Regional endothermy as a trigger for gigantism in some extinct macropredatory sharks

Abstract

Otodontids include some of the largest macropredatory sharks that ever lived, the most extreme case being Otodus (Megaselachus) megalodon. The reasons underlying their gigantism, distribution patterns and extinction have been classically linked with climatic factors and the evolution, radiation and migrations of cetaceans during the Paleogene. However, most of these previous proposals are based on the idea of otodontids as ectothermic sharks regardless of the ecological, energetic and body size constraints that this implies. Interestingly, a few recent studies have suggested the possible existence of endothermy in these sharks thus opening the door to a series of new interpretations. Accordingly, this work proposes that regional endothermy was present in otodontids and some closely related taxa (cretoxyrhinids), playing an important role in the evolution of gigantism and in allowing an active mode of live. The existence of regional endothermy in these groups is supported here by three different approaches including isotopic-based approximations, swimming speed inferences and the application of a novel methodology for assessing energetic budget and cost of swimming in extinct taxa. In addition, this finding has wider implications. It calls into question some previous paleotemperature estimates based partially on these taxa, suggests that the existing hypothesis about the evolution of regional endothermy in fishes requires modification, and provides key evidence for understanding the evolution of gigantism in active macropredators.

Fig 1. Oxygen isotopic evidence and the effect of regional endothermic taxa in previous paleotemperature estimates.

(A-C) Difference in the δ¹⁸O value between coexisting cretoxyrhinids/otodontids and ectothermic taxa in several localities/sedimentary beds plotted against the ectothermic taxa δ¹⁸O value (as a proxy of seawater temperature). Three different regression analyses have been performed: (A) including all cretoxyrhinids-otodontids and all associated ectothermic taxa, (B) including all cretoxyrhinids-otodontids and only associated pelagic ectothermic taxa; and (C) including only cretoxyrhinids-otodontids and associated pelagic ectothermic taxa from Kocsis et al. [38] (regression lines are showed with associated 95% confidence intervals). Details of each fossil locality (denoted by numbers) are given in Table 1 and S1 Table. (D) Regression analyses performed in living lamnid sharks for comparative purposes, considering direct water and body temperature records compiled in Lowe and Goldman [25] (DM, deep muscle; ST, stomach). In all cases, slope values close to -1 imply that body temperature is independent from that of the water, slope values close to 0 imply a complete dependence, and intermediate slope values indicate some degree of independence. (E-F) Campanian-Maastrichtian latitudinal gradients of δ¹⁸O and seawater temperature calculated from cretoxyrhinids and ectothermic taxa. (G-H) Campanian-Maastrichtian δ¹⁸O and seawater temperature estimates calculated for three different latitudinal ranges (11°-13°, 20°-23° and 36°-49°), considering only cretoxyrhinids (pink), all taxa (black) and only ectothermic taxa (green). Significance of pairwise mean contrasts are shown in each case. Data in E-H taken from Puceat et al. [42]. ** indicates significance at the 0.05 level and * indicates significance at the 0.1 level.

Fig 2. Scaling of swimming speed in extant fishes and swimming speed inferences in cretoxyrhinids and otodontids.

(A) Cruise and (B) burst relative swimming speeds (U, body lengths*s^-1) against body lengths (meters) of living ectothermic and regional endothermic fishes. Adjusted regression lines are showed with associated 95% confidence intervals. (C) Cruise and (D) burst swimming speed estimates (V, km*h^-1) of cretoxyrhinids and otodontids, considering them as ectothermic sharks (green) or regional endothermic sharks (pink), with associated 95% individual prediction intervals. Values of absolute (V, km*h^-1) and relative (U, BL*s^-1) speed estimates are also shown for each case. ** indicates significance at the 0.05 level.

Fig 3. Aspect ratio estimates of Cretoxyrhina mantelli.

(A-B) Regression analyses between the aspect ratio (AR) and two different caudal fin variables (Ca, Cobb’s angle; HRa, hypochordal ray angle) of living lamniform sharks. Extrapolated position of Cretoxyrhina mantelli is denoted by a red dot. (C) Morphometric data for caudal fins (AR, Ca and HRa) of lamniform sharks including Cretoxyrhina mantelli. Caudal fin profiles modified from Kim et al. [50].

Fig 4

(A) Comparison between net cost of swimming (NCS) and routine metabolic rate (RMR) of Cretoxyrhina mantelli at five different temperature scenarios (5°C, 10°C, 15°C, 20°C and 25°C) assuming ectothermy (green) and regional endothermy (pink). Green and pink gradations represent the NCS at different swimming speeds (see color code chart). Note that NCS are constant in all temperature scenarios (see text). RMR estimate is represented with associated 95% individual prediction intervals (in black). (B) Validation test performed in 17 living sharks, including ectothermic taxa (green background) and regional endothermic taxa (pink background), from simultaneous records of their cruise swimming speeds, water temperatures and body masses (data taken from [85]). Inferred RMR are denoted as green and pink intervals for the ectothermic and regional endothermic scenario respectively; Inferred NCS are represented by black dots.

Fig 5. Possible evolutionary scenarios for the origin of regional endothermy in lamniforms considering (A) only extant lamniform groups, (B) Cretoxyrhina within alopids, and (C) Cretolamna representatives as ancestors of both lamnids and otodontids, and Cretoxyrhina within lamnids.

Stratigraphic ranges taken from [1].

Fig 6

(A) Diagram showing the relationship between body mass, metabolic rate (≈ activity level and feeding strategy) and metabolic level (ecto, meso and endothermy) in aquatic vertebrates. (B) Schematic explanation of how shifts towards higher metabolic levels, promoted by different factors, contribute to maintaining a predatory lifestyle at bigger body sizes. (C) Diversity of body masses, feeding and thermoregulatory strategies of living and extinct aquatic vertebrates (ed, endotherm; ec, ectotherm; me, mesotherm; cross sign denotes an extinct taxon). A-C modified from Ferrón et al. [11]. (D-E) Diagrams showing body sizes, feeding and thermoregulatory strategies of mysticete cetaceans and otodontid sharks respectively. Mysticete skull and otodontid tooth outlines modified from Fitzgerald [185] and Pimiento and Balk [46]. Bluish and reddish tones represent lower and higher metabolic levels, respectively.