Combined effects of climate change stressors and predators with contrasting feeding-digestion strategies on a mussel species.

We investigated the combined effects of Ocean Warming (OW), Acidification (OA) and predator cues (Non-Consumptive Effects; NCEs) of two predators with contrasting feeding-digestion strategies on the mussel Perumytilus purpuratus. We considered starfish-NCEs (partially external digestion) and snail-NCEs (internal digestion). Mussels were exposed for 13 weeks to cross-factored OA (~500 and ~1400 µatm, pCO2) and OW (~15 and ~20 °C) conditions, in the presence/absence of NCEs from one or both predators. Mussels exposed to both NCEs exhibited smaller length and buoyant weight growth than those under control or snail-NCEs conditions. Mussels exposed to starfish-NCEs exhibited smaller wet mass than control mussels. OW and starfish-NCEs in isolation or combined with snail-NCEs increased mussel oxygen consumption. Byssal biogenesis was affected by the three-factors interaction. Clearance rates were affected by the OW × OA interaction. We suggest that mainly starfish-NCEs, in isolation or interacting with OA or/and OW, can threat mussel traits and the associated community.

Multiple-stressor effects of ocean acidification, warming and predation risk cues on the early ontogeny of a rocky-shore keystone gastropod.

To understand how climate change stressors might affect marine organisms and support adequate projections it is important to know how multiple stressors may be modulated by the presence of other species. We evaluated the direct effects of ocean warming (OW) and ocean acidification (OA) together with non-consumptive effects (NCEs) of the predatory crab Acanthocyclus hassleri on early ontogeny fitness-related traits of the commercially important rocky-shore keystone gastropod Concholepas concholepas. We measured the response of nine traits to these stressors at either the organismal level (survival, growth, feeding rates, tenacity, metabolic rate, calcification rate) or sub-organismal level (nutritional status, ATP-supplying capacity, stress condition). C. concholepas survival was not affected by any of the stressors. Feeding rates were not affected by OW or OA; however, they were reduced in the presence of crab NCEs compared with control conditions. Horizontal tenacity was affected by the OA × NCEs interaction; in the presence of NCEs, OA reduced tenacity. The routine metabolic rate, measured by oxygen consumption, increased significantly with OW. Nutritional status assessment determined that carbohydrate content was not affected by any of the stressors. However, protein content was affected by the OA × NCEs interaction; in the absence of NCEs, OA reduced protein levels. ATP-supplying capacity, measured by citrate synthase (CS) activity, and cellular stress condition (HSP70 expression) were reduced by OA, with reduction in CS activity found particularly at the high temperature. Our results indicate C. concholepas traits are affected by OA and OW and the effects are modulated by predator risk (NCEs). We conclude that some C. concholepas traits are resilient to climate stressors (survival, growth, horizontal tenacity and nutritional status) but others are affected by OW (metabolic rate), OA (ATP-supplying capacity, stress condition), and NCEs (feeding rate). The results suggest that these negative effects can adversely affect the associated community.

Effects of artificial light at night and predator cues on foraging and predator avoidance in the keystone inshore mollusc Concholepas concholepas.

The growth of Artificial Light At Night (ALAN) is potentially having widespread effects on terrestrial and coastal habitats. In this study we addressed both the individual effects of ALAN, as well as its combined effect with predation risk on the behaviour of Concholepas concholepas, a fishery resource and a keystone species in the southeastern Pacific coast. We measured the influence of ALAN and predation risk on this mollusc's feeding rate, use of refuge for light and crawling out of water behaviour. These behavioural responses were studied using light intensities that mimicked levels that had been recorded in coastal habitat exposed to ALAN. Cues were from two species known to prey on C. concholepas during its early ontogeny: the crab Acanthocyclus hassleri and the seastar Heliaster helianthus. The feeding rates of C. concholepas were 3-4 times higher in darkness and in the absence of predator cues. In contrast, ALAN-exposed C. concholepas showed lower feeding activity and were more likely to be in a refuge than those exposed to control conditions. In the presence of olfactory predator cues, and regardless of light treatment, C. concholepas tended to crawl-out of the waterline. We provide evidence to support the hypothesis that exposure to either ALAN or predation risk can alter the feeding behaviour of C. concholepas. However, predator cue recognition in C. concholepas was not affected by ALAN in situations where ALAN and predator cues were both present: C. concholepas continued to forage when predation risk was low, i.e., in darkness and away from predator cues. Whilst this response means that ALAN may not lead to increased predation mortality in C. concholepas, it will reduce feeding activity in this naturally nocturnal species in the absence of dark refugia. Such results may have implications for the long-term health, productivity and sustainability of this keystone species.

The combined effects of climate change stressors and predatory cues on a mussel species.

In order to make adequate projections on the consequences of climate change stressors on marine organisms, it is important to know how impacts of these stressors are affected by the presence of other species. Here we assessed the direct effects of ocean warming (OW) and acidification (OA) along with non-consumptive effects (NCEs) of a predatory crab and/or a predatory snail on the habitat-forming mussel Perumytilus purpuratus. Mussels were exposed for 10-14 weeks to contrasting pCO2 (500 and 1400 µatm) and temperature (15 and 20 °C) levels, in the presence/absence of cues from one or two predator species. We compared mussel traits at sub-organismal (nutritional status, metabolic capacity-ATP production-, cell stress condition via HSP70 expression) and organismal (survival, oxygen consumption, growth, byssus biogenesis, clearance rates, aggregation) levels. OA increased the mussels' oxygen consumption; and OA combined with OW increased ATP demand and the use of carbohydrate reserves. Mussels at present-day pCO2 levels had the highest protein content. Under OW the predatory snail cues induced the highest cell stress condition on the mussels. Temperature, predator cues and the interaction between them affected mussel growth. Mussels grew larger at the control temperature (15 °C) when crab and snail cues were present. Mussel wet mass and calcification were affected by predator cues; with highest values recorded in crab cue presence (isolated or combined with snail cues). In the absence of predator cues in the trails, byssus biogenesis was affected by OA, OW and the OA × OW and OA × predator cues interactions. At present-day pCO2 levels, more byssus was recorded with snail than with crab cues. Clearance rates were affected by temperature, pCO2 and the interaction between them. The investigated stressors had no effects on mussel aggregation. We conclude that OA, OW and the NCEs may lead to neutral, positive or negative consequences for mussels.

Combined effect of pCO2 and temperature levels on the thermal niche in the early benthic ontogeny of a keystone species.

We evaluated the effects of projected, near future ocean acidification (OA) and extreme events of temperature (warming or cooling) on the thermal tolerance of Concholepas concholepas, a coastal benthic keystone species. Three separate trials of an experiment were conducted by exposing juvenile C. concholepas for 1 month to one of two contrasting pCO2 levels (~500 and ~1200 µatm). In addition, each pCO2 level was combined with one of four temperature treatments. The control was 15 °C, whilst the other temperatures were 10 °C (Trial 1), 20 °C (Trial 2) and 25 °C (Trial 3). At the end of each trial, we assessed Critical Thermal maximum (CTmax) and minimum (CTmin) via self-righting success, calculated partial thermal tolerance polygons, measured somatic growth, determined transcription of Heat Shock Proteins 70 (HSP70) and measured oxygen consumption rates. Regardless of pCO2 level, HSP70 transcript levels were significantly higher in juveniles after exposure to extreme temperatures (10 °C and 25 °C) indicating physiological stress. Oxygen consumption rates increased with increasing temperature from 10 °C to 20 °C though showed a decrease at 25 °C. This rate was not affected by pCO2 or the interaction between temperature and pCO2. Juveniles exposed to present-day and near future pCO2 levels at 20 °C showed similar thermal tolerance polygonal areas; whilst changes in both CTmin and CTmax at 25 °C and 10 °C caused narrower and broader areas, respectively. Temperature affected growth, oxygen consumption and HSP70 transcription in small juvenile C. concholepas. Exposure to elevated pCO2 did not affect thermal tolerance, growth or oxygen consumption at temperatures within the thermal range normally experienced by this species in northern Chile (15-20 °C). At elevated pCO2 conditions, however, exposure to warmer (25 °C) or colder (10 °C) temperatures reduced or increased the thermal area, respectively. This study demonstrates the importance of examining the thermal-tolerance edges to better understand how OA and temperature will combine to physiologically challenge inter-tidal organisms.

Artificial light pollution influences behavioral and physiological traits in a keystone predator species, Concholepas concholepas.

Artificial Light At Night (ALAN) is an increasing global problem that, despite being widely recognized in terrestrial systems, has been studied much less in marine habitats. In this study we investigated the effect of ALAN on behavioral and physiological traits of Concholepas concholepas, an important keystone species of the south-eastern Pacific coast. We used juveniles collected in intertidal habitats that had not previously been exposed to ALAN. In the laboratory we exposed them to two treatments: darkness and white LED (Lighting Emitting Diodes) to test for the impacts of ALAN on prey-searching behavior, self-righting time and metabolism. In the field, the distribution of juveniles was observed during daylight-hours to determine whether C. concholepas preferred shaded or illuminated microhabitats. Moreover, we compared the abundance of juveniles collected during day- and night-time hours. The laboratory experiments demonstrated that juveniles of C. concholepas seek out and choose their prey more efficiently in darkened areas. White LED illuminated conditions increased righting times and metabolism. Field surveys indicated that, during daylight hours, juveniles were more abundant in shaded micro-habitats than in illuminated ones. However, during darkness hours, individuals were not seen to aggregate in any particular microhabitats. We conclude that the exposure to ALAN might disrupt important behavioral and physiological traits of small juveniles in this species which, as a mechanism to avoid visual predators, are mainly active at night. It follows that ALAN in coastal areas might modify the entire community structure of intertidal habitats by altering the behavior of this keystone species.

Ocean Acidification and Increased Temperature Have Both Positive and Negative Effects on Early Ontogenetic Traits of a Rocky Shore Keystone Predator Species.

The combined effect of ocean acidification and warming is expected to have significant effects on several traits of marine organisms. The gastropod Concholepas concholepas is a rocky shore keystone predator characteristic of the south-eastern Pacific coast of South America and an important natural resource exploited by small-scale artisanal fishermen along the coast of Chile and Peru. In this study, we used small juveniles of C. concholepas collected from the rocky intertidal habitats of southern Chile (39 °S) to evaluate under laboratory conditions the potential consequences of projected near-future levels of ocean acidification and warming for important early ontogenetic traits. The individuals were exposed long-term (5.8 months) to contrasting pCO2 (ca. 500 and 1400 µatm) and temperature (15 and 19 °C) levels. After this period we compared body growth traits, dislodgement resistance, predator-escape response, self-righting and metabolic rates. With respect to these traits there was no evidence of a synergistic interaction between pCO2 and temperature. Shell growth was negatively affected by high pCO2 levels only at 15 °C. High pCO2 levels also had a negative effect on the predator-escape response. Conversely, dislodgement resistance and self-righting were positively affected by high pCO2 levels at both temperatures. High tenacity and fast self-righting would reduce predation risk in nature and might compensate for the negative effects of high pCO2 levels on other important defensive traits such as shell size and escape behaviour. We conclude that climate change might produce in C. concholepas positive and negative effects in physiology and behaviour. In fact, some of the behavioural responses might be a consequence of physiological effects, such as changes in chemosensory capacity (e.g. predator-escape response) or secretion of adhesive mucous (e.g. dislodgement resistance). Moreover, we conclude that positive behavioural responses may assist in the adaptation to negative physiological impacts, and that this may also be the case for other benthic organisms.

Rocky intertidal zonation pattern in Antofagasta, chile: invasive species and shellfish gathering.

BACKGROUND: Biological invasions affecting rocky intertidal zonation patterns, yield information on species interactions. In the Bay of Antofagasta, northern Chile, the non-indigenous tunicate Pyura praeputialis, originally from Australia, has invaded (in the past century or so) and monopolized a major portion of the mid-intertidal rocky shore, displacing upshore the native mussel Perumytilus purpuratus. In Antofagasta the tunicate is subjected to intensive exploitation. Monitoring protocols show that in the past 10 years Antofagasta's tunicate population has experienced a drastic decline, affecting the intertidal zonation pattern. METHODOLOGY/PRINCIPAL FINDINGS: A 12.5 km of coastline, on the southern eastern shore of the Bay of Antofagasta, was studied. Eight sites were systematically (1993-1994) or sporadically (2003-2014) monitored for the seaward-shoreward expansion or reduction of the tunicate Pyura praeputialis, and native mussel and barnacle bands. A notable reduction in the mid-intertidal band of P. praeputialis and a seaward expansion of the mussel, Perumytilus purpuratus, and barnacle bands was observed. We suggest that the major cause for the decline in the tunicate is due to its intensive exploitation by rocky shore Pyura-gathers. The rate of extraction of tunicates by professional Pyura-gathers ranged between 256-740 tunicates hour-(1). Between 2009-2014 the density of professional Pyura-gather ranged between 0.5-4.5 km(-1) per low tide. Hence, 10 professional Pyura-gathers working 1 h for 10 low tides per month, during 6 months, will remove between 307-888 m(2) of tunicates. A drastic decline in tunicate recruitment was observed and several P. praeputialis ecosystems services have been lost. CONCLUSION AND SIGNIFICANCE: In Antofagasta, the continuous and intensive intertidal gathering of the invasive tunicate Pyura praeputialis, has caused a drastic reduction of its population modifying the zonation pattern. Thereby, native mussel Perumytilus purpuratus has regained its ecological center in the intertidal zone. We recorded a Pyura recruitment failure and loss of ecosystem services.

Ocean acidification disrupts prey responses to predator cues but not net prey shell growth in Concholepas concholepas (loco).

BACKGROUND: Most research on Ocean Acidification (OA) has largely focused on the process of calcification and the physiological trade-offs employed by calcifying organisms to support the building of calcium carbonate structures. However, there is growing evidence that OA can also impact upon other key biological processes such as survival, growth and behaviour. On wave-swept rocky shores the ability of gastropods to self-right after dislodgement, and rapidly return to normal orientation, reduces the risk of predation. METHODOLOGY/PRINCIPAL FINDINGS: The impacts of OA on this self-righting behaviour and other important parameters such as growth, survival, shell dissolution and shell deposition in Concholepas concholepas (loco) were investigated under contrasting pCO2 levels. Although no impacts of OA on either growth or net shell calcification were found, the results did show that OA can significantly affect self-righting behaviour during the early ontogeny of this species with significantly faster righting times recorded for individuals of C. concholepas reared under increased average pCO2 concentrations (± SE) (716 ± 12 and 1036 ± 14 µatm CO2) compared to those reared at concentrations equivalent to those presently found in the surface ocean (388 ± 8 µatm CO2). When loco were also exposed to the predatory crab Acanthocyclus hassleri, righting times were again increased by exposure to elevated CO2, although self-righting times were generally twice as fast as those observed in the absence of the crab. CONCLUSIONS AND SIGNIFICANCE: These results suggest that self-righting in the early ontogeny of C. concholepas will be positively affected by pCO2 levels expected by the end of the 21st century and beginning of the next one. However, as the rate of self-righting is an adaptive trait evolved to reduce lethal predatory attacks, our result also suggest that OA may disrupt prey responses to predators in nature.

Adaptive shell color plasticity during the early ontogeny of an intertidal keystone snail.

We report a mechanism of crypsis present during the vulnerable early post-metamorphic ontogeny (95%) of specimens bearing patterns of shell coloration (dark or light colored) that matched the background coloration provided by patches of Concholepas' most abundant prey (mussels or barnacles respectively). The variation in shell color was positively associated with the color of the most common prey (r = 0.99). In laboratory experiments, shell coloration of C. concholepas depended on the prey-substrate used to induce metamorphosis and for the post-metamorphic rearing. The snail shell color matched the color of the prey offered during rearing. Laboratory manipulation experiments, switching the prey during rearing, showed a corresponding change in snail shell color along the outermost shell edge. As individuals grew and became increasingly indistinguishable from the surrounding background, cryptic individuals had higher survival (71%) than the non cryptic ones (4%) when they were reared in the presence of the predatory crab Acanthocyclus hassleri. These results suggest that the evolution of shell color plasticity during the early ontogeny of C. concholepas, depends on the color of the more abundant of the consumed prey available in the natural habitat where settlement has taken place; this in turn has important consequences for their fitness and survivorship in the presence of visual predators.