Rethinking holotypes: how environmental silicon shapes sponge skeletons and their taxonomic interpretation

Abstract

Routine taxonomic identification of sponges (phylum Porifera) relies largely on skeletal features and, despite the development of molecular markers, the skeletal approach persists because of its practicality. However, skeletal variability of uncertain origin often complicates species-level diagnoses. Using three common Mediterranean siliceous sponges, we experimentally demonstrate that environmental concentrations of silicic acid (dSi)—the raw material used by sponges for skeleton formation—is a major driver of skeletal diversity, significantly influencing the diversity of skeletal elements (spicules) produced and their dimensions. Most wild individuals of these three demosponges exhibit underdeveloped spicule inventories in their natural habitats, which are characterized by low dSi concentrations (∼1 µM). When transferred to laboratory conditions with experimentally elevated environmental dSi (up to 100 µM), sponges develop more complex spicule inventories. The experimentally induced skeletal differences are so pronounced that low-dSi and high-dSi conspecifics could easily be misidentified as different species in skeletal-based studies. The findings further suggest that shallow-water siliceous demosponges, systematically outcompeted by diatoms in terms of dSi uptake, frequently encounter dSi concentrations in their habitats below the threshold required for full skeleton development. Importantly, this effect extends to museum-stored holotypes. Holotypes originating from sites with unusually high dSi relative to the mean across the species’ distribution range are likely to produce fully developed skeletons that do not match the naturally underdeveloped skeletons prevailing in most conspecifics. Conversely, holotypes from habitats with average dSi concentrations across the species’ natural distribution range (typically low dSi) will more accurately represent the skeleton found in most individuals, although this skeleton will probably correspond to an underdeveloped version of the species’ full skeletal potential. Sponge biologists need to rethink the way in which sponge species are represented by their holotypes and how holotype skeletal traits can be better used for species’ diagnosis. Holotype studies should be systematically contextualized through assessment of dSi concentrations at the type locality and across the species’ distribution ranges.