Losing ecosystem resistance to change: when grazers fail to compensate for primary productivity

Chair: Ivan Nagelkerken

Bayden D. Russell (1)*, Charlee A. Corra (2), Giulia Ghedini (3), Nicole L. Mertens (3) and Sean D. Connell (3)

1 The Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China.
2 Northeastern University, Boston, Massachusetts, 02155, USA
3 Southern Seas Ecology Laboratories, School of Biological Sciences, The University of Adelaide, Adelaide, SA, Australia.

Future temperature and CO2 are predicted to change the structure and function of marine ecosystems by altering rates of both primary productivity and consumption. Metabolic theories predict that increases in consumption should outstrip that of production, but this assumes that physiological rates will increase in consumers more than primary producers.

I draw together the results of several of our experiments assessing the effects of elevated temperature and CO2 (ocean acidification) in key subtidal marine grazers, from physiological to ecosystem levels (aquarium to mesocosm to CO2 vent).

We show that under near-future scenarios herbivory provides ecosystem resistance by countering increased primary productivity in algal species which dominate under altered conditions. However, both metabolic rates and consumption of algae by gastropods reach thresholds, and decline, at cooler temperatures than primary productivity. Therefore, under end-of-century conditions primary productivity is likely to outstrip consumption in some subtidal systems.

These results suggest that the ability of grazers to compensate for increasing primary production may be reduced under end of century conditions and, consequently, their ability to maintain ecosystem structure and function will be compromised

Antarctic Pteropods (Limacina helicina antarctica) as a Sentinel Organism for the Impact of ocean acidification

Chair: Vonda Cummings

Gretchen E Hofmann (1)*, Kevin M. Johnson (1), Umihiko Hoshijima (1), Juilet M. Wong (1)

1 Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara CA 93106 USA

The pteropod Limacina helicina antarctica is a dominant member of the zooplankton assemblage in the Antarctic marine ecosystem, and is an important member of a relatively simple food web in nearshore waters. Limacina is a shelled pteropod, and the formation of the shell is jeopardized by dissolution in response to ocean acidification. Pteropods in general have been proposed as indicator organisms for the stress induced by future ocean acidification. Our goal was to develop a transcriptomic resource for this species that would support mechanistic studies to examine the physiological response of Limacina to acidification stress. We hoped to explore how gene expression analysis might be part of a larger effort to use pteropods as sentinel organisms in response to ocean acidification.

RNA sequencing (RNA-Seq) was performed on individuals exposed to a range of pH environments and elevated temperature. De novo assembly of the transcriptome was performed using Trinity. For gene expression analysis, pteropods were exposed to variable pCO2 conditions in a flow-through CO2 system set-up at McMurdo Station, Antarctica.

Annotation of the assembled L. antarctica transcriptome resulted in the identification of 81,229 sequences and with genes in numerous functional pathways. Using the de novo transcriptome, after 1 week of exposure to one of three pH treatments (8.2, 7.9 and 7.7), we identified over 2,000 differentially expressed genes. Genes for numerous cellular pathways were represented, including pathways involved in ion pumping, metabolism, and calcification. [These pH values represented pCO2 levels of 257, 531 and 938 μatm CO2 , respectively.]

The study identified numerous genes of interest that would support employing a molecular ecology approach in studying the response of L. antarctica to environmental stress. We propose that this resource is also applicable to pteropods collected in all sectors of the Southern Ocean, the Arctic and temperate regions.

Impaired riverward migration behaviour of glass eels under climate change

Chair: Martin Grosell

Tiago F. Grilo1, José R. Paula1, Marta S. Pimentel1, Catarina Santos1, Rui Rosa1


1 MARE – Marine and Environmental Sciences Centre, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Av. Nossa Senhora do Cabo

939, 2750-374, Cascais, Portugal


Background: Eels are catadromous species of unquestionable ecological and economical relevance, reflecting quite well the environmental health and integrity of aquatic systems, from freshwater to the open sea. Upon arrival to the continental shelf the leptocephalus larva of the European eel (Anguilla anguilla) metamorphoses into juvenile glass eels. They orientate towards freshwater habitats using inland water odors (e.g. geosmin), temperature and salinity gradients. Odors are among the most important cues in glass eels migration, however their role in freshwater attractiveness  remains  poorly  understood.  Predicted  changes  in  Earth’s  climate might influence glass eels migration and olfactory sensitivity. Thus, the main goal was to evaluate the effects of ocean warming (∆ +3ºC) and high pCO2, with concomitant acidification (ΔpH −0.5 units) on glass eels behavior, specifically on their ability to detect olfactory cues.

Methods: The cues tested were geosmin, salinity and water flow. Animals were collected in three areas of the Minho estuary (mouth, intermediate and upstream), in Portugal, trying to reflect a salinity gradient. Responsiveness was measured according to the percentage of time that glass eels stayed on the cue.

Findings: Time spent by control organisms in all the cues tested was always higher than 65%. Under a warming scenario, glass eels responded in a similar way to the different cues as the control animals, suggesting that warming individually might not interfere with their sensory ability. Nevertheless, acidification by itself and the combined scenario of warming and acidification seem to have a disruptive effect in olfactory capacity, most evident for the glass eels under at higher salinities and tested for geosmin. Responsiveness in these cases declined significantly in relation to the controls, varying around 35%.

Conclusions:   Facing   these   results   if   acidification   continues   unabated,   the impairment of sensory ability will likely reduce eels population sustainability, with potentially profound consequences for marine diversity.

Heteroscedasticity is your friend: diurnally fluctuating acidification increases variance in – but not mean of – growth rate in barnacles

Chair: Philip Munday

Jon N Havenhand (1)*, Louise Eriander (2), Anna-Lisa Wrange (1)

1 Department of Marine Sciences, University of Gothenburg, Tjärnö, 45296 Strömstad, Sweden
2 Department of Marine Sciences, University of Gothenburg, 40530 Gothenburg, Sweden

Inshore marine habitats experience natural fluctuations in seawater chemistry far greater than those in the open oceans. In the shallow sublittoral, photosynthesis and respiration typically cause diurnal pH excursions of 0.2 – 0.4 units. Although these fluctuations have been known about for almost a century, their effects on organisms have been addressed only rarely.

We exposed multiple batches (different genotypes) of newly settled barnacles, Balanus improvisus, to constant “control” (pH 8.1), “acidified” (pH 7.7), or “fluctuating acidified” treatments (diurnally varying, pH 7.5 – 7.9) for 3 months. We measured multiple parameters of barnacle growth throughout the experiment, and shell mineralogy and shell hardness at the end of the experiment.

There was no effect of stable, or fluctuating, acidification on mean growth or shell mineralogy. However, variance in growth and mineralogy responses were ~20x greater in fluctuating acidification, such that some individuals grew up to 3x faster, (some also grew up to 3x more slowly), than in stable acidification. Both fluctuating and stable acidification caused significant reductions in shell hardness, and these reductions varied significantly among batches (genotypes).

Phenotypic variance is the raw material for natural selection. Our results show this variance can be far greater under diurnally fluctuating acidification than under stable acidification. As far as we’re aware, this has not been reported previously. We suggest that including simulated natural pH fluctuations in future experiments is likely to reveal ecologically and evolutionarily important responses that more traditional experimental designs would miss. Perhaps most importantly, these results show that rather than being a statistical headache that we might wish to transform away, unequal variances (“heteroscedasticity”) in our data can indicate important opportunities for selection and adaptation of responses to a future ocean.

Acid-base balance compensation is the unifying course of CO2 impact in fish

Chair: Ivan Nagelkerken

Martin Grosell (1)*, Rachael Heuer (2)

1 RSMAS, University of Miami, Miami Florida, 33149 USA
2 Department of Biological Sciences, University of North Texas, Denton, Texas 76203 USA

Fish are known to be excellent acid-base balance regulators and, by accumulation of plasma HCO3, successfully defend blood pH at ambient partial pressures of CO2 (pCO2) as high as 50,000 µAtm. The reaction to elevated PCO2 occurs within hours and persists for at least weeks leading to a new steady state of normalized pH but elevated plasma pCO2 and [HCO3] at levels as low as 750 µAtm.

Gulf Toadfish (Opsanus beta) were exposed to CO2 ranging from background to 1900 µAtm. Intestinal tissue transport properties were analysed using in vitro techniques along with isolated tissue measurements in Ussing chambers. Furthermore, isolated tissue metabolic rate was assessed by respiromery.

The steady state of elevated pCO2 and [HCO3] seen during exposure to elevated CO2 appears to be the product of HCO3 uptake across the gill rather than H+ extrusion and likely accounts for a number of observations of sublethal effects in fish exposed to environmentally relevant pCO2 levels. Such observations include altered otolith growth presumably due to altered levels of substrate for CaCO3 formation as well as altered transport of ion and acid-base equivalents by the marine fish intestinal epithelium and by the gill epithelium. The altered ion transport by osmoregulatory tissues has implications for integrative salt and water balance as well as energy utilization and consumption by these tissues.

The protection of extracellular pH during CO2 exposure results in a cascade of effects including altered intracellular acid-base balance and shifts in cellular transmembrane ion gradients with pronounced effects on sensory and central nervous system function.

Ocean acidification leaves dispersing fish larvae lost at sea

Chair: Martin Grosell

Tullio Rossi, Ivan Nagelkerken and Sean D. Connell

Southern Seas Ecology Laboratories, School of Biological Sciences and The Environment Institute, DX 650 418, The University of Adelaide, Adelaide, SA 5005, Australia.


The dispersal of larvae and their settlement to suitable habitat is fundamental to replenishment of marine populations and the communities in which they live. Sound is a critical part of this process for some species because it can act as a cue for larvae to orientate towards suitable settlement habitat. Because marine sounds are largely of biological origin, they not only carry information about the location of potential habitat, but also information about the quality of habitat. While ocean acidification is known to have profound effects on marine life, its effect on biological sound production and its reception by navigating oceanic larvae remains unknown. Here we show that ocean acidification can profoundly alter biological sound quantity and quality of future soundscapes. A quieter soundscape indirectly penalizes oceanic larvae by reducing the detection range of coastal habitats. Remarkably, ocean acidification also caused a switch in role of marine sound cues from attractor to repellent in the auditory preferences of fish larvae. Both of these indirect and direct effects of ocean acidification put at risk the complex processes of larval orientation, settlement, and habitat connectivity.