Trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia, evaluated through stable isotope analysis

doi:10.21203/rs.3.rs-1439817/v1

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Trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia, evaluated through stable isotope analysis

https://doi.org/10.21203/rs.3.rs-1439817/v1

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published 31 Dec, 2022

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Living beings inhabit heterogeneous environments, in which communities that are classified as discrete can be continuous and connected in innumerable ways. The components of food webs can cross borders between ecosystems, and as result, the structure and trophic dynamics of ecosystems can change. The goal of this study was to evaluate trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia (4º00’05.63” N; 81º36’36.41” W), based on the isotopic (δ¹³C and δ¹⁵N) assessment of 403 samples (107 terrestrial and 296 marine). Samples were collected in 2017–2021. δ¹³C_Terrestrial values ranged from − 30.3‰ to − 15.0‰ and δ¹³C_Marine ranged from − 24.0‰ to − 9.8‰; δ¹⁵N_Terrestrial ranged from 3.7‰ to 21.3‰ and δ¹⁵N_Marine ranged from 4.5 to 16.9‰. The mixing model (simmr package) indicated that detritus_Terrestrial (δ¹³C = − 18.9 ± 0.30‰ SE) contributed more to the food web than C₃ plants (–29.4 ± 0.22‰), and reflected high δ¹³C_Marine content. There was high isotopic overlap (65–82%) and a high trophic connection between environments of Malpelo Island due to high similarity between isospaces. These results evidence the role of the donor habitat (marine) on the receptor habitat (terrestrial) and the role of the Nazca booby Sula granti regarding nutrient transfers between the two environments. The presence and preservation of this seabird is essential to maintain the balance of this insular ecosystem. The analysis of δ¹³C and δ¹⁵N tracers was useful to establish the trophic relationships between small oceanic island environments with presence of large seabird communities.

chemical tracers

islands

Sula granti

trophic interactions

trophic webs.

Communities categorized as discrete can be open and connected in innumerable ways due to external factors (Holt 1993; Menge 1995; Schindler et al. 1996; Polis et al. 1996; Rooney et al. 2003) that allow the basic components of food webs (i.e., nutrients, detritus, and organisms) to cross the spatial limits of ecosystems (Polis et al. 1997a). This is related to the shape (complexity; Kent and Wong 1982) and size of the ecosystem (Post et al. 2000; Vander Zanden and Vadeboncoeur 2002; McCann et al. 2005; Dolson et al. 2009). The strength of the interactions of mobile generalist predators can be limited (McCann et al. 2005) by the degree of accessibility to different ecosystems (Dolson et al. 2009). These spatial processes impact the trophic structure and dynamics of ecosystems. This is evidenced by allochthonous inputs from different sources (e.g., transport of detritus and nutrients by mobile consumers) that can in turn influence energy, carbon, and nutrient reservoirs (i.e., nitrogen and phosphorus) (Polis and Hurd 1996a; Polis et al. 1997b; Schindler and Scheuerell 2002).

A key element in the trophic dynamics of islands and coastal areas is subsidy from a donor habitat through marine allochthonous inputs (Polis and Hurd 1996a; Polis et al. 1997b). Although islands can have low terrestrial primary productivity (Caut et al. 2012), they can support high abundance and biomass (i.e., secondary production) of consumers, such as spiders, scorpions, lizards, and rodents that are subsidized by marine contributions (Sánchez-Piñero and Polis 2000; Moore et al. 2004). On islands, these allochthonous inputs are mainly incorporated from two sources: 1) seabird colonies and 2) marine detritus transported across beaches (Polis and Hurd 1995, 1996b). This also contributes to combating nutrient limitation (i.e., nitrogen and phosphorus) of primary producers.

Malpelo Island is a small oceanic island (1.2 km²; Graham, 1975) located in the Colombian Pacific. Its geographical isolation and position at the convergence of several marine currents (Fig. 2) mean that this island is an ideal place for the aggregation of species (endemic and migratory). This has led to this island becoming part of the largest marine protected area in the Colombian Pacific, the Malpelo Fauna and Flora Sanctuary (FFS) (Fig. 2) (Ministry of Environment and Sustainable Development, 2017). It is a World Heritage Site (UNESCO) and is included in other important lists for the conservation of species (Management Plan, 2015). These characteristics and its importance for ecological communities mean that Malpelo FFS is an ideal site for the study of trophic interactions between ecosystems and of the input of marine nutrients to the terrestrial environment, due to its low terrestrial primary productivity. Considering its topography, complicated access, and the presence of the largest nesting colony of the Nazca booby Sula granti (> 80,000 individuals; López-Victoria and Rozo 2007; García 2013), terrestrial ecosystem structure and trophic dynamics could be directly and/or indirectly affected by the input of marine nutrients in the form of S. granti guano, chicks, food remains, and carcasses, denoting high connectivity between ecosystems (Wolda 1975; von Prahl 1990; López-Victoria et al. 2009).

Variations in the donor-controlled habitat (i.e., marine ecosystem; Polis et al. 1997a) could cause modifications in the community ecology of Malpelo FFS (Wolda 1975), with drastic consequences on species composition and trophic dynamics at landscape scales (Polis and Hurd 1995; Nakano et al. 1999). Changes in the feeding habits of S. granti could result in changes to the role this seabird plays in the trophic connectivity between the two ecosystems (Wolda 1975; von Prahl 1990; López-Victoria et al. 2009). Several studies have indicated that of the total energy contributed by S. granti, 99% corresponds to guano, 0.64% to eggs and chicks, and 0.06% to carcasses (López-Victoria et al. 2009). These are important dietary components of the dotted galliwasp Diploglossus millepunctatus, the Malpelo anole Anolis agassizi, the terrestrial crab Johngarthia malpilensis, and other invertebrates (López-Victoria 2006, López-Victoria and Werding 2008, López-Victoria et al. 2011).

Trophic studies based on the observation of terrestrial macro-species from Malpelo FFS (e.g., A. agassizi, D. millepunctatus, J. malpilensis, Phyllodactylus transversalis; López-Victoria 2006; López-Victoria and Werding 2008; López-Victoria et al. 2011; López-Victoria et al. 2013), including trophic relationships with S. granti, have shown the importance of this avian species in the trophic dynamics (López-Victoria et al. 2009) and stability of the terrestrial ecosystem, due to energy input from the sea (Wolda 1975; von Parhl 1990; López-Victoria et al. 2009). However, previous trophic studies based on direct observations, as well as stomach contents analysis carried out on several terrestrial species of Malpelo FFS, should be complemented with other methods to strengthen the hypothesis raised by other studies (i.e., Wolda 1975; von Parhl 1990; López-Victoria et al. 2009). Stable isotope analysis (SIA) is a complementary approach that counters some of the limitations of previous studies, e.g., use of stomach contents analysis and direct observations, which only provide a temporal snapshot of food ingested. SIA allows the identification of sources of carbon and nitrogen that constitute food assimilated over the short- and long-term (e.g., Kim et al. 2012; Estupiñán-Montaño et al. 2019). The isotopic signal depends on the trophic level and origin of the diet, as well as on ingestion rates, accumulation, turnover rates of assimilated tissue, and growth, among other factors (Fry and Arnorld 1982; Tieszen et al. 1983).

Three main objectives were addressed in this study to determine the degree of coupling between the terrestrial and marine environments of Malpelo Island: 1) the assessment of δ¹³C and δ¹⁵N values of the biological components of the terrestrial and marine environments of Malpelo FFS; 2) the identification of the primary sources that support the terrestrial food web; and 3) the evaluation of the trophic connectivity between the two ecosystems in Malpelo FFS. The general aim was to provide new evidence that S. granti is the main mediator in the transfer of matter and energy between the two ecosystems and generate new ideas to clarify some hypotheses, such as: i) the terrestrial food web has a low dependence on terrestrial C₃ plants due to their low abundance; therefore, terrestrial debris should provide the greatest contribution to the different components of the terrestrial food web; ii) the δ¹³C of terrestrial debris is similar and/or varies slightly in relation to δ¹³C of basal sources and consumers at low marine trophic levels, as well as S. granti eggs; iii) terrestrial C₃ plants should reflect high values of δ¹⁵N, since N is found in high concentrations in S. granti guano; and iv) terrestrial and marine ecosystems should evidence high isotopic overlap as a result of the high connectivity between them.

2.1. Study area

Malpelo Island (Fig. 1A) is the summit of a submarine mountain range called the Malpelo Ridge, which extends in a NE-SW direction; it is approximately 241.4 km long by 80.5 km wide (Fig. 1B, red polygon). The island has a maximum height of 300 m above sea level and emerges from approximately 4,000 m depth (Fig. 1C).

Malpelo Island constitutes the largest marine reserve in the Colombian Pacific and is commonly referred to as the Malpelo Fauna and Flora Sanctuary (FFS). It is located ~ 390 km from the coast of Buenaventura (4º00’05.63” N; 81º36’36.41” W; Fig. 1B; Management Plan 2015). Malpelo FFS comprises 11 islets (Fig. 1A) and a ~ 2.7 million hectare protected area (Fig. B; yellow polygon; Ministry of Environment and Sustainable Development, 2017). It is influenced by several marine currents due to its geographic location (Fig. 1D). Moreover, there is high productivity as a result of annual upwelling that supplies nutrients from deep waters. This upwelling supports a diverse and abundant community of consumers whose growth is reliant on this productivity (Rodríguez-Rubio and Stuardo 2002).

Despite its physical characteristics (volcanic rock), several plant and animal species inhabit the island (Management Plan 2015). There are 28 plant species on the island, including algae, lichens (i.e., Caloplaca sp., Candelabria sp., Lecidea sp., and Pyxine sp.), a moss (Octoblepharum albidum), a C₄ grass (Paspalum sp.), a legume, a fern (Pityrogramma calomelanos), and unidentified shrubs (von Prahl 1990; González-Román et al. 2014).

The terrestrial fauna of the island includes ~ 40 species of invertebrates (Wolda 1972; Management Plan 2015), such as ants (Odontomachus bauri), beetles (Platynini sp.), an endemic decapod crustacean (J. malpilensis), three species of endemic reptiles (A. agassizi, D. millepunctatus, and Phyllodactus transversalis), and a high diversity of migratory and resident birds (> 60 species; Management Plan 2015). The largest S. granti nesting colony in the world has been established on Malpelo Island; this is the most abundant bird in the area (López-Victoria and Rozo 2007; García 2013).

2.2. Collection of samples

Samples of 16 terrestrial and 38 marine species/functional groups (Table 1) were collected in 2017–2021 in Malpelo FFS, Colombia (Fig. 1A). All terrestrial samples were collected in October 2018. Samples of terrestrial vertebrates consisted in 1–2 cm of tissue collected from the posterior portion of the tail of A. agassizi and D. millepunctatus, and body feathers of S. granti. For invertebrates such as the land crab J. malpilensis, one of the hind limbs was collected, whereas invertebrates (i.e., millipedes, isopods, spiders, worms, crickets, and ants; Table 1) were collected whole.

Table 1
Components of the terrestrial and marine ecosystems of the Malpelo Fauna and Fauna Sanctuary represented by taxa with scientific and common names, number of samples (n), and average isotopic values ± standard deviation (SD) of δ¹³C and δ¹⁵N.
Code	Taxa		n			C:N		δ¹³C (‰)
Code	Scientific name	Common name	n			Mean ± SD		Min		Max			Mean			SD			Min			Max			Mean		SD
	Terrestrial Ecosystem
1	Anolis agassizi	Lizards			8		3.5 ± 0.10		–18.2		–16.0	–16.8			0.67			13.5			15.5			14.4					0.58
2	Araneae	Spiders			8		5.3 ± 1.31		–21.0		–17.5	–19.6			1.27			16.8			28.4			20.6					4.9
3	Diploglossus millepunctatus	Dotted galliwasp			9		3.6 ± 0.64		–18.3		–15.0	–15.8			1.03			13.6			15.3			14.5					0.48
4	–	Detritus			5		5.4 ± 0.22		–20.1		–18.4	–18.9			0.66			9.5			13.0			10.8					1.3
5	Gryllidae	Crickets			5		4.5 ± 0.42		–20.6		–18.4	–19.3			0.53			9.7			13.4			11.9					0.92
6	–	Guano			1		1.2		–		–	–19.3			–			–			–			14.2					–
7	Hymenoptera				4		4.5 ± 0.36		–20.3		–19.4	–20.0			0.39			11.0			14.3			13.3					1.53
8	Sula granti^§	Nazca booby (eggs)^†			8		4.3 ± 0.41		–19.5		–18.2	–18.6			0.44			13.1			14.1			13.6					0.36
9	Isopoda	Mealybugs			9		7.0 ± 0.29		–17.5		–15.0	–16.4			0.82			15.1			17.9			16.8					1.04
10	Johngarthia malpilensis	Terrestrial crabs			12		3.2 ± 0.07		–17.1		–15.5	–16.5			0.45			14.9			17.0			15.8					0.6
11	Diplopoda	Millepede			15		6.3 ± 0.91		–22.9		–18.6	–20.7			1.17			6.4			15.7			11.7					2.38
12	Lumbriculidae	Worm			6		4.8 ± 0.34		–18.7		–17.0	–18.1			0.6			17.2			20.4			19.1					1.12
13	Mycrocorifia	Rock jumpers			7		4.1 ± 0.30		–21.4		–19.6	–20.5			0.6			10.3			19.4			14.1					3.41
14	Odontomachus sp.	Ants			12		4.1 ± 0.41		–18.4		–16.3	–17.2			0.82			15.5			19.2			16.7					1.02
15	–	Mosses			8		15.9 ± 1.71		–30.3		–28.7	–29.4			0.62			3.8			10.1			7.4					2.25
16	Sula granti^§	Nazca booby (feathers)			9		3.3 ± 0.05		–16.7		–16.1	–16.3			0.2			13.5			15.2			14.3					0.49
	Marine Ecosystem
1	–	Green algaes		6			14.6 ± 2.71		–21.0		–17.1			–18.7			1.58			4.6			5.6			5.2		0.46
2	Padina sp.	Brown algaes		4			13.3 ± 1.42		–18.1		–16.0			–17.2			0.93			6.5			7.8			7.3		0.63
3	Arcidae	–		1			3.6		–		–			–17.8			–			–			–			9.0		–
4	Balanidae^‡	–		2			4.2 ± 0.35		–18.1		–15.7			–16.9			1.70			9.5			10.0			9.8		0.35
5	Balistidae	Triggerfishes		3			3.3 ± 0.00		–18.1		–17.8			–18.0			0.19			12.1			13.1			12.7		0.53
6	–	Unidentified shrimp		8			4.8 ± 0.45		–18.7		–16.5			–17.3			0.69			8.2			11.6			9.3		1.03
7	Carangidae^‡	Jacks		12			3.4 ± 0.20		–18.3		–17.6			–18.0			0.19			11.9			13.7			12.8		0.53
8	Carcharhinidae	Requiem sharks		12			3.0 ± 0.07		–16.7		–16.1			–16.3			0.21			14.8			15.9			15.3		0.33
9	Chaetodontidae^‡	Butterflyfishes		2			3.5 ± 0.21		–17.5		–17.3			–17.4			0.12			12.7			14.3			13.5		1.12
10	–	Unidentified crustaceans		3			6.2 ± 1.55		–19.0		–11.7			–16.4			4.03			7.1			9.1			8.0		1.03
11	Dendrophylliidae^‡	Anthozoos		3			3.6 ± 0.70		–23.0		–21.8			–22.5			0.60			4.7			6.6			5.5		0.96
12	Epialtidae^‡	Crabs		1			7.5		–		–			–13.2			–			–			–			7.0		–
13	–	Sponges^‡		5			4.0 ± 0.20		–16.3		–14.9			–15.7			0.58			4.9			9.4			7.2		1.96
14	Exocoetidae^‡	Flyingfishes		4			3.6 ± 0.10		–17.8		–16.8			–17.5			0.47			9.6			10.9			10.3		0.55
15	–	Unidentified gastropds^‡		5			4.1 ± 0.36		–19.1		–15.4			–16.9			1.58			7.1			13.5			10.3		2.39
16	Gecarcinidae^‡	Crabs		2			6.2 ± 0.85		–15.7		–14.9			–15.3			0.60			8.2			8.2			8.2		0.01
17	Grapsidae^‡	Cangrejos anfibios		21			5.3 ± 1.58		–19.6		–10.0			–14.6			3.45			6.9			16.9			10.5		3.48
18	Inachidae^‡	Spider crabs		3			6.2 ± 0.55		–15.0		–12.6			–14.2			1.41			8.7			9.4			8.9		0.41
19	Lophiidae^‡	Rapes		5			4.2 ± 0.33		–18.9		–18.1			–18.6			0.36			8.6			13.3			11.1		1.97
20	Lutjanidae^‡	Snappers		36			3.5 ± 0.28		–19.3		–16.4			–17.4			0.62			9.8			15.0			13.7		1.10
21	–	Macroplankton^‡		23			6.6 ± 1.28		–23.2		–17.8			–21.4			1.02			4.6			10.8			7.2		1.53
22	Malacanthidae	Tilefishes		8			3.3 ± 0.04		–18.8		–18.0			–18.5			0.27			11.7			14.0			12.9		0.79
23	–	Microplankton^‡		9			7.9 ± 0.72		–20.7		–15.5			–18.6			1.79			4.8			8.3			6.0		1.06
24	Myliobatidae	Eagle rays		1			3.5		–		–			–15.2			–			–			–			13.1		–
25	Ommastrephidae^‡	Squids		5			4.1 ± 0.13		–18.1		–17.4			–17.7			0.31			10.1			10.8			10.5		0.26
26	Ostreoida^‡	Oysters		9			4.0 ± 0.53		–20.1		–18.3			–19.4			0.46			4.8			7.8			6.1		0.98
27	Palinuridae^‡	Lobsters		4			4.0 ± 0.06		–16.2		–15.8			–15.9			0.16			12.2			12.6			12.4		0.17
28	Parthenopidae^‡	Crabs		2			8.2 ± 0.35		–17.0		–11.5			–14.2			3.90			5.9			6.5			6.2		0.46
29	Penaeidae^‡	Shrimp		12			4.5 ± 0.48		–20.1		–17.7			–19.7			0.65			7.5			9.5			8.4		0.60
30	Pomacanthidae	Angelfish		3			3.3 ± 0.06		–18.1		–18.0			–18.0			0.03			12.4			13.7			12.9		0.71
31	Scombridae^‡	Tunas		12			3.6 ± 0.43		–17.9		–15.9			–17.1			0.56			12.0			14.6			13.2		0.80
32	Scorpaenidae	Scorpion fish		2			3.3 ± 0.07		–17.8		–17.8			–17.8			0.04			14.8			15.0			14.9		0.13
33	Serranidae^‡	Groupers		34			3.7 ± 0.59		–21.5		–16.2			–18.1			1.20			8.4			15.0			12.7		1.48
34	Sphyrnidae	Hammerhead sharks		14			3.1 ± 0.07		–16.6		–14.8			–16.0			0.50			15.0			16.4			15.9		0.42
35	Squillidae^‡	Mantis shrimp		1			4.7		–		–			–16.4			–			–			–			11.5		–
36	Stromatidae	Butterfishes		1			3.3		–		–			–17.3			–			–			–			12.3		–
37	Sulidae^†	Nazca booby		17			3.8 ± 0.60		–20.0		–16.1			–17.5			1.35			13.1			15.2			14.0		0.56
38	Synodontidae^‡	Lizardfish		1			4.3		–		–			–18.3			–			–			–			8.6		–
39	Xanthidae^‡	Crabs		1			7.7		–		–			–11.8			–			–			–			6.9		–
§ Species present in both ecosystems.
† δ¹³C values corrected with Elliot et al. (2014).
‡ δ¹³C values corrected with Kiljunen et al. (2006).

Marine samples were obtained at different depths (between 10–30 m) by scuba diving at different sites around Malpelo Island. Muscle tissue of teleost fishes and rays was obtained with a harpoon and/or Hawaiian hook, and from fish that had been illegally caught and seized by the authorities. Scalloped hammerhead (Sphyrna lewini) and silky shark (Carcharhinus falciformis) muscle tissue was obtained from Estupiñán-Montaño et al. (2017).

Plankton samples were collected around Malpelo Island with a “bongo” type net of 68, 90, and 294 µm mesh size; surface tows were conducted from the M/N Seawolf inflatable boats for 10 min at each sampling site around the island. Samples of the other marine species/groups (e.g., algae, crustaceans, gastropods, and oysters; Table 1) were collected by hand.

All collected samples (terrestrial and marine) were placed in pre-labeled zip-lock plastic bags, except for the plankton samples, which were stored in 250 ml plastic bottles. Samples were kept frozen on board the Pacific Diving Company’s M/N Seawolf for subsequent transfer to the laboratory. Sampling procedures were endorsed by Parques Nacionales de Colombia, through Memorandum 20177730007973 of 30 May 2017, issued by the Planning and Management Group.

2.3. Sample preparation and analysis

Samples were washed with distilled water, freeze-dried in an oven at 60 ºC for 24 h, and ground to a fine powder with an agate mortar. Approximately 0.23 to 0.97 mg of powder were obtained for each terrestrial sample and packed in 3.2 × 4-mm tin capsules.

The C:N ratio was estimated and compared to reference values; a C:N value ≤ 3.5 indicates no effect of lipid contents (Post et al. 2007), whereas values > 3.5 suggest high lipid content. δ¹³C values of terrestrial and marine samples (Table 1) with C:N values > 3.5 were mathematically normalized according to Kiljunen et al. (2006):

Where δ¹³C_adjusted is the δ¹³C after normalization and δ¹³C_measured is the δ¹³C obtained from the sample without lipid removal. D = 7.018, I = 0.048, and L is the proportional lipid content of the sample, estimated as L = − 20.54 + (7.24 × C:N) (Post et al. 2007).

Arthropods (i.e., ants, isopods, and millipedes; Table 1) were analyzed without extracting lipids because these organisms have an exoskeleton characterized by high chitin contents (e.g., Liu et al. 2019), which are reflected in high C:N values (> 3.5). Therefore, δ¹³C values of arthropods with C:N values < 7.0 were not normalized mathematically (Schimmelmann and DeNiro 1986; Webb et al. 1997; Pringle and Fox-Dobbs 2008). Otherwise, δ¹³C values were normalized according to Post et al. (2007) (Eq. 1).

S. granti feathers were cleaned of surface lipids and contaminants using a 2:1 chloroform:methanol solution, followed by two successive methanol rinses (Jaeger et al. 2009). The δ¹³C values of S. granti eggs were mathematically normalized because lipid extraction can alter δ¹⁵N by washing out nitrogenous compounds. In this case, the formula proposed by Elliot et al. (2014) was used:

\({\text{δ}}^{\text{13}}{\text{C}}_{\text{lipid-extracted}}={{\text{δ}}^{\text{13}}\text{C}}_{\text{non-extracted}}+1.47-2.72 \times {Log}_{10} \left(\text{C:N}\right)\) (Eq. 2)

Where δ¹³C_{lipid−extracted} is the δ¹³C after normalization and δ¹³C_{non−extracted} is the δ¹³C obtained from the sample without lipid removal.

Extraction of lipids and urea from elasmobranch muscle samples (i.e., sharks and rays; Table 1) was performed following the procedure described by Kim and Koch (2012). Stable isotope analyses were carried out in the Stable Isotope Laboratory of the Instituto Andaluz de Ciencias de la Tierra in Granada (CSIC-UGR), Spain. The isotopic composition (i.e., carbon and nitrogen) of terrestrial specimens was obtained using an online Carlo Erba NA 1500 NC elemental analyzer coupled online via ConFlo III interface to a Delta Plus XP mass spectrometer (EA-IRMS; ThermoQuest). Stable isotopes were reported as δ values per mil (‰) based on the following equation:

\({\text{δ}}^{\text{13}}\text{C} \text{or} {\text{δ}}^{\text{15}}\text{N}= \left(\frac{{\text{R}}_{\text{sample}}}{{\text{R}}_{\text{standard}}}-1\right)\) (Eq. 3)

where R is the isotopic ratio (¹³C/¹²C or ¹⁵N/¹⁴N) of the sample or the standard (V-PDB and AIR for carbon and nitrogen, respectively). Commercial CO₂ and N₂ were used as the internal standard for isotopic analyses. Internal standards of − 30.6‰ and − 11.7‰ (V-PDB) were used for δ¹³C analysis and internal standards of − 1.0‰ and + 16.0‰ (AIR) were used for δ¹⁵N. Standards were systematically interspersed among analytical batches; daily drift of the mass spectrometer was corrected and a precision factor < ± 0.1‰ for δ¹³C and δ¹⁵N was calculated. Reference gases and in-house standards (with different C:N ratios and isotopic composition) were calibrated against International Reference Materials for carbon (USGS-24 and IAEA-C6) and nitrogen (IAEA-N1, IAEA-N2, and IAEA-N3).

2.4. Relative contribution of potential basal sources

The relative contribution of potential terrestrial basal sources to the diet of terrestrial consumer groups was estimated with the package simmr (version 0.3) in R (R Core Team 2018). This model uses a Bayesian isotopic framework based on δ¹³C and δ¹⁵N values to estimate the proportional contribution of potential prey (in this case, basal sources) to a consumer’s diet (Parnell et al. 2013), including variability in model inputs such as trophic discrimination factor (TDF) values of consumers.

The following four steps were implemented (Supplementary material S1): 1) we selected two potential basal sources: terrestrial C₃ plants and terrestrial detritus (sources that consist of decomposing organic matter [DOM] and seabird feces; López-Victoria et al. 2009); 2) all terrestrial organisms were considered potential prey, due to feeding preferences (López-Victoria 2006; López-Victoria and Werding 2008; López-Victoria et al. 2011), and also consumers (i.e., mixing), except C₃ plants and detritus (basal sources); 3) due to the lack of specific TDFs for each terrestrial organism, we used the estimated mean TDF for terrestrial ecosystems (Δ¹³C = 0.5 ± 0.19‰ SD and Δ¹⁵N = 2.3 ± 0.24‰ SD; McCutchan et al. 2003), to minimize sources of uncertainty (i.e., environmental and physiological factors, trophic position, metabolic rates, growth rates; Phillips et al. 2014), to which mixing models are highly sensitive (Bond and Diamnon 2011, Phillips et al. 2014); and 4) the mixing model was adjusted to verify that the TDFs, potential prey, and consumers were consistent with the assumptions of the model (Smith et al. 2013). The mixing model adjustment was run with 10³ iterations with a 95% probability for the mixing polygon (Smith et al. 2013). The model was considered adequate if isotopic values were within 1% of the mixing model polygons (Reum et al. 2020). Finally, if the model was correctly adjusted, we ran the mixing model with the isotopic values of terrestrial Malpelo FFS consumer groups (Table 1). The mixing model was run with 10⁶ iterations, 10⁴ burn-in period, 100 thinning period, and 4 Markov Chain Monte Carlo (MCMC).

The basal δ¹³C_detritus of the terrestrial ecosystem was compared to the δ¹³C values of the following five marine groups: macroalgae, marine crabs, zooplankton, S. granti eggs, and flying fish. The values of the marine groups were corrected with the mean TDF for marine environments (Δ¹³C = 0.4 ± 0.17‰ SD; McCutchan et al. 2003) and compared statistically with a non-parametric paired test (Wilcoxon rank sum test).

2.5. ¹⁵N enrichment

¹⁵N enrichment of terrestrial components was estimated using δ¹⁵N values of detritus, eggs, and feathers of Sula granti as reference, as this species provides marine nutrients to the terrestrial ecosystem (García and López-Victoria 2007; López-Victoria et al. 2009). Relative ¹⁵N enrichment was calculated using the algorithm proposed by Estrada et al. (2006):

\(\text{E}\text{n}\text{r}\text{i}\text{c}\text{h}\text{m}\text{e}\text{n}\text{t} \text{i}\text{n} Y=\left(\frac{ {\delta }^{z}{Y}_{ x }- {\delta }^{z}{Y}_{S. granti\text{ eggs and/or feathers}}}{{\delta }^{z}{Y}_{S. granti\text{ eggs and/or feathers}}}\right)\) (Eq. 4)

where: Y is the element of interest (¹⁵N), z is the atomic mass of the element, and x are the terrestrial components (i.e., plants, A. agassizi, J. malpilensis, D. millepunctatus, ants, millipedes, and Isopoda; Table 1) relative to the reference component (i.e., Sula granti eggs and feathers).

2.6. Niche amplitude and isotopic overlap

To quantify the isotopic niche and isotopic overlap between ecosystems (terrestrial [with and without C₃ plants] vs. marine), we used the Stable Isotope Bayesian Ellipses (SIBER, Jackson et al. 2011) method available in the R package (R Development Core Team 2008). This analysis estimates ellipses that represent the “core isotopic niche” (Standard Ellipse Corrected Area, SEA_C) using a Bayesian approach and calculating covariance matrices that define the shapes and areas of the ellipses (Jackson et al. 2011).

The ellipses were corrected using a posteriori randomly replicated sequences (SEA_C = standard ellipse area correction, Jackson et al. 2011) and they represent the isotopic niche width of consumers. In addition, this method allows the estimation of the isotopic niche overlap of the consumer (in this study, isospace), based on the overlap between ellipses (Newsome 2007).

SIBER results were supported by the nicheROVER package in R (Lysy et al. 2014), which uses a probabilistic method to calculate niche regions and pairwise niche overlap using multidimensional niche indicator data. The niche regions are defined as the joint probability density function of the multidimensional niche indicators at a user-defined probability alpha (95%), while the package provides directional estimations of niche overlap (x vs y and y vs x), according to the species-specific distributions in the multivariate niche space (Lysy et al. 2014).

A total of 403 samples were collected in Malpelo FFS, 26.6% of which (n = 107) corresponded to the terrestrial ecosystem and 73.4% (n = 296) to the marine ecosystem (Table 1).

3.1. Carbon and nitrogen stable isotopes

δ¹³C values of the terrestrial ecosystem ranged from − 30.3‰ to − 15.0‰ and δ¹⁵N ranged from 3.7‰ to 21.3‰ (Table 1). Terrestrial C₃ plants (mosses) had the lowest average δ¹³C value (–30.3‰) and the dotted galliwasp Diploglossus millepunctatus had the highest average value (–15.0‰), with a total range in δ¹³C values of 15.3‰ (Fig. 2). The lowest δ¹⁵N value corresponded to the terrestrial C₃ plants (3.7‰), whereas the highest value was obtained for arthropods from the family Araneae (21.3‰), with a δ¹⁵N range of 17.6‰ (Fig. 2).

The carbon isotopic space of the marine ecosystem ranged from − 23.2‰ to − 10.0‰ for δ¹³C and from 4.5‰ to 16.9‰ for δ¹⁵N (Table 1). In this ecosystem, corals Dendrophylliidae had the lowest average δ¹³C value (–22.5‰) and the scalloped hammerhead shark Sphyrna lewini (Sphyrnidae; − 14.8‰) had the highest average value, with a range of 7.7‰ (Fig. 3). Brown algae (Dictyotaceae) showed the lowest δ¹⁵N values (4.5‰), while the scalloped hammerhead shark had the most positive value (16.4‰), with a range of 11.8‰ (Fig. 3).

3.2. Contribution of terrestrial basal sources to the trophic web

The fitted model (i.e., mixing polygons, subsequent predictive validations; Supplementary material S2A), suggested that these results explained the uncertainty of the TDFs and of the isotopic values of the 13 consumer groups (Supplementary material S2A). Therefore, the implementation of the mixing model was adequate to estimate the relative contribution of the different basal sources, confirmed by the Gelman-Rubin (Rhat) convergence diagnostic statistics, which was 1.00 for all parameters and suggested that there was convergence.

The organic matter present in the soil (δ¹³C = − 20.1‰ to − 17.3‰) (Figs. 4 and 5), reflected the isotopic signal of organic matter transferred from marine primary production. These results suggest a high input of δ¹³C from detritus towards the lizard Anolis agassizi, the crab Johngarthia malpilensis, and the dotted galliwasp D. millepunctatus. Terrestrial C₃ plants contributed mainly to the Orders Hymenoptera, Diplopoda, and Microcoryphia, which presented low δ¹³C values, resulting in a greater contribution probability from terrestrial C₃ plants (Fig. 4, Table 2).

Table 2

Compación de la probabilidad de contribución relativa de dos fuentes basales terrestres del Santuario de Fauna y Flora Malpelo, con respecto todos los grupos de consumidores terrestres.
Consumers	Contribution probability (%)
Consumers	C₃ Plants	Detritus
Hymenoptera	78.0	22.0
Isopoda	29.5	70.5
Odontomachus sp.	25.3	74.7
Gryllidae	54.2	45.8
Araneae	67.0	33.0
Microcoryphia	93.6	6.4
Lumbriculidae	41.7	58.3
Diplopoda	78.5	21.5
Anolis agassizi	10.4	89.6
Diploglossus millepunctatus	9.8	90.2
Johngarthia malpilensis	9.2	90.8

The basal δ¹³C_detritus of the terrestrial ecosystem was contrasted with the δ¹³C_{Corrected*TDF} values of five marine groups: δ¹³C_macroalgae (Wilcoxon rank sum test, W = 14, P = 0.21), δ¹³C_{phytoplankton} (Wilcoxon rank sum test, W = 24, P = 90), δ¹³C_{marine crabs} (Wilcoxon rank sum test, W = 84.5, P = 0.37), and δ¹³C_{S. granti eggs} (Wilcoxon Rank sum test, W = 33, P = 0.07), with statistically significant differences between the basal source of detritus and δ¹³C_zooplankton (Wilcoxon rank sum test, W = 110, P = 0.002) (Fig. 5).

3.3. ¹⁵N enrichment

The range of δ¹⁵N values indicated that terrestrial C₃ plants, as well as crickets, millipedes, and Hymenoptera, presented values compatible with terrestrial primary production (Craine et al. 2009; Amundson et al. 2003). However, species such as A. agassizi, D. millepunctatus, J. malpilensis, Isopoda, Araneae, Lumbricullidae, and Odontomachus sp. were enriched in ¹⁵N, presenting values incompatible with a diet based on the primary productivity of the island (i.e., C₃ plants) and with some groups associated with organic matter decomposition processes (e.g., consumption of detritus) (Fig. 6). High δ¹⁵N levels of terrestrial animals could be related to the high trophic level of S. granti (trophic level = 4.2 [3.9–4.4, CI 95%]; Estupiñán-Montaño et al. unpublished), due to prey consumed in the marine environment.

3.4. Isotopic niche and isotopic overlap

The wide isotopic range of carbon, and especially of nitrogen, in the terrestrial ecosystem reflected an isospace (TA_Terrestrial) of 134.7‰² and an isotopic niche (SEA_{C_terrestrial}) of 30.4‰² (Fig. 6A). After excluding terrestrial C₃ plants, the isospace and the isotopic niche were 65.1‰² and 17.3‰², respectively (Fig. 6B). The isospace and isotopic niche of the marine ecosystem (TA_marine = 117.2‰² and SEA_{C_marine} = 21.0‰²) were very similar to those of the terrestrial ecosystem, excluding C₃ plants (Fig. 7A, B).

Taking into account the low contribution of terrestrial C₃ plants to the terrestrial trophic web, two isotopic overlap scenarios were considered: one including C₃ plants and one excluding them. The terrestrial (C₃ plants; red box, Fig. 6A) and marine isospaces reflected an isotopic overlap of 0.85 (SIAR overlap; Fig. 7A), suggesting an overlap probability of 65% (nicheROVER) between the two ecosystems. In contrast, the marine isospace indicated a higher overlap probability with the terrestrial isospace (76%; Fig. 7A). In the second scenario, the estimated isotopic overlap between the terrestrial and marine isospaces was 0.71 (SIAR overlap; Fig. 7B), corresponding to 82% (terrestrial vs. marine) and 70% (marine vs. terrestrial) overlap between the two isospaces (Fig. 7B).

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.

Acknowledgements

C.E.M. would like to thank National Geographic, Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico), Instituto Politécnico Nacional, Parques Nacionales Naturales de Colombia, Santuario de Fauna y Flora Malpelo, Pacific Diving, the M/N Seawolf and its crew, and the Fundación Alium Pacific. F.G.M., F.R.E.V., M.J.Z.R., and A.S.G. thank the Instituto Politécnico Nacional for fellowships granted (COFAA and EDI). Additional thanks to the anonymous reviewers for their valuable comments to improve this manuscript.

Funding Fundación Alium Pacific supported and provided funds for sampling, the Instituto Andaluz de Ciencias de la Tierra (CSIC-UGR) provided funds for laboratory analysis, and National Geographic (Grant No. CP-059ER-17) provided funds for field work.

Conflicts of interest The authors declare that they have no conflict of interest.

Ethics approval All procedures performed in this study were in accordance with Parques Nacionales Naturales de Colombia in Memorandum 20177730007973 of May 30, 2017 by the Planning and Management Group.

Availability of data and material All data produced in this study are provided in this manuscript.

Authors contributions Conceptualization, data curation, formal analysis, investigation, and methodology: Colombo Estupiñán-Montaño. Writing – original draft preparation: Colombo Estupiñán-Montaño. Writing – review and editing: Manuel J. Zetina-Rejón, Felipe Galván-Magaña, Antonio Delgado-Huertas, Fernando R. Elorriaga-Verplancken, Carlos J. Polo-Silva, and Alberto Sánchez-González. Funding acquisition: Colombo Estupiñán-Montaño and Antonio Delgado-Huertas. All authors read and approved the final manuscript.

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You are reading this latest preprint version

Trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia, evaluated through stable isotope analysis

Status:

Journal Publication

Version 1

Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Study area

2.2. Collection of samples

2.3. Sample preparation and analysis

2.4. Relative contribution of potential basal sources

2.5. ¹⁵N enrichment

2.6. Niche amplitude and isotopic overlap

3. Results

3.1. Carbon and nitrogen stable isotopes

3.2. Contribution of terrestrial basal sources to the trophic web

3.3. ¹⁵N enrichment

3.4. Isotopic niche and isotopic overlap

4. Discussion

Declarations

References

Supplementary Files

Status:

Journal Publication

Version 1

Trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia, evaluated through stable isotope analysis

Status:

Journal Publication

Version 1

Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Study area

2.2. Collection of samples

2.3. Sample preparation and analysis

2.4. Relative contribution of potential basal sources

2.5. 15N enrichment

2.6. Niche amplitude and isotopic overlap

3. Results

3.1. Carbon and nitrogen stable isotopes

3.2. Contribution of terrestrial basal sources to the trophic web

3.3. 15N enrichment

3.4. Isotopic niche and isotopic overlap

4. Discussion

Declarations

References

Supplementary Files

Status:

Journal Publication

Version 1

2.5. ¹⁵N enrichment

3.3. ¹⁵N enrichment