The diet of early birds based on modern and fossil evidence and a new framework for its reconstruction

Abstract

Birds are some of the most diverse organisms on Earth, with species inhabiting a wide variety of niches across every major biome. As such, birds are vital to our understanding of modern ecosystems. Unfortunately, our understanding of the evolutionary history of modern ecosystems is hampered by knowledge gaps in the origin of modern bird diversity and ecosystem ecology. A crucial part of addressing these shortcomings is improving our understanding of the earliest birds, the non-avian avialans (i.e. non-crown birds), particularly of their diet. The diet of non-avian avialans has been a matter of debate, in large part because of the ambiguous qualitative approaches that have been used to reconstruct it. Here we review methods for determining diet in modern and fossil avians (i.e. crown birds) as well as non-avian theropods, and comment on their usefulness when applied to non-avian avialans. We use this to propose a set of comparable, quantitative approaches to ascertain fossil bird diet and on this basis provide a consensus of what we currently know about fossil bird diet. While no single approach can precisely predict diet in birds, each can exclude some diets and narrow the dietary possibilities. We recommend combining (i) dental microwear, (ii) landmark-based muscular reconstruction, (iii) stable isotope geochemistry, (iv) body mass estimations, (v) traditional and/or geometric morphometric analysis, (vi) lever modelling, and (vii) finite element analysis to reconstruct fossil bird diet accurately. Our review provides specific methodologies to implement each approach and discusses complications future researchers should keep in mind. We note that current forms of assessment of dental mesowear, skull traditional morphometrics, geometric morphometrics, and certain stable isotope systems have yet to be proven effective at discerning fossil bird diet. On this basis we report the current state of knowledge of non-avian avialan diet which remains very incomplete. The ancestral dietary condition in non-avian avialans remains unclear due to scarce data and contradictory evidence in Archaeopteryx. Among early non-avian pygostylians, Confuciusornis has finite element analysis and mechanical advantage evidence pointing to herbivory, whilst Sapeornis only has mechanical advantage evidence indicating granivory, agreeing with fossilised ingested material known for this taxon. The enantiornithine ornithothoracine Shenqiornis has mechanical advantage and pedal morphometric evidence pointing to carnivory. In the hongshanornithid ornithuromorph Hongshanornis only mechanical advantage evidence indicates granivory, but this agrees with evidence of gastrolith ingestion in this taxon. Mechanical advantage and ingested fish support carnivory in the songlingornithid ornithuromorph Yanornis. Due to the sparsity of robust dietary assignments, no clear trends in non-avian avialan dietary evolution have yet emerged. Dietary diversity seems to increase through time, but this is a preservational bias associated with a predominance of data fro...

Diet of Mesozoic toothed birds (Longipterygidae) inferred from quantitative analysis of extant avian diet proxies

“…The diet of most non-avian avialans has been largely speculative so far [ 1 – 3 ]. We use Aves in this paper to refer to crown group birds, and Avialae to refer to crown group birds plus all coelurosaurian theropods closer to them than to either dromaeosaurids or troodontids [ 4 ].…”

“…Among Enantiornithes, the most diverse and widespread avialans in the Mesozoic, only Eoalulavis and Shenqiornis have good evidence (i.e. fossilised digestive tract contents or more than one line of quantitative proxy evidence) backing any particular diet [ 1 , 5 ] out of nearly 100 known species [ 6 ]. A more robust understanding of non-avian avialan diet will allow us to test key hypotheses in bird evolution, such as beak evolution allowing for extant bird dietary diversity [ 7 , 8 ], trophic level reduction driving powered flight development [ 9 ], and birds occupying a low-level consumer role in Mesozoic ecosystems [ 10 ].…”

“…Longirostravis , Rapaxavis and Shanweiniao have been proposed as probe feeders (in mud [ 11 , 15 ] and tree bark [ 17 ]) on the basis of their elongate rostra in analogy to those of oystercatchers ( Haematopus ) and shanks ( Tringa ) [ 15 , 17 ]. Longipterygids preserve more complete skulls than any other enantiornithine family [ 1 ], providing the best opportunity for family-level inferences for reconstruction of enantiornithine skull morphology (Fig. 1 ).…”

“…1 A, B). We investigate the ecology of these fossil birds using data from four lines of evidence: body mass estimation, traditional morphometrics (TM) of pedal unguals, mechanical advantage (MA) and functional index analysis of upper jaws, and finite element analysis (FEA) of the lower jaws [ 1 ].…”

“…Body mass has been found in recent studies [ 18 , 19 ] to be an effective predictor of bird diet, with developmental [ 20 ] or mechanical [ 1 ] constraints proposed as explanations. For extinct taxa, mass can be estimated with high accuracy from limb bone measurements [ 21 ].…”