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In the mid-1940's, Peruvian managers greatly increased the nesting space available to the three principal surface-nesting species of the Peruvian Coastal Current: the Guanay Cormorant (Phalacrocorax bougainvillii), the Peruvian Booby (Sula variegata), and the Peruvian Brown Pelican (Pelecanus occidentalis thagus). The combined populations of these...
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... species that was never used by a second species and the per- centage of quadrats used by two or more species over the years. 1909 and 1940, the combined populations of the three species increased as more islands came under the protection of Peruvian authorities (Jordan and Fuentes 1966). The population then leveled off at about 8 million birds (Fig. 1). The mean increase per year was 8% (SE mean = 4.2; n = 23; years of El Nino excluded). After 1946, with the creation of breeding sites free of ter- restrial predators on the mainland, the popu- lation of the three species rose as high as 20 million and the percentage annual increase more than doubled to 18% (SE mean= 4.5; n = 18; ...
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Citations
... The Humboldt Penguin (Spheniscus humboldti) has been recognized for nearly 2 decades as a species vulnerable to extinction, largely because of human activity (BirdLife International 2020). Population declines throughout the species' range of Peru and Chile are attributed to guano harvesting (Duffy 1983;Paredes and Zavalaga 2001), resource competition from commercial fisheries (Thiel et al. 2007), trophic restructuring following spatiotemporally cyclical El Niñ o Southern Oscillation events (Taylor et al. 2008), and industrial mining (Zavalaga and Paredes 1997). Although coastal mining operations have long threatened the species with habitat degradation and direct anthropogenic disturbance, including mass culls organized to remove the "nuisance" birds (Zavalaga and Paredes 1997;Paredes et al. 2002Paredes et al. , 2003, recent mining expansions near the species' largest Peruvian rookery, Punta San Juan Reserve (PSJ, 15˚22 0 S, 75˚11 0 W), have made heavy metal exposure a significant concern (Adkesson et al. 2019). ...
Humboldt Penguin (Spheniscus humboldti) population declines are attributable to several multifaceted anthropogenic impacts. At present, the exposure of Humboldt Penguins to high concentrations of heavy metals in the marine environment is a preeminent concern, due to mining along the Peruvian coast near key rookery sites. Metal and selenium concentrations were determined in eggs collected from September 2020 to April 2021 from a managed-care penguin population at the Brookfield Zoo to establish reference values for health indices conducted on wild populations. Concentrations of 16 elements, with emphasis on those found in mine efflux-arsenic, cadmium, copper, lead, mercury, selenium, and zinc-were assessed via inductively coupled plasma mass spectrometry in yolk, albumen, and eggshell. Data analyses indicate a clear delineation between egg constituents, with lipid-rich yolk displaying notably higher concentrations (μg/g) of arsenic (0.20 ± 0.064), chromium (0.086 ± 0.03), cobalt (0.01 ± 0.003), iron (238.65 ± 54.72), lead (0.32 ± 0.97), manganese (2.71 ± 0.66), molybdenum (0.57 ± 0.14), tin (3.29 ± 0.99), and zinc (64.03 ± 13.01) than other components (albumen and eggshell). These data confirm that heavy metals are partitioned differently across Humboldt Penguin egg components, which provides insight into the potential connection between embryonic nutrient source contamination and subsequent chick viability.
... For highly mobile marine vertebrates constrained to breed on land, such as seabirds, operating successfully within ocean systems is fraught with challenges. Access to suitable nesting habitat and widely-distributed prey can limit population processes [23][24][25], and these influences can become particularly pronounced during breeding periods when movements of central-place foragers are constrained in space and time [26]. Throughout the global oceans, these challenges result in the coexistence of multiple colonial seabird species within ecosystems, and thus in varied forms of ecological segregation [10,11,19]. ...
Background
Social interactions, reproductive demands and intrinsic constraints all influence foraging decisions in animals. Understanding the relative importance of these factors in shaping the way that coexisting species within communities use and partition resources is central to knowledge of ecological and evolutionary processes. However, in marine environments, our understanding of the mechanisms that lead to and allow coexistence is limited, particularly in the tropics.
Methods
Using simultaneous data from a suite of animal-borne data loggers (GPS, depth recorders, immersion and video), dietary samples and stable isotopes, we investigated interspecific and intraspecific differences in foraging of two closely-related seabird species (the red-footed booby and brown booby) from neighbouring colonies on the Cayman Islands in the Caribbean.
Results
The two species employed notably different foraging strategies, with marked spatial segregation, but limited evidence of interspecific dietary partitioning. The larger-bodied brown booby foraged within neritic waters, with the smaller-bodied red-footed booby travelling further offshore. Almost no sex differences were detected in foraging behaviour of red-footed boobies, while male and female brown boobies differed in their habitat use, foraging characteristics and dietary contributions. We suggest that these behavioural differences may relate to size dimorphism and competition: In the small brown booby population ( n < 200 individuals), larger females showed a higher propensity to remain in coastal waters where they experienced kleptoparasitic attacks from magnificent frigatebirds, while smaller males that were never kleptoparasitised travelled further offshore, presumably into habitats with lower kleptoparasitic pressure. In weakly dimorphic red-footed boobies, these differences are less pronounced. Instead, density-dependent pressures on their large population ( n > 2000 individuals) and avoidance of kleptoparasitism may be more prevalent in driving movements for both sexes.
Conclusions
Our results reveal how, in an environment where opportunities for prey diversification are limited, neighbouring seabird species segregate at-sea, while exhibiting differing degrees of sexual differentiation. While the mechanisms underlying observed patterns remain unclear, our data are consistent with the idea that multiple factors involving both conspecifics and heterospecifics, as well as reproductive pressures, may combine to influence foraging differences in these neighbouring tropical species.
... Cormorants form large colonies, exceeding 1000 pairs, with densities of up to 3 nests/ m 2 , and usually lay three eggs (Orta 1992). Nests are scraped on the ground and created from guano, feathers and other debris, with a diameter of 32 AE 4 cm (Duffy 1983). ...
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.
... This method consists of sketching the shape of the bird colony in a scaled map. The area of the colony is then calculated and multiplied by the bird or nest density (Duffy, 1983;Tovar, Guillen & Nakama, 1987;Tovar & Cabrera, 2005). The observer is at the ground level and often has a limited view of the whole colony. ...
Background:
Drones are reliable tools for estimating colonial seabird numbers. Although most research has focused on methods of improving the accuracy of bird counts, few studies have evaluated the impacts of these methods on bird behavior. In this study, we examined the effects of the DJI Phantom 3 drone approach (altitude, horizontal and vertical descent speeds) on changes in the intensity of behavioral response of guano birds: guanay cormorants (Phalacrocorax bougainvilli), Peruvian boobies (Sula variegata) and Peruvian pelicans (Pelecanus thagus). The breeding and non-breeding condition was also evaluated.
Methods:
Eleven locations along the Peruvian coast were visited in 2016-2017. Drone flight tests considered an altitude range from 5 to 80 m from the colony level, a horizontal speed range from 0.5 to 15 m/s, and a vertical descent speed range from 0.5 to 3 m/s. The intensity of the behavioral response of birds was scored and categorized as: 0-no reacting, 1-head pointing to the drone (HP), 2-wing flapping (WF), 3-walking/running (WR) and 4-taking-off/flying (TK). Drone noise at specific altitudes was recorded with a sound meter close to the colony to discriminate visual from auditory effects of the drone.
Results:
In 74% of all test flights (N = 507), guano birds did not react to the presence of the drone, whereas in the remaining flights, birds showed a sign of discomfort: HP (47.7%, N = 130), WF (18.5%), WR (16.9%) and TK (16.9%). For the drone approach tests, only flight altitude had a significant effect in the intensity of the behavioral response of guano birds (intensity behavioral response <2). No birds reacted at drone altitudes above 50 m from the colony. Birds, for all species either in breeding or non-breeding condition, reacted more often at altitudes of 5 and 10 m. Chick-rearing cormorants and pelicans were less sensitive than their non-breeding counterparts in the range of 5-30 m of drone altitude, but boobies reacted similarly irrespective of their condition. At 5 m above the colony, cormorants were more sensitive to the drone presence than the other two species. Horizontal and vertical flights at different speeds had negligible effects (intensity behavioral response <1). At 2 m above the ground, the noise of the cormorant colony was in average 71.34 ± 4.05 dB (N = 420). No significant differences were observed in the drone noise at different flight altitudes because the background noise of the colony was as loud as the drone.
Conclusions:
It is feasible to use the drone DJI Phantom 3 for surveys on the guano islands of Peru. We recommend performing drone flights at altitudes greater than 50 m from guano bird colonies and to select take-off spots far from gulls. Likewise, this study provides a first step to develop guidelines and protocols of drone use for other potential activities on the Peruvian guano islands and headlands such as surveys of other seabirds and pinnipeds, filming and surveillance.
... While the three species cohabit in coastal islands and headlands, they form monospecific colonies (Duffy 1983a), expressing different yet overlapping preferences for nesting places. Cormorants and pelicans prefer nesting in open ground and boobies prefer nesting in cliffs. ...
... During the early 1940s, Peruvian authorities began to fence-off coastal headlands in order to provide more nesting space for seabirds thereby enhancing guano production . This increase in secured nesting habitats resulted in an increase in the breeding populations of our three study species (Duffy 1983a). Nevertheless, our results show that seabirds still preferred to nest on islands rather than headlands, suggesting the latter may be suboptimal breeding habitat. ...
... Another surprising effect was the positive relationship between conspecific abundance and magnitude and timing of breeding. We expected a negative effect of density dependence due to competition for prey (Birt et al. 1987) and nesting space (Duffy 1983a). However seabirds, and especially cormorants, breed early and most of the years in nesting sites densely populated. ...
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.
... More generally, seabird-fisheries competition became a global concern in the 1970s and 1980s. Widespread declines in seabird populations were apparently related to the expansion (and in some cases collapse) of large-scale industrial fisheries for anchovies and sardines, as well as shifts in fisheries from groundfish to small pelagics, such as sandeels, which were important seabird food (Furness, 1978(Furness, , 1982Duffy, 1983;MacCall, 1984). The literature on seabird responses to fluctuations in food resources grew substantially at that time and is now diverse and substantial, covering aspects of seabird biology from foraging ecology to population biology (e.g., Cairns, 1987;Piatt et al., 2007). ...
... The literature on seabird responses to fluctuations in food resources grew substantially at that time and is now diverse and substantial, covering aspects of seabird biology from foraging ecology to population biology (e.g., Cairns, 1987;Piatt et al., 2007). In addition to previous references, early evidence of seabird populations tracking changes in forage fish abundance came from southern Africa (e.g., Furness and Cooper, 1982;Crawford et al., 1983), Peru (e.g., Duffy, 1983), and Norway (e.g., Vader et al., 1990). More often, however, changes in vital rates, as a proxy for population fluctuations, were attributed to changes in prey resource availability (e.g., Anderson et al., 1982 on brown pelicans off southern California; Monaghan et al., 1989 for Arctic terns (Sterna paradisaea) in the North Sea). ...
... As noted above, some seabird measurements (e.g., the number of chicks successfully fledged per breeding pair, chick growth rates, fledging weights) are easy to obtain, but key population parameters such as juvenile survival, breeding propensity, or adult survival may be missing, thereby limiting the capacity to model populations. Seabird population fluctuations often are also buffered by or lag changes in forage fish abundance (Duffy, 1983;Barrett and Krasnov, 1996;Anker-Nilssen et al., 1997;Jahncke et al., 2004;Crawford et al., 2011), such that it is impossible to establish relationships using simple correlations. Seabird populations integrate ocean and ecosystem conditions over ...
Worldwide, in recent years capture fisheries targeting lower-trophic level forage fish and euphausiid crustaceans have been substantial (∼20 million metric tons [MT] annually). Landings of forage species are projected to increase in the future, and this harvest may affect marine ecosystems and predator-prey interactions by removal or redistribution of biomass central to pelagic food webs. In particular, fisheries targeting forage fish and euphausiids may be in competition with seabirds, likely the most sensitive of marine vertebrates given limitations in their foraging abilities (ambit and gape size) and high metabolic rate, for food resources. Lately, apparent competition between fisheries and seabirds has led to numerous high-profile conflicts over interpretations, as well as the approaches that could and should be used to assess the magnitude and consequences of fisheries-seabird resource competition. In this paper, we review the methods used to date to study fisheries competition with seabirds, and present “best practices” for future resource competition assessments. Documenting current fisheries competition with seabirds generally involves addressing two major issues: 1) are fisheries causing localized prey depletion that is sufficient to affect the birds? (i.e., are fisheries limiting food resources?), and 2) how are fisheries-induced changes to forage stocks affecting seabird populations given the associated functional or numerical response relationships? Previous studies have been hampered by mismatches in the scale of fisheries, fish, and seabird data, and a lack of causal understanding due to confounding by climatic and other ecosystem factors (e.g., removal of predatory fish). Best practices for fisheries-seabird competition research should include i) clear articulation of hypotheses, ii) data collection (or summation) of fisheries, fish, and seabirds on matched spatio-temporal scales, and iii) integration of observational and experimental (including numerical simulation) approaches to establish connections and causality between fisheries and seabirds. As no single technique can provide all the answers to this vexing issue, an integrated approach is most promising to obtain robust scientific results and in turn the sustainability of forage fish fisheries from an ecosystem perspective.
... While the three species cohabit in coastal islands and headlands, they form monospecific colonies (Duffy 1983a), expressing different yet overlapping preferences for nesting places. Cormorants and pelicans prefer nesting in open ground and boobies prefer nesting in cliffs. ...
... During the early 1940s, Peruvian authorities began to fence-off coastal headlands in order to provide more nesting space for seabirds thereby enhancing guano production (Vogt 1942). This increase in secured nesting habitats resulted in an increase in the breeding populations of our three study species (Duffy 1983a). Nevertheless, our results show that seabirds still preferred to nest on islands rather than headlands, suggesting the latter may be suboptimal breeding habitat. ...
... Another surprising effect was the positive relationship between conspecific abundance and magnitude and timing of breeding. We expected a negative effect of density dependence due to competition for prey (Birt et al. 1987) and nesting space (Duffy 1983a). However seabirds, and especially cormorants, breed early and most of the years in nesting sites densely populated. ...
The Northern Humboldt Current System (NHCS) is a place of a high biological activity due to an intense coastal upwelling. It supports one of the biggest forage fish populations, the Peruvian anchovy, and the world-leading monospecific fishery in terms of landings. The NHCS also hosts large, although variable, seabird populations, composed among others by three guano-producing sympatric species: the Guanay cormorant (Phalacrocorax bougainvillii), the Peruvian booby (Sula variegata) and the Peruvian pelican (Pelecanus thagus), which all feed primarily on anchovy.In this work we reviewed the fluctuations of these three seabird populations, focusing on the seasonal cycle of their breeding, to address the following questions: How different are the seasonality of reproduction among species? To what extent may they be plastic in space and time? What from the natural environment and the anthropogenic activities impact more the breeding of seabirds?We addressed these questions using the monthly occupancy of breeders (1) in >30 Peruvian sites between 06°S and 18°S and from 2003 to 2014; and (2) in one site during three decadal periods (1952-1968, 1972-1989, 2003-2014). We also used environmental covariates from satellite and at-sea monitoring such as oceanographic conditions, prey abundance, availability and body conditions, and fisheries pressure covariates. We used multiseason occupancy models to characterize the seasonality of breeding and relate it with environmental covariates. We also used functional principal component analysis for classifying the differences in seasonality among sites, and random forest regression for analyzing the relative contribution of covariates in the variability of the seasonal breeding.We found that in average seasonal breeding mainly started during the austral winter/ early spring and ended in summer/ early fall, this pattern being stronger in boobies and pelicans than in cormorants. The breeding onset of seabirds is timed so that fledging independence occurs when primary production, prey conditions and availability are maximized. This pattern is unique compared with other upwelling ecosystems and could be explained by the year-round high abundances of anchovy in the NHCS.The average seasonal breeding may differ among nesting sites. Seabirds breed earlier and are more persistent when colonies are larger, located on islands, within the first 20km of the coast, at lower latitudes and with greater primary production conditions. These results suggest that in the NHCS, the seasonality of breeding is more influenced by local environmental conditions than by large-scale environmental gradients. These results provides critical information to a better coordination of guano extraction and conservancy policies.Seabirds may also adapt the seasonality of their breeding to drastic ecosystem changes caused by regime shifts. We found that the three study species exhibited a gradient of plasticity regarding the seasonality of their breeding. Cormorants showed a greater plasticity, modulating the timing and magnitude on their breeding seasonality. This is probably authorized by the greater foraging flexibility offered its great diving capacities. Fixed onset and magnitudes of breeding in boobies may be related to their specific foraging strategy and/or to changes of prey items when anchovy stock was low. We also suggested that boobies may adapt other fecundity traits as growth rate of chicks to lower abundance of anchovy.The specific differences in the adaptation of seasonal breeding allow seabirds to take profit differently from local prey conditions or to face differently regime shifts. Further researches, implementing a large-scale capture-recapture methodology in parallel with monthly census, are proposed in order to fulfill gaps in the basic knowledge on vital traits (adult survival, first age at reproduction, and juvenile recruitment) which are critical parameters to evaluate the dynamic of a population.
... Larger island provides more available ecological resources, most importantly nesting spaces, and competition for nesting sites among different birds may result in partitioning of bird species. One bird species could successfully defended occupied sites in cases of interspecific conflict and could prevent nesting by another (Duffy 1983;Duffy and La Cock 1985). ...
Seabird subfossils were collected on three islands of the Xisha Archipelago, South China Sea. Via elemental analysis, we identified that bird guano was a significant source for heavy metals Cu, Zn, and Hg. Cu and Zn levels in these guano samples are comparable to their levels in wildbird feces, but guano Hg was lower than previously reported. Trophic positions significantly impacted transfer efficiency of heavy metals by seabirds. Despite of a common source, trace elements, as well as stable isotopes (i.e., guano δ(13)C and collagen δ(15)N), showed island-specific characteristics. Bird subfossils on larger island had relatively greater metal concentrations and revealed higher trophic positions. Partition of element and isotope levels among the islands suggested that transfer efficacy of seabirds on different islands was different, and bird species were probably unevenly distributed among the islets. Island area is possibly a driving factor for distributions of seabird species.
... This increase in secured nesting habitats resulted in an increase in the breeding populations of 392 our three study species (Duffy 1983 The seasonal breeding pattern related to oceanographic and prey conditions described 402 above was more evident for pelicans and boobies than for cormorants. During the study 403 period, cormorants had an extended breeding period lasting for more than half of the year. ...
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 3 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.
... The pelicans are well known for their aggressive behavior toward other seabird species in the Humboldt Current region, including often usurping nests (Duffy (2016) 1983). Peruvian pelicans rest and/or nest on flat areas in higher grounds of the colonies, as their long wings cannot negotiate a safe landing on cliffs (Duffy 1983). However, the Imperial Cormorant also uses gentle slopes for nesting (Cursach et al. 2010); as a result, a greater frequency of competitive interactions for perching and/or nesting space would be expected between these two species in the Los Lagos region. ...
Over the past few years, an increase in Peruvian Pelican Pelecanus thagus presence has occurred in southern Chile, along the coast of the Los Lagos region, at the southern end of its range. We evaluate the presence of the pelicans in seabird colonies of this region and describe their behavior and interactions with other seabird species. Three colonies were surveyed: San Pedro Bay Islets (40°55′S), Kaikué-Lagartija Island (41°48′S) and Caicura Island (41°42′S). Counts were carried out from boats, and age structure was determined based on plumage color. Pelicans were found to be numerous and included a high proportion of juveniles. With the exception of one pelican egg (unhatched) found at Caicura Island in December 2013, there was no evidence of pelican nesting. Potential competitive interactions between the pelicans and other seabirds were evident.
