The world is green with plants. The world also has thousands of species of plant-eating insects and other organisms. Why don’t all those insects eat all the plants? Why does the world stay green? TCR White, an entomologist from New Zealand, asks this question in a book (White 2005) and a series of fascinating papers. White argues that the answer is not predators, it’s not a balance of nature, it’s not natural feedback loops that keep the world green, it’s the lack of quality food.
Because plant-eating insects are the most numerous of the herbivores and because they can increase their numbers rapidly when conditions allow, I will focus mainly on them, just as White did. What keeps all these plant-eating insects in check? Ecologists have done studies to see if it was the predators of these herbivores limiting their populations (“regulated” in ecological terminology). White summarizes the results: “Experimental and observational evidence reveals that predators in natural environments do not regulate their prey: they are passengers, not drivers” (White, 2013). Neither insect predators nor birds have much influence on the number of herbivore insects, despite the capability of many of these organisms to reproduce quickly (White, 2005).
When circumstances allow herbivore populations to increase rapidly (more on this below), research finds that predators can neither reproduce fast enough or hunt efficiently enough to provide any sort of control (White, 2013). It is only when the herbivore populations begin to decrease that predators appear to be controlling the abundance of herbivores. While White admits to exceptions, he believes these prove the rule.
“There are numerous other examples that demonstrated how predators of both vertebrates and invertebrates can be seen to apparently regulate their prey, but in reality can only depress their numbers when a shortage of food has already decreased the prey’s ability to reproduce.” (White 2013)
What else could keep herbivore populations in check?
Not Balance of Nature, nor Feedback Loops, nor Self-Regulation
“There is no such thing as an environment with a constant carrying capacity: the amount of food in a herbivore’s habitat is constantly changing, largely under the influence of changes in the weather.” (White, 2013).
Related to the idea that predators regulate herbivore populations, ecologists have published many papers looking at the density dependence of populations. A population is said to be regulated around an equilibrium level by the density of its population, or how crowded it is. The theory is that factors which affect the death rates of herbivores interact with their density such that when populations get higher, the death rate increases, providing a negative feedback loop. This is the “balance” in the balance of nature.
White contends that most observations of density dependence are conducted in enclosed environments with set amounts of space and food, where the herbivores cannot wander away in search of greener grass (White, 2007, 2008). Therefore, he concludes, the equilibrium around which an herbivore population fluctuates is simply a figment of our math, the average population that an environment can support. It is a correlation, not a cause, and does not explain how or why populations are what they are (White, 2014). It is also unreliable for prediction of populations because it describes what past factors have produced and those factors (weather effects on food supply) are always changing.
“Weather determines the amount of plant food available. The amount of quality food then determines the population. (White, 2008).
The Inadequacy of the Environment
If neither predators nor density-related factors can give us consistent control of herbivore populations, what prevents unlimited growth of herbivores and why do we sometimes see their populations explode? White concludes that the answer is food. Because of the limits in quantity, and especially quality of food available, food limits the populations of both prey and predators.
But it looks like there is plenty of food available, right? The world is still green and I have to mow my lawn. This is where the inadequate quality of food comes in. In particular, it is the insufficient availability of nitrogen to supply the protein needs of young herbivores that limits populations. In my lawn, they face plentiful, accessible food, most of which is carbon. Oxygen, hydrogen, and carbon, are all plentiful in the world or made plentiful by plants which have figured out how to use carbon for their structure. It is nitrogen that is most often the limiting factor. This is especially true for young herbivores.
“The productivity of all life on Earth, in both terrestrial and aquatic environments, is limited by biologically available nitrogen.” (White, 1993),
Most herbivores produce more offspring than the available resources can support. The problem for these young herbivores is that they cannot be herbivores and also survive. As White puts it, “Young herbivores are not herbivores.” (White 1985). Whether it be calves drinking milk, birds that are herbivores as adults eating insects when young, or young herbivorous fish feeding on plankton, the need for high-protein food is most acute at the very early stages of life. With a few noted exceptions, they will die without a supply of animal or microbial protein. This is an essential resource for which there is no substitute. And most do not survive; the “passive inadequacy of the environment” kills most young animals.
White cites many examples of studies showing that most young herbivores die from lack of quality food in their first few hours or days of life, unheard and unseen. Consider the nymphs of psyllids, most of which “die a day or two after they have settled and started to feed. No predators, parasites, or diseases attacked them, no competitors vied with them for any resource, nor was the weather too hot or too cold, too wet or too dry. And their food was abundant and palatable, but lethally inadequate, so they starved while eating their fill from the phloem.” White concludes that because this mass, early death is unobserved, other factors limiting populations are offered, “The ecologist is left to assume that predators ate them, or rain washed them away, or they died of cold…” (White 1993).
Yet, if you look at the total amount of nitrogen (protein) in an environment, it appears to be sufficient for many more organisms than are present. White identifies the problem: the nitrogen is diluted, spread too thinly in its sources, especially in plants. This dilution is in both space and time. In space, nitrogen is dilute in plants except in fresh growth. In time, from the viewpoint of a young, quickly growing organism needing protein to survive, they can’t eat it fast enough to get the protein they need. They can suck sap all day and still not get enough; they starve in the midst of air containing 78% nitrogen, present yet unavailable.
Although we are not strict herbivores, the availability of nitrogen/protein also restricts us, or it did. Before Haber-Bosch and synthetic nitrogen, humans were in the same predicament as other herbivores; where do we get enough nitrogen? Now that we have overcome this limitation, 48% of our population is reliant on synthetic nitrogen (Our World in Data), which we apply to the annual crops which supply most of our calories.
The Exception: Outbreaks of Herbivore Pests
While the norm is the White’s “inadequate environment,” there are brief windows when the inadequate environment disappears, when food, in quantity and quality, become suddenly available. Herbivores can then reproduce to their capacity, the young survive, and populations explode. Consider a grasshopper outbreak during a drought. As drought dries plants, proteins are broken down to soluble amino acids. This increases the quality of the plant food for the grasshoppers and so they reproduce more than a normal year where protein is not as concentrated.
Reay-Jones et al. (2005) observed similar with the Mexican Rice Borer, “Stress from a lack of water increased amino acids essential to insect growth and development in the cane, resulting in higher survival of the newly hatched moth larvae that bore in the stems. Irrigation resulted in a 2.5x reduction of injury.”
A different mechanism but the same result was found in a study of the African armyworm: rain falling on drought-heated-and-dried soil increased the availability of nitrogen. Grasses took up this nitrogen, allowing more young grass-feeding insect larvae to survive, and leading to an outbreak (Janssen 1993).
The world stays green
“The supply of available nitrogen is a limiting factor of life” (Keeble, as quoted in White, 1993)
What about in agriculture where we must supply nitrogen to crops to maintain yields and protein? A recent review of insect pest management in agriculture had this to say: “Fertilization is a key component in most cropping systems, with nitrogen (N) being among the most frequently applied fertilizers and triggering bottom-up effects on second [herbivores] and third [predators of herbivores] trophic levels,” (Han et al., 2022). White (2008) states similarly, “Insects feeding on plants with more nitrogen survive better, grow larger, develop more rapidly and achieve significantly higher densities, largely unaffected by their predators.” We can expect more plant feeding pests in agriculture because agriculture is a more adequate environment than unmanaged nature.
Agriculture aside, most of what grows is not eaten. In fact, decomposers end up with 90% of all plant biomass because herbivores cannot use it (White 1993). Does it always come down to the quality of food? No. White1 was acutely focused on food as a driver of herbivore populations. However, whenever we are focused on only one explanation, we tend to see only that explanation; scientists are not immune to confirmation bias. That is probably the case here, but the sheer number of examples which fit White’s food hypothesis show it is always a good place to start in looking for explanations of why the world stays green, and why I have to mow my lawn.
Han, P., A.-V. Lavoir, C. Rodriguez-Saona, and N. Desneux. 2022. Bottom-Up Forces in Agroecosystems and Their Potential Impact on Arthropod Pest Management. Annual Review of Entomology 67(1). doi: 10.1146/annurev-ento-060121-060505.
Janssen, J. a. M. 1993. Soil nutrient availability in a primary outbreak area of the African armyworm, Spodoptera exempta (Lepidoptera: Noctuidae), in relation to drought intensity and outbreak development in Kenya. Bulletin of Entomological Research 83(4): 579–593. doi: 10.1017/S0007485300040001.
Reay-Jones, F.P.F., A.T. Showler, T.E. Reagan, B.L. Legendre, M.O. Way, et al. 2005. Integrated Tactics for Managing the Mexican Rice Borer (Lepidoptera: Crambidae) in Sugarcane. Environmental Entomology 34(6): 1558–1565. doi: 10.1603/0046-225X-34.6.1558.
White, T.C.R. 1985. When is a herbivore not a herbivore? Oecologia 67(4): 596–597. doi: 10.1007/BF00790034.
White, T.C.R. 1993. The Inadequate Environment: Nitrogen and the Abundance of Animals. 1st edition. Springer, Berlin; New York.
White, T.C. 2005. Why does the world stay green?: nutrition and survival of plant-eaters. CSIRO Publishing.
White, T.C.R. 2007. Resolving the limitation – regulation debate. Ecol Res 22(2): 354–357. doi: 10.1007/s11284-006-0043-7.
White, T.C.R. 2008. The role of food, weather and climate in limiting the abundance of animals. Biological Reviews 83(3): 227–248. doi: 10.1111/j.1469-185X.2008.00041.x.
White, T.C.R. 2013. Experimental and observational evidence reveals that predators in natural environments do not regulate their prey: They are passengers, not drivers. Acta Oecologica 53: 73–87. doi: 10.1016/j.actao.2013.09.007.
White, T.C.R. 2014. Revisiting the ecological Tower of Babel: should the term ‘density dependence’ be abandoned? New Zealand Journal of Zoology 41(1): 77–78. doi: 10.1080/03014223.2013.827127.