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Communication

Feeding Ecology of Sicydium bustamantei (Greeff 1884, Gobiidae) Post-Larvae: The “Little Fish” of São Tomé Island

1
Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
2
Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixões, 4450-208 Matosinhos, Portugal
3
Associação Programa Tatô—Sítio da Pedragosa, 8600-013 Barão de São João, Portugal
*
Author to whom correspondence should be addressed.
Submission received: 28 August 2020 / Revised: 29 October 2020 / Accepted: 30 October 2020 / Published: 5 November 2020
(This article belongs to the Special Issue Fish Larval Biology and Ecology)

Abstract

:
The rivers of São Tomé Island are colonized by Sicydium bustamantei (Greeff 1882), an amphidromous fish that spawns in those areas. After hatching, larvae drift to the ocean with the river flow. In the marine realm, the planktonic larvae develop and migrate to freshwater as post-larvae. The migrations of post-larvae support important local fisheries at the mouth of rivers in tropical volcanic islands. Amphidromous post-larvae rely on plankton as their main source of organic matter. However, the biology and ecology of S. bustamantei in the West African islands are understudied, despite its importance for local fisheries. Thus, this study aimed to start bridging this gap by studying its feeding ecology. Our objectives were to identify the main prey of S. bustamantei post-larvae, combining gut content with stable isotope analyses. The gut contents included zooplankton (Chaetognatha, Ostracoda, and unidentified crustaceans), debris from plant and/or macroalgae-derived material, and microplastics (including microfibers). The stable isotopes analysis indicated that zooplankton and macroalgae detritus were the main sources of organic matter assimilated by this species. We also demonstrated that S. bustamantei post-larvae are omnivorous and secondary consumers. These data provide pioneering information that can be used in management plans that still need to be developed.

Graphical Abstract

1. Introduction

Amphidromy is a type of diadromy that requires freshwater-marine connectivity in the early stages of a species life cycle [1,2]. Amphidromous species such as gastropods, decapods, and fish are adapted to tropical and subtropical insular environments [2,3,4,5].
The Sicydiinae subfamily (Gobiidae) is typically associated with small oceanic islands with geologically recent volcanic origin [6,7,8]. They inhabit swift, high-gradient rainforest streams and rivers with large waterfalls and elevation changes [3] which are generally oligotrophic and exposed to extreme hydrological and climatic seasonal variability [3,8]. Sicydiinae fish are found in the Indo-Pacific, West Africa, Central America, and Caribbean regions [3,6,7,8,9] and have relatively high levels of endemism [6]. Adults spawn in freshwater and larvae drift seawards upon hatching (downstream migration), where they undergo a planktonic phase [3,6,7]. After several months at sea (one to nine months, depending on the species) [3,5,10,11], post-larvae recruit and migrate to rivers (upstream migration or return migration) where they settle, grow, and reproduce [3,6,7].
Post-larvae support significant artisanal fisheries during the return migration (goby-fry fisheries), with significant nutritional, cultural, and socio-economical value in developing tropical and sub-tropical countries [3,5,7,8,11]. Returning post-larvae can be caught using beach seine nets made from mosquito nets or traps (baskets) made from vegetable fibers [12,13]. Globally, goby-fry fisheries are declining due to the degradation and loss of suitable habitat and river–ocean connectivity due to instream barriers (e.g., channelization, riverine and coastal zone development), and overfishing [7,12,14,15]. Goby-fry fisheries are largely unmanaged, with insufficient biological and fishery data [7,15], albeit some species are listed as endangered [12].
In São Tomé island (São Tomé and Príncipe archipelago), Sicydium bustamantei (Greeff 1882), called “peixinho” (little fish), is caught as post-larvae in several rivers (e.g., the Io-Grande, Manuel Jorge, Malanza, and Ouro Rivers) and sold in local fish markets. This species is one of the main sources of income and protein for these communities. It has been found in several islands across the Gulf of Guinea (West Africa)—namely, Bioko, São Tomé, Príncipe, and Annobón [9,16,17,18]. Little is known about the biology and ecology of this species, particularly during the return migrations of early life-cycle stages. However, according to local knowledge in São Tomé, S. bustamantei forms shoals at the mouth of rivers. Here, fish are caught with baskets, mosquito nets, or even with cloths. The post-larvae are caught throughout the year, but mainly in the dry season during the full and new moon periods. These descriptions coincide with the scientific information available elsewhere for other Sicydiinae species [5,8,11,13,19].
The IUCN (International Union for Conservation of Nature) has not yet attributed a conservation status to S. bustamantei due to insufficient scientific data [20] and, given its importance to many human populations across the species distribution range, it is necessary to obtain scientific data to start implementing sound management plans. We opted to start studying the food web ecology of this species, as well as the prevalence of microplastics in their diet. There are two main reasons for this decision. First, food web ecology discloses the relationship patterns between species on the multidimensional mosaic of habitats where they live. This is especially true for migratory species that move across ecosystems and serve as links and conduits of energy between the land and the ocean. Second, the prevalence of microplastics off São Tomé and Príncipe is unknown but likely high when considering the high levels of plastic pollution in beaches. Studying microplastic pollution is relevant because the contaminants sorbed into it or that are incorporated in the microplastics may dysregulate the physiological processes of the animals that accumulate it in their organisms [21]. These contaminants may be transferred and accumulated throughout the food web, impacting the health of multiple species, including humans [21]. Thus, our specific objective was to identify the main food sources consumed and assimilated by S. bustamantei post-larvae in the Gulf of Guinea, using the population of São Tomé island (São Tomé and Príncipe) as a model population. For that, we combined gut content analysis with carbon (δ13C: 13C/12C) and nitrogen (δ15N: 15N/14N) stable isotope analysis. The gut content analysis also provided the first assessment of the seriousness of microplastic pollution in São Tomé and Príncipe and its prevalence in the guts of such an important species for the people of this country.

2. Materials and Methods

2.1. Study Area and Collection of Samples

The Democratic Republic of São Tomé and Príncipe includes two islands, São Tomé and Príncipe, that form an archipelago with the Bioko and Annobón islands (Equatorial Guinea) in the Gulf of Guinea. São Tomé island (Figure 1) is a volcanic island with a high relief, located about 150–200 km off the west coast of Africa, and is the second-largest island (859 km2) of the archipelago [22].
Sicydium bustamantei post-larvae were acquired in the city of São Tomé fish market (caught mostly in the southern part of the island) and caught in the Mangrove of Malanza River (in South of São Tomé) in January 2017 and August 2017, corresponding to the wet season (October to May) and dry season (June to September), respectively (Figure 1 and Figure 2). Samples were preserved in ethanol 96% and later identified as S. bustamantei, an endemic gobiid in the region of Gulf of Guinea, with the help of Dr. Peter Wirtz (independent researcher). Since samples from the fish market included multiple species, we separated and quantified the individuals by taxonomic groups. The total length of larvae (TL; ±0.01 mm) was measured based on photographs taken under a stereomicroscope (Leica 58APO, coupled with a Leica MC170 HC camera) and using Image J (v1.50i). The standard deviation was used as a measure of data dispersion in this paper. A t-test was used to analyze the differences in total length between the wet and dry seasons. The analysis was carried out using the R 3.5.3 statistical software, with the level of significance set at p ≤ 0.05.

2.2. Gut Content Analysis

The diet of S. bustamantei post-larvae was determined by analyzing the guts of 30 individuals collected in each season. The gut contents were exposed after dissecting the abdomen with fine needles and identified under a stereomicroscope (Leica 58APO) and an inverted microscope (Zeiss MB). The prey items were identified to the lowest taxonomic level possible. The presence of microplastics and microfibers was also recorded.
The incidence of food items was calculated as the percentage of post-larvae with at least one prey item in their guts. A chi-square test was used to compare the incidence of each food item between the wet and dry seasons. The analysis was carried out using the R 3.5.3 statistical software, with the level of significance set at p ≤ 0.05.
The graphical method proposed by Costello [23] and modified by Amundsen et al. [24] was used to analyze the feeding strategy of S. bustamantei post-larvae. Individuals with no gut content were excluded from the analysis. Briefly, each point in the plot corresponds to the frequency of occurrence (i.e., the percentage of guts with a specific prey item) and prey specific abundance (i.e., the percentage of a prey taxon in relation to all prey items in the guts in which this prey was present). The importance of prey and feeding strategy were inferred by examining the points’ distribution along the axes in the plot.

2.3. Stable Isotope Analyses

The main sources of organic matter assimilated by post-larvae were identified and quantified using carbon (δ13C: 13C/12C) and nitrogen (δ15N: 15N/14N) stable isotopes. We analyzed five individuals collected during the wet season. Samples were also collected during the dry season, but due to visible signs of deterioration after collection they were not included in the analysis. The potential prey were collected near the mouth of the Malanza River on the south coast of São Tomé island also during the wet season (January 2017) and included zooplankton (Chaetognata Pterosagitta draco (Krohn 1853), Copepoda Calanoida Candacia spp. (Dana 1846), and Siphonophora Muggiaea kochii (Will 1844)), macroalgae (Caulerpa sp. (Lamouroux 1809) and Dictyota sp. (Lamouroux 1809)), tree leaves (Cocoseae (Linnaeus 1753), Terminalia catappa (Linnaeus 1767), Pandanus thomensis (Henriques 1887), and Rhizophora mangle (Linnaeus 1753)), and seagrass (Halodule wright (Asch 1868)). Zooplankton were collected using a plankton net with a mesh size of 500 µm. Macroalgae and seagrasses were collected in the intertidal and subtidal areas through freediving. Tree leaves were hand collected on the beaches near the mouth of the Malanza River.
Samples were cleaned with deionized water, oven-dried at 60 °C for at least 48 h, and ground to a fine and homogenous powder using a mortar and pestle (animals) or a mixer mill (plants and macroalgae). Stable isotope ratios were measured using a Thermo Scientific Delta V Advantage IRMS via Conflo IV interface (Marinnova, University of Porto). The raw data were normalized by three-point calibration using international reference materials, such as IAEA-N-1 (δ15N = +0.4‰), IAEA-NO-3 (δ15N = +4.7‰), and IAEA-N-2 (δ15N = +20.3‰) for the nitrogen isotopic composition, and two-point calibration using USGS-40 (δ13C = −26.39‰) and USGS-24 (δ13C = −16.05‰) for the carbon isotopic composition. Stable isotope ratios were reported in δ notation, δX= (Rsample/Rstandard − 1) × 103, where X is the C or N stable isotope, and R is the ratio of heavy/light stable isotopes. Vienna Pee Dee Belemnite and air are standards for δ13C and δ15N, respectively. The analytical error, the mean standard deviation of the replicate reference material, was ±0.1% for δ13C and δ15N. The zooplankton and S. bustamantei post-larvae δ13C values were corrected for lipid content [25], and the δ13C and δ15N values were corrected for ethanol preservation [26].
To identify and quantify the contribution of the most likely food sources to the S. bustamantei post-larvae biomass, we combined biplot analysis (post-larvae δ13C and δ15N values were adjusted for trophic fractionation [27]), with the results from the dual-stable isotope mixing model produced by SIAR (Stable Isotope Analysis in R) [28,29]. This mixing model uses Bayesian inference to solve the indeterminate equations (more than n + 1 sources relative to n stable isotopes) and produces a probability distribution that represents the likelihood a given source contributes to the consumer biomass [28]. The model also allows each of the sources and the trophic fractionation (TEF; or trophic enrichment factor) to be assigned as a normal distribution [28]. SIAR produces a range of feasible solutions to the mixing problem to which are assigned credibility intervals (CIs) (in this study, 95% CI) [28]. SIAR also includes a residual error term. For the SIAR mixing model, the δ13C and δ15N values were adjusted for one trophic level using the trophic fractionation estimates from Vander Zanden and Rasmussen [27] (+0.47 ± 1.23‰ δ13C, +3.40 ± 0.41‰ δ15N).

3. Results and Discussion

Post-larvae collected during the wet season were larger than those collected during the dry season (t(29) = 67.08, p < 0.001). The total length of the S. bustamantei post-larvae varied between 17 and 30 mm (26.7 ± 2.9 mm) in the wet season and between 18 and 28 mm (24.8 ± 2.2 mm) in the dry season (Figure 3). These values are within the range described for the total length of post-larvae of other species of Sicydiinae during their return migrations (recruitment) [3,7].
The feeding incidence was higher during the wet season (53.3%) than during the dry season (20.0%) (Table 1). This may be due to the fact that runoff is higher during the wet season than during the dry season, which increases the downstream transport of food and nutrients from upriver to the estuaries/mangroves and adjacent coastal areas, consequently increasing food availability [30].
The incidence of each food was not statistically different between seasons (χ2(2) = 4.98, p = 0.082). However, zooplankton (16.7%), such as Chaetognatha, Ostracoda, and unidentified crustaceans, were only observed in the guts of post-larvae during the wet season. Most of the gut contents consisted of plant and/or macroalgae detritus (46.7% in the wet season and 20.3% in the dry season) and microplastics/microfibers (20.0% and 23.3% in the wet and dry seasons, respectively) (Table 1). Thus, S. bustamantei post-larvae showed a specialist food strategy [22,23], feeding on a dominant prey taxon-vascular and/or macroalgae-derived material, and occasionally on small proportions of other prey types (rarest items)—zooplankton (Figure 4).
The stable isotope values from S. bustamantei post-larvae, after being corrected for trophic fractionation, indicate that they assimilated 15N- and 13C-enriched sources, such as zooplankton and macroalgae detritus, and also tree detritus (Figure 5). In fact, based on the SIAR mixing model (95% CI), zooplankton was the source with the highest relative contribution to the S. bustamantei post-larvae biomass during the wet season, varying between 0.42 and 0.71, followed by macroalgae detritus (0.16–0.50) and tree detritus (0.02–0.18) (Table 2).
The stable isotopes and gut content analyses showed different results for the relative contribution of each food source during the wet season. While the gut contents were mainly composed of vascular and/or macroalgae-derived material, zooplankton was the source with the highest relative contribution to the post-larvae biomass. Detritus is not the main source of energy for most aquatic organisms [31], because it is less likely to be assimilated than animal-derived material [32,33]. Moreover, because we collected zooplankton using a net with 500 μm mesh size, small-sized zooplankton such as Ostracoda were not included in the stable isotope analysis. However, this would probably not change the main conclusions about the contribution of zooplankton to post-larvae biomass. We expect that larger zooplankton, such as the carnivore Chaetognatha, will present higher δ15N values than Ostracoda (or other small-sized zooplankton), which feed on phytoplankton and detritus. Because we do not know the origin of the basal sources that support their biomass (pelagic or benthic), we cannot speculate about the potential differences in their δ13C values. Thus, if Ostracoda had lower δ15N values than the one estimated for zooplankton, the contribution of zooplankton to the S. bustamantei post-larvae would likely increase.
Our data indicate that S. bustamantei post-larvae are secondary consumers and omnivorous during their pelagic phase. They feed on zooplankton, as reported for other Sicydiinae species [34,35], and on plant/macroalgae detritus. During recruitment, metamorphosis occurs and modifications to anatomical feeding structures lead to a change in the S. bustamantei diet, from being a carnivorous fish feeding on plankton to an herbivorous fish feeding on the benthos [3,5,34]. This may explain the omnivory of this species during the post-larval phase. Although the number of samples analyzed was small to draw firm conclusions about the foraging habitat of post-larvae, the fact they showed high δ13C values so close to those from marine zooplankton and macroalgae indicate that these fish spent part of their life in the marine environment before moving to freshwater streams, as described for other Sycidiinae post-larvae [36]. Still, other studies have reported that the biomass of recruiting amphidromous fishes have an inshore signature typical of environments influenced by freshwater. This suggests that S. bustamantei post-larvae can be retained temporarily in the freshwater plumes of rivers while waiting for the appropriate conditions to start the return migration [37,38].
Large amounts of microplastics/microfibers (20.0–23.3%) were found inside the guts of S. bustamantei, along with zooplankton and vascular and/or macroalgae-derived material (Table 1). Unfortunately, large amounts of plastic litter lay on the beaches of São Tomé, some of which will break into microplastics. The ingestion of microplastics by fish larvae has been associated with a decrease in growth rates, changes in feeding preferences, innate behavior, swimming behavior, response to olfactory cues, and increasing mortality [39,40]. Thus, plastic pollution may also increment the deleterious effect of overfishing upon several populations of this and other marine species across the Gulf of Guinea. It has been globally reported that amphidromous fishes suffer many anthropogenic threats beyond overfishing—namely, water abstraction, degradation and loss of suitable habitat and connectivity due to instream barriers, and pollution [1,7,12,14,15,41,42]—with consequences to their physiology, reproduction, and migration patterns between freshwater and marine coastal areas [13]. In fact, Bell [7] considered these land-use threats to be more likely to cause population declines than overfishing.
In samples collected during both wet and dry seasons, S. bustamantei post-larvae corresponded to 80% of the total biomass, while 20% included small crustaceans (19.4%) and other non-identified fish species (0.6%). As described for other countries, the goby-fry fishery in São Tomé and Príncipe is not selective and it is not regulated—i.e., when local people find fish schools they catch as much as they can. Small crustaceans (e.g., isopods and decapods) and post-larvae and juveniles of other fish species are commonly found performing upstream migrations together with S. bustamantei post-larvae. This has been observed for other Sicydiinae species, and by-catch is often discarded during goby-fry fishery [19,41].

4. Conclusions

Sicydium bustamantei is a secondary consumer with an omnivorous diet during the post-larval phase and is not exclusively carnivorous, as described for other species of the same genus. Additionally, large amounts of microplastics/microfibers were ingested by post-larvae. Plastic pollution may cause detrimental impacts on the conservation status of this species and not only its overexploitation. Thus, the silent health risk problem that microplastic pollution may cause to humans through the consumption of S. bustamantei, in tandem with the ecological and economic importance of this species, represents another compelling reason to undertake a critical long-term monitoring program to assess the conservation status of the species.

Author Contributions

Conceptualization, V.B. and M.A.T.; investigation, V.B., E.D., J.C., and M.A.T.; writing—original draft preparation, V.B., E.D., J.C., and M.A.T.; writing—review and editing, V.B., E.D., J.C., M.B., S.V., and M.A.T. All authors have read and agreed to the published version of the manuscript.

Funding

This study received Portuguese national funds from FCT—Foundation for Science and Technology—through project UIDB/04326/2020 and UIDB/04423/2020. Vânia Baptista was funded through project LuandaWaterFront—“Luanda Bay Ecological Assessment: A waterfront based approach to reduce environmental risks and increase quality of life” (333191101) supported by Aga Khan, Network for Development and the Portuguese Foundation for Science and Technology (FCT).

Acknowledgments

This study took place in the framework of an expedition made to the São Tomé island in 2017, in the framework of the course, “Ecology and biodiversity of sea turtles breeding ground on São Tomé Island the feeding ecology of marine turtles in São Tomé, West Africa”. This expedition and course was organized by the Centre of Marine Sciences (CCMAR) and the University of Algarve (UAlg) from Portugal, in collaboration with local institutions (ATM—Associação Tartarugas Marinhas, MARAPA—Mar Ambiente e Pesca Artesanal, Direção Geral do Ambiente de São Tomé e Principe, USTP—University of São Tomé and Principe—USTP). The authors also like to thank their colleagues Peter Wirtz (CCMAR), Ester Serrão (CCMAR, Universidade do Algarve), and Karim Erzini (CCMAR, Universidade do Algarve); all the participants on the course, “Ecology and biodiversity of sea turtle breeding grounds in São Tomé”; the CCMAR staff at the “Advanced Technologies and Training” department; the MARAPA, ATM, Direção Geral do Ambiente de São Tomé e Principe, and Universidade de São Tomé e Príncipe; and Paula Chainho (MARE, Universidade de Lisboa) for collecting a few samples for us. The authors are especially thankful to the anonymous reviewers and the guest editor Pedro Morais for their constructive comments on earlier versions of this paper.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analysis, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Morais, P.; Daverat, F. Definitions and concepts related to fish migration. In An Introduction to Fish Migration; Morais, P., Daverat, F., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 14–19. [Google Scholar] [CrossRef]
  2. Closs, G.P.; Warburton, M. Life histories of amphidromous fishes. In An Introduction to Fish Migration; Morais, P., Daverat, F., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 102–122. [Google Scholar]
  3. Keith, P. Biology and ecology of amphidromous gobiidae of the indo-pacific and the caribbean regions. J. Fish Biol. 2003, 63, 831–847. [Google Scholar] [CrossRef]
  4. McDowall, R.M. Early hatch: A strategy for safe downstream larval transport in amphidromous gobies. Rev. Fish Biol. Fish. 2009, 19, 1–8. [Google Scholar] [CrossRef]
  5. Lord, C.; Brun, C.; Hautecoeur, M.; Keith, P. Insights on endemism: Comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobioidei: Sicydiinae) from Vanuatu and New Caledonia. Ecol. Freshw. Fish 2010, 19, 26–38. [Google Scholar] [CrossRef]
  6. Keith, P.; Lord, C.; Lorion, J.; Watanabe, S.; Tsukamoto, K.; Couloux, A.; Dettal, A. Phylogeny and biogeography of Sicydiinae (Teleostei: Gobiidae) inferred from mitochondrial and nuclear genes. Mar. Biol. 2011, 158, 311–326. [Google Scholar] [CrossRef]
  7. Bell, K.N. An overview of goby-fry fisheries. Naga ICLARM Q. 1999, 22, 30–36. [Google Scholar]
  8. McDowall, R.M. On amphidromy, a distinct form of diadromy in aquatic organisms. Fish Fish. 2007, 8, 1–13. [Google Scholar] [CrossRef]
  9. Pezold, F.; Iwamoto, T.; Harrison, I.J. Multivariate analysis of sicydiines of São Tomé and Príncipe with redescription of Sicydium brevifile and S. bustamantei (Teleostei: Gobiidae) and a key to west African sicydiines. The california academy of sciences gulf of guinea expedition (2001). Proc. Calif. Acad. Sci. 2006, 57, 965–980. [Google Scholar]
  10. Radtke, R.L.; Kinzie, R.A.; Shafer, D.J. Temporal and spatial variation in length of larval life and size at settlement of the Hawaiian amphidromous goby Lentipes concolor. J. Fish Biol. 2001, 59, 928–938. [Google Scholar] [CrossRef]
  11. Hoareau, T.B.; Lecomte-Finiger, R.; Grondin, H.-P.; Conand, C.; Berrebi, P. Oceanic larval life of La Réunion ‘bichiques’, amphidromous gobiid post-larvae. Mar. Ecol. Prog. Ser. 2007, 333, 303–308. [Google Scholar] [CrossRef]
  12. Bell, K.N. What comes down must go up: The migration cycle of juvenile-return anadromous taxa. Am. Fish Soc. Symp. 2009, 69, 321–341. [Google Scholar]
  13. Sánchez-Garcés, G.C. A review of amphidromous freshwater fishes of the Choco biogeographical region (Colombia and Ecuador): Diversity, ecology, fisheries and conservation. Cybium 2017, 41, 157–169. [Google Scholar]
  14. Lagarde, R.; Teichert, N.; Boussarie, G.; Grondin, H.; Valade, P. Upstream migration of amphidromous gobies of la Réunion Island: Implication for management. Fish. Manag. Ecol. 2015, 22, 437–449. [Google Scholar] [CrossRef]
  15. Thomas, C.; Becheler, E.; Trinh, A.M.; Ellien, C. Spatial variability in post-larval traits of Sicyopterus lagocephalus Pallas 1770 around Reunion Island. Environ. Biol. Fishes 2018, 101, 813–827. [Google Scholar] [CrossRef]
  16. Castelo, R. Biogeographical considerations of fish diversity in Bioko. Biodivers. Conserv. 1994, 3, 808–827. [Google Scholar] [CrossRef]
  17. Jones, P.J. Biodiversity in the Gulf of Guinea: An overview. Biodivers. Conserv. 1994, 3, 772–784. [Google Scholar] [CrossRef]
  18. Wirtz, P.; Ferreira, C.E.L.; Floeter, S.R.; Fricke, R.; Gasparini, J.L.; Iwamoto, T.; Roch, L.; Sampaio, C.L.S.; Schliewen, U.K. Coastal fishes of São Tomé and Principe islands, Gulf of Guinea (eastern Atlantic Ocean)—An update. Zootaxa 2007, 1523, 1–48. [Google Scholar] [CrossRef]
  19. Bell, K.N. Opportunities in stream drift: Methods, goby larval types, temporal cycles, in situ mortality estimation, and conservation implications. Bish. Mus. Bull. Cult. Environ. Stud. 2007, 3, 35–61. [Google Scholar]
  20. Moelants, T. Sicydium Bustamantei. The IUCN Red List of Threatened Species 2010: E.T182284A7849800. Available online: https://0-dx-doi-org.brum.beds.ac.uk/10.2305/IUCN.UK.2010-3.RLTS.T182284A7849800.en (accessed on 7 October 2020).
  21. Carbery, M.; O’Connor, W.; Thavamani, P. Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environ. Int. 2018, 115, 400–409. [Google Scholar] [CrossRef] [Green Version]
  22. Afonso, P.; Porteiro, F.M.; Santos, R.S.; Barreiros, J.P.; Worms, J.; Wirtz, P. Coastal marine fishes of São Tomé Island (Gulf of Guinea). Arquipel. Cienc. Biol. Mar. 1999, 17A, 65–92. [Google Scholar]
  23. Costello, M.J. Predator feeding strategy and prey importance: A new graphical analysis. J. Fish Biol. 1990, 36, 261–263. [Google Scholar] [CrossRef]
  24. Amundsen, P.A.; Gabler, H.M.; Stald-Vik, F.J. A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. J. Fish Biol. 1996, 48, 607–614. [Google Scholar] [CrossRef]
  25. Smyntek, P.M.; Teece, M.A.; Schulz, K.L.; Thackeray, S.J. A standard protocol for stable isotope analysis of zooplankton in aquatic food web research using mass balance correction models. Limnol. Oceanogr. 2007, 52, 2135–2146. [Google Scholar] [CrossRef] [Green Version]
  26. Feuchtmayr, H.; Grey, J. Effect of preparation and preservation procedures on carbon and nitrogen stable isotope determinations from zooplankton. Rapid Commun. Mass Spectrom. 2003, 17, 2605–2610. [Google Scholar] [CrossRef]
  27. Vander Zanden, J.; Rasmussen, J. Variation in 15N and 13C trophic fractionation: Implications for aquatic food web studies. Limnol. Oceanogr. 2001, 46, 2061–2066. [Google Scholar] [CrossRef]
  28. Parnell, A.C.; Inger, R.; Bearhop, S.; Jackson, A.L. Source partitioning using stable isotopes: Coping with too much variation. PLoS ONE 2010, 5, e9672. [Google Scholar] [CrossRef]
  29. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018. [Google Scholar]
  30. Gallegos, C.L.; Jordan, T.E.; Correll, D.L. Event-scale response of phytoplankton to watershed inputs in a subestuary: Timing, magnitude, and location of blooms. Limnol. Oceanogr. 1992, 37, 813–828. [Google Scholar] [CrossRef]
  31. Deegan, L.A.; Garritt, R.H. Evidence for spatial variability in estuarine food webs. Mar. Ecol. Prog. Ser. 1997, 147, 31–47. [Google Scholar] [CrossRef] [Green Version]
  32. Evans-White, M.A.; Dodds, W.K.; Whiles, M.R. Ecosystem significance of crayfishes and stonerollers in a prairie stream: Functional differences between co-occurring omnivores. J. N. Am. Benthol. Soc. 2003, 22, 423–441. [Google Scholar] [CrossRef] [Green Version]
  33. Dodds, W.K.; Collins, S.M.; Hamilton, S.K.; Tank, J.L.; Johnson, S.; Webster, J.R.; Simon, K.S.; Whiles, M.R.; Rantala, H.M.; McDowell, W.H.; et al. You are not always what you think you eat: Selective assimilation across multiple whole-stream isotopic trace studies. Ecology 2014, 95, 2757–2767. [Google Scholar] [CrossRef] [Green Version]
  34. Keith, P.; Hoareau, T.; Lord, C.; Ah-Yane, O.; Gimmoneau, G.; Robinet, T.; Valade, P. Characterisation of post-larval to juvenile stages, metamorphosis, and recruitment of an amphidromous goby, Sicyopterus lagocephalus (Pallas, 1767) (Teleostei: Gobiidae: Sicydiinae). Mar. Fresh Res. 2008, 59, 876–889. [Google Scholar] [CrossRef]
  35. Kondo, M.; Maeda, K.; Hirashima, K.; Tachihara, K. Comparative larval development of three amphidromous Rhinogobius species making reference to their habitat preferences and migration biology. Mar. Fresh Res. 2013, 64, 249–266. [Google Scholar] [CrossRef] [Green Version]
  36. Engman, A.C.; Kwak, T.J.; Cope, W.G. Do postlarval amphidromous fishes transport marine-derived nutrients and pollutants to Caribbean streams? Ecol. Freshw. Fish 2018, 27, 847–856. [Google Scholar] [CrossRef]
  37. Sorensen, P.W.; Hobson, K.A. Stable isotope analysis of amphidromous Hawaiian gobies suggests their larvae spend a substantial period of time in freshwater river plumes. Environ. Biol. Fishes 2005, 74, 31–42. [Google Scholar] [CrossRef]
  38. Hobson, K.A.; Smith, R.J.F.; Sorensen, P.W. Applications of stable isotope analysis to tracing nutrient sources to Hawaiian gobioid fishes and other stream organisms. Bish. Mus. Bull. Cult. Environ.Stud. 2007, 3, 99–111. [Google Scholar]
  39. Lönnstedt, O.M.; Eklöv, P. Environmentally relevant concentrations of microplastic particles influence larval fish ecology. Science 2016, 352, 1213–1216. [Google Scholar] [CrossRef] [PubMed]
  40. Pannetier, P.; Morin, B.; Le Bihanic, F.; Dubreil, L.; Clérandeau, C.; Chouvellon, F.; Arkelc, K.V.; Daniond, M.; Cachot, J. Environmental samples of microplastics induce significant toxic effects in fish larvae. Environ. Int. 2020, 134, 105047. [Google Scholar] [CrossRef]
  41. Castellanos-Galindo, G.A.; Sanchez, G.C.; Beltran-Leon, B.S.; Zapata, L. A goby-fry fishery in the northern Colombian Pacific Ocean. Cybium 2011, 35, 391–395. [Google Scholar]
  42. Walter, R.P.; Hogan, J.D.; Blum, M.J.; Gagne, R.B.; Hain, E.F.; Gilliam, J.F.; McIntyre, P.B. Climate change and conservation of endemic amphidromous fishes in Hawaiian streams. Endanger. Species Res. 2012, 16, 261–272. [Google Scholar] [CrossRef] [Green Version]
Figure 1. Sampling locations of Sicydium bustamaneti (Greeff 1882) post-larvae collected in São Tomé Island in 2017. Maps retrieved from Google Earth Pro.
Figure 1. Sampling locations of Sicydium bustamaneti (Greeff 1882) post-larvae collected in São Tomé Island in 2017. Maps retrieved from Google Earth Pro.
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Figure 2. Sicydium bustamaneti (Greeff 1882) post-larvae collected in the island of São Tomé (São Tomé and Príncipe) in 2017.
Figure 2. Sicydium bustamaneti (Greeff 1882) post-larvae collected in the island of São Tomé (São Tomé and Príncipe) in 2017.
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Figure 3. Histogram of the total length (mm) of Sicydium bustamantei (Greeff 1882) post-larvae collected during the wet (n = 30) and dry (n = 30) seasons of 2017 in the island of São Tomé (São Tomé and Príncipe).
Figure 3. Histogram of the total length (mm) of Sicydium bustamantei (Greeff 1882) post-larvae collected during the wet (n = 30) and dry (n = 30) seasons of 2017 in the island of São Tomé (São Tomé and Príncipe).
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Figure 4. Frequency of occurrence and prey-specific abundance (%) present in the gut contents of Sicydium bustamaneti (Greeff 1882) post-larvae collected during the wet and dry seasons of 2017 in the island of São Tomé (São Tomé and Príncipe), and plotted according to the Costello method [23] modified by Amundsen et al. [24].
Figure 4. Frequency of occurrence and prey-specific abundance (%) present in the gut contents of Sicydium bustamaneti (Greeff 1882) post-larvae collected during the wet and dry seasons of 2017 in the island of São Tomé (São Tomé and Príncipe), and plotted according to the Costello method [23] modified by Amundsen et al. [24].
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Figure 5. δ15N and δ13C values (‰) (mean ± SD) of Sicydium bustamaneti (Greeff 1882) post-larvae and potential food items collected during the wet season of 2017 in the island of São Tomé (São Tomé and Príncipe). Stable isotope values for S. bustamaneti are corrected for trophic fractionation (0.47‰ δ13C, 3.40‰ δ15N; Vander Zanden and Rasmussen [27]).
Figure 5. δ15N and δ13C values (‰) (mean ± SD) of Sicydium bustamaneti (Greeff 1882) post-larvae and potential food items collected during the wet season of 2017 in the island of São Tomé (São Tomé and Príncipe). Stable isotope values for S. bustamaneti are corrected for trophic fractionation (0.47‰ δ13C, 3.40‰ δ15N; Vander Zanden and Rasmussen [27]).
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Table 1. Total number of Sicydium bustamantei (Greeff 1882) post-larvae guts examined and guts with food items; feeding incidence (%); and incidence of plant and/or macroalgae, zooplankton, microplastics, and microfibers (%). Samples were collected during the wet and dry seasons of 2017 in the island of São Tomé (São Tomé and Príncipe).
Table 1. Total number of Sicydium bustamantei (Greeff 1882) post-larvae guts examined and guts with food items; feeding incidence (%); and incidence of plant and/or macroalgae, zooplankton, microplastics, and microfibers (%). Samples were collected during the wet and dry seasons of 2017 in the island of São Tomé (São Tomé and Príncipe).
SeasonsExamined Guts (N)Guts with Food (N)Feeding Incidence (%)Plant and/or Macroalgae Incidence (%)Zooplankton Incidence (%)Microplastic and Microfiber Incidence (%)
Wet301653.346.716.720.0
Dry 30620.020.30.023.3
Table 2. Relative contribution of each food source to the biomass of Sicydium bustamaneti (Greeff 1882) post-larvae collected during the wet season of 2017 in the island of São Tomé (São Tomé and Príncipe). The mode values represent the most likely value, and the low 95% and high 95% values represent the 95% Bayesian credibility intervals calculated by a dual-stable isotope mixing model produced by SIAR (Stable Isotope Analysis in R) [28,29].
Table 2. Relative contribution of each food source to the biomass of Sicydium bustamaneti (Greeff 1882) post-larvae collected during the wet season of 2017 in the island of São Tomé (São Tomé and Príncipe). The mode values represent the most likely value, and the low 95% and high 95% values represent the 95% Bayesian credibility intervals calculated by a dual-stable isotope mixing model produced by SIAR (Stable Isotope Analysis in R) [28,29].
Food ItemsLow 95% High 95%Mode
Zooplankton0.420.710.56
Macroalgae detritus0.160.500.35
Tree detritus0.020.180.10
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Baptista, V.; Dias, E.; Cruz, J.; Branco, M.; Vieira, S.; Teodósio, M.A. Feeding Ecology of Sicydium bustamantei (Greeff 1884, Gobiidae) Post-Larvae: The “Little Fish” of São Tomé Island. Oceans 2020, 1, 300-310. https://0-doi-org.brum.beds.ac.uk/10.3390/oceans1040020

AMA Style

Baptista V, Dias E, Cruz J, Branco M, Vieira S, Teodósio MA. Feeding Ecology of Sicydium bustamantei (Greeff 1884, Gobiidae) Post-Larvae: The “Little Fish” of São Tomé Island. Oceans. 2020; 1(4):300-310. https://0-doi-org.brum.beds.ac.uk/10.3390/oceans1040020

Chicago/Turabian Style

Baptista, Vânia, Ester Dias, Joana Cruz, Maria Branco, Sara Vieira, and Maria Alexandra Teodósio. 2020. "Feeding Ecology of Sicydium bustamantei (Greeff 1884, Gobiidae) Post-Larvae: The “Little Fish” of São Tomé Island" Oceans 1, no. 4: 300-310. https://0-doi-org.brum.beds.ac.uk/10.3390/oceans1040020

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