Peruvian Boobies Sula Variegata Research Articles

Interactions between anchovy fisheries and Peruvian boobies revealed by bird-borne cameras and movement loggers

Fisheries threaten marine predator populations through bycatch and competition for the same resources, but may also provide feeding opportunities. Understanding benefits and mitigating impacts, therefore, requires a detailed understanding of fishery interactions. The Humboldt Current system supports the world’s largest single-species fishery (Peruvian anchoveta Engraulis ringens), along with abundant marine predators dependent on these forage fish, including seabirds. We combined bird-borne video cameras and GPS-acceleration-dive loggers to quantify the foraging behaviour of chick-rearing Peruvian boobies Sula variegata around Isla Macabi, Peru, in December 2020 and May 2021. Videos revealed that 18% of 77 Peruvian booby foraging trips included feeding at actively fishing purse seine vessels, diving in and around the nets. Most vessel interactions were close to the colony, and we found no difference in foraging effort (e.g. trip duration) between trips with and without vessel interactions. We recorded fishing effort in the foraging range of the colony using remotely sensed data from the vessel monitoring system accessed via Global Fishing Watch, finding more frequent interactions and catch depredation when fishing effort was high near the colony. We found no evidence that birds expended additional energy (e.g. dynamic body acceleration) or travelled to different locations to reach vessels. We emphasise the value of combining high-resolution movement and video loggers with remotely sensed fisheries data to monitor seabird-fishery interactions in detail, rather than just spatio-temporal overlap, and assess the potential for competition and bycatch. Threatened seabird populations may benefit from no-take zones or reduced fishing effort in core foraging areas of colonies.

The importance of guano birds to the Inca Empire and the first conservation measures implemented by humans

The Inca Empire was the largest ancient civilization in South America, extending across almost 4000 km of distinct environments from the Pacific coast to the Andes, and throughout most of the arid desert between. The present study highlights the importance of guano birds (Guanay Cormorant Leucocarbo bougainvillii, Peruvian Pelican Pelecanus thagus and Peruvian Booby Sula variegata) for the expansion and prosperity of the Inca Empire. The use of guano as a fertilizer was fundamental to sustain the agricultural development of the empire and, it has been argued, was the basis for its rapid growth. The access to guano on coastal islands and its subsequent transportation to highlands provided food security for a population of more than 8 million. The importance of guano birds to the Inca Empire led to the development of management plans based on a penal code aiming to preserve these species and their natural habitats. These protective actions may represent the first conservation measures ever implemented by humans based on the importance of species protection for human activities and livelihoods.

Long-term changes in the breeding seasonality of Peruvian seabirds and regime shifts in the Northern Humboldt Current System

In the highly productive Northern Humboldt Current System, 3 seabird species, the Guanay cormorant Phalacrocorax bougainvillii, the Peruvian booby Sula variegata and the Peruvian pelican Pelecanus thagus, commence breeding in austral spring, coinciding with the lowest availability of their prey, the Peruvian anchovy Engraulis ringens. This strategy ensures the matching of increased prey availability when young achieve independence in summer. This pattern was observed during the last decade when anchovy was abundant. However, over the last century, the abundance of anchovy has varied widely due to contrasting interdecadal regimes in oceanographic conditions and fishing activity. We hypothesized that these regime shifts affected the abundance and availability of prey and may have conditioned the breeding seasonality of seabirds. We examined the timing and magnitude of the onset of breeding using dynamic occupancy models and related these parameters to the seasonality of oceanographic conditions, abundance of anchovy and fishing pressure. During a regime of lower anchovy abundance (1977-1990), cormorants showed the highest flexibility, adjusting the timing of breeding from spring to winter and skipping reproduction in the worst conditions. Boobies showed the lowest flexibility, maintaining the same magnitude and timing of onset of breeding in spring. Pelicans showed intermediate flexibility, foregoing breeding during the worst conditions, but maintaining the onset of breeding in spring. The 3 species used sea surface temperature as a cue for the initiation of breeding. Furthermore, given their better diving abilities, cormorants could monitor prey availability changes associated with the reversion in the seasonality of the oxycline depth.

Density dependence, prey accessibility and prey depletion by fisheries drive Peruvian seabird population dynamics

In marine ecosystems top predator populations are shaped by environmental factors affecting their prey abundance. Coupling top predators’ population studies with independent records of prey abundance suggests that prey fluctuations affect fecundity parameters and abundance of their predators. However, prey may be abundant but inaccessible to their predators and a major challenge is to determine the relative importance of prey accessibility in shaping seabird populations. In addition, disentangling the effects of prey abundance and accessibility from the effects of prey removal by fisheries, while accounting for density dependence, remains challenging for marine top predators. Here, we investigate how climate, population density, and the accessibility and removal of prey (the Peruvian anchovy Engraulis ringens) by fisheries influence the population dynamics of the largest sedentary seabird community (≈ 4 million individuals belonging to guanay cormorant Phalacrocorax bougainvillii, Peruvian booby Sula variegata and Peruvian pelican Pelecanus thagus) of the northern Humboldt Current System over the past half‐century. Using Gompertz state–space models we found strong evidence for density dependence in abundance for the three seabird species. After accounting for density dependence, sea surface temperature, prey accessibility (defined by the depth of the upper limit of the subsurface oxygen minimum zone) and prey removal by fisheries were retained as the best predictors of annual population size across species. These factors affected seabird abundance the current year and with year lags, suggesting effects on several demographic parameters including breeding propensity and adult survival. These findings highlight the effects of prey accessibility and fishery removals on seabird populations in marine ecosystems. This will help refine management objectives of marine ecosystems in order to ensure sufficient biomass of forage fish to avoid constraining seabird population dynamics, while taking into account of the effects of environmental variability.

Ecomorphology and foraging behaviour of Pacific boobies

Wing size and shape, expressed as wing loading and aspect ratio respectively, together with bill morphology are parameters that can reveal differences related to the foraging ecology of seabirds. Six species of booby (Sulidae) that inhabit the Pacific are the focus of this study: four mainly pelagic species, Masked Booby Sula dactylatra, Nazca Booby Sula granti, Red‐footed Booby Sula sula and Brown Booby Sula leucogaster, and two coastal species, Blue‐footed Booby Sula nebouxii and Peruvian Booby Sula variegata. Pelagic boobies showed segregation among species in body mass and relative bill size, and they differed in wing morphology (wing loading and aspect ratio) from the coastal boobies. The coastal Peruvian and Blue‐footed Boobies are largely allopatric but overlap in northern Peru. In their area of sympatry, they showed evidence of character displacement in body size and in wing and bill morphology, which suggests that competition plays an important role in sympatry. This study improves our understanding of ecological interactions among Pacific boobies and of how selective pressures have shaped their ecomorphology and foraging behaviours.

Effects of variation in the abundance and distribution of prey on the foraging success of central place foragers

Summary Seabirds and pinnipeds are vulnerable to reductions in prey availability, especially during the breeding season when spatial constraints limit their adaptive capacity. There are growing concerns about the effects of fisheries on prey availability in regions where large commercial fisheries target forage fish. For breeding seabirds and pinnipeds, prey availability depends on a combination of abundance, accessibility, patchiness and distance from the colony. An understanding of the aspects of prey availability that determine foraging success is essential for the design of effective management responses. We used a mechanistic individual‐based foraging model based on observed data for two seabird species, the Peruvian Booby Sula variegata and Guanay Cormorant Phalacrocorax bougainvilliorum, to simulate the foraging patterns of seabirds feeding on schooling fish. We ran the model over simulated prey fields representing eight possible combinations of high or low prey abundance, shallow or deep prey, and broadly distributed or spatially concentrated prey. The results highlight the importance of the accessibility of prey. Depth distribution was the primary factor determining modelled foraging success for both species, followed by abundance, and then spatial configuration. Synthesis and applications. The individual‐based foraging model provides a spatially explicit framework for assessing the effects of fisheries on the foraging success of seabirds and other central place foragers, and for evaluating the potential effectiveness of marine‐protected areas and other fisheries management strategies for safeguarding central place foragers in dynamic ecosystems. Our analysis indicates that broad‐scale fisheries management strategies that maintain forage fish above critical biomass levels are essential, but may need to be supplemented by targeted actions, such as time–area closures, when environmental conditions lead to low prey abundance or reduce prey accessibility for seabirds or pinnipeds of conservation concern. The individual‐based foraging model is adaptable and could be reconfigured for application to other species and systems.

Seasonality in marine ecosystems: Peruvian seabirds, anchovy, and oceanographic conditions

In fluctuating environments, matching breeding timing to periods of high resource availability is crucial for the fitness of many vertebrate species, and may have major consequences on population health. Yet, our understanding of the proximate environmental cues driving seasonal breeding is limited. This is particularly the case in marine ecosystems, where key environmental factors and prey abundance and availability are seldom quantified. The Northern Humboldt Current System (NHCS) is a highly productive, low-latitude ecosystem of moderate seasonality. In this ecosystem, three tropical seabird species (the Guanay Cormorant Phalacrocorax bougainvillii, the Peruvian Booby Sula variegata, and the Peruvian Pelican Pelecanus thagus) live in sympatry and prey almost exclusively on anchovy, Engraulis ringens. From January 2003 to December 2012, we monitored 31 breeding sites along the Peruvian coast to investigate the breeding cycle of these species. We tested for relationships between breeding timing, oceanographic conditions, and prey availability using occupancy models. We found that all three seabird species exhibited seasonal breeding patterns, with marked interspecific differences. Whereas breeding mainly started during the austral winter/early spring and ended in summer/early fall, this pattern was stronger in boobies and pelicans than in cormorants. Breeding onset mainly occurred when upwelling was intense but ecosystem productivity was below its annual maxima, and when anchovy were less available and in poor physiological condition. Conversely, the abundance and availability of anchovy improved during chick rearing and peaked around the time of fledging. These results suggest that breeding timing is adjusted so that fledging may occur under optimal environmental conditions, rather than being constrained by nutritional requirements during egg laying. Adjusting breeding time so that fledglings meet optimal conditions at independence is unique compared with other upwelling ecosystems and could be explained by the relatively high abundances of anchovy occurring throughout the year in the NHCS.

Foraging in Guanay cormorant and Peruvian booby, the major guano-producing seabirds in the Humboldt Current System

The Humboldt Current System is the most productive upwelling system globally in terms of fish and sustains huge populations of guano-producing birds as well as the world's largest single-species fishery targeting the Peruvian anchovy Engraulis ringens. Peruvian boobies Sula variegata and Guanay cormorants Phalacrocorax bougainvillii are the most abundant seabird spe- cies in the system and feed mainly on anchovies. By using high precision GPS and timedepth recorders, we compared the horizontal and vertical movements of the 2 species to examine whether segregation occurs between their foraging areas and whether there is any evidence for prey depletion close to large colonies. A simultaneous acoustic cruise in the foraging area of the 2 bird species estimated the vertical and horizontal distributions of anchovy schools. During the study period in austral spring 2008, the 2 bird species foraged in the same area, at relatively short distance from the colony (average, 19 to 20 km). Both species foraged at similar times of the day, although Peruvian boobies tended to leave earlier in the morning and return later in the evening than did the cormorants. Foraging trips were similar in duration, distance covered and range. Peruvian anchovies were abundant and schools occurred at shallow depths (median, 7 m; range, 3 to 34 m), mainly to the north and west of the colony where foraging bouts of the 2 species over- lapped extensively. Cormorants are mainly pelagic surface divers, diving at shallow depths (median, 4 m) but reaching up to 32 m depth, and are thus able to track all the depths at which anchovies occurred during the study period. Peruvian boobies are plunge divers able to reach occasionally 10 m (median, 2 m), and are thus able to reach only shallow anchovy schools. No sex- specific differences in horizontal or vertical movements occurred between males and females in the 2 species. We suggest that the absence of significant differences between horizontal move- ments of boobies and cormorants, the relative short duration of their trips and the high number of chicks fledged were probably explained by the high abundance and accessibility of anchovies. Differences may be exacerbated during years of low anchovy abundance or accessibility, especially El Nino years.

At-sea movement patterns and diving behavior of Peruvian boobies Sula variegata in northern Peru

GPS loggers and time-depth recorders were used to characterize the foraging behavior of the sexually dimorphic Peruvian booby Sula variegata on 2 islands in northern Peru. We evaluated whether (1) its foraging behavior differed from tropical boobies and temperate gannets (the Peruvian boobies feed in areas of enhanced productivity and high fish density), and (2) females and males exploited different foraging habitats as a consequence of size dimorphism. Birds foraged only during daylight hours, 1 to 3 times a day, in trips of short duration (median = 1.8 h). Overall, 92% of the total foraging time was spent flying. They fed exclusively on anchovetas Engraulis ringens, which were captured in shallow dives (median = 2.5 m, max = 8.8 m) with a dive median rate of 11 dives h–1 (max = 37 dives h–1). The median foraging range was 25 km (max = 68 km), whereas the median total distance traveled was 69 km (max = 179 km). Foraging site fidelity was high, and the orientation of foraging flights in any given day was similar among birds that departed at the same time. There were no sex-specific differences in 13 of 15 foraging variables; however, females dived slightly deeper and spent a larger proportion of time sitting on the water. We speculate that (1) the foraging behavior of Peruvian boobies contrasts with that of their tropical and temperate relatives as a result of the proximity and predictability of food sources, elevated energetic demands of the brood (up to 4 chicks) and high prey encounter rate in the Peruvian upwelling system, and (2) the lack of spatial segregation between sexes may be related to the attraction of birds to feeding aggregations that are formed in the vicinity of the colonies. Once the foraging patches are localized, females dive deeper because of passive mechanisms associated with a heavier mass.

Breeding distribution and abundance of seabirds on islands off north-central Chile

Between 1999 and 2003 we collected information on the breeding distribution and abundance of 12 seabird species occurring on nine islands off the coasts of north and central Chile (27°-33°S). The Peruvian booby Sula variegata was the most abundant seabird with a breeding population of ca. 18,000 pairs concentrated in two islands, followed by the Humboldt penguin Spheniscus humboldti with ca. 9,000 pairs, the largest colony being at Chanaral Island with ca. 7,000 pairs. Kelp gulls Larus dominicanus bred at all the surveyed sites in colonies of variable size, ranging from 40 to 2,000 pairs. Peruvian diving-petrels Pelecanoides garnotii and Peruvian pelicans Pelecanus occidentalis bred at restricted sites, but generally in large colonies. Magellanic penguins Spheniscus magellanicus, wedge-rumped storm-petrels Oceanodroma tethys, Neotropical cormorants Hypoleucos brasiliensis, guanay cormorants Leucocarbo bougainvillii, red-legged cormorants Stictocarbo gairmardi, band-tailed gulls Larus belcheri and Inca terns Larosterna inca nested at few sites forming small colonies (from a few to 150 pairs). Two new breeding sites are reported for the Peruvian diving-petrel and nesting of the wedge-rumped storm-petrel is confirmed on the Chilean coast for the first time. Despite protective status, most of the islands showed human disturbance, derived mainly from guano harvesting, egging and tourism. On at least five of these islands we were able to confirm introduced mammals including rats, rabbits and cats. These factors are likely to be detrimental to seabirds and thus demand detailed assessment. Further comprehensive ornithological surveys in other areas are needed so as to improve the scarce knowledge that we currently have on the seabird populations along the Chilean coast

Comparison of trends in abundance of guano-producing seabirds in Peru and southern Africa

The abundant guano-producing seabirds in Peru and southern Africa feed mainly on the large populations of anchovy Engraulis spp. and sardine Sardinops sagax supported by the Humboldt and Benguela upwelling systems. Numbers of guanay cormorants Phalacrocorax bougainvillii in Peru and the breeding population of Cape cormorants P. capensis in South Africa are significantly related to the biomass of anchovy. For both species, reproductive success decreases in periods of anchovy scarcity, and there may also be substantial adult mortality. There has been long-term stability in numbers of Peruvian boobies Sula variegata, whereas the numbers of Cape gannets Morus capensis decreased as sardine decreased in southern Africa. Numbers of Peruvian pelicans Pelecanus (occidentalis) thagus are significantly related to the combined biomass of anchovy and sardine in Peru. They have been stable in the long-term. There have been ongoing severe decreases in populations of the Humboldt penguin Spheniscus humboldti and the Afri...

Environmental uncertainty and commercial fishing: Effects on Peruvian guano birds

The roles of the El Niño phenomenon, a cessation of upwelling, and of human fishing in limiting populations of Peruvian guano birds (Guanay cormorant Phalacrocorax bougainvillii, Peruvian booby Sula variegata, and Peruvian brown pelican Pelecanus occidentalis thagus) were investigated using historical records and the scientific literature. In normal years, the combined populations of the three species showed an 18% increase per year. El Niños occurred at approximately five-year intervals and caused a population decrease of 17% and 35% desertion of nesting areas. In severe El Niños at approximately 12-year intervals, there was a mean decrease of 47% and complete nesting failure. El Niños varied in severity and a possible explanation is presented. In non-El Niño years, commercial fishing did not directly control bird populations through starvation of adults or drowning in nets. Increased commercial fishing apparently led to decreased nesting success: the greater the quantity of fish landed, the lower the percentage increase of the bird population that year. Short-lived, heavily-fished species such as anchoveta are in constant danger of population collapse during years of occasional, unpredictable reproductive failure. Bird populations could be maintained as buffers to prevent terminally-destructive overfishing by humans.