Seabird guano reshapes intertidal reef food web in an isolated oceanic islet

Amaral FD, Hudson MM, Silveira FL, Migotto AE, Pinto SM, Longo L (2000) Cnidarians of Saint Peter and St. Paul Archipelago, northeast Brazil. In: Proceedings of 9th International Coral Reef Symposium, Bali, Indones, pp 23–27 Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46 Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574 Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Prim. Plymouth, 274 Andrades R, Jackson AL, Macieira RM, Reis-Filho JA, Bernardino AF, Joyeux J-C, Giarrizzo T (2019) Niche-related processes in island intertidal communities inferred from stable isotopes data. Ecol Indic 104:648–658 Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, Rose MD (2005) Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 109:145–153 Benemann VRF, Araújo LD, Fabbris AZ, Montone RC, Petry MV (2022) Nesting distribution of Masked Booby Sula dactylatra at Trindade Island, western South Atlantic Ocean. Mar Ornithol 195:189–195 Benkwitt CE, Wilson SK, Graham NAJ (2019) Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event. Glob Chang Biol 25:2619–2632 Benkwitt CE, Carr P, Wilson SK, Graham NAJ (2022) Seabird diversity and biomass enhance cross-ecosystem nutrient subsidies. In: Proc R Soc B Biol Sci, p 289. Bosman A, Hockey P (1986) Seabird guano as a determinant of rocky intertidal community structure. Mar Ecol Prog Ser 32:247–257 Bosman AL, Hockey PA (1988) The influence of seabird guano on the biological structure of rocky intertidal communities on islands off the west coast of southern Africa. South African J Mar Sci 7:61–68 Bosman AL, Du Toit JT, Hockey PAR, Branch GM (1986) A field experiment demonstrating the influence of seabird guano on intertidal primary production. Estuar Coast Shelf Sci 23:283–294 Both R, Freitas TR (2004) Aves marinhas no arquipélago de São Pedro e São Paulo. In: Branco JO (ed) Aves Marinhas e Insulares Brasileiras: Bioecologia e Conservação. Univali, Itajaí, pp 193–212 Caut S, Angulo E, Pisanu B, Ruffino L, Faulquier L, Lorvelec O, Chapuis JL, Pascal M, Vidal E, Courchamp F (2012) Seabird modulations of isotopic nitrogen on islands. PLoS ONE 7:1–7 Clarke KR, Gorley RN (2015) PRIMER v7: User Manual/Tutorial. Colombini I, Chelazzi L (2003) Influence of marine allochthonous input on sandy beach communities. Oceanogr Mar Biol an Annu Rev 41:115–159 Darwin C (1845) Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S. Beagle round the world: under the command of Capt. Fitz Roy, R.N. John Murray, London Darwin C (1873) Journal of researchers into the natural history and geology of the countries visited during the voyage of H.M.S Beagle round the world, under the command of Capt. Fitz Roy, R. A. D. Appleton and Company, New York De La Peña-Lastra S (2021) Seabird droppings: Effects on a global and local level. Sci Total Environ 754:142148 Duhart M, Ojeda FP (1994) Caracterización ictica de pozas intermareales y análisis trofico de peces herbivoros submareales de Isla de Pascua. Medio Ambient 12:32–40 Feitoza BM, Rocha LA, Luiz-júnior OJ, Floeter SR, Gasparini JL (2003) Reef fishes of St. Paul’s Rocks: new records and notes on biology and zoogeography. Aqua Int J Ichthyol 7:61–82 Ferreira RL (2019) Guano communities. In: White WB, Culver DC, Pipan T (eds) Encyclopedia of caves. Elsevier, Academic Press, pp 474–484 Fonseca-Neto FP (2004) Aves marinhas da Ilha Trindade. In: Branco JO (ed) Aves marinhas e insulares brasileiras: bioecologia e conservação. Editora da UNIVALI, Itajaí, SC, pp 119–146 Freire AS, Pinheiro MAA, Karam-Silva H, Teschima MM (2011) Biology of Grapsus grapsus (Linnaeus, 1758) (Brachyura, Grapsidae) in the Saint Peter and Saint Paul Archipelago, Equatorial Atlantic Ocean. Helgol Mar Res 65:263–273 Freire AS, Pinheiro MAA, Teshima MM, Madeira KC, Koettker AG, Silva H, Fonseca DB (2009) A vida do caranguejo Grapsus grapsus. In: Viana D.L., Hazin F.H.V., Souza M.A.C. (eds) O arquipélago de São Pedro e São Paulo: 10 anos de estação científica. SECIRM, Brasília, DF, pp 195–203 Fuentes EN, Zuloaga R, Almarza O, Mendez K, Valdés JA, Molina A, Pulgar J (2017) Upwelling-derived oceanographic conditions impact growth performance and growth-related gene expression in intertidal fish. Comp. Biochem. Physiol B Biochem Mol Biol 214:12–18 Gianuca D, Vooren CM (2007) Abundance and behavior of the sally lightfoot crab (Grapsus grapsus) in the colony of the brown booby (Sula leucogaster) in the São Pedro and São Paulo Archipelago. Investig Mar 35:121–125 Gouvêa AC, Mello TJ (2017) First record of a breeding colony of Masked Booby (Sula dactylatra Lesson, 1831; Sulidae) in the main island of the archipelago of Fernando de Noronha (Pernambuco, Brazil). Pap Avulsos Zool 57:137–139 Gove JM, McManus MA, Neuheimer AB, Polovina JJ, Drazen JC, Smith CR, Merrifield MA, Friedlander AM, Ehses JS, Young CW, Dillon AK, Williams GJ (2016) Near-island biological hotspots in barren ocean basins. Nat Commun 7:10581 Graham NAJ, Wilson SK, Carr P, Hoey AS, Jennings S, MacNeil MA (2018) Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559:250–253 Griffiths SP (2000) The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. J Fish Biol 57:1453–1464 Gunn RL, Benkwitt CE, Graham NAJ, Hartley IR, Algar AC, Keith SA (2023) Terrestrial invasive species alter marine vertebrate behaviour. Nat Ecol Evol 7:82–91 Herbert DA, Fourqurean JW (2008) Ecosystem structure and function still altered two decades after short-term fertilization of a seagrass meadow. Ecosystems 11:688–700 Hong J, Zhang J, Ma Y, Gu B, Lee R (2019) The fates of nitrogen in an experimental wetland food web: a stable isotope study. Wetlands 39:303–310 Horn MH, Martin KLM, Chotkowski MA (1999) Intertidal fishes: life in two worlds. Elsevier, San Diego Hutchinson GE (1950) Survey of existing knowledge of biogeochemistry. Bulletin of the American Museum of Natural History, New York Jones HP, Tershy BR, Zavaleta ES, Croll DA, Keitt BS, Finkelstein ME, Howald GR (2008) Severity of the effects of invasive rats on seabirds: a global review. Conserv Biol 22:16–26 Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated. Proc Natl Acad Sci U S A 105:3800–3804 Kussakin OG, Kostina EE (1996) The intertidal biota of volcanic Yankich Island (Middle Kuril Islands). Publ Seto Mar Biol Lab 37:201–225 Linhares BA, Bugoni L (2022) Seabirds subsidize terrestrial food webs and coral reefs in a tropical rat‐invaded archipelago. Ecol Appl, pp 1–16 Lorrain A, Houlbrèque F, Benzoni F, Barjon L, Tremblay-Boyer L, Menkes C, Gillikin DP, Payri C, Jourdan H, Boussarie G, Verheyden A, Vidal E (2017) Seabirds supply nitrogen to reef-building corals on remote Pacific islets. Sci Rep 7:1–11 Luiz OJ, Mendes TC, Barneche DR, Ferreira CGW, Noguchi R, Villaça RC, Rangel CA, Gasparini JL, Ferreira CEL (2015) Community structure of reef fishes on a remote oceanic island (St Peter and St Paul’s Archipelago, equatorial Atlantic): the relative influence of abiotic and biotic variables. Mar Freshw Res 66:739–749 MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, NJ Mancini PL, Bugoni L (2014) Resources partitioning by seabirds and their relationship with other consumers at and around a small tropical archipelago. ICES J Mar Sci 71:2599–2607 Mancini PL, Hobson KA, Bugoni L (2014) Role of body size in shaping the trophic structure of tropical seabird communities. Mar Ecol Prog Ser 497:243–257 Mancini PL, Serafini PP, Bugoni L (2016) Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Rev Bras Ornitol 24:94–115 Mendes LF (2000) História natural, biologia alimentar, repartição espacial, densidades populacionais e ecomorfologia dos gobióides e blenióides (Perciformes) do Arquipélago de Fernando de Noronha, PE. Universidade de São Paulo, SP Mendes LF (2009) Os peixes-macaco. In: Viana D.L., Hazin F.H.V., Souza M.A.C. (eds) O arquipélago de São Pedro e São Paulo: 10 anos de estação científica. SECIRM, Brasília, DF, pp 213–218 Metaxas A, Scheibling RE (1993) Community structure and organization of tidepools. Mar Ecol Prog Ser 98:187–198 Mohriak W (2020) Genesis and evolution of the South Atlantic volcanic islands offshore Brazil. Geo-Marine Lett, p 40. Pascoe P, Shaw J, Trebilco R, Kong S, Jones H (2021) Island characteristics and sampling methodologies influence the use of stable isotopes as an ecosystem function assessment tool. Ecol Solut Evid 2:1–12 Pequeño G (1986) Comments on fishes from the Diego Ramirez Islands. Chile Japanese J Ichthyol 32:440–442 Pimentel CR, Pinheiro HT, Giarrizzo T, Francini-Filho RB, Reis-Filho JA, Rocha LA, Ferreira CEL, Barbosa MC, Joyeux JC (2022) Ecological links between pelagic and mesophotic reef fishes in an oceanic archipelago of the equatorial Atlantic Ocean. Diversity 14:1–18 Pinheiro E, Layman CA, Castello JP, Leite TS (2017) Trophic role of demersal mesopredators on rocky reefs in an equatorial Atlantic Ocean island. J Appl Ichthyol 33:47–53 Plazas-Jiménez D, Cianciaruso MV (2020) Valuing ecosystem services can help to save seabirds. Trends Ecol Evol 35:757–762 Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147:396–423 Quimbayo JP, Giglio VJ, Ferreira CEL, Fraga A, Nunes JACC, Mendes TC (2020) Contrasting feeding and agonistic behaviour of two blenny species on a small and remote island in the equatorial Atlantic Ocean. J Fish Biol 96:74–82 Reddin CJ, Docmac F, O’Connor NE, Bothwell JH, Harrod C (2015) Coastal upwelling drives intertidal assemblage structure and trophic ecology. PLoS ONE 10:1–20 Richardson KM, Iverson JB, Kurle CM (2019) Marine subsidies likely cause gigantism of iguanas in the Bahamas. Oecologia 189:1005–1015 Saies AB (1973) The intertidal life of Ruamahua-Iti and Middle Island (Aldermen Islands). Tane 19:1–11 Sánchez-Piñero F, Polis GA (2000) Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81:3117–3132 Souza CS, Luz JAG, Macedo S, Montes MJF, Mafalda P (2013) Chlorophyll a and nutrient distribution around seamounts and islands of the tropical south-western Atlantic. Mar Freshw Res 64:168–184 Stapp P, Polis GA, Sánchez-Piñero F (1999) Stable isotopes reveal strong marine and El Niño effects on island food webs. Nature 401:467–469 Viana DF, Hazin FHV, Andrade HA, Nunes DM, Viana DL (2015) Fisheries in the Saint Peter and Saint Paul archipelago: 13 years of monitoring. Bol Do Inst Pesca 41:239–248 Vieira LM, Farrapeira CMR, Amaral FD, Lira SMA (2012) Bryozoan biodiversity in Saint Peter and Saint Pal Archipelago. Brazil Cah Biol Mar 53:159–167 Wait DA, Aubrey DP, Anderson WB (2005) Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity. J Arid Environ 60:681–695 Wootton JT (1991) Direct and indirect effects of nutrients on intertidal community structure: variable consequences of seabird guano. J Exp Mar Bio Ecol 151:139–153