Every hooked beak is maintained by a prey: Ecological signal in cephalopod beak shape

Abstract

1. Beaks are among the few hard parts of coleoid cephalopods and are informative for species identification. Although mandible shape has been shown to be adaptive in many vertebrate taxa, it has been suggested that the shape of coleoid beaks does not bear any ecological signal. Yet, previous studies only explored beak shape in 2D and none have provided an in-depth investigation of the potential relationship with ecological variables such as habitat use or diet.2. The goal of the present study was to understand whether variation in cephalopod beak shape reflects ecology and/or is more driven by phylogenetic relatedness as suggested previously.3. We imaged 101 lower and 108 upper beaks in 3D using underwater photogrammetry and micro-CT scanning. Our 3D morphometric analysis conducted on 75 species of cephalopod shows that there is a significant but moderate phylogenetic signal. However, comparative phylogenetically informed analyses demonstrate that beak shape is also driven by ecology.4. We detected significant differences in beak shape between species inhabiting different habitats (pelagic, benthic or demersal) and of different trophic levels.Our results further suggest that beak shape variation can be summarized along a continuum between two main functions: fast closing versus hard biting.5. These results provide novel insights into the drivers of beak shape diversity in coleoid cephalopods and suggest that beak shape has evolved adaptively in relation to diet and habitat use.

The significance of cephalopod beaks as a research tool: An update

“…Specifically, Fernández-Álvarez et al (2020) studied impacts of developmental malformations of the buccal mass on the trophic position of Eledone cirrhosa and found that the habitat and the trophic position were not significantly affected by the malformations. Other authors found significant differences in the beak shapes of pelagic and benthic species in relation to their trophic levels (Roscian et al, 2022), between species living in coastal and oceanic habitats (Pacheco-Ovando et al, 2021) and between species/populations living in different feeding habitats (Pacheco-Ovando et al, 2021). New phylogenomic techniques applied to cephalopods (Anderson and Lindgren, 2021;Sanchez et al, 2021;Fernández-Álvarez et al, 2022) may help to assess which morphological characters of the beaks are determined by phylogeny and which are explained by other drivers.…”

“…Several studies revealed the potential of beak shape analysis in ecological studies (Fernández-Álvarez et al, 2020;Pacheco-Ovando et al, 2021;Roscian et al, 2022). Specifically, Fernández-Álvarez et al (2020) studied impacts of developmental malformations of the buccal mass on the trophic position of Eledone cirrhosa and found that the habitat and the trophic position were not significantly affected by the malformations.…”

“…Some authors used 2-D images of the beak's lateral view (Fang et al, 2017;Jin et al, 2017;Tan et al, 2021), others used a complex system of mirrors to obtain combined 2-D images of frontal and lateral views (Crespi-Abril et al, 2010), and others used a combination of underwater photogrammetry and CT scanning to obtain 3-D images of beaks (Roscian et al, 2022). As results of studies based on 2-D images suggest, this is enough for routine identification of abundant species (Tan et al, 2021), although in-depth ecological, paleontological, or taxonomic studies may demand more complex method (Roscian et al, 2022). We argue that the use of beaks for identification purposes demands a simple approach, which can be adopted both in the field and in the laboratory.…”

“…Further studies on a large number of taxa, testing the phylogenetic signal carried by beak shape will be necessary to establish the level of accuracy that could be achieved in identification. Moreover, as 3-D reconstruction is timeconsuming and more complex than 2-D analyses, recent work using 3-D geometric morphometrics, which allows the complexity of beak shape to be better captured, has shown that the phylogenetic signal of upper and lower beaks is significant but moderate and that it cannot explain all the morphological variation in beaks on its own (Roscian et al, 2022). On the other hand, cephalopod beaks remain complex to image in three dimensions without damaging them.…”

“…On the other hand, cephalopod beaks remain complex to image in three dimensions without damaging them. The use and improvement of advanced imaging technologies such as X-ray tomography and underwater photogrammetry on small objects will allow most species to be digitized (Roscian et al, 2021;Ziegler and Sagorny, 2021;Roscian et al, 2022). Nevertheless, the digitization of specimens is a long task and the accumulation and accessibility of the data to the community is a major challenge in achieving a comprehensive sampling of cephalopod 3-D model beaks.…”