The land-sea interface is distinguished by near constant movement of materials between biomes. Allochthonous subsidies, originating in one location and transported to a disparate environment, often take the form of marine nutrients. Marine derived subsidies, when delivered to coastal regions or islands, can provide nutrient inputs that impact the functioning of terrestrial ecosystems (1–3). The iconic example of the decaying bodies of spawning salmon enhancing soil profiles and terrestrial plant biodiversity illustrates the importance of these multi-step trophic land-sea linkages (4, 5).
There are a number of examples of how trophic cascades alter ecosystem functioning. As noted, salmon species contribute to nutrient levels at their spawning sites, leaving a record of this marine-to-terrestrial transfer in the resulting nitrogen and carbon isotope ratios of the locality (6). Artic foxes have been shown to be ecosystem engineers by increasing soil nutrients and enhancing plant productivity and diversity at den sites (7, 8). Seabird species can be important vectors across the land-sea interface for nutrients from marine environments, increasing native tree abundance and soil nitrogen where they roost (9). Seabird guano, which is deposited on land in coastal regions or island systems, as well as seabird bodies themselves (dead adults, chicks, and eggs) are a prime example of land-sea connectivity. Commonly, nitrogen deposits of marine origin are delivered to terrestrial soil—potentially through decaying fish matter or seabird excrement—where changes in soil composition or plant production occurs (1, 4, 10). These inputs can greatly impact the nitrogen nutrients found in soils (11).
Globally, coastal areas represent only 8% of total land area but provide 20% of oceanic production (12). Seabirds are present in a wide range of high productivity marine systems around the world and are essential to nutrient cycling between land-sea systems. They facilitate the exchange of nitrogen and other chemical subsidies between the two biomes (11, 13–16) and alter physical and soil conditions directly affecting plant richness and distribution (17). In the San Juan archipelago, seabird derived guano in intertidal regions appears to increase the abundance of certain algal species while simultaneously decreasing intertidal plant biodiversity (18). In coastal areas where native plants create poor bird habitat, nutrient cycling is limited due to decreased seabird guano deposits (19). In Antarctica, penguin rookeries classically exhibit significant nitrogen deposition to the island ecosystem (11, 20, 21). Similarly, in the Gulf of California, areas of seabird influence possess increased nitrogen content and stable isotope ratios (16, 22).
Guano contains nitrogen in the form of NH4+, NO3-, and as a component of uric acid (C5H4N4O3). Each of these undergoes chemical alteration at different rates of decomposition (20). Previous research has demonstrated that the nitrogen isotope composition of bulk guano enriched soils is significantly elevated due to the volatilization of ammonia, leaving the remaining material with more positive δ15N values (11). Guano enriched soils have much higher nitrogen isotope ratios than non-guano enriched areas (10) and create spatial variation in the chemical soil composition of island systems (15).
In years of higher precipitation such as El Niño years in the Southwest U.S. or when hurricanes reach this region, there is an elevated presence of decomposed guano due the mobilization of the nutrients from the increased moisture. During these pulse years, the soil exhibits increased nitrogen levels with increased plant productivity (10). It is suggested that guano deposition in terrestrial ecosystems could increase soil nitrogen content by up to 100 times its original amount (13). Plants growing in areas with higher guano concentrations take up nitrogen sourced in guano and as a result have significantly elevated δ15N values (2, 15, 16, 23). These elevated δ15N values therefore become a tracer for the impact of seabird guano in the plant community.
The arid islands in the Gulf of California, Mexico manifest the effects of marine nutrient cycling to terrestrial systems. Bird islands— typically small (<3 km2), predator free, with low topography, that occur in high productivity waters — are utilized for habitat by a large quantity of seabirds. Due to high perimeter-to-area ratios, these small islands are disproportionally influenced by the surrounding marine environment (24). Guano excreta on bird islands is a significant component of both island appearance and island function, with bright white guano crusted over rock surfaces once as thick as 10 cm in some places (25). A variety of bird species are known to frequent bird islands; in the Gulf of California, species with the highest abundances include Heermann’s Gulls, Elegant Terns, Blue-footed Boobies, and Western Gulls (26).
These bird islands have also been shown to have significantly reduced plant diversity, likely due to the higher N and P nutrient concentrations that act as a filter (27), which has also been seen in other bird island systems (28). However, cacti are seen to occur in both higher diversity and abundance on bird islands (29). What then is the role of the marine nutrients on the structure of these island communities? We focus on the land-sea connections of several bird islands in the Midriff region of the Gulf of California, including several of the most important seabird islands in Mexico. These islands, especially San Pedro Mártir and Cholludo are distinguished by a forest of the widespread Sonoran Desert columnar cactus Pachycereus pringlei (S. Watson) Britton & Rose (cardón or sahueso, Cactaceae), which cover the island and contributes a shocking amount of plant biomass in such an arid setting (29) (Figure 1).
We use nitrogen stable isotope ratios to (a) test if there is a trophic cascade that originates in the ocean, is linked to land by seabirds and their guano, deposited into the soil, and then utilized by the tissue of the cardón, and (b) assess if this nutrient transfer is a manifestation of sea to land connections on seabird islands that is not found in mainland habitats or islands without seabird colonies.