Salmonid sensory system development is affected by climate change driven temperature increases

Abstract

Increases in water temperature due to global climate change are known to alter the course and timing of fish development. The mechanosensory lateral line (LL) system mediates flow-sensing behaviors vital for survival in fishes, but the effects of increased water temperatures resulting from climate change on its development have not been examined. Here LL development was documented in a cold-water salmonid (brook trout, Salvelinus fontinalis) reared at the thermograph of a long-term study stream (ambient) and two higher temperatures (+ 2 and + 4 °C) that reflect projected increases within their native range. At these two higher temperatures, fish reach crucial early life history transitions earlier (e.g., hatch, "swim-up" from gravel nests into the water column) and are larger in size through the parr (juvenile) stage. Early forming canal neuromast receptor organs are larger, and the process of canal morphogenesis is also accelerated suggesting potential consequences for neuromast function and presumably for LL-mediated behaviors. A potential mismatch between the timing of transitions in early life history stages, the ability to carry out LL-mediated behaviors (e.g., prey detection), and the timing of the seasonal emergence of their preferred prey, could have serious implications for cold-water salmonid ecology and survival.

Keywords: Brook trout; Flow sensing; Lateral line; Neuromast; Ontogeny.

Fig. 1

Representative brook trout cranial lateral line morphology and development. (A) Lateral line canals (canal neuromasts = red circles) and lines of superficial neuromasts (blue circles) derived from specimens via vital fluorescent staining and clearing and staining. Canals: SO-n = supraorbital canal, portion associated with the nasal bone, SO-f = supraorbital canal, portion associated with the frontal bone, PT = posttemporal canal, OT = otic canal, POT = post-otic canal, SCL = supracleithral canal, , IO = infraorbital canal, PM-p = preopercular-mandibular canal segments associated with preopercle. The PM-d (canal segments associated with dentary bone) and the PM-a (canal segments associated with anguloarticular bone) comprise the PM-m, the mandibular portion of the preopercular-mandibular canal (analyzed in detail, see text for more details). Superficial neuromast lines: adl = antero-dorsal line, mdl = midline, chl = cheek line, eth = ethmoidal line. Adapted from Jones et al.. (B,C) Scanning electron micrographs (SEM), illustrating (B) superficial neuromast (SN) and (C) canal neuromast (CN) morphology. (D) Fluorescent staining of a 38 mm parr (245 dpf, + 0 °C) with 4-Di-2-ASP in lateral view (images in ventral and dorsal view were also used for counting neuromasts on the left side of the head). (E–G) Stages of canal morphogenesis. (E) SEM of canal neuromasts on skin (Stage 1; arrows = neuromasts), (F) in groove with ossified canal walls (Stage 2b; arrows = neuromasts), and in (G) cleared and stained specimens showing a canal segment with ossified canal walls and a soft tissue roof (arrow, Stage 3), and two canal segments (arrowheads) with ossified canal walls and roof (Stage 4).

Fig. 2

Temperature regime in rearing system (refer to Materials and Methods section for additional details). Dashed line = fertilization date (November 17, 2020). Thickness of colored bars (Blue, + 0 °C [ambient]; yellow, + 2 °C; red, + 4 °C) reflects diel temperature fluctuations over the winter. Arrows = time at which fish, just prior to swim-up, were moved to 1-m round tanks. Temperature in each of the three treatments (in 1-m round tanks) increased with the same seasonal pattern as in the long-term study stream from which brood stock were obtained (as in).

Fig. 3

Size versus age for fish used for vital fluorescent staining in all three temperature treatments (refer to Fig. 1D). Rate of growth (best-fit linear regression, p < 0.05): 0.24 mm SL⋅day⁻¹ at + 4 °C (red, R² = 0.88, n = 44), 0.25 mm SL⋅day⁻¹ at + 2 °C (yellow, R² = 0.96, n = 47), and 0.26 mm SL⋅day⁻¹ at + 0 °C ([ambient], blue, R² = 0.93, n = 43). Fish size was significantly larger at + 4 °C than at + 2 °C and + 0 °C (ambient), and fish reared at + 2 °C were significantly larger than those reared at + 0 °C (ambient) (ANCOVA with Tukey Contrasts, p < 0.05). SL = standard length, dpf = days post-fertilization.

Fig. 4

Ontogenetic increase in canal or superficial neuromast number is not significantly different among temperature treatments (ANCOVA with Tukey Contrasts, p > 0.05; data derived from vital fluorescent staining). (A) Canal neuromast (CN) number increases linearly with fish size (standard length, mm SL) prior to canal enclosure; a breaking point (arrows, with 95% confidence) occurs at 21.2–23.7 mm SL, 22.0–24.9 mm SL, and 21.1–24.4 mm SL, at + 4 (red), + 2 (yellow), + 0 °C (blue [ambient]), respectively, indicating that number ceases to increase after these points (best-fit linear regression with segmented relationships; see Materials and Methods and S1 for more details). (B) Superficial neuromast (SN) number increases linearly with fish size throughout ontogeny (best-fit linear regression parameters reported in text and S1). Note differences in y-axis values for CNs and SNs, indicating that SNs become more numerous than CNs in individuals of comparable sizes.

Fig. 5

Size of canal neuromasts (CNs; in SO-f and PM-d canal series) and superficial neuromasts (SNs; in adl series) versus fish size (mm standard length [SL], left) and age (days post-fertilization [dpf], right) derived from SEM images. Neuromast size (length) was compared among treatments using ANCOVA with Tukey contrasts, α = 0.05; refer to text and S3, S4 for details. (A) Size of canal neuromasts in the SO-f canal (n = 70 neuromasts) vs. fish size was significantly larger in fish reared at higher temperatures (red = + 4 °C, p = 0.002; yellow = + 2 °C, p < 0.001) than at ambient temperature (+ 0 °C [ambient], blue). (B) Size of CNs PM-d canal (n = 84 neuromasts) was not significantly different among temperature treatments (ANCOVA, p > 0.05, S4). Data presented in A and B include only SO-f and PM-d canal neuromasts prior to their enclosure in canals, after which (in larger/older fishes) they could not be visualized with SEM. (C) Size of adl SNs (n = 185 neuromasts) was not significantly different among temperature treatments (ANCOVA, p > 0.05, S4). SO-f: supraorbital canal segments associated with frontal bone, PM-d: preopercular-mandibular canal segments associated with the dentary bone, adl = antero-dorsal SN line; refer to Fig. 1A.

Fig. 6

Onset (first segment at a given stage) and duration of each stage of canal morphogenesis (ending when last segment is observed at a stage) in two cranial lateral line canals for all three temperature treatments (red, + 4 °C; yellow, + 2; blue, + 0 °C [ambient]). (A) Supraorbital (SO) canal (associated with the nasal and frontal segments). (B) Preopercular-mandibular (PM) canal (associated with the dentary and anguloarticular segments). Onset of canal morphogenesis (Stage 2a) occurs at about the size at which swim up occurs (~ 21 mm SL) in all three temperature treatments. Canal morphogenesis progresses at an accelerated rate at higher temperatures such that more advanced stages of canal morphogenesis are reached in smaller fish at + 4 °C than at + 2 °C or + 0 °C (ambient).