The predictive performance of this model was good. The average model AUC: 0. Cross-validation scores were 0. Climatology of mean presence probability from a terns and c boobies and b, d associated uncertainty map SD of monthly predictions. Vessel-based observations of boobies showed a distribution pattern concentrated around Europa Fig.
No other individuals were observed in the rest of the surveyed area. Aerial observations of boobies were scarce too. They showed an aggregation around the Comoros and some individuals between the Comoros and the northwest coast of Madagascar. Since the model with the lowest AIC exhibited an A w of 0. Thus, the probability of presence of the boobies was higher close to the main colony Europa. Within the dynamic landscape of the Mozambique Channel they associated negatively to eddies fronts and positively with warm waters. Maximum uncertainties max.
Cross-validation values were 0. These model outputs showed that terns and boobies share similar habitats with frigatebirds, supporting the hypothesis of feeding association. Vessel-based surveys recorded sub-surface predators around Europa and along the coast of Mozambique Fig. Output of species distribution models for sub-surface predators represented by b mean probability of presence for October and c its associated uncertainty map SD of presence probability based on vessel-based observations between and Regarding modelling output, a model averaging approach was used since the model with the lowest AIC value showed an A w value of 0.
The average model showed a reasonable predictive performance AUC value of 0. Thus, sub-surface predators were associated with warm waters and negatively to fronts.
Small Fish's Predator Perception Makes a Splash
In spatial terms, maximum values occurred in the northern MC and, to a lesser extent, in the middle part of the Channel Fig. The average model is generalizable to other conditions since the AUC values of cross-validation scores did not include 0. Using thresholds at which sensibility and specificity calculated for each average model developed were maximised S1 Table , cells showing predicted probability over this threshold were classified as suitable while cells below the threshold were considered unsuitable.
Combining suitability maps for the four groups of species studied, which were calculated for each year of the study — during the breeding months September to December , a map of the important areas for the predators was designed. Then, an overlap index was estimated between pairs of taxa which show a mean overlap value ranging from 0.
Among the three groups of seabirds, the highest overlap value is found in pairs of taxa including frigatebirds, showing that this species is the most likely to cover the habitats of the other species in its distribution. Moreover, the output of the map of the important areas showed that suitable areas for all groups of birds and mammals tend to congregate. Cells predicted as suitable for all species were concentrated in the central and southern MC Fig. Finally, the lowest values occurred in the southern part of the study area. Uncertainties are very low Fig. Distribution data from both tracking and at-sea observations are complementary, and these sources of information are nowadays increasingly combined in conservation studies  ,  , .
Tracking data provide accurate information on individuals of known provenance, age and breeding status whereas at-sea observations allow large-scale investigation of the distribution pattern of all population components i. At-sea observations also inform on biological interactions, feeding behaviour and feeding events, which can only be speculated with tracking devices.
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In this study, distribution data of several species of seabirds and marine mammals obtained by a combination of data from three platforms were compared, with the ultimate aim of determining important areas for these marine predators. By combining two different but complementary approaches, tracking and vessel or aerial observations, we were able to show that two different components of the population have distinct distributions. Although breeding and non-breeding birds share similar foraging areas near Europa and its westward extension, densities were higher for breeders around Europa observed from tracking and vessel and for non-breeders in the northern sector of the Mozambique Chanel as indicated by tracking and aerial surveys.
While breeders forage as central place foragers around Europa, non-breeding adults move to the Comoros area to exploit different marine areas, using roosting sites as a central place for foraging . During breeding, birds perform foraging trips ranging around km to feed on flying fish and squids, which are the prey boobies and terns feed on as well . However, there is evidence for differences in the diet of frigatebirds according to their breeding status and age class.
Isotopic signatures of non-breeding birds exhibit higher variability and overall lower trophic levels in their prey, showing a shift in frigatebirds diet when they are no longer central place foragers. The distribution of frigatebirds is negatively influenced by Chlo a , suggesting that the birds do not seem to track high primary production areas in the Mozambique Channel. However, this result should be interpreted with caution as frigatebirds do not feed on primary producers.
A natural delay between phytoplankton development and presence of micronekton and associated fish species is likely to occur, especially when satellite imagery is used at a monthly scale. Successions of eddies moving southward in the Mozambique Channel mix water masses to create a dynamic ecosystem  where it is difficult to determine how seabirds respond to ephemeral biotic structures.
Moreover, high chlorophyll a concentration is associated with Zambezi river mouth in the MC.
The turbidity of this area may also explain the negative relationship observed. Terns are widely distributed in the Mozambique Channel, and breed in extremely large numbers on Europa, Juan de Nova and the Glorioso archipelago  , . Both vessel-based and aerial surveys revealed the wide oceanic distribution of brown terns represented mainly by sooty terns throughout the MC.
In particular, vessel-based observations show concentrations in the western part of the MC, where high densities of frigatebirds occur, suggesting the existence of shared foraging areas where they likely feed in common flocks in offshore waters  , . In the MC, the only large colony of boobies red-footed boobies is located on Europa . Boobies showed a distribution exclusively driven by the location of their colony. This is revealed by both at-sea observations and tracking data that indicate relative short ranges of breeding adults red-footed boobies from Europa.
It is consistent with previous studies which showed directly, using tracking or at-sea observations, that breeding red footed boobies from Europa forage close to their colony to a maximum of km from the island  , . Other booby species also have relatively short ranges compared to frigatebirds, especially brown boobies and masked boobies  ,  , these latter species being present in small numbers in the MC.
This is also in accordance with wide-ranging surveys indicating that boobies occur mainly in coastal flocks  , and show no dispersal of the non-breeding part of the population .
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The range of frigatebirds in the MC encompasses that of boobies, in agreement with the results of an isotopic study showing that frigatebirds and boobies share the same feeding area and overlap with terns . Sub-surface predators were widely distributed in the MC, with a higher density in the northern part Fig. Our model predicted their distribution in central and northern MC which is consistent with the distribution of purse seine fishing effort for tunas in the MC .
This distribution overlaps widely with those of the seabirds, which is in accordance with the well-known role of dolphins and tunas in aggregating multispecific feeding flocks in the Mozambique Channel . Despite the dynamic nature of the environmental parameters used here, all models presented satisfying predictive performance, and AUC values ranging from 0.
Some areas emerge as potential zones of importance for all the top predators. Marine predator hotspots were identified in offshore waters of the southern MC, represented by a longitudinal ellipsoide between the mouth of Zambezi River to the west and the coast of Madagascar to the east, including Europa Island Fig. The same species shown to form multispecific feeding flocks in previous studies  ,  were found to co-occur in this study. As a consequence, the species that share similar foraging areas are likely to be vulnerable to a shift in the density or distribution of any species that aggregate their prey or signals the presence of prey aggregations.
In particular, any depletion of tuna species, which are targeted by industrial fisheries, would be of great concern. In the case of seabirds, our results show a clear influence of the colony, in particular for frigatebirds and boobies. Breeding seabirds are central place foragers and need to return to the colony to incubate, brood or feed their chicks  , . Thus, their foraging trips are limited in time and distance from their nest.
This foraging behaviour is particularly evident in the case of tracking data from breeding frigatebirds equipped at Europa Island. However, the influence of the distance to the colony on seabird distribution is also highlighted in at-sea observations from both vessel-based and aerial surveys, although both breeding and non-breeding birds are involved.
Indeed, Europa Island is a major breeding site for numerous species of seabirds  , the only breeding site for frigatebirds in the MC, and distance to the colony has been shown to be an important predictor of their distribution . The neighbourhood of the colony or a roosting site could also be an important factor in the distribution of non-breeding birds, especially since frigatebirds are the only seabirds that never rest on the surface of the sea. These oceanographic conditions describe oceanic waters of the Mozambique Channel, characterised with low chlorophyll a levels and warm water.
In particular, the western oceanic sector of the MC appears to be an area where top predators concentrate, particularly frigatebirds, terns and dolphins.
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This area of high mesoscale activity, with several eddies flowing southward year long, is already known to be attractive for frigatebirds that forage at the edges of the eddies  , . Indeed, these oceanic processes enhance primary production, and concentrate micronekton at the periphery of eddies . The negative relation observed between the presence of predators and Chlo a could be linked to the absence of foraging in coastal areas, where highest values of Chlo a occurred, particularly on the mouth of the Zambesi River, off Mozambique.
The accuracy of the predicted presence areas is constrained by both the spatial and the temporal scales of the study. Indeed, monthly composite environmental data cannot reflect fine scale dynamic parameters such as upwelling filaments cool, elevated-chlorophyll a waters that have been shown to drive the distribution of frigatebirds  , .
In the same way, the use of monthly scale variables did not necessarily reflect temporal integration between the detection of primary production, and peak prey availability for top predators. However, using weekly data of SLA does not improve the performance of the model, which indicates that given the highly dynamic variability of these processes, defining the ideal temporal scale for habitat modelling in the MC is difficult. In addition, there is as yet no information on the time lag between the presence of high levels of chlorophyll a and a peak of prey in the Mozambique Channel.
Identifying foraging areas instead of presence areas for top predators in the Mozambique Channel might have improved the addressing of preliminary hypothesis, however, models using foraging information were not successful results not shown , because altitude data that indicate when frigatebirds are foraging  would be necessary to determine precisely when birds are feeding.
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In addition raw observations from this study show that foraging frigatebirds and boobies were often associated with foraging terns, and frequently with sub-surface predators. Tracking data on breeding birds can give a biased view of the distribution of a species if there are differences between breeding and non-breeding birds. Overall, habitat models do not predict precise hotspots apart from the vicinity of Europa, suggesting that although frigatebirds concentrate at sub-mesoscale features associated with the edge of eddies, because these habitats are very mobile over short periods of time, they are not predictable at a monthly scale.
This underlines again the high unpredictability of tropical waters, and the difficulty of identifying precisely important zones at fine temporal and spatial scales. Nevertheless, data from different sources in this study showed consistent results. Mapping high use areas reveals a wide overlap between the four groups of species studied here, suggesting that the distribution of frigatebirds is a good indicator of top predator concentrations at large and meso-scales. Map of the frigatebird trips collected from September to October , September to October and September to December Output of species distribution models for frigatebirds including DCol.
Climatology of mean presence probability a from frigatebirds in October based on tracking data from and and c vessel-based observations and b, d associated uncertainty map standard deviation of monthly predictions. Ranked set of best candidates frigatebirds tracking model and average model integrating distance to the colony DCol.
Ranked set of best candidates frigatebirds tracking model and average model. Ranked set of best candidates frigatebirds at-sea observations model and average model. Ranked set of best candidates terns at-sea observations model and average model.