Environmental context explains Levy and Brownian movement patterns of marine predators

An optimal search theory, the so-called Levy-flight foraging hypothesis(1), predicts that predators should adopt search strategies known as Levy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey(2-4). Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Levy behaviour has recently been questioned(5,6). Consequently, whether foragers exhibit Levy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory's central predictions. Here we use maximum-likelihood methods to test for Levy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Levy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Levy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Levy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Levy-flight foraging hypothesis(1,7), supporting the contention(8,9) that organism search strategies naturally evolved in such a way that they exploit optimal Levy patterns.

Identifying optimal feeding habitat and proposed Marine Protected Areas (pMPAs) for the black-legged kittiwake (Rissa tridactyla) suggests a need for complementary management approaches

Marine Protected Areas (MPAs) are an important conservation tool. For marine predators, recent research has focused on the use of Species Distribution Models (SDMs) to identify proposed sites. We used a maximum entropy modelling approach based on static and dynamic oceanographic parameters to determine optimal feeding habitat for black-legged kittiwakes (Rissa tridactyla) at two colonies during two consecutive breeding seasons (2009 and 2010). A combination of Geographic Positioning System (GPS) loggers and Time-Depth Recorders (TDRs) attributed feeding activity to specific locations. Feeding areas were <30 km from the colony, <40 km from land, in productive waters, 25–175m deep. The predicted extent of optimal habitat declined at both colonies between 2009 and 2010 coincident with declines in reproductive success. Whilst the area of predicted optimal habitat changed, its location was spatially stable between years. There was a close match between observed feeding locations and habitat predicted as optimal at one colony (Lambay Island, Republic of Ireland), but a notable mismatch at the other (Rathlin Island, Northern Ireland). Designation of an MPA at Rathlin may, therefore, be less effective than a similar designation at Lambay perhaps due to the inherent variability in currents and sea state in the North Channel compared to the comparatively stable conditions in the central Irish Sea. Current strategies for designating MPAs do not accommodate likely future redistribution of resources due to climate change. We advocate the development of new approaches including dynamic MPAs that track changes in optimal habitat and non-colony specific ecosystem management.

Validating the use of intrinsic markers in body feathers to identify inter‑individual differences in non‑breeding areas of northern fulmars

Many wildlife studies use chemical analyses to explore spatio-temporal variation in diet, migratory patterns and contaminant exposure. Intrinsic markers are particularly valuable for studying non-breeding marine predators, when direct methods of investigation are rarely feasible. However, any inferences regarding foraging ecology are dependent upon the time scale over which tissues such as feathers are formed. In this study, we validate the use of body feathers for studying non-breeding foraging patterns in a pelagic seabird, the northern fulmar. Analysis of carcasses of successfully breeding adult fulmars indicated that body feathers moulted between September and March, whereas analyses of carcasses and activity patterns suggested that wing feather and tail feather moult occurred during more restricted periods (September to October and September to January, respectively). By randomly sampling relevant body feathers, average values for individual birds were shown to be consistent. We also integrated chemical analyses of body feather with geolocation tracking data to demonstrate that analyses of δ13C and δ15N values successfully assigned 88 % of birds to one of two broad wintering regions used by breeding adult fulmars from a Scottish study colony. These data provide strong support for the use of body feathers as a tool for exploring non-breeding foraging patterns and diet in wide-ranging, pelagic seabirds.

Predatory fish loss affects the structure and functioning of a model marine food web

The rate of species loss is increasing on a global scale and predators are most at risk from human-induced extinction. The effects of losing predators are difficult to predict, even with experimental single species removals, because different combinations of species interact in unpredictable ways. We tested the effects of the loss of groups of common predators on herbivore and algal assemblages in a model benthic marine system. The predator groups were fish, shrimp and crabs. Each group was represented by at least two characteristic species based on data collected at local field sites. We examined the effects of the loss of predators while controlling for the loss of predator biomass. The identity, not the number of predator groups, affected herbivore abundance and assemblage structure. Removing fish led to a large increase in the abundance of dominant herbivores, such as Ampithoids and Caprellids. Predator identity also affected algal assemblage structure. It did not, however, affect total algal mass. Removing fish led to an increase in the final biomass of the least common taxa (red algae) and reduced the mass of the dominant taxa (brown algae). This compensatory shift in the algal assemblage appeared to facilitate the maintenance of a constant total algal biomass. In the absence of fish, shrimp at higher than ambient densities had a similar effect on herbivore abundance, showing that other groups could partially compensate for the loss of dominant predators. Crabs had no effect on herbivore or algal populations, possibly because they were not at carrying capacity in our experimental system. These findings show that contrary to the assumptions of many food web models, predators cannot be classified into a single functional group and their role in food webs depends on their identity and density in 'real' systems and carrying capacities.

Manipulating Interaction Strengths and the Consequences for Trivariate Patterns in a Marine Food Web

We are experiencing a global extinction crisis as a result of climate change and human-induced alteration of natural habitats, with large predators at high trophic levels in food webs being particularly vulnerable. Unfortunately, there is a scarcity of food web data that can be used to assess how species extinctions alter the structure and stability of temporally and spatially replicated networks. We established a series of large experimental mesocosms in a shallow subtidal benthic marine system and constructed food webs for each replicate. After 6 months of community assembly, we removed large predators from the core communities of 20 experimental food webs, based on the strength of their trophic interactions, and monitored the changes in the networks' structure and stability over an 8-month period. Our analyses revealed the importance of allometric relationships and size-structuring in natural communities as a means of preserving food web structure and sustainability, despite significant changes in the diversity, stability and productivity of the system.

Marine reserve designation, trophic cascades and altered community dynamics

Marine ecosystems and their associated populations are increasingly at risk from the cumulative impacts of many anthropogenic threats that increase the likelihood of species extinction and altered community dynamics. In response, marine reserves can be used to protect exploited species and conserve biodiversity. The increased abundance of predatory species in marine reserves may cause indirect effects along chains of multi-trophic interactions. These trophic cascades can arise through direct predation, density-mediated indirect interactions (DMIIs), or indirect behavioural effects, termed trait-mediated indirect interactions (TMIIs). The extent of algal cover and the abundance of 4 primary consumers were determined in Lough Hyne, which was designated Europe's first marine nature reserve in 1981. The primary consumers were the sea urchin Paracentrotus lividus, the topshell Gibbula cineraria, the oyster Anomia ephippium, and the scallop Chlamys varia. The abundances of 3 starfish species (Marthasterias glacialis, Asterias rubens, and Asterina gibbosa) were also determined, as were 2 potential crustacean predators, Necora puber and Carcinus maenas. These data were compared with historical data from a 1962 (prey) and a 1963 (predator) survey to determine the nature of community interactions over adjacent trophic levels. The present study reveals a breakdown in population structure of the 4 surveyed prey species. Marine reserve designation has led to an increase in predatory crabs and M. glacialis, a subsequent decrease in primary consumers, especially the herbivore P. lividus, and an increase in macroalgal cover which is indicative of a trophic cascade. The study shows that establishing a Marine Reserve does not guarantee that conservation benefits will be distributed equally.

Distinguishing between direct and indirect effects of predators in complex ecosystems

1. Global declines in biodiversity have stimulated much research into the consequences of species loss for ecosystems and the goods and services they provide. Species at higher trophic levels are at greater risk of human-induced extinction yet remarkably little is known about the effects of consumer species loss across multiple trophic levels in natural complex ecosystems. Previous studies have been criticized for lacking experimental realism and appropriate temporal scale, running for short periods that are not sufficient to detect many of the mechanisms operating in the field.
2. We manipulated the presence of two predator species and two groups of their prey (primary consumers) and measured their independent and interactive effects on primary producers in a natural marine benthic system. The presence of predators and their prey was manipulated in the field for 14 months to distinguish clearly the direct and indirect effects of predators on primary producers and to identify mechanisms driving responses.
3. We found that the loss of either predator species had indirect negative effects on species diversity and total cover of primary producers. These cascading effects of predator species loss were mediated by the presence of intermediate consumers. Moreover, the presence of different intermediate consumers, irrespective of the presence or absence of their predators, determined primary producer assemblage structure. We identified direct negative effects of predators on their prey and several indirect effects of predators on primary producers but not all interactions could have been predicted based on trophic level.
4. Our findings demonstrate the importance of trophic cascade effects coupled with non-trophic interactions when predicting the effects of loss of predator species on primary producers and consequently for ecosystem functioning. There is a pressing need for improved understanding of the effects of loss of consumers, based on realistic scenarios of diversity loss, to test conceptual frameworks linking predator diversity to variation in ecosystem functioning and for the protection of biodiversity, ecosystem functioning and related services.

Trait-mediated indirect interactions in a marine intertidal system as quantified by functional responses

Studies of trait-mediated indirect interactions (TMIIs) typically focus on effects higher predators have on per capita consumption by intermediate consumers of a third, basal prey resource. TMIIs are usually evidenced by changes in feeding rates of intermediate consumers and/or differences in densities of this third species. However, understanding and predicting effects of TMIIs on population stability of such basal species requires examination of the type and magnitude of the functional responses exhibited towards them. Here, in a marine intertidal system consisting of a higher-order fish predator, the shanny Lipophrys pholis, an intermediate predator, the amphipod Echinogammarus marinus, and a basal prey resource, the isopod Jaera nordmanni, we detected TMIIs, demonstrating the importance of habitat complexity in such interactions, by deriving functional responses and exploring consequences for prey population stability. Echinogammarus marinus reacted to fish predator diet cues by reducing activity, a typical anti-predator response, but did not alter habitat use. Basal prey, Jaera nordmanni, did not respond to fish diet cues with respect to activity, distribution or aggregation behaviour. Echinogammarus marinus exhibited type II functional responses towards J. nordmanni in simple habitat, but type III functional responses in complex habitat. However, while predator cue decreased the magnitude of the type II functional response in simple habitat, it increased the magnitude of the type III functional response in complex habitat. These findings indicate that, in simple habitats, TMIIs may drive down consumption rates within type II responses, however, this interaction may remain de-stabilising for prey populations. Conversely, in complex habitats, TMIIs may strengthen regulatory influences of intermediate consumers on prey populations, whilst potentially maintaining prey population stability. We thus highlight that TMIIs can have unexpected and complex ramifications throughout communities, but can be unravelled by considering effects on intermediate predator functional response types and magnitudes.