Piero Calosi

Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification?

Human‐assisted, trans‐generational exposure to ocean warming and acidification has been proposed as a conservation and/or restoration tool to produce resilient offspring. To improve our understanding of the need for and the efficacy of this approach, we characterized life‐history and physiological responses in offspring of the marine polychaete Ophryotrocha labronica exposed to predicted ocean warming (OW: + 3°C), ocean acidification (OA: pH −0.5) and their combination (OWA: + 3°C, pH −0.5), following the exposure of their parents to either control conditions (within‐generational exposure) or the same conditions (trans‐generational exposure). Trans‐generational exposure to OW fully alleviated the negative effects of within‐generational exposure to OW on fecundity and egg volume and was accompanied by increased metabolic activity. While within‐generational exposure to OA reduced juvenile growth rates and egg volume, trans‐generational exposure alleviated the former but could not restore the latter. Surprisingly, exposure to OWA had no negative impacts within‐ or trans‐generationally. Our results highlight the potential for trans‐generational laboratory experiments in producing offspring that are resilient to OW and OA. However, trans‐generational exposure does not always appear to improve traits and therefore may not be a universally useful tool for all species in the face of global change.

An in situ assessment of local adaptation in a calcifying polychaete from a shallow CO2 vent system

Ocean acidification (OA) is likely to exert selective pressure on natural populations. Our ability to predict which marine species will adapt to OA and what underlies this adaptive potential is of high conservation and resource management priority. Using a naturally low‐pH vent site in the Mediterranean Sea (Castello Aragonese, Ischia) mirroring projected future OA conditions, we carried out a reciprocal transplant experiment to investigate the relative importance of phenotypic plasticity and local adaptation in two populations of the sessile, calcifying polychaete Simplaria sp. (Annelida, Serpulidae, Spirorbinae): one residing in low pH and the other from a nearby ambient (i.e. high) pH site. We measured a suite of fitness‐related traits (i.e. survival, reproductive output, maturation, population growth) and tube growth rates in laboratory‐bred F2 generation individuals from both populations reciprocally transplanted back into both ambient and low‐pH in situ habitats. Both populations showed lower expression in all traits, but increased tube growth rates, when exposed to low‐pH compared with high‐pH conditions, regardless of their site of origin suggesting that local adaptation to low‐pH conditions has not occurred. We also found comparable levels of plasticity in the two populations investigated, suggesting no influence of long‐term exposure to low pH on the ability of populations to adjust their phenotype. Despite high variation in trait values among sites and the relatively extreme conditions at the low pH site (pH < 7.36), response trends were consistent across traits. Hence, our data suggest that, for Simplaria and possibly other calcifiers, neither local adaptations nor sufficient phenotypic plasticity levels appear to suffice in order to compensate for the negative impacts of OA on long‐term survival. Our work also emphasizes the utility of field experiments in natural environments subjected to high level of pCO2 for elucidating the potential for adaptation to future scenarios of OA.

Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life-history and physiology in a marine metazoan?

ABSTRACT Ocean warming and acidification are concomitant global drivers that are currently threatening the survival of marine organisms. How species will respond to these changes depends on their capacity for plastic and adaptive responses. Little is known about the mechanisms that govern plasticity and adaptability or how global changes will influence these relationships across multiple generations. Here, we exposed the emerging model marine polychaete Ophryotrocha labronica to conditions simulating ocean warming and acidification, in isolation and in combination over five generations to identify: (i) how multiple versus single global change drivers alter both juvenile and adult life-history traits; (ii) the mechanistic link between adult physiological and fitness-related life-history traits; and (iii) whether the phenotypic changes observed over multiple generations are of plastic and/or adaptive origin. Two juvenile (developmental rate; survival to sexual maturity) and two adult (average reproductive body size; fecundity) life-history traits were measured in each generation, in addition to three physiological (cellular reactive oxygen species content, mitochondrial density, mitochondrial capacity) traits. We found that multi-generational exposure to warming alone caused an increase in juvenile developmental rate, reactive oxygen species production and mitochondrial density, decreases in average reproductive body size and fecundity, and fluctuations in mitochondrial capacity, relative to control conditions. Exposure to ocean acidification alone had only minor effects on juvenile developmental rate. Remarkably, when both drivers of global change were present, only mitochondrial capacity was significantly affected, suggesting that ocean warming and acidification act as opposing vectors of stress across multiple generations. Summary: The multi-generational acclimation capacity of a species to ocean warming and acidification is determined by the flexibility of its mitochondrial electron transport system.

Does sex really matter? Explaining intraspecies variation in ocean acidification responses

Ocean acidification (OA) poses a major threat to marine ecosystems globally, having significant ecological and economic importance. The number and complexity of experiments examining the effects of OA has substantially increased over the past decade, in an attempt to address multi-stressor interactions and long-term responses in an increasing range of aquatic organisms. However, differences in the response of males and females to elevated pCO2 have been investigated in fewer than 4% of studies to date, often being precluded by the difficulty of determining sex non-destructively, particularly in early life stages. Here we highlight that sex can significantly impact organism responses to OA, differentially affecting physiology, reproduction, biochemistry and ultimately survival. What is more, these impacts do not always conform to ecological theory based on differential resource allocation towards reproduction, which would predict females to be more sensitive to OA owing to the higher production cost of eggs compared with sperm. Therefore, non-sex-specific studies may overlook subtle but ecologically significant differences in the responses of males and females to OA, with consequences for forecasting the fate of natural populations in a near-future ocean.

Contrasting physiological responses to future ocean acidification among Arctic copepod populations

Widespread ocean acidification (OA) is modifying the chemistry of the global ocean, and the Arctic is recognized as the region where the changes will progress at the fastest rate. Moreover, Arctic species show lower capacity for cellular homeostasis and acid-base regulation rendering them particularly vulnerable to OA. In the present study, we found physiological differences in OA response across geographically separated populations of the keystone Arctic copepod Calanus glacialis. In copepodites stage CIV, measured reaction norms of ingestion rate and metabolic rate showed severe reductions in ingestion and increased metabolic expenses in two populations from Svalbard (Kongsfjord and Billefjord) whereas no effects were observed in a population from the Disko Bay, West Greenland. At pHT 7.87, which has been predicted for the Svalbard west coast by year 2100, these changes resulted in reductions in scope for growth of 19% in the Kongsfjord and a staggering 50% in the Billefjord. Interestingly, these effects were not observed in stage CV copepodites from any of the three locations. It seems that CVs may be more tolerant to OA perhaps due to a general physiological reorganization to meet low intracellular pH during hibernation. Needless to say, the observed changes in the CIV stage will have serious implications for the C.xa0glacialis population health status and growth around Svalbard. However, OA tolerant populations such as the one in the Disko Bay could help to alleviate severe effects in C.xa0glacialis as a species.

Ocean acidification alters zooplankton communities and increases top‐down pressure of a cubozoan predator

The composition of local ecological communities is determined by the members of the regional community that are able to survive the abiotic and biotic conditions of a local ecosystem. Anthropogenic activities since the industrial revolution have increased atmospheric CO2 concentrations, which have in turn decreased ocean pH and altered carbonate ion concentrations: so called ocean acidification (OA). Single-species experiments have shown how OA can dramatically affect zooplankton development, physiology and skeletal mineralization status, potentially reducing their defensive function and altering their predatory and antipredatory behaviors. This means that increased OA may indirectly alter the biotic conditions by modifying trophic interactions. We investigated how OA affects the impact of a cubozoan predator on their zooplankton prey, predominantly Copepoda, Pleocyemata, Dendrobranchiata, and Amphipoda. Experimental conditions were set at either current (pCO2 370xa0μatm) or end-of-the-century OA (pCO2 1,100xa0μatm) scenarios, crossed in an orthogonal experimental design with the presence/absence of the cubozoan predator Carybdea rastoni. The combined effects of exposure to OA and predation by C.xa0rastoni caused greater shifts in community structure, and greater reductions in the abundance of key taxa than would be predicted from combining the effect of each stressor in isolation. Specifically, we show that in the combined presence of OA and a cubozoan predator, populations of the most abundant member of the zooplankton community (calanoid copepods) were reduced 27% more than it would be predicted based on the effects of these stressors in isolation, suggesting that OA increases the susceptibility of plankton to predation. Our results indicate that the ecological consequences of OA may be greater than predicted from single-species experiments, and highlight the need to understand future marine global change from a community perspective.

Metabolic and reproductive plasticity of core and marginal populations of the eurythermic saline water bug Sigara selecta (Hemiptera: Corixidae) in a climate change context

Ongoing climate change is driving dramatic range shifts in diverse taxa worldwide, and species responses to global change are likely to be determined largely by population responses at geographical range margins. Here we investigate the metabolic and reproductive plasticity in response to water temperature and salinity variation of two populations of the eurythermic saline water bug Sigara selecta: one population located close to the northern edge of its distribution, in a relatively cold, thermally stable region (SE England - marginal), and one close to the range centre, in a warmer and more thermally variable Mediterranean climate (SE Spain - core). We compared metabolic and oviposition rates and egg size, following exposure to one of four different combinations of temperature (15 and 25°C) and salinity (10 and 35gL-1). Oviposition rate was significantly higher in the marginal population, although eggs laid were smaller overall. No significant differences in oxygen consumption rates were found between core and marginal populations, although the marginal population showed higher levels of plasticity in both metabolic and reproductive traits. Our results suggest that population-specific responses to environmental change are complex and may be mediated by differences in phenotypic plasticity. In S. selecta, the higher plasticity of the marginal population may facilitate both its persistence in current habitats and northward expansion with future climatic warming. The less plastic core population may be able to buffer current environmental variability with minor changes in metabolism and fecundity, but could be prone to extinction if temperature and salinity changes exceed physiological tolerance limits in the future.

Bird is the word – on the importance of ethical and effective scientific communication

Back in 1963, the proto-punk band The Trashmen released the single Surfin ’ bird (written by Frazier, White, Harris & Wilson Jr. and released in November 1963 by Garrett label; https://www.youtube.com/watch?v=ZThquH5t0ow ). Fifty years later and despite the obscure lyrics, the song remains iconic in western pop culture; e.g. through the recurrent appearance in the TV show Family Guy (e.g. I dream of Jesus episode, released on 5 October 2008; https://www.youtube.com/watch?v=2WNrx2jq184 ). It is thought that the line ‘ everybody knows that the bird is the word ’ was inspired by a highly successful and catchy radio jingle released/commissioned in post prohibitionist USA by the Gallo brothers to boost the sales of their inexpensive fortified Thunderbird wine: ‘ Whats the word? Thunderbird ’ ( http://www.absurdintellectual.com/2009/06/05/everybodys-heard-that-the-bird-is-the-word-but-its-not-what-they-think/ ). This illustrates how a simple and catchy message can have a profound and long-lasting influence on society.

Early life stages of Northern shrimp (Pandalus borealis) are sensitive to fish feed containing the anti-parasitic drug diflubenzuron

Increasing use of fish feed containing the chitin synthesis inhibiting anti-parasitic drug diflubenzuron (DFB) in salmon aquaculture has raised concerns over its impact on coastal ecosystems. Larvae of Northern shrimp (Pandalus borealis) were exposed to DFB medicated feed under Control conditions (7.0u202f°C, pH 8.0) and under Ocean Acidification and Warming conditions (OAW, 9.5u202f°C and pH 7.6). Two weeks exposure to DFB medicated feed caused significantly increased mortality. The effect of OAW and DFB on mortality of shrimp larvae was additive; 10% mortality in Control, 35% in OAW, 66% in DFB and 92% in OAWu202f+u202fDFB. In OAWu202f+u202fDFB feeding and swimming activity were reduced for stage II larvae and none of the surviving larvae developed to stage IV. Two genes involved in feeding (GAPDH and PRLP) and one gene involved in moulting (DD9B) were significantly downregulated in larvae exposed to OAWu202f+u202fDFB relative to the Control. Due to a shorter intermoult period under OAW conditions, the OAWu202f+u202fDFB larvae were exposed throughout two instead of one critical pre-moult period. This may explain the more serious sub-lethal effects for OAWu202f+u202fDFB than DFB larvae. A single day exposure at 4u202fdays after hatching did not affect DFB larvae, but high mortality was observed for OAWu202f+u202fDFB larvae, possibly because they were exposed closer to moulting. High mortality of shrimp larvae exposed to DFB medicated feed, indicates that the use of DFB in salmon aquaculture is a threat to crustacean zooplankton.

The evolution of phenotypic plasticity under global change

Marine ecosystems are currently in a state of flux, with ocean warming and acidification occurring at unprecedented rates. Phenotypic plasticity underpins acclimatory responses by shifting the mean phenotype in a population, which may buffer the negative effects of global change. However, little is known about how phenotypic plasticity evolves across multiple generations. We tested this by reciprocally-transplanting the polychaete Ophryotrocha labronica between control and global change scenarios (ocean warming and acidification in isolation and combined) over five generations. By comparing the reaction norms of four life-history traits across generations, we show that juvenile developmental rate in the combined scenario was the only trait that changed its plastic response across generations when transplanted back to control conditions, and that adaptive plasticity was conserved in most traits, despite significant levels of selection and strong declines in individual fitness in the multi-generational exposure. We suggest the change in level of plasticity in the combined scenario is caused by differential allocation of energy between the mean and the plasticity of the trait along the multigenerational exposure. The ability to maintain within-generational levels of plasticity under global change scenarios has important eco-evolutionary and conservation implications, which are examined under the framework of assisted evolution programs.