Emersion and microhabitat selection
Nudibranchs are known for their sudden appearance and disappearance in intertidal areas (see Table 1), but reports of emerged nudibranchs are scarce [10, 11, 27]. The present work constitutes the first comprehensive report of the seasonal occurrence of emerged nudibranchs during low tides. In contrast to other molluscs, nudibranchs do not possess a shell that protects them from desiccation and allows them to create a high humidity environment within their shells. Instead, they usually seek areas of great humidity and refuge beneath rocks or other shelters (see more about microhabitat selection in [28]). Although nudibranchs are generally not found in unsheltered and open areas, in the present study we showed that dozens of individuals were emerged at low tides during spring months. Nevertheless, it is worth mentioning that the texture of the substratum (i.e. oyster shell bank) seems to play an important role in microhabitat selection by Dendrodoris species, since all the other intertidal banks in the surrounding area—without oyster shells coverage and mostly constituted by mud substrate with little sand—never revealed any emerged specimens. From this, we argue that oyster shells must provide some crypsis by providing a disrupted visual background that might contribute to a reduction in visual predation. Also, this could mean that oyster shells protect nudibranchs from dehydration. However, the fact that most nudibranchs were not beneath the shells makes this microhabitat selection argument incomplete.
Horizontal migrations and spawning
There is a great diversity of theories that explain the sudden appearance and disappearance of nudibranchs in intertidal areas (as synthesized in Table 1). However, it is still unknown if these events are related with horizontal migrations, and what are the causes that motivate these movements. Some authors state that, as a result of these horizontal migrations, nudibranchs seasonally appear as mass aggregations in intertidal areas to mate and spawn [4, 6]. In our surveys, organisms were mostly seen isolated and no egg masses were seen in the study site. This way, it seems unlikely that the nudibranchs were in the study area to mate or to spawn. Nonetheless, the individuals that were brought to the laboratory immediately started to copulate and spawned, indicating that they were sexually mature. Thus, the hypothesis of a horizontal migration to intertidal areas to mate should not be set aside and further studies are necessary to clear this out.
The sudden disappearance of nudibranchs from intertidal areas has often been attributed to death after spawning [4, 6]. During our surveys, we did not observe dead individuals in the field or any evidence of death after spawning in the specimens kept in the laboratory, with some nudibranchs spawning more than once. This way, our results with Dendrodoris spp. do not support this hypothesis. However, and like other molluscs, death after spawning may be a species-specific trait. While a similar pattern was observed for Onchidoris bilamellata, a species that spawns several times before dying [29], other nudibranchs seem to experience death after spawning (e.g. Archidoris montereyensis, in [11]).
Environmental determinants
The abundance of D. herytra and D. grandiflora was correlated with most of the assessed environmental factors, namely water temperature, turbidity and dissolved oxygen. Our long-term survey consistently showed that both species appeared emerged during the low tides of the spring months. They started to appear in March and their abundance was highest between April and May, when water temperatures were generally between 17 and 21 °C (except for 2014, when it reached 24 °C). Both species completely disappear in July, before the high summer temperatures. A study conducted in the western Atlantic revealed that most nudibranchs have high thermal sensitivity and that some species disappear with rising summer temperatures [30]. A negative impact of high temperatures on D. herytra and D. grandiflora may in part explain their disappearance from the intertidal area at the end of the spring. Nevertheless, temperature alone cannot explain their presence only during spring, since no nudibranchs were observed at similar temperatures in autumn.
The presence of D. herytra and D. grandiflora in the intertidal area was consistently related with a peak in turbidity and dissolved oxygen. Elevated turbidity and oxygen super saturation (values exceeding 100%) can be related with spring blooms that result from an increase in phytoplankton biomass and photosynthesis during spring [31,32,33]. As a result, secondary productivity also increases, including zooplankton grazers [34], which benefits D. grandiflora’s planktotrophic larvae [22]. In addition, high turbidity and dissolved oxygen may be a result of turbulence which in turn will help the distribution of planktonic larvae in the water column [35]. This way, Dendrodoris planktonic life stages may benefit from increasing phytoplankton concentration. However, it is noteworthy that no sponges (the prey of the adults of Dendrodoris spp. [24]) were found in the study location during the 5 years of survey. It is also important to notice that elevated turbidity consistently preceded an increase in nudibranchs abundance (also accompanied by the peak of dissolved oxygen). Thus, we hypothesize that the increase in turbidity is the key environmental factor that triggers the migration of nudibranchs.
In conclusion, the present work constitutes an additional example of a nudibranch population that seasonally appears in intertidal areas, but the first comprehensive report of nudibranchs under tidal emersion. The sudden appearance and disappearance of Dendrodoris nudibranchs in intertidal areas may result from a seasonal horizontal movement of adult nudibranchs from subtidal areas to mate in intertidal areas during spring, when phytoplankton production is enhanced and planktotrophic larvae may benefit from greater food availability. However, further studies are required to test this hypothesis.