Pacific Spiny Lumpsucker armor—Development, damage, and defense in the intertidal

Abstract

Predation, combat, and the slings and arrows of an abrasive and high impact environment, represent just some of the biotic and abiotic stressors that fishes are armored against. The Pacific Spiny Lumpsucker (Eumicrotremus orbis) found in the subtidal of the Northern Pacific Ocean is a rotund fish covered with epidermal, cone-shaped, enamel odontodes. The Lumpsucker is a poor swimmer in the wave swept rocky intertidal, and this armor may be a lightweight solution to the problem of collisions with abiotic obstacles. We use micro-CT and scanning electron microscopy to reveal the morphology and ontogeny of the armor, and to quantify the amount of mineralization relative to the endoskeleton. The non-overlapping odontodes are organized into eight rows-six rows on the body, one row surrounding the eye, and one row underneath the chin. Odontodes start as a single, hooked cone; and they grow by the addition of cusps that accrete into a spiral. The mineral investment in armor compared to skeleton increases over ontogeny.Damage to the armor occurs both through passive abrasion and breakage from impact; and there is no evidence of replacement, or repair of damaged odontodes.

Ontogeny of a tessellated surface: Carapace growth of the longhorn cowfish Lactoria cornuta

“…Instead of individual scutes becoming relatively more massive with age, as with lumpsucker odontodes (Woodruff et al, 2022), the comparatively thicker-walled scutes of younger cowfish become wider but relatively thinner in adults (although, in an absolute sense, more than 2× as thick as scutes of the youngest animals in our study). The relative thinning of scutes is comparable to the tessellated cartilage of stingrays, where the tesserae that form the tiled crust of the skeleton grow more rapidly in width than thickness, resulting in a comparative thinning of the skeletal cortex as animals age (Dean et al, 2009).…”

“…This is accomplished by a constant relative elongation of the body along the anteroposterior axis and relative lateromedial narrowing, as indicated, respectively, by the strong positive allometric scaling of carapace length as well as negative allometric scaling of carapace height, and the negative allometric scaling of body width relative to surface area (Figure 3 ). This carapace growth is not accomplished by the addition of new scutes, as in the armor of the Pacific spiny lumpsucker, where smaller odontodes arise in gaps between larger ones (Woodruff et al, 2022 ). Rather, cowfish armors, like the keratinous scutes of turtle shells (Alibardi, 2005 ; Wyneken et al, 2007 ), establish a set number of scutes early in life (~370 on average) and those scutes are then enlarged during ontogeny.…”

“…Tessellations are common natural geometric architectures, involving arrays of hard geometric elements (tiles), often linked by softer connecting tissues (Fratzl et al, 2016 ). The diverse tessellations of vertebrate animals typically comprise mineralized (carbonated apatite‐based) tiles with collagenous links, as in the armored cartilage of sharks and rays (Dean et al, 2009 ; Seidel et al, 2016 ), armadillo osteoderms (Chen et al, 2011 ), turtle shells (Chen et al, 2015 ; Magwene & Socha, 2013 ), and the armors of many fishes (Kolmann et al, 2020 ; Woodruff et al, 2022 ; Yang et al, 2015 ). Tessellations can also provide fundamental structuring at far finer scale, as with mineralization foci (tesselles, ~2 μm long) in developing bone, which pack together in multilayered 3D formations to structure skeletal tissue (McKee et al, 2022 ).…”

“…Among the tens of thousands of bony and cartilaginous fish species, external body armors, and scalations are common, but structurally diverse. However, except in some heavily‐armored species with interlocking armors (e.g., bichir, gar, seahorses; Bruet et al, 2008 ; Porter et al, 2013 ; Yang, Gludovatz, et al, 2013a ), fish scales, and scutes tend to be embedded in the skin quite separate from one another, with varying degrees of overlap (as in most fishes; Meyer & Seegers, 2012 ; Kolmann et al, 2020 ; Wainwright et al, 2018 ) or none at all (e.g., as in lumpsuckers; Woodruff et al, 2022 ). Whereas such overlapping or gapped armors allow a combination of flexibility and protection (e.g., Bruet et al, 2008 ; Lin et al, 2011 ; Vernerey & Barthelat, 2014 ; Yang, Gludovatz, et al, 2013a ), as well as ready room for interstitial growth, the mineralized scutes of boxfish abut at their edges via jagged sutures, forming a relatively rigid encasement (Besseau & Bouligand, 1998 ; Naleway et al 2016 ; Yang, Chen, et al, 2013b ; Yang et al, 2015 ; Zhu et al, 2012 ).…”

Ladies in armor: A micro‐computed tomographic study of skin calcification in European toads (genus Bufo)

“…This approach is especially useful to study well ossified bones (Waltenberger et al, 2021), including the B. bufo and B. spinosus cranial skeleton (Ivanović et al, 2022). Other dense dermal structures such as osteoderms (Broeckhoven et al, 2017; Paluh et al, 2017; Broeckhoven and du Plessis, 2018; Williams et al, 2022) and epidermal enamel structures (Woodruff et al, 2022) can also be explored with high precision while the material is kept intact. To further investigate skin structures that are visible on the micro‐CT scans, we used traditional histology.…”