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Article

An Insight into the Feeding Ecology of Serranus scriba, a Shallow Water Mesopredator in the Northern Adriatic Sea, with a Non-Destructive Method

by
Ana Lokovšek
1,2,*,
Martina Orlando-Bonaca
1,
Domen Trkov
1 and
Lovrenc Lipej
1
1
Marine Biology Station Piran, National Institute of Biology, Fornače 41, SI-6330 Piran, Slovenia
2
Jozef Stefan International Postgraduate School, Jamova Cesta 39, SI-1000 Ljubljana, Slovenia
*
Author to whom correspondence should be addressed.
Fishes 2022, 7(4), 210; https://doi.org/10.3390/fishes7040210
Submission received: 8 June 2022 / Revised: 18 August 2022 / Accepted: 19 August 2022 / Published: 20 August 2022
(This article belongs to the Section Biology and Ecology)
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Abstract

:
Serranus scriba is a common member of the coastal fish community in the Adriatic Sea, but knowledge about its feeding ecology is scarce. The aim of this paper is to present new evidence about its food preferences and feeding habits. An innovative non-destructive method of fecal pellet analysis was used for this study. This method does not require sacrificing specimens and the fish can be released back into the sea alive after the laboratory work. The results demonstrated that S. scriba mainly preys on decapods, followed by polychaetes, isopods, fish, mollusks and swarming shrimps. The calculated index of trophic diversity (ITD) value of 0.89 indicates that it is an opportunistic feeder that feeds on a wide range of different prey. According to the calculated trophic level of 3.43, which is higher than that of other members of the community, S. scriba is also an important piscivorous predator. With age, S. scriba undergoes an ontogenetic shift. The proportion of crustaceans, gastropods and polychaetes decreases with age and body size, while the proportion of fish increases.

1. Introduction

The northern Adriatic Sea is a shallow coastal sea, where infralittoral habitats are home to rich fish assemblages, with many members closely associated with the seabed [1]. Anthropogenic activities can lead to habitat disturbances, changes in fish community structure and changes in ecosystem functioning [2,3,4,5]. Therefore, some fish groups can be used as a tool to assess changes in habitat conditions. Currently, robust methodologies are being developed in an effort to assess the most suitable indicator species for the evaluation of the status of coastal fish assemblages [6].
The most important coastal fish families in the Mediterranean Sea in terms of abundance and frequency of occurrence include Gobiidae, Labridae, Bleniidae, Sparidae, Tripterygiidae, Atherinidae, Mugilidae, Mullidae, Pomacentridae, Sygnathidae and Serranidae [1]. The family Serranidae includes 538 species from temperate and tropical seas [7]. This study focuses on one of the smaller members of the group, the most common member of the family in the coastal area of the Mediterranean, the painted comber (Serranus scriba (Linnaeus, 1758)). S. scriba is a subtropical species that inhabits rocky habitats with algal covers and seagrass meadows, distributed in the Mediterranean Sea, the Black Sea and the eastern Atlantic Ocean from the Bay of Biscay to Mauritania [8,9]. S. scriba is very common throughout the Mediterranean Sea, and is usually found at a depth of 0 to 30 m [10]. Normally it does not grow larger than 200 mm, but the largest specimen captured to date measured 323 mm and weighed 456.7 g [11]. S. scriba is not commercially exploited in the Mediterranean area, but it is often caught as by-catch by recreational fishermen [12]. Despite its wide distribution, the ecology and feeding habits of the species are poorly known. According to some studies, S. scriba is often predating on crustaceans, especially decapods [10] and smaller necto-benthic and crypto-benthic fish species [13,14]. It has also been documented that the removal of a mesopredator such as S. scriba, may result in the proliferation of small fishes and could, thus, affect the populations of small invertebrates [15]. Studies on the feeding ecology of S. scriba in the Adriatic Sea have not been conducted yet, although species is widespread and common in the area. S. scriba is supposed to play an important role in the trophic web [16,17,18]; therefore, there is a need for in-depth knowledge of its food and feeding habits.
Feeding ecology describes the diverse feeding modes and morphological, physiological and senso-neural adaptations to the prey type and the prey abundance in the habitat [19,20,21] and contributes to the understanding of resource partitioning [22,23], habitat selection [21], predation [24,25,26,27], evolution [28], competition, trophic ecology [29,30] and energy transfer within and between ecosystems [31,32,33].
The feeding habits of fish species are usually based on the examination of stomach contents [34,35,36], which requires a large number of sacrificed fish. Therefore, it is ethically questionable and particularly unsuitable for the study of endangered or rare fish, and species with low population densities or inhabiting marine protected areas [37,38,39]. Alternatives to traditionally used method of stomach content analysis are non-lethal methods, among which the most effective method is stomach flushing [40]. Although stomach flushing is one of the most efficient non-lethal methods used to date [40,41,42], this procedure can cause mortality of up to 60% in some fish species [42] and can have a negative effect on fish condition [41]. Most non-lethal methods cannot be regarded as non-destructive, because the process of obtaining samples is still quite invasive and can cause injuries or even death [42]. In our study, we used a non-destructive method that is less invasive and does not harm the fish.
The aim of this study is to present the first data on the feeding ecology of S. scriba in the northern Adriatic Sea and to propose the application of a recently developed non-destructive and non-lethal method for isolating undigested prey from feces in order to study the fish diet. The main goals of the paper are (i) to identify and categorize the prey items of S. scriba in the northern Adriatic Sea, (ii) to estimate the trophic level (TROPH) of S. scriba and compare it with other species in the community and that respective to other studies, and (iii) to calculate the index of trophic diversity (ITD).

2. Materials and Methods

2.1. Study Area

The Gulf of Trieste is the northernmost part of the Adriatic Sea, stretching across the coasts of Italy, Slovenia, and Croatia. It extends from Cape Savudrija to Grado and is partially enclosed by the Istrian peninsula to the south. It covers an area of 551 km2 and includes a water volume of 9.5 km3 [43]. The Gulf is very shallow, with an average depth of only 18.7 m and a maximum depth of 37 m. The area is known for the highest amplitudes between high and low tides (average = 88 cm; [44]) and the lowest temperatures in winter [43]. Water temperature and salinity are strongly influenced by river outflows. In winter, the temperature can drop down to 6 °C and in summer it warms up to 26 °C, while the average salinity is around 37–38 [45,46]. Between April and September, temperature stratification occurs in the water column, with a seasonal thermocline in spring [43].
The Slovenian part of the Gulf of Trieste accounts for one third of the entire surface of the Gulf [47]. The coastal relief varies from steep rocky cliffs to gradual sloping beaches. The lower part of the coast, in particular, has already been heavily modified due to anthropogenic development and urbanization. Today, only one fifth of the coastline remains in its natural state [44,47]. The bottom along the coast is mainly rocky and consists of alternating layers of flysch, sandstone and soft marl.

2.2. Fieldwork

Between August 2020 and June 2021, 150 specimens of S. scriba were collected in shallow Slovenian waters, at a depth range of 0.5–5 m. The sampling sites were selected according to the benthic habitat type, since S. scriba predominantly inhabits a rocky bottom with different algal cover, sometimes also bordering with seagrass meadows (mostly Cymodocea nodosa). Fish were caught at eight locations in the Slovenian part of the Adriatic Sea (Figure 1, Table 1). The majority of specimens were caught in front of the National Institute of Biology-Marine Biology Station in Piran, for a total of 44 fish, 22 of which were caught in autumn between the end of September and October 2020 and 22 in spring, between the end of April and June 2021. The rest were caught at other localities (Table 1). Additionally, at the Cape Piran, Cape Ronek and Pacug sites, the parallel transect method [1,48] was used to monitor the density of painted comber populations. A measuring tape (50 m long) was laid on the rocky bottom at depths ranging from 1.5 to 4 m. After a few minutes, when the fish had become accustomed to the diver’s presence [49], all the fish were counted 1 m to the left and then 1 m to the right of the transect line. The data were transformed into densities expressed per 100 m2.
Before specimen collection, we took 15 min each time to observe feeding behavior. We were interested in how S. scriba approaches and grasps its prey, where it hunts and what interactions they have with each other and with other species. During the observation, the snorkeler calmly floated on the surface of the water, carefully observing the action while moving the bait along the seafloor.
Fish were collected by snorkeling, using a barbless hook (size 6, Crivit Lasercut Selection) with a bait. During the first few days of fieldwork, different baits were tested, from pieces of squid, snails of the genus Gibbula, chunks of anchovy, to hermit crabs, which proved to be the best bait to attract S. scriba. The hook was attached to a 3 m long nylon line (0.20 mm, 3.1 kg, Crivit Specimen Line) hanging from a modified wooden pole. After the fish took the bait (hook and bait were completely in its mouth), we achieved that the hook was anchored in the oral cavity of the fish with a short pull on the nylon. Therefore, the fish did not swallow the hook, which could lead to internal injuries of the esophagus or stomach and thus death. As soon as the fish was hooked, we pulled it over the surface of the water as quickly as possible and took it off the hook. On one snorkeling session, 1–15 S. scriba individuals were caught and placed in buckets of filtered seawater. Each fish was placed in its own bucket with filtered seawater (through a 125-µm sieve) to remove any impurities that might affect the results. The specimens were transported to the laboratory of the National Institute of Biology-Marine Biology Station in Piran as soon as possible (in less than one hour after the sampling was completed).

2.3. Laboratory Work

At the laboratory of the National Institute of Biology-Marine Biology Station in Piran, each bucket was labeled with the serial number of the fish and equipped with an aerator to supply air. The aerator was placed above the bottom of the bucket to prevent the feces from fragmenting due to air bubbles.
The fish were then accurately weighed using the Sartorius CP 225D balance and measured with caliper to the nearest millimeter. Total body length (TL, length from the tip of the snout to the end of the caudal fin), standard body length (SL, length from the tip of the snout to the base of the tail) and fork length (FL, length from the tip of the snout to the center of the fork in the tail), were measured. The measured fish were classified into age groups of 1, 2, 3 and 4 years according to the study of Tuset et al. [50].
The buckets were then left covered for at least 24 h. During this period, all fish digested the prey and defecated. After 24 h, no feces containing prey items were excreted; only white, “empty” feces were excreted by a few fish after this period. Thin, white, stringy feces are an indicator of an empty gut. The fecal pellets were then carefully removed using a modified pipette and stored in 70% ethanol. Fecal pellets from each fish were stored separately in a labeled vial with the serial number of the fish. The contents of the bucket were filtered through a 125 µm sieve to capture any remaining pieces of prey and fish that were released back into coastal waters. Almost all the fish survived the procedure, but two out of 150 fish died in the buckets due to internal injuries after swallowing the hook. When released, the fish were in good condition and swam away immediately.
The contents of the fecal pellets were examined under an Olympus SZx16 stereo microscope with an Olympus DP74 camera. Fecal pellets consist of undigested prey items and peritrophic membranes. The undigested prey items were determined to the lowest possible taxonomic level and counted. The number of prey specimens was identified by the presence of its typical body parts, such as carapace or claws, in the sample. For example, when we found a pair of claws or a carapace of an anomurid crab of the genus Pisidia, we assumed that the fish had caught and digested just one Pisidia sp. specimen. In addition to taxa with hard body parts, taxa with soft bodies were also recognized by their undigested parts such as outer body layers (e.g., polychaetes or fish eggs). The prey items were identified using identification keys for the marine fauna of the Mediterranean and northwestern Europe [51,52,53]. Each prey was measured and photographed under an Olympus SZx16 stereo microscope with an Olympus DP74 camera. Fish species were determined through the identification of otoliths in pellets, using the Atlas of Otoliths for the Western Mediterranean [54] and the AFORO online database [55]. According to the formulas in the AFORO online data base [55], we calculated the total length of prey fish using the lengths of the otoliths.

2.4. Data Analyses

The prey frequency of occurrence (prey occurrence in the fecal pellets) (%PF; [56]) was calculated as follows: %PF = ns/NS, where ns represents the number of fecal pellets with prey s and NS the number of total fecal pellets. Additionally, the numerical index (%PN; [56]) of prey in the fecal pellets was calculated: %PN = ni/NI ∗ 100, where ni represents the total number of prey belonging to taxon i, and NI represents the total number of all prey in all taxonomic units.
The prey were divided into four categories: main prey, secondary prey, complementary prey and accidental prey (Table 2), as listed by Hureau [57].
Diet diversity was expressed by the index of trophic diversity (ITD), which is a modified Shannon-Wiener diversity index (H′; [58]):
ITD = 1 − H′.
The ITD value ranges from 0 to 1, where 0 means no diversity and 1 means maximum diversity. ITD was calculated at the consistent taxonomic level that is at the order level.
TrophLab, a stand-alone Microsoft access for estimating trophic levels, was downloaded from www.fishbase.org (accessed on 20 July 2021) [59] and used to calculate the TROPH index of the species studied. The trophic levels of S. scriba were calculated [59,60] as:
𝑇𝑅𝑂𝑃𝐻𝑖 = 1 + Σ𝐷𝐶𝑖𝑗 ∗ 𝑇𝑅𝑂𝑃𝐻𝑗,
where DCij represents the proportion of prey j in the diet of species i and TROPHj represents the partial trophic level of prey j. To demonstrate the importance of each taxon in the diet, the SIMPER function in the R programming environment [61] was used:
[𝑖𝑗𝑘] = 𝑎𝑏𝑠(𝑥[𝑖𝑗] − 𝑥[𝑖𝑘])/𝑠𝑢𝑚(𝑥[𝑖𝑗] + 𝑥[𝑖𝑘]),
where x represents the abundance of prey taxon i in samples j and k. The index is the sum of the individual contributions of all prey taxa of species S:
d[jk] = sum (i = 1…S) d[ijk].
The SIMPER function performs a pairwise comparison of prey groups and returns the average contributions of each taxon to the overall Bray-Curtis diversity index (Available at: https://www.rdocumentation.org/packages/vegan/versions/2.4-2/topics/SIMPER; accessed on 26 July 2021). Spearman’s correlation and multivariate analysis (Bray-Curtis similarity for differences between fishes, locations and between ages for S. scriba) were performed in R (R 4.0.2 software package; R Development Core Team 2008, Vienna, Austria) using the PRIMER v7+ (PERMANOVA software, Albany, New Zeland) [61,62] package. A p-value of <0.05 was chosen to determine the statistical significance of the trend.

3. Results

3.1. S. scriba Density and Biometry

On performed visual parallel transects, S. scriba density varied between 6 and 12 ind./100 m2 at different localities and depths. The highest density was calculated at Cape Ronek, where 11–12 ind./100 m2 were observed at 1.5 m depth (Table 3). Average density at Cape Ronek was 11 ind./100 m2 and 6.5 ind./100 m2 in Pacug and 7 ind./100 m2 at Cape Piran (Table 3). Based on the results for the Slovenian part of the Gulf of Trieste, the calculated average density of S. scriba is 8.34 ind./100 m2. The total length of the 150 specimens caught, ranged from 108 mm to 217 mm, while the weight ranged from 17 g to 163 g (Table 4). According to the length structure of the fish, we estimated that most fish were 1 or 2 years old (Table 5), indicating that the majority of caught fish were juveniles.

3.2. Feeding Habits of S.scriba

A total of 32 taxa were identified as prey items in the fecal pellets of S. scriba (Table 6). The most abundant prey of S. scriba were crustaceans (%PN = 69.21%, %PF = 98.67%), followed by polychaetes (%PN = 12.63%, %PF = 40.67%), mollusks (gastropoda: %PN = 4.66%, %PF = 17.33%; bivalvia: %PN = 0.67%, %PF = 2.67%) and fish (%PN = 6.82%, %PF = 20.67%; Table 6). Among crustaceans, the most abundant and also most frequent prey items were decapods (PN% = 46.75%, %PF = 96.67%), followed by isopods (PN% = 13.64%, %PF = 37.33%). The most common prey items found was Pisidia sp. which alone accounted for 18.80% of all prey. Polychaetes, mainly vagile species (suborder Errantia), accounted for 12.63% of prey items, which is the second most frequent prey (Table 2 and Table 6). Teleost fishes (6.82% of total prey items) constituted the complementary prey of 1st order (Table 2). The following fish species were identified (see Table 6): Atherina hepsetus Linnaeus, 1758, Gobius fallax Sarato, 1889, Symphodus ocellatus (Linnaeus, 1758), S. cinereus (Bonnaterre, 1788), Pomatoschistus bathi Miller, 1982, Mullus surmuletus Linnaeus, 1758 and Gobius cruentatus Gmelin, 1789. In some cases, only fish vertebrae were found in the fecal pellets and species identification was not possible. In addition to prey with hard parts, prey with soft body structure were also identified in the feces such as fish eggs (N% = 5.99, %PF = 11.33%) and cuticles of polychaete worms. The diet of S. scriba specimens was compared between age groups. The majority of the captured S. scriba in our study were less than 3 years old and less than 173 mm long (TL). While the adult specimens of S. scriba prey mainly on decapods, isopods and fish, the diet of juveniles consists of polychaetes and small crustaceans such as mysids, amphipods and shrimps. Two-year old and older individuals tend to supplement their diet with epibenthic and nectobenthic fish, which coincides with the increase of the trophic level with age (up to 3+) (Table 7). The proportion of fish in the diet increased from an initial 3.97% at age 1 to around 10% by age 4. The proportion of crustaceans decreased from 71.52% to 40.66% between the 1st and the 4th year (Figure 2). The proportion of eggs in the diet increased from 1.99% in 1-year-old individuals to 35.16% in 4-year-old individuals. The average calculated trophic diversity index (ITD) was 0.89 (on a scale of 0 to 1, where 0 means no diversity and 1 means highest diversity). No statistically significant difference was found between the diet and age/length composition of S. scriba at the different sampling sites (Bray-Curtis, p < 0.05).
During the fieldwork, it was noted that S. scriba specimens are more active in the morning and evening, when they were observed to be feeding actively. Our personal observations also demonstrated that S. scriba usually monitors visually open areas and upon detection of a passing prey (or a bait) performs a short but very fast burst chase and then upon completion of prey pursuit occupies another waiting spot. The waiting spot was usually within heterogenous rocky reefs, but we also observed them waiting in Posidonia oceanica meadows or hiding in algae. In many cases, S. scriba was observed lurking behind a rock or under a boulder, waiting for a prey to come close enough to grab it and suck it into their mouths. The prey was consumed with a quick suction. If the prey was too large, it was usually spat out several times before consumption. This activity often attracted several other S. scriba, who then competed for the prey. Larger, dominant S. scriba often exhibited aggressive behavior and chased off smaller specimens. On the other hand, on a few occasions, younger S. scriba (juvenile and subadult individuals) were also observed cooperating and hunting between rocks in groups of up to 6 individuals. Regarding interspecific interactions, in a few cases S. ocellatus was observed to clean parasites from S. scriba. The latter stood vertically with their heads down and allowed S. ocellatus to remove parasites.

4. Discussion

4.1. Advantages and Disadvantages of Non-Destructive Methods of Sampling and Analyses

A recently developed non-destructive method [63] was tested in this study on S. scriba to detect prey in fecal pellets. The advantage of the fecal examination method is that it can be used on smaller-sized fish, even smaller than 15 mm [63], and that the survival of all specimens makes these procedures suitable for use in protected marine areas and for the study of protected species or species with low population densities [37,40], and also renders the research more ethical without compromising quality. Another modern method that is also non-lethal and frequently used for diet estimation is stable isotope analysis; however, this method cannot provide taxonomic resolution and is more useful for describing a long-term assimilated diet [64]. This method can be complementary to stomach contents analysis or analysis of feces. Advantage of this non-destructive method is also shorter handling time, since a shorter handling time means a higher chance of survival and a less stressful experience for the animal [42,63]. The method is easy to use on less mobile, small and medium-sized coastal fishes, as the fish can be placed in buckets overnight and complex aquarium equipment is not needed. The method is far more complicated to use on open-water fish or larger fish, which cannot be housed in buckets or similar small containers. Nevertheless, most members of coastal fish assemblages are small to medium in size, and therefore the feeding habits of many species can be studied using this method.
While the fieldwork for the capture of fish proved to be particularly time consuming, since it required 4 to 6 h of snorkeling to catch 10 specimens of S. scriba, it should be noted that long capturing times may be connected with the use of a barbless hook, which can reduce catch efficiency, but it also significantly reduces unhooking time, stress and hooking injuries [65,66,67]. Another important factor is the size of the hook, as larger hooks decrease the incidence of deep hooking and consequently prevent serious injuries and bleeding [68,69,70,71]. In our study, we used large and thin hooks (size 6). Only 2 fish out of 150 died due to hooking. Thus, our fishing technique proved to be suitable for the non-destructive diet analysis method. The diameter of the nylon line is another important factor. We used nylon line, 0.20 mm in diameter, because S. scriba has sharp teeth that can bite through thinner thread.
In other studies, S. scriba were caught using traditional fishing gears, such as floating nets and longlines, but these methods are more likely to injure or kill the fish [10,14,17,72,73,74]. Working with live fish requires appropriate living conditions for the captured specimens, which means regular water changes, adequate oxygen levels and appropriate water temperature.
During our sampling surveys, mostly juvenile and sub-adult fish were caught, since young fish are less wary and more curious than older, experienced fish. Due to the predominance of juveniles in the sample, the data on trophic levels and prey proportions for all S. scriba individuals are biased to some extent, so it is better to consider trophic levels and prey proportions separately for each length (age) class.
Prey items in the fecal pellets of S. scriba were sometimes so decomposed that identification down to the lowest taxonomic units was impossible, but because their prey consisted mainly of crustaceans, polychaetes, fish and other taxa with hard, distinguishable body parts that are not so easily decomposed, identification of family, class or order was still possible (see Figure 3 and Figure 4). Even some soft parts of prey, such as the cuticle of polychaetes and fish eggs, were found, demonstrating that species with softer bodies can also be recognized in feces. The quality of the fecal examination method was tested on five dead adult specimens of S. scriba obtained as bycatch from fishermen. These individuals were dissected and the stomach contents were isolated to compare the stage of decomposition in the stomach and feces of S. scriba. We were able to confirm that the stage of decomposition was similar. Fish exanimated by the non-destructive method probably defecated faster due to stress and consequently the prey did not decompose well, making it easier for us to determine the prey [75]. This was confirmed by the finding of whole juvenile Gobius sp. (Figure 4B), whole tanaids of species Tanais dulongii (Figure 3D), whole sphaeromatids (Figure 3C), anthurids and some whole Pisidia sp. in the feces. We did not find any soft or hard prey in the stomachs examined that was not also found in the feces. Soft prey was also not found in the diet of S. scriba by the authors of other studies, regardless of the method used [10,14,17]. Thus, the non-destructive method does not lead to worse results. Even with the traditional method of stomach content analysis, there is always a possibility of overestimating the proportions of prey that decompose more slowly [35,76,77].
Some differences in the results of previous studies are due to the fact that they did not always use standardized methodology to study feeding ecology in ichthyology. To determine the importance of the prey, it is best to use a numerical index as well as frequency of occurrence and categorize the prey as regards to these two criteria (see Table 2). These parameters applied for food spectra analysis are set accordingly and are used to quantitatively describe and graphically represent diet [35,78,79,80].

4.2. Feeding Habits and Trophic Levels of S. scriba in the Northern Adriatic and in Other Mediterranean Areas

Our results indicate that S. scriba in the northern Adriatic Sea feeds on both slow-moving and fast-moving prey [13]. The calculated average trophic diversity index value (ITD) indicates a highly diverse diet. The calculated trophic levels demonstrated that in general, adults feed on higher trophic level than juveniles. This change in diet during development is referred to as an ontogenetic shift and has been confirmed for another Serranus species [81]. According to literature data [50], around 50% of individuals are sexually mature at 173 mm, which indicates that the majority of individuals used in the study were juveniles. Given the observed trend towards an increasing proportion of fish in the diet with body size, it is reasonable to assume that this proportion and therefore trophic level is even higher for older and larger S. scriba. The value of trophic level for 4-year-old S. scriba and older is, however, most likely biased due to the very small sample of these individuals and is not representative.
According to the analyses of otoliths found in the fecal pellets of S. scriba (see Figure 4), G. fallax was highlighted as the most common fish prey (Table 6), a finding that is attributed to its high abundance in the area [31] and its suitable shape and size for consumption by S. scriba. The suitable size of the prey is determined by limits of visual detection and size of the jaw apparatus [82,83,84,85]. Consuming one large prey means better energy efficiency than feeding on numerous small prey, but it is more time consuming, as prey handling time is longer [81]. Even though fish prey is not as important as regards to %PN and %PF, their mass and volume are larger than other prey and they are therefore a very important part of the diet. Piscivores generally reorient their prey head-first and lying on their side before swallowing it [84,86]. Therefore, the greatest width of the prey fish when swallowed is body depth (i.e., maximum distance between the dorsal and ventral portions of the fish). Prey with lower body depth is preferred, as it is easier to catch and consume [86]. Larger individuals of S. scriba are able to prey on fish species with greater body depth (S. ocellatus) (Figure 4), while smaller individuals prefer fish with shallow body-depth (Gobius sp.), as they are easier to capture and consume. Price et al. [87] have shown that handling time increases with prey body depth. Longer handling time increases the risk of losing the prey and being exposed to predators [88]; therefore, greater body depth is an anti-predatory adaptation [86].
Predators most often prey on fish that are well below the maximum ingestible size [82]. In wrasses, we noticed another anti-predatory behavior; in the presence of S. scriba, lateral positioning and display of the dorsal and ventral fin have been observed both in the wild and in captivity (pers. observation). Such a display makes the prey fish appear larger and is often sufficient to deter the predator from swallowing it [87,89]. Wrasses have a greater body depth than gobies at the same body length; therefore, wrasses are consumed by larger individuals of S. scriba, as observed in our study. Interestingly, smaller wrasses such as Symphodus ocellatus were observed to be removing parasites from S. scriba, although the latter is its potential predator (our study). Such behavior, i.e., approaching potentially dangerous clients, has been studied on cleaning gobies [90,91,92].
Our observations regarding specimens of S. scriba often predating from behind rocks, or lurking under boulders, are in accordance with previous studies [93,94]. The observed hunting behavior is known as the “sit and wait” predation mode and “burst chase” prey pursuit mode [19,94]. Vandewalle et al. [94] described that the majority of individuals occupy waiting spot above or within the algal cover or an overhang within heterogeneous rocky reefs, but they have also been observed hiding in algal thalli or Posidonia oceanica meadows, bordering sandy substrate.
S. scriba were observed searching for smaller crustaceans in cavities, holes and crevices under stones. Therefore, it was not surprising that crabs of the genus Pisidia were the most common prey items among the preyed crustaceans (see Figure 3), occurring in more than 50% of the examined samples (%PF = 56.67%, %PN = 18.80%). A crab, Pilumnus hirtellus, occurred in more than one tenth of the samples (% PF = 12.67%, %PN = 3.16%), while other crustaceans in the fecal pellets were mostly too decomposed to be identified to a species level. Isopods were a secondary common prey, mostly species of the family Sphaeromatidae, which are common inhabitants of rocky bottom communities [95]. Among complementary prey, well-preserved, almost whole specimens of Tanais dulongii (Tanaidacae), a widely distributed amphipod species along the entire Slovenian coast [96], were found.
Analyses of the diet of S.scriba have been conducted in different parts of the Mediterranean Sea and Canary Islands (Table 8 and Table 9). In general, all the results confirm that crustaceans, especially decapods, are the main food source for S. scriba, while fish mainly represent secondary food. The highest proportion of fish in the diet was observed in a study from the Canary Islands (%PN = 22.64%), while this proportion was the lowest in our study (%PN = 6.82%). In terms of frequency of occurrence, fish were present in 38.32% of the stomachs of S. scriba from the Canary Islands, 30.1% of those from the Tyrrhenian Sea and 20.67% of the fecal pellets of S. scriba from the northern Adriatic (see Table 8). The proportion of polychaetes in the diet of S. scriba was significantly higher in the northern Adriatic compared to other areas (%PN = 12.65%, %PF = 40.67%). In the Tyrrhenian Sea and in the Atlantic, authors observed a significantly higher proportion of caridean shrimps than observed in our study.
The trophic levels for S. scriba in different parts of the Mediterranean Sea were calculated (see Table 9) and ranged from 3.43 ± 0.52 in the northern Adriatic (our study) to 3.94 +/± −0.63 in the Aegean Sea [29]. The TROPH values for the same species may vary between sampling sites, seasons and years [97], and such changes in feeding habits may be influenced by changes in habitats [97] and prey availability [98]. The TROPH value also varies between different sizes and phases of the predator’s biological cycle [99] as well as sampling time [48,99]. These parameters should be taken into account when interpreting and comparing results for the same geographic area. Indeed, if we compare two results from the Aegean Sea [14,100], we may assume that the differences in TROPH values are probably due to differences in fish body lengths (see Table 9), which may explain the difference in the values for the same region. Moreover, the trophic level for S. scriba calculated in our study (TROPH = 3.43 ± 0.53) is most similar to that of Labrus merula (TROPH = 3.47 ± 0.55), Symphodus ocellatus (TROPH = 3.4 ± 0.51), Mullus surmuletus (TROPH = 3.44 ± 0.53), Diplodus annularis (TROPH = 3.4 ± 0.46), Diplodus sargus (TROPH = 3.38 ± 0.51) and Diplodus vulgaris (3.5 ± 0.46), as calculated by Stergiou and Karpouzi [29]. All these species feed on decapod crustaceans, polychaetes, bivalves and echinoderms [29], which means that S. scriba may compete with them for available food resources. Furthermore, according to Stergiou and Karpouzi [29], the trophic level of S. scriba adults (3.7 ± 0.58) is higher than the trophic levels of other members of the coastal fish community (i.e., Sparidae, Labridae, Bleniidae and Gobiidae), that are abundant in the northern Adriatic Sea [1]. Therefore, S. scriba can be considered as a top predator of the community. As one of the most abundant piscivorous species on the rocky bottom in the coastal zone of Slovenian waters, it could play an important role as a predator of the goby family, especially of Gobius cruentatus and Gobius fallax, which are among the most numerous fish species in the area [101]. S. scriba feeds also on juvenile Chromis chromis,, a key fish species with an important role in transferring carbon, nitrogen and phosphorus from pelagic systems to the littoral zone [102,103].

4.3. Implications for Conservation

Fish are a crucial bioindicator of the ecological integrity of aquatic systems at different levels, from microhabitat to catchment; thus, they represent an important monitoring tool [104]. Species that are suitable bioindicators have high specificity and fidelity, i.e., they are found only in a particular type of environment and are widespread and abundant in that environment [105]. Because S. scriba is site-faithful [74], widespread throughout the Mediterranean [73], easy to collect and identify [104], and feeds opportunistically, it is suitable as a bioindicator species.
Data on feeding habits are essential for species and habitat conservation [103,106]. S. scriba is known as one of the nine most aggressive predators in the Adriatic fish communities, as defined by approaching, attacking and lure ingestion [93]. Aggressive predators play a very important role in the environment, as their behavior is the primary organizing force shaping the assembly of fish communities and driving preference and occupancy of heterogeneous and homogenous benthic habitats [104]. The most aggressive predators in Adriatic fish communities were found to be nine taxa of families Serranidae (3), Gobidae (3), Sparidae (2) and Labridae (1) [93].
The Adriatic Sea is a heavily exploited part of the Mediterranean basin, where the number of large apex predators, such as sharks and rays, have declined dramatically over the past two centuries [107] and mesopredators (mid-range predators in the middle of a trophic level [3] that typically prey on smaller animals), have taken over their role [108]. The loss of an aggressive mesopredator, such as S. scriba, may result in a drastic change in the fish community, including an increase in prey populations, and may have a major impact on the ecosystem as a whole [109]. S. scriba is an abundant opportunistic predator in the coastal fish community and is helping to maintain stability of the ecosystem [110,111] due to its generalist foraging strategy. Although nowadays the species does not require special protection, efforts should be made to maintain the overall variety and diversity of marine habitat types in the northern Adriatic Sea. Anthropogenic impacts on marine ecosystems should be monitored regularly and appropriate conservation actions taken before populations declines are recorded. For monitoring fish assemblages, it is recommended to use non-destructive methods such as a visual census whenever possible.

5. Conclusions

S. scriba is an important opportunistic mesopredator of the northern Adriatic rocky bottom fish communities. It preys on a wide range of different prey such as small epibenthic invertebrates and small coastal fishes (e.g., gobies, wrasses and Atherina spp.). While younger S. scriba tend to feed on small invertebrates such as polychaetes, mysids, and shrimp, they later undergo an ontogenetic shift and feed on a higher trophic level (with fish and decapod crustaceans). This paper supports previous research on the feeding habits of S. scriba and confirms the usefulness of the new non-lethal method [63] for studying the diet of small- to medium-sized coastal fish.

Author Contributions

Conceptualization, A.L., L.L. and D.T.; methodology, A.L., L.L. and D.T.; investigation, A.L., L.L., D.T. and M.O.-B.; writing—original draft preparation, A.L., D.T. and M.O.-B.; writing—review and editing, A.L., L.L., D.T. and M.O.-B.; project administration and funding acquisition, A.L., L.L., D.T. and M.O.-B. All authors have read and agreed to the published version of the manuscript.

Funding

The authors acknowledge the financial support from the Slovenian Research Agency (ARRS), research core funding No. P1-0237.

Institutional Review Board Statement

Our research was conducted at the Marine Biology Station Piran of the National Institute of Biology of Slovenia, where researchers have the government authorization for fish culture and experimentation. Moreover, Serranus scriba is not on the list of protected species in Slovenia and therefore no special permits are required for catching and studying the species. We confirm that ethical cost of the research is balanced by the scientific value of the research. Knowledge about food and feeding habits of S. scriba is important for understanding local ecosystem dynamics, it helps us identify changes in the environment at an early change and contributes to the general advancement of knowledge. The authors assure that the present research complies with the commonly accepted ‘3Rs’: replacement of animals by alternatives wherever possible, reduction in number of animals used, and refinement of experimental conditions and procedures to minimize the harm to animals.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available, since they originate from the research program funded by the Slovenian Research Agency (ARRS).

Acknowledgments

The authors would like to thank Milijan Šiško, Tihomir Makovec, Leon Lojze Zamuda, Luka Preložnik, Jure Zaman, Urška Bizjak, Gaja Jenko, Mojca Pungerčar, Doroteja Erhatič and Romina Bonaca for their assistance during the fieldwork and laboratory work. Special thanks to Valentina Pitacco and Milijan Šiško for their help in the statistical analyses.

Conflicts of Interest

The authors declare no conflict of interest.

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Fishes 07 00210 g001 550
Figure 1. Map of the study area with 8 sampling sites for Serranus scriba (for the names of the sites see Table 1).
Figure 1. Map of the study area with 8 sampling sites for Serranus scriba (for the names of the sites see Table 1).
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Fishes 07 00210 g002 550
Figure 2. Comparison of prey proportions (%PN) in S. scriba diet.
Figure 2. Comparison of prey proportions (%PN) in S. scriba diet.
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Fishes 07 00210 g003 550
Figure 3. Prey items isolated from feces of S. scriba: (A) unidentified eggs, (B) carapace and claws of Pisidia sp., (C) isopod from family Sphaeromatidae and (D) Tanais dulongii.
Figure 3. Prey items isolated from feces of S. scriba: (A) unidentified eggs, (B) carapace and claws of Pisidia sp., (C) isopod from family Sphaeromatidae and (D) Tanais dulongii.
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Fishes 07 00210 g004 550
Figure 4. Otoliths and undigested Gobius sp. found in fecal pellets of S. scriba: (A) otolith of Gobius cruentatus, (B) Gobius sp., (C) otolith of Atherina hepsetus and (D) Gobius fallax.
Figure 4. Otoliths and undigested Gobius sp. found in fecal pellets of S. scriba: (A) otolith of Gobius cruentatus, (B) Gobius sp., (C) otolith of Atherina hepsetus and (D) Gobius fallax.
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Table
Table 1. Coordinates of the sampling sites for S. scriba in Slovenian coastal waters, sampling dates and number of fish collected.
Table 1. Coordinates of the sampling sites for S. scriba in Slovenian coastal waters, sampling dates and number of fish collected.
Sampling SiteSite NameLatitude (N)Longitude (E)Sampling DatesTotal n of Fish
1Žusterna45.54702713.70884127 May 2021, 11 June 20214
2Belveder45.53279613.64069224 June 202113
3Cape
Ronek		45.54017413.61556925 May 202111
4Pacug45.52577113.58992628 May 202118
5Fiesa45.52598913.5834075 June 202128
6Cape
Piran		45.52940113.57153720 May 20215
7Marine Biology Station Piran45.51783013.56832522 September 2020, 30 September 2020, 1 October 2020, 11 May 2021, 20 May 2021, 26 May 2021,
27 May 2021		44
8Bernardin45.51548613.56973531 May 2021, 1 June 2021, 2 June 2021, 3 June 202127
Table
Table 2. Prey categories according to Hureau [57] (%PF = frequency of occurrence, %PN = numerical index).
Table 2. Prey categories according to Hureau [57] (%PF = frequency of occurrence, %PN = numerical index).
%PN%PFPrey Category
>50>30Main preferential prey
<30Main occasional prey
10 < %PN < 50>10Secondary frequent prey
<10Secondary frequent prey
1 < %PN < 10>10Complementary prey of 1st order
<10Complementary prey of 2nd order
<1 Accidental prey
Table
Table 3. Painted comber densities at sampling locations in Slovenian waters.
Table 3. Painted comber densities at sampling locations in Slovenian waters.
Sampling LocationDateLength (m)Depth (m)Average Density
(ind./100 m2)
Cape Piran20 May 2021501.57
3.0–3.58
Cape Ronek25 May 2021501.511.5
3.810
Pacug23 June 2021501.57
3.56.5
Table
Table 4. Average minimal and maximal sizes (TL = total length, FL = fork length, SL = standard length) and weight of 150 specimens of S. scriba.
Table 4. Average minimal and maximal sizes (TL = total length, FL = fork length, SL = standard length) and weight of 150 specimens of S. scriba.
TLFLSL
Average size (mm)140.38
(SD = ±19.12)		137.31
(SD = ±18.28)		117.23
(SD = ±16.50)
Max. size (mm)216.98213.62180.02
Min. size (mm)108.30107.4068.88
Average weight (g)42.68
(SD = ±21.74)
Min. weight (g)17.00
Max. weight (g)163.80
Table
Table 5. Total length (TL) and groups of 150 specimens of S. scriba.
Table 5. Total length (TL) and groups of 150 specimens of S. scriba.
AgeTL (mm)N%
1+108–1305033.3
2+130–1526040.0
3+152–1702919.3
4+170–200117.3
Table
Table 6. Numerical index (%PN) and frequency of occurrence (%PF) of particular prey taxa of S. scriba in the northern Adriatic Sea.
Table 6. Numerical index (%PN) and frequency of occurrence (%PF) of particular prey taxa of S. scriba in the northern Adriatic Sea.
Taxa%PF (n= 150)%PNPrey Category (Hureau 1970)
CRUSTACEA (total)98.6769.21Main preference prey
AMPHIPODA (total)2.670.83Accidental prey
Caprellidae2.670.83
CIRRIPEDIA2.000.50Accidental prey
Crustacea indeterminata1.330.33
DECAPODA (total)96.6746.75Secondary frequent prey
ANOMURA (total)79.3325.45Secondary frequent prey
Anomura indeterminata5.331.66
Pisidia sp.56.6718.80
Porcellana platycheles6.001.66
BRACHYURA (total)30.677.65Complementary prey of 1st order
Brachyura indeterminata16.674.16
Pilumnus hirtellus12.673.16
Majidae1.330.33
CARIDEA (total)11.333.33Complementary prey of 1st order
Athanas nitescens2.670.67
Caridea indeterminata8.672.66
Decapoda indeterminata38.0010.32
ISOPODA (total)37.3313.64Secondary frequent prey
Anthuridae2.670.83
Idoteidae0.670.17
Isopoda indeterminata18.675.32
Sphaeromatidae20.677.32
MYSIDA15.333.99Complementary prey of 1st order
OSTRACODA2.670.67Accidental prey
TANAIDACEA
(Tanais dulongii)		8.672.50Complementary prey of 2nd order
POLYCHAETA (total)40.6712.63Secondary frequent prey
Polychaeta-Errantia39.3311.81
Polynoidae0.670.17
Spirorbis sp.2.670.65
MOLLUSCA5.33 Accidental prey
BIVALVIA2.670.67Accidental prey
GASTROPODA17.334.66Complementary prey of 1st order
TELEOSTEI20.676.82Complementary prey of 1st order
Atherina hepsetus5.331.50
Gobius cruentatus2.671.00
Gobius fallax3.331.33
Mullus surmuletus0.670.17
Osteichtyes indeterminata8.002.00
Pomatoschistus bathii2.000.50
Symphodus cinereus0.670.17
Symphodus ocellatus0.670.17
Eggs11.335.99Complementary prey of 1st order
Table
Table 7. Trophic level (TROPH) of different age groups of S. scriba.
Table 7. Trophic level (TROPH) of different age groups of S. scriba.
AgeTROPHSD
1+3.42±0.53
2+3.46±0.56
3+3.48±0.57
4+3.36±0.56
Table
Table 8. Diet of Serranus scriba in various parts of the Mediterranean and Canary Islands (%PN = numerical index, %PF = frequency of occurrence).
Table 8. Diet of Serranus scriba in various parts of the Mediterranean and Canary Islands (%PN = numerical index, %PF = frequency of occurrence).
Our ResearchMoreno-Lopes et al., 2002Arculeo et al., 1993
Northern Adriatic,
Gulf of Trieste		Lanzarote, Atlantic OceanThyrrenian sea, Gulf of Palermo
N=150351244
%PN %PF%PN%PF%PN%PF
CRUSTACEA (total)69.2198.6775.0895.5260.9
AMPHIPODA0.832.670.981.870.70.02
CIRRIPEDIA0.502.00
Crustacea indeterminata0.331.33
DECAPODA (total)46.7596.676082.24
ANOMURA25.4579.3313.4423.36
Galatheidae 18.624.1
Paguridae 0.02<0.1
Porcellanidae 3.42.2
BRACHYURA (total)7.6530.6721.6446.730.412.9
CARIDEA (total)3.3311.3324.9237.3849.827.7
ISOPODA13.64 0.330.933.1
MYSIDA3.9915.33 1.50.1
OSTRACODA0.672.67
STOMATOPODA 0.330.93
TANAIDACEA2.508.672.508.67
MOLLUSCA5.33 1.975.610.9
BIVALVIA0.672.67
CEPHALOPODA 0.982.800.21.5
GASTROPODA4.6617.330.982.800.7<0.01
POLYCHAETA (total)12.6340.670.330.930.80.7
TELEOSTEI6.8220.6722.6438.3210.230.1
Teleostei indeterminata2.008.0011.1520.56
Atherinidae
Atherina sp.1.505.332.36.65
Blennidae
Blennidae indeterminata 0.330.93
Parablennius pilicornis 1.312.80
Scartella cristata 0.330.93
Gobiesocidae
Lepadogaster sp. 0.660.93
Gobiidae
Gobius cruentatus1.002.67
Gobius fallax1.333.33
Gobius niger 0.661.87
Pomatoschistius bathi0.502.00
Labriidae
Centrolabrus trutta 0.330.93
Labridae indeterminata 2.625.61
Symphodus cinereus0.170.67
Symphodus ocellatus0.170.67
Mullidae
Mullus surmuletus0.170.67
Serranidae
Serranus sp. 0.330.93
Scorpaenidae
Scorpaena maderensis 0.661.87
Sygnathidae
Sygnathus sp. 0.661.87
Synodontidae
Synodus synodus 0.330.93
Trypterygiidae
Tripterygion delaisi 0.661.87
Eggs5.9911.33
Table
Table 9. Trophic levels of Serranus scriba in the Mediterranean Sea.
Table 9. Trophic levels of Serranus scriba in the Mediterranean Sea.
Authors and Year of PublicationSampling LocationTROPHTL (mm)
Our study, 2021Northern Adriatic, Gulf of Trieste3.43 ± 0.52108–217
Karachle and Stergiou, 2017Northwest Aegean Sea3.94 ± 0.63106–236
Stergiou and Karpouzi, 2002(Review–average from various locations in Mediterranean)3.7950–230
Khoury, 1984Tyrrhenian Sea, Gulf of Napoli3.8
Arculeo et al., 1993Tyrrhenian Sea, Gulf of Palermo3.87100–230
Vasilki, 2016South-West Lesvos, Aegan Sea, 3.8173+
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Lokovšek, A.; Orlando-Bonaca, M.; Trkov, D.; Lipej, L. An Insight into the Feeding Ecology of Serranus scriba, a Shallow Water Mesopredator in the Northern Adriatic Sea, with a Non-Destructive Method. Fishes 2022, 7, 210. https://doi.org/10.3390/fishes7040210

AMA Style

Lokovšek A, Orlando-Bonaca M, Trkov D, Lipej L. An Insight into the Feeding Ecology of Serranus scriba, a Shallow Water Mesopredator in the Northern Adriatic Sea, with a Non-Destructive Method. Fishes. 2022; 7(4):210. https://doi.org/10.3390/fishes7040210

Chicago/Turabian Style

Lokovšek, Ana, Martina Orlando-Bonaca, Domen Trkov, and Lovrenc Lipej. 2022. "An Insight into the Feeding Ecology of Serranus scriba, a Shallow Water Mesopredator in the Northern Adriatic Sea, with a Non-Destructive Method" Fishes 7, no. 4: 210. https://doi.org/10.3390/fishes7040210

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