Living in the subterranean time: exploring biological rhythms in cave invertebrates

Abstract

The manuscripts presented in this dissertation emerged from the need to expand knowledge regarding existing gaps in the field of chronobiology in caves, especially concerning invertebrates, which exhibit a diversity of morphologies, physiologies, and behaviors associated with different levels of adaptation to these cyclic environments. In this context, these ecosystems are characterized by low abiotic variability and the absence of clear-dark cycles. Consequently, organisms manifest their biological rhythms in diverse ways individually and among different taxa, without presenting a clear pattern among the ecological-evolutionary categories that compose cave fauna. This perception served as the basis for the hypotheses investigated in the second and third manuscripts. The general objective of this dissertation was not only to understand the manifestation of biological rhythms in cave invertebrate fauna but also to understand how these rhythms may vary among different taxonomic classes. The literature highlights the adaptation of the biological clock in underground natural cavities, where factors such as light, temperature, and food play a

significant role in regulating biological rhythms. Studies demonstrate the evolution of non- circadian clocks due to the absence of diurnal cycles, resulting in infradian or ultradian cycles.

Despite the progress made, there are still gaps to be explored in research on the rhythmicity of invertebrates in underground environments. The first manuscript, a review article, focused on four main questions: (i) the most studied geographic regions regarding the chronobiology of cave invertebrates, (ii) the most frequently studied taxa, (iii) the evolutionary characteristics

of documented taxa, and (iv) the manifestation of rhythmic behavior of invertebrates in cycle- less environments and its correlation with functional morphology. The second manuscript

emerged from a gap in research on the rhythmic behavior of isopods in underground ecosystems, emphasizing the importance of investigating this little-explored group regarding patterns of locomotor activity. In this context, the research focused on the possibility of losing rhythmic elements due to convergent evolution in underground environments. The hypothesis was formulated that different species of obligatory semiaquatic isopods present aperiodic patterns in their locomotor activity due to the lack of light cycles in caves and thermal variability, crucial factors for the regulation of biological rhythms. The results indicated synchronization of the circadian rhythm within the LD treatment, albeit without clearly defined patterns under constant light and darkness conditions. The third manuscript arose from the gap in chronobiological studies involving amblypygids and investigated possible differences in rhythmic patterns between troglophile species (capable of establishing populations both inside and outside caves) and troglobite species (obligatorily confined to caves). Variability in rhythmic behavior was identified, but there were no significant differences between groups or species; the distinctions were individual. These findings underline the need to expand research on rhythmicity in caves, encompassing more geographical areas and taxonomic groups. It is crucial to investigate biological rhythms to understand subterranean adaptations, especially in the face of threats like climate change and habitat loss, contributing to conservation and advancing the ecological and evolutionary understanding of these environments.