Long-term declines in dietary nutritional quality for North American cattle

With over 1 billion cattle in the world as well as over 2 billion sheep, goats and buffalo, these livestock species contribute approximately 15% of the global human protein supply while producing a significant proportion of anthropogenic emissions of greenhouse gases and global nutrient fluxes (Steinfeld et al 2006, Bouwman et al 2011, Estell et al 2012, Ripple et al 2013, FAOSTAT 2017). Despite increasing reliance on grazers for protein production globally, the future of grazers in a changing world is uncertain. Factors such as elevated temperatures, reduced precipitation, rising atmospheric CO₂ concentrations, and sustained nutrient export all have the potential to reduce cattle performance by reducing the nutritional quality of forage. Yet, there are no analyses of whether cattle are becoming more nutritionally stressed over time, rendering us unable to determine whether there will be reduced livestock production or a greater need for nutritional supplementation in the future, which would strain natural resources even more.

The crude protein concentration ([CP]) of cattle diet—essentially tissue nitrogen concentrations of consumed plants—often limit cattle weight gain throughout the US, with metabolizable energy derived from digestible organic matter (DOM) in forage a secondary limitation (Craine et al 2010a). Focusing on [CP], despite a number of factors likely to be affecting [CP] in cattle diet, there are little data to assess how [CP] responds to environmental conditions and whether there have been any long-term trends in cattle dietary [CP]. For example, drought might reduce dietary [CP] if water stress promotes senescence (Heckathorn and Delucia 1994). Alternatively drought could increase dietary [CP] if drought reduces photosynthesis more than N uptake, limits protein-poor culm production, or cattle shift which species they consume (Heckathorn and Delucia 1996, Craine et al 2010b). If droughts become more common in the future, the subsequent reduced forage production in isolation would be expected to lower cattle production. Yet, these reductions in productivity could be either offset or exacerbated by changes in [CP] depending on how [CP] responds to drought at a particular time of year (Craine et al 2013). Beyond the specific consequences of droughts for dietary quality, a number of other factors such as rising atmospheric CO₂, warming, and sustained export of nutrients contained in animal biomass all have the potential to chronically reduce soil nutrient availability and consequently dietary nutritional quality (Ainsworth and Long 2005, An et al 2005, McLauchlan 2007).

To test how cattle dietary quality responds to drought and whether there have been trajectories in cattle dietary quality independent of any trends in drought, we utilize a long-term dataset of 36 599 independent measurements of cattle dietary quality obtained throughout the US over a 22 year period. Dietary quality metrics include [CP], as well as digestible organic matter concentration ([DOM]), which is an index of energy availability in forage (Moore et al 1999). As drought conditions have been becoming more common in the central US over the past 20 yr (Dai 2012), we first determine how dietary quality responds to drought for each of ten US ecoregions (figure S1, available at stacks.iop.org/ERL/12/044019/mmedia). We examine relationships between dietary quality metrics that have been standardized for typical seasonal patterns in these metrics and the Palmer Drought Severity Index (PDSI) (Alley 1984) quantified at the time of dietary quality assessment.

Data acquisition

Sample analysis

Data analysis

Modeling weight gain

Calculating economic costs

Across all samples collected from spring through autumn, irrespective of location of origin, [CP] was an average of 9.57 ± 0.12 mg g⁻¹ lower in 2005–2015 than 1994–2004 when compared on the same day of year (100.0 mg g⁻¹ vs. 90.5 mg g⁻¹, respectively; P < 0.001; figure 1). In contrast to [CP], [DOM] was higher in later years than earlier years (2.0 ± 0.2 mg g⁻¹, P < 0.001; figure 1). The increase over time in [DOM] and decline in [CP] led to an increase in [DOM]:[CP], which was 13% higher in 2005–2015 than 1994–2004 (P < 0.001; figure 1).

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As the degree of drought and shifts in the geographic location of samples being analyzed could be driving the observed increases in protein limitation, we first determined residual quality after accounting for the typical seasonal patterns of quality in each of 10 regions for which there were sufficient data to examine interannual trajectories of dietary quality (online supplementary figure S3–S5, table S1). Examining the patterns of PDSI over time, average PDSI of sampled sites was declining or tending to decline for all domains (figure 2(c)). For nine of the ten regions, summer drought increased or tended to increase [CP] (figure 2, table 1). The responses of [DOM] and [DOM]:[CP] to summer drought among regions paralleled those for [CP] (online supplementary figure S6). Those regions for which summer drought increased [CP] the most, summer drought was more likely to increase [DOM] and decrease [DOM]:[CP] (r = 0.86 −0.89 for correlations between coefficients of PDSI responses of [CP] and coefficients of PDSI responses for [DOM], [DOM]:[CP], respectively; P = 0.002, < 0.001 respectively).

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After accounting for the interannual variation in PDSI and drought effects on [CP], [CP] was declining or tending to decline over time in all 10 regions (figure 2(b)) leading to an overall decline in summer [CP] over the 22 yr (figure 2(d)). The greatest declines in [CP] over time were in the Prairie Peninsula (−1.4 ± 0.2 mg g⁻¹ y⁻¹) (figure 2). With the smallest declines, [CP] showed only a trend for declines over time in the Southeast (−0.2 ± 0.3 mg g⁻¹ y⁻¹, P = 0.44). While [CP] has generally been declining over time, [DOM] has been typically increasing (online supplementary figure S7). With the typically increasing trajectory in [DOM] coupled with declining [CP], independent of drought, from 1994–2015, cattle have been becoming more protein limited in summer. [DOM]:[CP] increased in all regions (P ≤ 0.16 for all regions, P < 0.05 for 7 regions) with the Southeast exhibiting the smallest increase (0.018 ± 0.013 y⁻¹; P = 0.16) (figure S7).

In general, patterns in drought response and dietary quality trajectories tended to be similar in spring and autumn as summer. For example, those regions where drought increased [CP] in the summer, also tended to increase [CP] in the autumn (r = 0.51, P = 0.13). After accounting for responses of [CP] to drought, overall, [CP] declined in the spring and autumn from 1994–2015 (online supplementary figure S8). Regions that had the greatest decreases in summer [CP] over time also tended to have the greatest decreases in spring [CP] and autumn [CP] (r = 0.33, P = 0.36; r = 0.52, P = 0.12). Average regional declines in [CP] during the summer (−0.71 mg g⁻¹ y⁻¹) were similar to those in the spring (−0.51 mg g⁻¹ y⁻¹, P = 0.27, n = 10, paired t-test) and were greater than in the autumn (−0.48 mg g⁻¹ y⁻¹, P = 0.005, n = 10, paired t-test), with both spring and autumn trajectories in [CP] typically negative. Only one region showed significant increases in [CP] over time in the spring (Southern Rocky Mountains), and two regions in the autumn (Ozarks and Desert Southwest). [DOM] generally increased over time in the spring and autumn (figure S7, 10), which when paired with declining [CP] during these seasons, led to increases in [DOM]:[CP] (figure S7, 10), signifying greater protein limitation for cattle in spring and autumn as well as summer.

The economic cost of the increasing protein debt was calculated as the amount of soy that would have to be supplemented to cattle in the US to compensate for the declines in protein that have occurred. Over the 270 d spring–autumn period, mean [CP] declined by an average of 10.6 mg g⁻¹ from 1994–2015. In July 2015, there were 86 million cattle not on feed in the US, 27 million of which were calves. Given differences in body size between calves and older cattle while assuming a 2.5% of body weight daily intake rate, the 2015 protein debt relative to 1994 projects to a loss of the equivalent of 5.3 × 10⁹ kg of soybean worth of protein. At US$0.36 kg⁻¹ market price for soy meal, by 2015, the protein debt had increased to a US$1.9 billion annual reduction in protein provision. For reference, this amount is the equivalent of 47% of all soy produced in Iowa in 2015.

Given the long-term declines in [CP], we calculated the consequences of shifts in forage quality between 1994 and 2015 for weight gain of two classes of cattle using the NUTBAL model of cattle performance. Inputs into the model included the modeled nutritional quality of forage in 1994 and 2015. Weather conditions were the same for both simulations and were set to average weather conditions during this period. During the summer, each class of cattle gained less weight in 2015 than 1994, but the temporal pattern and magnitude of reduction in weight gain varied among classes depending on the temporal pattern of their specific nutritional requirements. For a representative cow with calf, the greater protein limitation in 2015 compared to 1994 reduced weight gain over the growing season. In 2015, cows with calves that started at 454 kg at day of year 60 gained 4.9 kg less over the next 270 d than they would have in 1994 given the same environmental conditions with periods in 2015 when weight was actually lost (figure 3). Weight gain reduction was even greater for steers than cows—11.6 kg less weight gain in 2015 than 1994 (figure 3).

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Although minerals are often supplemented for cattle, nitrogen is infrequently supplemented and thus could be depleted long-term. Given the broad declines in [CP] and increases in [DOM]:[CP], three factors stand out as likely to reduce soil nitrogen availability and consequently protein availability: elevated atmospheric CO₂, climatic warming, and sustained nutrient exports associated with animal products export. While CO₂ concentrations have risen by 12% from 1994–2015, mean temperatures have increased on average by 0.34 °C ± 0.02 °C (online supplementary figure S9). Also, nutrients have continued to be exported from grasslands in the form of animal biomass generally without replacement. The relative contributions of each to the decline in forage quality are currently unknown, which limits our ability to mitigate future changes, no less reverse the protein decline already experienced in grasslands. For example, elevated CO₂ can reduce N availability in grasslands via progressive N limitation, which is a series of feedbacks in the N cycle initiated by enhanced photosynthetic rates (Luo et al 2004). With progressive N limitation, N might accumulate in the ecosystem and plant productivity actually increase due to CO₂ fertilization (Luo et al 2006). Yet, with progressive N limitation, even when plant productivity increases, the availability of N relative to photosynthetic potential declines, leading to reduced N concentrations in plants. In contrast, warming reduces N availability long-term by increasing N losses from the ecosystem and reducing ecosystem N stocks (Link et al 2003, An et al 2005). Animal export serves as a loss, too, though it also leads to the export of other elements besides N. As such, warming and N export lead to declines in forage quality by reducing ecosystem N stocks and likely plant productivity.

The declines in [CP] observed here are similar to the declines in foliar N concentrations quantified from herbarium specimens in Kansas over the past 90 yr, where protein was declining at a rate of 0.54 mg protein g⁻¹ y⁻¹ (McLauchlan et al 2010), which is similar to the 0.68 mg protein g⁻¹ y⁻¹ observed across all samples independent of region.

Given the analyses here, the general trends in forage quality over time occur independent of the trends in drought observed over time. The declines in PDSI over time observed here, a pattern consistent with previous analyses (Dai 2012), would likely be reducing the long-term trends in [CP] declines. When drought does occur, it almost universally tended to increase [CP] and [DOM]. Although drought has the potential to reduce plant protein concentrations by increasing resorption of N (Heckathorn and Delucia 1994), other processes must be dominating over this since [CP] is higher during drier times. Drought could be associated with greater [CP] by limiting accumulation of carbohydrates, but [DOM] also increased with drought. This suggests that drought might reduce the production of indigestible fractions such as lignin, which could correspond to reduced culm production that occurs with drought (Craine et al 2010b). Drought might also shift the selection of intake from low-quality to high-quality plant species, but this hypothesis requires more testing. In general, drought increasing forage quality would suggest that weight gain should be higher in drier years assuming sufficient forage availability. Some patterns of weight gain for cattle seem independent of precipitation or even reduced by drought (MacNeil 2012), but reduced precipitation increasing weight gain has been observed for bison (Craine et al 2009).

If the drivers of the reduction of protein in plants cannot be identified and reversed, or adaptation strategies enacted, the protein debt is only likely to grow, which might begin to cause a net decline in cattle production barring further improvements to cattle genetics. The consequences of declining [CP] and increasing [DOM]:[CP] extend beyond greater nutritional stress as they would also promote greater methane production, which could serve as a positive feedback to warming (Johnson and Johnson 1995). Barring wide-spread mitigation of reduction in greenhouse gases, scenarios for adaptation should begin to be examined unless reductions in forage quality are to be tolerated. In response to declining forage quality, managers could also opt to increase the use of N fertilizer for hay production, promote N₂-fixing plant species, increase transport of hay and supplemental feeds, and/or increase the seasonal transport of animals from lower protein areas to higher protein areas (Zilverberg et al 2011, Joyce et al 2013). Among the most likely efforts to be attempted, the economic viability and ecological consequences of increasing nitrogen availability on grasslands to counter the growing protein debt will need assessment.

The authors would like to acknowledge Sandra Hamel for advice on statistics and Joe Fargione for comments on the manuscript. The forage quality results presented here would not have been possible without the vision and work of the late Jerry Stuth, the initial fecal NIRS calibrations for cattle developed by Robert K Lyons, the contributions of the GAN Lab staff in sample processing and analysis, and livestock producers participating in nutritional monitoring. The work by Angerer was conducted under the USDA National Institute of Food and Agriculture, Hatch/Evans-Allen/McIntire Stennis project 1009337. Data for the paper are archived in Dryad at https//doi.org/10.5061/dryad.n856r.