Introduction

The crocodile shark, Pseudocarcharias kamoharai (Matsubara 1936), is the only member of the family Pseudocarhariidae (order Lamniformes). It has a wide distribution in tropical and subtropical waters of the Pacific, Atlantic, and Indian Oceans (Compagno et al. 2005). Pseudocarcharias kamoharai is considered a small species (122 cm total length) with an occurrence that varies from sporadic to locally abundant. Although it uses oceanic environments, it can also be found in coastal areas; vertical distribution is epipelagic and mesopelagic, inhabiting from the surface up to depths of 590 m (Ebert 2016). This species shows a diel pattern of vertical migration toward the surface at night and away from it during daylight hours (Last and Stevens 1994; Martin 2003).

The feeding habits of P. kamoharai are scarcely known. General anatomical features consist of long and flexible teeth and strong and large jaws, in which its vigorous activity allows the capture of moderately large oceanic prey. Its jaws can protrude a considerable distance from its head. The large eyes of the crocodile shark, equipped with a reflective green or yellow and lacking an expanded iris, suggest that it is a nocturnal hunter that relies on sight to pick out the silhouettes or bioluminescence of its prey (Martin 2003). This shark is a carnivorous species that feeds on luminous fish (Gonostomatidae), lanternfish (Myctophidae), cranch squid (Cranchiidae), clubhook squid (Onychoteutidae), scaled squids (Pholidoteuthidae), sharpear enope squid (Ancistrocheiridae), and small shrimp (Compagno 2001).

The crocodile shark is globally captured as a bycatch from pelagic longline industrial swordfish, Xiphias gladius, and tuna fisheries (family Scombridae) (Hazin et al. 1990). It is also caught with other fishing gears such as gillnets (Compagno 2001). Globally, the total catches for 2007 were 14 t (FAO 2021). In Ecuador, this species has a targeted fishery, and according to Martínez-Ortiz and García-Domínguez (2013), it is captured both artisanal and industrially for local consumption. Moreover, the kind of fishing gears employed are shallow longlines and gillnets, as well as trawl nets. Despite its commercial importance, there are no current statistics regarding landings. A total of 37,748 t of chondrichthyans, including more than 30 species of sharks and rays, were landed during September 2007–December 2011 (Subsecretaría de Recursos Pesqueros 2013), out of which 0.73 t were P. kamoharai. It is important to mention that there are no records of the species since then, and there has been a high local consumption in Salinas (Santa Elena) during the last decade.

This species has a relatively rapid growth rate (k = 0.14–0.18/year), an early sexual maturation (5 years in females and 3–4 years in males), an unknown gestation period, and it presents small litters (4 pups per litter) (Fujita 1981; White 2007; Oliveira et al. 2010; Dai et al. 2012; Lessa et al. 2015; Kindong et al. 2020; Wu et al. 2020); thus, its fecundity is considered low when compared with other sharks. Most Chondrichthyan populations can only resist moderate levels of mortality before their stock is exhausted and collapsed (Camhi et al. 1998; Musick 1999; Cortés 2000), which results in a faster decline compared to other bony fishes (Sminkey and Musick 1995, 1996). Overfishing of oceanic sharks is the primary cause of population declines and increased extinction risk. Since 1970, the global abundance of oceanic sharks and rays has declined by 71%, owing to an 18-fold increase in relative fishing pressure (Pacoureau et al. 2021). Furthermore, the absence of landing records and the lack of biological and ecological studies prevent the knowledge of its current population status both locally and globally. Even though the International Union for the Conservation of Nature (IUCN) has classified this species as the least concern (Kyne et al. 2019), other authors have cataloged it as highly susceptible and vulnerable to fishing due to its low biological productivity (Murua et al. 2018).

Some of the most important biological and ecological aspects of any species are feeding, age and growth, reproductive biology, population dynamics, demography, genetics, and fisheries. Regarding trophic ecology, diet and feeding habit analyses are relevant to evaluate the ecological role and the position of a species in the trophic web (Allan and Castillo 2007). The stomach content analysis of fish provides information concerning the feeding patterns and the quantitative evaluation of the trophic habits; it is an important aspect of the management of fisheries. The diet of fish represents the integration of the most relevant ecological aspects, such as behavior, condition, habitat use, energy consumption, and intraspecific and interspecific interactions (Sagar et al. 2018). Dietary information provides support for the management of aquatic resources, mainly in aquaculture and conservation (Saikia 2015). There is scarce information on the trophic ecology of P. kamoharai, although other aspects have been studied in more detail, such as its distribution, age and growth, reproductive biology, and genetics.

The objective of the present study was to describe the diet composition and feeding habits of P. kamoharai in the Ecuadorian Pacific Ocean, along with its relationship with sex, years, and maturity stages for the estimation of the trophic niche, overlap, and level.

Methods

Sampling

The fishing port of Santa Rosa is an urban parish in Salinas, located in the Santa Elena Province, Ecuador (02° 12′ 56″ S, 80° 57′ 26″ W). The economy of the community in this area depends on fishing activity (Fig. 1). It is important to consider that there are only two seasons in Ecuador: rainy season (December–May) and dry season (June–November).

Fig. 1
figure 1

Location of Santa Rosa (●) within the continental coastal profile of Ecuador, Southern Pacific Ocean

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The Santa Rosa fishing camp was visited for two years (June 2012–May 2013 and June 2017–2018) to collect samples of P. kamoharai landings from artisanal fisheries. The total length (TL) was recorded in cm, as well as the sex of the individuals. The criteria from Conrath (2005) and Oliveira et al. (2010) were considered to evaluate the maturity stages of each organism. Sexual maturity was identified based on the following criteria: In males, the size and the condition of the clasper were evaluated (rotation, calcification, rhipidion aperture, and semen presence); while in females, the form of the cloaca (open or close) was observed to identify evidence of reproductive activity. Moreover, the mating marks and embryos were noted; in these cases, the sex, TL, and weight were annotated.

The stomach was obtained from each shark, and its gastric filling state was estimated using the reference values of Stillwell and Kohler (1982), classifying them as follows: 0 (empty), 1 (25% full), 2 (50% full), 3 (75% full), and 4 (100% full). Posteriorly, the stomach contents were placed in plastic bags and ice for their transportation to the laboratory, where they were frozen.

Laboratory work

Samples were thawed to separate the prey species found in the stomachs by taxonomic groups; they were also counted, measured (cm), and weighed (g). They were grouped according to their digestive degree according to Olson and Galván-Magaña (2002): state 1 (individuals that present complete morphological characteristics, which make it easily identifiable); state 2 (individuals without skin or eyes and exposed muscles); state 3 (individuals without a head, some body parts present and axial skeleton); and state 4 (otoliths, skeletons, and squid beaks). The identification of prey with a minimum state of digestion (state 1) was based on fish identification guides (Fischer et al. 1995; Jiménez and Beárez 2004; Robertson and Allen 2015). The axial skeleton and otoliths were used for those with an advanced state of digestion (states 3 and 4). For the vertebrae count, the works of Clothier (1950) and Clothier and Baxter (1969) were used, while for otoliths, the works of García-Godos (2001), Muñoz (2012), and Vinueza (2015) were used. The identification guides of Wolff (1982, 1984), Clarke (1986), Ingrid et al. (1971), and Xavier and Cherel (2009) were used to identify cephalopods. The rostrum length of the upper and/or inferior jaw of cephalopod beaks were recorded in order to carry out a retro-calculation of the weights, according to Wolff (1982) and Clarke (1986).

It is worth mentioning that, in the case of fishes with an advanced digestive state, the otoliths and skeletons were identified to know if they belonged to the same or different individual of one species for its respective counting. The same process was carried out for different fish species. When fragments of fishes were found (e.g., part of a head, fish eyes, skin, muscle tissue, an incomplete skeleton, only vertebrae, or an incomplete otolith), they were classified as fish remains and they were counted. Likewise, in the case of cephalopods with an advanced digestive state, the upper and lower beaks were identified to investigate if they belonged to the same or different individual of one species for its respective counting. The same process was carried out for the different cephalopod species. When fragments of squids and octopus were found (e.g., part of a mantle, part of the tentacles, cephalopod eyes, skin, muscle tissue, pens, or worn beaks), they were classified as cephalopod remains and they were counted. Lastly, we did not find detritus in any of the stomachs.

Data analysis

A parametric Kruskal–Wallis (H) test was applied for the comparison of sizes since data on length did not have a normal distribution, and it presented heterogeneity of variances both by sexes and time (Daniel 1991, Celis-De la Rosa and Labrada-Martagón 2014). Regarding the temporal analysis, females and males were grouped independently of their sex based on their sizes.

The cumulative prey curve was applied to determine whether a sufficient number of stomachs had been examined to precisely describe the diet of P. kamoharai (Hoffman 1978; Ferry and Cailliet 1996; Cortés 1997; Jiménez-Valverde and Hortal 2003). It consists in plotting the number of stomachs with food on the horizontal axis versus the accumulated diversity of the consumed prey on the vertical axis to obtain the cumulative curve and the number of tracts where the asymptote will be reached, which indicates the minimum sample size. Moreover, the coefficient of variation for each digestive tract was obtained and graphed as a secondary axis; the latter coefficient was obtained as the relationship between the standard deviation and the average diversity. For this purpose, the number of stomachs was estimated with the software EstimateS V. 8.0 (Colwell 2019), in which the number of analyzed stomachs was subjected to 100 permutations to eliminate bias with an α = 0.05. The variation of the respective number of selected stomachs was 0.05.

The ecological indices used were the numeric methods (% Ni) (Hyslop 1980) of frequency of occurrence (% FOi) and weight (% Wi) (Peláez 1997). The contribution importance to the diet of P. kamoharai of each species was evaluated through the Prey-Specific Index of Relative Importance (% PSIRI) (Brown et al. 2012):

$$\% PSIRI=\frac{[\mathrm{\% FOi}*\left(\mathrm{\% PNi}+\mathrm{\% PWi}\right)]}{2}$$

where % PNi is the prey-specific abundance and % PWi is the prey-specific weight. These parameters were obtained based on the models:

$$\% PNi=\frac{\mathrm{\% Ni}}{\mathrm{\% FOi}}$$
$$\% PWi=\frac{\mathrm{\% Wi}}{\mathrm{\% FOi}}$$

Additionally, the arrangement of the taxonomic order of the species consumed by the crocodile shark was carried out based on Young et al. (2019) for cephalopods and Van der Laan et al. (2021) for bony fishes.

The amplitude of the predator’s diet was calculated through the Levin’s Index (Bi) (Krebs 1985):

$$Bi=\frac{1}{n-1}* \left[\left(\frac{1}{\sum {Pij}^{2}}\right)-1\right]$$

where Pij is the proportion of prey j in the predator’s diet i and n is the number of prey species. The values of this index range from 0 to 1, where values < 0.6 indicate that the diet is dominated by few prey species, and thus, it would be a specialist predator; while results > 0.6 indicate generalist predators (Labropoulou and Eleftheriou 1997). Furthermore, sharks can also be classified as selective and opportunistic predators. Selective predators are those that use resources (habitats and food) out of proportion or in different proportions to their availability; while opportunistic predators use resources in the same proportion as their availability (Johnson 1980; Buskirk and Millspaugh 2006). Additionally, Munroe et al. (2014) suggest the use of patterns and defining behaviors when studying shark resources, given it is more appropriate to measure and refer to a species’ degree of specialization, rather than categorizing a species as a generalist or specialist. Sharks can be categorized with a low or high degree of specialization. In this context, a shark species with a low degree of specialization would feed on a diverse array of prey such as ctenophores, sea anemones, nematodes, crustaceans, mollusks, squids, elasmobranchs, teleostean fishes, sea turtles, sea birds, and marine mammals. Conversely, shark species with a high degree of specialization would feed on a small array of prey such as zooplankton, as well as fish in the case of certain species of sharks; in other cases, cephalopods and fish; crustaceans, cephalopods, and fish; only crustaceans; only cephalopods; only teleostean fishes, etc.

The trophic overlap analysis between sexes, sexual maturity, and annual season was carried out through the Morisita-Horn Index (Cλ) (Morisita 1959; Horn 1966; Smith and Zaret 1982):

$$C\lambda =\frac{2\sum (\mathrm{Pxi}*\mathrm{Pyi})}{\sum {\mathrm{Pxi}}^{2}+\sum {\mathrm{Pyi}}^{2}}$$

where Cλ is the Morisita and Horn Index between the sex of x and the sex of y; Pxi is the prey proportion i of the total prey consumed by the sex of the predator x; Pyi is the prey proportion i of the total prey consumed by the sex of the predator y. According to Langton (1982), values from 0 to 0.29 indicate a low overlap; from 0.30 to 0.59, a medium overlap; and from 0.60 to 1, a high overlap. Additionally, the diet composition was compared with each category based on a one-way analysis of similarities (ANOSIM) through the Bray–Curtis Index (R), where values close to 0 indicate that there are no differences between groups or confronted categories; while values close to 1 suggest that there is a difference between groups or that they are completely separated (Clarke 1993). The program Past V. 4.01 was used to calculate this index (Hammer 2020).

The trophic level (Tlk) was obtained through the equation proposed by Cortés (1999):

$$Tlk=1+\left({\sum }_{j=1}^{n=24}Pjx*Tlj\right)$$

where Tlk is the trophic level of the predatory species, n is the number of prey species, Pjx is the relative proportion of prey that compose the diet of the consumer, and Tlj is the trophic level of prey. The trophic levels of the consumed prey employed in the Tlk estimations of P. kamoharai were obtained from Cortés (1999), Froese and Pauly (2021), and Palomares and Pauly (2021).

Results

Characteristics of the sample

A total of 401 sharks were analyzed, out of which 200 were females (49.9%) and 201 were males (50.1%). Females measured between 50 cm TL and 117 cm TL (mean \(\overline{x }\)  = 102.5 SD ± 9.2) and males between 72.5 cm TL and 110 cm TL (\(\overline{x }\) = 94.2 ± 7.1). Females were bigger than males, and significant differences were observed between sizes by sex (H = 123.6; p < 0.05). Regarding sample times, the sharks from the first period of the study were slightly bigger than in the second, and temporal significant differences were observed (H = 132.1; p < 0.05).

Out of the 401 analyzed stomachs, 149 contained food (37.2%) and 252 were completely empty (62.8%). More than half of the stomachs had a gastric filling state of 0 (n = 260, 64.8%), followed by state 1 (n = 129, 32.2%), state 2 (n = 7, 1.7%), state 4 (n = 3, 0.7%), and state 3 (n = 2, 0.5%). The number of prey that conformed the diet (n = 318) where in a completely digested state, or in state 4 (n = 294, 90%); followed by an advanced digestive state, or state 3 (n = 18, 6%); then a state of digestion 1 (n = 5, 3%); and finally a state 2 (n = 1, 1%). The number of stomachs with analyzed content was sufficient to characterize the general dietary spectrum of P. kamoharai since the asymptote was reached in 100 digestive tracts. The variability of the prey items decreased sharply when stomach 36 was reached (Fig. 2).

Fig. 2
figure 2

General cumulative curve of the prey species consumed by Pseudocarcharias kamoharai in Santa Rosa, Province of Santa Elena, Ecuador. Graph plot depicting Shannon–Weiner diversity index values and coefficients of variation against the numbers of stomachs analyzed. Arrow indicates the number of stomachs where the curve got the asymptote

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Food composition

A total of 24 prey species or food components were found, of which 16 were cephalopods and eight were bony fishes. The diet of P. kamoharai was composed of 318 individuals with a total weight of 27,549.8 g. The most abundant food components were three: the cockeyed squid, Histioteuthis heteropsis (% PSIRI = 27.6), the sharpear enope squid, Ancistrocheirus lesueurii (% PSIRI = 27.4), and the purpleback squid, Sthenoteuthis oualaniensis (% PSIRI = 63.7) (Table 1).

Table 1 Species consumed by the crocodile shark Pseudocarcharis kamoharai in Santa Rosa, Ecuador, Pacific Ocean, during June 2012–May 2013 and June 2017–May 2018, along with its respective indices: percentage in number (% N), percentage of frequency of occurrence (% FO), percentage in weight (% W), percentage of prey-specific abundance (% PNi), percentage of prey-specific weight (% PWi), percentage of prey-specific index of relative importance (% PSIRI), and trophic level (Tlj). TL values were taken from Cortés (1999), Froese and Pauly (2021), and Palomares and Pauly (2021)
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Concerning feeding by sex, females presented 21 prey species distributed in 200 organisms with a weight of 16,346.2 g. The most abundant food components were three: A. lesueurii (% PSIRI = 28.6), H. heteropsis (% PSIRI = 25.0), and S. oualaniensis (% PSIRI = 10.8). The male’s diet was composed of 17 species represented by 118 specimens and weight of 11,203.6 g. The most abundant food components were three: H. heteropsis (% PSIRI = 31.4), A. lesueurii (% PSIRI = 25.5), and S. oualaniensis (% PSIRI = 13.4) (Fig. 3). There were no significant differences between the diet composition of P. kamoharai by sexes (H = 0.07; p > 0.05).

Fig. 3
figure 3

Percentages of prey-specific index of relative importance (% PSIRI) of females and males of Pseudocarcharias kamoharai for each main species and others that composed its diet in the Pacific Ocean

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The crocodile sharks obtained during 2012–2013 fed on 14 species (n = 109 specimens) with a total weight of 14,611.8 g. The most abundant food components were four: H. heteropsis (% PSIRI = 27.0), A. lesueurii (% PSIRI = 21.1), S. oualaniensis (% PSIRI = 20.3), and the neon flying squid, O. bartramii (% PSIRI = 10.3). The sharks from 2017 to 2018 had a diet composed of 19 species represented by 209 organisms and a weight of 12,938 g. The most abundant species were three: A. lesueurii (% PSIRI = 30.9), H. heteropsis (% PSIRI = 30.0), and the Jumbo flying squid, Dosidicus gigas, (% PSIRI = 14.9) (Fig. 4). No significant differences were observed between the diet composition of P. kamoharai by years (H = 0.00; p > 0.05).

Fig. 4
figure 4

Percentages of prey-specific index of relative importance (% PSIRI) of Pseudocarcharias kamoharai during 2012–2103 and 2017–2018 for each main species and others that composed its diet in the waters of Ecuador

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Immature sharks had a diet composed of seven species distributed in 18 individuals with a weight of 1864.7 g. The most abundant species were two: H. heteropsis (% PSIRI = 46.6) and A. lesueurii (% PSIRI = 25.0). The diet of mature sharks was composed of 21 species represented by 300 specimens and a total weight of 25,685.1 g. The most abundant food components were three: A. lesueurii (% PSIRI = 27.6), H. heteropsis (% PSIRI = 26.2), and S. oualaniensis (% PSIRI = 12.7) (Fig. 5). Significant differences were registered between the diet composition of P. kamoharai by maturity stages (H = 6.12; p < 0.05).

Fig. 5
figure 5

Percentages of prey-specific index of relative importance (% PSIRI) of Pseudocarcharias kamoharai for immature and mature individuals for each main species and others that composed its diet in the Southeastern Pacific Ocean

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Feeding habits

Amplitude of the trophic niche

Pseudocarcharias kamoharai was a specialist predator that preferred between three and five species of the total 24 (Bi = 0.09). This behavior was similar to the rest of the analyzed categories. Males (Bi = 0.18) presented twice the value compared to females (Bi = 0.09). The sharks from the first year (Bi = 0.27) had a triple value compared to the second (Bi = 0.08). Similarly, immature organisms (Bi = 0.38) registered a value three times higher than mature individuals (Bi = 0.10 for mature). In addition, this specialist predator is selective because it fed on its prey in different proportions based on their availability; it also showed a high degree of specialization due to its preference for squids and teleostean fishes.

Trophic overlap

The trophic overlap was high both in females and males (Cλ = 0.98), as well as for the years 2012–2013 and 2017–2018 (Cλ = 0.91) and immature and mature individuals (Cλ = 0.95). Therefore, there was no feeding segregation based on sexes, years, nor maturity stages. This feeding pattern in each category was confirmed by the Bray–Curtis Index for the prey that compose the diets, which confirmed the trophic overlap between sexes (R = 0.03; p = 0.02), years (R = 0.08; p = 0.01), and maturity stages (R = 0.06; p = 0.29).

Trophic level

The trophic level estimated was Tlk = 4.37, which indicated that P. kamoharai is a top predator, either a quaternary consumer or a tertiary carnivore. The trophic levels by sexes, years, and maturity stages were similar and ranged between Tlk = 4.37 and 4.38.

Discussion

Food composition

The present study demonstrated that the diet of P. kamoharai is mainly composed of cephalopods, which were more abundant than bony fishes. The squids A. lesueurii, H. heteropsis, S. oualaniensis, D. gigas, and O. bartramii were the most abundant species in its trophic spectrum. Cephalopods are crucial in the diets of other top predators that inhabit the same area, e.g., Alopias pelagicus had preferences for O. bartramii, D. gigas, and S. oualaniensis (Calle-Morán and Galván-Magaña 2020); Sphyrna zygaena preferred D. gigas, S. oualaniensis, A. lesueurii, and the dart squid L. diomedeae as its main prey (Estupiñán-Montaño et al. 2019); the diet of P. glauca was dominated by A. lesueurii, H. dofleini, and D. gigas (Loor-Andrade et al. 2017); the shortfin mako shark Isurus oxyrinchus mainly consumed A. lesueuri, D. gigas, and the diamond squid Thysanoteuthis rhombus (Rosas-Luis et al. 2016). Cephalopods are an abundant and ecologically important group within marine ecosystems, including the Ecuadorian Pacific; they are one of the major food sources for top predators such as sharks and large pelagic fish, i.e., Xiphiidae and Istiophoridae (Rosas-Luis et al. 2015).

Feeding habits

The crocodile shark is an active oceanic and coastal swimmer; it is considered epipelagic and mesopelagic and inhabits from the surface down to 590 m of depth (Ebert 2016). This allows the shark to access prey from different ecosystems, both neritic as well as oceanic, which is why its trophic spectrum varies. Jereb and Roper (2010) sustain that the squids A. lesueurii, H. heteropsis, S. oualaninesis, D. gigas, and O. bartramii, among others, are oceanic, epipelagic, mesopelagic, and abyssopelagic species that carry out considerable horizontal and vertical migrations from the surface down to 1,000 m deep. Their average depth during the day ranges from 200 and 400 m, while their range during the night is between the surface and 200 m deep. Squid are active and fast hunters that feed during the night near the surface (down to 70 m) on fish such as sardines, tuna, hake, and others. According to their morphological characteristics and behavior, as well as the theory of optimal foraging, it is possible that P. kamoharai feeds on such species during the night, taking advantage of the arrival of squid shoal to the surface or close to it to ingest their prey. Thus, it would employ less energy in the search and persecution of these cephalopods, and it would obtain more energy at a lower cost.

The Changos octopus, Octopus mimus, prefers habitats from the surface down to 30 m of depth. This species lives in rocky reefs, and it is common in intertidal reefs, where it looks for shelter in the cracks and below the rocks. It feeds on grapsid crabs and bivalve mollusks (Jereb et al. 2014), and P. kamoharai benefits from this coastal habitat to feed on this species of the octopus when it comes out to eat.

The frigate tuna, Auxis thazard brachydorax, the South Pacific hake, Merluccius gayi peruanus, and the pilot fish, Naucrates ductor, are coastal and oceanic, except for the last species which is completely oceanic; also, they are epipelagic, and M. gayi peruanus is also mesopelagic; they are distributed from the surface down to 500 m of depth (Robertson and Allen 2015). Pseudocarcharias kamoharai would take advantage of the horizontal movements of bony fishes to coastal and oceanic areas to consume them. However, the blue-barred parrotfish Scarus ghobban is a coastal and epipelagic species that inhabits shallow reefs and adjacent areas with sandy and rocky bottoms and feeds on detritus and benthic algae (Robertson and Allen 2015). The crocodile shark would exploit this type of habitat to feed on this species, as well as on O. mimus.

Based on the feeding behavior of P. kamoharai, as well as its specialist and selective high degree of specialization that prefers a reduced number of prey species within its trophic spectrum, it is suggested that this shark would be exploiting a common feeding zone. Independently from sex, time, and maturity stage, it benefits from these zones with high availability of prey, which allows a selection based on its energy requirements. Furthermore, this topic is of great significance because in the past, sharks have been depicted as mobile generalists with wide, sometimes global ranges, that feed opportunistically rather than forage for specific prey items (Wetherbee et al. 1990). Based on the number of prey found in the stomach analysis of the sharks, different proportions of cephalopods and teleostean fishes were consumed by sexes combined, in females and males, immatures and matures, and by year. This elucidates how the predator and its prey are distributed in the environment. There is no method to analyze the exact number of available prey items in their ecosystems, but it is possible to know the number of prey consumed by this predator due to their trophic spectrum.

The trophic level of this species suggests that it is a top predator, either a quaternary consumer or a tertiary carnivore. These values were similar to those from the common thresher Alopias vulpinus (Tlk = 4.20, Cortés 1999), P. glauca (Tlk = 4.20, Córdova-Zavaleta et al. 2018), I. oxyrinchus (Tlk = 4.23, Rosas-Luis et al. 2016), and the white shark Carcharodon carcharias (Tlk = 4.50, Cortés 1999), while A. pelagicus obtained higher values (Tlk = 5.00, Calle-Morán and Galván-Magaña 2020). The latter is in accordance with Cortés (1999), which sustains sharks are a group of tertiary consumers with trophic levels higher than four, and that they occupy similar trophic positions than marine mammals but higher than birds.

Conclusions

The present study provided relevant information regarding the diet and feeding habits of P. kamoharai on a regional and global scale due to the lack of information on the trophic ecology of this species. This predator demonstrated a preference between three and five prey species from a diet constituted by 24 dietary components, of which 16 were cephalopods and eight were bony fishes. It is a specialist predator, with a trophic level of a quaternary consumer or a tertiary carnivore. A high overlap was observed between sexes, years, and maturity stages. This study on the feeding behavior of the crocodile shark and the species that compose its diet, that is, those that coexist in its habitat, is relevant given it allows us to understand the trophic relationships between the predator and its prey, as well as the flow of matter and energy that characterizes an ecosystem. This is the first study that provides information regarding the ecological importance of the crocodile shark in the marine ecosystems of the Pacific Ocean, given they act as natural regulators of the population density of their prey.