Nematodes are roundworms and are the most abundant group of animals on the planet, representing an estimated four out of five animals on Earth (Bongers, 1999). The nematode community contains herbivorous (plant-parasitic), mycophagous (fungivores), bacterivorous (bacterivores), omnivorous (omnivores), and predaceous (predators) nematodes. Because plant-parasitic nematodes account for $216 billion in global crop losses per year, agricultural nematology efforts focus on their management with little regard to impacts on the rest of the nematode community (Nyaku
Bongers and Ferris (1999) developed a method for evaluating ecosystem health by partitioning groups of nematodes based on their feeding strategies, which were further developed into nematode ecological indices (Ferris
Nematode ecological indices, c-p groups, and interpretation.
Index name | Abbreviation | c-p nematodesa | Indication (high value)b |
---|---|---|---|
Maturity | MI | 1–5 | Stable/enriched environment |
Enrichment | EI | 1–2 | Enriched environment |
Structure | SI | 3–5 | High food web complexity |
Channel | CI | 1–2 | Fungal-dominated decomposition |
Basal | BI | 2 | Stressed/degraded environment |
aBased on weighted proportions of colonizer-persister series included in calculation of index (Bongers and Bongers, 1998).
bHigh value as an indication of environmental status (Ferris
BI, Basal Index; CI, Channel Index; EI, Enrichment Index; MI, Maturity Index; SI, Structure Index.
Crop rotation is one form of cultural management and a common method used to control plant pathogens. One year of peanut (
Another common method of managing plant-parasitic nematodes is chemical management with the use of non-fumigant nematicides (Moore and Lawrence, 2012; Khanal
Trials were conducted in 2017 and 2018 at a longterm research site (established in 2000) at the North Florida Research and Education Center (NFREC) in Quincy, FL (30°32.79’N, 84°35.50’W). Strip tillage was used along with an oat cover crop planted in December and terminated in March of each year. Based on prior site recommendations, a 5–15–30 (N–P–K) fertilizer was applied prior to planting each year at a rate of 280.2 kg/ha.
Detailed experimental design was described by Schumacher
Soil sampling was conducted in 2017 and 2018 using an Oakfield tube (Oakfield Apparatus, Oakfield, WI) sampled to a depth of approximately 30 cm in a zigzag pattern between the center two rows of each plot (Schumacher
Response variables were nematode population densities and ecological indices and these were analyzed separately by sampling date (preplant, midseason, and harvest) in 2017 and 2018 using a three-way split–split plot ANOVA procedure in R version 3.3.1 (The R Foundation for Statistical Computing, Vienna, Austria). Assumptions of normality were checked graphically and using Levene’s test and transformed if necessary to achieve normality (Levene, 1960; Cook and Weisburg, 1999). Significant (
Overall, there were relatively few impacts of irrigation, crop phase, or nematicide on any of the response variables (Tables 2–7). Additionally, there were no significant main effects of irrigation, crop phase, or nematicide on predator population densities observed in any sampling date (data not shown). Significant results for individual response variables are continued below.
Effects of irrigation, crop phase, and nematicide application on fungivore population density in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 189a | 150 | 131 | 236 | 172 | 256 |
Rainfed | 103b | 140 | 142 | 254 | 176 | 240 |
Crop phasey | ||||||
CS | 224A | 178 | 79B | 286 | 153 | 220 |
C1 | 104B | 129 | 81B | 221 | 182 | 244 |
C2 | 110B | 129 | 249A | 228 | 186 | 281 |
Nematicide | ||||||
Without fluopyram | 147 | 141 | 132 | 259 | 140 | 270 |
With fluopyram | 144 | 149 | 141 | 231 | 208 | 226 |
ANOVA ( |
||||||
Irrigation (I) | 0.04* | 0.85 | 0.20 | 0.42 | 0.91 | 0.51 |
Crop (C) | 0.02* | 0.33 | <0.01** | 0.50 | 0.75 | 0.84 |
I × C | 0.48 | 0.26 | 0.45 | 0.32 | 0.63 | 0.96 |
Nematicide (N) | 0.94 | 0.66 | 0.75 | 0.38 | 0.08 | 0.11 |
I × N | 0.77 | 0.14 | 0.71 | 0.43 | 0.40 | 0.13 |
C × N | 0.93 | <0.01** | 0.86 | 0.79 | 0.64 | 0.37 |
I × C × N | 0.95 | 0.06 | 0.44 | 0.68 | 0.86 | 0.85 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean nematode population densities (per 100 cm3 soil) prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
LSD, least significant difference.
Effects of irrigation, crop phase, and nematicide application on bacterivore population density in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 730 | 387 | 151 | 726 | 525 | 314 |
Rainfed | 602 | 430 | 196 | 898 | 608 | 516 |
Crop phasey | ||||||
CS | 798 | 431 | 84B | 824 | 518 | 355 |
C1 | 692 | 333 | 70B | 808 | 505 | 432 |
C2 | 507 | 461 | 367A | 804 | 675 | 458 |
Nematicide | ||||||
Without fluopyram | 718 | 433 | 176 | 828 | 538 | 414 |
With fluopyram | 614 | 383 | 172 | 797 | 595 | 416 |
ANOVA ( |
||||||
Irrigation (I) | 0.35 | 0.41 | 0.23 | 0.37 | 0.23 | 0.13 |
Crop (C) | 0.39 | 0.34 | <0.01** | 0.99 | 0.55 | 0.72 |
I × C | 0.78 | 0.15 | 0.23 | 0.36 | 0.27 | 0.31 |
Nematicide (N) | 0.14 | 0.27 | 0.93 | 0.80 | 0.55 | 0.98 |
I × N | 0.21 | 0.67 | 0.79 | 0.29 | 0.86 | 0.13 |
C × N | 0.31 | 0.02* | 0.62 | 0.94 | 0.36 | 0.03 |
I × C × N | 0.07 | 0.90 | 0.38 | 0.71 | 0.24 | 0.51 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean nematode population densities (per 100 cm3 soil) prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
LSD, least significant difference.
Effects of irrigation, crop phase, and nematicide application on omnivore population density in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 19 | 76a | 18 | 55 | 58 | 58 |
Rainfed | 14 | 60b | 12 | 64 | 50 | 45 |
Crop phasey | ||||||
CS | 22 | 58 | 23 | 44 | 63 | 25 |
C1 | 22 | 84 | 9 | 73 | 38 | 59 |
C2 | 5 | 62 | 13 | 62 | 61 | 69 |
Nematicide | ||||||
Without fluopyram | 17 | 87 | 17 | 80a | 71a | 84a |
With fluopyram | 15 | 48 | 13 | 39b | 37b | 19b |
ANOVA ( |
||||||
Irrigation (I) | 0.59 | 0.04* | 0.30 | 0.86 | 0.45 | 0.11 |
Crop (C) | 0.18 | 0.67 | 0.17 | 0.63 | 0.59 | 0.53 |
I × C | 0.40 | 0.97 | 0.63 | 0.35 | 0.73 | 0.91 |
Nematicide (N) | 0.72 | 0.07 | 0.40 | 0.04* | <0.01** | <0.01** |
I × N | 0.12 | 0.74 | 0.06 | 0.66 | 0.25 | 0.74 |
C × N | 0.66 | 0.38 | 0.27 | 0.18 | 0.43 | <0.01** |
I × C × N | 0.02 | 0.48 | 0.70 | 0.61 | 0.97 | 0.43 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean values of nematode ecological indices prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
MI, Maturity Index; LSD, least significant difference.
Effects of irrigation, crop phase, and nematicide application on BI in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 30 | 28b | 38 | 35 | 37 | 36 |
Rainfed | 26 | 33a | 43 | 42 | 42 | 43 |
Crop phasey | ||||||
CS | 22B | 25 | 32 | 37 | 35 | 41 |
C1 | 21B | 28 | 40 | 35 | 38 | 40 |
C2 | 41A | 38 | 50 | 44 | 46 | 37 |
Nematicide | ||||||
Without fluopyram | 25 | 30 | 38 | 36 | 39 | 37 |
With fluopyram | 31 | 30 | 44 | 41 | 40 | 42 |
ANOVA ( |
||||||
Irrigation (I) | 0.32 | 0.05* | 0.62 | 0.28 | 0.31 | 0.44 |
Crop (C) | 0.03* | 0.11 | 0.16 | 0.40 | 0.30 | 0.85 |
I × C | 0.66 | 0.85 | 0.66 | 0.22 | 0.90 | 0.98 |
Nematicide (N) | 0.15 | 0.98 | 0.29 | 0.25 | 0.84 | 0.34 |
I × N | 0.69 | 0.87 | 0.15 | 0.66 | 0.70 | 0.30 |
C × N | 0.24 | 0.29 | 0.06 | 0.92 | 0.01** | 0.24 |
I × C × N | 0.35 | 0.55 | 0.46 | 0.37 | 0.65 | 0.84 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean values of nematode ecological indices prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
LSD, least significant difference; BI, Basal Index.
Effects of irrigation, crop phase, and nematicide application on EI in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 66 | 56 | 46 | 53 | 46 | 48 |
Rainfed | 71 | 53 | 43 | 40 | 38 | 47 |
Crop phasey | ||||||
CS | 76A | 65A | 45 | 52 | 47 | 48 |
C1 | 75A | 58AB | 43 | 47 | 44 | 44 |
C2 | 54B | 40B | 45 | 40 | 34 | 51 |
Nematicide | ||||||
Without fluopyram | 70 | 54 | 46 | 49 | 38 | 47 |
With fluopyram | 67 | 54 | 43 | 44 | 45 | 48 |
ANOVA ( |
||||||
Irrigation (I) | 0.30 | 0.71 | 0.75 | 0.16 | 0.25 | 0.98 |
Crop (C) | 0.02* | 0.01** | 0.99 | 0.34 | 0.13 | 0.55 |
I × C | 0.74 | 0.99 | 0.64 | 0.12 | 0.24 | 0.72 |
Nematicide (N) | 0.40 | 0.98 | 0.61 | 0.32 | 0.07 | 0.72 |
I × N | 0.77 | 0.88 | 0.88 | 0.51 | 0.92 | 0.51 |
C × N | 0.43 | 0.91 | 0.38 | 0.63 | 0.02* | 0.58 |
I × C × N | 0.23 | 0.91 | 0.68 | 0.17 | 0.92 | 0.19 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean values of nematode ecological indices prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
EI, Enrichment Index; LSD, least significant difference.
Effects of irrigation, crop phase, and nematicide application on MI in 2017 and 2018.
2017 |
2018 |
|||||
---|---|---|---|---|---|---|
Pix | Pm | Pf | Pi | Pm | Pf | |
Irrigation | ||||||
Irrigated | 1.84 | 2.23 | 2.33 | 2.09 | 2.19 | 2.25 |
Rainfed | 1.71 | 2.17 | 2.24 | 2.13 | 2.21 | 2.08 |
Crop phasey | ||||||
CS | 1.71 | 2.09 | 2.46 | 2.02 | 2.21 | 2.09 |
C1 | 1.73 | 2.27 | 2.45 | 2.17 | 2.19 | 2.24 |
C2 | 1.88 | 2.23 | 1.97 | 2.13 | 2.20 | 2.16 |
Nematicide | ||||||
Without fluopyram | 1.77 | 2.25 | 2.31 | 2.12 | 2.26a | 2.27a |
With fluopyram | 1.78 | 2.15 | 2.25 | 2.09 | 2.14b | 2.06b |
ANOVA ( |
||||||
Irrigation (I) | 0.17 | 0.07 | 0.06 | 0.75 | 0.44 | 0.16 |
Crop (C) I × C | 0.23 0.84 | 0.07 0.91 | 0.16 0.90 | 0.25 0.73 | 0.95 0.59 | 0.58 0.81 |
Nematicide (N) | 0.84 | 0.31 | 0.93 | 0.41 | 0.02* | <0.01** |
I × N | 0.67 | 0.83 | 0.08 | 0.27 | 0.77 | 0.35 |
C × N | 0.45 | 0.28 | 0.61 | 0.08 | 0.30 | 0.01** |
I × C × N | 0.14 | 0.80 | 0.64 | 0.17 | 0.61 | 0.22 |
Different letters in columns denote means separation for significant (
xPi, Pm, and Pf are mean nematode population densities (per 100 cm3 soil) prior to planting, at midseason (52 d and 56 d after planting in 2017 and 2018), and at harvest (150 d and 151 d after planting in 2017 and 2018), respectively.
yC1 and C2 are first- and second-year conventional cotton, respectively, with previous 1 yr peanut; CS is sod-based cotton with previous 1 yr peanut with previous 2 yr bahiagrass.
* and ** represent significant effects at
LSD, least significant difference.
In preplant 2017 soil samples, fungivore population density was significantly greater in irrigated plots than rainfed plots, but irrigation did not significantly affect fungivores in any other season (Table 2). Fungivore population density was greater in preplant CS plots than conventional cotton plots in preplant 2017 soil samples (Table 2). Both fungivore and bacterivore populations were greater in C2 in harvest 2017 soil samples (Tables 2 and 3, respectively). There were significant rotations by nematicide interactions for both fungivores and bacterivores in midseason 2017 (Tables 2 and 3) as fungivores and bacterivores were both greater in nematicide-treated plots of CS in midseason 2017 soil samples (Fig. 1). However, bacterivores and fungivores were both greater in untreated plots of C2 than plots with nematicide in midseason 2017. There was also a significant interaction in harvest 2018 for bacterivores (Table 3), and bacterivore abundances were greater in untreated plots of C1 and greater in nematicide-treated plots of C2 (Fig. 2).
Fungivore (left) and bacterivore (right) population density (nematodes/100 cm3 soil) in midseason 2017 soil samples. CS is the cotton phase of the sod-based rotation, C1 is first-year conventional cotton, and C2 is second-year conventional cotton. Without Nematicide and With Nematicide refer to absence or presence of fluopyram, respectively. Different letters denote significant differences between nematicide treatments within crop phase (Fisher’s LSD,
Bacterivore population density (nematodes/100 cm3 soil) in harvest 2018 (right) soil samples. CS is the cotton phase of the sod-based rotation, C1 is first-year conventional cotton, and C2 is second-year conventional cotton. Without Nematicide and With Nematicide refer to absence or presence of fluopyram, respectively. Different letters denote significant differences between nematicide treatments within crop phase (Fisher’s LSD,
Omnivore population density was greatest in irrigated plots and significantly lower in rainfed plots in midseason 2017 soil samples (Table 4). Untreated plots had significantly more omnivores than nematicide-treated plots in preplant 2018, midseason 2018, and harvest 2018 soil samples (Table 4). There was a nematicide by crop rotation interaction in harvest 2018, but nematicide significantly decreased omnivore population density in each crop phase in harvest 2018 soil samples (Fig. 3).
Omnivore population density (nematodes/100 cm3 soil) in harvest 2018 soil samples. CS is the cotton phase of the sod-based rotation, C1 is first-year conventional cotton, and C2 is second-year conventional cotton. Without Nematicide and With Nematicide refer to absence or presence of fluopyram, respectively. * indicates significant nematicide effect within the given crop (Fisher’s LSD,
In 2017 preplant soil samples, C2 plots had a significantly greater BI value than CS or C1 plots (Table 5). In midseason 2017 soil samples, rainfed plots had a significantly greater BI value than irrigated plots (Table 5). In midseason 2018 soil samples, nematicide effects on BI were significant in CS and C1, but not C2 (Table 5 and Fig. 4). In CS, BI was greatest in nematicide-treated plots and significantly lower in untreated plots. In C1, however, the opposite trend was observed where BI was greatest in untreated plots and significantly lower in nematicide-treated plots.
Basal Index (left) and EI (right) based on midseason 2018 soil samples. CS is the cotton phase of the sod-based rotation, C1 is first-year conventional cotton, and C2 is second-year conventional cotton. Without Nematicide and With Nematicide refer to absence or presence of fluopyram, respectively. Different letters denote significant differences between nematicide treatments within crop phase (Fisher’s LSD,
Preplant CS and C1 plots had significantly greater EI values than preplant C2 plots in preplant 2017 soil samples (Table 6). EI was significantly affected by crop phase in midseason 2017 soil samples, where EI was greatest in CS and least in C2 (Table 6). There was a significant crop phase by nematicide interaction for EI in midseason 2018 soil samples (Fig. 4). Nematicide effects were significant in C1, but not in CS or C2. In C1, EI was greatest in nematicide-treated plots and significantly lower in untreated plots.
Nematicide-treated plots had a lower MI value than untreated plots in both midseason 2018 and harvest 2018 soil samples (Table 7). Nematicide effects on MI were significant in CS and C2, but not C1 in harvest 2018 soil samples. In CS and C2, MI was greatest in untreated plots and significantly lower in nematicide-treated plots. Nematicide-treated plots had a significantly lower CI value than untreated plots (39 and 57, respectively) in harvest 2018 soil samples (
Maturity Index (left) and SI (right) based on harvest 2018 soil samples. CS is the cotton phase of the sod-based rotation, C1 is first-year conventional cotton, and C2 is second-year conventional cotton. Without Nematicide and With Nematicide refer to absence or presence of fluopyram, respectively. Different letters denote significant differences between nematicide treatments within crop phase (Fisher’s LSD,
Nematodes are important indicator taxa and assessment of nematode communities may enhance understanding of global distribution patterns and help in predicting impacts of various agricultural management practices and ecosystem health (Bongers and Ferris, 1999; Cesarz
Previous research on irrigation showed that plant-parasitic nematode population densities were greater during periods of reduced precipitation/irrigation (Bird
Tracking differences in nematode community structure in sod-based and conventional cotton provided insight on how free-living nematodes responded to different crop rotation phases. In our study, we did not observe consistent effects on any response variable as none were affected in both years of our study and only a few had effects in multiple seasons within a single year. Although fungivores were affected by crop phase in more sampling dates than bacterivores, neither group was consistently affected by crop phase. Similarly, neither omnivores nor predators were affected by crop phase. Rotation was expected to affect trophic groups, particularly microbe feeders like bacterivores as they thrive on simple resources with low C:N ratios whereas fungivores thrive on recalcitrant resources that are more difficult to break down (Neher, 2010). Hou
It is evident that the type of crop is a driver for the associated free-living nematode community. For instance, long-term corn promoted a mature, fungal-based ecosystem while long-term soybean promoted a more disturbed, enriched, bacterial-based system (Grabau and Chen, 2016). Grabau
High MI or EI values indicate a stable and/ or enriched environment, high SI values indicate high food web complexity, high CI values indicate fungal-dominated decomposition pathways, and high BI values indicate stressed and/or degraded environments (Ferris
Fluopyram nematicide had minimal impacts on free-living nematode population densities, aside from omnivores. None of the nematicide effects were consistent across seasons, especially regarding nematicide effects under individual crop phases. Hodson
If environmental disturbance can be defined in the context of applying agricultural chemicals, such as nematicides, then nematodes that serve as environmental indicators are useful to study ecological effects. In general, nematode populations decrease after agricultural chemical management (Desaeger
Generally, nematode communities with greater population densities of omnivores and predators (i.e., higher c-p nematodes) have higher MI values (Hodson
Nematicide application negatively impacted certain free-living nematodes in the conventional rotation. The underlying reason for sensitivity to nematicides is due to the permeable nematode cuticle, which can come into direct contact with pollutants (Yeates, 1999; Neher, 2010; Hodson
Other integrated management systems have seen varied effects on the nematode community. The link between nematode community diversity and ecological processes is still unclear, with several attempts to elucidate these concepts made in past research (Schafer, 1973; Rosenberg, 1976; Ettema, 1998; Neher and Darby, 2006). Our results were inconsistent with other research assessing management effects on the nematode community based on MI values. Porazinska
This study highlighted the importance of understanding how plant-parasitic nematode management practices (i.e., irrigation, crop rotation phase, and nematicide application) affect non-target, free-living nematodes. Assessing the effects of sustainable farming practices, like sod-based rotation, can therefore be accomplished by examining these nematode communities. Overall, none of the factors consistently affected the nematode community. Because our rotations utilized the same crop (i.e., cotton), perhaps less overall differences in nematode community structure were observed than in other crop rotation studies. In our study, omnivores were more sensitive to environmental disturbance in terms of nematicide application. However, nematode ecology was not consistently influenced by nematicide application in sod-based and conventional crop rotation systems. Fluopyram nematicide had a negative impact on omnivores, but minimal impact on the rest of the nematode community, regardless of crop rotation phase. Free-living nematodes were not negatively impacted by nematicide when sod-based rotation was used. This supports the idea that nematicide application can be reduced in sod-based rotation while not adversely affecting lower c-p nematodes.