Miocene fossils from the southeastern Pacific shed light on the last radiation of marine crocodylians

Abstract

The evolution of crocodylians as sea dwellers remains obscure because living representatives are basically freshwater inhabitants and fossil evidence lacks crucial aspects about crocodylian occupation of marine ecosystems. New fossils from marine deposits of Peru reveal that crocodylians were habitual coastal residents of the southeastern Pacific (SEP) for approximately 14 million years within the Miocene (ca 19 to 5 Ma), an epoch including the highest global peak of marine crocodylian diversity. The assemblage of the SEP comprised two long and slender-snouted (longirostrine) taxa of the Gavialidae: the giant Piscogavialis and a new early diverging species, Sacacosuchus cordovai. Although living gavialids (Gavialis and Tomistoma) are freshwater forms, this remarkable fossil record and a suite of evolutionary morphological analyses reveal that the whole evolution of marine crocodylians pertained to the gavialids and their stem relatives (Gavialoidea). This adaptive radiation produced two longirostrine ecomorphs with dissimilar trophic roles in seawaters and involved multiple transmarine dispersals to South America and most landmasses. Marine gavialoids were shallow sea dwellers, and their Cenozoic diversification was influenced by the availability of coastal habitats. Soon after the richness peak of the Miocene, gavialoid crocodylians disappeared from the sea, probably as part of the marine megafauna extinction of the Pliocene.

Keywords: Gavialoidea; biogeography; longirostrine ecomorphs; marine crocodylians; phylogenetics.

Figure 1.

Fossil record of Sacacosuchus and Piscogavialis in the Neogene deposits of the Pisco Basin, southern Peru. (a) Schematic stratigraphic columns of the Chilcatay (yellow) and Pisco (light blue) formations with crocodylian-bearing localities at the Ica-Pisco Valleys (left; from ca 20 to 7 Ma) and the Sacaco area (from ca 9.6 to 4.85 Ma). (b) Location and map of the East Pisco basin showing the Chilcatay (yellow) and Pisco (blue) deposits within putative continental flooded areas (in white). Map modified from [30]. AGL, Aguada de Lomas; CCO-n, Cerro Colorado norte; CCO-s, Cerro Colorado sur; CLQ, Cerro Los Quesos; COM, Comatrana; CVT, Correviento; ELJ, EL Jahuay; MTM, Montemar; MTM-n, Montemar norte; MTM, Montemar; SAO-e, Sacaco east; SAS-w, Sud-Sacaco west; SUL, Sula Site; YAU, Yauca; ZAM, Zamaca. (Online version in colour.)

Figure 2.

Photograph and schematic drawing of the skulls of Sacacosuchus cordovai gen. et sp. nov. from Sacaco at different ontogenetic stages. Adult specimen (holotype: MUSM 162) in dorsal (a), ventral (b), right lateral (e) and occipital (f) views. Sub-adult specimen (MUSM 161) in dorsal (c), ventral (d), left lateral (g; inverted) and occipital (h) views. Juvenile specimen (MUSM 160) in dorsal (i) view. ba, basioccipital; bs, basisphenoid; CH, choana; cq, cranioquadrate foramen; ec, ectopterygoid; ec.mx, maxilla surface for ectopterygoid; EN, external naris; eo, exoccipital; f, frontal; fcp, foramen carotideum posterior; IF, incisive foramen; ITF, infratemporal fenestra; j, jugal; j.la, lacrimal surface for jugal; j.mx, maxilla surface for jugal; l, lacrimal; ls, laterosphenoid; m5, m9, m14, maxillary tooth positions; mx, maxilla; n.pm, premaxilla surface for nasal; na, nasal; OR, orbit; p, parietal; pa, palatine; pa.mx, maxilla surface for palatine; pf, prefrontal; pm, premaxilla; p3, p4, premaxillary tooth positions; po, postorbital; pt, pterygoid; q, quadrate; qj, quadratojugal; qj.q, quadrate surface for quadratojugal; s, shelf; so, supraoccipital; sq, squamosal; STF, supratemporal fenestra; SOF, suborbital fenestra; v, foramen vagus; xii, foramen for hypoglossal nerve. All photographs to the same scale. Scale bar equals 5 cm. (Online version in colour.)

Figure 3.

Phylogenetic position of Sacacosuchus cordovai and other marine taxa (represented by their skulls) recovered within and outside the Crocodylia, with ancestral range reconstructions provided by S-DIVA. (a) Time-calibrated, strict consensus tree on the constrained and equal-weighted analysis. Crocodylians found in marine deposits pertain to the gavialoid clade. The ancestral range reconstructions are summarized as pie charts and shown for critical nodes of the Gavialoidea (73: Eogavialis + Gavialis; 79: Gryposuchinae; 81: Aktiogavialis; 82: Argochampsa, Aktiogavialis, advanced gavialids; 83: ‘gharials’ + MUSM 1513; 86: Miocene African forms; 89: Thecachampsa; 90: Gavialosuchus, Sacacosuchus, Thecachampsa + unnamed node 87; 92: Gavialidae), Crocodylidae (99: node 97 + Crocodylus porosus); and ‘thoracosaurs’ (node 121). Geographical areas of distribution are represented by colours and capital letters. Wide bars within branches show stratigraphic range of taxa. Black triangles at the branches leading to Gryposuchus, Gavialis and Tomistoma schlegelii indicate major shifts from marine to freshwater habitats. Eocene palaeomap (b) is from Blackey [49].

Figure 4.

Diversity of crocodylians during the last 90 my. (a) Observed range-through (OR) diversity of crocodylian genera (OR bys: red dashed line), OR of marine (OR mg: blue solid line) and non-marine genera (OR n-mg: black solid line) calculated per chronostratigraphic stages. (b) Estimated richness based on the Chao1 extrapolation estimator calculated per chronostratigraphic stages (red dots) and second-order Jackknife richness estimator calculated using 3-million year time-bins for marine (mg: blue line) and non-marine (n-mg: black line) crocodylian genera. Grey solid line represents a smoothed global sea-level curve after Miller et al. [37] and the orange solid line a global mean temperature curve after Zachos et al. [34]. The time spam of the southeastern Pacific gavialid crocodylians record (SEP C) encompasses the estimated highest peak of genera and species of marine forms. PLI, Pliocene. (Online version in colour.)

Figure 5.

The pPCA of the snout of the Crocodylia defined by PC1 and PC2. Black dots denote non marine taxa and blue dots (with or without skulls) correspond to extinct taxa (gavialoids and Thoracosaurus) recovered from marginal to fully marine environments and the living saltwater crocodile, Crocodylus porosus. Positive values of PC1 depict forms with longirostrine ecomorphs. All gavialoids pertain to these ecomorphs but bearing large variation along positive and negatives values of PC2, with morphological ‘tomistomines’ restricted to the positive values and ‘gharials’ confined to the negative values. The sole ‘thoracosaur’ included in this analysis is positioned close to the ‘gharial’ ecomorph. Grey polygon encompasses the gavialoid morphospace and blue areas correspond to distinct ecomorphs of marine gavialoids within the morphological ‘tomistomines’ (upper) and ‘gharials’ (lower). (Online version in colour.)