to be important for the recovery and long-term survival of this species.

Large-scale assessment of benthic communities across multiple marine protected areas using an autonomous underwater vehicle

Marine protected areas (MPAs) are designed to reduce threats to biodiversity and ecosystem functioning from anthropogenic activities. Assessment of MPAs effectiveness requires synchronous sampling of protected and non-protected areas at multiple spatial and temporal scales. We used an autonomous underwater vehicle to map benthic communities in replicate ‘no-take’ and ‘general-use’ (fishing allowed) zones within three MPAs along 7o of latitude. We recorded 92 taxa and 38 morpho-groups across three large MPAs. We found that important habitat-forming biota (e.g. massive sponges) were more prevalent and abundant in no-take zones, while short ephemeral algae were more abundant in general-use zones, suggesting potential short-term effects of zoning (5–10 years). Yet, short-term effects of zoning were not detected at the community level (community structure or composition), while community structure varied significantly among MPAs. We conclude that by allowing rapid, simultaneous assessments at multiple spatial scales, autonomous underwater vehicles are useful to document changes in marine communities and identify adequate scales to manage them. This study advanced knowledge of marine benthic communities and their conservation in three ways. First, we quantified benthic biodiversity and abundance, generating the first baseline of these benthic communities against which the effectiveness of three large MPAs can be assessed. Second, we identified the taxonomic resolution necessary to assess both short and long-term effects of MPAs, concluding that coarse taxonomic resolution is sufficient given that analyses of community structure at different taxonomic levels were generally consistent. Yet, observed differences were taxa-specific and may have not been evident using our broader taxonomic classifications, a classification of mid to high taxonomic resolution may be necessary to determine zoning effects on key taxa. Third, we provide an example of statistical analyses and sampling design that once temporal sampling is incorporated will be useful to detect changes of marine benthic communities across multiple spatial and temporal scales.

Assessing the Use of Area- and Time-Averaging Based on Known De-correlation Scales to Provide Satellite Derived Sea Surface Temperatures in Coastal Areas

Satellite derived sea surface temperatures (SSTs) are often used as a proxy for in situ water temperatures, as they are readily available over large spatial and temporal scales. However, contamination of satellite images can prohibit their use in coastal areas. We compared in situ temperatures to SST foundation (~10 m depth) at 31 sites inshore of the East Australian Current (EAC), the dynamic western boundary current of the south Pacific gyre, using an area averaging approach to overcome coastal contamination. Varying across- and along-shelf distances were used to area average SST measurements and de-correlation time scales were used to gap fill data. As the EAC is typically anisotropic (dominant along-shore flow) the choice of across-shelf distances influenced the correlation with in situ temperatures more than along-shelf distances. However, the “optimal” distances for both measurements were within known de-correlation length scales. Incorporating both SST area and time averaging (based on de-correlation time scales) produced data for an average of 96% of days that in situ loggers were deployed, compared to 27% (52%) without (with) area averaging. Temperature differences between the in situ data and SSTs varied depending on time of year, with higher differences in the austral summer when daily in situ temperatures can range by up to 4.20°C. The differences between the in situ and SST measurements were, however, significant with or without area averaging (t-test: p-values < 0.05). Nevertheless, when using the area averaging approaches SSTs were only an average of ~1.05°C different from in situ temperatures and less than in situ temperature fluctuations. Linear mixed models revealed that latitude, distance to the coast and nearest estuary did not influence the difference between the in situ and satellite data as much as the water depth. This study shows that using de-correlation length and time scales to inform how to process satellite data can overcome contamination and missing data thereby greatly increasing the coverage and utility of SST data, particularly in coastal areas.