In this Issue

Aim: Molluscivorous shorebirds supposedly developed their present wintering distribution after the last ice age. Currently, molluscivorous shorebirds are abundant on almost all shores of the world, except for those in the Indo-West Pacific (IWP). Long before shorebirds arrived on the scene, molluscan prey in the IWP evolved strong anti-predation traits in a prolonged evolutionary arms race with durophagous predators including brachyuran crabs. Here, we investigate whether the absence of molluscivorous shorebirds from a site in Oman can be explained by the molluscan community being too well-defended. Location: The intertidal mudflats of Barr Al Hikman, Oman. Methods: Based on samples from 282 locations across the intertidal area the standing stock of the macrozoobenthic community was investigated. By measuring anti-predation traits (burrowing depth, size and strength of armour), the fraction of molluscs available to molluscivorous shorebirds was calculated. Results: Molluscs dominated the macrozoobenthic community at Barr Al Hikman. However, less than 17% of the total molluscan biomass was available to shorebirds. Most molluscs were unavailable either because of their hard-to-crush shells, or because they lived too deeply in the sediment. Repair scars and direct observations confirmed crab predation on molluscs. Although standing stock densities of the Barr Al Hikman molluscs were of the same order of magnitude as at intertidal mudflat areas where molluscivorous shorebirds are abundant, the molluscan biomass available to shorebirds was distinctly lower at Barr Al Hikman. Main conclusions: The established strong molluscan anti-predation traits against crabs precludes molluscan exploitation by shorebirds at Barr Al Hikman. This study exemplifies that dispersal of "novel" predators is hampered in areas where native predators and prey exhibit strongly developed attack and defence mechanisms, and highlights that evolutionary arms races can have consequences for the global distribution of species

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

Facilitation of a tropical seagrass by a chemosymbiotic bivalve increases with environmental stress

Facilitation of foundation species is critical to the structure, function and persistence of ecosystems. Understanding the dependence of the strength of this facilitation on environmental conditions is important for informed ecosystem management and for predicting the impacts of global change. In coastal seagrass habitats, chemosymbiotic lucinid bivalves can facilitate seagrasses by decreasing potentially toxic levels of sulphide in sediment porewater. However, variation in the strength of lucinid–seagrass facilitation with environmental context has not been experimentally investigated. We tested the hypothesis that the presence of the tiger lucine Codakia orbicularis becomes more important to the growth and survival of the seagrass Thalassia testudinum under decreased light availability and increased sulphide stress. In a mesocosm experiment, we reduced average ambient-light to T. testudinum by 64% and/or increased sediment porewater sulphide concentrations by ~200% and compared growth and tissue chemistry of T. testudinum with and without C. orbicularis. We found that T. testudinum was better able to maintain growth under shading and sulphide stress when C. orbicularis was present. C. orbicularis strongly decreased sediment porewater sulphide, an effect that minimized sulphur build-up in seagrass tissue and was likely achieved through bioirrigation as well as chemoautotrophy. The relative effects of C. orbicularis on T. testudinum growth were strongest in the presence of environmental stressors. Synthesis. The strength of lucinid–seagrass facilitation increases under environmental conditions that hinder the ability of seagrass to detoxify sulphide. Our results provide evidence of a potential mechanism by which the spatiotemporal association between lucinids and seagrasses is maintained and support the incorporation of interspecific facilitation into conservation and restoration strategies for foundation species in the face of increasing anthropogenic impact and global change

The interactive role of predation, competition and habitat conditions in structuring an intertidal bivalve population

Habitat characteristics, predation and competition are known to interactively drive population dynamics. Highly complex habitats, for example, may reduce predation and competition, allowing more individuals living together in a certain area. However, the strength and direction of such interactions can differ strongly and are context dependent. Furthermore, as habitat characteristics are rapidly changing due to anthropogenic impacts, it becomes increasingly important to understand such interactions. Here, we studied the interactive effects of predation and competition on common cockle (Cerastoderma edule) recruitment, growth and survival under different habitat characteristics in the Wadden Sea, one of the world's largest intertidal ecosystems. In a predator-exclosure experiment, we manipulated cockle densities (100 vs. 1000 individuals m-2) and shorebird predation at two sites differing in habitat characteristics, namely at the wake of a blue mussel bed (Mytilus edulis) and at an adjacent sandy site. We found that recruitment was higher in the mussel-modified habitat, most likely due to reduction of hydrodynamic stress. Although bird predation strongly reduced recruit density, the combined effects still yielded more recruitment at the vicinity of the mussel bed compared to the sandy area. Furthermore, we found that high cockle densities combined with high densities of other potential prey (i.e. mussels) at the mussel-modified site, mitigated predation effects for adult cockles. Apart from these positive effects on adults, mussel-modified habitat reduced cockle growth, most likely by reducing hydrodynamics in the wake of the mussel bed and by increasing inter-specific competition for food. Our study experimentally underpins the importance of habitat characteristics, competition and predation in interactively structuring intertidal communities

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

Reductions in body size are increasingly being identified as a response to climatewarming. Here we present evidence for a case of such body shrinkage, potentially dueto 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 itshigh-Arctic breeding grounds, produces smaller offspring with shorter bills duringsummers with early snowmelt. This has consequences half a world away at their tropicalwintering grounds, where shorter-billed individuals have reduced survival rates. This isassociated with these molluscivores eating fewer deeply buried bivalve prey and moreshallowly buried seagrass rhizomes. We suggest that seasonal migrants can experiencereduced fitness at one end of their range as a result of a changing climate at theother end

Central-West Siberian-breeding Bar-tailed Godwits (<i>Limosa lapponica</i>) segregate in two morphologically distinct flyway populations

Long-distance migratory species often include multiple breeding populations, with distinct migration routes, wintering areas and annual-cycle timing. Detailed knowledge on population structure and migratory connectivity provides the basis for studies on the evolution of migration strategies and for species conservation. Currently, five subspecies of Bar-tailed Godwits Limosa lapponica have been described. However, with two apparently separate breeding and wintering areas, the taxonomic status of the subspecies L. l. taymyrensis remains unclear. Here we compare taymyrensis Bar-tailed Godwits wintering in the Middle East and West Africa, respectively, with respect to migration behaviour, breeding area, morphology and population genetic differentation in mitochondrial DNA. By tracking 52 individuals from wintering and staging areas over multiple years, we show that Bar-tailed Godwits wintering in the Middle East bred on the northern West-Siberian Plain (n = 19), while birds from West Africa bred further east, mostly on the Taimyr Peninsula (n = 12). The two groups differed significantly in body size and shape, and also in the timing of both northward and southward migrations. However, they were not genetically differentiated, indicating that the phenotypic (i.e. geographical, morphological and phenological) differences arose either very recently or without current reproductive isolation. We conclude that the taymyrensis taxon consists of two distinct populations with mostly non-overlapping flyways, which warrant treatment as separate taxonomic units. We propose to distinguish a more narrowly defined taymyrensis subspecies (i.e. the Bar-tailed Godwits wintering in West Africa and breeding on Taimyr), from a new subspecies (i.e. the birds wintering in the Middle East and breeding on the northern West-Siberian Plain)

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

Drought, mutualism breakdown, and landscape-scale degradation of seagrass beds

In many marine ecosystems, biodiversity critically depends on foundation species such as corals and seagrasses that engage in mutualistic interactions [1-3]. Concerns grow that environmental disruption of marine mutualisms exacerbates ecosystem degradation, with breakdown of the obligate coral mutualism ("coral bleaching") being an iconic example [2, 4, 5]. However, as these mutualisms are mostly facultative rather than obligate, it remains unclear whether mutualism breakdown is a common risk in marine ecosystems, and thus a potential accelerator of ecosystem degradation. Here, we provide evidence that drought triggered landscape-scale seagrass degradation and show the consequent failure of a facultative mutualistic feedback between seagrass and sulfide-consuming lucinid bivalves that in turn appeared to exacerbate the observed collapse. Local climate and remote sensing analyses revealed seagrass collapse after a summer with intense low-tide drought stress. Potential analysis-a novel approach to detect feedback-mediated state shifts-revealed two attractors (healthy and degraded states) during the collapse, suggesting that the drought disrupted internal feedbacks to cause abrupt, patch-wise degradation. Field measurements comparing degraded patches that were healthy before the collapse with patches that remained healthy demonstrated that bivalves declined dramatically in degrading patches with associated high sediment sulfide concentrations, confirming the breakdown of the mutualistic seagrass-lucinid feedback. Our findings indicate that drought triggered mutualism breakdown, resulting in toxic sulfide concentrations that aggravated seagrass degradation. We conclude that external disturbances can cause sudden breakdown of facultative marine mutualistic feedbacks. As this may amplify ecosystem degradation, we suggest including mutualisms in marine conservation and restoration approaches

Bottom-up and top-down forces in a tropical intertidal ecosystem: The interplay between seagrasses, bivalves and birds

Zeegrassen zijn zogenaamde ‘biobouwers’ en zijn de basis voor veel kustecosystemen. Het Waddengebied Banc d’Arguin is zo’n kustgebied. Het zeegras Zostera noltii hier barst van het leven waar o.a. de kanoet (Calidris canutus canutus) van leeft. Zeegrassen hebben een belangrijke sturende rol als fundering van onderuit het ecosysteem (bottom-up). Ze creëren geschikte leefomstandigheden voor zichzelf én voor veel andere soorten. Zeegrasvelden die cruciaal zijn voor de biodiversiteit en kustbescherming worden echter op een onverwachte manier bedreigd door klimaatverandering. Door droogte en hittegolven stopt zeegras met het leveren van zuurstof aan schelpdieren (Loripes lucinalis) die samenleven met sulfide-etende bacteriën. Hierdoor sterven de schelpdieren en hun bacteriën, waarna ophopend sulfide in de zeebodem het zeegras vergiftigt. Kanoeten beschikken over een uniek zintuig in het puntje van hun snavel waarmee ze efficiënt prooien kunnen detecteren zonder direct contact. Men zou verwachten dat kanoeten in staat zouden moeten zijn om Loripes weg te eten. Maar wat blijkt in hoge zeegras dichtheden verbergt zeegras indirect zijn detoxificerende schelp. In combinatie met de toxiciteit van de schelpen voorkomt dit een sterke doorwerking op het systeem van bovenaf (top-down). Een computer model liet zien dat de stabiliseerde werking van het mutualisme weldegelijk kon worden verstoord door kanoeten. Het model liet zien dat in afstervend zeegras kanoeten mogelijk in staat waren om het afsterf proces te versnellen. Door hier de resterende Loripes weg te eten nam het giftige sulfide toe. Daarom kunnen we concluderen dat het top-down effect van kanoeten waarschijnlijk een cumulatief effect is wat het afsterven van het zeegras doet versnellen