Philippa Kaur

Theropod dinosaurs such as Tarbosaurus bataar grew large or small in a range of ways.Credit: Marco Ansaloni/SPL

A sweeping analysis of shin bones has given researchers a glimpse into how some dinosaurs evolved into mega-beasts such as Tyrannosaurus, and others into smaller, bird-like creatures. The work, published this week in Science1, reveals that dinosaurs used more than one evolutionary trick to become larger — or smaller — over time.Prevailing wisdom held that large-bodied animals are bigger than their smaller-bodied relatives because they grow faster during their most rapid period of growth. That trend holds true for modern animals including birds and mammals — elephants and ostriches grow faster than chihuahuas and sparrows, for example.It’s not the case for all animals. Crocodiles and alligators, for instance, become large because they grow for a long time. But palaeontologists had assumed that for theropod dinosaurs — a group that includes the iconic T. rex and which spawned modern birds — large species got big through rapid growth spurts. “It’s kind of become the established idea in dinosaurs,” says palaeontologist Michael D’Emic at Adelphi University in Garden City, New York.But that’s not what D’Emic found when he sawed into the bones of Majungasaurus, a 7-metre-long T. rex relative that lived 66 million years ago on what is now Madagascar. The speed of growth in dinosaurs is recorded in rings laid down each year in their bones. Instead of seeing wide rings corresponding to a rapid adolescent growth spurt, D’Emic found lots of narrow growth rings, suggesting that Majungasaurus had become large over a prolonged period.“I was very surprised,” he says. The next dinosaur he examined, a similar-sized beast called Ceratasaurus, was the opposite — a big dinosaur that grew fast during its growth spurt, says D’Emic.Bone growth ringsOver a decade, D’Emic and his colleagues amassed bone growth-ring measurements from 42 theropod species to see which strategies led to large and small bodies. They found that 31% of theropod species were larger than their ancestors because of faster growth and 28% because of prolonged growth. Meanwhile, 21% became smaller than their ancestors by shortening their growth spurts, and 19% by slowing growth.The study covered theropod species that lived between 230 million years ago and the end of the Cretaceous period 66 million years ago, when a mass-extinction event wiped out the non-avian dinosaurs. It’s “a huge evolutionary timescale”, to include in an analysis, says Vera Weisbecker, an evolutionary biologist at Flinders University in Adelaide, Australia. “That is really impressive,” she says. “It’s just fascinating that there are so many developmental ways to become big or small.”Palaeontologist Kevin Padian at the University of California, Berkeley, says the analysis is the kind of work that needs to be done, animal group by animal group, to understand how body size evolves.Drivers of changeBut Meike Köhler, an evolutionary palaeobiologist at the Catalan Institution for Research and Advanced Studies in Barcelona, Spain, says the findings are not surprising because previous work has shown a range of growth strategies across animal species. Köhler would like to see an analysis that considers what ecological circumstances influenced how animals changed in size over time.Weisbecker says that the growth strategy used might be related to evolutionary pressures. “If you looked at all the ones with explosive early growth, you might be able to test if they happen to be the ones that are more likely to be predated on, for example,” she says.For each species, the growth strategy that led to its individual body size probably related to its unique environment, says Padian. “It’s not a one-size-fits-all, which is a good thing for us to learn,” he says. “We might have thought that, but they’ve documented it.”D’Emic says he and his team are conducting similar analyses on other groups, including mammals — a group that contains many more species to sample — to see whether the diversity is found in other branches of the evolutionary tree. More

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These are located within four distinct marine biogeographic provinces and three realms (Tropical Atlantic, Central Indo-Pacific, and Temperate Australasia)43. At each location fish were collected using barrier nets, dip nets, clove oil or hook and line, and immediately transferred to aquaria facilities at the Cape Eleuthera Institute, Heron Island and Moreton Bay Research Stations, and the Palau International Coral Reef Center. Fish were held in a range of tanks (60, 400, or 1400 L in the Bahamas, 10, 60, 100, 120, or 400 L in Heron Island and Moreton Bay, and 8, 80, 280, or 400 L in Palau) of suitable dimensions for different fish sizes ( 5). Each sample was titrated with 0.01–0.5 N HCl (with continuous aeration with CO2-free air) until the end point (grey-lavender; pH~4.80) was reached and stable for at least 10 min. If the sample was over-titrated (pink), 0.01–0.1 N NaOH was added to titrate back to the end point and the amount of base used was subtracted from the amount of acid. Acid and base were added using an electronic multi-dispenser pipette (Eppendorf Repeater ®E3X, Eppendorf, Hamburg, Germany) with a precision of  ± 1 ({{{{{rm{mu }}}}}})L. Additionally, the pH of several samples was monitored using a pH microelectrode (Mettler Toledo InLab Micro) to ascertain the correctness of the colorimetric end point. The amount of carbonate in the sample was then calculated using Eq. (1). The method was validated using certified reference material (Alkalinity Standard Solution, 25,000 mg/L as CaCO3, HACH) and the accuracy in the determination of solid samples was verified using certified CaCO3 powder (Suprapur, ≥ 99.95% purity, Merck) samples (60–500 ({{{{{rm{mu }}}}}})g) and resulted in 96.53 ± 1.94% accuracy (mean ± SE; n = 8).To compare values obtained with the two titration methods we further analysed 12 samples collected at Lizard Island, Australia, in February 2016. Samples were collected at 24 h intervals from one individual of Lethrinus atkinsoni (f. Lethrinidae, body mass: 245 g), a group of five Lutjanus fulvus (f. Lutjanidae, mean body mass: 21 g), and an individual of Cephalopholis cyanostigma (f. Serranidae, body mass: 295 g), following the procedures described above. During sample collection water temperature ranged from 29.1 °C during the night to 32.6 °C during the day, with an average of ~31 °C, mean salinity was 35.4, and pHNBS ranged from 8.13 to 8.21. To compare the amount of carbonate measured by the two methods we added carbonate samples to 20 ml ultrapure water and disaggregated crystals via sonication. We then used a Metrohm Titrando autotitrator and Metrohm Aquatrode pH electrode to measure initial pH of the suspension of carbonates, then titrated each sample of carbonate in two stages. Firstly, they were titrated down to pH 4.80 using 0.1 M HCl, adding 20 µl increments of acid until this was sufficient to keep pH below 4.80 for 10 min whilst bubbling with CO2-free air. This first stage was comparable to the single end point titration used for samples collected in Palau. Secondly, whilst continuing to bubble with CO2-free air, further acid was added to the sample until it reached pH 3.89 and was stable for 1 min. Then 0.1 M NaOH was added to the samples to return them to the initial pH. For all samples the first end point titration (to pH 4.80) yielded slightly higher values for carbonate content than the second double titration. The ratio between the two methods (single end point/double titration) was 1.08 ± 0.01 (mean ± SE; range: 1.04–1.14; Supplementary Table 2). As we found a small but consistent difference between the two methods, all following analyses were initially performed on the actual data obtained with the double titration for samples from Australia and The Bahamas, and the single end point titration for samples from Palau. Then, to assess the robustness of the results, we repeated the analyses after applying a correction factor of 1.08 to the excretion rates of Palauan fishes (that used the single end point titration method). All results were consistent and robust to the measured difference between the titration methods (Supplementary Figs. 8, 9).Finally, measurements of multiple samples from each individual collected over periods of 18–169 h (median: 64 h) were combined to produce an average individual excretion rate in ({{{{{rm{mu }}}}}})mol h−1. For fish held in groups, carbonate excretion rates per individual (of average biomass) were obtained by averaging the total excretion rate of the group across the sampling period and dividing it by the number of individuals in the tank. Excretion rates obtained from fish groups thus evened the intraspecific variability within tanks, and are therefore more robust than those directly obtained from fish held individually. This aspect was considered in our models by fitting weighted regressions (see the “Statistical modelling” section). In total, we measured the carbonate excretion rates of 382 individual fishes arranged in 192 groups (i.e., independent observations), representing 85 species from 35 families across three tropical regions (180 individuals from 29 species in Australia, 90 individuals from 10 species in the Bahamas, and 112 individuals from 46 species in Palau; Supplementary Table 1).We assume that during the sampling of carbonates fishes were close to their resting metabolic rate and that their carbonate excretion rates are representative of fish at rest. Although the ratio of tank volume to fish volume in our study (median ~660; inter-quartile range ~180–1700) typically greatly exceeds the guideline ideal range for measuring resting metabolic rate (20–50)85, fishes were fasted prior to and throughout sampling, and in most instances their movement was somewhat constrained by tank volume. 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