Elegant terns (Thalasseus elegans) are precise predictors of the fishery catch per unit effort of the Pacific sardine in the Gulf of California.
PHOTO: OCTAVIO ABURTO/ILCP
For millennia, humans have used seabird sightings and behavior as indicators of conditions of the marine environment. Seabirds are highly visible and nest in large colonies in normally constant locations, allowing efficient data gathering. Different species can provide information on different parts of the food chain. Individuals are often easier to observe and capture than other marine organisms, allowing behavioral, anatomical, physiological, demographic, and genetic information to be gathered (1). In recent decades, seabird breeding and feeding observations have revealed the connection between sea surface temperatures in upwelling regions and seabird reproductive success, as well as the frequency with which warm oceanographic anomalies occur and the evolution of seabird life history strategies (2, 3). These insights provide valuable information for sustainable ecosystem management. Coordinated efforts to gather standardized seabird data will be essential for monitoring the health of the global ocean.
Seabirds have evolved a set of adaptations to their environment, such as being able to fly long distances, locate and capture prey underwater, and find nesting sites safe from predators and near highly productive marine regions, where they obtain food. Seabirds have comparatively long life spans (20 to 60+ years), reach sexual maturity late (between 2 and 10 years of age), reproduce annually, and have small clutch sizes (one to three eggs) and long periods of chick development (50 to 350 days) (4). These traits likely evolved because of the large effort required in delivering food to offspring from the open ocean, which can negatively affect the chances of adults’ survival to the next reproduction. Because seabirds are long-lived and reproduce annually, a failed breeding in years of low food availability has a smaller negative impact on their overall fitness (4).
Seabirds are sentinels in two ways. First, they can serve as biomonitors of ecosystem-scale changes, such as the presence of organic pollutants or heavy metals in their tissues and marine litter such as plastics and microplastics in their stomachs (5). Second, they can be quantitative indicators of ecosystem components such as fish abundance. Many instances of seabird breeding failures or population declines have presaged fisheries collapses and, through their diet composition and distribution shifts, they provide reliable signals of many fish stocks (1, 2, 6). These correlations are used to understand the dynamics of the ocean environment (6). Excessive fishing can also contribute to seabird distribution shifts and population decline when seabirds and fishers compete for the same resource (1, 7).
Seabird diet reflects the abundance of prey species within their foraging range (usually a radius of hundreds of kilometers). This allows monitoring of the fish populations on which they feed, which may be relevant to fisheries. However, the relationship between seabird diet and prey abundance is often nonlinear and threshold-driven, and the functional response of seabirds’ food choice to fluctuations in prey abundance must be known. For example, three seabird species in the Gulf of California track sardine populations through their diet, showing a strong relationship with industrial fisheries’ catch per unit effort (CPUE) (6).
Seabirds are affected by changes at a range of time scales. Changes in the environment on a scale of weeks or months may be reflected in reproductive performance. Because of their longevity and annual reproduction, seabirds have relatively stable populations on a year-to-year basis, so longer-term variability in environmental conditions can be detected from fluctuations in population size (7), changes in distributional ranges, or remote sensing of tagged individuals.
Different seabird parameters can be used in a complementary way and combined with environmental parameters to provide useful information about marine ecosystem functioning (2). For example, to understand the impact of oceanographic phenomena on ecosystem components, Bost et al. (8) used long-term datasets (∼18 years) on king penguins, including nesting population size, breeding success, diet composition, food consumption, and foraging distance, depth, time, and success, together with environmental variables such as sea surface temperature, thermocline depth, and distance to polar front. They found that under conditions of subtropical anomalies, the birds could find their prey only by diving deeper and farther from their colony, resulting in a reduction in breeding success and colony size.
Most fish stocks have been seriously depleted, lowering ocean biodiversity and dangerously threatening the structure and resilience of marine ecosystems. The practice of monitoring and managing fish populations through single-stock models has failed repeatedly, leading to the present critical state of global marine ecosystems. Ecosystem-based management, an alternative proposed for better ocean management, requires deep knowledge of complex ocean dynamics, including the impact of fishing activity on ecosystem processes, to attain sustainable stocks. Unfortunately, this approach is difficult to implement in ecosystems with limited data, as is the case in most of the world’s oceans. The use of indicator species such as seabirds that react quickly to ecosystem changes and provide early warnings of unsustainable stock harvest may be more appropriate (1, 6).
Another application of seabirds as sentinels is to inform about the effects of growing variability in ocean conditions due to climate change, which causes changes in the abundance and distribution of forage fish (9). Seabirds are used directly to inform on the state of fish stocks (1, 6), or indirectly through changes in critical habitat linked with changes in marine productivity and interactions in the food web. These studies reveal the capability of sentinel species to adjust to large-scale changes, a dynamic that needs to be better understood to determine the possible results of ocean management strategies.
Data loggers (small devices deployed on wild animals to record or transmit environmental and physiological data) can play a key role in this effort by providing information such as foraging area, water temperature, or diving depth (8). For example, Harwood et al. (10) have shown that population size, date of arrival at breeding areas, body condition, and breeding success are affected by environmental variables. Because seabirds adjust behaviorally to environmental changes, monitoring of foraging activity and prey taken to nestlings may reveal high-productivity areas or switches in diet to demersal prey when water temperature increases (10, 11).
Recent demographic history studies by Ruiz et al. (12) have shown that the coupled trophic relationship between seabirds and forage fish likely evolved over hundreds of thousands of years. They found that Heermann’s gulls (Larus heermanni) nesting in the Gulf of California had two population expansions that roughly coincided with population expansions of their two main fish prey, the Pacific sardine (Sardinops sagax, ∼317,000 to 218,000 years before the present) and the northern anchovy (Engraulis mordax, ∼92,000 to 30,000 years before the present), in the same region.
A better understanding of regime changes affecting fish body condition, fish behavior, and fish and seabird migrations will be crucial for developing sustainable fisheries (13). This will require a globally coordinated effort to study environmental changes relevant to marine species. Many local or regional programs for gathering diverse ocean variables, such as mangrove cover, fish abundance, plankton diversity, and seabird parameters, are in development (13), but internationally coordinated efforts to gather and use such data are in their infancy. Such coordinated efforts would also help in the development of ocean observation programs, which can use seabird data and oceanographic variables to generate ocean health standards and best practices (11, 13, 14). For example, Moore and Kuletz (11) have shown how marine bird and mammal research can be included in protocols of ocean observatories to develop marine ecosystem models.
The Oslo and Paris Convention in the North Sea uses the northern fulmar (Fulmarus glacialis) as an indicator species for acceptable ecological quality. The maximum acceptable level is that fewer than 10% of fulmars may have more than 0.1 g of plastic in their stomachs. Currently, more than 60% of fulmars exceed this amount, and only remote Arctic locations approach the Oslo and Paris Convention standards (5). Other large-scale, long-term international programs for the observation of marine ecosystems and biodiversity, such as the Commission for the Conservation of Antarctic Marine Living Resources (14), the Poseidon system (15), the Distributed Biological Observatory, the Global Ocean Observing System, and others (11, 13), are identifying essential ocean variables to monitor the global ocean and its biological resources with standardized international procedures (13).
It is unclear how quickly different seabird species will be able to adapt to rapidly changing environmental conditions, but, as sentinels of the health of the global ocean, they are clearly providing a warning of the drastic effects that this fast pace of changes is having on marine species worldwide. We have a chance to use the knowledge provided by seabirds to make the right decisions to prevent the loss of biodiversity and at the same time develop sustainable ways to harvest it.