Higher apical meristem in tall fescue as adaptation strategy to recurring short-term inundation

Abstract

Soil inundation frequency and intensity in the central United States are predicted to increase because of climate change. Soil inundation is expected to negatively affect plant growth and persistency. Our objective was to measure tiller and apical meristem height, leaf area index (LAI), and leaf-to-stem ratio effects on tall fescue (Schedonorus arundinaceus (Schreb.)) under different levels of soil inundation intensity. The study was conducted on a commercial farm in northwestern Ohio, from spring to fall 2021. Three different levels of inundation were observed and assigned as treatments: no inundation, low inundation (LI), and high inundation (HI). LI and HI were defined by the duration on which the soil was inundated after heavy rain events: 1–2 and 3–5 days after rain, respectively. Meristem and tiller height were higher during spring (p < 0.001), and lower in late summer across treatments (p < 0.001). The higher LAI and leaf-to-stem ratio occurred in spring, probably due to higher leaf mass (p < 0.001). As seasons progressed, plant and meristem height, LAI, and leaf mass decreased (p < 0.001). Despite not being considered an inundation-tolerant species, tall fescue showed morphological adaptation to the inundation levels of our study, suggesting that this species can be used to manage fields prone to short-term inundation.

Abbreviations

HI

high inundation

LAI

leaf area index

LI

low inundation

NI

no inundation

1 INTRODUCTION

Soil inundation frequency and intensity in the central United States are predicted to increase because of variations in precipitation patterns resulting from climate change (Mallakpour & Villarini, 2015). In Ohio and other Midwestern states, recurring short-term soil inundation is common in agriculturally productive areas (Starr, 2019; Turner, 2017). In this region, inundation happens after intense rainfall, with approximately 100 m of water accumulated above the soil surface, lasting 4–5 days. Inundation is present primarily during spring and fall, three–four times every year. State programs, such as the Working Lands Buffer Program (Ohio Department of Agriculture, 2019), encourage the conversion of inundation-prone row crop fields into perennial forage crops to reduce nutrient loss via runoff (Bohlen & Villapando, 2011; Bohlen et al., 2009). Nonetheless, soil inundation is expected to negatively affect plant growth (Loka et al., 2019; Vashisht et al., 2011).

Following soil saturation, available oxygen is decreased, reducing root respiration and photosynthesis rates, nutrient uptake, and plant development (Ploschuk et al., 2017). Inundation-tolerant forage species, such as reed canary grass (Phalaris arundinacea L.) (Kercher & Zedler et al., 2004) and timothy (Phleum pratense L.) (Jørgensen et al., 2020), increase stem elongation and meristem height to keep leaves above the water level (Baruch, 1994), but at the expense of reduced forage quality due to lower leaf–stem ratio (Moore et al., 2020). Additionally, higher heights place meristem at risk of more frequent removal during hay mowing or grazing. According to literature, tall fescue (also called Kentucky 31 fescue or meadow fescue, Schedonorus arundinaceus Schreb.) is not considered tolerant to long-term inundation (>3 weeks) (Jansen et al., 2005); however, it is currently planted under shorter duration in Ohio. Under these conditions, tall fescue may respond in a manner similar to inundation-tolerant species by exhibiting a higher stem elongation rate that results in not only greater tiller and apical meristem heights but also lower leaf-to-stem ratio. Tall fescue represents the main cool-season forage species in the US Midwest region (Stuedemann & Hoveland, 1988), hence knowing how this forage can perform under prone-to-inundation areas is of interest for appropriate management strategies. Therefore, our objective was to measure tiller and apical meristem height, leaf area index (LAI), and leaf-to-stem ratio effects on tall fescue under different levels of soil inundation intensity.

2 MATERIALS AND METHODS

The study was conducted on a commercial farm in Jenera, northwestern Ohio (40.8922° latitude and 83.71° longitude, 857 feet altitude). The climate of the location is a Dfa, according to Koppen, with 858 mm of annual average rain precipitation, 5 mm of annual average snowfall, and 10.5°C annual average temperature. The farm is located within the Lake Erie Basin, where fields are inundation prone. Fields had been cultivated with corn–soybeans rotation for the past 20 years. In fall 2019, a few of the farm fields were converted to a forage mix for hay, as part of the Working Lands Buffer Program, covering an area of 3.7 ha. The mix seeding rate was 37.5 kg ha⁻¹ and contained 30% endophyte-free tall fescue 12.5% of timothy (Phleum pratense L.), 22.5% of red clover (Trifolium pratense L.), 12.5% birdsfoot trefoil (Lotus corniculatus L.), and 22.5% Italian ryegrass (Lolium multiflorum Lam.). Although a diverse species mixture was planted, only tall fescue and red clover germinated and established. The area was never grazed. Hay was first cut in Spring 2020 and followed a schedule of three cuttings per year (spring, summer, late summer, or early fall). Fertilization rates were 10–20 kg N ha⁻¹, 40–60 kg P ha⁻¹, and 140–160 kg K ha⁻¹ applied each year in the fall.

Core Ideas

• Tall fescue meristem and tiller height increased in response to inundation intensity.
• Inundation resulted in higher stem mass but leaf proportion remained stable.
• Tall fescue showed morphological adaptation to persist the short-term inundation events.

Three different levels of inundation were observed and assigned as treatments: no inundation (NI), low inundation (LI), and high inundation (HI), each covering approximately one-third of the hayfield area. Here, inundation was naturally occurring, not simulated nor controlled, and varied between treatments due to differences in landscape position across the field (Figure 1). Despite different levels of inundation, duration, intensity, and timing, the entire field had similar management practices described in this document (seed rate, hay mix seeds, fertilization, and harvest). This study evaluated effects of inundation intensity on tall fescue only. Effects on red clover were not evaluated. Leaves and stems growth in legumes is not linear because they expand in two different directions: length and width. Legume leaf elongation, for instance, cannot be determined based on linear measurements of leaf length, as it is usually done for grass species. Additionally, red clover is not planted as the main crop in inundation-prone areas in the Midwest, as is tall fescue.

FIGURE 1

Inundated and non-inundated experimental fields in Jenera, OH. Hayfield treatments are allocated as no inundation (NI), low inundation (LI), and high inundation (HI). Red circles represent wells placement.

Inundation intensity was first identified by the farmer over the past 30 years of cultivation in this area. During the present experiment, inundation intensity was monitored and characterized. To describe treatments, water table level, occurrence of soil inundation, and water height above the soil during inundation were monitored. In May 2021, three pressure transducers with groundwater wells were installed, one in each treatment area, to monitor the water table level (Figure 1). Pressure transducers (Onset–HOBO water level data logger) captured well pressure (psi) and well water temperature (°F) every 15 min. The data were collected using a shuttle (Onset–HOBO waterproof shuttle). The wells were installed to a depth of 1.2–1.4 m, depending on bed rock. The occurrence of soil inundation and the water height above soil surface during inundation were monitored during the experimental period (May to November 2021), based on the squelchy noise methodology adapted from Rinderer et al. (2012). Plots were screened for inundation following all rain events during the experimental period. In each plot, 20 spots distanced approximately 1 m were set in a “zigzag walk.” In each spot, the soil was categorized as (1) non-saturated at the surface, totally dry; (2) saturated at the surface but with no visible water above the soil surface (squelchy noise could be heard when stepping on the ground; Rinderer et al., 2012); and (3) saturated at the soil surface and with visible water. For the purposes of this study, spots categorized as (2) were also considered “inundated” because the water table was high enough to interfere with forage growth and development. Therefore, the sum of observations (2) and (3) was considered as the total number of inundated soil observations. When five or more inundation observations were present, field was considered inundated. To identify a threshold water table height that would result in inundation, the height of water table provided by wells was correlated with the total number of observed inundated soil spots in the field during inundation events. Figure 2 shows the water table height of the treatments during the experimental trial. Three plots (20 m × 20 m) in each treatment were monitored.

FIGURE 2

Water table depth, air temperature, and precipitation from May to December 2021. The dashed line at 400-mm water table depth indicates the threshold on which inundation happens. This was defined as the relation between visual identification of inundation, according to Rinderer et al. (2012), and the water table level measured at the plots. HI, high inundation; LI, low inundation; NI, no inundation.

Soil samples were collected in May 2021 for baseline texture and fertility analyses. Soil samples were collected at 15-cm depth and analyzed for pH, soil organic matter, cation exchange capacity, phosphorus (P), potassium (K), magnesium (Mg), calcium (Ca), zinc (Zn), copper (Cu), sulfur (S), and soil texture (sand, silt, and clay percentage) (Table 1).

TABLE 1. Soil texture and fertility at the study site, before experiment implementation in Jenera, OH.

	NI	LI	HI
pH	6.2	5.9	6.2
SOM (%)	2.8	4	4.1
CEC (cmolc kg^−1 soil)	14	23.1	20.5
P (mg kg^−1 soil)	45	59	44
K (cmolc kg^−1 soil)	0.31	0.36	0.30
Mg (cmolc kg^−1 soil)	2.43	3.88	3.81
Ca (cmolc kg^−1 soil)	7.41	12.61	12.54
Zn (cmolc kg^−1 soil)	3	4.1	3.6
Cu (cmolc kg^−1 soil)	3.3	6.3	7.6
S (cmolc kg^−1 soil)	8.3	8.3	8.5
Sand (%)	35.2	28.6	34.2
Silt (%)	35.2	29.3	27.3
Clay (%)	29.6	42.1	38.5

• Abbreviations: CEC, cation exchange capacity; HI, high inundation; LI, low inundation; NI, no inundation; SOM, soil organic matter.

In 2021, hay was cut at late boot stage in spring on May 29, early summer on July 24, and late summer on September 8 at 10-cm height. Approximately 2 weeks prior to each hay cutting, 30 tillers of tall fescue from different plants were randomly collected per plot at soil level. Tillers were evaluated by total height and split longitudinally to identify apical meristem height to the soil level. Leaves were separated from stems, and blades were analyzed in leaf area meter (LI-COR LI-3100C) to obtain LAI. Leaves and stems were dried and weighed separately, and leaf-to-stem ratio was calculated.

Data were analyzed on SAS with a mixed model (PROC MIXED; SAS 9.4; SAS Institute Inc.). Treatments are the inundation levels. Since inundation is expected primarily during spring and fall, seasons effect was also explored (effects of seasonality). Treatment allocation could not be truly randomized because inundation was neither simulated nor controlled. The experiment design is completely randomized, with pseudoreplicates. For tiller height and meristem height, pseudoreplicates were tillers nested within plots (Drinkwater, 2002; Fiksel, 2006; n = 3 plots per treatment) and the random term. For LAI, leaves and stems proportion and leave-to-stem ratio, values were determined per plot, and plot was considered the pseudoreplicate (n = 3). The season by treatment interaction was tested and the effects were significant for all variables measured (p < 0.01).

3 RESULTS AND DISCUSSION

3.1 Inundation and forage composition

The water table height provided by wells (Figure 2) shows water level variation that is in accordance with levels of inundation in the treatment's plots (lower water level for NI, followed by LI, and then HI). The water level represents the water inside the well; values closer to 0 mm indicate high water table, closer to the soil surface. Water level was consistently higher in HI, followed by LI and NI, respectively, representing a pattern consistent with expected inundation levels. During the experimental duration, no inundation was observed in NI treatment, which might be related to its slightly higher elevation than other treatments. LI and HI also presented a higher organic matter and clay contents than NI, which might be related to the deposition of fine-grain sediments and litter during the recurring inundation events (Bai et al., 2020).

Timothy, birdsfoot trefoil, and Italian ryegrass did not emerge and were not observed in the field. These results are interesting, since timothy grass has been previously described as an inundation-tolerant species (Jørgensen et al., 2020). We did not evaluate further effects of inundation on establishment of timothy and other grasses and recommend this topic to be explored. In 2021, botanical composition remained constant overall, as there were no effects of inundation levels on tall fescue and red clover proportions (p > 0.05). Across treatments, tall fescue proportion was 41% and red clover was 51%. The remainder was dead material (on average, 8%).

3.2 Effects of seasonality

Analysis showed a clear season effect for all measured variables (Table 2). Meristem and tiller height were higher during spring, and lower in late summer (Table 2). The higher LAI and leaf-to-stem ratio occurred in spring as a result of higher leaf mass (Table 2). As seasons progressed, plant and meristem height, LAI, and leaf mass decreased (p < 0.05). These results indicate the negative effects of summer slump on cool-season grasses, as the higher temperatures and lower precipitation during summer (Figure 2) result in a lower regrowth rate (Waldron et al., 2018).

TABLE 2. Average tiller height, meristem height, leaf area index (LAI), tiller leaves and stems dry matter (DM), and leaf-to-stem during spring, early summer, and late summer, 2021 in no inundation (NI), low inundation (LI), and high inundation (HI) forge plots in Jenera, OH.

	Spring	Early summer	Late summer	p-value
Tiller height (cm)
NI	75.9bA	54.9bB	46.1bC	Treat < 0.001
LI	72.2cA	56.0bB	52.2aC	Season < 0.001
HI	86.5aA	64.7aB	42.1cC	Treat × season < 0.001
Meristem height (cm)
NI	35.4bA	29.5bB	14.5bC	Treat < 0.001
LI	29.1cA	30.2bA	21.0aB	Season < 0.001
HI	40.7aA	34.7aB	19.2aC	Treat × season < 0.001
LAI (cm)
NI	777.8bA	232.9abB	267.5bB	Treat < 0.001
LI	793.7bA	245.1aB	376.7aB	Season < 0.001
HI	1062.0aA	214.7bB	190.1cB	Treat × season < 0.001
Leaves DM (g)
NI	6.7cA	1.8aC	2.5aB	Treat < 0.001
LI	7.7bA	1.9aC	2.7aB	Season < 0.001
HI	9.8aA	1.6aC	2.0bB	Treat × season < 0.001
Stems DM (g)
NI	19.1bA	12.8bB	6.7aC	Treat < 0.001
LI	19.1bA	13.9bB	7.3aC	Season < 0.001
HI	29.4aA	15.5aB	6.2aC	Treat × season < 0.001
Leaf-to-stem ratio
NI	0.36bA	0.14aB	0.39aA	Treat < 0.001
LI	0.41aA	0.14aC	0.37aB	Season < 0.001
HI	0.35bA	0.11aC	0.31bB	Treat × season < 0.001

• Note: Standard error (n = 3) for tiller height is 0.76; for meristem height is 0.63; for LAI is 7.86; for leaves DM is 0.18; for stems DM is 1.01; and for leaf-to-stem ratio is 0.01. Lowercase letters indicate differences between treatments (NI, LI, and HI) within seasons at the 0.005 probability level. Capital letters indicate differences between seasons within treatments at the 0.005 probability level.

3.3 Effects of inundation

Tall fescue under HI occurrence presented higher meristem height and, in general, increased tiller height (Table 1). During early summer, HI had higher tiller and apical meristem height but lower LAI in comparison with NI and LI. During spring, the same pattern was observed for tiller and apical meristem height, but HI resulted in higher LAI. During late summer, however, HI presented lower tiller height and LAI in comparison to NI. Additionally, in later summer, HI and LI had higher apical meristem height than NI. In general, HI also resulted in higher stem mass than LI and NI.

The larger differences in the morphological attributes between inundated and NI plants occurred during spring and early summer, when inundation occurrence was higher (Figure 1), suggesting higher stem elongation under recurring short-term soil inundation, which is different from previous studies evaluating long-term soil inundation (Jansen et al., 2005). The implication of higher apical meristem height is a greater risk of its removal by harvest, which leads to slower regrowth rate and eventually tiller death. For the hayfields studied, the apical meristem height was always greater than hay cutting height. If the pastures were grazed, target grazing heights should be adjusted to forage removal of less than 50% (average across seasons) to avoid apical meristem removal, allowing faster regrowth, tiller survival, and an increased number of grazing cycles.

Lack of clear inundation effects on LAI and leaf-to-stem ratio suggests that stem elongation was not severe enough to affect leaf production and proportion. As these parameters are often associated with forage quality, our results suggest that tall fescue can be a viable forage alternative for the management of areas prone to inundation. Tall fescue under soil inundation inferior to 5 days presented higher meristem and tiller height, demonstrating a similar survival strategy to inundation-tolerant forage species (i.e., greater tiller and apical meristem heights).

4 CONCLUSION

Our hypothesis was that under short-term inundation, tall fescue may respond in a manner similar to inundation-tolerant species, with higher stem elongation rate that results in not only greater tiller and apical meristem heights but also lower leaf-to-stem ratio. The hypothesis was only partially corroborated. Tall fescue demonstrated some morphological adaptation to inundation, such as higher tiller and meristem height. However, no clear effects were observed on leaf-to-stem ratio. Tiller density and forage productivity were not evaluated and could also have been affected by inundation levels. Although a diverse forage mix was planted, only tall fescue and red clover were established. We did not evaluate the effects of forage species competition for resources under inundation to understand the lack of establishment of the additional species. Especially considering that timothy grass was sowed, and is considered an inundation-tolerant species. We recommend further research on these topics. Nevertheless, lack of emergence of these grasses corroborates the successful establishment and productivity of tall fescue in areas prone to recurring short-term soil inundation.

AUTHOR CONTRIBUTIONS

Marina Miquilini: Data curation; formal analysis; funding acquisition; methodology; writing—original draft. Ricardo Henrique Ribeiro: Data curation; formal analysis; methodology; writing—original draft; writing—review and editing. Spencer Bauman: Data curation. Steve W. Lyon: Conceptualization; investigation; methodology; supervision; writing—review and editing. Marília B. Chiavegato: Conceptualization; funding acquisition; investigation; methodology; project administration; supervision; writing—original draft; writing—review and editing.

ACKNOWLEDGMENTS

The authors would like to acknowledge the National Institute of Food and Agriculture, U.S. Department of Agriculture, under agreement number 2019-38640-29879, through the North Central Region Sustainable Agriculture Research and Education (NCR-SARE) progaram under project number GNC20-309. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the aauthors and do not necessarily reflect the view of the U.S. Department of Agriculture.

CONFLICT OF INTEREST STATEMENT

Authors declare no conflicts of interest.