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Article

Proximate Composition, Predictive Analysis and Allometric Relationships, of the Edible Water Frog (Pelophylax epeiroticus) in Lake Pamvotida (Northwest Greece)

by
Marianthi Hatziioannou
,
Efkarpia Kougiagka
,
Ioannis Karapanagiotidis
and
Dimitris Klaoudatos
*
Department of Ichthyology and Aquatic Environment, School of Agricultural Sciences, University of Thessaly, Fytokou Street, 384 45 Volos, Greece
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(6), 3150; https://doi.org/10.3390/su14063150
Submission received: 12 February 2022 / Revised: 4 March 2022 / Accepted: 6 March 2022 / Published: 8 March 2022
(This article belongs to the Topic Aquatic Living Resources, Conservation and Oceanography in an Era of Change: Insights from the 4th International Congress on Applied Ichthyology, Oceanography & Aquatic Environment)
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Abstract

:
The edible water frog Pelophylax epeiroticus, distributed mainly in Northwest Greece and utilized commercially as food, was investigated in lake Pamvotida (Ioannina). The objective was to assess aspects of population structure (sex ratio, morphometric characteristics, allometric relationships) and proximate composition of the Epirus water frog (Pelophylax epeiroticus). Commercial samples (31 females and 54 males) were obtained and sex ratio, morphometric characteristics, allometric relationships and proximate composition were assessed. A significantly lower abundance of females was indicated (31 females and 54 males). Body length range was higher in females (females 3.4 mm, males 2.6 mm), whereas total weight range was higher in males (females 45.08 gr, males 48.35 gr). Differences in allometric relationships were indicated between sexes. The high protein (15.93 ± 3.32) and low lipid (0.25 ± 0.13) contents indicated that P. epeiroticus is an excellent food source of high nutritional value. A tree classification algorithm indicated that the principal contributing component for sex classification was dry matter, followed by a proportion of edible flesh and protein content. A predicted future increase in demand for wild-caught individuals requires the use of a suitable management plan, coupled with the development of farming practices aiming to assure the sustainable exploitation of this important resource and alleviate the pressure on its populations.

1. Introduction

Pelophylax epeiroticus is an edible water frog species native to the Ionian zone [1], distributed mainly in the western part of Greece along the Ionian coast, including the island of Kerkyra [2]. The species is also present in Albania; however, the main part of its range is within Greece [3]. The western Palaearctic water frog of the genus Pelophylax includes several distinct species and has been investigated in several phylogenetic, morphological, and ecological studies [4,5,6,7,8,9,10]. The populations of P. epeiroticus (Epirus Water Frog) are suspected to be decreasing due to ongoing decline in the extent and quality of its habitat, thus improved management measures are required for the protected areas and Natura 2000 sites where the species appears [3]. Subpopulations are fragmented due to extensive areas of unsuitable habitat within its range. The species occurs in many protected areas within its range and is listed in Appendix III of the Berne Convention. The main threats for the species are general loss of wetland habitat, water pollution, climate change, dam construction and hydro-power developments [3]. P. epeiroticus is utilized commercially as food; however, consumption is not currently considered a major issue for its sustainability since it is consumed in low numbers. Furthermore, there is no evidence that the species is collected excessively in Albania, despite the 2008 assessment that reported an established fishery harvesting measurable quantities [3], and Greece [11].
The amphibian fauna of Greece includes 22 species out of a total of 64 European species, a significant number given the small size of Greece [2]. Perhaps the most important threat that amphibians face in Greece is the degradation and loss-destruction of their habitats and breeding sites, which occurs either because of natural change (increase in temperature, decrease in precipitation, drought) or as a result of anthropogenic activities (inland water agricultural and industrial pollution, livestock activities, development of residential and tourist infrastructure, water overdraft, recreational activities) [2,3,12]. Aquatic frogs are an important part of biota in the natural wetlands, playing an essential role in the food chain, functioning both as predators (adults feed mainly on invertebrates: insects and arthropods) and prey (they can serve as food for both aquatic and terrestrial predators). Adult anurans have highly permeable skin [13], making them sensitive to various environmental stressors (including toxins of anthropogenic origin). The latest research has indicated that human industrial activity (e.g., mining, agriculture) is amongst the main reasons for the decline of amphibian anuran populations [13,14,15,16,17,18,19,20].
Large-bodied frogs are under additional pressure by the national and international demand for their meat [21,22,23,24]. In some cultures—notably Asian, Greek and Roman—frog meat has been considered a delicacy for centuries [25]. Consumption and trade of frogs are of great interest in Europe and the USA, with the largest importers of frog legs being France, USA, Belgium and Luxembourg, whereas the largest exporters are Indonesia, China, Belgium and Luxembourg [26,27,28,29]. European frog populations, particularly of the European green frog complex (Pelophylax spp.) were heavily exploited, especially in France (with 40–70 tonnes of frogs captured per year), followed by Belgium and the Netherlands [30].
The present study is the first that describes the proximate composition of wild-caught P. epeiroticus. Frog leg meat is considered a traditional delicacy in Western Greece and of great gastronomic interest worldwide, offering an excellent source of protein [31,32]. Frog meat has the potential to attract the attention of food technologists and dieticians as a new healthy food source based on its excellent nutritional composition. European countries tend to prefer species of the genus Pelophylax that are small in weight (i.e., 50–60 g) [33]. Proximate frog leg composition of wild and cultured species (P. ridibundus, P. esculentus, Lithobates catesbeianus and Holobatrachus rugulosus) is characterized by low lipid content [34,35,36,37]. According to [22], in 2018 the global production of frogs was 107.3 thousand tonnes. Frog farming is not sufficiently developed in Greece [38], resulting in the increased fishing pressure on wild populations, threatening their sustainability.
The aim of this study was to contribute to the literature of the Epirus water frog Pelophylax epeiroticus in Lake Pamvotida (Ioannina) on aspects of population structure through assessing sex ratio, morphometric characteristics and allometric relationships. Furthermore, we aimed to highlight its nutritional value by comparing its proximate composition with other popular freshwater commercial species. Predictive analysis on proximate composition was further used to identify principal contributing components that could classify the opposite sexes of the species.

2. Materials and Methods

In total, 85 water frogs P. epeiroticus were sampled in 2016 from lake Pamvotida (Figure 1) monthly between March and May (24, 30, 31 individuals in March, April, and May accordingly). Adult water frogs were captured by net or hand and were directly transported to the Laboratory of Aquaculture (using plastic 50 lt containers containing a small volume of freshwater and plant material from the lake) in the Department of Ichthyology and Aquatic Environment, School of Agricultural Sciences, University of Thessaly, where they were kept for one day in freshwater aquariums (40 × 20 × 20 cm).

2.1. Study Area

Pamvotida is the largest lake of Epirus, located in the northwestern part of Greece in the Ioannina regional unit, with mount Mitsikeli located at its northwestern edge. Lake Ioannina (also known as lake Pamvotida) is a shallow lake with an average depth of 4.5 m and a polymictic stratification regime, situated at 470 m elevation, occupying an area of 22 km2 [39]. The local climate consists of cold wet winters with daily averages <0 °C and hot dry summers with temperatures in excess of 30 °C. The location of Ioannina within the Pindus mountains and the proximity of the Ionian Sea result in high levels of precipitation, with annual means of 1100–1200 mm recorded in the proximity of the lake. Annual mean evaporation and precipitation are approximately equal [40].
The lake was formed by water concentration and is fed by the mountain Mitsikeli springs, with no physical surface outlet. The outflow of the water is carried through the Lapsista’s ditch and is diverted to the Kalamas river. It is a sensitive ecosystem, which belongs to the European Network of Protected Areas, NATURA 2000 because of the important habitats and the rare species of flora and fauna [41]. Lakes in the Mediterranean climate zone experience high variation in rainfall and are vulnerable to changes in climate, land cover and anthropogenically induced effects on water level and salinity [42].
A major city (Ioannina, pop. 100,000) lies along its western shoreline. A decrease in the external load of nutrients and pollutants occurred in 1990 with the removal of the Ioannina sewage outfall from the lake along with industrial discharges on the southern shoreline. The lake has undergone cultural eutrophication over the past 40 years and is currently eutrophic. Fish stocking has occurred annually in the lake since 1986 to promote commercial fishery [40]. Sampling was conducted in the proximity of the village Amphithea (latitude 39.6832448, longitude 20.8697307) in the north part of the lake next to the shore.

2.2. Morphometry

Morphometric characteristics were recorded for all 85 individuals caught (31 females and 54 males): total body weight (TW) with a digital scale (accurate to 0.1 g) and body length (BL), femur length (FL), tibia length (TL), maximum head length (MHL) from the tip of the snout to the posterior margin of the tympanum, maximum head width (MHW) the largest pre-tympanum head width [43] and snout eye distance (SED) from the tip of the head to the posterior corner of the eye, with a digital caliper (accurate to 0.01 mm) (Figure 2).

2.3. Proximate Composition

A total of 27 individuals (31 females and 54 males) were analyzed for the estimation of edible parts and proximate composition. All animals were euthanized by dipping in 0.5% MS-222 solution. The removal of the skin and clipping of the feet were carried out immediately after. The hind legs from each frog were removed by full extension and severed from the body by an incision close to the waist. The total weight of hinds was assessed immediately after anatomy. Using body weight (BW) and net weight of frog leg hinds (LW), the edible part (EP) (%) was assessed according to the equation:
EP = (LW/BW) × 100
Moisture, protein (as total nitrogen content) and lipid (as total lipid content) and ash content of frog leg meat were determined in line with the procedures of the Association of Official Analytical Chemists in triplicate [44]. Samples were placed for 24 h at 105 °C to determine moisture content. Crude protein and crude fat were assessed by Kjeldahl (N × 6.25; Behr Labor-Technik, Dusseldorf, Germany) and exhaustive Soxhlet extraction with petroleum ether (40–60 °C) using a Soxtherm Multistat/SX PC (Sox-416 Macro, Gerhardt, Germany) respectively, whereas a water-free sample was combusted in a muffle furnace (Nabertherm L9/12/C6, Lilienthal, Germany) by heating at 600 °C for 3 h and the ash content was measured gravimetrically [44]. The proximate composition was expressed as a percentage of dry matter and as a percentage of wet weight.

2.4. Statistical Analysis

Data for statistical analysis were evaluated for normal distribution by employing the Shapiro–Wilk test for normality and homogeneity of variance by employing Levene’s test. Student’s t-test was employed for comparisons of body length and total weight among sexes since data were approximately normally distributed and homogenous. Welch’s analysis of variance (ANOVA) was employed for monthly comparisons when data were normally distributed but violated the assumption of homogeneity of variance [45]. Mood’s median test was used for comparisons where data failed both assumptions of normality and homogeneity [46]. Chi-Square goodness-of-fit and Chi-Square test for association were employed for the comparison of categorical values. Statistical analysis was performed with Jamovi Software (2.2.5) [47]. Nonlinear regression was performed with Minitab software (Minitab, PA, USA) between body length, total weight, femur length, tibia length, maximum head length, maximum head width and snout eye distance. Proximate composition of P. epeiroticus was compared with frog and fish proximate composition values from the literature, using one sample t-test. A tree algorithm with forward pruning was used to compute the contribution of proximate composition to the phyletic identification. Before classification, data preprocessing techniques were applied to improve the efficiency of the algorithm and correctly classify the data [48]. A prediction was inferred by measuring the increase in the prediction error of the model after permuting the feature’s values, using Orange software (3.30.2) [49].

3. Results

3.1. Sex Ratio

The Chi-Square goodness-of-fit test (Table 1) indicated a significant difference between observed (31) and expected (42.5) male and female (observed 54 and expected 42.5) abundance, with a significantly lower abundance of females and higher in males than expected.
The Chi-Square test for association indicated no significant difference in the sex ratio between different sampling periods (p > 0.05).

3.2. Population Structure

No significant difference was indicated in body length and total weight between sexes (t-test, p > 0.05). No significant difference was indicated in body length between sampling periods (Mood’s Median test, p > 0.05); however, a significant difference was indicated in total weight between sampling periods with a significantly higher total weight for individuals sampled in April (Mood’s Median test, p < 0.05).
Range of body length among sexes (Figure 3) was higher for females (3.4 mm) compared to males (2.6 mm), whereas the opposite trend was indicated for total weight where females exhibited lower range (45.08 gr) compared to males (48.35 gr).
Monthly distribution of body length and total weight indicated a greater range in body length during all sampling periods for females, and similarly, the range of total weight was greater in females during most sampling periods except March, where the opposite trend was indicated (Figure 4).

3.3. Allometry

A significant allometric relationship was indicated between body length, femur length, tibia length and snout eye distance. A significant difference in the allometric relationships among sexes was indicated between body length and femur length and between body length and snout eye distance (Table 2). No significant allometric relationship was indicated between total weight and body length as well as between maximum head length and maximum head width.

3.4. Proximate Composition

The proximate composition of frog and freshwater fish species (cultured and wild) and their comparison with estimated values for P. epeiroticus in lake Pamvotida is illustrated in Table 3 and Table 4.
Moisture, crude protein, crude fat and ash content of P. epeiroticus were found to be 81.5 ± 3.63, 15.93 ± 3.32, 0.25 ± 0.13 and 1.10 ± 0.30, respectively. Cultured frog species recorded a protein content ranging from 15.24 to 22.95% (Table 3). Proximate composition exhibited a high degree of similarity to wild-caught P. ridibundus from Turkey and Lithobates catesbeianus from Mexico.
Compared to freshwater fish, protein content of the Epirus water frog (15.93 ± 3.32) was similar to Salvelinus fontinalis (16.31 ± 0.09), Oreochromis niloticus (16.4 ± 0.6) and Cyprinus caprio (16.7 ± 0.8). Moisture content (81.50 ± 3.63) exhibited high similarity to Oreochromis niloticus (81.20 ± 1.0) and Liza abu (80.20). However, fat content (0.25 ± 0.13) was significantly lower compared to all freshwater fish species.

Predictive Analysis

Predictive analysis was applied to identify patterns and generate predictions for sex identification based on proximate composition. Through visual programming, five supervised machine learning algorithms were utilized (CN2 induction, random forest, logistic regression, neural network and decision tree algorithms) and the one that applied best to our dataset was identified (decision tree algorithm) by scoring the performance of each model. The workflow applied for the identification of the appropriate model classifier identification is shown in Figure 5.
The tree classification algorithm used to compute the contribution of proximate composition to the phyletic identification of P. epeiroticus identified that the principal contributing component was the proportion of dry matter (Figure 6 and Figure 7) followed by the proportion of edible flesh and protein.
The output of the decision tree algorithm is shown in Figure 6.

4. Discussion

Significantly lower abundance of females than expected (Table 1) could be potentially attributed to differential mortality between sexes, previously reported in frogs, where males exhibit more conspicuous behavior than females and can be easily detected by predators [12]. According to [58], differential mortality between sexes has been previously reported in frogs, where males exhibit more conspicuous behavior than females and can be easily detected by predators.
Females exhibited higher weight (35.69 ± 13.13) compared to males (31.01 ± 10.57) and larger body length (females: 7.11 ± 0.76, males: 6.92 ± 0.57); however, this is not statistically significant (Figure 3). According to [33], female frogs weigh more than their male counterparts. Alternations of morphological traits can be explained by the biological cycle of the frog and variation of abiotic and biotic parameters. Significant morphological variation reported across Pelophylax species, and particularly between mainland P. epeiroticus, P. ridibundus and P. kurtmuelleri species, does not always allow a reliable morphological discrimination of the different species in their overlapping regions [8]. According to [59], there is a strong sexual size dimorphism in P. epeiroticus, with females growing larger than males, related to differences in the age at which maturity is reached. Furthermore, a significant difference in body length between P. epeiroticus sexes was reported [12].
A significant difference was indicated in total weight between sampling periods with a significantly higher total weight for individuals sampled in April (Figure 4) possibly attributed to hibernation of the species. It has been reported [60] that minimum fat body weight was observed in February in R. epeiroticus due to the fact that lipid was used for ovarian follicle growth through hibernation.
The divergence of shape and size, due to the development of an organism is known as allometry [61]. Allometry is common in nature and is exhibited during the developmental stage of an organism between individuals of a population at the same developmental stage and between different species [62,63]. Allometric relationships identified several morphological differences among P. epeiroticus sexes (Table 2). The relationship of total weight versus body length exhibited the opposite allometric growth, with negative allometry indicated for females and positive for males; however, this is not statistically significant. Significant differences among sexes were indicated between body length, femur length and between body length and snout eye distance (Table 2). Environmental conditions coupled with ecological interactions and habitat utilization are known to affect development [64,65]. Both size and shape affect the biological processes of an organism [66]. According to [67], anurans are known to vary little in body size compared to other vertebrates, resulting in high lability of body dimensions as a result of abiotic factors [68].
Overall, P. epeiroticus proximate composition exhibited a high degree of similarity with cultured and wild frog species Lithobates catesbeianus from Brazil and Mexico, respectively [34,47]. P. epeiroticus moisture and protein content were similar to the frog species P. ridibundus and L. catesbeianus species caught in the wild [33,50,52].
Significant differences were exhibited with wild-caught frog species Pelophylax esculentus and Lithobates catesbeianus [28,37,51] (from Turkey and Thailand respectively) and cultured Holobatrachus rugulosus [36]. Protein content was higher in females (16.89 ± 4.88) in comparison to males (15.36 ± 1.91); however, this is not statistically significant.
Notably, fat content exhibited significantly lower value compared both to cultured and wild frog species [28,33,34,50,51], possibly attributed to the timing the individuals were caught, in the onset of spring right after winter when body fat tissue had not returned to normal values after a fasting period. No significant difference was indicated for P. epeiroticus fat content between sexes, with males exhibiting higher fat content (0.28 ± 0.12) compared to females (0.11 ± 0.07). A number of studies showed that marked seasonal changes in fat body and liver occur in amphibians living in seasonal environments [69,70]. In a study by [71], on P. epeiroticus, the emergence from wintering and the subsequent breeding season (February to May) was accompanied by a sharp decrease in fat body weight.
In amphibians, climate change mainly affects habitat suitability, the spread of infectious diseases, population size, phenology of reproduction, growth, and morphology [72,73,74,75]. In temperate areas, the increase in air and water temperature during spring appears important for initiating certain behaviors, including emergence from hibernation and initiation of reproductive activities [76]. Studies on Phelophylax in the Balkans [75] and north Europe [74] highlighted the important role of temperature increase on development, growth and body size.
The considerable similarity was indicated in the protein content between P. epeiroticus and several fresh water fish species, notably Salvelinus fontinalis, Oreochromis niloticus, and Cyprinus carpio [54,55,56], whereas lipid content was significantly lower, indicating P. epeiroticus excellent nutritional value. Proximate composition of P. epeiroticus was used in predictive analysis aiming to identify the principal contributing proximate composition components that classify opposite sexes (Figure 3, Figure 4 and Figure 5). Predictive models are used to construct a model by using the results of the known data and predict the results of unknown data sets by using the constructed model [77].
The tree classification algorithm indicated that the principal contributing component for sex classification was dry matter, followed by a proportion of edible flesh and protein content. Sexual dimorphism was indicated in the limb muscles of Pelophylax nigromaculata [78]. Sexual dimorphism in size and morphology is widespread in the animal kingdom [79,80]. Three major hypotheses proposed to explain the evolution of dimorphism in secondary sexual characters include: mechanisms of sexual selection, intersexual food competition and reproductive role division [79,81]. Sexual size dimorphism is widespread among anurans [82,83], linked to intersexual differences in growth rate, time of sexual maturation, age structure and mortality schedules [84,85].
Epirus water frog is included in the list of European edible green frog complex (Pelophylax spp.) and is a sought-after food item, captured and consumed extensively in Western Greece. Frog leg meat is considered by many to be a delicacy and except for alive frogs and frozen frog legs, the food industry uses preservation techniques and cooking methods in order to prepare new food products [23,35] and increase shelf life [28]. P. epeiroticus could be marketed and further promoted as an excellent food choice with a rich nutritional profile. However, an increase in demand for frog leg meat should be combined with a suitable management plan regulating fishing pressure and fishing practices of wild captures, thus assuring a sustainable exploitation of the species. Steps should be taken to facilitate the development of farming of indigenous frog species in Greece in a further measure to alleviate the pressure on the wild populations.

5. Conclusions

This is the first study that describes the proximate composition of wild-caught P. epeiroticus distributed mainly in Northwest Greece in lake Pamvotida (Ioannina) and utilized commercially as food. Proximate composition with high protein and low lipid content demonstrated the high nutritional value of the species in comparison with other popular freshwater commercial species. Aspects of the population structure of the species indicated that the sex ratio was in favor of males. Females exhibited a higher body length range, whereas males exhibited a higher total weight range. A tree classification algorithm identified dry matter, followed by a proportion of edible flesh and protein content as the principal contributing components for sex classification. The combination of habitat degradation, coupled with a predicted increase in demand, will require the implementation of a suitable management plan to ensure the sustainability of the edible water frog populations in the western part of Greece along the Ionian coast.

Author Contributions

Conceptualization, M.H. and D.K.; data curation, M.H.; formal analysis, I.K. and D.K.; funding acquisition, M.H.; investigation, E.K.; methodology, M.H., I.K. and D.K.; software, D.K.; validation, M.H., E.K. and I.K.; visualization, D.K.; writing—original draft, M.H., E.K. and D.K.; writing—review and editing, M.H., E.K., I.K. and D.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

All experimental procedures were conducted according to the guidelines of the EU Directive 2010/63/EU regarding the protection of animals used for scientific purposes. The experiments were performed at the registered experimental facility (EL-43BIO/exp-01) of the Laboratory of Aquaculture, Department of Ichthyology and Aquatic Environment, University of Thessaly by FELASA accredited scientists (functions A–D).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the article itself.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Location and view of Lake Pamvotida (sampling location is indicated by an arrow).
Figure 1. Location and view of Lake Pamvotida (sampling location is indicated by an arrow).
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Figure 2. Morphological traits measured (MHL = maximum head length, MHW = maximum head width, BL = body length, FL = femur length, TL = tibia length, SED = snout eye distance).
Figure 2. Morphological traits measured (MHL = maximum head length, MHW = maximum head width, BL = body length, FL = femur length, TL = tibia length, SED = snout eye distance).
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Figure 3. Body length (A) and total weight (B) frequency distribution of P. epeiroticus male and female populations with overlaid fitted normal distribution.
Figure 3. Body length (A) and total weight (B) frequency distribution of P. epeiroticus male and female populations with overlaid fitted normal distribution.
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Figure 4. Monthly body length (A) and total weight (B) distribution of male and female P. epeiroticus populations. Values are means (dots), medians (lines), standard deviation (interquartile range box), minimal and maximal value (whiskers) and outliers (asterisks *).
Figure 4. Monthly body length (A) and total weight (B) distribution of male and female P. epeiroticus populations. Values are means (dots), medians (lines), standard deviation (interquartile range box), minimal and maximal value (whiskers) and outliers (asterisks *).
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Figure 5. Workflow of the most appropriate model classifier identification.
Figure 5. Workflow of the most appropriate model classifier identification.
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Figure 6. Predictive analysis classification of P. epeiroticus according to its proximate composition.
Figure 6. Predictive analysis classification of P. epeiroticus according to its proximate composition.
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Figure 7. Identification of the most important proximate composition component in the phyletic identification of P. epeiroticus according to the tree classification algorithm.
Figure 7. Identification of the most important proximate composition component in the phyletic identification of P. epeiroticus according to the tree classification algorithm.
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Table
Table 1. Chi-Square goodness-of-fit test for sex ratio.
Table 1. Chi-Square goodness-of-fit test for sex ratio.
Sex Number of IndividualsProportionχ² Goodness of Fit
FemaleObserved31.00.36χ²dfp
Expected42.50.506.221<0.05
MaleObserved54.00.64
Expected42.50.50
Table
Table 2. Allometric equations between body length (BL), total weight (TW), femur length (FL), tibia length (TL), maximum head length (MHL), maximum head width (MHW) and snout eye distance (SED) of P. epeiroticus. populations.
Table 2. Allometric equations between body length (BL), total weight (TW), femur length (FL), tibia length (TL), maximum head length (MHL), maximum head width (MHW) and snout eye distance (SED) of P. epeiroticus. populations.
Morphometric RelationshipsEquation Comparison
Sampling SiteEquationNR2t-TestAllometrySlopesIntercepts
Total populationTW = 0.0793345 × BL 3.082498584.4%nsPositive
FemalesTW = 0.147744 × BL 2.783353185.7%nsNegativensns
MalesTW = 0.0446303 × BL 3.367665485.6%nsPositive
Total populationBL = 2.62897 × FL 0.7232728593.3%***Negative
FemalesBL = 2.2427 × FL 0.8393183196.3%nsNegative******
MalesBL = 2.9084 × FL 0.6476125495.6%***Negative
Total populationBL = 2.90683 × TL 0.6964328592.8%***Negative
FemalesBL = 3.13275 × TL 0.6327223194.7%***Negativensns
MalesBL = 2.70909 × TL 0.7586385496.5%***Negative
Total populationBL = 6.14082 × SED 0.702858587.8%**Negative
FemalesBL = 5.81649 × SED 0.959483192.9%nsNegative***ns
MalesBL = 6.25962 × SED 0.5929455492.5%***Negative
Total populationMHL = 1.24333 × MHW 0.9586278594.8%nsNegative
FemalesMHL = 1.41502 × MHW 0.8290753196.8%nsNegativensns
Total populationMHL = 1.24333 × MHW 0.9586278594.8%nsNegative
N: number of individuals, R2: coefficient of determination, t-test: statistical significance of the allometric relationship, allometry: allometric relationship between the two variables, slopes (b): statistical comparison between the slopes of the equations, intercepts (a): statistical comparison between the intercepts of the equations, significance level (ns: non-significant, **: p < 0.01, ***: p < 0.001).
Table
Table 3. Proximate composition (percentage of wet weight) of wild and cultured frog species, and statistical comparison using one sample t-test, with values estimated for P. epeiroticus in lake Pamvotida. Data are mean values.
Table 3. Proximate composition (percentage of wet weight) of wild and cultured frog species, and statistical comparison using one sample t-test, with values estimated for P. epeiroticus in lake Pamvotida. Data are mean values.
OriginSpeciesMoistureAshProteinFatOriginReference
CulturedPelophylax ridibundus74.79 ± 0.25 *** 1.00 ± 0.15 ns22.95 ± 0.16 *** 0.93 ± 0.20 *** Turkey[34]
Pelophylax ridibundus79.15 ± 0.77 *** 1.03 ± 0.01 ns19.69 ± 0.17 *** 0.71 ± 0.03 **Turkey[33]
Lithobates catesbeianus84.81 ± 0.12 *** 0.94 ± 0.27 ns15.24 ± 0.67 ns0.06 ± 0.0 *Brazil[35]
Holobatrachus rugulosus79.47 ± 0.12 **0.77 ± 0.05 **21.89 ± 0.16 *** 0.8 ± 0.07 *** Thailand[36]
Pelophylax epeiroticus81.5 ± 3.631.10 ± 0.315.93 ± 3.320.25 ± 0.13GreecePresent study
WildPelophylax ridibundus79.37 ± 0.50 **1.37 ± 0.23 *18.52 ± 0.70 *** 0.74 ± 0.15 **Turkey[34]
Pelophylax ridibundus81.67 ± 0.11 ns0.82 ± 0.05 **16.58 ± 0.14 ns0.89 ± 0.07 *** Turkey[50]
Pelophylax ridibundus81.2 ± 2.12 ns1.26 ± 0.06 ns18.88 ± 0.48 *** 0.82 ± 0.03 *** Turkey[33]
Pelophylax esculentus79.72 ± 0.94 *0.56 ± 0.02 *** 19.23 ± 0.15 *** 0.68 ± 0.03 **Turkey[37]
Pelophylax esculentus79.47 ± 0.59 **1.83 ± 0.16 *** 22.21 ± 1.19 *** 1.05 ± 0.34 *** Turkey[28]
Pelophylax esculentus78.83 ± 0.48 *** 0.85 ± 0.02 **18.83 ± 0.48 *** 1.04 ± 0.00 *** Turkey[51]
Lithobates catesbeianus80.77 ± 0.74 ns0.63 ± 0.04 *** 17.01 ± 0.12 ns0.61 ± 0.07 **Mexico[52]
Lithobates catesbeianus80.02 ± 0.13 *0.58 ± 0.06 *** 19.31 ± 0.06 *** 0.71 ± 0.05 **Thailand[36]
Significance level (ns: non-significant, *: p < 0.05, **: p < 0.01, ***: p < 0.001).
Table
Table 4. Proximate composition (percentage of wet weight) of wild freshwater fish species and statistical comparison using one sample t-test, with values estimated for P. epeiroticus in lake Pamvotida. Data are mean values.
Table 4. Proximate composition (percentage of wet weight) of wild freshwater fish species and statistical comparison using one sample t-test, with values estimated for P. epeiroticus in lake Pamvotida. Data are mean values.
SpeciesMoistureAshProteinFatOriginReference
Pelophylax epeiroticus81.5 ± 3.631.10 ± 0.315.93 ± 3.320.25 ± 0.13GreecePresent study
Salmo trutta fario78.3 ***1.16 ± 0.03 ns17.36 ± 0.37 *2.71 ± 0.21 ***Turkey[53]
Salvelinus fontinalis76.54 ***1.89 ± 0.04 ***16.31 ± 0.09 ns2.33 ± 0.02 ***Turkey[54]
Oreochromis niloticus81.2 ± 1.0 ns0.5 ± 0.2 ***16.4 ± 0.60 ns2.00 ± 0.60 ***Poland[55]
Cyprinus carpio77.7 ± 2.6 ***0.6 ± 0.3 ***16.7 ± 0.80 ns5.1 ± 3.00 ***Poland[55]
Cyprinus carpio73.73 ± 0.24 ***0.88 ± 0.05 *16.69 ± 0.40 ns7.13 ± 0.10 ***Serbia[56]
Oncorhynchus mykiss73.00 ± 1.5 ***0.80 ± 0.2 **18.90 ± 0.80 ***7.4 ± 1.60 ***Poland[55]
Liza abu80.2 ns1.10 ns19.60 ***1.40 ***Iraq[57]
Aspius aspius78.51 ± 0.2 ***1.16 ± 0.05 ns18.07 ± 0.09 ***2.78 ± 0.11 ***Serbia[56]
Abramis brama78.66 ± 0.19 ***0.80 ± 0.04 **17.59 ± 0.22 *3.24 ± 0.15 ***Serbia[56]
Barbus barbus72.39 ± 0.29 ***1.33 ± 0.03 *18.61 ± 0.37 ***7.78 ± 0.15 ***Serbia[56]
Acipenser ruthenus75.38 ± 0.35 ***0.93 ± 0.09 ns17.54 ± 0.23 *5.39 ± 0.14 ***Serbia[56]
Esox lucius79.00 ± 0.14 **0.64 ± 0.03 ***18.43 ± 0.21 ***1.61 ± 0.01 ***Serbia[56]
Significance level (ns: non-significant, *: p < 0.05, **: p < 0.01, ***: p < 0.001).
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Hatziioannou, M.; Kougiagka, E.; Karapanagiotidis, I.; Klaoudatos, D. Proximate Composition, Predictive Analysis and Allometric Relationships, of the Edible Water Frog (Pelophylax epeiroticus) in Lake Pamvotida (Northwest Greece). Sustainability 2022, 14, 3150. https://doi.org/10.3390/su14063150

AMA Style

Hatziioannou M, Kougiagka E, Karapanagiotidis I, Klaoudatos D. Proximate Composition, Predictive Analysis and Allometric Relationships, of the Edible Water Frog (Pelophylax epeiroticus) in Lake Pamvotida (Northwest Greece). Sustainability. 2022; 14(6):3150. https://doi.org/10.3390/su14063150

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Hatziioannou, Marianthi, Efkarpia Kougiagka, Ioannis Karapanagiotidis, and Dimitris Klaoudatos. 2022. "Proximate Composition, Predictive Analysis and Allometric Relationships, of the Edible Water Frog (Pelophylax epeiroticus) in Lake Pamvotida (Northwest Greece)" Sustainability 14, no. 6: 3150. https://doi.org/10.3390/su14063150

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