BIOTROPIKA Journal of Tropical Biology
https://biotropika.ub.ac.id/
Vol. 11 | No. 1 | 2023 | DOI: 10.21776/ub.biotropika.2023.011.01.07 ACCUMULATION OF MICROPLASTICS IN THE DIGESTIVE TRACT AND
GONADS AND ITS EFFECTS ON GONAD QUALITY OF SEA URCHINS Tripneustes gratilla
Vanela Chatrin Lekatompessy1)*, Agung Pramana Warih Marhendra1), Nia Kurniawan1)
ABSTRACT
Marine plastic debris will move with the flow of water and float and then be fragmented into smaller particles, namely microplastics, sink, and settle on the substrate. Sea urchins, as deposit feeders, can potentially ingest microplastic particles, which can influence changes in behaviour, growth, enzyme production, reproduction, and tissue structure. This study used a purposive sampling method with descriptive analysis for data related to the recording of morphometrics and gonadal quality, followed up with the Tukey and Pearson tests. This study aims to analyze how the accumulation of microplastics in the organs (digestive tract and gonads) affects the gonadal quality of sea urchins Tripneustes gratilla.
The results show that the number of microplastic particles found in fi [1ve sea urchins from each beach was 233 particles/individual in the digestive tract of sea urchins and 205 particles/individual in the gonads with the colour variants transparent, multicolour, blue, yellow, red, green, and purple. Gonadal quality assessment indicators are colour, firmness, and gonadal index. Gonads with good quality were shown by sea urchins from Laha beach (site 1) with a composition of 40% bright orange, 40% yellow/pale yellow, and 20% brown, very firm of 80% and not firm of 20%, and a gonadal index value of 7.57 %. In contrast, gonads with poor quality were shown by sea urchins from Erie beach (site 4) with a composition of 80% brown and 20% grey, a very firm of 60% and firm of 40%, and a gonadal index value of 3.08%. This different quality is thought to be the result of microplastic accumulation in the sea urchin organs, which causes the satiated delusion.
This study shows that sea urchins in the waters of Outer Ambon Bay have been affected by the dangers of microplastics by decreasing the quality of the gonads produced. Therefore, it is necessary to prevent the waste problem in the waters of Ambon Bay and to cultivate long-term sea urchins.
Keywords: microplastic accumulation, gonadal quality, Tripneustes gratilla
INTRODUCTION
Marine plastic debris will move with the flow of water and float and then be degraded into smaller particles, namely microplastics, sink and settle on the substrate [1]. Microplastics are small pieces of plastic, less than 5 mm (0.2 inches) in length [2] that occur in the environment due to plastic pollution. The spatial distribution of microplastics in the marine environment can be affected by several factors, including wind, currents, waves and the density of plastic materials [3, 4] but still has the same chemical structure as plastic and does not experience changes in chemical structure or its constituent atoms [5] in various sizes such as fibre, fragment, film, granules, films, and foams [6].
Ecologically, Ambon Bay waters have the characteristics of minor island conditions and are usually homogeneous, so the resources used are more multiple uses [7]. Ambon Bay waters consist of parts, namely Ambon Inner Bay and Outer Ambon Bay, which are separated by a shallow and narrow threshold, namely the Poka-Galala Threshold. Due to the semi-enclosed water type,
tidal parameters greatly influence water circulation [8]. On several beaches in the waters of Outer Ambon Bay, the direction of surface currents that occur in the low tide period is towards the bay caused by the flow of water leading out of the bay to the northeast [9]. So there is an accumulation of residential waste washed out during the low tide period [10].
The results of Noya and Tuahatu's research [11]
showed that the maximum percentage value of floating marine waste is plastic waste at 93.44%, followed by metal waste at 1.17%, glass waste at 0.47%, cloth and paper waste with a minimum percentage of 0.23%. Microplastics deposited on the substrate will cover the last sediment deposits in the top layer and will likely enter the bodies of biota that live on the bottom of the waters, such as sea urchins Tripneustes gratilla, along with ingested food.
Microplastic particles ingested by sea urchins can cause pathological manifestations and physical injuries that damage the digestive organs, cause satiated delusions, reduce consumption, and compromise nutrition and energy, disrupting enzyme production, growth, reproduction, and
Submitted : November, 22 2022 Accepted : June, 19 2023
Authors affiliation:
1)Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Brawijaya, Indonesia
Correspondence email:
How to cite:
Lekatompessy, VC, Marhendra APW, Kurniawan N. 2023. Accumulation of microplastics in the digestive tract and gonads and its effects on gonad quality of sea urchins Tripneustes gratilla. Journal of Tropical Biology 11 (1): 53-63.
even death [12, 13]. Cocci et al. demonstrated that the accumulation of microplastics leads to increased levels of inflammation-associated cytokinin mRNA in gut tissue [14].
Several studies have reported that the toxicity of microplastics, such as polyethylene microparticles, was found to have a significant effect on the sea urchin Tripneustes gratilla [15]. The accumulation of microplastic polystyrene causes oxidative stress and increases ROS production, which correlates with gonadal damage, such as thinning of the basement membrane [16], penetrating the cell membrane, and inducing cell damage [17].
Furthermore, microplastics not only impact exposed biota but also, because of their ability, can act as vectors for the transport of other compounds and contaminants. This has been suggested by Mato et al., who reported the ability of polypropylene microparticles to absorb and accumulate large amounts of polychlorinated biphenyl (PCBs) from the surrounding water with an adsorption coefficient, translocating these compounds into the biota [18]. Therefore, this study analyzing the accumulation of microplastics in the organs of the digestive tract and gonads affects the quality of the gonads of the sea urchin Tripneustes gratilla in the water of Outer Ambon Bay.
METHODS
This research was conducted in February 2022 at the Ecology Laboratory, Department of Biology, Pattimura University, Ambon. The sea urchin Tripneustes gratilla samples were taken from several beaches in Outer Ambon Bay (Figure 1).
Sea urchin collection and morphometric measurements. A total of five sea urchins, Tripneustes gratilla, with a shell diameter >40 mm (mature adult), were taken from each several beaches in Outer Ambon Bay using a purposive sampling method at low tide (Table 1).
Morphometric measurements of sea urchins included shell diameter and body height using a digital calliper (Mitutoyo type CD-8"C5X, Japan) and total body weight using a digital scale (Ohaus type adventurer pro, USA).
Identification of microplastics in the digestive tract and gonads. Dissected organs of the digestive tract and gonads of sea urchins were then mixed with KOH (ratio 3:1). The sample was put into the oven for 24 hours at 50°C [19]. After the organic components were destroyed, the liquid was then filtered using Sartorius 1288 filter paper (12-15 mm) and filtered again using a qualitative filter (5 µm cellulose nitrate membrane, Whatmann) and observed using a stereo microscope with 100x magnification and 50 µm scale bar to identify the type, colour and size of microplastics.
Gonad quality analysis. Gonadal quality was assessed qualitatively based on colour assessment using the PENTONETM colour card (Figure 2) and the level of gonadal firmness (Figure 3) [20, 21].
The gonadal index (GI) is calculated using the following equation:
Gonadal Index (𝐺𝐼) = (𝑊𝑔⁄𝑊𝑡) × 100%
Note:
Wg = gonad weight (g) Wt = total body weight (g)
Data analysis. Descriptive analysis for data related to morphometry, gonadal quality, and the amount, colour, and size of microplastics found in the digestive tract and gonads of sea urchins.
Normality tests were performed for microplastic analysis data in the gonads and digestive tract, followed by the Tukey and Pearson test to analyze the correlation of microplastic accumulation in the digestive tract and gonad organs on gonad quality.
Figure 1. Geographical maps showing the sampling site
Table 1. Site coordinates, description location, and substrate type of sea urchin habitat
Site Location
Coordinate sites
Description of Substrate type Longitude Latitude
1 Laha Beach 128.101879 -3.71096 The gravel sand substrate is dominated by macroalgae Ulva sp. and a little Gracillaria sp.
2 Tawiri Beach 128.113086 -3.69112243 The sandy substrate and overgrown with macroalgae Gracillaria sp.
3 Hative Besar Beach
128.127541 -3.68432669 The rocky sand substrate and a few massive rocks are dominant in Turf algae and overgrown with Padina sp. macroalgae and Thalassia hemprichii seagrass with sandy reefs
4 Erie Beach 128.128897 -3.74952154 The muddy sand substrate, dead coral and overgrown with macroalgae Padina sp.
Figure 2. The colour classification of the PENTONETM colour card based on the colour libraries of the Adobe Photoshop CS5 Extended program
Figure 3. Firmness scale describing the texture of gonads
RESULTS AND DISCUSSION
Morphometry of sea urchins Tripneustes gratilla. Sea urchins taken from the four beaches in the waters of Outer Ambon Bay showed the criteria of having mature gonads with an average body shell diameter of >40 mm. The results of the morphometric recording showed that individual sea urchins had body shell diameters ranging from 70.87 mm – 79.01 mm. Sea urchin body height ranged from 47.95 mm – 53.61 mm. The total body weight of sea urchins ranged from 154.28 g – 265.05 g (Table 2). The individual sea urchins from the Erie beach had the largest morphometry
compared to the breeders from the other three beaches.
Tripneustes gratilla body weight is influenced by gonad maturity, where the range of body weights is due to differences in shell diameter and gonad weights. The increase in shell diameter is affected by increasing body weight. The larger the diameter of the shell, the greater the body weight of the sea urchin [20].
Variations in the size of the body shell diameter and total body weight are thought to be influenced by the condition of the substrate and the type of feed found in the broodstock habitat of sea urchins in the waters of Outer Ambon Bay (Table 1). The
nutritional content of red algae is chlorophyll a (74.920%), chlorophyll a derivative (16.419%), carotene (0.947%), xanthophyll (0.727%), and lutein (6.988%) [21]. The content and composition of the pigments in Padina sp., namely violaxanthin (5.99%), β-carotene (4.70%), and chlorophyll-a (4.93%). Pigment content and composition of Sargassum sp., namely chlorophyll a (52.82%);
fucoxanthin (20.95%); chlorophyll a derivative (14.88%); total xanthophyll (8.46%); β-carotene (1.49%); chlorophyll c (1.05%); as well as chlorophyll c derivatives (0.35%) [21, 22]. β- carotene increases gonadal growth, egg content, energy, and larval development rate in Strongylocentrotus droebachiensis [23].
Fucoxanthin, β-carotene, and β-echinenone enhance the biological defence reactions and increase egg production [24].
Microplastic accumulation in the digestive tract and gonads. The highest number of microplastic particles found in the gonads of sea urchins (Table 3) were sea urchins originating from Erie beach (site 4) with 98 particles/individual,
Laha beach (site 1) with 45 particles/individual, Hative Besar beach (site 3) with 40 particles/individual and the least was sea urchins from Tawiri beach (site 2) with 22 particles/individual.
The highest number of microplastic particles found in the digestive tract of sea urchins (Table 4) were sea urchins originating from Erie beach (site 4) with 85 particles/individual, Tawiri beach (site 2) with 80 particles/individual, Hative Besar beach (site 3) with 40 particles/individual and the least were sea urchins from Laha beach (site 1) with 28 particles/individual.
Microplastic particles can enter and accumulate in the digestive tract of sea urchins (Figure 4), supported by particle size (Table 5). The smallest size found is possible because smaller particles will easily enter the biota's body either through the food consumed or through the circulation of water that enters the biota's body outside. Microplastics from primary sources are already small in size (µm – mm), so when they are broken down, they will become even smaller [25].
Table 2. The average of sea urchin morphometric
Morphometric
Shell diameter (mm) Body height (mm) Total body weight (g)
St 1 70.87±3.03 47.95±2.11 147.43±20.58
St 2 79.01±4.60 51.95±3.64 199.18±37.05
St 3 74.41±1.62 49.63±1.46 145.28±27.12
St 4 78.34±5.53 53.61±2.91 265.05±67.22
Note: St 1: Laha Beach, St 2: Tawiri Beach, St 3: Hative Besar Beach, St 4: Erie Beach Table 3. Number of microplastic particles found in gonads
Number of microplastic (particle/L)
Total particles
Fibre Fragment Film Pellet
St 1 25 2 8 10 45
St 2 10 0 9 3 22
St 3 32 3 5 0 40
St 4 21 13 37 27 98
Table 4. Number of microplastic particles found in the digestive tract Number of microplastic (particle/L)
Total particles
Fibre Fragment Film Pellet
St 1 25 2 8 10 28
St 2 10 0 9 3 80
St 3 32 3 5 0 40
St 4 21 13 37 27 85
Table 5. The average width of microplastics found in the digestive tract
The average width of microplastics (µm)
Fibre Fragment Film Pellet
St 1 0.61±0.40 2.62±1.70 10.68±8.92 3.71±0.26
St 2 1.38±0.20 2.88±1.17 7.79±3.43 4.02±1.92
St 3 0.61±0.14 1.55±0 19.73±19.35 3.86±0.67
St 4 0.78±0.21 1.97±0.22 13.28±0 8.03±0
The types and colours of microplastics found in the digestive tract are types of fibre, fragments, films, and pellets with different colours:
transparent, multicolour, blue, red, yellow, green, and purple (Figure 4). While the types and colours of microplastics found in the gonads are types of fibre, fragments, films, and pellets with different colours: transparent, multicolour, blue, red, yellow, green, and purple (Figure 5).
The percentage of microplastic abundance found in samples of the digestive tract of sea urchins (Figure 6) and gonads (Figure 8) showed that the most common type of film was found while the least was pellet and fragment with transparent, multicolour, blue-red, yellow, green colour variants, and purple (Figures 7 and 9).
Microplastic fibre types come from the results of fishing activities such as fishing gear such as
nets and lake ropes, and also from domestic waste (household waste), namely the result of washing cloth which can release the remaining threads and sources of plastic material (Table 1) found on the coast beach [16]. The colour variations in these microplastic particles indicate the colour of the source of the plastic and/or other organic particles absorbed in the microplastics. In addition, the colour of the microplastic particles is also affected by the length of time these particles are exposed to UV light so that over time they will undergo oxidation which causes discolouration of the microplastics [27]. The results of the Tukey test showed that the abundance of microplastics in the gonads of individual sea urchins from Erie beach (site 4) was not significantly different from the abundance of microplastics found in the gonads of individual sea urchins from Laha beach (site 1).
Figure 4. Types and colours of microplastics found in samples of the sea urchin digestive tract in the waters of Outer Ambon Bay; A1: fibre (blue), A2: fibre (red), B1: film (green). C1: fragment (multicolour), C2:
fragment (transparent), D1: pellet (yellow). Magnification observation 100x and scale bar 50 µm.
Figure 5. Types and colours of microplastics found in a sample of sea urchin gonads in the waters of Outer Ambon Bay; A1: fibre (blue), A2: fibre (yellow), A3: fibre (red). A4: fibre (red), B1: film (transparent), C1:
fragment (purple), C2: fragment (blue), D1: pellet (green), D2: pellet (multicolour). Magnification observation 100x and scale bar 50µm.
Figure 6. The percentage of microplastic abundance found in samples of sea urchin gonads in the waters of Outer Ambon Bay
Figure 7. The percentage of microplastic colours found in gonad samples of individual sea urchins in the waters of Outer Ambon Bay
Figure 8. The percentage of microplastic abundance found in samples of sea urchin digestive tract in the waters of Outer Ambon Bay
Figure 9. The percentage of microplastic colour found in samples of sea urchin digestive tract in the waters of Outer Ambon Bay
Evaluation of gonadal quality. In this study, gonadal quality assessment indicators for sea urchins Tripneustes gratilla were colour, firmness and gonadal index. Gonad colour composition with good quality was seen in individual gonads of sea urchins from Laha beach (site 1) with a composition of 40% bright orange, 40%
yellow/pale yellow and 20% brown. Individual gonad colour of sea urchins from Tawiri beach (site 2) and Hative Besar beach (site 3) has a composition of 20% yellow/pale yellow, 60%
brown and 20% grey. Meanwhile, gonad colour with poor quality was seen in the gonads of individual sea urchins from Erie beach (site 4), with a composition of 80% brown and 20% grey.
The gonad quality of Tripneustes gratilla sea urchins is strongly influenced by the intake of carotenoids which are transferred through the available feed in the brooders' habitat. Because the feeding process is an important aspect of feeding for the growth and development of sea urchins.
Food eaten throughout life contains carotenoids, which act as gonadal pigments, and the rest as an optional food reservoir that parents store in yolk- stored eggs [28].
The colour of the gonads varies and is influenced by sex and the degree of maturity of the gonads [29]. Gonads of very good quality are bright yellow or orange-red in colour; gonads with
good quality are light yellow or orange in colour;
gonads of poor quality are pale or grey in colour [30].
The colour of the gonads varies and is influenced by sex and the degree of maturity of the gonads [31]. Gonads of very good quality are bright yellow or orange-red; gonads of good quality are light yellow or orange; gonads of poor quality are pale or grey.
The yellow and orange colours of sea urchin gonads are influenced by carotenoids such as ß- carotene, which is the main pigment in sea urchin gonads [32]. Carotenes absorbed from the intestine are converted to retinol in the retina, transported to the circulatory system, and bound to retinol- binding protein (RBP) in plasma. RBP is synthesized in the liver and enters oocytes. In sea urchin gonads, most carotenes are converted to echinenone via isocryptoxanthin.
Besides affecting the colour of the gonads, the maturity level of the gonads also affects their firmness of the gonads (Table 7). Kobayashi in his research suggested that the gonads of Diadema setosum sea urchins in a mature condition (mature) have a soft, slimy texture, while in the recovery phase, they have a firm texture(dense/compact) and during the gonad maturation stage, gonadal firmness will decrease (soften) [31, 33].
Table 6. The composition of sea urchin gonad colour found in Outer Ambon Bay
% Gonad colour composition
Bright orange Dark orange Yellow/pale yellow Brown Gray
St 1 40 - 40 20 -
St 2 - - 20 60 20
St 3 - - 20 60 20
St 4 - - 80 20
Table 7. The texture of sea urchin gonads found in the waters of Ambon Outer Bay
% Gonad texture composition
1 = very soft 2 = soft 3 = neither soft nor firm 4 = firm 5 = very firm
St 1 - - 20 - 80
St 2 - - - 80 20
St 3 - - - 20 80
St 4 - - - 40 60
Table 8. The gonadal index of sea urchin gonads found in the waters of Outer Ambon Bay
Average body weight (g) Average gonad weight (g) Gonadal index (%)
St 1 147.43±20.58 11.16±3.68 7.57
St 2 199.18±37.05 7.75±1.84 3.89
St 3 145.28±27.12 6.81±2.03 5.45
St 4 265.05±67.22 8.18±3.87 3.08
In addition, gonads that contain low water content have a dense texture, whereas gonads that contain high water content will produce gonads that are soft to runny. Good gonads for sea urchins are firm in texture, sweet, and smell like fresh seaweed.
The gonads of sea urchins from Erie beach (site 4) had a heavier average size than sea urchins gonads from Hative Besar beach (site 3) and Tawiri beach (site 2) but had the smallest gonadal index value (Table 8). The decrease in the gonadal index (GI) value was caused by a decrease in feed consumption by individual sea urchins. The difference in feed consumption is determined by the persistence to eat, not the food selection [34].
This difference in gonadal quality is thought to be the result of the accumulation of microplastics in the sea urchin organs resulting in satiated delusions [13].
Correlation between microplastic and gonad quality of sea urchin Tripneustes gratilla. The results showed that the correlation values for each colour are 0.127 (bright orange), -0.6618 (yellow), 0.480 (brown), and 0.1274 (grey) (Figure 10 a, b, c, and d). These results showed that the brown colour had a strong correlation with the coefficient of determination of 0.2304 or 23.04%. The correlation between microplastic and firmness, which describes the texture of the gonads of Tripneustes gratilla sea urchins, shows a very strong correlation of 0.29558, firm -0.20745 and
not soft or firm is -0.12744 (Figure 10 e, f, and g).
These results indicate a low category correlation between the very firm firmness scale and gonad quality with a determination value of 0.0873 or 8.73% shows a moderate correlation with a correlation value of 0.40345 and a coefficient of determination of 0.1627 or 16.27%, which means that the gonad index value represents the effect of microplastics at 16.27%, and other factors influence the rest (Figure 10 h).
As an export commodity for commercial purposes and cultivation for scientific research, the sea urchin Tripneustes gratilla has gonads with a high protein content. Sea urchin gonads contain high nutritional value. Gonads contain fat, protein, calcium, phosphorus, glycogen, vitamin A and B complex vitamins, and several amino acids that are good for growth. In fresh condition, the gonads of Tripneustes gratilla sea urchins contain 81.39%
moisture, 14.43% protein, 1.89% fat, and 3.92%
ash [35].
Sea urchin gonad development begins with the domination of nutritive phagocytic cells which have a thin layer of follicles. When entering the mature gonadal stage, the thickness of the follicular lining increases, and the number of nutritive phagocytic cells decreases, then accumulates in the lumen and follicle centre so that the follicle wall thickens as a sign of the partial spawning stage. The gonad quality index is in the same direction as the
gonad colour pattern. Gonad colour will be formed according to the level of colour development. In the early growth and maturation phases, the gonads show high-quality colours, whereas in the late maturation phase or after spawning, the gonads generally show low-quality colours [36].
Sea urchins on a restricted diet reabsorb skeletal material, whereas when food is abundant, energy is allocated to somatic cells and gonadal growth [37].
During gonad maturation, sea urchins do not grow in size under favourable nutritional conditions but instead allocate energy to gonad production and food reserves stored in their shells [38]. However, due to the craving of sea urchin saturation and malnutrition due to the effects of accumulation of microplastic particles in the gastrointestinal tract of sea urchins, the availability of forage in habitat has been neglected.
Microplastic particles in the digestive tract can move to other parts through the cell membrane and can enter the blood circulation system. This indicates that microplastic particles can move to all tissues and organs and then accumulate in these places. In this case, microplastic particles can accumulate in the gonads, as the main components of the gonads are macromolecular phospholipids and proteins because the main components of the gonads are macromolecular phospholipids and proteins with strong adhesion to microplastics [39, 40]. This affects the quality of the gonads produced by sea urchin broodstock. As found in this study, the gonads of sea urchins from habitats with a high abundance of microplastics from both water and sediment and the digestive tract of this sea urchin may have a heavier gonad weight, but the resulting gonad colour is poorer and darker.
CONCLUSION
In the waters of Outer Ambon Bay, Tripneustes gratilla sea urchins exposed to microplastics were found in their gonads and digestive tract, showing a decrease in gonad quality. The gonad colour with a bright orange percentage only reached 40%, while the brown colour reached 80%, and the gonadal index value only reached 7.75%, with the lowest value of 3.08%.
ACKNOWLEDGMENT
We thank Lembaga Pengelola Dana Pendidikan (LPDP), Republic of Indonesia, for supporting this research.
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0 5 10 15 20 25 30 35 40 0
10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Bright orange Pearson's -0.12744 R-Square 0.01624 Y 53.33+ -0.208X
0 5 10 15 20 25 30 35 40
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Yellow Pearson's r -0.6618
R-Square 0.43798 Y 77.75+-1.325
20 30 40 50 60 70 80 90
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Brown Pearson's r 0.48007 R-Square 0.23047 Y 16.94+0.623X
0 2 4 6 8 10 12 14 16 18 20 22
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Grey Pearson's r 0.12744
R-Square 0.01624 Y 45+0.416X
20 30 40 50 60 70 80
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Very firm Pearson's 0.29558 R-Square 0.08737 Y -0.36895
0 10 20 30 40 50 60 70 80
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Firm
Pearson's r -0.20745 R-Square 0.04304 Y 58.2+ -0.19
0 3 6 9 12 15 18 21
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Neither soft nor firm Pearson's r -0.12744
R-Square 0.01624
Y 53.33+ -0.426X
3 4 5 6 7 8
0 10 20 30 40 50 60 70 80 90 100
Microplastics (particle/ind)
Gonad Index (%)
Pearson's r 0.40345 R-Square 0.16277 Y 84.61+ -6.672X Gonad Index vs MPs
Figure 10. Correlation plot between microplastics accumulated in the gonads and gonadal quality (color, texture and gonadal index); (a) light orange colour, (b) yellow colour, (c) brown colour, (d) gray colour, (e) gonad texture scale: very firm, (f) texture: firm, (g) texture: neither soft nor firm, (h) gonadal index (%).
Pearson/Spearman correlation coefficient p>0.05.
a b
c d
e f
g h
