Bison and seasonal protein

Forage crude protein concentrations (%N * 6.25) for male and female bison over the season from Konza.

Bison are the largest native grazers in North America left. Their history is interesting, having almost gone extinct with the Pleistocene megafauna, and not having evolved into their modern form until about six to eight thousand years ago. Most of the attention on the evolution of the animals has been regarding changes in their morphology. Most of the attention to the modern animals has been their genetics and the introgression of cattle genes—finding “pure” bison. Most of the interest in their modern ecology has been on their role as a keystone in ecosystems.

Almost entirely missing from the study of modern bison has been their nutrition. There has been some work on diet—do they eat forbs or grasses; cool- or warm-season grasses. Yet, animals that ranged throughout North America and never had access to grasses like the progenitors of modern cattle would have found in northern Europe would likely face strong nutritional stress throughout much of the year. The adaptations of bison to low forage quality, no less the basic patterns of the availability of energy and protein to bison have gone all but unasked.

At Konza, Gene Towne has been collecting fecal material throughout 2009. Every two weeks, he has collected fresh pies from both males and females. Then we send the samples off to Texas A&M’s GANLab to see what the crude protein (nitrogen) and digestible organic matter (energy) was of the grass that they were eating.

If you look at the patterns from 2009, a few fascinating patterns stand out. First, the minimum protein requirements for mass gain for cattle are about 6% crude protein. Bison at Konza have about 100 day window to gain mass during the growing season. After that, there is little protein available beyond what is required for maintenance.

Second, the differences between males and females has never been observed before. Males tend to form “bachelor” herds and do their own thing until the rut—roughly August. After that, they often go off on their own again. The CP patterns show that the males are not selecting as high a quality forage early in the season, but the peak is broader. During the rut, quality is about the same as females. Afterwards, the males are selecting lower quality forage than the females. Why? Why wouldn’t the males feed in the same places on the higher forage quality. A mystery right now.

Lastly, by mid-October, CP had dropped to roughly 4.5%. Not much good green out there for anyone. Gene’s found that the bison lose about 10% of their weight during the winter, which can be up to 200 pounds for the large males. We’re beginning to see why.

Hopefully, data like this will continue to be taken at Konza for a couple of years. It’ll be fascinating to see the differences between wet and dry years on forage quality. With any luck, we can start similar measurements at a number of other TNC sites with bison to being broader comparisons.

Climate change and cattle nutritional stress

If you read the latest IPCC report, there is little text on the potential effects of climate change on cattle performance. Considering there are more than 1 billion head of cattle in the world with probably about a trillion dollars in value, small changes in their performance would have large economic effects.

Here’s what the IPCC had to say about climate change and forage quality:

New Knowledge: Changes in forage quality and grazing behaviour are confirmed. Animal requirements for crude proteins from pasture range from 7 to 8% of ingested dry matter for animals at maintenance up to 24 % for the highest-producing dairy cows. In conditions of very low N status, possible reductions in crude proteins under elevated CO2 may put a system into a sub-maintenance level for animal performance (Milchunas et al., 2005). An increase in the legume content of swards may nevertheless compensate for the decline in protein content of the non-fixing plant species (Allard et al., 2003; Picon-Cochard et al., 2004). The decline under elevated CO2 (Polley et al., 2003) of C4 grasses, which are a less nutritious food resource than C3 (Ehleringer et al., 2002), may also compensate for the reduced protein content under elevated CO2. Yet the opposite is expected under associated temperature increases (see Section 5.4.1.2). Large areas of upland Britain are already colonised by relatively unpalatable plant species such as bracken, matt grass and tor grass. At elevated CO2 further changes may be expected in the dominance of these species, which could have detrimental effects on the nutritional value of extensive grasslands to grazing animals (Defra, 2000).

In all, there really wasn’t all that much that we knew about the topic.

I won’t go into detail here, but here's the latest press release from Kansas State on the Global Change Biology paper that I mentioned in an earlier post on the Wisconsin Paradox. I think that the next IPCC report should be able to say a little bit more…

K-STATE RESEARCHERS STUDYING LINK BETWEEN CLIMATE CHANGE AND CATTLE NUTRITIONAL STRESS

MANHATTAN -- Kansas State University's Joseph Craine, research assistant professor in the Division of Biology, and KC Olson, associate professor in animal sciences and industry, have teamed up with some other scientists from across the United States to look into the possible effects of climate change on cattle nutrition.
Comparing grasslands and pastureland in different regions in the U.S., the study, published in Global Change Biology, discusses data from more than 21,000 different fecal samples collected during a 14-year period and analyzed at the Texas A&M University Grazingland Animal Nutrition Lab for nutritional content.
"Owing to the complex interactions among climate, plants, cattle grazing and land management practices, the impacts of climate change on cattle have been hard to predict," said Craine, principal investigator for the project.
The lab measured the amount of crude protein and digestible organic matter retained by cattle in the different regions. The pattern of forage quality observed across regions suggests that a warmer climate would limit protein availability to grazing animals, Craine said.
"This study assumes nothing about patterns of future climate change; it's just a what if," Olson said. "What if there was significant atmosphere enrichment of carbon dioxide? What would it likely do to plant phenology? If there is atmospheric carbon dioxide enrichment, the length of time between when a plant begins to grow and when it reaches physiological maturity may be condensed."
Currently, cattle obtain more than 80 percent of their energy from rangeland, pastureland and other sources of roughage. With projected scenarios of climate warming, plant protein concentrations will diminish in the future. If weight gain isn't to drop, ranchers are likely going to have to manage their herds differently or provide supplemental protein, Craine said.
Any future increases in precipitation would be unlikely to compensate for the declines in forage quality that accompany projected temperature increases. As a result, cattle are likely to experience greater nutritional stress in the future if these geographic patterns hold as a actual example of future climates, Craine said.
"The trickle-down to the average person is essentially thinking ahead of time of what the consequences are going to be for the climate change scenarios that we are looking at and how ranchers are going to change management practices," Craine said.
"In my opinion these are fully manageable changes," Olson said. "They are small, and being prepared just in case it does happen will allow us to adapt our management to what will essentially be a shorter window of high-quality grazing."
Additional investigators on the project include Andrew Elmore at the University of Maryland's Center for Environmental Science and Doug Tolleson from the School of Natural Resources at the University of Arizona, along with the assistance of Texas A&M's Grazingland Animal Nutrition Lab.

Why be efficient? A question for C4 plants

C4 grassland in South Africa with a 1.7 m Carl Morrow for scale.

Species with the C4 photosynthetic pathway are in the minority in terms of species, but fix a large amount of the world's carbon, not to mention world's calories that humans consume.

Species with the C4 photosynthetic pathway differ from C3 species in a number of ways. We know that the C4 photosynthetic pathway evolved, or at least radiated during times of declining atmospheric CO2 concentrations. In accordance, C4 species have higher photosynthetic rates at glacial CO2 concentrations (~200 ppm) than C3 species. Therefore, it is generally thought to be an evolutionary response to low CO2 concentrations. In conditions of high light, low CO2, and warm temperatures, the C4 pathway reduces photorespiration and generates greater photosynthetic rates over C3 species.

Yet, the C4 photosynthetic pathway also confers greater resource use efficiency. The C4 pathway comes with increased energetic costs, but also confers greater photosynthetic water use and nitrogen use efficiency. More carbon is fixed in C4 species per unit water and nitrogen allocated to photosynthesis as internal CO2 concentrations are lower, which drives the greater WUE, and less N is needed for the same amount of photosynthesis, which drives greater NUE.

Some of the characteristics of C4 are a bit mythological. For example, although C4’s can have higher photosynthetic nitrogen use efficiency, many C4’s have high tissue N concentrations and many C3’s have as low an N concentration as the lowest C4. Not everything about plants is destined from photosynthetic properties.

That said, is there selective advantage to being more efficient with resources? Efficiency always comes at a cost. This much we know. You have to be inefficient with one resource to be more efficient with another. Light use efficiency comes at the expense of N use efficiency. N use efficiency comes at the expense of water use efficiency. Efficiency also costs time.

So what is the benefit of being efficient? For C4’s, under what conditions is it beneficial to be more efficient with water or nitrogen than C3’s. In a competitive world, efficiency in and of itself benefits no one but your competitors. The less water or nitrogen you use, the more there is for another. The benefit only comes if efficiency allows one to reduce the availability of the limiting resource below the level needed to sustain a potential competitor. Or tolerate more stressful conditions. Do C4’s reduce water or nitrogen availability to lower levels than C3’s? No evidence of that. Do C4’s tolerate lower water or nitrogen availability than C4’s? No evidence of that, either.

We also know that C4’s span a wide range of water and nitrogen availability. NADP-me type C4’s increase with mean annual precipitation, not decrease. And C4’s like the grasses we use in many lawns and golf courses have high nutrient requirements, not low, having evolved in grazing lawns that have high nutrient availability. In all, there is no evidence that C4’s preferentially occupy low water or low nitrogen habitats.

The efficiency of C4 species is one of the great mysteries of evolution. Is it an interesting by-product of selection for carbon gain under certain conditions? Or is it indirectly linked to success in ways that are not obvious? Likely, until we better understand the fundamental question of “Who wins and why?” in the plant world, that aspect of C4’s will still be a mystery.

When will SLA R.I.P.?

Relationship between leaf tissue density and the abundance of grassland species in uplands at Konza Prairie. Each point is a different species with its abundance measured over 14 years.

For almost two decades, SLA (or its inverse alter-ego, LMA) has reigned supreme as the central functional trait of plants. SLA, i.e. specific leaf area--the ratio of leaf area to mass, has stood to represent the amount of investment into light acquisition. Entire pyramids of approaches to traits are built on the fundamental supremacy of SLA. The only thing more important than SLA in these pyramids is relative growth rate (RGR).

But why SLA? Why the ratio of area to mass? The thinking is that plants that grow fast need to absorb as much light as possible with the least amount of investment. Hence, selection favors plants that produce a lot of leaf area with little carbon investment, i.e. a high SLA. Plants in stressful or low-resource areas have low SLA, which presumably aids plants in resisting stress or maximizing the utilization of a limiting resource. Consistently, there are good correlations between SLA and RGR as well as other leaf characteristics such as photosynthetic rates, which have reinforced the primacy of SLA.

For almost all of the 20 years, there has always been a countervailing opinion of SLA that has never been rectified. If it ever was squared, SLA would likely never be measured again.

A leaf can high SLA either because it is thin or because it has low tissue density—thickness and density are the two components of SLA. In 1991, Witkowski and Lamont examined thickness and density across a series of ecological contrasts for sclerophyllous species. In short, from the patterns they observed, the authors concluded that “leaf density and thickness may respond to independently to resource and other gradients, and thus are more appropriate measures than [SLA] which confounds them.” Because thickness is so easy to measure—a quick squeezing of calipers—there is no good reason to not break down SLA to density and thickness every time.

Thickness and density have different functional roles in a leaf. They often vary independently across ecological contrasts. A thick, low density leaf and a thin, high density leaf would have the same SLA, but very different performances in most environments. By extension, SLA might be important to plant ecologists, but not to selection.

But maybe this is a bit hasty. SLA is supposed to be ecologically important and help explain the abundance of species across contrasts. Maybe SLA explains abundance better than thickness or tissue density. Surprisingly, the relative explanatory of SLA and its components have rarely been tested quantitatively. In general, this is probably the Achilles heel of most traits work. We spend more time examining relationships among traits than rigorously testing their relative predictive capacity.

Refuting the ecological importance of SLA or either of its components will not be a simple affair. It’ll take a number of studies before we understand their relative empirical importance. I’ve now done two. The first was at Cedar Creek along fertilization and disturbance gradients. The second is at Konza where I measured leaf traits for 130 grassland herbaceous species and tested their predictive capacity for species abundance across topographic, burning, and grazing contrasts. The results for Konza? SLA explained no variation in the abundance of species. Yet, tissue density did. Consistently across gradients it was tissue density not SLA that explained the abundance of species. The Cedar Creek work largely concluded the same thing.

SLA should not be buried yet, but at some point, we are going to have to fundamentally reexamine the hierarchy of traits in the ecology of plants. A dichotomous world of high SLA and low SLA (if not high RGR and low RGR) plant species might have to be replaced. Until then, at the very least, measure thickness.

Canopy interception and the dispersed puddle

Taking a walk through grass after a light rain is a soaking affair. Even walking through a recently mowed lawn in the morning would wet your sneakers while going to school. It was always better to let the sun come out for a little bit before short-cutting across a yard.

The principle that most children learn at a young age likely has important ramifications for understanding the dynamics of how grasslands work. Through one of two mechanisms, my guess is that canopy interception sets up a negative feedback loop that constrains how much grass is produced.

First, a quick review.

In grasslands, approximately half of the precipitation can be intercepted by biomass without reaching the soils. For small precipitation events, 70% of the precipitation can be intercepted by a dry canopy, with the fraction of precipitation intercepted declining with event size (Ataroff and Naranjo 2009). A single square meter of grassland can withhold 2 L of water from reaching the soil.

Relationship between precipitation and canopy interception for a tropical pasture grass. From Ataroff and Naranjo 2009.

Half of the precipitation that could fall on a grassland might never reach the soil. And the more grass there is, the less precipitation would reach the soil. Seasonally, as grass grows and canopies develop, the demand for water would be ever increasing. Yet, because of interception, less and less precipitation would reach the soil.

Increasing demand, decreasing supply. A classic negative feedback that would be limiting growth. Even if plants had access to deep water, the consequences might be greater for N supply and cause transitive limitation as surface soils where N mineralization occurs would be prevented from rewetting.

Evolutionarily, we haven't explored whether there would be selection on herbaceous species to promote (or not promote!) throughfall of precipitation. Altered leaf angle, waxy cuticles, stemminess, would all alter how much water is retained or passed on to the soil. Ecologically, with just a few papers on the topic, there are likely some large unexplored ramifications besides promoting seasonal water limitations. For example, from first principles, rain coming in larger events should promote growth, not retard it, as the water is stored in the soil rather than the canopy.

Most importantly of all, if you haven't learned it yet, never cut across a wet lawn in the morning wearing sneakers. Might as well jump in a puddle.

The nuts and bolts of transitive limitation

Patterns of soil moisture in the lowlands of an annually burned watershed at Konza Prairie. Soil moisture is expressed on a relative basis at 6 depths for 1993 (wet year) and 1994 (dry year).

Earlier, I had discussed a potentially interesting case of transitive limitation, i.e. when the low availability of one resource reduces the availability of another. In the case of water and nitrogen, it is unclear in grasslands whether the limitation ascribed to water could actually be due to low N availability. N mineralization is known to decrease with decreasing soil moisture. As such, as soil moisture declines, so should N mineralization.

The correlation between soil moisture and N mineralization does not necessarily mean that the two should co-limit across a range of soil moistures. In a given soil profile, soil organic N is generally concentrated in shallow depths, while soil moisture is more evenly distributed throughout the soil profile, if not greater at depth. As such, plants can have access to plenty of water at depth even if shallow soils have dried out. Soil N mineralization and moisture might be correlated for a given volume of soil, but not over the whole soil profile.

Konza is an interesting example. At different times, productivity is said to be limited by water and nitrogen, but the two have never been rectified. Do they simultaneously limit production? Does limitation vary over the course of a season, or across years? Or is it transitive?

If it is transitive, disentangling the two is not easy. Standard factorial resource addition experiments do not work since adding water would also increase N availability. Is there a way to add water without increasing N? Not easily from above. But you could add it from below.

Inferentially, if you look at Konza soil moisture patterns, there is always plenty of water at depth, even in dry times. In the above example, in 1994, soil moistures are depleted in shallow soils, but there is very little draw down of deep soils. Proximally, this could be due to the lack of roots at depth, but we are only talking 1 m. The dominant species could easily produce roots at 1 m--if there was a benefit to doing so. If productivity was water limited, there would be a benefit. Yet, if productivity was actually N limited, accessing deep water provides little benefit when N is not being mineralized.

There are other lines of evidence that support the dominant role of transitive limitation at Konza. For example, regardless of whether you add N or water, the same species--Panicum virgatum--comes to dominate. If N was limiting, wouldn't adding N dry out the soils more and favor a low-water, high-N species?

One of the tough things to demonstrate is the roll that soil water potential plays in productivity. I'll likely expand on this later, but there are no relationships between water potential and productivity, only conductance. If we could show that productivity should not be diminished by lowering soil water potential to say -2 MPa, we might be able to demonstrate that it is not water that is limiting directly, but transitively by reducing N supplies.

There are still multiple pieces to assemble before the story is complete, but transitive limitation is likely a linchpin in understanding grasslands.

Finding the needles in the haystack

There are a fair number of papers that are impressive for the number of times they are cited. “Instant classics” that accrue a hundred citations in a year—most in the first paragraph of a paper—and have helped define some part of a discipline.

These papers are impressive and worthy of study in hopes of replicating them, but I am more interested in papers that are likely just as important but have rarely been cited. Any scientist can use Web of Science to find the most cited paper on a topic and then cite it themselves in order to seem authoritative. But, the true scholar knows the obscure paper, one that might only have been cited a few times a year, but can make the case that the paper is as important as one cited a hundred times a year, if only the obscure one were discovered.

I do not have a comprehensive list, but it is an interesting exercise to think about what are the most important papers never to have been cited. If we restrict the list to the papers published over five years ago and have received less than five citations a year on average. And one cannot put one’s own papers on the list, which is unfortunate since most of my CV is obscure but important. (Except for the one soil CO2 flux paper in GCB. That one deserves to be obscure.) Here are ones that I came up with:

1) Wahl, S. and P. Ryser. 2000. Root tissue structure is linked to ecological strategies of grasses. New Phytologist 148:459-471. If ever there was a golden key to unlocking root function in different environments, this would be it. Why this study has not been replicated a dozen times, I do not understand. (30 cites)

2) Dietz, H. and F. H. Schweingruber. 2002. Annual rings in native and introduced forbs of lower Michigan, USA. Canadian Journal of Botany 80:642-649. The idea that you can dig up grassland plants and age them should have set fire to our understanding of plant population dynamics in grasslands. (12 cites)

3) McManus, W. R., V. N. E. Robinson, and L. L. Grout. 1977. Physical Distribution Of Mineral Material On Forage Plant-Cell Walls. Australian Journal of Agricultural Research 28:651-662. The idea that plants accumulate minerals on their cell walls and might use them for structural purposes fundamentally alters how we think of plant structure and turns plant stoichiometry on its ear. It’s never been followed up on as far as I know. (12 cites)

4) McNaughton, S. J., J. L. Tarrants, M. M. McNaughton, and R. D. Davis. 1985. Silica as a defense against herbivory and a growth promotor in African grasses. Ecology 66:528-535. This one came to mind after the previous one. Silica as structure changes the game. This became cited a bit more in 2006-7, but other than those two years never had more than 5 citations a year. (85 cites)

I’ll give this some more thought later. This is a hard list to compile (and my kids are awake now). I should be able to come up with a top ten list of obscure papers later.