Coral reefs of the Florida Keys typically experience seasonal temperatures of 20-31°C. Deviation outside this range causes physiological impairment of reef-building corals, potentially leading to coral colony death. In January and February 2010, two closely spaced cold fronts, possibly driven by an unusually extreme Arctic Oscillation, caused sudden and severe seawater temperature declines in the Florida Keys. Inshore coral reefs [e.g., Admiral Reef (ADM)] experienced lower sustained temperatures (i.e., < 12°C) than those further offshore [e.g., Little Grecian Reef (LG), minimum temperature = 17.2°C]. During February and March 2010, we surveyed ADM and observed a mass die-off of reef-building corals, whereas 12 km away LG did not exhibit coral mortality. We subsequently measured the physiological effects of low-temperature stress on three common reef-building corals (i.e., Montastraea faveolata, Porites astreoides, and Siderastrea siderea) over a range of temperatures that replicated the inshore cold-water anomaly (i.e., from 20 to 16 to 12°C and back to 20°C). Throughout the temperature modulations, coral respiration as well as endosymbiont gross photosynthesis and maximum quantum efficiency of photosystem II were measured. In addition, Symbiodinium genotypic identity, cell densities, and chlorophyll a content were determined at the beginning and conclusion of the experiment. All corals were significantly affected at 12°C, but species-specific physiological responses were found indicating different coral and/or Symbiodinium cold tolerances. Montastraea faveolata and P. astreoides appeared to be most negatively impacted because, upon return to 20°C, significant reductions in gross photosynthesis and dark respiration persisted. Siderastrea siderea, however, readily recovered to pre-treatment rates of dark respiration and gross photosynthesis. Visual surveys of inshore reefs corroborated these results, with S. siderea being minimally affected by the cold-water anomaly, whereas M. faveolata and P. astreoides exhibited nearly 100% mortality. This study highlights the importance of understanding the physiological attributes of genotypically distinct coral-Symbiodinium symbioses that contribute to tolerance, recovery, and consequences to an environmental perturbation. These data also document effects of a rarely studied environmental stressor, possibly initiated by remote global climate events, on coral-Symbiodinium symbioses and coral reef communities.
The flight behaviour of Griffon Vultures Gyps fulvus was studied at a major migration bottleneck, the Strait of Gibraltar in southernmost Spain, during the autumns of 2004 to 2007. The 14‐km‐wide sea channel significantly impeded the southern migration of the species into Africa, with many birds attempting repeated passage for weeks before crossing, and others not crossing at all and overwintering in Southern Spain. Water‐crossing attempts were restricted to times between 11:00 and 14:00 h on days with light or variable winds, or on days with strong winds from the north or west. No crossing attempts were made on days with strong winds from the south or east. Vultures attempted to cross the Strait in large flocks and never attempted to do so alone. Although 29% of the birds soared during crossing attempts, at least until they flew beyond visible range of approximately 4 km, most engaged in considerable flapping flight when attempting to cross. Overall, birds flying over water flapped more than 10 times as frequently as those flying over land prior to crossing attempts. Vultures did not flap continuously, but intermittently in brief bouts of flapping interspersed with periods of gliding or soaring flight. The number of flaps per bout over water was significantly greater than the number of flaps per bout over land. Vultures flying over water that flapped at rates of 20 flaps or more per minute typically aborted attempted crossings and returned to Spain in intermittent flapping and gliding flight. There are numerous reports of Vultures falling into the Strait and drowning while attempting to cross, as well as reports of returning Vultures collapsing on the beach having reached Spain in spring (Barrios Partida 2006). Our observations indicate that passage of Griffon Vultures at the Strait of Gibraltar is limited by the species’ over‐water flapping‐flight abilities, including its inability to flap continuously for even short periods of time. We suggest that even relatively short sea crossings represent significant obstacles to migrating Vultures and discuss the implications of this limitation on the distribution and abundance of the species.
Predicting how combinations of stressors will affect failure risk is a key challenge for the field of ecomechanics and, more generally, ecophysiology. Environmental conditions often influence the manufacture and durability of biomaterials, inducing structural failure that potentially compromises organismal reproduction, growth, and survival. Species known for tight linkages between structural integrity and survival include bivalve mussels, which produce numerous byssal threads to attach to hard substrate. Among the current environmental threats to marine organisms are ocean warming and acidification. Elevated pCO2 exposure is known to weaken byssal threads by compromising the strength of the adhesive plaque. This study uses structural analysis to evaluate how an additional stressor, elevated temperature, influences byssal thread quality and production. Mussels (Mytilus trossulus) were placed in controlled temperature and pCO2 treatments, and then, newly produced threads were counted and pulled to failure to determine byssus strength. The effects of elevated temperature on mussel attachment were dramatic; mussels produced 60% weaker and 65% fewer threads at 25°C in comparison to 10°C. These effects combine to weaken overall attachment by 64–88% at 25°C. The magnitude of the effect of pCO2 on thread strength was substantially lower than that of temperature and, contrary to our expectations, positive at high pCO2 exposure. Failure mode analysis localized the effect of temperature to the proximal region of the thread, whereas pCO2 affected only the adhesive plaques. The two stressors therefore act independently, and because their respective target regions are interconnected (resisting tension in series), their combined effects on thread strength are exactly equal to the effect of the strongest stressor. Altogether, these results show that mussels, and the coastal communities they support, may be more vulnerable to the negative effects of ocean warming than ocean acidification.
Ocean acidification lowers the saturation state of calcium carbonate, decreasing net calcification and compromising the skeletons of organisms such as corals, molluscs and algae. These calcified structures can protect organisms from predation and improve access to light, nutrients and dispersive currents. While some species (such as urchins, corals and mussels) survive with decreased calcification, they can suffer from inferior mechanical performance. Here, we used cantilever beam theory to test the hypothesis that decreased calcification would impair the mechanical performance of the green alga Acetabularia acetabulum along a CO 2 gradient created by volcanic seeps off Vulcano, Italy. Calcification and mechanical properties declined as calcium carbonate saturation fell; algae at 2283 matm CO 2 were 32% less calcified, 40% less stiff and 40% droopier. Moreover, calcification was not a linear proxy for mechanical performance; stem stiffness decreased exponentially with reduced calcification. Although calcifying organisms can tolerate high CO 2 conditions, even subtle changes in calcification can cause dramatic changes in skeletal performance, which may in turn affect key biotic and abiotic interactions.
The biomechanics of specialized mechanical structures produced by organisms provides crucial fitness advantages. The energetic cost associated with producing these structural materials and the resulting energetic trade‐off with growth, however, is rarely quantified. We integrate resource allocation to structural material production with an energetic framework by combining an experimental manipulation with an energetic model. Mytilid bivalves produce byssus, a network of collagen‐like threads that tethers individuals to hard substrate. We hypothesized that a manipulation that induces the production of more byssal threads would result in increased energetic cost and decreased growth of the species Mytilus trossulus. In month‐long field experiments in spring and autumn, we severed byssal threads across a range of frequencies (never, weekly, daily), and measured shell and tissue growth. We then quantified the costs associated with the production of byssal threads using a Scope for Growth model. We found that byssal thread removal increased byssal thread production and decreased growth. The cost calculated per byssal thread was similar in the spring and autumn (~1 J/thread), but energy budget calculations differed by season, and depended on thread quantity and seasonal differences in assumptions of metabolic costs. This work demonstrates that the cost of producing a structural material has a substantial effect on mussel energetic state. The energetic cost of producing byssal threads was 2%–8% percent of the energy budget in control groups that had low byssal thread production, and increased six to 11‐fold (up to 47%) in mussels induced to produce threads daily. We propose that characterizing the trade‐off between the cost of biomaterial production and growth has implications for understanding the role of trade‐offs in adaptive evolution, and improved natural resource management and conservation practices. A free Plain Language Summary can be found within the Supporting Information of this article.
Synopsis Organisms rely on the integrity of the structural materials they produce to maintain a broad range of processes, such as acquiring food, resisting predators, or withstanding extreme environmental forces. The production and maintenance of these biomaterials, which are often modulated by environmental conditions, can therefore have important consequences for fitness in changing climates. One well-known example of such a biomaterial is mussel byssus, an array of collagen-like fibers (byssal threads) that tethers a bivalve mollusk securely to benthic marine substrates. Byssus strength directly influences mortality from dislodgement, predation, or competition and depends on the quantity and quality of byssal threads produced. We compared the temperature sensitivity of byssal attachment strength of two mussel species common to the west coast of North America, Mytilus trossulus and M. galloprovincialis, when exposed to seawater temperatures ranging from 10 to 24°C in the laboratory. We found that the two species attached equally strong in seawater ≤18°C, but higher temperatures caused byssal thread production rate and quality (break force and extensibility) to be greatly reduced in M. trossulus and increased in M. galloprovincialis, leading to a 2–10-fold difference in overall byssus strength between the two species. Using this threshold value (18°C), we mapped habitat for each species along the west coast of North America based on annual patterns in sea surface temperature. Estimated ranges are consistent with the current distribution of the two species and suggest a potential mechanism by which ocean warming could facilitate the northern expansion of M. galloprovincialis and displacement of native M. trossulus populations.
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