Deciphering the trophic niche of the nearly extinct vaquita (Phocoena sinus) and its variability through time
Introduction
The vaquita (Phocoena sinus) is currently the most endangered marine mammal in the world (NOM-059- SEMARNAT-, 2010, IUCN (International Union for Conservation of Nature)., 2008, Gerrodette et al., 2011, Jaramillo-Legorreta et al., 2019), with probably fewer than 20 individuals left in the wild (Jaramillo-Legorreta et al. 2019). Endemic to the Upper Gulf of California (UGC), the vaquita has the narrowest geographic range among cetaceans (IUCN (International Union for Conservation of Nature)., 2008, Gerrodette et al., 2011). Since it’s description in 1950 (Norris & McFarland 1958), the vaquita’s population has been known to decline due to incidental entanglement in gillnets for finfish and shrimp, and mainly in illegal gillnets for the endangered totoaba (Totoaba macdonaldi) (Vidal, 1995, D'Agrosa et al., 1995, D’agrosa et al., 2000, Rojas-Bracho et al., 2006, Gulland et al., 2020). Between 1997 and 2008, the annual population decline was estimated to be 7–8% (Gerrodette et al. 2011), and 50% since 2016 (Jaramillo-Legorreta et al. 2019). The considerable reduction of river flow into the UGC delta has been argued to could have affected to the species diversity and yielding a more complex impact of habitat loss for the indigenous species and pottencially contribute to the extinction of the vaquita (Gallo-Reynoso, 1998, Galindo-Bect et al., 2000, Lluch-Cota et al., 2007, Galindo-Bect et al., 2021). However, no research has been conducted to evaluate changes in elemental cycling and community structure of this unique ecosystem pre and post the construction of dams and reduction of freshwater flow. Conservation and monitoring efforts to protect the vaquita has focused on stopping illegal fisheries because it is known to be the main cause of mortality (Rojas-Bracho et al., 2006, Jaramillo-Legorreta, 2008, Gulland et al., 2020). However, these activities continue, and there has been no more negotiation between México and the USA to stop the illegal fisheries and to increase river flow to the UGC since the last amendment in 2014 (IBWC 2014).
The near extinction of the vaquita adds to the long list of species lost in recent centuries, highlighting once more the current extinction crisis that our planet faces due to human activities (Ceballos et al., 2015, CIRVA (Comision Internacional para la Recuperacion de la Vaquita), 2019), and raises questions regarding the consequences of marine biodiversity loss in unique ecosystems. The UGC is considered one of the most productive regions in the world and hosts more than 400 species from macro-invertebrate to larger fish (Brusca et al., 2005, Hastings and Findley, 2007). The UGC presents a complex wasp waist system where vaquitas seem to have limited top-down control on the estuary community, but they have an important role in the community organization (Riofrío-Lazo et al. 2012).
To gain insight into the marine communities in the vaquita’s habitat, it is important to estimate the vaquita’s trophic position and evaluate its variability through time with the reduction of its population. However, our knowledge regarding vaquita’s feeding ecology is very limited because it is difficult to observe a “midwater pelagic dweller” that exhibits elusive behavior, and has a small population size (Gallo-Reynoso, 1998, Silber and Norris, 1991, Gerrodette et al., 1995). There are only two specific studies on vaquitás foraging habits that were based on analysis of stomach contents that partially described prey items but in an advanced state of digestion (Findley et al., 1994, Pérez-Cortés et al., 1996). These studies suggest that the vaquita is a generalist consumer feeding mainly on fish ∼87.2% of the Engraulidae family, ∼40% on Isopisthus altipinnis, and ∼21% on Porichthys mimeticus, while squid species represent ∼16% (Findley et al., 1994, Pérez-Cortés et al., 1996). Given its endangered status, other methods are needed to investigate the vaquita trophic level and its variability over time.
Stable isotope analysis (SIA) of carbon (δ13C) and nitrogen (δ15N) is an important tool for studying the foraging habits of cetacean populations and individuals including oceanic and coastal species difficult to investigate due to their remote habitat (Ruiz-Cooley et al., 2004, Ruiz-Cooley et al., 2017). This is made possible because δ13C and δ15N are both indicators of habitat baseline values (primary producers) and consumers’ trophic position. Animals integrate biochemical characteristics of their habitat through their diet (DeNiro and Epstein, 1978, Schoeninger and DeNiro, 1984). The main factor influencing the δ13C and δ15N enrichment between consumers bone protein (mainly collagen) and their diet is associated with tissue turnover rates (Schoeninger & DeNiro 1984). Bone has low turnover rates, and represents a long-term isotopic bio-archive record of animal diet and habitat biochemistry (Newsome et al. 2010). In pinnipeds, for instance, skull bone contains information about the assimilated diet for a period of months in juveniles and up to five years in matures individuals (Sealy et al., 1995, Riofrío-Lazo and Aurioles-Gamboa, 2013). Variability in δ13C values can be associated with changes in diet, however, it mainly reflects variation in C sources and primary production (Peterson and Fry, 1987, Fry and Wainright, 1991, Díaz-Gamboa et al., 2018, Aurioles-Gamboa et al., 2013). The δ15N baseline values vary between coastal and pelagic habitats across large ecosystems, and consumers reflect similar variation (DeNiro & Epstein 1981). In a given habitat composed of resident species, δ15N increase in a predictable way with trophic steps, allowing estimations of trophic level (Post 2002). Hence, SIA is an efficient approach for reconstructing food web structures (Layman et al. 2007), evaluate variability in consumers’ resource use (Bolnick et al. 2003), the composition of ecological communities (Wiens & Graham 2005), and infer species’ trophic niches (Rubenstein and Hobson, 2004, West et al., 2006).
Understanding the trophic niche of the vaquita and its temporal variation can provide insights into changes in prey composition, overall community, and habitat because trophic interactions connect multiple species (Paine 1966). The reduction or removal of important predators from a given community can drive drastic changes in the food web structure (Paine 1966). In this study, we used SIA of δ13C and δ15N from skull bone to reconstruct vaquita’s isotopic niche as a proxy of its trophic niche and to gain insight into its feeding strategy to determine whether it is a specialist or generalist consumer. We hypothesized that the vaquita’s isotopic niche varies by maturity-stage classes and sex due to different energy demands and possibly diet composition. We also hypothesized that the vaquita’s isotopic niche varies between years given that the Upper Gulf of California ecosystem undergoes interannual environmental changes related to the anthropogenic use of the Colorado River (Lavı́n and Sánchez, 1999).
Section snippets
Methodology
We collected vaquita bone collagen samples from the inner dorsal section of the skull of 33 individuals from the vertebrate collection at the Research Center for Food and Development (CIAD-Guaymas, Sonora). These individuals were opportunistically collected along the coast of the Upper Gulf of California (Fig. 1) from 1985, 1986, 1990, 1991, 1992 and 1993. Maturity-stage and sex were determined previously by Hohn et al. (1996).
Stable isotopes values of vaquita
When comparing the bone samples values with (LE; δ13C = -11.8 ± 0.9 ‰, δ15N = 20.9 ± 0.8 ‰) and without lipid extraction (non-LE; δ13C = -13.0 ± 1.2 ‰, δ15N = 20.8 ± 0.8 ‰), no significant differences were found for δ15N (Mann-Whitney U test (n = 6) = 10.00, Z = 1.20, p = 0.2403), but statistically significant differences were found for δ13C (Mann-Whitney U test (n = 6) = 5.00, Z = 2.00, p = 0.0411).
After making the necessary lipid correction to the vaquita samples, no significant differences
Vaquita’s isotopic niche variation by sex, maturity, and year
The trophic overlap observed between males and females SEAC (Fig. 2A, Table 2) indicated that in these groups there was no significant partition of resources and supported that both sexes were feeding in the same geographic area over several years (Rodríguez-Pérez et al. 2018). Other odontocete species such as Tursiops truncatus (Díaz-Gamboa et al. 2018), Pontoporia blainvillei (Troina et al. 2016), and Monodon monoceros (Louis et al. 2021) also exhibited similar isotope values between males
CRediT authorship contribution statement
Mónica Y. Rodríguez-Pérez: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing, Funding acquisition. Rocio I. Ruíz-Cooley: Conceptualization, Methodology, Writing – review & editing, Visualization, Supervision. David Aurioles-Gamboa: Conceptualization, Resources, Project administration, Supervision, Visualization, Writing – original draft, Writing – review
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank the project ‘Ecological Monitoring of the Upper Gulf of California’, financed by the David and Lucile Packard Foundation (contract no. 2010-36137) through the University of Arizona PANGAS. Support was also received from project CONACYT 2008-105922 ‘Asociaciones de larvas de peces, hábitat trófico y su relación con la estructura física en giros del Golfo de California’ and projects SIP-IPN 1451 “Estado de Salud, uso sustentable y conservación del Golfo de California”, SIP-20110297
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