Perca flavescens (Mansueti, 1964)

Fraz, Shamaila, Laframboise, Lisa, Manzon, Richard, Somers, Christopher M. & Wilson, Joanna Y., 2024, Embryonic and larval development of yellow perch (Perca flavescens) and its sensitivity to incubation temperature, Journal of Fish Biology 105 (3), pp. 735-751 : 745-747

4.1 | Developmental progression in P. flavescens (constant 12 C)

The development of yellow perch ( P. flavescens ) was originally described in Mansueti (1964, incubation at seasonal temperature between 10 and 22 C) but was missing the key initial embryonic stages (cleavage, cell division, and migration) and lacked microscopic images (but had excellent drawings). Mansueti (1964) had no information about the effect of temperature on the developmental progression and survival and did not describe morphological abnormalities. Thus, we used Mansueti (1964) and Eurasian perch development ( Alix et al., 2015, incubation at constant 13 ± 0.5 C) as main guides to describe perch development, providing microscopic imaging of developmental stages. P. flavescens and P. fluviatilis are congeneric ( Hokanson & Kleiner, 1974), suggesting that development should be highly similar in these species. Developmental comparisons to other percids were made with use of Kestemont et al. (2015); the developmental staging series for zebrafish was utilized for the characterization of early development (cell cleavage to gastrulation; Kimmel et al.,1995). Overall, our results suggest that the development of P. flavescens embryos at the constant 12 C regime is comparable with other percids, especially P. fluviatilis . A detailed developmental stagewise comparison of the two species is discussed below.

During embryogenesis in the constant 12 C regime, the first two cell cleavages occurred at a vertical plane and divided the cytoplasm into meroblasts aggregated at the animal pole to form a bilateral arrangement of cells. Cleavage occurred in two planes starting from 3rd cell division forming two rows of cells like zebrafish ( Kimmel et al., 1995); the planes became irregular at the 16-cell stage, and asynchronous between the 64- and 128-cell stage similar to P. fluviatilis ( Alix et al., 2015) . In constant 12 C regime, the duration of development from the start of cleavage to the end of blastulation was 26 h, similar to previous reports in this species (26 h, Mansueti, 1964; 30 h, Kestemont et al., 2015) and other percids like walleye ( Stizostedion vitreum , 25 h, Kestemont et al., 2015) and P. fluviatilis (24 h, Alix et al., 2015).

The timing of the onset and duration of gastrulation in the constant 12 C regime (2 dpf, 30 h) agrees with P. fluviatilis ( Alix et al., 2015) , and prior studies of P. flavescens (29 h, Mansueti, 1964) but not with others (18 h, Kestemont et al., 2015). Like P. fluviatilis ( Kestemont et al., 2015) and zebrafish ( Kimmel et al., 1995), the embryonic shield was visible from 50% epiboly onward. In contrast to percids like walleye and logperch ( Percina caprodes ), a 90 rotation of the embryo in gastrulation for repositioning of the oil droplet was not observed in our constant 12 C regime ( Alix et al., 2015; Kestemont et al., 2015).

The chronology of organogenesis is analogous in percids; however, they may differ in the substages with regard to completion of each organ during the embryonic or larval periods ( Kestemont et al., 2015). Some overlap between gastrulation and organogenesis 1 is reported for percids like P. fluviatilis, ( Alix et al., 2015) and rainbow darter ( Etheostoma caeruleum, Paine & Balon, 1984 ). Such observations were noted in our constant 12 C regime because optic primordia appeared before tail bud closure. The translocation movement decreasing the distance between the embryo's head and the oil droplet in the constant 12 C regime was a finding analogous to P. fluviatilis ( Alix et al., 2015) , walleye, and logperch ( Kestemont et al., 2015). Concordant to the records for other percids ( Kestemont et al., 2015), the first morphological sign of cell differentiation in P. flavescens was the appearance of the neural plate (61 hpf in constant 12 C regime), which is close to the documented (63.5 h, Hokanson & Kleiner, 1974). Eyes were the first organ that began to develop followed by the formation of notochord and the otic vesicles, similar to the records of P. flavescens ( Mansueti, 1964) and P. fluviatilis ( Alix et al., 2015) .

The duration of organogenesis 2 and 3 and the landmark differentiation events between P. fluviatilis ( Alix et al., 2015) and P. flavescens (this study, constant 12 C regime) were comparable. The timing of heartbeat onset and complete retinal pigmentation in P. flavescens constant 12 C regime were comparable to Hokanson and Kleiner (1974; heartbeat at 6.5 – 7 dpf, eye pigmentation at 9.5 dpf) but different from P. fluviatilis (heartbeat at 4 dpf, eye pigmentation at 8 dpf, Alix et al., 2015). Overall chronology of the developmental events in the constant 12 C regime was congruent to Manuseti 1964. The presence of coordinated fin flutter in organogenesis 3 of the constant 12 C regime of the current study was a feature not reported in P. fluviatilis ( Alix et al., 2015) .

A much longer duration of organogenesis 4 was recorded in P. flavescens (7 days, constant 12 C regime) as compared to P. fluviatilis ( Alix et al., 2015) . This was expected because hatching occurred 3 – 6 days earlier in P. fluviatilis as compared to P. flavescens when incubated at temperatures less than 13 C. In the constant 12 C regime, the timing of mass hatch, hatching duration, and developmental landmarks (formation of gills, mouth, and pharyngeal cartilages) were similar to the earlier records of P. flavescens ( Hokanson & Kleiner, 1974; Kestemont et al., 2015). In our study (constant 12 C), gaping of the mouth in the newly hatched larvae and the presence of gills and digestive tract showed that the larvae hatch quite mature in agreement to Mansueti (1964) but contrasts with other percids and P. fluviatilis , in which mouth gaping occurs later (10 dph, Alix et al., 2015, Kestemont et al., 2015). In our constant 12 C regime, the larvae of P. flavescens were passive swimmers like P. fluviatilis ( Alix et al., 2015) , which differs from the reports of active swimming at this stage (Manuseti 1964). The difference could be reasonably explained from the use of a variable temperature (10 – 22 C) by Manuseti (1964).

Organogenesis 5 is a relatively long substage corresponding to the advanced development of fins, circulatory, branchial, digestive, and skeletal systems, and body pigmentation. In accordance with reports for P. flavescens ( Hokanson & Kleiner, 1974, 20 dpf), the larvae in our study (constant 12 C regime) were able to swim to the surface for the first feed between 19 and 21 dpf, whereas this was noted in P. fluviatilis at 11 and 15 dpf ( Alix et al., 2015). In the constant 12 C regime larvae, inflation of the swim bladder occurred concomitantly with the start of feeding when the digestive system was still immature ( Kestemont et al., 2015). Unfed larvae did not survive in the constant 12 C regime beyond 32 dpf, whereas this phase was described to end at around 35 dpf previously ( Hokanson & Kleiner, 1974). Overall, the chronology and timing of fin differentiation, and morphological changes in the shape of the body, head, eye, upper and lower jaws, and body pigmentation in the constant 12 C regime larvae occurred, consistent with the findings of Mansueti (1964) and Urho (1996). The total duration of organogenesis in our constant 12 C regime was 30 days, longer than the 23 days reported earlier ( Kestemont et al., 2015), with the use of a variable temperature regime (10 – 22 C). The total developmental time (fertilization to exogenous feeding at constant 12 C) was around 32 days, which is close to the previous reports for P. flavescens (29 days, Kestemont et al., 2015).

Considering the close analogy between the developmental ontogeny of P. flavescens and P. fluviatilis , we suggest that saltatory development model is appropriate for P. flavescens . This is owing to the presence of developmental steps similar to P. fluviatilis that mark important thresholds defined by the acquisition of new abilities. These thresholds include the zygote, cell cleavage, gastrulation, and organogenesis, which is further divided into five substages (O1 – 5) corresponding to the development of specific organs and systems. The swim up, first oral feeding, switch to exogenous feeding are the phases constituting O5. The pre-juvenile period is also considered a threshold that defines the larval to adult-like transition of fish with the loss of larval structures.