An osteometric approach to reconstruct the length and weight of Lutjanus argentiventris (Perciformes: Lujtanidae) for archaeological and ecological purposes

María Fernanda Martínez-Polanco^1,2 and Philippe Béarez³

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Abstract​

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Introduction​

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The Lutjanidae family consists of 17 genera and 112 species, which are distributed in tropical and subtropical seas worldwide, but mostly in the Indo-Pacific (Fricke et al., 2020). The genus Lutjanus Bloch, 1790 is by far the most speciose, containing 73 species, including nine in the Eastern Pacific: Lutjanus aratus (Günther, 1864); L. argentiventris (Peters, 1869); L. colorado Jordan, Gilbert, 1882; L. guttatus (Steindachner, 1869); L. inermis (Peters, 1869), L. jordani (Gilbert, 1898); L. novemfasciatus Gill, 1862; L. peru Nichols, Murphy, 1922; and L. viridis (Valenciennes, 1846). The maximum total length (TL) of these species ranges between 300 mm (L. viridis) and 1700 mm (L. novemfasciatus) (Allen, 1985, ¹⁹⁹⁵).

Snappers are important resources to artisanal and commercial fisheries worldwide, with the biggest catches in the Western Central Pacific and Western Central Atlantic (Allen, 1985; Salas et al., 2011). In the Tropical Eastern Pacific (TEP), the catch is less, however L. argentiventris is an important species for small-scale fisheries (e.g.Alava et al., 2015). In Mexico, the annual landings of the artisanal fleet have oscillated between 0.5 and 1.5 t (Espino-Barr et al., 2004). A long-term study (1983-1998) of artisanal marine fisheries in Colima, Mexico, shows that L. argentiventris is the seventh most abundant species in the region’s catches (Espino-Barr et al., 2002). At Bahia de Navidad, Jalisco, Mexico, another study, covering 47 months (5 days per month in 1994-1995 / 1998-2000) reveals that ten species accounted for more than 60% of the total abundance and biomass, with L. argentiventris in eighth place (Rojo-Vázquez et al., 2008). In the southwestern Gulf of California, Mexico, L. argentiventris is among the eight most commercially important reef fishes (Erisman et al., 2010). It is normally captured using various types of craft nets, gillnets, harpoons, and hook-and-lines (Rojas et al., 2004; Lucano-Ramírez et al., 2014).

The archaeological record shows the importance of the species along the Pacific coast for millennia. In Mexico, archaeo-ichthyological samples from the site of Huatabampo (Sonora) exhibit high numbers (Number of identified specimens [NISP] = 106; Minimum number of individuals [MNI] = 10) of snappers (Lutjanus cf. argentiventris). The presence of this species suggests that the ancient inhabitants of Huatabampo were fishing in areas with a strong marine influence (Guzmán, 2008). In Panama, snappers are present in the archaeological material of Cerro Mangote (Cooke, Ranere, 1999) and, more commonly, in the Pearl Islands archipelago, in Pedro Gonzalez (Cooke, Jiménez, 2009) and Bayoneta Island (Martínez-Polanco et al., 2009). Pre-Ceramic occupations at Pedro Gonzalez (4030-3630 BC) and Ceramic occupations at Bayoneta Island (ca. 900 and 1300 AD) fishing data suggest that snappers were taken with similar frequency during both time periods (Cooke, Jimenez-Acosta, 2009; Martínez-Polanco et al., 2009). Snappers are evenly distributed in low numbers in Ecuadorian sites (e.g.Béarez, 1996; Béarez et al., 2012).

Just as the weight increases with the size of the fish, bone size also increases with body size. The growth rate of each body part varies depending on species ontogeny and morphology (Teissier, 1948). In archaeology, fish body size and weight are used to study human diet, and to infer on fishing strategies and techniques, human exploitation and the overexploitation of fish faunas (e.g.Reitz et al., 1987; Lambrides, Weisler, 2015; Thieren, Van Neer, 2016; Prestes-Carneiro, Béarez, 2017; Lidour et al., 2018; Rurua et al., 2020). In particular, some aspects of fishing can be studied in depth: (1) changes in the geographic ranges of species, (2) reductions in their abundances, (3) signatures of trophic cascades and (4) marine fisheries trophic level changes (Erlandson, Rick, 2010).

On the other hand, Karachle, Stergiou (2012) summarize the importance of length-weight models in three aspects of modern ecology studies: (1) use of length data as an estimation of biomass; (2) to ascertain the condition of the species; and (3) to compare the life history of different populations of the same species. In fisheries management, the weight and the size of fish are used to estimate population parameters, life history characteristics and to develop programs for the protection and management of the species (Castellanos-Galindo, Zapata-Padilla, 2019). This kind of information could be used to determine the minimum permissible lengths of capture and identification of suitable periods for a closed fishing season. The identification of age-classes and male to female ratios are relevant to evaluate the status of an exploited stock and to establish future harvest levels, and the relationship between fish-size and its life-history traits and habitats (Castellanos-Galindo, Zapata-Padilla, 2019; Froese, Pauly, 2019).

In modern fisheries, the concept of baseline is understood as the fish population that was present before human influence (Pauly, 1995). This author addresses the shifting baseline syndrome, but this can only be resolved by developing a pre-industrial baseline that extends beyond the origins of modern fishing, both artisanal and commercial (Froyd, Willis, 2008; Betts et al., 2011, ²⁰¹⁴; Barrett, 2019). Baselines should not assume static environments but rather dynamic systems (Rick, Lockwood, 2012). It is in this point where zooarchaeology and particularly ichthyoarchaeology can contribute with information to manage modern fisheries (Betts et al., 2011, ²⁰¹⁴; Barrett, 2019). Fish size comparison between modern, historical and archaeological data could be used to regulate marine protected areas and to propose clear conservation objectives. For example, if archaeological data are used as baselines, new indicators could be proposed, and compared over time. Similarly, reference levels of objectives, thresholds or limits could be developed to inform the management of marine resources and ecosystems (Schwerdtner-Máñez et al., 2014). At the same time, it could determine the absolute magnitude of the changes that can occur in a heavily exploited fish stock. Analysis of long-term trends in fish size can provide a key indicator of changes in ecological baselines (Betts et al., 2011, ²⁰¹⁴; Barrett, 2019). Other contributions of the study of the archaeological fish size are to measure fluctuations in the aquatic environment and the intensity of exploitation (Betts et al., 2011, 2014; Barrett, 2019).

In this article, the attention will focus on the yellow snapper, L. argentiventris, which has a subtropical distribution, ranging in the Eastern Pacific from southern California to northern Peru, including the Galapagos Islands (Allen, 1985) (Fig. 1). The species is found in coral and rocky reefs at a depth range of 3-60 m and also in estuaries and river mouths, being tolerant to freshwater. It is characterized by a pinkish red colour of the anterior part of the body, which becomes bright orange to yellow in its posterior part. The fins are mainly yellow or orange. The yellow snapper is an active predator, feeding mainly at night on fish, shrimp, crabs and mollusks (Allen, 1985). Individuals can form small aggregations during the day or shelter in caves. The species also form seasonal spawning aggregations, a trait that makes many species vulnerable to overfishing (Sala et al., 2003). The species has been recorded up to a TL of 760 mm and a maximum weight (W) of 6550 g (Béarez, 1996: 44). For Gorgona Island in Colombia, Rojas et al. (2004) reported that the average size at sexual maturity was 515 mm TL and that the length-weight relationships were not significantly different between sexes. In the case of the central Mexican Pacific, the size range at sexual maturity was 260-330 mm for females and 240-320 mm for males (Lucano-Ramírez et al., 2014).

FIGURE 1| Lutjanus argentiventris geographical distribution (Map adapted from Robertson, Allen, 2015; Image represents a 645 mm TL individual).

Our purpose is to present an allometric model that enables the length and weight of Lutjanus argentiventris to be predicted, using the isolated bones from archaeological and paleontological contexts or the stomach contents of ichthyophagous species. Length-weight relationships for L. argentiventris can be found for Mexico (González et al., 2004; Aburto-Oropeza et al., 2009; García-Contreras et al., 2009; Piñón et al., 2009; Velázquez-Velázquez et al., 2009), Panama (Bonilla-Gómez et al., 2014) and Colombia (Rojas et al., 2004) but not for Ecuador. As there is no information available for the southernmost part of the range of L. argentiventris, it is useful to check whether this relationship is similar or different from those already known in more northern countries. Rojas et al. (2004) reported that the species is moderately slow growing, appears to be long-lived and has a low natural mortality rate, making it easily vulnerable to overfishing. It is therefore important to build osteometric models that could be used for in-depth long-term studies of L. argentiventris populations, with the aim of proposing management strategies.

Material and methods

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All the skeletons came from the fish collection of the Muséum national d’histoire naturelle in Paris. The modern collection of Lutjanus argentiventris is composed of 37 individuals covering a wide range of sizes and weights: 36 are from Ecuador and one is from Panama. The TL of the sample ranged between 210 and 760 mm, and the SL between 164 and 627 mm. The W ranged between 123 and 6550 g. The fish from Ecuador (MNHN-ICOS-1776 to -1811) were sampled between 1992 and 1998 in the vicinity of Puerto López (Fig. 1) mostly over rocky reefs, and using harpoons. The specimen from Panama (MNHN-ICOS-1812) was sampled at Isla del Rey (Pearl Island Archipelago) in 2000. All individuals have complete information about their total length (TL) and standard length (SL), which were recorded in millimeters (mm), and their total fresh weight (W) in grams (g).

Specimens from other Lutjanus species were also used, such as: L. novemfasciatus (n = 3); L. colorado (n = 1); L. peru (n = 1); L. guttatus (n = 4) and L. argentimaculatus (n = 1). These specimens were also collected from the same locations and at the same time period as L. argentiventris, except for the last one which comes from Kenya (Indian Ocean). For this study, all the specimens were used, including the Panamanian specimen and the other species individuals, to test the model. We included other species because in the archaeological record it is sometimes very difficult to arrive at a species level determination, at times we only succeed to determine the genus, which is quite often the case within the genus Lutjanus (e.g.Guzmán, 2008).

Among the most frequently preserved bones in the archaeological archives, 15 were selected, 39 measurements were taken, and otoliths were included (Tab. 1, Fig. 2). Measuring points were chosen in such a way that they had a good probability of being found among archaeological remains; for this reason, the slender and fragile parts were discarded and the robust parts were preferred (Desse, 1984). The measurements were taken using a digital caliper with a precision of two decimal points. Following convention, the left side bones were measured. However, in the case of the otoliths, both sagittae (left and right) were measured and a two-sample (paired samples) t-test was performed in order to identify eventual differences between sides (the null hypothesis being that the means of two populations are equal).

FIGURE 2| Lutjanus argentiventris bone measurements.

TABLE 1 | Lutjanus argentiventris bone measurements descriptions (see also Fig. 2).

An allometric regression model was employed to determine the length-length and length-weight relationships for the L. argentiventris collection. This model assumes that the growth of each body part is relative to its total body length and weight, but with distinct growth rates (Teissier, 1948; Reitz et al., 1987; Marean et al., 2001). The length-weight relationship is represented by a power function:

Where “Y” is the total weight of the fish, “X” is the total length, “a” a constant and “b” the allometric coefficient. To create this model, we also used 11 more specimen data (TL, SL, W) measured in Ecuador from fresh fishes that could not be preserved. The total sample was 48 (37 collected and preserved fishes + 11 fresh fishes not preserved).

In the case of the length-length relationships the same function was used; however, “Y” is the total length, and “X” is the body part measurement. The quality of the relationship is given by the coefficient of determination (R ² ). The best fitted measurements allowed us to reliably estimate the length and the weight of the fish from its isolated bones.

Desse et al. (1989) proposed to establish Global Rachidian Profiles (GRP) to identify the position of the vertebrae along the spine. This approach is really helpful in archaeological cases where the vertebrae are the most common element. At the same time, by knowing the height of an archaeological vertebra it is possible to estimate the size of an individual. To construct the GRP of L. argentiventris, four individuals with different sizes were selected, and measurements were taken on the caudal (diameters M1 and M2) and ventral faces (M3) of the vertebrae (Tab. 1, Fig. 2).

Results​

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The total length-weight relationships reflected a slight allometric growth (b = 3.1513), with a high coefficient of determination (R ² = 0.997) (Tab. 2, Fig. 3).

FIGURE 3| Total length (TL) to weight relationship of the modern sample of Lutjanus argentiventris.

TABLE 2 | Lutjanus argentiventris length to length and length to weight equation parameters (Length in mm and weight in g) (n = 37).

In general, it was observed that the relationships had a strong correlation (R² > 0.95) (see Tab. 1, Fig. 2 for bone measurements). The measurements relating to the maximal length of the element were well correlated with the TL. However, other measurements, based on small parts of the bones, which are the most frequently preserved, were also well correlated (see Fig. 4 for other Lutjanus species and the Panamanian specimen).

FIGURE 4| Examples of Lutjanus argentiventris graphs modelling the regression formulae. A. Dentary (Dn1); B. Maxilla (M1); C. Premaxilla (Pmx1); D. Hyomandibula (Hm2); E. Preopercle (Pop1) and F. Quadrate (Qd3).

Regarding the GRP, four M2 profiles from four individuals are represented in Fig. 5A, and profiles for the M1, M2 and M3 of a single individual are represented in Fig. 5B. In both figures, two main zones could be distinguished: the anterior zone from vertebrae 1 to 7, and the posterior zone from vertebrae 8 to 24. The anterior zone is more heterogeneous while the posterior zone is more homogeneous.

FIGURE 5| Global Rachidian Profiles of Lutjanus argentiventris. A. Measurement 2 of four Lutjanus argentiventris individuals (TL = 384 mm; TL = 509 mm; TL = 625 mm; TL = 760 mm). B. Measurements 1, 2 and 3 of one Lutjanus argentiventris individual (TL = 509 mm).

In the case of the otoliths, it was observed that the exponent of the allometric equation was superior to 1 (Tab. 2). This implies that they grow more slowly than the rest of the body. There were no significant differences between the length, height and weight of the right and left otoliths (Tab. 3).

TABLE 3 | Lutjanus argentiventris otholith measurements.

Some degree of similarity was observed between the “b” values of the length-weight relationship obtained in this study and those from previous studies from Mexico, Panama and Colombia (Tab. 4). These results indicate that Lutjanus argentiventris has a similar, often isometric, growth all along its range.

TABLE 4 | Lutjanus argentiventris total length to weight equation parameters from Mexico, Panama and Colombia (*data in cm were transformed into mm).

The tests made using other species of the same genera (Fig. 4) showed that the model could be used, at least in some instances, at genus level without much distortion. This is an important issue when dealing with Lutjanus species from other geographic areas. With regards the GRP profiles, the similar M2 values of the vertebrae of the posterior zone (Fig. 5) allowed us to use their measurement without knowing their exact rank in the rachis, which is often difficult to determine with isolated caudal vertebrae.

The otoliths on both sides can be used to estimate the size of the fish (Tab. 3).

Discussion​

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The relationships between bone measurements and body-length were robust (Tab. 2), which makes us confident that they can be used with archaeological samples. Also, it is interesting to point out that the model also works with small fish, such as the 109 mm TL Panamanian specimen (Fig. 4). Such applications have already been carried out and have shown their interest. This is notably the case of recent studies in the fresh waters of South America (Peña-León, 2011, 2013; Prestes-Carneiro et al., 2019) or in the marine waters of the Persian Gulf (Yeomans, 2015; Lidour et al., 2018).

However, this kind of study is not frequent in Latin American archaeological literature of despite its great informative potential. The study of the body length of the archaeological L. argentiventris could provide information on where the specimens were captured, depending on their size, and on ancient fishing techniques. The early life stages of L. argentiventris are found in mangroves, estuaries or shallow bays, which provide them with food and protection from large predators; adults then move to the outer rocky reefs where they continue to grow (Rojas et al., 2004). With this in mind, small-sized archaeological fish are expected to have been captured in mangroves, or at least close inshore, while larger fish came from deeper waters. The proportion of juveniles to adults can also provide information about fishing grounds and/or the health of nurseries and, beyond that, mangroves. However, these inferences should be accepted with caution because different populations of the same species may present different life history characteristics (e.g.Rojas et al., 2004, Lucano-Ramírez et al., 2014), and direct interpolation with the past could be risky. Ancient size data obtained from archaeological material could be helpful in modern ecological studies and fisheries management, given that such information could provide insight into: (1) the long-term effects of human activities on fisheries and aquatic ecosystems; (2) the acceleration and geographical extension of these effects over time; (3) the distribution and ecology of past fish populations (Erlandson, Rick, 2010).

The allometric model presented here can be used to predict the size and weight, not only of L. argentiventris, but also of its congeners, using isolated bones found in archaeological and paleontological contexts or the stomach contents of piscivorous species. This model could be useful not only for archaeologists but also for biologists working in historical ecology.

Acknowledgments​

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The authors wish to thank Héctor Parrales, Cruz Elías Pincay, Enrique Toro, Johnny Vera and the numerous other fishermen who helped to obtain the fish. The Institut français d’études andines (IFEA) provided financial support to the second author. Thanks to Jill Cucchi for the copy-editing, to María del Pilar Martínez Polanco for preparing the map, and to the reviewers and to the editor for their valuable comments

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Authors

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María Fernanda Martínez-Polanco^1,2 and Philippe Béarez³

^[1]    Àrea de Prehistòria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain.

^[2]    Institut Català de Paleoecologia Humana i Evolució Social (IPHES), C. Marcel.lí Domingo s/n, Campus Sescelades URV (EdificiW3), 43007 Tarragona, Spain. mfmartinezp@gmail.com (corresponding author).

^[3]    Archéozoologie, archéobotanique: sociétés, pratiques et environnements (AASPE), Muséum national d’histoire naturelle, CNRS. CP 56, 57 rue Cuvier, 75005 Paris, France. bearez@mnhn.fr.

Authors’ Contribution

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María Fernanda Martínez-Polanco: Conceptualization, Data curation, Formal analysis & Writing- original draft.

Philippe Béarez: Conceptualization, Data curation, Formal analysis, Funding acquisition & Writing- original draft.

Ethical Statement​

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Not applicable.

Competing Interests

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The authors declare no competing interests.

How to cite this article

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Martínez-Polanco MF, Béarez P. An osteometric approach to reconstruct the length and weight of Lutjanus argentiventris (Perciformes: Lutjanidae) for archaeological and ecological purposes. Neotrop Ichthyol. 2020; 18(3):e190106. https://doi.org/10.1590/1982-0224-2019-0106

Copyright​

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This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2020 The Authors.

Diversity and Distributions Published by SBI

Accepted June 10, 2020 by Fernando Gibran

Submitted September 07, 2019

Epub September 04, 2020