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Marine Ecology Progress Series 519:13 Vol. 519: 13–27, 2015 MARINE ECOLOGY PROGRESS SERIES Published January 20 doi: 10.3354/meps11071 Mar Ecol Prog Ser Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem Renato Mitsuo Nagata1,*, Marcelo Zacharias Moreira2, Caio Ribeiro Pimentel3, André Carrara Morandini1 1Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, trav. 14, n. 101, 05508-090, São Paulo, Brazil 2Laboratório de Ecologia Isotópica, Centro de Energia Nuclear na Agricultura, Campus Luis de Queiroz, Universidade de São Paulo, Piracicaba, Brazil 3Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, Brazil ABSTRACT: Human-induced stresses on the marine environment seem to favor some jellyfish spe- cies to the detriment of other competitors such as planktivorous fishes. In pristine ecosystems, trophic relationships among these consumers are poorly understood. We determined stable carbon and nitrogen isotope signatures of representative consumers in the relatively pristine ecosystem of the Cananéia Estuary, Brazil, in order to understand the food web structure. We described isotopic niche breadth, position, and overlaps between fish and jellyfish (including comb jelly) species. Most of the δ13C values suggest that phytoplankton is the major carbon source, especially for pelagic consumers. Sessile benthic invertebrates had enriched δ13C values, suggesting a contribu- tion of microphytobenthic algae. Seasonal variation of values was significant only for 13C, with dif- ferent patterns for pelagic and benthic organisms. Isotopic niche breadth of some jellyfishes was wider than those of fish species of the same trophic group, possibly as a consequence of their broad diets. Isotopic niche overlaps of fish and jellyfish species were related to: (1) trophic diversity, since planktivorous species occupied niches distinct from macroinvertebrate/fish feeders; and (2) life stages, since isotopic niche partitioning pattern can change during species ontogeny. Replacement of declining populations of fish by jellyfish competitors probably depends on the pool of other compensatory species, as well as on reproductive, growth, and feeding performance of other con- sumers. Description of isotopic niches provides a general picture of trophic roles, interactions and the degree of functional redundancy among species, allowing an evaluation of possible directions of community shifts resulting from the removal or proliferation of keystone consumers. KEY WORDS: Gelatinous zooplankton · Trophic position · Forage fish · Dietary overlap · Stable isotopes Resale or republication not permitted without written consent of the publisher INTRODUCTION may increase have been widely discussed, and it has been speculated that human-induced stresses to the Although some controversies exist concerning marine environment (eutrophication, species intro- changes in the number and extension of jellyfish duction, climate change, overfishing) seem to favor blooms (Condon et al. 2012, Gibbons & Richardson the proliferation of gelatinous zooplankton species 2013), historical data from some parts of the world (Purcell 2012). Trophic interactions may account for show that jellyfish populations are increasing (Brotz these increases, since evidence suggests that the et al. 2012, Purcell 2012). Factors whereby jellyfish depletion of fish stocks has shifted some ecosystems *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 14 Mar Ecol Prog Ser 519: 13–27, 2015 from planktivorous fish- to jellyfish-dominated, such consumers (Sherwood & Rose 2005, Layman et al. as in the northern Benguela Current (Richardson et 2012). The position of consumers in the isotopic space al. 2009). (δ-space) also illustrates some aspects of the actual Because many jellyfish feed on fish eggs and ecological niche, such as habitat and resources used, larvae, top-down control is a possible explanation for in the concept of the ‘isotopic niche’ (Newsome et al. the inverse relationship between these populations, 2007). The isotopic values of a given group of com- as first stated by Möller (1980). The predation impact munity members can be analyzed to quantify aspects of jellyfish species can be high, with some species of their trophic ecology, such as species niche like Chrysaora melanaster in the Bering Sea and breadth and niche overlaps (Newsome et al. 2007, Aurelia sp. in Japan consuming 33% d–1 and 26% Jackson et al. 2011, Newsome et al. 2012). d−1, respectively, of standing stock zooplankton The productive waters of estuaries are used by dif- (Brodeur et al. 2002, Uye & Shimauchi 2005). Jelly- ferent fish species (including coastal and oceanic fish species have diverse feeding habits, yet their populations) to feed and as nurseries (Potter et al. ecological roles are often oversimplified (Condon et 2001). Because larvae and juveniles of most fish spe- al. 2012). Species occupy a variety of trophic levels, cies are zooplanktivorous, regardless of what they feeding on micro- and mesozooplankton, epibenthic eat in adulthood (Bond 1996), it is reasonable to sug- invertebrates, other jellyfish, and fish (Purcell 1997), gest that the trophic niche of juveniles of many fish and potentially use the same resources as many other species overlaps with that of zooplanktivorous jelly- consumers (such as crustaceans and fishes). Trophic fish. The South Brazilian Bight (SBB) (23° to 28°S) is a overlap between planktivorous jellyfish and fish transitional region of mixed climate and faunal com- populations was demonstrated in studies applying ponents with warm-temperate characteristics (Heile- stomach-content methods (Purcell & Grover 1990, man & Gasalla 2008). The coast of the central SBB Purcell & Sturdevant 2001) and stable-isotope ana - receives outflows from large adjacent estuarine sys- lyses (Brodeur et al. 2002, Brodeur et al. 2008, Shoji tems (Cananéia and Paranaguá) and harbors high et al. 2009). Richardson et al. (2009) argued that in zooplankton biomasses and ichthyoplankton densi- ecosystems dominated by fish, jellyfish populations ties (Lopes et al. 2006). A relatively high diversity of are kept in check through predation and competi- large jellyfishes (10 species of Cubozoa and Scypho- tion. Nevertheless, jellyfish may overtake fish com- zoa) (Morandini et al. 2005) with distinct trophic roles petitors when overfishing opens a vacant niche for is present. A historical baseline of field population the former, but also under some conditions such as: abundances and seasonality is lacking for jellyfish low oxygen concentrations, when feeding perform- (but see Nogueira et al. 2010), although a few studies ance of fish decreases (Shoji et al. 2005); and low have mentioned episodes of high biomasses in near - visibility, when visual foraging of fish is hampered by areas (Moreira 1961, Mianzan & Guerrero 2000, (Eiane et al. 1999). Graça-Lopes et al. 2002, Nagata et al. 2009). Because In order to understand the ecosystem’s response to of the good conservation status of the Cananéia the removal of a consumer, it is important to examine Lagoon Estuarine System (CLES) area (MMA 2007), the trophic position of several keystone species, an analysis of its food web structure represents a which probably will fill that vacated trophic niche. unique opportunity to understand the trophic role of Stable Isotope Analysis (SIA) has been used over the jellyfish at lower levels of anthropogenic stresses that past ~25 yr to describe food web structures of differ- are presumed to favor their proliferation. ent ecosystems, leading to huge advances in this field This study, thus, aims to provide a general picture (Layman et al. 2012). SIA data integrate spatial and of the food web structure of the CLES based on 13C temporal information and provide long-term evi- and 15N isotope signatures of species of mesozoo- dence of trophic relationships that cannot be gleaned plankton, gelatinous zooplankton, demersal macro- from ‘snapshot’ dietary analysis (Layman et al. 2012). fauna, and nekton. We analyzed isotope data in order Although stomach-content analyses provide valu- to answer the following questions: (1) Knowing that able insights into feeding relationships, they have the main sources of organic matter in the CLES, analytical limitations, since they require many sam- phytoplankton, mangrove litterfall, and microphyto- ples and do not always reflect the assimilated food. benthos (Schaeffer-Novelli et al. 1990), have distinct Studies with SIA can evaluate the trophic structure of δ13C values, what is their respective contribution to many coastal ecosystems, by investigating issues the consumers of this ecosystem? (2) How much do such as the primary sources of organic matter, as well isotopic signatures vary during an annual cycle? (3) as the energy pathways through a large number of Based on recently developed Bayesian statistical Nagata et al.: Isotopic niche partitioning between fish and jellyfish 15 tools for SIA, do jellyfish and other consumers (mainly fish) occupy similar isotopic niches in this ecosystem? For this last question, we compared iso- tope data of known dominant pelagic species (jelly- fish and fish consumers) to assess isotopic niche breadth, seasonal variability, and possible overlaps. Note that in this article we use the term jellyfish syn- onymously with the term gelatinous zooplankton, i.e. we include ctenophores as well as cnidarians.
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