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17.23: Predation and Herbivory - Biology

17.23: Predation and Herbivory - Biology



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Learning Objectives

  • Discuss the importance of predation and herbivory in the ecosystem, including how organisms defend against these

Perhaps the classical example of species interaction is predation: the hunting of prey by its predator. Nature shows on television highlight the drama of one living organism killing another. Populations of predators and prey in a community are not constant over time: in most cases, they vary in cycles that appear to be related. The most often cited example of predator-prey dynamics is seen in the cycling of the lynx (predator) and the snowshoe hare (prey), using nearly 200 year-old trapping data from North American forests (Figure 1). This cycle of predator and prey lasts approximately 10 years, with the predator population lagging 1–2 years behind that of the prey population. As the hare numbers increase, there is more food available for the lynx, allowing the lynx population to increase as well. When the lynx population grows to a threshold level, however, they kill so many hares that hare population begins to decline, followed by a decline in the lynx population because of scarcity of food. When the lynx population is low, the hare population size begins to increase due, at least in part, to low predation pressure, starting the cycle anew.

The idea that the population cycling of the two species is entirely controlled by predation models has come under question. More recent studies have pointed to undefined density-dependent factors as being important in the cycling, in addition to predation. One possibility is that the cycling is inherent in the hare population due to density-dependent effects such as lower fecundity (maternal stress) caused by crowding when the hare population gets too dense. The hare cycling would then induce the cycling of the lynx because it is the lynxes’ major food source. The more we study communities, the more complexities we find, allowing ecologists to derive more accurate and sophisticated models of population dynamics.

Herbivory describes the consumption of plants by insects and other animals, and it is another interspecific relationship that affects populations. Unlike animals, most plants cannot outrun predators or use mimicry to hide from hungry animals. Some plants have developed mechanisms to defend against herbivory. Other species have developed mutualistic relationships; for example, herbivory provides a mechanism of seed distribution that aids in plant reproduction.

Defense Mechanisms against Predation and Herbivory

The study of communities must consider evolutionary forces that act on the members of the various populations contained within it. Species are not static, but slowly changing and adapting to their environment by natural selection and other evolutionary forces. Species have evolved numerous mechanisms to escape predation and herbivory. These defenses may be mechanical, chemical, physical, or behavioral.

Mechanical defenses, such as the presence of thorns on plants or the hard shell on turtles, discourage animal predation and herbivory by causing physical pain to the predator or by physically preventing the predator from being able to eat the prey. Chemical defenses are produced by many animals as well as plants, such as the foxglove which is extremely toxic when eaten. Figure 2 shows some organisms’ defenses against predation and herbivory.

Many species use their body shape and coloration to avoid being detected by predators. The tropical walking stick is an insect with the coloration and body shape of a twig which makes it very hard to see when stationary against a background of real twigs (Figure 3a). In another example, the chameleon can change its color to match its surroundings (Figure 3b). Both of these are examples of camouflage, or avoiding detection by blending in with the background.

Some species use coloration as a way of warning predators that they are not good to eat. For example, the cinnabar moth caterpillar, the fire-bellied toad, and many species of beetle have bright colors that warn of a foul taste, the presence of toxic chemical, and/or the ability to sting or bite, respectively. Predators that ignore this coloration and eat the organisms will experience their unpleasant taste or presence of toxic chemicals and learn not to eat them in the future. This type of defensive mechanism is called aposematic coloration, or warning coloration.

While some predators learn to avoid eating certain potential prey because of their coloration, other species have evolved mechanisms to mimic this coloration to avoid being eaten, even though they themselves may not be unpleasant to eat or contain toxic chemicals. In Batesian mimicry, a harmless species imitates the warning coloration of a harmful one. Assuming they share the same predators, this coloration then protects the harmless ones, even though they do not have the same level of physical or chemical defenses against predation as the organism they mimic. Many insect species mimic the coloration of wasps or bees, which are stinging, venomous insects, thereby discouraging predation (Figure 5).

In Müllerian mimicry, multiple species share the same warning coloration, but all of them actually have defenses. Figure 6 shows a variety of foul-tasting butterflies with similar coloration.

In Emsleyan/Mertensian mimicry, a deadly prey mimics a less dangerous one, such as the venomous coral snake mimicking the non-venomous milk snake. This type of mimicry is extremely rare and more difficult to understand than the previous two types. For this type of mimicry to work, it is essential that eating the milk snake has unpleasant, but not fatal, consequences. Then, these predators learn not to eat snakes with this coloration, protecting the coral snake as well. If the snake were fatal to the predator, there would be no opportunity for the predator to learn not to eat it, and the benefit for the less toxic species would disappear.


Induced defences in plants reduce herbivory by increasing cannibalism

Plants are attacked by myriad herbivores, and many plants exhibit anti-herbivore defences. We tested the hypothesis that induced defences benefit tomato plants by encouraging insects to eat other members of their species. We found that defences that promote cannibalism benefit tomatoes in two ways: cannibalism directly reduces herbivore abundance, and cannibals eat significantly less plant material. This previously unknown means of defence may alter plant–herbivore dynamics, plant evolution and pathogen transmission.

Plants are not passive bystanders in their interactions with herbivores: plants alter their chemistry, morphology and other components of their phenotype to reduce herbivory 1 , often using cues from their environment to initiate these defences before any actual attack occurs 2,3,4 . Because induced defences in plants are so ubiquitous 1 and may have important effects on herbivores 1,5 and other trophic levels 6 , fundamental goals in plant–herbivore ecology are to understand the benefits of induced defences to plants in terms of reduced herbivory 7 , to describe how induced defences operate (for example whether they reduce herbivore feeding, survival or reproduction), and to characterize how plants’ induced defences may affect other organisms 6,8 . We advance these goals by demonstrating a means by which induced defences in plants reduce herbivory: altering cannibalism among herbivores.


Herbivory

Herbivores eat plant material, which is much more difficult to digest than animal tissue. The nutrition of plants is locked up inside rigid cell walls and contains many molecules that are difficult to digest. Herbivores deal with this conundrum by having complex digestive systems that can tease apart plant tissues and extract the nutrition inside. But even with this powerful digestive system, plant material is still not as high in fat and protein as animal tissue, so herbivores have to eat a lot to maintain their bodies. Animals that eat the most nutritious parts of plants (nuts, seeds, and fruit) can get away with eating a modest amount, but animals that eat low-quality plants or parts of plants (grass blades, bark, leaves) have to eat an enormous amount to stay healthy. Take an adult African elephant for example. In order to maintain its body weight and keep up with all its bodily functions, it has to eat over 100 pounds of vegetation a day, even more when its mating/breeding season.

Herbivory Examples

Some examples of animals with herbivorous feeding habits include: zebras, wildebeests, antelope, deer, rhinos, hippos, gazelles, sheep, goats, cattle, giraffes, elephants, moose, alpacas and llamas, rabbits, beavers, camels, horses, manatees, sloths, tapirs, okapis, reindeer, musk oxen, bison, buffalo, and iguanas. Below is a list of different types of feeding strategies for plant eaters:

  • Granivores- grain eaters (ie: some rodents)
  • Graminivore- grass eaters (ie: zebra)
  • Frugavores- fruit eaters (ie: flying foxes)
  • Foliovores- leaf eaters (ie: koalas)
  • Nectivores- nectar eaters (ie: hummingbirds)
  • Palynivore- pollen eaters (ie: some insects)

Which Type of Fermenter are You?

Hindgut fermenters have a single, simple stomach. They digest plant material with the help of bacteria that live in their digestive system. Fermentation takes place primarily in the cecum (tissue pouch where bacteria live) and large intestine. Examples of animals that use this type of digestion are zebras, horses, rhinos, tapirs, rodents, rabbits, and pikas.

Foregut fermenters (ruminants) have a complex, four-chambered stomach. These animals can actually
digest cellulose without the help of bacteria, using their high-tech stomach. After they chew and swallow their food, it’s sent down to be partially digested, then, when the animal is resting, it regurgitates the food in the form of a cud (ball of chewed grass) and chews it again to break it down further.

Energetically speaking, foregut fermentation is more efficient than hindgut fermentation, but there are benefits and drawbacks to each strategy. While usually bulk-eaters, hindgut fermenters have the ability to get more out of eating small quantities of food as opposed to ruminants. Ruminants can digest cellulose more effectively, but are limited to areas where the quality of forage is higher than what hindgut fermenters could survive on.

Obligate Herbivory

Some herbivores have become so specific in their food habits that their bodies have developed special strategies to process their food. Take the koala for example it exclusively eats eucalyptus leaves which are low in protein and high in indigestible materials. It’s very specific diet is likely an evolutionary response to a high availability of a food that other animals were not eating. Since the food was readily available and abundant, the koala took advantage of it, and its body responded by developing special ways to process this unique food. This phenomenon is also observed in other herbivores like pandas and sloths. If you notice, the things these animals have in common are a low metabolic rate and extensive periods of rest during the day…another adaptation to a nutrient-poor source of food.


Ecology: from cells to Gaia

This course presents the principles of evolution and ecology for citizens and students interested in studying biology and environmental sciences. It discusses major ideas and results. Recent advances have energised these fields with evidence that has implications beyond their boundaries: ideas, mechanisms, and processes that should form part of the toolkit of all biologists and educated citizens. Major topics covered by the course include fundamental principles of ecology, how organisms interact with each other and their environment, evolutionary processes, population dynamics, communities, energy flow and ecosystems, human influences on ecosystems, and the integration and scaling of ecological processes through systems ecology. This course will also review major ecological concepts, identify the techniques used by ecologists, provide an overview of local and global environmental issues, and examine individual, group and governmental activities important for protecting natural ecosystems. The course has been designed to provide information, to direct the student toward pertinent literature, to identify problems and issues, to utilise research methodology for the study of ecology and evolution, and to consider appropriate solutions and analytical techniques. Needed Learner Background: general biology and a good understanding of English. This course has the following expectations and results: 1) covers the theoretical and practical issues involved in ecology and evolution, 2) conducting surveys and inventories in ecology, 3) analyzing the information gathered, 4) and applying their analysis to ecological and conservation problems.

Рецензии

such a nice course, presentation is so good , specially thanks to university "Tomsk State University".

It is very useful to understand about the biodiversity and it is fabulous

In this module, we will talk about agonistic and foraging interactions between species (such as predation, herbivory and parasitism) and mutualistic interactions (such as symbiosis, commensalism, endosymbiosis, etc.). Then we will see how these interactions influence the evolutionary ecology of species and their diversity. In the last lesson of this module we will analyse the energy flux and biogeochemical cycles that keep alive Earth’s ecosystems and the whole biosphere (e.g. Gaia).

Преподаватели

Roberto Cazzolla Gatti

Текст видео

Hi learners, welcome to the sixth lecture on my course "Ecology: from cells to Gaia." Today, we will talk about foraging interaction between species: predation, herbivory, and parasitism. A predator may be defined as any organism that consumes all or part of another living organism, that is, prey or a host, thereby benefiting itself, but under at least some circumstances reducing the growth, the fecundity, and the survival of the prey. So, true predators invariably kill their prey and do so more or less immediately after attacking them and consumes several or many prey items them in the course of their life. Grazer also attack several many prey items in the course of their life but consume only part of each prey item and do not usually kill their prey. Parasites instead consume only part of each host and also do not usually kill their host, especially in the short term but attack one or very few host in the course of their life, with which they therefore often form a relative intimate association. Grazer and parasites in particular often exert their harm not by killing their prey immediately like true predators, but by making their prey more vulnerable to some other form of mortality. The effect of grazer and parasites on the organism they attack are often less profound than they first seemed because individual plants can compensate for the effect of herbivory and the host may have defensive responses to attack by parasites. The effect of predation on a population of prey are complex to predict because the surviving prey may experience reduced competition for a limiting resource or produce more offspring, or other predators may take fewer of the prey. True predators and grazer typically forage, moving around within their habitat in search of their prey. Other predators sit and wait for their prey almost always in a selected location. With parasites and pathogens, there may be direct transmission between infection and uninfected host, or contact between free-living stages of the parasite and uninfected host may be important. Optimal foraging theory aims to understand why particularly patterns of foraging behavior have been favored by natural selection because they give rise to the highest net rate of energy intake. Generalist predators spend relatively little time searching but include relatively low profitable items in their diet. Specialists only include high-profitability items in their diet but spend a relatively large amount of their time searching for them. There is an underlying tendency for predators and prey to exhibit cycles in abundance, and cycles are observed in some predator-prey or host-parasite interactions. However, there are many important factors that can modify or override the tendency to cycle. Many population of predators and prey exist as a metapopulation. In theory and in practice, asynchrony in population dynamics in different patches and the process of dispersal tend to dampen any underlying population cycles. There are many situations when predation may hold down density of population so the resources are not limiting and individuals do not compete for them. When predation promotes the coexistence of species amongst which there would otherwise be competitive exclusion, because the density of some or all of them are reduced to levels at which competition is relatively unimportant, this is known as predator-mediated coexistence. The effect of predation generally on a group of coexisting species depends on which species suffer most. If it is a rare species, then this may be driven to extinction and the total number of species in the community will decline. If it is the dominant that suffer most, however, the result of every predation will usually be the free space and resources for other species as species number may then increase. It is not unusual for the number of species in a community to be greatest at the intermediate levels of predation. So at the end of this lecture, I have some question for you. First, with the aid of example, try to answer: what are the feeding characteristic of two predators, grazer, parasites, and parasitoids? Second, why there is an underlying tendency for a population of predators and prey to cycle? So thanks for your attention and see you in next lecture.


Discussion

Comparative digestive physiology studies demonstrate that the evolution of digestive system molecules adapts for the amounts of nutrient components (e.g., carbohydrates, fats, and proteins) in the diets of animals 16,17 . Our results showed that the ancestral archosaur exhibited a marked selection of the genes related to PDA and FDA, whereas the CALB presented a predominant selection of the genes involved in CDA and FDA (Fig. 2, Table 1, and Supplementary Data 2). These results remained largely unchanged even after the Bonferroni multiple testing correction of the p-values of PSGs (Table 1). Especially for the ancestral archosaur, our positive selection analyses revealed the highest number of PSGs in PDA, followed by FDA, with the lowest number of PSGs found in CDA (Fig. 2). This may suggest that the diet of the ancestral archosaur was characterized by a high amount of proteins, followed by fats, with a minimum load of carbohydrates. This nutrient profile is highly consistent with the presumable carnivory of ancestral archosaurs 68 , as meats are generally rich in proteins, followed by fats, with the minimum amount of carbohydrates 27 . Contrary to the ancestral archosaur, for the CALB, our results based on two different methods (PAML and RELAX) consistently demonstrated that it showed a relatively strong selection in CDA- and FDA-related genes, with the weakest selection found in PDA-related genes (Fig. 2, Table 1, and Supplementary Data 2). This may suggest that the diet of the CALB is characterized by high amounts of carbohydrates and fats, with a relatively minimal amount of proteins, representing a high-energy diet. This seems to be more consistent with herbivory compared to carnivory, considering that plant foods are rich in carbohydrates, whereas meats are particularly high in proteins 27 . In particular, most PSGs involved in CDA (SI, SLC5A1, SLC2A5, HK3, and LCT) were found in the CALB center on the digestion and absorption of sugars (e.g., glucose, sucrose, and fruit sugar), indicating its high-sugar diet. A high-sugar diet may suggest their eating of fruits, which are characterized by relatively high amounts of sugars among plant foods 24,27,69 . In particular, one PSG, SLC2A5, found in the CALB is mainly involved in the transports of fruit sugar 38,39,40 . These lines of evidence may suggest that the CALB involved fruits in its diet. On the other hand, for the PSGs found in FDA, one gene, ABCG5, plays a critical role in the transport of plant sterols, which are mainly found in nuts and seeds 43,47 . This may suggest that the CALB ingests seeds and/or nuts as well, which are rich in fat 27 . The predominant selection of the CALB in FDA is similar to parrots, which consume considerable amounts of seeds and nuts, and are found to present a strong Darwinian selection in FDA as well with four PSGs found, of which three (ABCG5, APOA4, and APOB) are shared with the CALB 29 . In all, our molecular study suggests that the ancestral archosaur is probably a carnivore, whereas the CALB is more likely an herbivore, ingesting fruits, seeds, and/or nuts (Fig. 1).

Regarding digestive system-related genes, in addition to diets, other factors (e.g., flight and microbial fermentation) may affect their evolution as well. With respect to flight, previous studies show that in favor of flight, fliers (e.g., birds and bats) have evolved to have a smaller intestinal size and shorter retention times of digesta relative to nonfliers 70,71,72 , and thus there may be an increased selection for the digestion and absorption of nutrient substrates as a compensation for the constraints on the digestive system in fliers 70,72 . This may alternatively explain our observed enhanced selection of the digestion and absorption of carbohydrates and fats of the CALB however, it is difficult to interpret why such an enhanced selection was not found in the PDA of the CALB, as observed in this study (Table 1). Moreover, previous studies show that the increased digestion and absorption of nutrient substrates in fliers (birds) compared to nonfliers (mammals) seem to be restricted to the paracellular absorption pathway, in which nutritional substances move through the tight junctions adjoining cells, rather than the transcellular absorption pathway, which include CDA, PDA, and FDA, as examined in this study 70,72 . Thus, the possible effects of flight on the evolution of the digestive system-related genes of the CALB examined in this study may be relatively small. In addition to flight, microbial fermentation, which transfers dietary carbohydrates (e.g., cellulose) to volatile fatty acids and microbe proteins for the utilization of herbivores, may be another possible factor that affected the evolution of digestive system-related genes however, its importance is considered to be mainly restricted to herbivores (e.g., ungulates) that rely mainly on microbial fermentation and is relatively trivial to other animals 16 . These lines of evidence may suggest that the selection differences of the digestive system-related genes observed in the CALB and the ancestral archosaurs may be mainly due to their dietary differences, although there exist possible effects of flight and microbial fermentation on the evolution of their digestive system-related genes.

Our molecular results are highly consistent with the fossil evidence showing that ancestral archosaurs are generally typically meat eaters 68 and a great number of ancestral Mesozoic birds, including the basal birds, such as Jeholornis, Confuciusornis, and Sapeornis, show features or gut contents indicating that they ate fruits and/or seeds 2,3,5,6,7,8,10,12 . In particular, for the herbivory of the CALB found in this study, it is consistent with the widespread herbivory observed in many living bird lineages across bird phylogeny (Fig. 1). In line with this, one previous study shows evidence of seeds as an important dietary component of the CALB using maximum likelihood reconstruction 73 . Considering that ancestral birds lived in a conifer-dominated ecosystem 9,74 , the seeds that they ate might partly come from conifers 11 . Indeed, the seeds of many conifers (e.g., pines) are relatively rich in lipids 75,76 , which might have led to the evolutionary enhancement of FDA of the CALB found in this study. In addition, previous studies show that the Late Jurassic/Early Cretaceous radiation of more advanced birds temporally coincides with that of angiosperm plants 77 and it is likely that the fruit- and/or seed-eating habitat of ancestral birds may have partly helped for their dispersal of seeds 2 . The herbivory of the CALB is also consistent with the occurrence of ceca observed in the majority of living birds, including the basal lineages (e.g., ratites), which is generally considered to be helpful for cellulose digestion and fermentation linked to herbivory 18,78 . The dietary shift of the CALB to herbivory is also consistent with the observation of reductions in both the teeth 3,8 and biting force 79,80 across the theropod-bird transition, which is considered to have resulted from the dietary shift from carnivorous to herbivorous diets 15,79 . The similar transition from carnivory to herbivory occurs multiple times in theropods 15,81,82 . The causes underlying the evolutionary shift to the herbivory of the CALB are not clear, but the possible competition from carnivorous theropods and pterosaurs is proposed as a possible candidate 14,79 . The finding of the herbivory of the CALB ingesting fruits, seeds, and/or nuts, which characterize seed plants adapted to dry land environments 83 , may strongly suggest that the CALB mainly occurred in terrestrial habitats rather than an aquatic environment, as hypothesized previously 84 . These findings are consistent with the fact that the phylogenetically most basal extant neornithine birds—i.e., Palaeognathae and Galloanseres—are predominantly herbivorous or omnivorous and they mainly occur in terrestrial habitats 2 .

Our results demonstrate an evolutionary shift of the CALB to an herbivorous diet (fruit, seed, and/or nut eater) (Fig. 1), suggesting that the CALB may be a low-level consumer. Evolutionarily, birds are widely believed to be derived from a group of small maniraptoran theropods, including dromaeosaurids and troodontids 2,4,5,85 . Among these maniraptoran theropods, many of them, including most dromaeosaurids and derived troodontids, show carnivory 2,3,5,8,15,82,86,87,88,89,90,91 (Fig. 3). However, unlike their maniraptoran relatives, many bird lineages, including the basal bird lineages, such as Jeholornis and Sapeornis, may have evolved to exploit herbivorous niches, as evidenced by both the molecular (Fig. 1) and fossil evidence mentioned above 2,3,4,5,6,7,8,10,11,15,79 (Fig. 3). The dietary shift from carnivory to herbivory may suggest a shift of the trophic niche of bird ancestors from that of a high-level consumer to a low-level consumer as a primary and/or secondary consumer 74,89 . This is consistent with the marked reduction or loss of teeth along with the evolution of birds 3,4,5,92 , a feature indicative of low-level consumers rather than high-level consumers (e.g., top predators), which would otherwise show a predation feature of well-developed teeth 86,93 . Moreover, although diverse diets (e.g., seeds, fish, and insects) among ancestral bird lineages have been found, there is no direct fossil evidence indicative of their preying on terrestrial vertebrates 3 , strengthening their ecological niches as low-level consumers. Ancestral birds were abundant in Mesozoic terrestrial ecosystems 74 , occurring globally 94 and representing a potential food source for carnivores. Becoming a low-level consumer, ancestral birds may be under increased predation risk. This is particularly the case for ancestral birds, as they evolve toward miniaturization suitable for powered flight 95,96 and their small body size may be particularly vulnerable to predators. More importantly, their evolution of endothermy and powered flight requires much more energy and, consequently, frequent foraging 3,5,30,97 . Frequent foraging may have, most often, exposed them to predators, hence leading to their high predation risk. In support of this, fossil evidence shows that ancestral birds, such as enantiornithines and Confuciusornis, have a precocial development style 5,6,98 , although there is an evolutionary transition of a reduced precocity in ornithurine birds 99 and precocity is generally considered to be an anti-predation strategy for facing historically strong predation pressure 100,101 . Moreover, one recent study shows that the CALB was probably cathemeral (i.e., active in both day and night), and that it may have evolved an enhanced visual capability to detect motion 30 . Cathemerality is considered to be linked to high predation risk 102,103 and the promoted motion detection ability of the CALB may mainly help to detect approaching predators 104 given its herbivory. Therefore, the dietary shift may have made ancestral birds become the prey of high-level consumers, possibly leading to their high predation risk.

The predation of gliding predatory non-avian maniraptorans (pennaraptorans) on ancestral birds in the context of the arboreal theory is shown (please see text for details). Paraves phylogeny with digestive system characteristics (gastric mill, crop, and tooth) and taxonomic definition (e.g., Aves) are based on one previous study 3 . The dietary information follows published studies 3,15,82 . The flight-related anatomical features (wings, fused tail, and keeled sternum) along phylogeny follow one published study 146 . The progressive enhancement of flight performance from gliding to soaring, flapping flight, and maneuvering flight within Aves is based on published literature 5 . Species silhouettes corresponding to each of phylogenetic taxa used are from phylopic.org and are designed by (from left to right) the following: Troodontidae (Scott Hartman), Dromaeosauridae (Scott Hartman, modified by T. Michael Keesey), Archaeopteryx (Dann Pigdon), Jeholornis (Matt Martyniuk), Confuciusornis (Scott Hartman), Sapeornis (Matt Martyniuk), Enantiornithes (Matt Martyniuk), and Ornithuromorpha (Juan Carlos Jerí).

Knowing the possible predators of ancestral birds is important to determine their potential predation risk. According to arboreal theory, birds evolved from a group of arboreal and gliding maniraptorans, and that ancestral birds may be primarily arboreal and capable of gliding flight, although they spent some time on the ground as well 4,5,6,10,105,106 . Given the possible arboreality and gliding lifestyle of ancestral birds, while there are many potential predators, such as carnivorous theropods, carnivorous mammals (e.g., Repenomamus), snakes (e.g., Sanajeh), and crocodylomorphs, in the Mesozoic terrestrial ecosystem 74,86 , four lines of evidence may suggest that one group of carnivorous theropods—non-avian maniraptorans (e.g., dromaeosaurids)—is likely one of the main predators of ancestral birds, as proposed previously 5,90,107 . Primarily, a wealth of small feathered non-avian maniraptorans, such as Aurornis, Anchiornis, Bambiraptor, Buitreraptor, Changyuraptor, Eosinopteryx, Jinfengopteryx, Microraptor, Rahonavis, and Xiaotingia, are found to have hallmark anatomical characteristics indicative of their capability of gliding flight or even some forms of powered flight 2,4,5,6,85,88,108,109 , and many of these volant non-avian maniraptorans, such as Microraptor, Anchiornis, and Changyuraptor, show predatory features 2,3,8,15,82,86,87,88,89,90,91,107 , representing one of the potential aerial predators of ancestral birds. The predation pressure from these aerial predators may be more significant than those ground predators given the arboreality and gliding lifestyle of ancestral birds. On the other hand, both ancestral birds and gliding non-avian maniraptorans have a relatively small body size among the dinosaurs known 86,95,96,110 , suggesting that ancestral birds may be a suitable prey for them. This is because there is a general positive correlation of body size between predators and their target prey, and small predators tend to prey on small prey 111,112,113,114 . Moreover, previous studies show that, among theropods, non-avian maniraptorans show a relatively high metabolic level (e.g., endothermy) comparable to birds 115,116 , suggesting that they possibly had a relatively high activity level. The high activity level of non-avian maniraptorans supports the feasibility of their predation on ancestral birds. Finally, and more importantly, there is already direct fossil evidence indicative of the predation of ancestral arboreal bird (adult enantiornithine bird) by arboreal and gliding predatory non-avian maniraptorans, such as Microraptor, which is known from hundreds of specimens, despite the extreme scarcity of preserved fossils 90 . In addition, the possible predation of ancestral birds by another predatory non-avian maniraptoran, Sinornithosaurus, which might be capable of gliding flight 117 , was proposed previously 107 . These lines of ecological and fossil evidence suggest that the predation pressure of ancestral birds during their early evolution may, at least partly, mainly have come from those arboreal and gliding non-avian maniraptorans.

The predation from gliding non-avian maniraptorans as described may be one important selection pressure of ancestral birds, which may have then led to their evolution of anti-predator traits. Among many possible anti-predator traits of ancestral birds, powered flight (e.g., flapping flight) has long been considered to be, at least partly, helpful to escape from predators 5 . Regarding the powered flight of birds, different theories have been proposed to account for its evolution 4,5 . Further, arboreal theory invokes a natural transition of powered flight via gliding flight 4,5,10,105,106 , but a basic question remains: what was the selection pressure for the natural transition 118 ? Although gliding flight is common among both living and extinct animals, powered flight is rare and is only known in insects, pterosaurs, birds, and bats 119 , suggesting that powered flight may less likely occur without certain selection pressures. This is particularly true for birds, as their powered flight demands high energy and substantial evolutionary alternation (e.g., keeled sternum and flight muscles) compared to gliding flight, a simple and cheap way of flying 5 . Early birds, such as Archaeopteryx and Jeholornis, are believed to be primarily arboreal and be capable of gliding flight, which are believed to be descended from maniraptorans that had already evolved gliding flight 4,5,106 . Indeed, many maniraptorans possess asymmetric flight feathers to generate lift and, in particular, the discovery of many bird-like paravians, such as Microraptor, Anchiornis, Xiaotingia, and Aurorornis, is the most unusual in developing four wings, suggesting their possible high performance of gliding flight 4,5,109 . However, given the diet divergence between non-avian maniraptorans and ancestral birds, and particularly that many of gliding non-avian maniraptorans (e.g., Microraptor and Sinornithosaurus) were potential predators of early birds 5,90,107 , it is plausible that early birds may have then evolved powered flight (e.g., flapping flight) based on their gliding flight to escape from gliding predatory non-avian maniraptorans. The predation pressure from gliding predatory non-avian maniraptorans may have worked as a driver to stimulate the evolution of powered flight of their arboreal prey. Moreover, the flapping flight of birds may be critical to flee from those gliding predators. Fossil evidence shows that ever since the evolutionary divergence of early birds from their maniraptoran relatives, the evolution of birds has shown a major trend in the improvement of flight, such as from gliding to flapping and maneuvering flight with the acquisition of flight-related characteristics such as a shortening of the tail and a keeled sternum 2,4,5,85 (Fig. 3). The continuous evolutionary enhancement of the flight of ancestral birds may essentially help for an increase of speed and maneuverability of locomotion, both of which are considered to be crucial for escape success 120 . This may be the case particularly for birds, as they could not become large in body size, a potential anti-predator strategy observed in many animals 121 , to evade predators due to their miniaturization constraints in favor of flight 95,96 . Indeed, for many birds, flying is an important means used to escape from predators 5,122 , suggesting predation is an important selection pressure for powered flight 5,119 . This is consistent with the observation that birds frequently become flightless in predator-free islands 123 . Thus, the predation pressure from gliding predatory non-avian maniraptorans may be an important candidate contributing to the evolutionary shift from gliding flight to powered flight at the theropod-to-bird transition, although it remains unknown as to whether there were gliding predators other than non-avian maniraptorans contributing to the evolution of powerful flight of birds as well.

Besides the evolutionary specialization of locomotion (e.g., flapping flight), birds have a specialized digestive system. Living birds are toothless and they swallow their food whole, which is temporally stored in their crop and then grinded up by their muscular gizzard. Fossil evidence shows that the specialization of the digestive system occurs in multiple lineages of ancestral birds 3,6,8,11,92,124,125,126 (Fig. 3). A recent genomic study shows that modern birds lost their teeth since their common ancestor about 116 million years ago 127 . Regarding the evolutionary specialization of the digestive system of birds, its adaptive significance is, however, less clear. Previous studies indicate that the loss of teeth in birds seems to be linked to an herbivorous diet 5,11,15,81 , which is consistent with the herbivory of the CALB found in this study, but the underlying mechanism remains unknown. Optimal foraging theory states that predation has a profound influence on the foraging strategies of animals and animals must trade off two conflicting demands of maximizing foraging efficiency and minimizing predation risk 128,129,130 . In light of this optimal foraging theory, for the evolutionary specialization of the digestive system of birds, we propose here that herbivores (e.g., ancestral birds) are low-level consumers and, consequently, at relatively high risk to predators. Under high predation risk, the time needed to acquire and process food using the teeth may be limited, but the evolutionary specialization of the digestive system of birds may allow them to gather more food as fast as possible (maximizing foraging efficiency), as food can be stored in their crop without expending too much time processing it using their teeth, and then they can seek a safe place to process their food via their gizzard (minimizing predation risk). Consequently, the reduced reliance on teeth for the processing of food as a result of predator avoidance may have then led to the selection relaxation of the teeth, leading to their subsequent reduction or loss thereof. This may be particularly true for early birds that would necessarily demand frequent foraging 3 and much time for the oral processing of their food (e.g., hard seeds) 8 if no gizzard were available under relatively high predation risk (including both aerial, arboreal, and ground predators), whereas the evolution of the bird-like digestive system may help to maximize foraging efficiency and minimize their exposure to predators. This is consistent with previous studies showing that ancestral birds seem not to have used their teeth to process food rather, their teeth, if any, were mainly used for the acquisition of food 10,11,79,97,125 .

Regarding the reduction or loss of the teeth of birds, it is traditionally attributed to lightening the body for flight 11,126 . This, however, cannot explain the occurrence of numerous toothed Mesozoic birds (e.g., Enantiornithes and Ichthyornis) 3,126,131 and hence the teeth were probably not a limiting factor for flight 2,6,97,132 . Alternatively, teeth reduction or loss is considered to be partly due to the functional replacement by the muscular gizzard 3,125,133 . However, this raises a new question: given that teeth and muscular gizzard have a similar function, why the teeth got lost rather than muscular gizzard? One possibility is that it must expend considerable time processing food using teeth without a gizzard during foraging, which may then largely increase their predation risk. In line with this reasoning, the crop is also suggested to help to gather more food quickly, to avoid competitors and/or predators 11,18,125 , although an alternative explanation exists 3,97 . Given the possible importance of predation, we argue that the evolution of digestive system characteristics of birds, including teeth reduction or loss, crop, and gizzard, are not independent rather, their evolution is probably mutually dependent. The integrative and/or collective evolution of these characteristics may be a result of both maximizing foraging efficiency and minimizing predation risk. Predation pressure is also believed to be a potential selection pressure for the evolutionary specialization of the digestive system (e.g., four-chambered stomach) of ruminants 18,134 . Besides birds, teeth reduction or loss is frequently observed in many other tetrapod lineages as well (e.g., toads and turtles) 81,133,135 and future studies would be beneficial to determine whether their teeth reduction or loss was due to historically high predation risks as well.


Branch-Localized Induction Promotes Efficacy of Volatile Defences and Herbivore Predation in Trees

Induction of plant defences can show various levels of localization, which can optimize their efficiency. Locally induced responses may be particularly important in large plants, such as trees, that show high variability in traits and herbivory rates across their canopies. We studied the branch-localized induction of polyphenols, volatiles (VOCs), and changes in leaf protein content in Carpinus betulus L., Quercus robur L., and Tilia cordata L. in a common garden experiment. To induce the trees, we treated ten individuals per species on one branch with methyl jasmonate. Five other individuals per species served as controls. We measured the traits in the treated branches, in control branches on treated trees, and in control trees. Additionally, we ran predation assays and caterpillar food-choice trials to assess the effects of our treatment on other trophic levels. Induced VOCs included mainly mono- and sesquiterpenes. Their production was strongly localized to the treated branches in all three tree species studied. Treated trees showed more predation events than control trees. The polyphenol levels and total protein content showed a limited response to the treatment. Yet, winter moth caterpillars preferred leaves from control branches over leaves from treated branches within C. betulus individuals and leaves from control Q. robur individuals over leaves from treated Q. robur individuals. Our results suggest that there is a significant level of localization in induction of VOCs and probably also in unknown traits with direct effects on herbivores. Such localization allows trees to upregulate defences wherever and whenever they are needed.

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