Tracking the Course of Evolution


by Bruce H. Tiffney

There are two accompanying graphics showing (1) a simple time line of plant predation and (2) the relationship of plant diversification and the phylogeny of vertebrate plant predators.


A. The purpose of this lecture is fourfold:
1. To provide raw data on the interaction of terrestrial plants and animals through time.
2. To emphasize that ecological interactions evolve through time just as do organisms.
3. To illustrate that, while we may use our knowledge of the biology of living organisms to help us understand the past ("The present is the key to the past"), we must be cautious that we do not think that the present and the past are precisely alike (that the present is the past).
4. To underscore that we do not "know it all" yet!!!

B. Focus:
1. Primarily upon the vertebrates, as a synthetic picture of arthropod - plant interactions is just beginning to emerge.
2. However, the arthropods are a major portion of this story, as they are today.
A. Timing:
1. Plants appear on land "seriously" in late Silurian, forming base of food chain
2. Arthropods followed by at least Early Devonian, radiating by Pennsylvanian
3. Vertebrates appear in Late Devonian, radiating by Pennsylvanian

B. The Puzzle:
1. Amphibians are all Carnivores
2. Pennsylvanian Reptiles are all carnivores.
3. Synapsids (e.g., Edaphosaurus ) are almost the only Carboniferous herbivores.
4. So what feeds the carnivores? Who is the missing herbivore before the Permian (assuming Edaphosaurus not extremely numerous, which it does not seem to be)?

C. Hypotheses:
1. One — The herbivores are all aquatic insects or fish, and the terrestrial vertebrate pyramid is supported by aquatic productivity.
2. Two — Arthropods are primarily detritivores, and energy flows Plant -> detritus -> insect detritivore -> vertebrate carnivore.
a. There is excellent evidence for an active detritivore community from the Devonian on including Oribatid mites and various millipedes.
3. Three — A variant of two. Arthropods are direct herbivores and terrestrial vertebrate carnivores are consuming insects.
a. There is growing evidence that some late Paleozoic insects were serious herbivores with "piercing & sucking" mouthparts to suggest direct feeding.
b. Insects become quite diverse in Carboniferous
c. And "invent" flight — perhaps because the much higher Oxygen content (~35% of total atmosphere) made both flight & muscle activity easier.
d. These spread in their feeding functions — leaf chewers join "piercers" and there may even be gall-formers. In addition, insects find themselves — and become carnivores.
4. The three hypotheses are not mutually exclusive, but none create a system "like the present day".
5. Side question - What effect (if any) on other biogeochemical cycles does the apparently low level of herbivory have?

D. Summary:
1. Some questions are unresolved: Why did it take so long to establish terrestrial vertebrate herbivores?
a. Did it involve adaptations necessary to establish microbial stomach symbionts?
b. Did terrestrial vertebrates have to achieve a certain size in order to be able to support themselves through herbivory, due to its relatively "low" food quality??
2. In any case, the Late Pz terrestrial food web was not at all similar to modern food web. At best, insect herbivores support the carnivores, although possibly plants existed in a relatively "predator-free" environment.
a. One might ask how this affected patterns of plant evolution, but not here.
A. Therapsid herbivores radiate:
1. The first successful herbivores were dicynodont therapsids (e.g. Lystrosaurus) — early members of the "synapsids", the lineage from which mammals arose.
a. These animals develop a grinding jaw motion appropriate for breaking vegetation down.
b. And apparently possess the necessary bulk and gut fauna to consume plants.
c. Great numbers of individuals found, suggesting a radiation in response to this new food resource.
2. This creates a "modern" trophic pyramid, underwriting the therapsid hegemony of later Permian -> Early Tr.
3. In the Early- Mid Tr the Therapsids crash and reptiles rise, presumably in response to global "continentalization" of climate and the resulting change to a conifer-cycad dominated vegetation.

B. Insects continue to diversify
The Usual view: Mesozoic = Cenozoic, but with Dinosaurs, not mammals. Probably t'ain't so.
A. The Players:
1. Plants
a. Late Tr - mid K: Dominated by gymnosperms with an understory of ferns (where moisture permits) Relative to angiosperms, the community has relatively low productivity, and low disturbance tolerance, and forms a fairly open community in lower latitudes. It may be more closed towards the poles. This reflects the wide-spread occurrence of relatively arid climates towards the equator, and relatively more mesic climates towards the poles.
b. Mid K through K/T: Angiosperms radiate. The plant community generates higher productivity, greater tolerance of disturbance, and may generally become more "closed" as angiosperms fill in space. Mesic climates become somewhat more globally wide spread as Pangea breaks up.
2. Insects
a. Undergo a virtual explosion of adaptations
b. New forms include carnivores and blood-suckers, but also several new adaptations to foliage-feeding, sap-sucking and . . . nectar.
c. In addition insects with a juvenile caterpillar/maggot generation became more common.
d. An example of the spread of interaction: the earliest leaf mine is Triassic.
e. Important to angiosperms, several lineages are in place by the beginning of the Cretaceous that consume pollen and are good pollinators.
f. In truth, at least in terms of major insect groups, the appearance of angiosperms did not "force" a great radiation of insects. Rather existing insects simply moved onto new resources
3. Vertebrates:
a. Initially dominated by huge dinosaur herbivores (10x largest living terrestrial herbivore).
b. These fed at many levels, and probably consumed whole plants.
c. Numbers — for 160 MY of Dinosaurs, we know of about 400+ spp. At a liberal guess there might be 1500 species (excluding birds) to be known. That is about 9 spp/MY. There are some 8000 species of mammals known from the Tertiary (65 MY) or about 123 Ps/MY.
4. These numbers bespeak something odd.
a. Either we are missing a lot of the dinosaurian fossil record, or the Mesozoic is not similar to the present day. If the latter . . . Well, let us offer a hypothesis to tie the observations together.

B. Plant-Vertebrate Interaction I: Late Tr - Mid K
1. Big herbivores tend to live in open environments, feed on large quantities of "low quality" food, and are destructive of plants. This model from living big herbivores gives a clue as to dinosaur herbivore biology.
2. The low damage resistance and nutritive value of available plants suggest that:
a. Dinosaur species might have had fewer individuals
b. And that perhaps dinosaurs had to migrate over large areas to find new food.
c. And that dinosaurs are a tremendous source of disturbance in the community.

C. Plant-Vertebrate Interaction II: Mid-Late K
1. Angiosperms evolve (perhaps even in response to great disturbance created by dinosaurs), resulting in a more disturbance-tolerant group of seed plants.
2. Old prediction: Angiosperms "poisoned" the dinosaurs, leading to extinction. Hah!
3. Observations a. Ornithischian radiation corresponds to angiosperm rise. Ornithischians feed much lower to ground, and angiosperms appear as shrubs.
b. Note, Sauropods continue to dominate in gymnosperm-dominated regions.
c. Further, numbers of dinosaurs up
— 50% of all species known from last 20 Million years
— Numbers of individuals up to the thousands.

D. Plant/Insect/Vertebrate interactions?
1. Advanced synapsids (Mammals) survived in the shadows of the dinosaurs through much of the Mesozoic.
a. As insectivores! So the plants were supporting mammals indirectly.
2. In later Cretaceous, mammals begin to diversify
a. In this time, insect-angiosperm interactions (pollination) are becoming increasingly important.
b. Are the mammals again a beneficiary of plant/insect interactions?
c. Is it possible that plant-mammal interactions (herbivory & seed dispersal) arise from the initial introduction mammals got to plants through insects?
A. Why?
1. I suspect that it has many causes, not just an asteroid, etc. It could be that climatic features had destabilized the ecosystem before the asteroid arrived.

B. Features
1. Plants
a. A second radiation occurs, involving modern families & genera of angiosperms.
b. The modern three-dimensional forest comes into being for the first time.
2. Animals
a. Mammals & birds radiate in early Tertiary.
b. This creates a drop in the size of largest herbivore of over 5 orders of magnitude - it is 20MY before a "large" mammalian herbivore evolves (about a ton!).

C. Apparent effect
1. Herbivore disturbance drastically reduced. "Organism" scale herbivory disappears.
2. Radiation of birds & mammals creates intense "Organ" level herbivory.
3. This leads to appearance of many dietary specializations among herbivores and of signs of animal dispersal among plants (coevolution)
4. Parenthetically, the "closed" environment of the Tertiary forests is scaled to mammal/bird herbivore size. Very large mammal herbivores reappear only as grassland (open) habitats evolve.
5. While present data suggest no radiation of insect diversity at the family level, we assume massive diversification below the family level (or have insects always been diverse?)
A. Terrestrial SYSTEMS have evolved, much as individual animals have evolved.
1. Paleozoic: Initially plants predator-free, then slowly attacked by invertebrates, and finally in the Permian, by vertebrates. "Modern" terrestrial ecosystem energy flow appear s only in the later Permian.
2. Mesozoic: The common plants were often of lower productivity, and may have not been particularly disturbance tolerant. Herbivorous vertebrates were dominated by big dinosaurs. This juxtaposition may have dictated a non-modern trophic dynamic, including very few vertebrate herbivores causing great disturbance. This altered in the late Mesozoic with the radiation of disturbance-tolerant angiosperms and "smaller" ornithischia.
3. Cenozoic: Dominated by much smaller herbivores feeding on organs, often of high food value; communities generally were more closed and 3-dimensional. This led to a greater coevolution, perhaps leading to the higher density & diversification of both plants and animals in the Tertiary and present.

B. The Present is not the past, it is only a key to it.

C. Animal evolution appears to track plant evolution.

D. The role of insects in this story is dimly understood.
1. While insects are the most important modern herbivores we are just beginning to develop a sense of their importance in past ecosystems.

E. Diversity is the greatest in the present day that it has ever been on land — perhaps in large part because of the evolution of ecosystems.


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