1. Introduction
Otoliths are hard structures composed mainly of calcium carbonate situated in the membranous region of the inner ear of all teleost fish. These structures are primarily studied since they can provide a wide array of information on fish physiology, history, and environments such as growth characteristics, life history, migratory patterns, homing fidelity, microchemistry, and age data [
1]. The potential application of fish otoliths to fishery science continues to advance and is being maximized by recently gaining the focus and attention of scientists [
2]. Another factor strengthening the use of phenotypic markers such as otoliths is that phenotypic variations may exist even in the absence of genetic variation [
3,
4,
5]. Fish otoliths are widely used for species and population segregation because of the variations in appearance and shape [
6,
7,
8,
9]. Further, otolith morphology was shown as a powerful indicator of fish stock and population structures [
10,
11,
12,
13,
14,
15,
16]. For instance, otolith morphometrics and shape analysis were shown to discriminate stocks of several fish species such as
Gadus morhua Linnaeus, 1758 [
17],
Glossogobius sparsipapillus Akihito and Meguro, 1976 [
18], and
Serranus cabrilla Linnaeus, 1758 [
19].
Fish stocks, as defined by Hilborn and Walters [
20], are a large group of fish that have similar life history traits and can independently sustain the population. Differences in distribution, life history, and genetics are a few of the key elements that identify fish stocks [
21]. Certain manifestations of these include variations in morphology, genetics, movement patterns, maturity, growth, and other life traits [
22]. Many works have shown that variation of fish otolith features (morphometry, shape, and microchemistry) of different stocks may be affected by several factors. Two of the main combined factors usually associated are environmental conditions (depth, salinity, and temperature) and genetics [
2,
8,
23,
24]. Other factors which may also affect otolith features are feeding habits and food availability [
15,
25,
26]. The possible effects of fishing pressure in various fishing grounds on otolith shape and morphometry were also raised by various scientists [
27,
28,
29,
30].
The inherent characteristic of the Philippines as an archipelagic country with over 7000 islands that are separated by interconnected water bodies invites questions on the possible delineation of fish stocks. As these waters are constantly interacting with each other, the active exchange of fauna and nutrients that support them are certain. Additionally, the intrinsic characteristic of fish to migrate in various temporal and spatial scales needs to be factored in as this promotes mixing among separate populations. Treating separate stocks as one may lead to the localization of overfishing and management efforts. The fishing grounds within the Philippines are delineated into 12 Fisheries Management Areas (FMAs) for the purposes of resource management [
31,
32] but the scientific basis for the delineation of the boundaries of these areas to support fishery management initiatives is scanty. This study would provide a good opportunity for validating and possibly refining arbitrarily drawn boundaries of designated FMAs for managing fish stocks that are now largely under overfished conditions.
Information on the segregation of fish stocks in an archipelagic country like the Philippines is important, especially in studies on the assessment of stocks and their dynamics, thereby guiding management interventions that would promote the sustainable harvest of shared resources in an open-access fishing industry. The study of intraspecific phenotypic variations is essential to make strategies for sustainable harvest and conservation as it describes the flexibility of species in response to diverse habitats and the prevailing conditions therein [
33,
34,
35,
36].
The genus
Decapterus is one of the most economically important fish groups in the Philippines that are widely distributed in various fishing grounds including the Bohol Sea (FMA 10), Davao Gulf (FMA 2), Moro Gulf (FMA 3), Sibuyan Sea (FMA 12), Sulu Sea (FMA 4), and Visayan Sea (FMA 11) [
37,
38]. At present, there are 11 species listed under the genus [
39,
40]. Species under the group are collectively locally known and reported as “galunggong” even in fishery statistics. Past and recent fishery production reports show that “galunggong” or roundscads are among the top commercially important small pelagic species in the Philippines, providing 4.24 to 4.59% (180,137.67 to 202,003.85 T) of the country’s total annual volume of fish production from 2020 to 2021 [
41].
A subgroup in the genus is known as the redfin group clustered by Kimura et al. [
39]. One member of this cluster is the redtail scad,
Decapterus kurroides Bleeker, 1855, the species of interest in this study. The three other species are
Decapterus akaadsi Abe, 1958,
Decapterus tabl Berry, 1968, and
Decapterus smithvanizi Kimura, Katahira and Kuriiwa, 2013 [
42,
43]. The
D. kurroides is one of the main species caught in ring net and purse seine operations observed in selected fishing grounds such as Iligan Bay [
44], Davao Gulf [
45], Lingayen Gulf [
46], and West Philippine Sea [
37]. However, despite its economic importance, dominance in commercial gear catch, and ubiquity within Philippine waters, only a few studies were carried out to understand its biology, fishery, and stock dynamics.
At present, species delineation alone is difficult without the aid of molecular methods, which are expensive and time-consuming. Apparently, for this reason, the investigation of pelagic fish structures in the Philippines is rarely performed. In this study, we focus on two adjacent fishing grounds that are designated as FMA 4, represented herein by the Sulu Sea, and FMA 12, represented by the Sibuyan Sea. Both areas have basin-like characteristics and have limited water exchange with adjacent water bodies. The main goal of the study is to determine the possible separation of D. kurroides stocks using otoliths as this offers simpler and less expensive tools for fisheries management. Successful implementation of this investigation would offer a cheaper alternative for implementing population studies of other species and in other FMAs throughout the country and would provide inputs to support policies that are urgently needed for arresting declining fish populations in the central Philippines.
4. Discussion
In this study, morphometric and shape indices of otoliths were used to delineate stocks of
D. kurroides from two adjacent fishing grounds in the Philippines. The
D. kurroides from the Sibuyan Sea are longer and heavier than those collected from the Sulu Sea. Primary results have shown significant positive relationships between the fish length and the otolith descriptors. The positive relationships between fish length and the direct (OL, OH, OW, OA, and OP) and derived (EL, AR, and CO) descriptors are to be expected as these attributes (length, weight, and hence area and perimeter) go along with fish growth. From thereon, it can be drawn that with growth, the otolith becomes more elliptic, its aspect ratio increases, and it becomes more compact. Otoliths are known to grow continually subsequently with fish growth. New materials are deposited incrementally which contributes to the increase in values in these indices, while also incorporating materials that can be analyzed to trace back migration and environmental history (e.g., [
54,
55,
56,
57,
58,
59,
60]). The negative relationships between fish length and the derived descriptors, RE, SQ, RO, and FF mean that as the fish grows, the rectangularity, circularity, and form factor decrease. This trend in the relationships between fish length and otolith size and shape descriptors was also observed in
Merluccius capensis Castelnau, 1861 [
61],
Neogobius melanostomus (Pallas, 1814) [
62,
63],
Decapterus macarellus (Cuvier, 1833) [
64],
Mulloidichthys flavolineatus (Lacepède, 1801) [
47], and
Terapon jarbua (Forsskål, 1775) [
65]. Since otolith shapes are species-specific, it is not surprising that the relationship of the
D. kurroides length can be directly or indirectly proportional to a specific otolith descriptor. Aside from being species-specific, otolith shapes can also vary from region to region, which may also be used to delineate fish stocks [
6,
66].
The independent sample
t-tests revealed which descriptors separate the stocks from Sulu from those of Sibuyan. It was evident that
D. kurroides from the Sibuyan Sea have longer, heavier, and wider otoliths than those from the Sulu Sea. In addition, the otoliths of
D. kurroides from the Sulu Sea are less elliptical and less irregular than the Sibuyan Sea samples. These data are further elucidated in
Figure 4 and
Figure 5. Size-related indices (OL, OW, OA, and OP) were most important in distinguishing the otoliths of
D. kurroides from the two fishing grounds. The observations in this study are consistent with the definition of Hilborn and Walters [
20] for different stocks. Data on the mean shapes (
Figure 6) of the otoliths have also shown clear regions of difference between the two populations.
Otolith shape is known to correspond to the distinct environment that the species is in [
24], with genetics [
67] or the interactions between the fish, environment, and its genetic make-up [
68]. This then leads to the segregation of species into populations or stocks, sharing the same parameters for growth and mortality, as defined in Sparre and Venema [
69]. In the case of
D. kurroides from the seas of Sibuyan and Sulu, the populations may be treated as discrete based on the signatures derived from otoliths defined in shape and morphometry. It is, however, not proven or studied whether there is mixing between these two populations, which are in close proximity to each other (refer to
Figure 1). Fish, especially pelagics, have an inherent characteristic to migrate in various spatial and temporal scales as a function of life history, foraging, and as an adaptive response.
A population study of
Auxis thazard (Lacepède, 1800),
Selar crumenophthalmus (Bloch, 1793),
Rastrelliger kanagurta (Cuvier, 1816), and
Sardinella lemuru Bleeker, 1853 collected from Celebes and Sulu seas did not reveal the occurrence of distinct stocks [
70], and this is probably due to the effects on water exchange of the much larger Pacific Ocean to the Celebes Sea and of the West Philippine Sea on the Sulu Sea. Although our study is based on otoliths, the consistent difference of
D. kurroides, which indicates the occurrence of different stocks based on the analyses of the samples themselves and their otoliths, is most likely due to the differences between the two water bodies. Although, the monthly sea surface temperatures between the Sulu (29.45 ± 0.71 °C) and Sibuyan (29.40 ± 0.95 °C) seas for the past decade are statistically similar [
71] (
p < 0.05), their sea surface salinity oscillates differently, due to their respective adjacent main water tributaries. Results from this previous study revealed that water salinity in the Sibuyan Sea is higher (>35 PSU) than in the Sulu Sea (<35 ppt), apparently because water exchange with adjacent water bodies is limited from the Pacific Ocean [
72]. The salinity of the Sulu Sea is also affected by the less saline waters of the West Philippine Sea. These earlier results from others are worth reporting because salinity is one of the major factors that affects otolith variation among populations [
5,
57,
73]. This is due to its ability to affect otolith’s aragonite development and element uptake [
2]. These effects potentially cascade to several otolith features due to the variable formation of fish otoliths. It was also observed that fish exposed to more saline waters have longer [
74], heavier otoliths with higher isotopic carbon and oxygen concentrations [
75], and greater and wider otolith growth and increment depositions [
76,
77]. These may be attributed to the
D. kurroides in the Sibuyan Sea having longer (more elliptic), larger, and heavier otoliths. Additionally, remote-sensed chlorophyll-a data from NASA [
71] revealed that the Sibuyan Sea is more productive than the Sulu Sea, and this may also be a factor in the different otolith features and shapes between the two sites. Food availability potentially increases somatic growth, consequently increasing otolith growth [
15,
26]. In some cases, not only growth may be affected but also even otolith shape. Otolith shape analysis was successful at separating the otolith shapes of fish that experienced scarcity or an abundance of food [
25]. This may have brought about the significant irregular (CO) and wider (AR) otoliths of Sibuyan Sea individuals.
In sum, this study demonstrates the application of otoliths as a tool for fishery management. It reveals the possible occurrence of different fish populations of D. kurroides in adjacent basin-like fishing grounds. It is necessary to consider investigating other sentinel pelagic species to confirm these results but the use of otoliths as a first recourse or in lieu of the more expensive molecular methods offers a powerful surrogate tool for generating inputs for fisheries policies at a much faster rate. This would undoubtedly help resolve species connectivity issues across the different FMAs and for managing critically threatened pelagic fisheries throughout the Philippines.