Uncovering Sexual Differences in the External Morphology, Appendicular Muscles, and Internal Organs of a Fossorial Narrow-Mouth Frog (Kaloula borealis)
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals
2.2. 3D Reconstruction
2.3. External Morphological Characteristics
2.4. Appendicular Muscle Mass
2.5. Internal Organ Mass
2.6. Statistical Analyses
3. Results
3.1. Results of Statistical Analysis
3.1.1. External Morphological Comparisons (Table 2)
External Morphological Characteristics | Mean ± Standard Deviation | R2 | F | p | |
---|---|---|---|---|---|
Males | Females | ||||
Independent sample t-test | |||||
1. Snout-vent length | 1.61 ± 0.02 | 1.63 ± 0.04 | / | 9.266 | 0.03 |
2. Body mass | 0.80 ± 0.06 | 0.83 ± 0.11 | / | 7.039 | 0.12 |
Covariance analysis | |||||
3. Head length | 0.95 ± 0.03 | 0.96 ± 0.04 | <0.001 | 0.189 | 0.67 |
4. Head width | 1.10 ± 0.03 | 1.09 ± 0.03 | 0.003 | 4.697 | 0.04 |
5. Eye diameter | 0.49 ± 0.05 | 0.53 ± 0.04 | 0.009 | 4.091 | 0.05 |
6. Upper arm length | 0.96 ± 0.03 | 0.97 ± 0.03 | <0.001 | 0.321 | 0.57 |
7. Upper arm width | 0.42 ± 0.06 | 0.41 ± 0.06 | 0.004 | 1.434 | 0.24 |
8. Lower arm width | 0.33 ± 0.05 | 0.32 ± 0.05 | 0.005 | 2.400 | 0.13 |
9. Lower arm and hand length | 1.27 ± 0.02 | 1.37 ± 0.39 | 0.174 | 2.211 | 0.14 |
10. Thigh width | 0.59 ± 0.04 | 0.58 ± 0.05 | 0.010 | 6.470 | 0.01 |
11. Tibia length | 1.08 ± 0.03 | 1.09 ± 0.03 | <0.001 | 0.731 | 0.40 |
12. Tibia width | 0.49 ± 0.05 | 0.50 ± 0.06 | <0.001 | 0.033 | 0.86 |
13. Tarsal length | 0.86 ± 0.03 | 0.87 ± 0.04 | <0.001 | 0.009 | 0.93 |
14. Tarsal width | 0.42 ± 0.03 | 0.44 ± 0.02 | <0.001 | 0.355 | 0.56 |
15. Foot length | 1.21 ± 0.02 | 1.20 ± 0.03 | 0.001 | 3.865 | 0.06 |
16. Thigh length | 1.18 ± 0.03 | 1.19 ± 0.03 | <0.001 | 0.249 | 0.62 |
3.1.2. Appendicular Muscle Mass Comparisons (Table 3)
Appendicular Muscles | Mean ± Standard Deviation of Dry Mass (mg) | R2 | F | p | |
---|---|---|---|---|---|
Males | Females | ||||
Pectoral girdle muscles | |||||
1. Coracobrachialis longus | 0.03 ± 0.21 | 0.06 ± 0.13 | 0.001 | 0.025 | 0.88 |
2. Coracobrachialis brevis | 0.20 ± 0.17 | 0.19 ± 0.13 | 0.009 | 0.441 | 0.51 |
3. Deltoideus scapularis | 0.51 ± 0.09 | 0.52 ± 0.12 | 0.016 | 3.316 | 0.08 |
4. Pectoralis | 0.37 ± 0.12 | 0.40 ± 0.14 | 0.010 | 0.089 | 0.77 |
5. Pectoralis abdominis, lateral portion | 0.39 ± 0.09 | 0.42 ± 0.11 | 0.002 | 0.384 | 0.54 |
6. Coracoradialis | 0.27 ± 0.09 | 0.26 ± 0.11 | 0.022 | 2.588 | 0.12 |
Forelimb muscles | |||||
1. Flexor carpi radialis | 0.02 ± 0.22 | −0.03 ± 0.29 | 0.069 | 1.065 | 0.31 |
2. Flexor digitorum communis | 0.03 ± 0.13 | 0.14 ± 0.11 | 0.087 | 6.122 | 0.02 |
3. Anconaeus | 0.19 ± 0.15 | 0.06 ± 0.16 | 0.314 | 16.137 | 0.01 |
4. Extensor carpi radialis | 0.17 ± 0.17 | 0.11 ± 0.11 | 0.062 | 3.280 | 0.08 |
5. Extensor carpi ulnaris | 0.03 ± 0.15 | 0.12 ± 0.16 | 0.014 | 0.782 | 0.38 |
6. Triceps brachii | 0.76 ± 0.09 | 0.81 ± 0.12 | <0.001 | 0.005 | 0.95 |
7. Flexor carpi ulnaris | 0.00 ± 0.12 | 0.07 ± 0.16 | 0.007 | 0.401 | 0.53 |
Abdominal muscles | |||||
1. Musculus rectus abdominis | 0.82 ± 0.13 | 0.69 ± 0.10 | 0.260 | 29.458 | 0.01 |
2. Obliquus abdominis externus | 1.59 ± 0.11 | 0.90 ± 0.16 | 5.170 | 676.250 | 0.01 |
3. Obliquus abdominis internus | 1.62 ± 0.24 | 1.02 ± 0.13 | 4.327 | 145.663 | 0.01 |
Hindlimb muscles | |||||
1. Biceps femoris | 0.27 ± 0.12 | 0.21 ± 0.14 | 0.103 | 7.305 | 0.01 |
2. Triceps femoris | 1.33 ± 0.07 | 1.36 ± 0.11 | 0.002 | 0.661 | 0.42 |
3. Adductor longus | 0.46 ± 0.09 | 0.52 ± 0.15 | 0.005 | 0.396 | 0.53 |
4. Sartorius | 0.26 ± 0.14 | 0.27 ± 0.13 | 0.005 | 0.308 | 0.58 |
5. Adductor magnus | 0.98 ± 0.08 | 0.99 ± 0.13 | 0.011 | 2.288 | 0.14 |
6. Gracilis major | 0.84 ± 0.07 | 0.83 ± 0.09 | 0.029 | 8.396 | 0.01 |
7. Gracilis minor | 0.46 ± 0.11 | 0.44 ± 0.19 | 0.048 | 2.5475 | 0.12 |
8. Semimembranosus | 0.59 ± 0.09 | 0.56 ± 0.11 | 0.053 | 8.796 | 0.01 |
9. Semitendinosus | 0.64 ± 0.07 | 0.63 ± 0.11 | 0.021 | 4.943 | 0.03 |
10. Piriformis | 0.07 ± 0.11 | 0.09 ± 0.19 | <0.001 | 0.007 | 0.93 |
11. Iliopsoas | 0.30 ± 0.12 | 0.27 ± 0.19 | 0.075 | 4.008 | 0.05 |
12. Tibialis anticus longus | 0.79 ± 0.08 | 0.81 ± 0.12 | 0.007 | 1.384 | 0.25 |
13. Tastrocnemius | 0.87 ± 0.14 | 0.90 ± 0.09 | <0.001 | 0.022 | 0.88 |
14. Peroneus | 0.54 ± 0.09 | 0.58 ± 0.10 | <0.001 | 0.005 | 0.95 |
15. Extensor cruris | 0.03 ± 0.09 | 0.06 ± 0.11 | <0.001 | 0.008 | 0.93 |
16. Tibialis posticus | 0.05 ± 0.09 | 0.01 ± 0.16 | 0.079 | 7.399 | 0.01 |
3.1.3. Internal Organ Mass Comparisons (Table 4)
Mean ± Standard Deviation of Dry Mass (mg) | R2 | F | p | ||
---|---|---|---|---|---|
Males | Females | ||||
1. Heart | 1.25 ± 0.15 | 1.22 ± 0.21 | 0.112 | 6.778 | 0.01 |
2. Liver | 1.58 ± 0.15 | 1.64 ± 0.29 | 0.015 | 0.534 | 0.47 |
3. Spleen | −0.61 ± 0.35 | −0.77 ± 0.29 | 0.386 | 3.934 | 0.06 |
4. Lung | 1.11 ± 0.09 | 1.04 ± 0.11 | 0.138 | 24.952 | 0.01 |
5. Kidney | 0.89 ± 0.06 | 0.94 ± 0.14 | 0.002 | 0.169 | 0.68 |
6. Digestive tract | 1.67 ± 0.10 | 1.71 ± 0.14 | 0.001 | 0.072 | 0.80 |
7. Corpus adiposum | 0.37 ± 0.65 | 0.24 ± 0.90 | 0.650 | 1.140 | 0.29 |
8. Vesica fellea | −0.39 ± 0.51 | −0.49 ± 0.34 | 0.154 | 0.780 | 0.38 |
3.2. Results of Principal Component Analysis (Table 5; Figure 3)
3.3. Results of Allometric Analysis for Significantly Sexual Different Traits (Figure 4)
4. Discussion
4.1. Sexual Dimorphism in the External Morphological Characteristics
4.2. Sexual Dimorphism in the Appendicular Muscle Mass
4.3. Sexual Differences in the Internal Organs
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Functional Groups | Muscles | References |
---|---|---|
1. Pectoral girdle flexors | Deltoideus scapularis (DS); coracobrachialis longus (COL); coracobrachialis brevis (COB) | Duellman and Trueb [50]; Myatt, Crompton, and Thorpe [51]. |
2. Upper arm flexor | Pectoralis (PE); pectoralis abdominis, lateral portion (PALP); | Zhou [52]. |
3. Forearm flexor | Coracoradialis (CO) | Abdala and Diogo [53]. |
4. Carpus flexors | Flexor carpi ulnaris (FCU); flexor carpi radialis (FCR); flexor digitorum communis (FDC) | Manzano, Abdala, and Herrel [54]; Böhmer et al. [55]. |
5. Elbow extensors | Anconaeus (AN); triceps brachii (TB) | Böhmer et al. [55]. |
6. Carpus extensors | Extensor carpi ulnaris (ECU); extensor carpi radialis (ECR) | Böhmer et al. [55]. |
7. Abdominal muscle | Musculus rectus abdominis (MRA); obliquus abdominis internus (OAI), obliquus abdominis externus (OAE) | Zhou [52]. |
8. Knee flexors | Biceps femoris (BF); semimembranosus (SEM); sartorius (SA); gastrocnemius (GA) | Zhou [52]; Taylor-Burt and Biewener [56]. |
9. Knee flexors and internal tibial rotators | Gracilis major (GMA); gracilis minor (GMI); semitendinosus (SET) | Chin et al. [57]. |
10. Hip adductors | Adductor magnus (AM); adductor longus (AL) | Přikryl et al. [58]. |
11. Knee extensor | Triceps femoris (TF) | Padilla, Courant, and Herrel [59]. |
12. Long extensors | Peroneus (PE); tibialis anticus longus (TAL); tibialis posticus (TP); extensor cruris (EC) | Padilla, Courant, and Herrel [59]. |
13. Others | Piriformis (PI); iliopsoas (IL) | Zhou [52]. |
External Morphological Characteristics | PC1 | PC2 | PC3 | PC4 | PC5 | PC6 | Forelimb, Chest, and Abdominal Muscles | PC1 | PC2 | PC3 | PC4 | Hindlimb Muscles | PC1 | PC2 | PC3 | Internal Organs | PC1 | PC2 | PC3 |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1. HL | 0.16 | −0.02 | 0.38 | 0.61 | 0.05 | −0.34 | 1. COL | 0.46 | −0.02 | 0.69 | −0.28 | 1.BF | 0.47 | −0.81 | 0.09 | 1.HE | 0.66 | −0.67 | −0.01 |
2. HW | 0.12 | 0.18 | −0.43 | 0.70 | −0.22 | −0.06 | 2. COB | 0.50 | −0.09 | −0.52 | −0.12 | 2.TF | 0.38 | 0.86 | 0.04 | 2.LI | 0.82 | −0.24 | 0.27 |
3. UAL | 0.24 | 0.46 | 0.37 | −0.27 | 0.17 | −0.52 | 3. DS | 0.81 | 0.06 | 0.31 | −0.16 | 3.AL | 0.74 | −0.03 | −0.07 | 3.SP | 0.62 | 0.48 | −0.07 |
4. UAW | 0.63 | −0.27 | 0.15 | 0.27 | 0.31 | 0.25 | 4. PE | 0.67 | −0.27 | −0.19 | −0.20 | 4.SA | 0.69 | −0.46 | −0.05 | 4.LU | 0.67 | 0.25 | −0.49 |
5. LAHL | −0.14 | 0.11 | 0.61 | 0.21 | 0.39 | 0.29 | 5. PALP | 0.82 | −0.13 | −0.01 | −0.07 | 5.AM | 0.91 | 0.05 | 0.03 | 5.KI | 0.73 | −0.18 | 0.18 |
6. LAD | 0.68 | −0.21 | 0.05 | −0.05 | 0.18 | −0.22 | 6. CO | 0.69 | 0.01 | −0.26 | 0.45 | 6.GMA | 0.88 | −0.11 | 0.23 | 6.DI | 0.36 | 0.51 | 0.72 |
7. THIL | 0.17 | 0.81 | −0.08 | −0.12 | 0.06 | 0.29 | 7. FCR | 0.47 | −0.08 | −0.38 | 0.20 | 7.GMI | 0.72 | 0.11 | −0.01 | 7.COAD | 0.53 | 0.25 | −0.45 |
8. THIW | 0.65 | 0.17 | −0.45 | 0.04 | −0.19 | 0.07 | 8. FCU | 0.49 | −0.36 | −0.27 | −0.36 | 8.SEM | 0.71 | 0.51 | 0.26 | ||||
9. TL | 0.27 | 0.66 | 0.17 | −0.31 | −0.17 | 0.14 | 9. FDC | 0.27 | −0.65 | 0.20 | 0.18 | 9.SET | 0.91 | −0.01 | −0.02 | ||||
10. TW | 0.82 | −0.18 | 0.00 | −0.11 | −0.16 | 0.00 | 10. AN | 0.64 | 0.39 | −0.20 | 0.21 | 10.PI | 0.54 | 0.26 | −0.53 | ||||
11. TARL | 0.01 | 0.34 | −0.41 | 0.22 | 0.65 | 0.21 | 11. ECR | 0.43 | 0.20 | 0.49 | 0.55 | 11.IL | 0.54 | −0.05 | 0.68 | ||||
12. TARW | 0.86 | −0.08 | 0.09 | −0.09 | 0.05 | 0.02 | 12. ECU | 0.68 | −0.47 | 0.01 | 0.19 | 12.TAL | 0.93 | −0.02 | −0.06 | ||||
13. FL | 0.00 | 0.59 | 0.21 | 0.44 | −0.28 | −0.19 | 13. MRA | 0.62 | 0.57 | 0.08 | −0.24 | 13.GA | 0.59 | −0.12 | −0.09 | ||||
14. ED | 0.11 | −0.12 | 0.45 | 0.15 | −0.44 | 0.54 | 14. OAE | 0.34 | 0.85 | −0.09 | 0.07 | 14.PE | 0.77 | −0.05 | −0.16 | ||||
15. OAI | 0.34 | 0.85 | 0.02 | −0.16 | 15.EC | 0.72 | −0.09 | −0.45 | |||||||||||
16. TB | 0.78 | −0.28 | 0.14 | −0.11 | 16.TP | 0.68 | 0.14 | 0.15 | |||||||||||
Explanatory rate | 20.87 | 14.33 | 10.88 | 10.36 | 8.26 | 7.59 | 34.63 | 18.09 | 9.51 | 6.59 | 51.51 | 12.45 | 7.11 | 41.29 | 16.28 | 15.23 |
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Wang, X.; Zhang, M.; Zhang, W.; Jiang, J.; Dong, B. Uncovering Sexual Differences in the External Morphology, Appendicular Muscles, and Internal Organs of a Fossorial Narrow-Mouth Frog (Kaloula borealis). Animals 2025, 15, 2118. https://doi.org/10.3390/ani15142118
Wang X, Zhang M, Zhang W, Jiang J, Dong B. Uncovering Sexual Differences in the External Morphology, Appendicular Muscles, and Internal Organs of a Fossorial Narrow-Mouth Frog (Kaloula borealis). Animals. 2025; 15(14):2118. https://doi.org/10.3390/ani15142118
Chicago/Turabian StyleWang, Xiuping, Meihua Zhang, Wenyi Zhang, Jianping Jiang, and Bingjun Dong. 2025. "Uncovering Sexual Differences in the External Morphology, Appendicular Muscles, and Internal Organs of a Fossorial Narrow-Mouth Frog (Kaloula borealis)" Animals 15, no. 14: 2118. https://doi.org/10.3390/ani15142118
APA StyleWang, X., Zhang, M., Zhang, W., Jiang, J., & Dong, B. (2025). Uncovering Sexual Differences in the External Morphology, Appendicular Muscles, and Internal Organs of a Fossorial Narrow-Mouth Frog (Kaloula borealis). Animals, 15(14), 2118. https://doi.org/10.3390/ani15142118