Swimming and defence: competing needs across ontogeny in armoured fishes (Agonidae)

Abstract

Biological armours are potent model systems for understanding the complex series of competing demands on protective exoskeletons; after all, armoured organisms are the product of millions of years of refined engineering under the harshest conditions. Fishes are no strangers to armour, with various types of armour plating common to the 400–500 Myr of evolution in both jawed and jawless fishes. Here, we focus on the poachers (Agonidae), a family of armoured fishes native to temperate waters of the Pacific rim. We examined armour morphology, body stiffness and swimming performance in the northern spearnose poacher ( Agonopsis vulsa ) over ontogeny. As juveniles, these fishes make frequent nocturnal forays into the water column in search of food, while heavily armoured adults are bound to the benthos. Most armour dimensions and density increase with body length, as does body stiffness. Juvenile poachers have enlarged spines on their armour whereas adults invest more mineral in armour plate bases. Adults are stiffer and accelerate faster than juveniles with an anguilliform swimming mode. Subadults more closely approximate adults more than smaller juveniles, with regards to both swimming and armour mechanics. Poacher armour serves multiple functions over ontogeny, from facilitating locomotion, slowing sinking and providing defence.

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

“…However, stickleback armor imposes a far smaller penalty on both swimming speed and turning ability. When the armor fully encases the fish there are still informative nuances-the fully fused armor of a boxfish restricts body undulation, while the rail and channel system that connects the overlapping plates of a Northern Spearnose Poacher allows these fish to retain the ability to c-start (Kolmann, Peixoto, et al, 2020;Yang et al, 2015).…”

“…Spalling, or the removal of a section of surface, is also evidence of a shearing impact. These damage modes can be quantified across or among individuals and species by a close examination of the surface, either by scanning electron microscopy (SEM) or CT scanning (Kolmann, Peixoto, et al, 2020;Kolmann, Urban, & Summers, 2020;Kruppert et al, 2020). Intact armor subjected to known damage can then be visualized for ground truthing the results in field caught specimens.…”

How to Survive a (Juvenile) Piranha Attack: An Integrative Approach to Evaluating Predator Performance

“…Despite the early appearance of bony armors in vertebrates, armor has been lost, reduced, modified, and regained many times over 500 million years of evolution, making armor just one of the many axes of phenotypic variation defining the most diverse vertebrates, the bony fishes ( Sire et al. 2009 ; Kolmann et al. 2020b ; Gai et al.…”

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

“…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 ).…”