Interspecific differences and ecological correlations between scale number and skin structure in freshwater fishes

Abstract

Fish skin is mainly composed of the epidermis, dermis, and its derivative scales. There is a wide diversity in scale number in fishes, but the diversity of skin structure lacks systematic histological comparison. This research aimed to improve our understanding of the functional relationship between the scale number and the skin structure in freshwater fishes and to determine which ecological factors affect the scale number and skin structure. First, we presented a method to quantify skin structure in fish and histologically quantified the skin structure of 54 freshwater fishes. Second, we collected the scale number and habitat information of 509 Cyprinidae fishes in China and explored which ecological factors were related to their scale number. Third, common carp and scaleless carp were used as models to study the effects of scale loss on swimming. We found a strong negative correlation between scale thickness and scale number. The main factor affecting the skin structure of fishes was the species' water column position, and the skin of benthic fishes was the most well-developed (thicker skin layers (dermis, epidermis) or more/larger goblet cells and club cells). The scale number was related to two factors, namely, temperature and water column position, and cold, benthic and pelagic adaptation may have contributed to increased scale numbers. Only in benthic fishes, the more well-developed their skin, the more scales. In common carp, scale loss did not affect its swimming performance. In summary, we suggest that there is a rich diversity of skin structure in freshwater fishes, and the scales of fish with well-developed skin tend to degenerate (greater number/smaller size/thinner, or even disappear), but the skin of fish with degenerated scales is not necessarily well developed.

Keywords: ecological adaptation; functional antagonism; scale degeneration; scale number; skin structure.

Figure 1

Reference figure for quantitative indicators. (A) Reference figure for quantitative scale number. The red rectangular box represents the skin tissue section area. (B) Reference figure for quantitative skin structure. The scale is 100 μm. SOLL: the number of scales on the lateral line; SALL: the number of scales above the lateral line; SBLL: the number of scales below the lateral line; TS: transverse scales; LS: longitudinal scales. TS and LS are usually used in fish with no lateral lines or with incomplete lateral lines.

Figure 2

Relationship between the degree of scale degradation (DSD) and relative scale thickness of experimental fishes. The circle and whiskers indicate the mean ± SE.

Figure 3

The phylogenetic relationship, degree of scale degradation (DSD), the comprehensive skin index (CSI) and habitat water layer of experimental fishes. The CSIs are standardized to 0–100 based on minimum and maximum values in all species. * represents a bootstrap value of less than 70.

Figure 4

Relationship between the degree of scale degradation (DSD) and the comprehensive skin index (CSI) of experimental fishes. (A) Traditional correlation between the DSD and CSI of experimental fishes. (B) Corrected correlation between the DSD and CSI of all fishes by phylogenetic independent contrasts (PIC). (C) Corrected correlation between the DSD and CSI of Cyprinidae fishes by PIC. (D) Corrected correlation between the DSD and CSI of non-Cyprinidae fishes by PIC. The circle and whiskers indicate the mean ± SE.

Figure 5

Relationship among the habitat layers, the degree of scale degradation (DSD) and the comprehensive skin index (CSI) of experimental fishes. (A) Relationship between the DSD and CSI of experimental fish in different water column positions. (B) Comparison of the CSI of fish in different water column positions. (C) Examples of large and small pelagic fishes. (D) Comparison of the DSD of pelagic fishes with different body types. In (B), each dot represents data for each tissue image of each species. The different superscripts differ (A, B) significantly at P < 0.01 based on Tukey test, the different superscripts differ (A, B) significantly at P < 0.05 based on Phylogenetic ANOVA, and whiskers indicate mean ± SE. Figure (C) from Guo et al. (2021).

Figure 6

Relationship between the degree of scale degradation (DSD) and temperature, altitude, and latitude in Cyprinidae fishes. (A) Correlation analysis between the DSD and mean temperature (T_mean), mean temperature in warm months (WM T_mean), and mean temperature in cold months (CM T_mean). * represents P < 0.001; r represents Pearson’s bivariate correlation analysis. (B) Relationship between the DSD and WM T_mean. (C) Relationship between the DSD and altitude. (D) Relationship between the DSD and latitude. r and r_p indicate Pearson’s correlation analysis and partial correlation analysis with latitude or altitude as a control variable, respectively.

Figure 7

Comparison of swimming performance between common carp and scaleless carp. (A) Comparison of critical swimming speed (U_crit) between common carp and scaleless carp. (B) Comparison of critical swimming speed relative to body length (U_crit/BL) between common carp and scaleless carp. (C) Relationship between swimming speed and metabolic rate of common carp and scaleless carp. The height gives the mean, the thick lines give the medians, and whiskers indicate mean ± SE.