Population Dynamics of Empoasca fabae (Hemiptera: Cicadellidae) in Central Iowa Alfalfa Fields.

Adults and nymphs of Empoasca fabae Harris (Hemiptera: Cicadellidae) and adults of predatory species in the families Coccinellidae, Anthocoridae, Nabidae, Chrysopidae, and Hemerobiidae were sampled in Iowa alfalfa fields from June to September in 1999 and 2000. The relationship between each predatory taxa and E. fabae was examined using regression analysis. In 2000, all predators were found to be positively correlated with the presence of E. fabae during all periods sampled and most likely contributed to mortality. Orius insidiosus (Say) (Hemiptera: Anthoridae) was the most numerous insect predatory species; population numbers ranged from 0 to 1 and 0.1 to 3.7 adults per 0.25 m(2) in 1999 and 2000, respectively. Partial life tables were constructed for E. fabae nymphs for two alfalfa-growing periods. Nymphs were grouped into three age intervals: first and second, third and fourth, and fifth instars. For the first alfalfa growing period examined, E. fabae nymphal mortality was 70% in 1999 and 49% in 2000. During the last growing period of each season (August-September), total nymphal mortality was relatively low (<25%). Adult E. fabae density ranged from 5.4 to 25.6 and 1.4-9.2 per 0.25 m(2) in 1999 and 2000, respectively. E. fabae population peaks were similar for each age interval in all growing periods. This study provides further information on the population dynamics of E. fabae and its relationship with select predatory species in Iowa alfalfa fields.

The potato leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae) is a key pest of alfalfa (Medicago sativa L.) in the midwestern United States (Giles et al. 1999, Chasen et al. 2014). E. fabae overwinters in states along the Gulf of Mexico on evergreens (Pinaceae) and herbaceous vegetation (mostly Fabaceae) and then migrates north in spring (Medler 1957, Taylor et al. 1993, Taylor and Shields 1995, Sidumo et al. 2005). The first appearance of E. fabae in the midwestern United States occurs in late-April to mid-May (Medler 1957, Maredia et al. 1998). Arrival of E. fabae in these areas coincides with low-pressure weather systems, suggesting transport is passive on warm low-level jet streams (Carlson et al. 1992). While E. fabae are found in alfalfa at this time, populations do not reach damaging levels in Iowa alfalfa fields until after the first cutting (mid-May to early June) (Steffey and Armbrust 1991, DeGooyer et al. 1998a, Giles et al. 1999).

Most alfalfa is typically harvested approximately every 45 d, which results in three harvests a season. However, for high-performance livestock, alfalfa may be harvested every 35 d resulting in four harvests a season (Barnhart 2010). Feeding on alfalfa by E. fabae reduces quality and yield by reducing the amount of photosynthate produced in the plant (Medler 1941). Eggs are laid singly in stems or petioles of host plants, and nymphs develop through five instars (Fenton and Hartzell 1923, Simonet and Pienkowski 1977). In Iowa, there are three overlapping generations of E. fabae per year (DeGooyer et al. 1998b).

Natural enemies of E. fabae have been identified, but little is known about their impact on E. fabae populations in alfalfa (Fenton and Hartzell 1923, Yadava and Shaw 1968, Lavallee and Shaw 1969, Wheeler 1977, Martinez and Pienkowski 1982, Rensner et al. 1983, Flinn et al. 1985). In laboratory studies, several coccinellid species prey upon E. fabae including Coleomegilla maculata (DeGeer), Coccinella novemnotata Herbst., and Hippodamia convergens (Guérin-Menéville) (Martinez and Pienkowski 1982, Weiser Erlandson and Obrycki 2010, Chasen et al. 2014). Weiser Erlandson and Obrycki (2010) observed attack rates of 0.6 and 4.6 E. fabae per day by C. maculata adults and Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) larvae, respectively. Similarly, adult Nabis roseipennis (Reuter) (Hemiptera: Nabidae) consumed 4–5 E. fabae adults and 8–10 nymphs per day in the laboratory (Rensner et al. 1983). Other predatory species, such as Nabis americoferus Carayon and Orius insidiosus (Say) (Hemiptera: Anthoridae), locate and attack E. fabae eggs found in plant tissue (Martinez and Pienkowski 1982). Rensner et al. (1983) observed that nabid populations peak with E. fabae populations in Illinois alfalfa fields. In Virginia, O. insidiosus and N. americoferus were the most abundant predatory species, comprising 35% and 32% of predators collected in alfalfa (Martinez and Pienkowski 1982).

The objective of this study was to examine population dynamics of E. fabae and its relationship to associated predatory species in Iowa alfalfa fields.

Materials and Methods

Sampling Methods

E. fabae populations were sampled in two alfalfa fields in Ames, IA, in 1999 and 2000. Each field was sectioned into 10 25-m2 quadrats. Samples were taken using a drop trap and a leaf blower with a suction attachment (WeedEater, Model BV1650, Shreveport, LA) and a mesh collection net (DeGooyer et al. 1998a). The drop trap consisted of a Plexiglas box (0.5 by 0.5 by 0.5 m = 0.125 m3) with an open bottom. The drop trap was randomly dropped over alfalfa foliage in each quadrat. Care was taken to ensure that there was no disruption of the foliage prior to dropping the trap. One suction sample was taken from each quadrat twice weekly from first harvest (late May to early June) until last harvest (August to September). Suction samples were collected by inserting the leaf blower through a 20-cm diameter hole on the top of the drop trap and vacuuming insects from within. Insects left on the top of the drop trap were counted directly. Samples were placed in plastic bags and transported to the laboratory. The number of E. fabae nymphs, adults, and adult insect predators was recorded from each sample. Immature predators were excluded from the analysis due to labor constraints. The insects counted from the top of the drop box were added to the sample. Based on size and wing pad development, E. fabae nymphal stages were divided into three age groups: first–second, third–fourth, and fifth instars (Fenton and Hartzell 1923).

Data analysis

For comparison, partial life tables were calculated for only the last two growing periods of alfalfa during 1999 (second and third growing periods) and 2000 (third and fourth growing periods) to determine within-generation E. fabae population change. Data were not collected for the first growing period because E. fabae are migrating into Iowa and populations are not yet fully established. E. fabae age intervals used were first–second, third–fourth, and fifth instars; adult E. fabae were not used in life table analysis because of fluctuating numbers due to immigration and emigration. E. fabae eggs were not included in analysis because of problems encountered in chemical clearing alfalfa stems for visual identification of eggs. Calculation of life table statistics followed Southwood (1978): x = age interval of E. fabae, l = number of E. fabae at the beginning of each age interval, d = number dying during the age class x interval, 100q = percent mortality for age interval, S = survival rate within age interval x. Estimates of l were determined by calculating the area under a curve method (Southwood 1978) using ENSTAT 4.0 (Pedigo and Zeiss 1996).

Regression analysis was performed for the relationship between each of the individual predator groups and combined predators, and each developmental stage of E. fabae and combined all stages of E. fabae using Excel data analysis tool (Excel 2010). Because of higher variation in field studies, statistical significance was set at P ≤ 0.055. Voucher specimens of all predators and E. fabae were deposited in the Department of Entomology Insect Collection, Iowa State University, Ames, IA.

Results

In 1999, E. fabae densities (±SE) ranged from 5.4 ± 2.9 to 25.6 ± 2.6 adults and 0.1 ± 0.1 to 3.3 ± 0.6 nymphs, collected per 0.25 m2 (Fig. 1a). Percent mortality during the second growing period was 44% for first–second and 47% for third–fourth instars (Table 1). Total mortality from first to fifth instar was 70% (Table 1). During the third growing period, mortality was low for first to fifth instar resulting in a negative mortality (the number of fifth instars collected was greater than the number of first instars) (Table 1).

Fig. 1.

Mean number ± SEM first–second instar, third–fourth instar and fifth instar, and adult E. fabae collected per 0.25 m2 in Iowa alfalfa fields. (a) 1999. (b) 2000

Table 1.

Partial life tables for E. fabae nymphs in alfalfa at Ames, IA, in 1999 and 2000

Year	Growing perioda	Xb	lxc	dxd	100qxe	Sxf
1999	2	1–2 instars	38.02	16.77	44.11	55.89
1999	2	3–4 instars	21.25	9.99	47.01	52.99
1999	2	5 instars	11.26
1999	2	Total		26.76	70.38	29.62
1999	3	1–2 instars	34.79	4.14	11.9	88.1
1999	3	3–4 instars	30.65	−4.21	−13.74	113.74
1999	3	5 instar	34.86
1999	3	Total		−0.07	−0.2	100.2
2000	3	1–2 instars	36.21	7.59	20.96	79.04
2000	3	3–4 instars	28.62	10.07	35.19	64.81
2000	3	5 instars	18.55
2000	3	Total		17.66	48.77	51.23
2000	4	1–2 instars	14.28	4.5	31.51	68.49
2000	4	3–4 instars	9.78	−1.29	−13.19	113.19
2000	4	5 instars	11.07
2000	4	Total		3.21	22.48	77.52

aIn 1999, first growing period May–6 June, second growing period 7 June–28 June, third growing period 29 June–10 August; and in 2000, first growing period May–27 May, second growing period 28 May–18 June, third growing period 19 June–27 July, and fourth growing period 28 July–10 September

bx, age interval of E. fabae.

cl, number of E. fabae at the beginning of each age interval.

dd, number dying during the age class x interval.

e100q, percent mortality for age interval.

fS, survival rate within age interval

Compared with E. fabae, the number of predatory insects collected was relatively low (0–1 per 0.25 m2) (Table 3). The only anthocorid species collected in this study was O. insidiosus; it also was the most numerous predatory species collected (0.1 ± 0.1–1.0 ± 0.3 per 0.25 m2) (Fig. 2a). Nabid populations, including N. roseipennis and N. americoferus, ranged from 0 to 0.4 ± 0.2 adults per 0.25 m2 (Fig. 2a). Coccinellid species collected were C. maculata, H. convergens, Hippodamia tredecimpunctata (Say), Harmonia axyridis (Pallas), Cycloneda munda (Say), Hippodamia parenthesis (Say), and Coccinella septempunctata L. Coccinellid densities ranged from 0 to 0.1 ± 0.1 per 0.25 m2 (Fig. 2a). Neuropterans collected consisted of both Chrysopidae and Hemerobiidae. However, chrysopids, including Ch. carnea and Chrysopa occulata Say, were more abundant than Hemerobiidae. Densities of neuropterans ranged from 0 to 0.1 ± 0.1 per 0.25 m2 (Fig. 2a). The only positive correlation of a predator group with E. fabae found during this year was that of the relationship between nabids and 3–4 instar E. fabae (Table 2; F = 7.40; df = 1, 4; P = 0.053).

Table 3.

Predator minimum and maximum densities (±SE) per 0.25m2 found in Iowa alfalfa fields in 1999 and 2000

	1999		2000
Predator	Min	Max	Min	Max
Coccinellidae	0.00 (0.0)	0.10 (0.1)	0.00 (0.0)	0.40 (0.2)
Neuroptera	0.00 (0.0)	0.10 (0.1)	0.00 (0.0)	0.40 (0.2)
Anthocoridae	0.01 (0.1)	1.00 (0.3)	0.10 (0.1)	3.70 (0.6)
Nabidae	0.00 (0.0)	0.40 (0.2)	0.00 (0.0)	0.50 (0.2)

Fig. 2.

Mean number ± SEM Coccinellidae, Neuroptera, Anthocoridae, and Nabidae collected per 0.25 m2 in Iowa alfalfa fields. (a) 1999. (b) 2000

Table 2.

Significant R2 values obtained for relationships between predators and various stages of E. fabae in Iowa alfalfa fields in 1999 and 2000

Year	Growing perioda	Predator (adult)	Stage of E. fabae	R2	F (df)	F	P	Line equation
1999	2	Nabidae	3–4 instars	0.649	1, 4	7.40	0.053	Y = 0.0520x + 0.0627
2000	2	Nabidae	1–2 instars	0.707	1, 4	9.67	0.036	Y = 0.8895x + 0.0897
2000	2	Nabidae	Adult	0.918	1, 4	44.53	0.003	Y = 0.0941x − 0.1885
2000	2	Nabidae	All stages	0.958	1, 4	90.50	0.000	Y = 0.3270x − 0.1650
2000	3	Orius	1–2 instars	0.594	1, 5	7.32	0.043	Y = 0.2467x + 0.5339
2000	3	Orius	3–4 instars	0.583	1, 5	6.98	0.046	Y = 0.3141x + 0.5300
2000	3	Orius	5 instars	0.553	1, 5	6.18	0.055	Y = 0.5452x + 0.4846
2000	3	Orius	Adult	0.618	1, 5	8.10	0.036	Y = 0.1432x − 0.0307
2000	3	Orius	All stages	0.654	1, 5	9.47	0.028	Y = 0.2729x + 0.2223
2000	3	All predators	1–2 instars	0.606	1, 5	7.69	0.039	Y = 0.0725x + 0.1730
2000	3	All predators	3–4 instars	0.597	1, 5	7.40	0.042	Y = 0.0926x + 0.1717
2000	3	All Predators	5 instars	0.612	1, 5	7.89	0.038	Y = 0.1671x + 0.1533
2000	3	All predators	Adult	0.764	1, 5	16.16	0.010	Y = 0.0464x − 0.0208
2000	3	All predators	All stages	0.736	1, 5	13.93	0.014	Y = 0.0842x + 0.0713
2000	4	Neuroptera	1–2 instars	0.657	1, 7	13.40	0.008	Y = 0.2559x + 0.0142
2000	4	Neuroptera	3–4 instars	0.950	1, 7	133.29	0.000	Y = 0.4129x − 0.0131
2000	4	Neuroptera	All stages	0.688	1, 7	15.46	0.005	Y = 0.2648x − 0.1252
2000	4	Nabidae	1–2 instars	0.447	1, 7	5.67	0.049	Y = 0.2027x + 0.0477
2000	4	Nabidae	All stages	0.453	1, 7	5.80	0.047	Y = 0.2063x − 0.0595

aIn 1999, first growing period May–6 June, second growing period 7 June–28 June, third growing period 29 June–10 August; and in 2000, first growing period May–27 May, second growing period 28 May–18 June, third growing period 19 June–27 July, and fourth growing period 28 July–10 September.

In 2000, E. fabae densities collected per 0.25 m2 ranged from 1.4 ± 0.4 to 9.2 ± 1.0 adults and 0 to 3.4 ± 1.0 nymphs (Fig. 1b). Percent mortality during the third growing period was 21% and 35% for first–second and third–fourth instars, respectively (Table 1). For this same growing period, total mortality for first to fifth instar was 49% (Table 1). During the fourth growing period, percent mortality was 23% for first to fifth instar (Table 1).

Although the same predatory species were collected in both years, predator numbers were higher in 2000 (Table 3). Densities of anthocorids (O. insidiosus) ranged from 0.1 ± 0.1 to 3.7 ± 0.6 adults per 0.25 m2, with higher numbers occurring during the last growing period (Fig. 2b). O. insidiosus was the most numerous insect predator collected (Table 3). The second most abundant predatory group was Nabidae with densities ranging from 0 to 0.5 ± 0.2 adults per 0.25 m2 (Fig. 2b). Coccinellids and neuropterans had similar densities of 0 to 0.4 ± 0.2 adults per 0.25 m2 (Fig. 2b).

In addition, all predators were found to be positively correlated with the presence of E. fabae in 2000 during all periods sampled (Table 2). The relationship of O. insidiosus was strongest during the July sampling period, while neuropterans and nabids exhibited a strong relationship during the last sampling period (August to September) (Table 2).

Discussion

In 1999, E. fabae densities were 2–3 times higher than in 2000 (Fig. 1a). This is consistent with other studies that examined E. fabae populations in Iowa alfalfa fields from 1998 to 2000 (Weiser et al. 2003); E. fabae densities in Iowa alfalfa fields during 1999 were 3–10 times higher than those in 1998 and 2000. Adult E. fabae were consistently found in suction samples from the start of sampling and nymphs were first collected during the third week of sampling (11 June 1999). Flinn et al. (1990) observed that adult E. fabae usually do not colonize alfalfa regrowth until alfalfa reached a height of 5 cm, 10–15 d after alfalfa harvest. In contrast, we observed adult immigration somewhat earlier, at approximately 7 d after harvest. Early colonization of alfalfa regrowth may result in a higher number of E. fabae in the next generation. Adult E. fabae oviposit 2–3 eggs per day during their lifetime (DeLong 1938) which is, on average, 76–122 d for females depending on temperature (Sher and Shields 1991); and since E. fabae are continuously reproducing, there is the potential for rapid population growth (Hogg 1985).

E. fabae population peaks were synchronous for each age interval in all growing periods (Fig. 1). However, we did not observe successive density peaks for each age interval. This pattern was consistent for each growing period and year. Sampling intervals were relatively short (every 3–4 d) providing adequate resolution of changes in population dynamics.

Percent mortality of E. fabae was consistently higher in the first life tables constructed (second and third alfalfa growing periods in 1999 and 2000, respectively) than in the second life tables in the same years. For the second life table of each year, E. fabae percent mortality was relatively low (<25%) because higher numbers of older instar E. fabae were collected. This trend was not found in any of the other growing periods sampled and, therefore, is unlikely to be due to sampling error. There are two possible explanations for this observation. First, in 2000, we found a correlation in the number of predators with E. fabae (Table 2), especially with the nabids and neuropterans during the last growing period. These predators may have contributed to the mortality of E. fabae during this time. In addition, the number of O. insidiosus was correlated with all stages of E. fabae during the third growing period (Table 2) and its numbers in the alfalfa were highest during the last growing period (Fig. 2). Each of these predatory species feeds on E. fabae and may have contributed to the mortality of younger instars, causing the difference between age intervals (Weiser Erlandson and Obrycki 2010). In addition, Weiser Erlandson and Obrycki (2010) observed in laboratory studies that O. insidiosus feeds on proportionally more of the younger than the older instars of E. fabae nymphs and may prefer to prey upon smaller insects in the field. However, many of these predatory species are polyphagous and feed on other insects found in alfalfa. For example, coccinellids which are thought to be primarily aphidophagous will diversify their diet with other prey items, such as dipterans (Moser et al. 2011), as well as E. fabae (Weiser Erlandson and Obrycki 2010), when aphid availability is low. Smaller E. fabae populations were observed in 2000 than in 1999 (Figs. 1a and b) while higher populations of predators were observed in 2000 than in 1999 (Fig. 2a and b). Although these predatory species may not be significant mortality factors in this study, we did not collect their immature stages and, collectively with the adults, they may be important in maintaining low E. fabae population densities in the field.

Another factor that may have affected our data is that E. fabae begin their reproductive diapause before their southward migration in late summer to fall (Taylor et al. 1995). Taylor et al. (1995) determined that in New York, mid-July, only 50% of late instar E. fabae females would become reproductively mature. This coincides with decreasing photoperiod (e.g., 15:9 [L:D] h). By mid-August and September, the number of late instar females predicted to become reproductively mature drastically dropped to about 25% and 9%, respectively. In Iowa, daylight hours decrease to about 14 h around mid-August and to about 13 h by early September. The decrease of the number of early instars shown in our data supports the induction of reproductive diapause beginning in late July.

Population dynamics may fluctuate from year to year based on environmental conditions and how many alfalfa growing periods occur in a particular season. Although we found the same population trend in each year, population numbers of adult E. fabae were higher in 1999 compared with those found in 2000. Hogg (1985) observed that temperature affected E. fabae developmental time, natality, and mortality in laboratory studies; reproductive rates were higher and generation times were shorter at higher temperature regimes. We did not find a substantial difference in average temperatures between 1999 and 2000, but rainfall was much higher in 1999 during the months of May, July and, August (www.wunderground.com). The higher rainfall in 1999 may have contributed to faster alfalfa growth and larger plants that may have attracted more adult E. fabae to the alfalfa fields. Adult E. fabae adults colonized alfalfa regrowth about 1 wk after harvest (DeGooyer et al. 1998b, this study), which may contribute to higher numbers of E. fabae and possibly more generations. However, this may not be as significant during the second growth of alfalfa due to high nymphal mortality (70% in 1999 and 49% in 2000).

This study offers further insight to the population dynamics of E. fabae and predatory species in alfalfa. Several predatory species occur simultaneously with E. fabae in alfalfa including O. insidiosus, nabids, neuropterans, and coccinellids. We found their numbers to be positively correlated with those of E. fabae once in 1999 and many times in 2000 (Table 2). These data show that these predators may have an effect on the percent mortality of E. fabae (especially the younger instars) in alfalfa fields. While some pest management programs discount the impact that natural enemies have on maintaining lower populations of pest species, such as E. fabae, we believe that collectively these natural enemies have an impact on E. fabae populations.