Ecophysiological and behavioural response of juveniles of the Chilean cold-water coral Caryophyllia (Caryophyllia) huinayensis to increasing sediment loads.

Chilean Patagonia is a hotspot of biodiversity, harbouring cold-water corals (CWCs) that populate steep walls and overhangs of fjords and channels. Through anthropogenic activities such as deforestation, roadworks, aquafarming and increased landslide frequency, sediment input increases in the fjord region. While the absence of CWCs on moderately steep slopes has been suggested to reflect high vulnerability to sedimentation, experimental evidence has been lacking. Here, we investigated the sensitivity of CWCs to sediment stress, using juvenile Caryophyllia (Caryophyllia) huinayensis as a model. A 12-week aquarium experiment was conducted with three sediment loads: the average natural sediment concentration in Comau Fjord, 100- and 1000-fold higher sediment levels, expected from gravel road use and coastal erosion. Changes in coral mass and calyx dimensions, polyp expansion, tissue retraction and respiration were measured. For CWCs exposed to two and three order of magnitude higher sediment concentrations, 32% and 80% of the animals experienced a decrease in tissue cover, respectively, along with a decrease in respiration rate of 34% and 66%. Under the highest concentration corals showed reduced polyp expansion and a significantly reduced growth of ~ 95% compared to corals at natural concentration. The results show that C. huinayensis is affected by high sediment loads. As human activities that increase sedimentation steadily intensify, coastal planners need to consider detrimental effects on CWCs.

Life cycle of the cold-water coral Caryophyllia huinayensis.

Little is known about the biology of cold-water corals (CWCs), let alone the reproduction and early life stages of these important deep-sea foundation species. Through a three-year aquarium experiment, we described the reproductive mode, larval release periodicity, planktonic stage, larval histology, metamorphosis and post-larval development of the solitary scleractinian CWC Caryophyllia (Caryophyllia) huinayensis collected in Comau Fjord, Chilean Patagonia. We found that C. huinayensis is a brooder releasing 78.4 ± 65.9 (mean ± standard deviation [SD]) planula larvae throughout the year, a possible adaptation to low seasonality. Planulae had a length of 905 ± 114 µm and showed a well-developed gastrovascular system. After 8 ± 9.3 days (d), the larvae settled, underwent metamorphosis and developed the first set of tentacles after 2 ± 1.5 d. Skeletogenesis, zooplankton feeding and initiation of the fourth set of tentacles started 5 ± 2.1 d later, 21 ± 12.9 d, and 895 ± 45.9 d after settlement, respectively. Our study shows that the ontogenetic timing of C. huinayensis is comparable to that of some tropical corals, despite lacking zooxanthellae.

The shrunk genetic diversity of coral populations in North-Central Patagonia calls for management and conservation plans for marine resources.

The Chilean Patagonia is a complex puzzle of numerous fjords, channels, bays, estuaries, and islands. The largest part of it is very remote, hampering the generation of scientific knowledge and effective management planning that could balance conservation of the marine resources with the increasing development of aquaculture activities. The present study focuses on the deep-water emergent cold-water coral Desmophyllum dianthus, dwelling in Chilean Patagonia, with the aim to illustrate its population genetic structure, demography and adaptation of the species along this coast. Microsatellite loci analysis included D. dianthus individuals from twelve sampling localities along bathymetric and oceanographic gradients from the latitude 40°S to 48°S. The results showed a lack of genetic structure with an asymmetric dispersion of individuals, and relevant heterozygosity deficiency in some populations. This study also analyses the natural and human impacts affecting the region (e.g., climate change, increasing salmon farming activities), and stresses the importance of including genetic information in the process of management and conservation of marine resources. In particular, the relevance of using interdisciplinary approaches to fill the gaps in scientific knowledge especially in remote and pristine areas of western Patagonia. Therefore, information on genetic spatial distribution of marine fauna could become pivotal to develop a holistic ecosystem-based approach for marine spatial planning.

Environmental stability and phenotypic plasticity benefit the cold-water coral Desmophyllum dianthus in an acidified fjord.

The stratified Chilean Comau Fjord sustains a dense population of the cold-water coral (CWC) Desmophyllum dianthus in aragonite supersaturated shallow and aragonite undersaturated deep water. This provides a rare opportunity to evaluate CWC fitness trade-offs in response to physico-chemical drivers and their variability. Here, we combined year-long reciprocal transplantation experiments along natural oceanographic gradients with an in situ assessment of CWC fitness. Following transplantation, corals acclimated fast to the novel environment with no discernible difference between native and novel (i.e. cross-transplanted) corals, demonstrating high phenotypic plasticity. Surprisingly, corals exposed to lowest aragonite saturation (Ωarag < 1) and temperature (T < 12.0 °C), but stable environmental conditions, at the deep station grew fastest and expressed the fittest phenotype. We found an inverse relationship between CWC fitness and environmental variability and propose to consider the high frequency fluctuations of abiotic and biotic factors to better predict the future of CWCs in a changing ocean.

Seasonal and diel variations in the vertical distribution, composition, abundance and biomass of zooplankton in a deep Chilean Patagonian Fjord.

Comau Fjord is a stratified Chilean Patagonian Fjord characterized by a shallow brackish surface layer and a >400 m layer of aragonite-depleted subsurface waters. Despite the energetic burden of low aragonite saturation levels to calcification, Comau Fjord harbours dense populations of cold-water corals (CWC). While this paradox has been attributed to a rich supply of zooplankton, supporting abundance and biomass data are so far lacking. In this study, we investigated the seasonal and diel changes of the zooplankton community over the entire water column. We used a Nansen net (100 µm mesh) to take stratified vertical hauls between the surface and the bottom (0-50-100-200-300-400-450 m). Samples were scanned with a ZooScan, and abundance, biovolume and biomass were determined for 41 taxa identified on the web-based platform EcoTaxa 2.0. Zooplankton biomass was the highest in summer (209 g dry mass m-2) and the lowest in winter (61 g dry mass m-2). Abundance, however, peaked in spring, suggesting a close correspondence between reproduction and phytoplankton spring blooms (Chl a max. 50.86 mg m-3, 3 m depth). Overall, copepods were the most important group of the total zooplankton community, both in abundance (64-81%) and biovolume (20-70%) followed by mysids and chaetognaths (in terms of biovolume and biomass), and nauplii and Appendicularia (in terms of abundance). Throughout the year, diel changes in the vertical distribution of biomass were found with a daytime maximum in the 100-200 m depth layer and a nighttime maximum in surface waters (0-50 m), associated with the diel vertical migration of the calanoid copepod family Metridinidae. Diel differences in integrated zooplankton abundance, biovolume and biomass were probably due to a high zooplankton patchiness driven by biological processes (e.g., diel vertical migration or predation avoidance), and oceanographic processes (estuarine circulation, tidal mixing or water column stratification). Those factors are considered to be the main drivers of the zooplankton vertical distribution in Comau Fjord.

The carbon and nitrogen budget of Desmophyllum dianthus-a voracious cold-water coral thriving in an acidified Patagonian fjord.

In the North Patagonian fjord region, the cold-water coral (CWC) Desmophyllum dianthus occurs in high densities, in spite of low pH and aragonite saturation. If and how these conditions affect the energy demand of the corals is so far unknown. In a laboratory experiment, we investigated the carbon and nitrogen (C, N) budget of D. dianthus from Comau Fjord under three feeding scenarios: (1) live fjord zooplankton (100-2,300 µm), (2) live fjord zooplankton plus krill (>7 mm), and (3) four-day food deprivation. In closed incubations, C and N budgets were derived from the difference between C and N uptake during feeding and subsequent C and N loss through respiration, ammonium excretion, release of particulate organic carbon and nitrogen (POC, PON). Additional feeding with krill significantly increased coral respiration (35%), excretion (131%), and POC release (67%) compared to feeding on zooplankton only. Nevertheless, the higher C and N losses were overcompensated by the threefold higher C and N uptake, indicating a high assimilation and growth efficiency for the krill plus zooplankton diet. In contrast, short food deprivation caused a substantial reduction in respiration (59%), excretion (54%), release of POC (73%) and PON (87%) compared to feeding on zooplankton, suggesting a high potential to acclimatize to food scarcity (e.g., in winter). Notwithstanding, unfed corals 'lost' 2% of their tissue-C and 1.2% of their tissue-N per day in terms of metabolism and released particulate organic matter (likely mucus). To balance the C (N) losses, each D. dianthus polyp has to consume around 700 (400) zooplankters per day. The capture of a single, large krill individual, however, provides enough C and N to compensate daily C and N losses and grow tissue reserves, suggesting that krill plays an important nutritional role for the fjord corals. Efficient krill and zooplankton capture, as well as dietary and metabolic flexibility, may enable D. dianthus to thrive under adverse environmental conditions in its fjord habitat; however, it is not known how combined anthropogenic warming, acidification and eutrophication jeopardize the energy balance of this important habitat-building species.

Effects of low pH and feeding on calcification rates of the cold-water coral Desmophyllum dianthus.

Cold-Water Corals (CWCs), and most marine calcifiers, are especially threatened by ocean acidification (OA) and the decrease in the carbonate saturation state of seawater. The vulnerability of these organisms, however, also involves other global stressors like warming, deoxygenation or changes in sea surface productivity and, hence, food supply via the downward transport of organic matter to the deep ocean. This study examined the response of the CWC Desmophyllum dianthus to low pH under different feeding regimes through a long-term incubation experiment. For this experiment, 152 polyps were incubated at pH 8.1, 7.8, 7.5 and 7.2 and two feeding regimes for 14 months. Mean calcification rates over the entire duration of the experiment ranged between -0.3 and 0.3 mg CaCO3 g-1d-1. Polyps incubated at pH 7.2 were the most affected and 30% mortality was observed in this treatment. In addition, many of the surviving polyps at pH 7.2 showed negative calcification rates indicating that, in the long term, CWCs may have difficulty thriving in such aragonite undersaturated waters. The feeding regime had a significant effect on skeletal growth of corals, with high feeding frequency resulting in more positive and variable calcification rates. This was especially evident in corals reared at pH 7.5 (ΩA = 0.8) compared to the low frequency feeding treatment. Early life-stages, which are essential for the recruitment and maintenance of coral communities and their associated biodiversity, were revealed to be at highest risk. Overall, this study demonstrates the vulnerability of D. dianthus corals to low pH and low food availability. Future projected pH decreases and related changes in zooplankton communities may potentially compromise the viability of CWC populations.

Largest baleen whale mass mortality during strong El Niño event is likely related to harmful toxic algal bloom.

While large mass mortality events (MMEs) are well known for toothed whales, they have been rare in baleen whales due to their less gregarious behavior. Although in most cases the cause of mortality has not been conclusively identified, some baleen whale mortality events have been linked to bio-oceanographic conditions, such as harmful algal blooms (HABs). In Southern Chile, HABs can be triggered by the ocean-atmosphere phenomenon El Niño. The frequency of the strongest El Niño events is increasing due to climate change. In March 2015, by far the largest reported mass mortality of baleen whales took place in a gulf in Southern Chile. Here, we show that the synchronous death of at least 343, primarily sei whales can be attributed to HABs during a building El Niño. Although considered an oceanic species, the sei whales died while feeding near to shore in previously unknown large aggregations. This provides evidence of new feeding grounds for the species. The combination of older and newer remains of whales in the same area indicate that MMEs have occurred more than once in recent years. Large HABs and reports of marine mammal MMEs along the Northeast Pacific coast may indicate similar processes in both hemispheres. Increasing MMEs through HABs may become a serious concern in the conservation of endangered whale species.

Global conservation outcomes depend on marine protected areas with five key features.

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km(2)), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.