Jimmy de Fouw

A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems

Ancient Associations Submarine seagrass meadows are critical to fisheries and coastline protection and provide feeding grounds for many endangered species, including dugongs and turtles, and serve as a nursery for coral reef fish. The persistence and maintenance of seagrass ecosystems have been mysterious, because accumulation of organic matter in the beds should rapidly lead to toxic sulphide levels in the sediment. Using a meta-analysis and a field study, van der Heide et al. (p. 1432) atttribute the 100-million-year success of seagrasses to a three-stage symbiosis. Seagrass beds worldwide contain high densities of small lucinid bivalves that have symbiotic sulphide-oxidizing bacteria in their gills. This association appears to relieve any sulphide stress for seagrasses, while the lucinids and their symbionts profit from the accumulation of degradable organic matter and oxygen release from seagrass roots. A marine plant, small molluscs, and their resident sulfide-oxidizing bacteria survive together. Seagrasses evolved from terrestrial plants into marine foundation species around 100 million years ago. Their ecological success, however, remains a mystery because natural organic matter accumulation within the beds should result in toxic sediment sulfide levels. Using a meta-analysis, a field study, and a laboratory experiment, we reveal how an ancient three-stage symbiosis between seagrass, lucinid bivalves, and their sulfide-oxidizing gill bacteria reduces sulfide stress for seagrasses. We found that the bivalve–sulfide-oxidizer symbiosis reduced sulfide levels and enhanced seagrass production as measured in biomass. In turn, the bivalves and their endosymbionts profit from organic matter accumulation and radial oxygen release from the seagrass roots. These findings elucidate the long-term success of seagrasses in warm waters and offer new prospects for seagrass ecosystem conservation.

Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range

Consequences conferred at a distance Migratory animals have adapted to life in multiple, sometimes very different environments. Thus, they may show particularly complex responses as climates rapidly change. Van Gils et al. show that body size in red knot birds has been decreasing as their Arctic breeding ground warms (see the Perspective by Wikelski and Tertitski). However, the real toll of this change appears not in the rapidly changing northern part of their range but in the apparently more stable tropical wintering range. The resulting smaller, short-billed birds have difficulty reaching their major food source, deeply buried mollusks, which decreases the survival of birds born during particularly warm years. Science, this issue p. 819; see also p. 775 A warming Arctic decreases the fitness of migratory red knots in their distant wintering range. Reductions in body size are increasingly being identified as a response to climate warming. Here we present evidence for a case of such body shrinkage, potentially due to malnutrition in early life. We show that an avian long-distance migrant (red knot, Calidris canutus canutus), which is experiencing globally unrivaled warming rates at its high-Arctic breeding grounds, produces smaller offspring with shorter bills during summers with early snowmelt. This has consequences half a world away at their tropical wintering grounds, where shorter-billed individuals have reduced survival rates. This is associated with these molluscivores eating fewer deeply buried bivalve prey and more shallowly buried seagrass rhizomes. We suggest that seasonal migrants can experience reduced fitness at one end of their range as a result of a changing climate at the other end.

Climate change and the increasing impact of polar bears on bird populations

The Arctic is becoming warmer at a high rate, and contractions in the extent of sea ice are currently changing the habitats of marine top-predators dependent on ice. Polar bears (Ursus maritimus) depend on sea ice for hunting seals. For these top-predators, longer ice-free seasons are hypothesized to force the bears to hunt for alternative terrestrial food, such as eggs from colonial breeding birds. We analyzed time-series of polar bear observations at four locations on Spitsbergen (Svalbard) and one in east Greenland. Summer occurrence of polar bears, measured as the probability of encountering bears and the number of days with bear presence, has increased significantly from the 1970/80s to the present. The shifts in polar bear occurrence coincided with trends for shorter sea ice seasons and less sea ice during the spring in the study area. This resulted in a strong inverse relationship between the probability of bear encounters on land and the length of the sea ice season. Within, 10 years after their first appearance on land, polar bears had advanced their arrival dates by almost 30 days. Direct observations of nest predation showed that polar bears may severely affect reproductive success of the barnacle goose (Branta leucopsis), common eider (Somateria mollissima) and glaucous gull (Larus hyperboreus). Nest predation was strongest in years when the polar bears arrived well before hatch, with more than 90% of all nests being predated. The results are similar to findings from Canada, and large-scale processes, such as climate and subsequent habitat changes, are pinpointed as the most likely drivers in various parts of the Arctic. We suggest that the increasing, earlier appearance of bears on land in summer reflects behavioral adaptations by a small segment of the population to cope with a reduced hunting range on sea ice. This exemplifies how behavioral adaptations may contribute to the cascading effects of climate change.

Digestive capacity and toxicity cause mixed diets in red knots that maximize energy intake rate.

Among energy-maximizing animals, preferences for different prey can be explained by ranking the prey according to their energetic content. However, diet choice also depends on characteristics of the predator, such as the need to ingest necessary nutrients and the constraints imposed by digestion and toxins in food. In combination, these factors can lead to mixed diets in which the energetically most profitable food is not eaten exclusively even when it is abundant. We studied diet choice in red knots (Calidris canutus canutus) feeding on mollusks at a West African wintering site. At this site, the birds fed primarily on two species of bivalves, a thick-shelled one (Dosinia isocardia) that imposed a digestive constraint and a thin-shelled one (Loripes lucinalis) that imposed a toxin constraint. The latter species is toxic due to its symbiotic association with sulfide-oxidizing bacteria. We estimated experimentally the parameters of a linear programming model that includes both digestive and toxin constraints, leading to the prediction that red knots should eat a mixture of both mollusk species to maximize energy intake. The model correctly predicted the preferences of the captive birds, which depended on the digestive quality and toxicity of their previous diet. At our study site, energy-maximizing red knots appear to select a mixed diet as a result of the simultaneous effects of digestive and toxin constraints.

A facultative mutualistic feedback enhances the stability of tropical intertidal seagrass beds

Marine foundation species such as corals, seagrasses, salt marsh plants, and mangrove trees are increasingly found to engage in mutualistic interactions. Because mutualisms by their very nature generate a positive feedback between the species, subtle environmental impacts on one of the species involved may trigger mutualism breakdown, potentially leading to ecosystem regime shifts. Using an empirically parameterized model, we investigate a facultative mutualism between seagrass and lucinid bivalves with endosymbiotic sulfide-oxidizing gill bacteria in a tropical intertidal ecosystem. Model predictions for our system show that, by alleviating the build-up of toxic sulfide, this mutualism maintains an otherwise intrinsically unstable seagrass ecosystem. However, an increase in seagrass mortality above natural levels, due to e.g. desiccation stress, triggers mutualism breakdown. This pushes the system in collapse-and-recovery dynamics (‘slow-fast cycles’) characterized by long-term persistent states of bare and seagrass-dominated, with rapid transitions in between. Model results were consistent with remote sensing analyses that suggest feedback-mediated state shifts induced by desiccation. Overall, our combined theoretical and empirical results illustrate the potential of mutualistic feedbacks to stabilize ecosystems, but also reveal an important drawback as small environmental changes may trigger shifts. We therefore suggest that mutualisms should be considered for marine conservation and restoration of seagrass beds.