Some isolated systems, such as oceanic islands, can support relatively complex food webs due to the input of nutrients via seabirds (Polis and Hurd 1996; Polis et al. 1997a; Ellis 2005). This allows a connection between low-productivity habitats (“receptor habitats”) and environments with higher primary productivity (“donor habitats”); these processes drive the trophic and ecological dynamics of connected ecosystems (Polis and Hurd 1995; 1996a, Polis and Strang 1996; Polis et al. 1996, 1997a; Anderson and Polis 1999; Caut et al. 2012).
The terrestrial ecosystem of Malpelo FFS is a small insular system with a limited capacity for atmospheric nitrogen fixation; it is therefore highly dependent on external nitrogen. Sula granti plays an important role in supplying nitrogen from the marine environment (Wolda 1975; López-Victoria et al. 2009), resulting in an increase in the isotopic nitrogen concentration of the terrestrial environment. This seabird provides high quantities of nutrients in the form of guano, feathers, eggs, carcasses, chick remains, juveniles, and adults, in addition to food waste of marine origin, such as fish and squid (López-Victoria and Werding 2008; López-Victoria et al. 2009, 2013). This highlights its importance in the transport of nutrients from the marine to the terrestrial ecosystem (Burger et al. 1978; López-Victoria et al. 2009). The same seabird-dependent process of transfer of energy and matter has been observed in the islands of the Gulf of California, Mexico (Anderson and Polis 1999; Sánchez-Piñero and Polis 2000), in Baccalieu Island, Canada (Duda et al. 2020), the Pacific and Indian Oceans, as well as in the Mediterranean Sea (Caut et al. 2012).
Terrestrial macro-species (i.e., A. agassizi, D. millepunctatus, and J. malpilensis) had similar δ13C values to those of the marine ecosystem; they were supported by the presence of seabirds as nutrient assimilators from the marine to the terrestrial ecosystem (Caut et al. 2012). This could be due to: 1) the similarity in isospace amplitude between the terrestrial (excluding terrestrial C3 plants) and marine ecosystems; 2) the high isotopic overlap between the two ecosystems; and 3) the similarity between the δ13C of terrestrial detritus, S. granti eggs, marine macroalgae, and marine crustaceans. The high contribution of detritus to terrestrial consumers (Fig. 4B) suggests that the carbon in terrestrial organisms comes from the marine environment (Table 1). Their δ13C signals are similar to those of marine primary producers in Malpelo FFS (i.e., macroalgae: − 21.0‰ to − 16.0‰; phytoplankton: − 20.7‰ to − 15.5‰ [this study]), as a result of transport and deposition of nutrients by S. granti and its “byproducts” (López-Victoria and Werding 2008; López-Victoria et al. 2009, 2013), and not from terrestrial primary producers (i.e., terrestrial C3 plants). Conversely, grasses (i.e., Paspalum sp.) are C4 plants, and similarly to C3 plants, they have a high C:N ratio (C3 Malpelo Island = 13.5–18.7); thus, they would not be the main source of protein of the terrestrial ecosystem. However, it should be noted that no samples of C4 or CAM plants were collected, mainly due to the reduced plant cover in the study area.
On the contrary, the orders Diplopoda (millipedes) and Microcoryphia reflected a higher contribution of terrestrial C3 plants (Fig. 4B), which is consistent with the food preferences of these taxa (Bueno-Villegas 2012; Bach de Roca et al. 2015). These results reinforce the hypothesis that suggests a high reliance and trophic interaction between the marine and terrestrial ecosystems of Malpelo FFS (Wolda 1975; López-Victoria et al. 2009).
The decomposition of naturally 15N-enriched guano and seabird tissue (Anderson and Polis 1999) could be further 15N enriched due to the volatilization of 14N (Lindeboom 1984; Mulder et al. 2011) and to the fast mineralization of uric acid to ammonium (NH4+) from guano (Wainright et al. 1998). This leads to greater isotopic fractionation, provoking 15N-enrichment of the residual NH4+ reservoir (Mizutani and Wada 1988; Wainright et al. 1998). Plants fertilized with guano have 15N-enriched values (Anderson and Polis 1999), similar to the soil (Croll et al. 2005; Maron et al. 2006). Conversely, organisms that consume guano and those who include other seabird byproducts in their diet (i.e., feathers, eggs, carcasses; Barrett et al. 2005; López-Victoria et al. 2009) have higher δ15N values; consequently, they have a higher trophic position than their prey (e.g., seabirds) or present higher tissue 15N-enrichment.
In this regard, terrestrial C3 plants of Malpelo FFS should reflect 15N-enrichment, as has been documented for islands in the Gulf of California (C3 plants = 24.5 ± 1.1‰, C4 = 24.3 ± 1.4‰; Barrett et al. 2005). However, terrestrial C3 plants of Malpelo FFS evidenced a different pattern (low δ15N values; Fig. 2). Values found for these plants are consistent with atmospheric nitrogen fixation, and were impoverished in 15N relative to the eggs and feathers of S. granti (Fig. 7). Similar results were reported for Possession Island in the Indian Ocean (plants = 5.2 ± 1.05‰ SD, seabirds = 9.34 ± 0.45‰ SD, enrichment = − 0.44; Caut et al. 2012). Therefore, it seems that terrestrial C3 plants of Malpelo FFS do not obtain N indirectly from guano nor from the solids of seabirds (Caut et al. 2012). Primary consumers (i.e., Isopoda and ants Odontomachus sp.) and terrestrial secondary consumers (i.e., A. agassizi, D. millepunctatus, and J. malpilensis), incorporate 15N directly from the consumption of S. granti and its byproducts (López-Victoria and Werding 2008; López-Victoria et al. 2009, 2013). This indicates 15N-enrichment relative to the eggs and feathers of S. granti (Fig. 6).
The S. granti colony positively impacts terrestrial communities of Malpelo FFS due to the high contributions of guano and other “byproducts” that terrestrial species consume directly (Polis and Hurd 1996; Sánchez-Piñero and Polis 2000). This is reflected in the high abundances of J. malpilensis (estimated population: 833,000 individuals; López-Victoria and Werding 2008), D. millepunctatus (12,000–18,000 individuals; López-Victoria et al. 2011), and A. agassizi (60,000–102,000 individuals; López-Victoria et al. 2011) present in Malpelo FFS. In contrast, the large S. granti colony could negatively affect the population of terrestrial C3 plants (28 species; González-Román et al. 2014) by reducing their cover on the island.
This phenomenon has been observed on Malpelo island (S. Bessudo Lion, personal communication). It could be related to: 1) the high concentrations of guano during the dry season that could exceed the concentration limits of essential nutrients and eventually toxify the soil and limit the development of plants; this could also prevent the establishment of native plants in places where there is a high density of seabirds (Boutin et al. 2011; Sánchez-Piñero and Polis 2000) and 2) the reduction of nutrients due to guano washing off during the rainy season, which limits soil formation and affects the adequate development of plants (Caita and Guerrero 2000).
There is a high input of nutrients (mainly from marine origin) from the terrestrial environment (e.g., organic matter, seabird guano, etc.) into the sea at Malpelo FFS, due to runoff from frequent and abundant rains between May and December (annual precipitation ~ 2,500 mm; von Prahl 1990; López-Victoria and Estela 2007). Terrestrial nutrients could affect primary producers locally, altering the typical values of marine primary productivity surrounding Malpelo FFS and modifying seasonal marine trophic dynamics (Ishida 1996; Wait et al. 2005); as a result, this would be reflected in their isotopic values. Despite the contributions of terrestrial nutrients to the sea and the effects that these contributions may have on the dynamics of this ecosystem, more studies are necessary to validate these hypotheses and identify other trophic connectivity routes between the terrestrial and marine ecosystems of Malpelo FFS.
Finally, an important control by the “donor” habitat (marine ecosystem) over the “receptor” habitat (terrestrial habitat) was evidenced by the transport and contribution of matter and energy between ecosystems (Polis et al. 1997a). The transport of nutrients from sea to land in Malpelo FFS is governed mainly by S. granti. However, there are other inputs in the sea-land interface, which are generated in the intertidal zone when J. malpilensis and D. millepunctatus consume marine algae and marine crabs (Grapsus grapsus), respectively (López-Victoria et al. 2009, 2013). Nevertheless, this source of input of marine nutrients into the terrestrial ecosystem has not been studied in detail. More studies are necessary to estimate the contribution of the intertidal zone and terrestrial ecosystem in Malpelo FFS. In turn, this would improve ecological knowledge regarding the dynamics of this small oceanic island.
Given the impact exerted by the donor habitat on the receptor habitat, it is possible that an eventual disturbance of marine populations may alter food webs, due to the transitional interphase between the marine and insular environment (Sullivan and Manning 2019). The present study documented trophic interactions between marine and terrestrial ecosystems, providing support to how diverse species can cross the limits of distinct environments (e.g., terrestrial and aquatic). Furthermore, this study evidenced how stable isotope analysis constitutes a useful tool in the identification of trophic interactions between terrestrial and marine ecosystems.