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Piranha Predation Could Not Have Driven the Evolution of Arapaima gigas Scales

2020; Elsevier BV; Volume: 3; Issue: 6 Linguagem: Inglês

10.1016/j.matt.2020.10.028

2590-2393

Steve Huskey, Mark W. Westneat, Justin R. Grubich,

Paleontology and Evolutionary Biology

Over the last decade, several researchers have perpetuated the notion that the large Amazonian fish Arapaima gigas evolved specialized, calcium-deficient, hydroxyapatite scales to resist piranha predation.1Lin Y.S. Wei C.T. Olevsky E.A. Meyers M.A. Mechanical properties and the laminate structure of Arapaima gigas scales.J. Mech. Behav. Biomed. Mater. 2011; 4: 1145-1156Crossref PubMed Scopus (116) Google Scholar, 2Meyers M.A. Lin Y.S. Olevsky E.A. Chen P.Y. Battle in the Amazon: Arapaima versus piranha.Adv. Eng. Mater. 2012; 14: B279-B288Crossref Scopus (84) Google Scholar, 3Zimmermann E.A. Gludovatz B. Schaible E. Dave N.K. Yang W. Meyers M.A. Ritchie R.O. Mechanical adaptability of the Bouligand-type structure in natural dermal armour.Nat. Commun. 2013; 4: 2634Crossref PubMed Scopus (181) Google Scholar, 4Sherman V.R. Quan H. Yang W. Ritchie R.O. Meyers M.A. A comparative study of piscine defense: The scales of Arapaima gigas, Latimeria chalumnae and Atractosteus spatula.J. Mech. Behav. Biomed. Mater. 2017; 73: 1-16Crossref PubMed Scopus (33) Google Scholar, 5Yang W. Quan H. Meyers M.A. Ritchie R.O. Arapaima fish scale: One of the toughest flexible biological materials.Matter. 2019; 1: 1557-1566Abstract Full Text Full Text PDF Scopus (11) Google Scholar The primary aim of these publications has been to test the material properties of the fish scales, but each has made the assertion that the large, hard scales of Arapaima evolved in response to or are currently specialized for resistance to predation by piranhas where the two coexist within the Amazon Basin. There is no scientific support for this claim, as revealed by numerous evolutionary, ecological, and biomechanical lines of evidence, including: (1) phylogenetic history, (2) diet analyses, (3) jaw biomechanics, (4) feeding behavior of piranhas, (5) in vivo bite force, and (6) known present-day Amazonian food web dynamics and prehistoric predator-prey interactions. Lin et al.1Lin Y.S. Wei C.T. Olevsky E.A. Meyers M.A. Mechanical properties and the laminate structure of Arapaima gigas scales.J. Mech. Behav. Biomed. Mater. 2011; 4: 1145-1156Crossref PubMed Scopus (116) Google Scholar made first mention of piranha predation as the driving force behind the evolution of Arapaima scales. One year earlier, Currey6Currey J.D. Mechanical properties and adaptations of some less familiar bony tissues.J. Mech. Behav. Biomed. Mater. 2010; 3: 357-372Crossref PubMed Scopus (56) Google Scholar suggested Arapaima scales "make them effectively immune to attack," and cited Torres et al.7Torres F.G. Troncoso O.P. Nakamatsu J. Grande C.J. Gomez C.M. Characterization of the nanocomposite laminate structure occurring in fish scales from Arapaima gigas.Mater. Sci. Eng. C. 2008; 28: 1276-1283Crossref Scopus (73) Google Scholar in his summation, but never once mentioned piranhas. Torres et al.,7Torres F.G. Troncoso O.P. Nakamatsu J. Grande C.J. Gomez C.M. Characterization of the nanocomposite laminate structure occurring in fish scales from Arapaima gigas.Mater. Sci. Eng. C. 2008; 28: 1276-1283Crossref Scopus (73) Google Scholar likewise, provided a thorough description of the mechanical properties of Arapaima scales without ever implicating piranhas as the reason for their evolution. Lin et al.1Lin Y.S. Wei C.T. Olevsky E.A. Meyers M.A. Mechanical properties and the laminate structure of Arapaima gigas scales.J. Mech. Behav. Biomed. Mater. 2011; 4: 1145-1156Crossref PubMed Scopus (116) Google Scholar were the first to make such a claim. In fact, Lin et al.1Lin Y.S. Wei C.T. Olevsky E.A. Meyers M.A. Mechanical properties and the laminate structure of Arapaima gigas scales.J. Mech. Behav. Biomed. Mater. 2011; 4: 1145-1156Crossref PubMed Scopus (116) Google Scholar incorrectly cite Currey6Currey J.D. Mechanical properties and adaptations of some less familiar bony tissues.J. Mech. Behav. Biomed. Mater. 2010; 3: 357-372Crossref PubMed Scopus (56) Google Scholar as having "proposed that the scales of Arapaima serve as an armor-like protection against the sharp piranha teeth." Currey6Currey J.D. Mechanical properties and adaptations of some less familiar bony tissues.J. Mech. Behav. Biomed. Mater. 2010; 3: 357-372Crossref PubMed Scopus (56) Google Scholar never makes such a claim about piranha predation in his work (see Currey6Currey J.D. Mechanical properties and adaptations of some less familiar bony tissues.J. Mech. Behav. Biomed. Mater. 2010; 3: 357-372Crossref PubMed Scopus (56) Google Scholar). Here, we present evidence from phylogenetics, ecology, behavior, and our own work measuring piranha jaw morphology and in vivo bite forces of piranhas in the wild to refute the idea that piranhas have affected the evolution of Arapaima gigas scale morphology or function. The evidence supports the opposite hypothesis, that piranha predation has had a negligible effect on Arapaima scale evolution or function. The claim that the armored scales of Arapaima gigas evolved in response to piranha predation (first made by Lin et al.1Lin Y.S. Wei C.T. Olevsky E.A. Meyers M.A. Mechanical properties and the laminate structure of Arapaima gigas scales.J. Mech. Behav. Biomed. Mater. 2011; 4: 1145-1156Crossref PubMed Scopus (116) Google Scholar and repeated by Meyers et al.,2Meyers M.A. Lin Y.S. Olevsky E.A. Chen P.Y. Battle in the Amazon: Arapaima versus piranha.Adv. Eng. Mater. 2012; 14: B279-B288Crossref Scopus (84) Google Scholar Zimmerman et al.,3Zimmermann E.A. Gludovatz B. Schaible E. Dave N.K. Yang W. Meyers M.A. Ritchie R.O. Mechanical adaptability of the Bouligand-type structure in natural dermal armour.Nat. Commun. 2013; 4: 2634Crossref PubMed Scopus (181) Google Scholar Sherman et al.,4Sherman V.R. Quan H. Yang W. Ritchie R.O. Meyers M.A. A comparative study of piscine defense: The scales of Arapaima gigas, Latimeria chalumnae and Atractosteus spatula.J. Mech. Behav. Biomed. Mater. 2017; 73: 1-16Crossref PubMed Scopus (33) Google Scholar and Yang et al.5Yang W. Quan H. Meyers M.A. Ritchie R.O. Arapaima fish scale: One of the toughest flexible biological materials.Matter. 2019; 1: 1557-1566Abstract Full Text Full Text PDF Scopus (11) Google Scholar) is firmly rejected by the phylogenetic history of these groups of fish. The osteoglossids (arowanas) and arapaimids (bony tongues) split from other osteoglossomorph lineages in the mid-Cretaceous, between 140–100 million years ago (mya).8Hilton E.J. Lavoué S. A review of the systematic biology of fossil and living bony-tongue fishes, Osteoglossomorpha (Actinopterygii: Teleostei).Neotrop. Ichthyol. 2018; 16Crossref Scopus (21) Google Scholar These fish, both fossil and living, are all heavily armored, with the Neotropical Arapaima sharing a sister-group relationship with the heavily armored Heterotis of Africa and their minimum age of divergence being 54 million years ago.8Hilton E.J. Lavoué S. A review of the systematic biology of fossil and living bony-tongue fishes, Osteoglossomorpha (Actinopterygii: Teleostei).Neotrop. Ichthyol. 2018; 16Crossref Scopus (21) Google Scholar Thus, the general osteoglossomorph armor evolved over 100 mya, and the specific armored morphology of Arapaima gigas evolved at least 54 mya. Piranhas did not exist until greater than 30 million years later, and fossil time-calibrated phylogenies reveal that the predatory serrasalmine piranhas (Pygocentrus and Serrasalmus) originated approximately 20 mya. The earliest carnivorous piranha tooth in the fossil record is 16.5 million years old.9Lundberg J.G. Fishes of the Miocene La Venta Fauna: additional taxa and their biotic and paleoenvironmental implications.in: Kay R.F. Madden R.H. Cifelli R.L. Flynn J.J. Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, DC1997: 67-91Google Scholar Thus, it is temporally impossible for Arapaima, or any other living osteoglossomorph fish species, to have had their dermal armor evolution influenced by piranhas. Arapaima scales evolved tens of millions of years before piranhas even existed, so any claim of co-evolution is baseless. The major predators of large freshwater fish during the early origins of osteoglossomorph armor were mosasaurs and crocodylians, with the diversification of caimans temporally aligning with armored scale evolution and predation of Arapaima by caimans continuing today. Surprisingly, Sherman et al.4Sherman V.R. Quan H. Yang W. Ritchie R.O. Meyers M.A. A comparative study of piscine defense: The scales of Arapaima gigas, Latimeria chalumnae and Atractosteus spatula.J. Mech. Behav. Biomed. Mater. 2017; 73: 1-16Crossref PubMed Scopus (33) Google Scholar even attribute the evolution of ganoid scales in alligator gar to predation by American alligators, yet do not recognize the ecological similarity to assign Arapaima elasmoid scale evolution to predation by caimans, choosing the diminutive piranha instead. With the exception of Catoprion mento and Pygopristis denticulata, both scale-eaters, all other piranhas are carnivores. Piranhas predate mainly other fish, and predominantly the fins of other fish, while also being opportunistic on insects, other small vertebrates, and plant matter.10Winemiller K.O. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan Llanos.Environ. Biol. Fishes. 1989; 26: 177-199Crossref Scopus (283) Google Scholar The hyperbole around their consumption of entire capybaras, deer, or cattle are founded in the glorification of a few poorly presented stories that lack scientific integrity. Unprovoked attacks on humans, or any other large animals, are extremely rare because piranhas tend to focus their energy on the fins of conspecifics and the weak and injured fish among them. In the numerous feeding studies conducted on piranhas, nearly every type of prey was identified as a relatively small-bodied organism or, more commonly, a fin from a comparable-sized individual. Winemiller10Winemiller K.O. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan Llanos.Environ. Biol. Fishes. 1989; 26: 177-199Crossref Scopus (283) Google Scholar quantified the ontogenetic diet shifts of four piranha species (Pygocentrus notatus, Serrasalmus irritans, S. medini, and S. rhombeus) and found that subadults and adults of these species focused the majority of their efforts on clipping fins or consuming whole fish that did not require biting (see Figure S1). Pygocentrus notatus will gouge fleshy bites out of smaller fish; however, Figure S1 highlights the reduced gape of piranha species revealing the shallow angle of attack by their teeth that prevents biting prey or sections of prey larger than can fit between their jaws. Thus, piranhas are gape-limited predators that predominantly feed by fin-clipping and serrating other smaller, whole-fish components. Large-girth prey are not targeted for anything other than their fins, which undoubtedly excludes Arapaima from predation by piranhas. Gape-limitation is a phenomenon whereby prey attain sizes that exclude them from predation because the predator has a limited oral jaw gape. Piranha jaws are hypertrophied to accommodate the large forces their jaw muscles can produce (e.g., for clipping fins made primarily of bony components—spines and rays). To facilitate the transmission of large bite forces, the piranha upper jaw is fused to the skull and demonstrates no rotation or protrusion. The lower jaw has a limited range of motion because of its robust size. These upper and lower jaw characteristics result in gape-limitation in virtually all piranha species. As such, piranhas focus their feeding tendencies on clipping easily accessible fins of cohorts or on prey small enough to be swallowed whole. When they do require biting to excise a chunk of flesh, their strongest bite force occurs as the jaws are nearly occluded and the teeth from opposing jaws are directed toward each other. That is, at its maximum gape, which would be required to attack an Arapaima, the jaws translate substantially weaker bite forces to the teeth (i.e., < 10% of maximum bite force; S. rhombeus unpublished data n = 611MandibLever: a computational model of jaw biomechanics (Westneat, 2003). Version 4.0 released 12/10/2018.https://github.com/mwestneat/MandibLever2018Google Scholar). Bite force in piranhas increases exponentially as the mechanical advantage of the lower jaw and adductor muscle complex increases during jaw closure. Thus, piranhas only begin to maximize force when their jaws have closed 50% of maximum gape to best transfer muscle forces into effective biting.11MandibLever: a computational model of jaw biomechanics (Westneat, 2003). Version 4.0 released 12/10/2018.https://github.com/mwestneat/MandibLever2018Google Scholar This effectively eliminates large-circumference prey, like Arapaima, from being bitten. Grubich et al.12Grubich J.R. Huskey S. Crofts S. Orti G. Porto J. Mega-Bites: extreme jaw forces of living and extinct piranhas (Serrasalmidae).Sci. Rep. 2012; 2: 1009Crossref PubMed Scopus (32) Google Scholar were the first to document in vivo bite forces of live, wild-caught piranhas. Our results produced realized bite forces of 320 N for adult black piranhas up to 37 cm total length. Although the short, robust jaws of a fish this size are extremely powerful, a piranha this size would only have a maximum gape of approximately 3.5–4 cm. With this limited gape, the largest piranhas are only able to get their jaws around an object approximately the size of a golf ball and could only effectively attempt to attack an object the circumference of a softball because of the minimal angle of attack of their teeth (see Figures S1A and S1B). However, at this maximum gape, the aforementioned 37 cm black piranha would only generate approximately 24 N of bite force,11MandibLever: a computational model of jaw biomechanics (Westneat, 2003). Version 4.0 released 12/10/2018.https://github.com/mwestneat/MandibLever2018Google Scholar which is barely half of the force used in previous compression tests on Arapaima scales (e.g., 45 N3Zimmermann E.A. Gludovatz B. Schaible E. Dave N.K. Yang W. Meyers M.A. Ritchie R.O. Mechanical adaptability of the Bouligand-type structure in natural dermal armour.Nat. Commun. 2013; 4: 2634Crossref PubMed Scopus (181) Google Scholar). Given the large circumference of Arapaima and the trivial forces produced by piranhas with their mouths open wide, no piranha would even attempt at attack on the body of an Arapaima. Arapaima gigas are known to provide parental care for their offspring for at least 20 days after hatch, whereas fry grow up to approximately 12 cm because, at this size, they are easy prey for many predatory species, including piranhas. Arapaima scales, at this age and size, would be completely useless against piranha predation. Adult piranhas are known to bite with forces greater than 320 N,12Grubich J.R. Huskey S. Crofts S. Orti G. Porto J. Mega-Bites: extreme jaw forces of living and extinct piranhas (Serrasalmidae).Sci. Rep. 2012; 2: 1009Crossref PubMed Scopus (32) Google Scholar well above the compressive resistance of juvenile Arapaima scales. Piranhas bite only what they can fit in their mouths (e.g., relatively small-circumference organisms or appendages like fins) and their teeth work as one cohesive unit with all teeth fused to the upper and lower jaw bones (i.e., premaxilla and dentary, respectively) and to each other along their lateral edges to function as a saw-like blade. The aggressive lateral head-shaking behavior exhibited by piranhas facilitates their fused, serrated teeth into acting as an oscillating carving knife. As such, juvenile Arapaima that fit between the jaws of piranhas would receive relatively little protection from their specialized scales. If Arapaima scales are being maintained in response to predation by sympatric piranhas then the scales should exhibit a reverse-ontogenetic pattern with the most robust scales occurring in juveniles, when they can fit between the jaws of gape-limited piranhas, and less functional scales beyond year 1. Arapaima are capable of reaching 50 cm total length in 3 months and 67–88 cm total length within their first year (Figure S1C). At this size, they are no longer at risk of predation by even the largest piranha species because piranhas cannot open their mouths wide enough to get purchase on an Arapaima of this girth (Figure S1D). Arapaima can live up to a decade, maybe longer, and can reach lengths of nearly 3 m. This suggests they exhibit extremely fast growth and, in so doing, they quickly (within 6 months) move beyond the gape limitations of piranhas and thus are not bitten for anything other than their fins. In closing, although the results of the tenacity and durability of Arapaima scales might be intriguing for their unique structural qualities and biomechanical traits, their evolutionary origin as well as the ecomorphological limitation of piranha jaws make any inferences about co-evolution or adaptation linking these two species spurious and unfounded. Download .pdf (.27 MB) Help with pdf files Document S1. Figure S1 Arapaima Fish Scale: One of the Toughest Flexible Biological MaterialsYang et al.MatterOctober 16, 2019In BriefMany fish scales are efficient natural dermal armors that protect fish from predators without impeding their flexibility; therefore, mimicking their design in synthetic materials may lead to improved lightweight armor. The scales of arapaima fish are particularly effective because they enable its survival in piranha-infested waters. With a highly mineralized outer layer to resist penetration and a tougher lower layer with a twisted arrangement of mineralized collagen fibrils to absorb deformation, these scales are one of nature's toughest flexible materials. Full-Text PDF Open Archive