Gillanders Aquatic Ecology Lab
2020 publications (links to each paper available at Read More)
Environmental controls on the geochemistry of a short-lived bivalve in Southeastern Australian estuaries
Chamberlayne, BK, JJ Tyler, BM Gillanders. 2020. Estuaries and Coasts
Geochemical signals in bivalve carbonate hold the potential to record environmental change over timescales from months to centuries; however, not all bivalves provide reliable proxy records, and modern studies are essential to calibrate these relationships prior to use in palaeo-environmental reconstruction. In this study, 19 shells of the estuarine bivalve Arthritica helmsi, from 14 sites in Southeastern Australia, were obtained from museum collections and analysed for trace elemental (Sr/Ca,Mg/Ca, Sr/Li and Ba/Ca) and stable isotopic ratios (18O/16O and 13C/12C). Mean Sr/Ca and Mg/Ca exhibited significant negative correlations to temperature (R2 = 0.49, p = 0.001; R2 = 0.25, p = 0.02) in agreement with previously published models for trace element partitioning into inorganic aragonite. In addition, the within-shell range of Sr/Ca and Mg/Ca, as measured by laser ablation ICPMS, correlated to the temperature range (R2 = 0.22, p = 0.03; R2 = 0.46, p = 0.002, respectively). Sr/Li ratios were also negatively correlated to temperature (R2 = 0.34, p = 0.008); however, a significant difference in the model coefficients with previous studies
indicates this proxy should be applied with caution. Both oxygen and carbon isotope values exhibited large differences between shells from terrestrial, estuarine and marine waters, suggesting that these stable isotopes hold a potential to record large environmental changes such as sea-level changes or freshening/salinisation in estuarine environments. This study presents the first geochemical study of Arthritica helmsi, highlighting its potential as an environmental tracer.
Images: Briony Chamberlayne
Image: Figure 1 from paper depicting the information that can be gathered from an environmental DNA analysis on coastal sediments. There is a clear change from saltmarsh to mangrove to seagrass from the past to the present day. Additionally, the seagrass community has changed at the species level, which can be detected via eDNA analysis methods of high resolution, i.e. hybridisation capture.
A muddy time capsule: using sediment environmental DNA for the long-term monitoring of coastal vegetated ecosystems
Foster, NR, BM Gillanders, AR Jones, JM Young, M Waycott. 2020. Marine and Freshwater Research
Seagrass, saltmarsh and mangrove habitats are declining around the world as anthropogenic activity and climate change intensify. To be able to effectively restore and maintain healthy coastal-vegetation communities, we must understand how and why they have changed in the past. Identifying shifts in vegetation communities, and the environmental or human drivers of these, can inform successful management and restoration strategies. Unfortunately, long-term data (i.e. decades to hundreds of years) on coastal vegetated ecosystems that can discern community-level changes are mostly non-existent in the scientific record. We propose implementing DNA extracted from coastal sediments to provide an alternative approach to long-term ecological reconstruction for coastal vegetated ecosystems. This type of DNA is called ‘environmental DNA’ and has previously been used to generate long-term datasets for other vegetated systems but has not yet been applied to vegetation change in coastal settings. In this overview, we explore the idea of using sediment eDNA as a long-term monitoring tool for seagrass, saltmarsh and mangrove communities. We see real potential in this approach for reconstructing long-term ecological histories of coastal vegetated ecosystems, and advocate that further research be undertaken to develop appropriate methods for its use.
Image: Red eared slider turtle. From Wikimedia Commons, the free media repository
Pet or pest? Stable isotope methods for determining the provenance of an invasive alien species
Hill, KGW, KE Nielson, JJ Tyler, FA McInerney, ZA Doubleday, GJ Frankham, RN Johnson, BM Gillanders, S Delean, P Cassey. 2020. Neobiota
The illegal pet trade facilitates the global dispersal of invasive alien species (IAS), providing opportunities for new pests to establish in novel recipient environments. Despite the increasing threat of IAS to the environment and economy, biosecurity efforts often lack suitable, scientifically-based methods to make effective management decisions, such as identifying an established IAS population from a single incursion event. We present a proof-of-concept for a new application of a stable isotope technique to identify wild and captive histories of an invasive pet species. Twelve red-eared slider turtles (Trachemys scripta elegans) from historic Australian incursions with putative wild, captive and unknown origins were analysed to: (1) present best-practice methods for stable isotope sampling of T. s. elegans incursions; (2) effectively discriminate between wild and captive groups using stable isotope ratios; and (3) present a framework to expand the methodology for use on other IAS species. A sampling method was developed to obtain carbon (δ13C) and nitrogen (δ15N) stable isotope ratios from the keratin layer of the carapace (shells), which are predominantly influenced by dietary material and trophic level respectively. Both δ13C and δ15N exhibited the potential to distinguish between the wild and captive origins of the samples. Power simulations demonstrated that isotope ratios were consistent across the carapace and a minimum of eight individuals were required to effectively discriminate wild and captive groups, reducing overall sampling costs. Statistical classification effectively separated captive and wild groups by δ15N (captive: δ15N‰ ≥ 9.7‰, minimum of 96% accuracy). This study outlines a practical and accessible method for detecting IAS incursions, to potentially provide biosecurity staff and decision-makers with the tools to quickly identify and manage future IAS incursions.
Image: A group of Port Jackson Sharks, Heterodontus portusjacksoni, at Nepean Bay, Port Phillip, Victoria. Source: Mark Norman / Museum Victoria. License: CC by Attribution
Port Jackson shark growth is sensitive to growth
Izzo, C, BM Gillanders. 2020. Frontiers in Marine Science
Climatic effects on the growth of apex marine predators – such as sharks – are poorly understood; moreover, shifts in shark growth are primarily attributed to fishing pressure. This paucity of information impedes management and conservation planning for these taxa. Using vertebral increment patterning as a proxy of somatic growth, this study reconstructed mean growth of the philopatric and demersal Heterodontus portusjacksoni population from Gulf St Vincent (South Australia). A biochronology of shark growth spanning a 15 year period (1996–2010) was developed using mixed effects models. The biochronology showed considerable year-to-year deviations in growth that were significantly and negatively correlated with mean sea surface temperatures during the species’ breeding season (July to November). These findings are consistent with mesocosm experiments and support the influence of changing climates on shark growth; particularly in an inshore, demersal, and highly philopatric shark species. It is likely that the effects of environmental variation occur in a species specific manner, governed by life history strategies and ecological requirements. In this manner, life history traits might aid in estimating species vulnerability to climate change.
Top graphic: Alice Jones; bottom image: Bronwyn Gillanders
Estimating mangrove tree biomass and carbon content: a comparison of forest inventory techniques and drone imagery
Jones, AR, RR Segaran, K Clarke, M Waycott, WSH Goh, BM Gillanders. 2020. Frontiers in Marine Science
Mangroves provide many ecosystem services including a considerable capacity to.sequester and store large amounts of carbon, both in the sediment and in the above-ground biomass. Assessment of mangrove above-ground carbon stock relies on accurate measurement of tree biomass, which traditionally involves collecting direct measurements from trees and relating these to biomass using allometric relationships. We investigated the potential to predict tree biomass using measurements derived from unmanned aerial vehicle (UAV), or drone, imagery. This approach has the potential to dramatically reduce time-consuming fieldwork, providing greater spatial survey coverage and return for effort, and may enable data to be collected in otherwise hazardous or inaccessible areas. We imaged an Avicennia marina (gray mangrove) stand using an RGB camera mounted on a UAV. The imaged trees were subsequently felled, enabling physical measurements to be taken for traditional biomass estimation techniques, as well as direct measurements of biomass and tissue carbon content. UAV image-based tree height measurements were highly accurate (R2 = 0.98). However, the variables that could be measured from the UAV imagery (tree height and canopy area) were poor predictors of tree biomass. Using the physical measurement data, we identified that trunk diameter is a key predictor of A. marina biomass. Unfortunately, trunk diameter cannot be directly measured from the UAV imagery, but it can be predicted (with some error) using models that incorporate other UAV image-based measurements, such as tree height and canopy area. However, reliance on second-order estimates of trunk diameter led to increased uncertainty in the subsequent predictions of A. marina
biomass, compared to using physical measurements of trunk diameter taken directly
from the trees. Our study demonstrates that there is potential to use UAV-based
imagery to measure mangrove A. marina tree structural characteristics and biomass.
Further refinement of the relationship between UAV image-based measurements and tree diameter is needed to reduce error in biomass predictions. UAV image-based estimates can be made far more quickly and over extensive areas when compared to traditional data collection techniques and, with improved accuracy through further model-calibration, have the potential to be a powerful tool for mangrove biomass and carbon storage estimation.
Graphic: Kelsey Kingsbury
Range-extending coral reef fishes trade-off growth for maintenance of body condition in cooler waters.
Kingsbury, KM, BM Gillanders, DJ Booth, EOC Coni, I Nagelkerken. 2020. Science of the Total Environment
As ocean waters warm due to climate change, tropical species are shifting their ranges poleward to remain within their preferred thermal niches. As a result, novel communities are emerging in which tropical species interact with local temperate species, competing for similar resources, such as food and habitat. To understand how range-extending coral reef fish species perform along their leading edges when invading temperate ecosystems, we studied proxies of their fitness, including somatic growth (length increase), feeding rates, and body condition, along a 730-km latitudinal gradient situated in one of the global warming hotspots. We also studied co-occurring temperate species to assess how their fitness is affected along their trailing edges under ocean warming. We predicted that tropical fishes would experience reduced performance as they enter novel communities with suboptimal environmental conditions. Our study shows that although tropical fish maintain their body condition (based on three proxies) and stomach fullness across all invaded temperate latitudes, they exhibit decreased in situ growth rates, activity levels, and feeding rates in their novel temperate environment, likely a result of lower metabolic rates in cooler waters. We posit that tropical fishes face a growth–maintenance trade-off under the initial phases of ocean warming (i.e. at their leading edges), allowing them to maintain their body condition in cooler temperate waters but at the cost of slower growth. Temperate fish exhibited no distinct patterns in body
condition and performance along the natural temperature gradient studied. However, in the face of future climate change when metabolism is no longer stymied by low water temperatures, tropical range-extending species are likely to approach their native-range growth rates along their leading edges, ultimately leading to increased
competitive interactions with local species in temperate ecosystems.
Trophic niche segregation allows range-extending coral reef fishes to co-exist with temperate species under climate change
Kingsbury, KM, BM Gillanders, DJ Booth, I Nagelkerken. 2020. Global Change Biology.
Changing climate is forcing many terrestrial and marine species to extend their ranges poleward to stay within the bounds of their thermal tolerances. However, when such species enter higher latitude ecosystems, they engage in novel interactions with local species, such as altered predator–prey dynamics and competition for food. Here, we evaluate the trophic overlap between range‐extending and local fish species along the east coast of temperate Australia, a hotspot for ocean warming and species range extensions. Stable isotope ratios (δ15N and δ13C) of muscle tissue and stomach content analysis were used to quantify overlap of trophic niche space between vagrant tropical and local temperate fish communities along a 730 km (6°) latitudinal gradient. Our study shows that in recipient temperate ecosystems, sympatric tropical and temperate species do not overlap significantly in their diet—even though they forage on broadly similar prey groups—and are therefore unlikely to compete for trophic niche space. The tropical and temperate species we studied, which are commonly found in shallow‐water coastal environments, exhibited moderately broad niche breadths and local‐scale dietary plasticity, indicating trophic generalism. We posit that because these species are generalists, they can co‐exist under current climate change, facilitating the existence of novel community structures.
Graphical abstract: Jasmin Martino
See the blog here with larger version of graphical abstract
Experimental support towards a metabolic proxy in fish using otolith carbon isotopes
Martino, JC, ZA Doubleday, MT Chung, BM Gillanders. 2020. Journal of Experimental Biology
Metabolic rate underpins our understanding of how species survive, reproduce and interact with their environment, but can be difficult to measure in wild fish. Stable carbon isotopes (δ13C) in ear stones (otoliths) of fish may reflect lifetime metabolic signatures but experimental validation is required to advance our understanding of the relationship. To this end, we reared juvenile Australasian snapper (Chrysophrys auratus), an iconic fishery species, at different temperatures and used intermittent-flow respirometry to calculate standard metabolic rate (SMR), maximum metabolic rate (MMR) and absolute aerobic scope (AAS). Subsequently, we analysed δ13C and oxygen isotopes (δ18O) in otoliths using isotope-ratio mass spectrometry. We found that under increasing temperatures, δ13C and δ18O significantly decreased, while SMR and MMR significantly increased. Negative logarithmic relationships were found between δ13C in otoliths and both SMR and MMR, while exponential decay curves were observed between proportions of metabolically sourced carbon in otoliths (Moto) and both measured and theoretical SMR. We show that basal energy for subsistence living and activity metabolism, both core components of field metabolic rates, contribute towards incorporation of δ13C into otoliths and support the use of δ13C as a metabolic proxy in field settings. The functional shapes of the logarithmic and exponential decay curves indicated that physiological thresholds regulate relationships between δ13C and metabolic rates due to upper thresholds of Moto. Here, we present quantitative experimental evidence to support the development of an otolith based metabolic proxy, which could be a powerful tool in reconstructing lifetime biological trends in wild fish.
Image: Figure 3 (bottom half) from paper
Water and otolith chemistry: implications for discerning estuarine nursery habitat use of a juvenile flatfish
Martinho, F, B Pina, M Nunes, RP Vasconcelos, VF Fonseca, D Crespo, AL Primo, A Vaz, MA Pardal, BM Gillanders, SE Tanner, P Reis-Santos. 2020. Frontiers in Marine Science
Variations in otolith elemental composition are widely used to reconstruct fish movements. However, reconstructing habitat use and environmental histories of fishes within estuaries is still a major challenge due to the dynamic nature of these coastal environments. In this study, we performed a laboratory experiment to investigate the effects of variations in salinity (three levels; 5, 18, 30) and temperature (two levels; 16, 21 C) on the otolith elemental composition (Mg:Ca, Mn:Ca, Sr:Ca, Ba:Ca) of juvenile Senegalese sole Solea senegalensis. Temperature and salinity treatments mirrored the natural conditions of the estuarine habitats occupied by juvenile Senegalese sole, thereby providing information on the applicability of otolith microchemistry to reconstruct habitat use patterns within estuarine nurseries, where individual fish move across complex salinity and temperature gradients. While Sr:Ca and Ba:Ca in otoliths were both positively related to salinity, no temperature effect was observed. Partition coefficients, proxies for element incorporation rates increased with increasing salinity for Sr (DSr) and Ba (DBa). In contrast, salinity and temperature had little influence on otolith Mn:Ca and Mg:Ca, supporting physiological control on the incorporation of these elements. Our results are a stepping stone for the interpretation of otolith chemical profiles for fish collected in their natural habitats and contribute to better understanding the processes involved in otolith element incorporation.
Graphical abstract: Cristian Monaco
Dietary generalism accelerates arrival and persistence of coral-reef fishes in their novel ranges under climate change
Monaco, CJ, CJA Bradshaw, DJ Booth, BM Gillanders, DS Shoeman, I Nagelkerken. 2020. Global Change Biology
Climate change is redistributing marine and terrestrial species globally. Life-history traits mediate the ability of species to cope with novel environmental conditions, and can be used to gauge the potential redistribution of taxa facing the challenges of a changing climate. However, it is unclear whether the same traits are important across different stages of range shifts (arrival, population increase, persistence). To test which life-history traits most mediate the process of range extension, we used a 16-year dataset of 35 range-extending coral-reef fish species and quantified the importance of various traits on the arrival time (earliness) and degree of persistence (prevalence and patchiness) at higher latitudes. We show that traits predisposing species to shift their range more rapidly (large body size, broad latitudinal range, long dispersal duration) did not drive the early stages of redistribution. Instead, we found that as diet breadth increased, the initial arrival and establishment (prevalence and patchiness) of climate migrant species in temperate locations occurred earlier. While the initial incursion of range-shifting species depends on traits associated with dispersal potential, subsequent establishment hinges more on a species’ ability to exploit novel food resources locally. These results highlight that generalist species that can best adapt to novel food sources might be most successful in a future ocean.
Image: Figure 4 from paper showing modeled population geographic range of great hammerhead sharks (Sphyrna mokarran).
Predicting geographic ranges of marine animal populations using stable isotopes: a case study of great hammerhead sharks in eastern Australia.
Raoult, V, CN Trueman, KM Kingsbury, BM Gillanders, MK Broadhurst, JE Williamson, I Nagelkerken, DJ Booth, V Peddemors, LIE Couturier, TF Gaston. 2020. Frontiers in Marine Science
Determining the geographic range of widely dispersed or migratory marine organisms is notoriously difficult, often requiring considerable costs and typically extensive tagging or exploration programs. While these approaches are accurate and can reveal important information on the species, they are usually conducted on only a small number of individuals and can take years to produce relevant results, so alternative approaches may be preferable. The presence of latitudinal gradients in stable carbon isotope compositions of marine phytoplankton offers a means to quickly determine likely geographic population ranges of species that rely on productivity from these resources. Across sufficiently large spatial and temporal scales, the stable carbon isotopes of large coastal or pelagic marine species should reflect broad geographic patterns of resource use, and could be used to infer geographic ranges of marine populations. Using two methods, one based on a global mechanistic model and the other on targeted low cost latitudinal sampling of fishes, we demonstrate and compare these stable isotope approaches to determine the core population geography of an apex predator, the great hammerhead (Sphyrna mokarran). Both methods indicated similar geographic ranges and suggested that S. mokarran recorded in south-eastern Australia are likely to be from more northern Australian waters. These approaches could be replicated in other areas where coastlines span predictable geographic gradients in isotope values and be used to determine the core population geography of highly mobile species to inform management decisions.
Image: Seagrass meadow. CC-BY-CA-4.0; Milorad Mikota
A meta-analysis of multiple stressors on seagrasses in the context of marine spatial cumulative impacts assessment
Stockbridge, J., AR Jones, BM Gillanders. 2020. Scientific Reports
Humans are placing more strain on the world’s oceans than ever before. Furthermore, marine ecosystems are seldom subjected to single stressors, rather they are frequently exposed to multiple, concurrent stressors. When the combined effect of these stressors is calculated and mapped through cumulative impact assessments, it is often assumed that the effects are additive. However, there is increasing evidence that different combinations of stressors can have non-additive impacts, potentially leading to synergistic and unpredictable impacts on ecosystems. Accurately predicting how stressors interact is important in conservation, as removal of certain stressors could provide a greater benefit, or be more detrimental than would be predicted by an additive model. Here, we conduct a meta-analysis to assess the prevalence of additive, synergistic, and antagonistic stressor interaction effects using seagrasses as case study ecosystems. We found that additive interactions were the most commonly reported in seagrass studies. Synergistic and antagonistic interactions were also common, but there was no clear way of predicting where these non-additive interactions occurred. More studies which synthesise the results of stressor interactions are needed to be able to generalise interactions across ecosystem types, which can then be used to improve models for assessing cumulative impacts.
Graphical abstract from paper
Fundamental questions and applications of sclerochronology: Community-defined research priorities
Trofimova, T, SJ Alexandroff, MJ Mette, E Tray, PG Butler, SE Campana, EM Harper, ALA Johnson, JR Morrongiello, M Peharda, BR Schone, C Andersson, CFT Andrus, BA Black, M Burchell, ML Carroll, KL DeLong, BM Gillanders, P Grønkjær, D Killam, AL Prendergast, DJ Reynolds, JD Scourse, K Shirai, J Thebault, C Trueman, N de Winter. 2020. Estuarine, Coastal and Shelf Science
Horizon scanning is an increasingly common strategy to identify key research needs and frame future agendas in science. Here, we present the results of the first such exercise for the field of sclerochronology, thereby providing an overview of persistent and emergent research questions that should be addressed by future studies. Through online correspondence following the 5th International Sclerochronology Conference in 2019, participants submitted and rated questions that addressed either knowledge gaps or promising applications of sclerochronology. An initial list of 130 questions was compiled based on contributions of conference attendees and reviewed by expert panels formed during the conference. Herein, we present and discuss the 50 questions rated to be of the highest priority, determined through an online survey distributed to sclerochronology community members post the conference. The final list (1) includes important questions related to mechanisms of biological control over biomineralization, (2) highlights state of the art applications of sclerochronological methods and data for solving long-standing questions in other fields such as climate science and ecology, and (3) emphasizes the need for common standards for data management and analysis. Although research priorities are continually reassessed, our list provides a roadmap that can be used to motivate research efforts and advance sclerochronology toward new, and more powerful, applications.
Near Calperun Station, SA
Giant Australian cuttlefish