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DATE DUE DATE DUE DATE DUE

5108 K:IProj/Aoc&Pres/ClRC/Dateoua.indd PREDATION, SOIL MOISTURE AND MOWING HEIGHT AS POTENTIAL FACTORS IN THE SKEWED DISTRIBUTION OF ATAENI US SPERE T UL US (COLEOPTERA: SCARABAEIDAE) ON GOLF COURSE FAIRWAYS AND ROUGHS

By

Young-Ki J o

A THESIS

Submitted to Michigan State University In partial fulfillment of the requirements For the degree of

MASTERS OF SCIENCE

Department of Entomology

2000 ABSTRACT

Predation, Soil Moisture and Mowing Height as Potential Factors in the Skewed Distribution of Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs

By

Young-Ki J o

Ataenius spretulus (Haldeman) is more abundant and causes more damage to golf course fairways than to the roughs. This study focuses on how predation by carabids and staphylinids affects the distribution of A. spretulus grubs in the fairway and rough and how soil moisture and mowing height affect oviposition and colonization of A. spretulus adults in the fairway and rough. In initial tests, adults of 6 of the most abundant species of carabids and staphylinids found in turfgrass in Michigan were placed individually in small petri dishes with A. spretulus eggs or grubs. Consumption of eggs varied from 64 to 100% and consumption of larvae from 14 to 100% depending on the species being tested. Predation of A. spretulus larvae was investigated in field plots by introducing A. spretulus grubs and recovering them 1 wk later. In 4 separate trials more grubs were recovered from the fairway (73%) than the rough (56%) each time. In a growth chamber,

A. spretulus adults were released into turf arenas consisting of fairway turf and rough turf placed into soil held at different moisture levels in different treatments. Mowing height did not affect colonization by adult beetles, but they preferred turf in moist soil Q 13% water by volume) to turf in dry soil (8-9%). Adult beetle preference for moist soil and predation by carabids and staphylinids may contribute to the skewed distribution of A. spretulus grubs towards golf course fairways, which tend to have higher soil moisture and

lower predator activity than roughs. DEDICATION

To Chookyung Jo and Youngsun Chun

iii TABLE OF CONTENTS

LIST OF TABLES ...... v

LIST OF FIGURES ...... vii

Impact of Predation on the Skewed Distribution of Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Abstract ...... 1 Introduction ...... 2 Materials and Methods ...... 3 Results ...... 8 Discussion ...... 11 Reference cited ...... 19 Tables and Figures ...... 25

Impact of Soil Moisture and Mowing Height on the Skewed Distribution of Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Abstract ...... 40 Introduction ...... 41 Materials and Methods ...... 42 Results ...... 46 Discussion ...... 48 Reference cited ...... 52 Tables and Figures ...... 57

APPENDIX 1: Record of Deposition of Voucher Specimens ...... 62 APPENDIX 1.1: Voucher Specimen Data ...... 63

iv LIST OF TABLES

Impact of Predation on the Skewed Distribution of Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Table Page 1 . Schedule of fertilizer, herbicide and fungicide treatments applied to the annual bluegrass fairway and adjacent rough at the Hancock Turfgrass Research Center, 2000 ...... 25

Consumption of corn rootworm eggs and third instar A. spretulus by staphylinids and carabids found in turfgrass at the Hancock Turfgrass Research Center ...... 26

. Suitability of corn rootworm eggs compared with A. spretulus eggs for consumption by staphylinids and carabids found in turfgrass at the Hancock Turfgrass Research Center ...... 27

Recovery of A. spretulus grubs in fairway and rough soil columns one wk after grubs were released at the Hancock Turfgrass Research Center ...... 28

Proportion of A. spretulus grubs recovered 7 d after grubs were released at the Hancock Turfgrass Research Center, 2000 ...... 29

Predacious insects in our experimental plots ...... 30

Statistics (P-value) testing the effects of block, time, boundary type and mowing height on the density of insects in predator-enhanced and predator- suppressed plots at the Hancock Turfgrass Research Center, 2000 ...... 31

Predators and A. spretulus grubs recovered from our research areas where the number of adult staphylinids and carabids were manipulated with different boundary types in the fairway and rough at the Hancock Turfgrass Research Center, 2000 ...... 32

Parameters of a multiple linear regression model with the independent variables (mowing height, adult carabid and adult staphylinid) and the dependant variable (A. spretulus grubs). For this linear model, 1'2 = 0.32, n = 24,F=3.l4 andP=0.048 ...... 33

Impact of Soil Moisture and Mowing Height on the Skewed Distribution of Ataem'us spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Table Page 1. Percentage of A. spretulus adult beetles recovered from the total number of released beetles ...... 57 . Factorial ANOVA for testing the effects of time, block, soil moisture, and mowing height on the colonization of A. spretulus adults ...... 58

. Recovery of A. spretulus eggs, first instars and adults from turf arenas introduced with A. spretulus adults collected from a golf course in Lansing, MI ...... 59

vi LIST OF FIGURES

Impact of Predation on the Skewed Distribution of Black Turf Ataenius, Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Figure Page 1. Experimental block (18 by 18 m) of annual bluegrass fairway and its adjacent rough at the Hancock Turfgrass Research Center, MI ...... 34

2. Vertical cross-section of two types of boundaries around our plots. The 30°- boundary for a predator-enhanced plot (A) allowed predators to immigrate. The v-shape boundary for a predator-suppressed plot (B) interfered with the movement of predators ...... 35

3. Seasonal captures of Carabidae per pitfall trap per wk in the fairway and rough of control plots at the Hancock Turfgrass Research Center, MI, 2000 ...... 36

4. Seasonal captures of Staphylinidae per pitfall trap per wk in the fairway and rough of control plots at the Hancock Turfgrass Research Center, MI, 2000 ...... 37

5. Seasonal captures of Carabidae per pitfall trap per wk in the fairway and rough of predator-enhanced and predator-suppressed plots at the Hancock Turfgrass Research Center, MI, 2000 ...... 38

6. Seasonal captures of Staphylinidae per pitfall trap per wk in the fairway and rough of predator-enhanced and predator-suppressed plots at the Hancock Turfgrass Research Center, MI, 2000 ...... 39

Impact of Soil Moisture and Mowing Height on the Skewed Distribution of Black Turf Ataenius, Ataenius spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs Figure Page 1. Module consisting of two fairway pots and two rough pots in our greenhouse experiment ...... 6O

2. Turf arenas consisting of two different turf cores (fairway turf core and rough turf core) placed into soils having different moisture levels: one moisture level (A), two moisture levels (B) and four moisture levels (C) ...... 61

vii Impact of Predation on the Skewed Distribution of Ataenius spretulus (Coleoptera:

Scarabaeidae) on Golf Course Fairways and Roughs

ABSTRACT

Ataenius spretulus (Haldeman) is more abundant and causes more damage to golf course fairways than to the roughs. This study focuses on how predation by carabids and staphylinids affects the distribution of A. spretulus grabs in the fairway and rough. In

initial tests, adults of 6 of the most abundant species of carabids and staphylinids found in turfgrass in Michigan were individually placed into petri dishes with A. spretulus eggs or

larvae. Consumption of eggs varied from 64 to 100% and consumption of larvae from 14 to 100% depending on the species being tested. Predation of A. spretulus larvae was

investigated in field plots by introducing A. spretulus grubs and recovering them 1 wk

later. In 4 separate trials more grubs were recovered from the fairway (65%) than the

rough (49%). In a different field study, carabid and staphylinid adults were enhanced or

suppressed through the use of directional barriers. A. spretulus adults were added to all

of the plots at a time when females are expected to deposit eggs. About 8 wk later a

similar number of A. spretulus larvae was found in both treatments despite a 6-fold

difference in the activity of carabid and staphylinid adults. Most carabid and staphylinid

adults are capable of consuming A. spretulus eggs and larvae. However, field conditions

they may not be the most important predators, perhaps because most of their activity is

near the turf surface. Although our experiments support that predation is important, more

work is needed to determine the relative importance of carabid and staphylinid adults and

larvae as predators of A. spretulus and other white grubs.

Key words: Ataem'us spretulus, predators, golf courses. Introduction

As a native species in North America, Ataenius spretulus (Haldeman) is found throughout the continental United States. It is most prevalent in the midwestern and northeastern states. The first damage to turfgrass by A. spretulus was reported in

Minnesota in 1932 (Hoffman 1935). By 1980, turf damage was reported fi'om at least 12 states (Cartwright 1974, Kawanishi et al. 1974, Weaver and Hacker 1978, Wegner and

Niemczyk 1979, Wegner and Niemczyk 1981). Most of the damage caused by A. spretulus occurs on golf course fairways (N iemczyk and Dunbar 1976, Vittum 1995,

Smitley et al. 1998, Vittum et al. 1999). Damage to home lawns or golf course roughs is very rare.

The importance of generalist predators for regulating populations of insect pests has been investigated in some agricultural systems. Carabid beetles in particular are the most studied predators because of their abundance and obvious predation. Carabids are known to be important predators of aphids in cereal crops (Scheller 1984, Winder 1990),

Caterpillars in soybean (Fuller 1988), and fly maggots in onion (Grafius and Warner

1989). Staphylinid beetles are considered the most important predators of dung- inhabiting flies (Roth 1983, Hu and Frank 1997), but little work has been done with staphylinids in turfgrass.

Research on how to alter conditions to support the conservation of natural enemy communities has been conducted in field crop systems. Common agricultural practices such as pesticide applications (Los and Allen 1983, Frarnpton and Cilgi 1992) and tillage (Andersen 1999, Kromp 1999) reduce carabid beetle abundance. Organic farming (Pfiffirer and Niggli 1996, Clark 1999), low-input production systems (Fan et a1.

1993) and dense vegetation (Armstrong and McKinlay 1997, Thomas and Marshall 1999) help sustain a high density of beetle predators.

Previous studies about natural enemies in the turfgrass ecosystems provide some evidence for pest regulation by indigenous natural enemies (Cockfield and Potter 1985,

Potter 1992). Disruption of natural enemies by insecticides incurs outbreaks of some turf pest insects that have been under control by predators (Cockfield and Potter 1983,

Cockfield and Potter 1984, Potter 1993, Terry et al. 1993).

Smitley et al. (1998) in Michigan studied the spatial distribution of natural predators and A. spretulus in golf course fairways and roughs. Predacious insects are relatively more active in roughs than in fairways but conversely A. spretulus adults are less active in roughs. They suggested that the low density of A. spretulus in roughs may be caused by predation and a high incidence of milky disease caused by a Bacillus sp.

(Smitley et al. 1998, Rothwell and Smitley 1999).

More data are needed to define the relationship between natural predators and A. spretulus grubs in golf course fairways and roughs. The objective of this research was to evaluate predation of A. spretulus by carabids and staphylinids in turfgrass. As part of this work we tested individuals of different carabid and staphylinid species to determine their capacity to consume A. spretulus eggs and larvae under laboratory conditions.

Materials and Methods

Laboratory Feeding Experiments. The most abundant turf-dwelling staphylinids and carabids were tested as potential predators of A. spretulus eggs and grubs. In July 2000, we tested the most frequently captured staphylinids, Apocellus sphaericollis (Say), Philonthus carbonarius (Grabvenhorst), Philonthus cognatus

Stephens and immature Philonthus sp., and the most abundant carabids, Amara impuncticollis (Say), Harpalus aflinus (Schrank) and Stenolophus ochropezus (Say). We collected staphylinids and carabids in empty pitfall traps (1.5 cm diameter, 10 cm deep and 32 ml) in turfgrass. The traps were checked every morning and healthy predators were collected for testing. Individual predators were held in separate petri dishes (90 mm diameter, 15 mm height) lined with moist filter paper. They were starved in a growth chamber (dark, 25°C, and 60 % relative humidity) for 24 h.

We used third instars of A. spretulus collected at Royal Scot Golf Course,

Lansing, MI in July. Six A. spretulus grubs were put in each petri dish containing a single predator. The predation on grubs was determined after 24 h in a grth chamber.

The experiment was repeated 4-9 times, depending on the number of live predators obtained from pitfall traps.

In the egg predation experiment, corn rootworm eggs (Diabrotica virgifera virgifera LeConte) were substituted for A. spretulus eggs because A. spretulus eggs were difficult to obtain. Corn rootworrns eggs were supplied by the Northern Grain Insects

Lab, Brookings, SD. A com rootworm egg is a little smaller than an A. spretulus egg (0.7 mm by 0.5 mm). Ten corn rootworm eggs were introduced into each petri dish containing a single predator. Dishes were held in a growth chamber (dark, 25°C, and

60 % relative humidity) and the number of consumed eggs was determined after 24 h.

We also evaluated the efficiency of corn rootworm eggs as a substitute for A. spretulus eggs. We conducted a choice test where each predator was exposed to corn rootworm and A. spretulus eggs at the same time. On moist filter paper in a petri dish, three corn rootworm eggs and three A. spretulus eggs were alternated with each other and equally spaced in a circular pattern. A single predator was released into this petri dish with eggs. Afier 24 h in a growth chamber, the remaining eggs were counted. Proportions of consumed eggs were arcsine square root transformed. All statistical analyses were performed using SAS software (SAS Institute 1990). We tested for differences in predation rates between A. spretulus eggs and corn rootworm eggs by all carabid species combined, and all staphylinid species combinded using PROC MIXED.

Predation of A. spretulus Grubs in the Fairway and Rough. Third instars of

A. spretulus were used as a prey item to evaluate the activity of predacious insects. A. spretulus larvae were collected from Royal Scot Golf Course in July 1999 and 2000. We visually located adult beetles on the surface of greens and picked them by hand. This experiment was conducted in an annual bluegrass (Poa annua reptans L.) fairway and its adjacent rough at the Hancock Turfgrass Research Center of Michigan State University,

East Lansing, MI. The fairway and rough were established in 1995 and have been maintained on a standard program of fertilizer, herbicide and fungicide treatments (Table

1). There was no history of damage by insects or insecticide application.

In 1999, four spots were randomly chosen in one fairway block (18 by 18 m) and additional four spots were chosen in its adjacent rough, 0.8 m from the fairway/rough interface. We pulled a soil column with a standard cup-cutter (10 cm diameter and 10 cm deep) from each spot. The column was wrapped around its side with burlap and put back into the ground. Ten grubs were released on the top of each column and observed until they burrowed into the soil. If individuals failed to burrow within 5 min, they were replaced with new ones. The burlap kept released grubs within the soil column. The released grubs were recovered and counted 7 d later. Three trials were conducted on 7

July, 14 July and 21 July 1999, respectively.

In July 2000, we increased the number of replicates to 6. We randomly chose eleven spots in each of 6 fairway blocks and 6 adjacent rough blocks: five in the fairway, five in the rough, and one control in either fairway or rough. At this time we used plastic

cups (6 cm diameter and 70 ml) to contain A. spretulus grubs. Each cup was punctured

with a pin to allow water drainage. A turf/soil column was cut to fit into the shape of the

cup with a knife. The cup containing the turf/soil column was put back into the ground.

Five A. spretulus grubs were released into each cup. The control cups were covered with

fine mesh immediately after A. spretulus grubs were introduced to prevent access by

surface predators. The cups were recovered 7 d later and examined for surviving grubs.

To meet the assumptions of analysis of ANOVA, the proportion of larvae

recovered was arcsine square root transformed before analysis. The mowing height effect

was tested using a one-way ANOVA with PROC MIXED.

. Predacious Insect Manipulation and A. spretulus Grub Infestation. This

field study was conducted at the Hancock Turfgrass Research Center. Our experimental

area consisted of 6 annual bluegrass fairway blocks and their adjacent rough (18 by 18 m).

By changing the mowing pattern in each annual bluegrass block in April 2000, we

expanded the rough I m inward into the fairway (Fig. 1). This new rough, therefore, has

the same irrigation coverage, turf species, soil quality and thatch development as its

adjacent fairway. The fairway was mowed three times per wk and the rough one time per

wk. The entire area received daily irrigation.

We monitored the activity of predacious insects along the fairway/rough interface with pitfall traps. Eight pitfall traps were arranged within each experimental block: 2 traps in the rough and 2 traps in the fairway, 0.8 m from the interface, and 2 in the rough and 2 in the fairway, 0.2 m from the interface (Fig. l). The pitfall traps were

1.5 cm—diameter, 10 cm-deep and 32 ml empty glass vials. We monitored pitfall trap

captures over a 24 h period, 3-5 times per wk. The pitfall traps were capped when we did not monitor traps or inclement weather was forecasted. We did not count captures from pitfall traps that were flooded by rain or irrigation.

At the fairway/rough interface in each experimental block, two rectangular plots

(0.6 by 0.45 m) were installed (Fig. 1). In previous studies of predatory arthropods, ingress and egress boundaries were used to change their density in barley (Chiverton

1986, Chiverton 1987), in corn (Menalled et al. 1999) and in vegetable gardens (Snyder and Wise 1999). We assigned predator-enhanced and predator-suppressed boundaries to our rectangular plots (Fig. 2). The predator-enhanced boundary emulated the ingress boundary (Menalled et al. 1999). Each plot was surrounded by a trench with a 10 cm- deep vertical slope on the outside wall and a 30-degree incline on the inside wall. The vertical slope was lined by 2.5 mm-thick epoxy glass (Fig. 2A). Once turf-inhabiting predators fell into the ingress trench, they could move only into the plot but not back out.

Our predator-suppressed plot had a v-shaped trench with an epoxy-glass wall in the middle on the trench to prevent predators form crossing (Fig. 2B). Predators that fell into the v-shaped trench could climb back only to their original side of the plot.

We implanted two pitfall traps inside the barriers in each plot: one in the fairway and one in the rough, 0.2 m from the fairway/rough interface (Fig. 1). Captured predatory insects were counted and identified in the field. Data of predators captured in pitfall traps were converted to the number of predators per pitfall trap per wk. Insects caught in the predator—enhanced plots were returned to the plots but those in the predator- suppressed plots were eliminated from the plots. Insect activity was monitored for ten wk from 28 May to 29 July 2000.

For inoculation of A. spretulus to our plots, adult beetles were collected at Royal

Scot Golf Course. We released a total of 21 8 beetles into each plot: 20 beetles on 31 May, 37 on 1 June, 30 on 7 June, 26 on 21 June, and 10 on 22 June. On 31 July, approximately, eight wk after releasing adult beetles, the abundance of A. spretulus grubs in the plots was determined. We pulled ten soil cores (10 cm diameter, 10 cm deep) from each plot with a standard golf course cup-cutter: five fiom the fairway and five from the rough. We broke up the soil samples and counted A. spretulus larvae, pupae and immature predators.

Our experiment was designed as a split block model with the location of an 18 by 18-m fairway/rough plots as the block effect. To test whether the density of predators was different at 0.2 m and 0.8 m from the interface, the distance was the split effect, assigned into each mowing height. To test whether the density of predators was different in predator-enhanced compared with predator-suppressed plots, mowing height was the split effect, assigned into each boundary plot.

Count data were square root transformed to make the data distribution more appropriate for analysis of variance (AN OVA). The converted count data were used to test effects of time, mowing height, boundary type and distance by PROC MIXED with a

REPEATED measure statement. Multiple comparisons between different levels of the effects were made by a least squares means (LSMEAN S) statement.

The relationship between the independent variables (carabid densities, staphylinid density and mowing height) and the dependent variable (abundance of A. spretulus grubs) was tested with multiple linear regression statistics in PROC GLM.

Results

Laboratory Feeding Experiments. Two of the most abundant carabid species in our experimental areas (A. impuncticollis and S. ochropezus) consumed all ten corn rootworm eggs within 24 h in all replicates. They also consumed more than 50% of available A. spretulus grubs (Table 2).

A. sphaericollis, the predominant staphylinid species, showed relatively less

predation, consuming 57% of the eggs and 14% of the grubs in 24 h. Adult Philonthus sp.

consumed most of the applied eggs and 54% of the grubs. P. cognatus consumed 1.7

times more grubs than P. carbonarius, which consumed more eggs than P. cognatus.

Immature Philonthus sp. showed a different predation preference from adult Philonthus

sp. The immature Philonthus sp. fed on a few eggs but actively preyed on all the released

grubs in 24 h (Table 2).

In the choice test, carabids consumed nearly equal amounts of A. spretulus eggs

and corn rootworm eggs while staphylinids consumed more A. spretulus eggs than corn

rootworm eggs (Table 3). Therefore, corn rootworm eggs were a good substitute for A.

spretulus eggs in feeding studies. If any bias was introduced through this substitution, it

would be to underestimate the amount of staphylinid predation of A. spretulus eggs.

Predation of A. spretulus Grubs in the Fairway and Rough. In 1999, more A.

spretulus grubs were recovered from the fairway than the rough (P < 0.001). The

recovery of grubs was different in different trials. The highest recovery of A. spretulus

grubs was in the first trial (88% in the fairway and 62% in the rough) and the lowest

recovery was found at second trial (63% in the fairway and 49% in the rough).

In 2000, the recovery of grubs was not different in the rough and fairway (P =

0.40) (Table 4). When recovery rates in the fairway and rough were compared to

recovery in the control, less grubs were recovered in the rough than in the control, while recovery of grubs in the fairway was not different from the control (Table 5). About 8% of the grubs missing from screened control plots may be due to predation fiom carabid or

staphylinid larvae already present in the soil columns, or mortality from unknown causes. Predacious Insect Manipulation and A. spretulus Grub Infestation. Among arthropods caught in our pitfall traps, we counted only potential predators. We collected

1101 predacious insects, representing 4 families: Carabidae, Staphylinidae, Formicidae and Histeridae (Table 6). F ormicidae and Histeridae were not captured fi'equently, comprising 1% and 0.5% of total insects, respectively. The most abundant predators caught by pitfall trap were Carabidae (44%) and Staphylinidae (3 8%). Two species of carabids, A. impuncticollis and S. ochropezus, accounted for 75% of all carabids captured.

A. sphaericollis and Philonthus sp. were the most abundant staphylinid species, comprising 96% of all staphylinids captured.

Adult carabids and staphylinids were active at different times of the season

(Table 7). When their captures in May, June, and July were compared using an

ESTIMATE statement of SAS MIXED, carabids were most active in May and June, while staphylinids were most active in May and July (Figs. 3,4,5 and 6).

In control plots, the numbers of adult predators caught in the fairway and rough were not different between 0.2 m and 0.8 m from the fairway/rough interface (P = 0.62).

The density of staphylinid adults was different in the fairway and rough. More adult staphylinids were caught in the rough than in the fairway, while carabids did not show any difference between the fairway and rough (Table 7).

In predator-enhanced and predator-suppressed plots, captures of adult predators were different depending on the different types of boundaries (Tables 7 and 8). Predators did not increase in the plots having predator-enhanced boundaries compared with control plots. Predator-suppressed boundaries decreased the captures of predators by 4-fold compared with control plots. No difference was found in the densities of carabids adults

(P = 0.57) and staphylinid adults (P = 0.33) in the fairway and rough within predator-

10 enhanced and predator-suppressed plots. The interaction between the boundary and mowing height effect on the carabid density was significant (P < 0.01). Because of this, the interaction effect was analyzed depending on the boundary types, using a SLICE option of PROC MIXED of SAS. The interaction was significant in predator-enhanced plots (P < 0.05) but was not significant in predator-suppressed plots (P = 0.14). This suggested that the carabid density was greater in the fairway than in the rough of predator-enhanced plots. An average of 6 immature predators was isolated per 0.1 m2.

Their abundance was not different in the fairway and rough (P = 0.32) or in predator- enhanced and predator-suppressed plots (P = 0.62) (Tables 7 and 8).

Releasing A. spretulus adult beetles was a successfirl way to infest plots with A. spretulus grubs. At the end of experiment we found the average of 85 A. spretulus grubs per 0.1 m2. There was no difference in the numbers of grubs found in predator-enhanced compared with predator-suppressed plots (P = 0.85) and a marginal difference in the fairway and rough (P = 0.06). In predator-suppressed plots, more grubs were found in the fairway than in the rough (Tables 7 and 8).

With multiple linear regression analysis, we determined how the numbers of adult carabids and staphylinids, and mowing height were related to the number of A. spretulus grubs in predator-enhanced and predator-suppressed plots (T able 9). The density of staphylinid adults was positively related with grub density while the adult carabid density was negatively correlated to the grub density.

Discussion

Laboratory Feeding Tests. Little is known of the feeding habits of staphylinids and carabids inhabiting turfgrass because actual observation of predation on grubs or

11 eggs under field conditions is difficult. Staphylinids and carabids were shown to be beneficial predators of pest insects in previous laboratory feeding tests. Adults and larvae of dung-inhabiting Philonthus sp. contribute to the control of horn fly eggs and larvae in northern Florida (Roth 1983, Hu and Frank 1997). Some Philonthus sp. collected in turfgrass in KY also prey on 24% of 10 Japanese beetle (Popilliajaponica Newman) eggs and 47% of 10 first instars of Japanese beetle in 48 h. In the same experiment, an

Amara sp. ate up to 77% of 10 Japanese beetle eggs in 48h (Terry et al. 1993).

The most abundant staphylinid species at our research site in MI, A. sphaericollis, is reported to be a scavenger, feeding on humus and decaying vegetation

(Chittenden 1915). Thus, it did not feed A. spretulus grubs in our laboratory tests.

However, it consumed up to 50% of the available A. spretulus eggs in 24 h. P. carbonarius and P. cognatus, our second and third most abundant staphylinid species, both consumed A. spretulus eggs and grubs. In petri dishes, Philonthus larvae were voracious predators of A. spretulus grubs. They preyed on all the available grubs in our tests. More field research is needed to determine their role in grub predation.

Our feeding tests clearly demonstrated that adults of the most abundant carabids and Philonthus sp. found in turfgrass are capable of feeding on A. spretulus eggs and grubs. Furthermore, Philonthus sp. larvae were more efficient predators of A. spretulus grubs than any other predator except adult H. afi‘inus. However, adult A. sphaericollis, the most abundant staphylinids species, was only a moderate egg-feeder and did not feed on A. spretulus grubs.

Predation of A. spretulus Grubs in the Fairway and Rough. Grub predation in turfgrass has received little attention so far. Most of the previous experiments have focused on surface predation. In these tests, predators consumed up to 75% of 5 sod

12 webworm (Crambus and Pediasia sp.) eggs, 73% of 10 Japanese beetle eggs and 27-53% of 10 fall arrnyworrn (Spodopterafiugiperda (J. E. Smith» pupae in 48 h of exposure on the soil surface in Kentucky bluegrass (Poa pratensis L.) (Cockfield and Potter 1984)

(Terry et al. 1993).

In our experiments, the actual missing rate of A. spretulus grubs in the fairway and rough was 16-26% in 7 d if missing rates in the fairway and rough were subtracted by missing rates in controls. Compared to the immobile eggs or pupae used in previous tests, relatively less predation of grubs in our experiment may be due to the habitation of grubs in the soil and the fact that they were healthy and unrestrained.

Overall, more A. spretulus grubs disappeared in the rough than in the fairway.

The density of staphylinid adults was much higher in the rough compared with the fairway in our experimental areas, but we only assume that the density of staphylinid larvae were also greater in the rough because we could not sample them effectively. The difference in predation rates may have been caused by the distribution of predators in the rough and fairway (Smitley et al. 1998, Rothwell and Smitley 1999).

Predacious Insect Manipulation and A. spretulus Grub Infestation. In

Kentucky bluegrass lawns in KY, centipedegrass turf in GA and golf courses in MI, ants are the most abundant surface insects. Staphylinids and carabids account for over 90% of the total number of predacious insects other than Formicidae (Cockfield and Potter 1985,

Braman and Pendley 1993, Smitley et al. 1998). Most of the staphylinids in Kentucky bluegrass in KY are less than 5 mm long(Amold and Potter 1987). A. sphaericollis is the most abundant staphylinid in centipedegrass (Eremochloa ophuiroides (Munro) Hack) in

GA (Braman and Pendley 1993). Most of the staphylinids found in perennial ryegrass

(Lolium perenne L.) fairways and roughs in M] are Philonthus sp. and the most common

13 carabids are species of Bembidion, Amara and Stenolophus (Rothwell and Smitley 1999).

The community of predacious insects in our experimental areas at the Hancock Turfgrass

Research Center, MI was similar to that described in previous studies, with the exception that ants were not abundant. Ants comprised only 1% of total collected predacious insects in our experimental areas while 46% of all predacious insects were ants on golf courses in MI (Smitley et al. 1998).

Coincidence in time with A. spretulus is important for potential predators to become efficient control agents. In MI, A. spretulus adult beetles appear on turfgrass in early May and lay eggs in the thatch and soil from late May to early July. Eggs hatch and grubs grow under turfgrass until late July or early August (Smitley et al. 1998, Vittum et al. 1999). The most vulnerable period of A. spretulus for predation may be from late May to late July when it is in the egg or the immature life stages.

Seasonal activities of adult staphylinids and adult carabids were monitored in this experiment. The greater activity of adult carabids was concurrent with the eggs and grubs of A. spretulus, allowing the potential for predation. Also, the most abundant carabids, A. impucticollis and S. ochropezus, consumed A. spretulus eggs and grubs in petri dish tests. According to the fluctuation of adult staphylinid activity in our experiment over time, they may have less impact on the survival of A. spretulus eggs and grubs in May and July. However, we do not know when carabid and staphylinid larvae are the most active.

In previous research, mowing practices are suggested as a potential factor affecting the spatial distribution of adult predacious insects in golf course fairways and roughs. When crossing fiom rough into fairway, the numbers of staphylinids and in some case the numbers of carabids dropped 3-fold within a distance of 1 m from the

14 fairway/rough border (Smitley et al. 1998). In our control plots, we found 1.5-fold more adult staphylinids were trapped in the rough than in the fairway, but the activity of adult carabids remained similar throughout.

The v-shaped boundary in predator-suppressed plots decreased predator activity as we proposed. Compared to the control plots, 4-fold less carabid adults and 10-fold less staphylinid adults occurred in the predator-suppressed plots. In predator-enhanced plots, the numbers of carabids and staphylinids were not different from those in control plots. In predator-enhanced plots, carabid catches were 65% greater in the fairway than in the rough. This indicates that carabids are either more active or denser in the fairway.

Our experiment was conducted using new roughs that have the same soil conditions as the adjacent fairways. Only mowing practices from April to August 2000 were altered to create the rough from the fairway. We, thus, eliminated all soil conditions, except perhaps soil moisture, which varies depending on the extent of root and mowing height. Two-fold more A. spretulus grubs were found in the fairway than in the rough of predator-suppressed plots, while similar numbers of grubs were found in the fairway and rough of predator-enhanced plots. Female ovipositional preference and different predation rates in the fairway and rough may explain this distribution of A. spretulus grubs in predator-enhanced and predator-suppressed plots. A. spretulus females may have preferred the fairway for their oviposition. Site suitability for scarab beetles is influenced by soil moisture (Potter 1983, Allsopp et al. 1992). Although we did not collect soil moisture data, it is possible that moisture levels were higher in the fairway because fairway turf has a much reduced root system compared with rough turf (Madison and Hagan 1962, Morhard and Schulz 1998). The fairway may be attractive to female A. spretulus for other unknown reasons.

15 Predator activity may explain the similar numbers of grubs found in the fairway and rough of predator-enhanced plots. If A. spretulus females prefer the fairway to oviposit, it is expected that grub density would be greater in the fairway of predator- suppressed plots. In the predator-enhanced plots, carabids were more active on the fairway side, which may cover-up the effect of A. spretulus ovipositional preference.

Thus, their predation may prevent the overpopulation of A. spretulus grubs in the fairway of predator-enhanced plots.

With the multiple linear regression analysis, the number of grubs is adversely affected by adult carabid density, according to the negative slope of its parameter.

However, the positive parameter of adult staphylinid density implies that adult staphylinids may not be effective predators of A. spretulus. The predominant staphylinid species in our experimental areas, A. sphaericollis, is a scavenger, feeding on plant materials (Chittenden 1915), and it was the least likely to feed on A. spretulus grubs. We used this multiple linear regression model only to evaluate the positive or negative relationship to grub density because this was a weak model. Additional factors may be needed to supplement this model.

The density of carabid and staphylinid larvae may be more important for explaining the density of grubs than adult predators, because we saw little difference in A. spretulus grubs between predator-enhanced and predator-suppressed plots. In our experimental plots, we did not detect any difference in the density of immature predators between predator-enhanced and predator-suppressed plots or between fairway and rough sides. This may be caused from the density of carabid and staphylinid larvae, which depends on the density of adults in the previous year. Turf conditions in our plots were uniform in the year previous to our experiment. The density of predator larvae in

16 predator-suppressed plots may be less than in predator-enhanced plots in 2001 , according to the density of adult predators in 2000. Sampling from our plots in 2001 will test this hypothesis. Similar results were observed in previous research. A. spretulus grub infestation levels were not different in the new fairway and rough in the first year after altering the fairway/rough border of a golf course in MI, but changed significantly in the second year after alteration (Rothwell and Smitley 1999).

Our research raised a question about the damage threshold for A. spretulus grubs.

An economic threshold for A. spretulus grubs has not been determined but levels as low as 30 grubs per 0.1 m2 have been suggested (V itturn et al. 1999). In annual bluegrass roughs of our plots we found from 3 to 178 A. spretulus grubs per 0.1 m2 but none of the roughs had turf damage. Five of our annual bluegrass fairways of our plots contained more than 100 grubs per 0.1 m2. Two of them showed slight discoloration and dead spots.

Damage to turf is determined by the vigor of the turf and by the population density of A. spretulus grubs. Our data suggest that turfgrass in the rough may be more tolerant of grub injury than fairway turf and that more than 100 A. spretulus grubs per 0.1 m2 are necessary to cause significant turf damage in healthy annual bluegrass fairways. Our observations agree with the previous study by Vittum(1995), where heat-stressed and closely mowed bentgrass (Agrostis sp.) did not support 20 A. spretulus grubs per 0.1 m2 while up to 250 grubs per 0.1 m2 thrived in the same species of grass under moderate conditions without visible symptoms.

In previous studies, A. spretulus grubs were found to be 3 to 10-fold more abundant in golf course fairways than roughs. At the same time, staphylinids and carabids were much more abundant in the rough, suggesting that predation was greater in the rough. Our study showed that adults of the most abundant species of carabids and

17 staphylinids found in turfgrass are capable of consuming A. spretulus eggs and gurbs. We also discovered that staphylinid larvae collected fi'om turfgrass prey on A. spretulus grubs.

When A. spretulus grubs were released into the fairway and rough, more grubs survived in the fairway than in the rough. These experiments provide additional evidence that predation is important for keeping A. spretulus grubs under control in golf course fairways and that lack of predation contributes to outbreaks of A. spretulus grubs in fairways.

18 Reference Cited

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20 Hu, G. Y., and J. H. Frank. 1997. Predation on the horn fly (Diptera: Muscidae) by five species of Philonthus (Coleoptera: Staphylinidae). Environ. Entomol. 26: 1240-1246.

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23 Figure Captions

Fig. 1. Experimental block (18 by 18 m) of annual bluegrass fairway and its adjacent rough at the Hancock Turfgrass Research Center, MI.

Fig. 2. Vertical cross-section of two types of boundaries around our plots. The 30°- boundary for a predator-enhanced plot (A) allowed predators to immigrate. The v-shape boundary for a predator-suppressed plot (B) interfered with the movement of predators.

Fig. 3. Seasonal captures of Carabidae per pitfall trap per wk in the fairway and rough of control plots at the Hancock Turfgrass Research Center, MI, 2000.

Fig. 4. Seasonal captures of Staphylinidae per pitfall trap per wk in the fairway and rough of control plots at the Hancock Turfgrass Research Center, MI, 2000.

Fig. 5. Seasonal captures of Carabidae per pitfall trap per wk in the fairway and rough of predator-enhanced and predator-suppressed plots at the Hancock Turfgrass Research

Center, MI, 2000.

Fig. 6. Seasonal captures of Staphylinidae per pitfall trap per wk in the fairway and rough of predator-enhanced and predator-suppressed plots at the Hancock Turfgrass Research

Center, MI, 2000.

24 Table 1. Schedule of fertilizer, herbicide and fungicide

treatments applied to the annual bluegrass fairway and adjacent

rough at the Hancock Turfgrass Research Center, 2000.

Application date Treatment Rate (kg/ha) Targets

11 May fluazifop-P-butyl 1.8 annual grasses

17 May nitrogen 48.8

31 May fluazifop-P-butyl 1.8 annual grasses

1 June chlorothalonil 4.6 dollar spot

14 June chlorothalonil 4.6 dollar spot

26 June nitrogen 48.8

27 June chlorothalonil 4.6 dollar spot

6 July chlorothalonil 4.6 dollar spot

20 July iprodion 9.2 dollar spot

27 July nitrogen 48.8

3&9 iprodion 9.2 dollar spot

25

(%)

7.3

8.0

0.0

0.0

10.2

5.5

11.1

11.4

SE

1

i

i

1:

:1:

i

_t

i

_1;

offigLrubsb

8.0

100

100

13.9

66.7

38.9

55.6

50.0

‘

Center.

Mean by

Predation (DCDOJV'CO

CD 6

n 4

Research

spretulus

A.

(%)

1.3

5.0

7.3 5.7

0.0

0.0

0.0

Turfgrass 18.0 SE

1

i

1;

i

instar

i

_t

;l-_

eggs8

i

_t

of

0.0

100

100

15.0

98.7 77.8 56.7

64.3

third

Mean

Hancock

and

eggs.

the

Predation

2

7

n

15

18

15

15

grubs.

14

18 at

- .7 eggs

rootworm

spretulus

turfgrass

com

rootworm

A.

in

10

6

of of

corn

(Say)

found

(Gravenhorst)

(Say)

out out

of

sp.

Stephens

(Say)

(Schrank)

carabids

ochropezus

consumed consumed

carbonan’us cognatus

sphaen'collis

Philonthus

affinus

and

Consumption

insects

impucticollis

2.

Immature

Philonthus

Philonthus

Stenolophus

Harpalus

Apocellus

Amara

a'Proportions bProportions

Table

Control

Staphylinidae

Predacious Carabidae staphylinids

26

Pa

0.35

002*

by

(%)

8.7

0.0

0.0

13.3

33.3

0.0

spretulus

SE

1

i

i

1-

i

g

1

A.

33.3 33.3

l 0.0

I!

100

100 rOOMOijgS

_J 583183

'r

61.9

86.7

66.7

consumption Mean

.

Center.

for

Corn between

".1.‘thh:u~

i ,

eggs

different Research (%)

eggs spretulus

0.0 0.0

0.0

16.7 0.0

SE

A. 1

i

i

Turfgrass g _t

100

significantly

100.0

is 0.0

1001 10010.0 100

100

905105

with 83.3 spretulus

Mean rate

A.

Hancock

the compared

7 at

2

predation

eggs

the

level.

turfgrass

5%

means

in

rootworm

the

at

(Say)

found

asterisk

corn

(Gravenhorst)

(Say)

Stephens

of

eggs

(Say)

one

(Schrank)

by

carabids

ochropezus

carbonan'us

cognatus

rootworm

and

sphaericollis

Suitability

affinus

insect

followed

3.

impucticollis

corn

Carabidae

Staphylinidae

and

Table

Stenolophus

Harpalus Philonthus Philonthus

Apocellus

Amara All

All

aP-value

staphylinids

Predacious

Staphylinidae Carabidae

Control eggs

27 Table 4. Recovery of A. spretulus grubs in fainlvay and

rough soil columns one wk after grubs were released at the

Hancock Turfgrass Research Center.

Date Grubs recovered (%) Pa

Fairway Rough

7-14 July 1999” 4 87.5 1 7.5 62.5 1 7.5 0.0022**

14-21July 1999b 4 63.2 i 4.4 49.2 i 4.4 0.21

21-28 July 1999b 4 77.7 1 4.1 58.6 i 1.8 0.07 20-27 July 2000° 6 71.3 i 11.7 54.3 1 9.7 0.40

“P-value followed by two asterisks means the grub recovery

is significantly different between the fairway and rough at the

1 % level.

bConducted in one 18 by 18 m annual bluegrass fairway and its adjacent rough. A soil column was 10 cm diameter and

10 cm deep.

°Conducted in six 18 by 18 m annual bluegrass fainlvays and their adjacent roughs. A soil column was 6 cm diameter and 3 cm deep. Table 5. Proportion of A. spretulus grubs recovered

7 d after grubs were released at the Hancock

Turfgrass Research Center, 2000.

Treatment n A. spretulus lubs recovered (%)

Fairway 6 71.3 1 11.7ab

Rough 6 54.3 1 9.7a

”Control 6 91.9 1 8.1b

Means 1 SE within a column followed by the same

letter are not significantly different (P = 0.05; LSMEANS

statement in SAS MIXED).

“Control plots which prevented surface predators

from accessing A. spretulus grubs.

29 Table 6. Predacious insects in our experimental plots.

Relative

Taxa rla abundance (%)

Carabidae

Amara impuncticollis (Say) 304 27.6

Stenolophus ochropezus (Say) 140 12.7

Harpalus afi‘inus (Schrank) 37 3.4

Stenolophus comma (Fabricius) 23 2.1

Anisodactylus sanctaecmcis (Fabricius) 10 0.9

Acupalpus partiarl'us Say 7 0.6

Other species 77 6.7

Staphylinidae

Apocellus sphaericollis (Say) 255 23.2

Philonthus cognatus Stephens 69 6.3

Philonthus carbonan‘us (Gravenhorst) 55 5.0

Immature Philonthus sp. 36 3.3

Other species 19 1.7

Formicidae 61 1 .0

Histeridae 1 1 0.5

‘3 Total captures in pitfall traps at the Hancock Turfgrass Research

Center from 21 May to 29 July 2000.

30 0.85 0.06

0.31 0.14 spmtuluggrubs A. Hancock the at

_ -. mowing ._

_. predatorsa

‘Jn'rnfi" and

plots 0.22 0.62 0.32 0.28 '3‘

‘3 ....

respectively. 165‘

type

level,

Immature

1%

or

boundary 2000.

**

5%

July

time, the predator-suppressed

0.48 0.33 0.35 0.32

0.06 31

staphylinids at

0.0001

0.0043” 0.0001“ on

and block,

Adult

of

data

significant

effects are

carabids 0.57

0.21

0.75 0.17 0.03*

0.008“ the

0.0004” 0.0006“ observational

Adult

predator-enhanced

asterisks one

in

testing

two

only

2000.

or

hem

of -value)

insects

one (P

of

by

Center,

height

Mowing

because

X height

density

followed

Statistics

effect

Mowing Research

the

7.

variation

X

height

time

Boundary

of

Boundary Mowing

on

X X

X

Table

P-values

aNo

height Turfgrass

Block

Boundary

Source

Boundary

Mowing

Time

Time Time Time

31

0.8b i

plot ngh of 02101c

091026 3.7 05103a rough and

Predator-

0.1c 0.1c

0.3a number

1 1 LSMEANS

1

suppressed the

Fainlvay

0.2

0.3

0.5 98130a fainlvay "F 0.05; I“ = the where in (P -A“ '3'

0.3b 0.3b areas types

1 :t Rough different

plot 2.2 2.4 research boundary control

0.3b

No-boundary our

1 significantly

Fairway 16103a

2.5 not from

different

are column. with

letter soil 0.3b

2.2ab recovered 1

1

2000. plot Rough same 1J102a

06102a 2.5

6.4

grubs cm-deep the

manipulated 10

by Center,

Predator-

2.0ab enhanced

1 and were

meqr wk.

15103a

spretulus 0.410.1a

41106a

6.7 followed

per

A. Research row carabids

and trap

a cm-diameter

and

MIXED).

10 pitfall

within

Turfgrass

per per

SE

SAS fllbsb Predators

1

in predatorsb

8. Hancock

staphylinids

staphylinids“ carabidsal

Numbers Captures Means

Table

a

b

spretulus

the statement

Insects

Immature

Adult

Adult A. adult at

32 Table 9. Parameters of a multiple linear regression model with the independent variables (mowing height, adult carabid and adult staphylinid) and the dependant variable (A. spretulus grub). For this linear model, 3 =

0.32, n = 24, F = 3.14 and P = 0.048.

Parameter Estimate P for estimates

Intercept 2.00 0.0001

Mowing height 0.77 0.056

Adult carabid -1.09 0.044

Adult staphylinid 1.68 0.018

33

18m

Fainlvay

Pitfall

trap .

34

enhanced

A.

suppressed

B.

Predator-

Predator-

plot

plot

35 22. ocaw _ 48.2

36 eepgquec)

.3361 ll sméaulol

22.

6:33

>m2camflol

cmsom

I? >32

eepluufiudms

37

plots

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39 Impact of Soil Moisture and Mowing Height on the Skewed Distribution of Ateam'us spretulus (Coleoptera: Scarabaeidae) on Golf Course Fairways and Roughs ABSTRACT

Ateanius spretulus (Haldeman) grubs are more common in golf course fairways than roughs and the grubs are more likely to damage fairway turf. We evaluated the effects 5‘ 1

w of soil moisture and mowing height on the preference of A. spretulus adults for MA'A

{Am

-‘ oviposition and colonization. In grth chambers, A. spretulus adults were released .k- into turf arenas consisting of two different types of turf cores (cut at fairway height and rough height) placed into soils held at different moisture levels. Seven days afier releasing adult beetles, we examined turf cores for eggs and first instars. Seven different experiments were conducted at different time intervals from August 1999 to

July 2000. Mowing height did not affect colonization by adult beetles, but they preferred moist soil Q 13% water by volume) to dry soil (8-9%). Adult beetle preference for moist soil may contribute to the skewed distribution of A. spretulus grubs towards golf course fairways, which tend to have higher soil moisture than roughs. The univoltine life cycle of A. spretulus in Michigan is discussed.

Key words: Ateam'us spretulus, soil moisture, mowing height, golf courses, colonization, oviposition.

40 Introduction

Ataenius spretulus (Haldeman) (Coleoptera: Scarabaeidae) is an important pest of golf course turfgrass (Cartwright 1974, Kawanishi et al. 1974, Weaver and Hacker

1978, Wegner and Niemczyk 1979, Wegner and Niemczyk 1981). The distribution of A. spretulus grubs on golf courses is skewed toward fairways and results in more frequent damage to fairways compared with adjacent roughs. Natural enemies have been proposed to cause this distribution pattern of A. spretulus grubs (Smitley et al. 1998).

Mowing practices and chemical use may affect the distribution of A. spretulus and its predators on golf course turf (Smitley et al. 1998, Rothwell and Smitley 1999).

When the mowing regime on a golf course was changed, the density of A. spretulus grubs remained the same in the first year, but increased in the new fairway and decreased in the new rough in the second year. At the same time, predators became more active in the new rough and less active in the new fairway (Rothwell and Smitley

1999). Similarly, more predacious beetles were found on uncut grassland compared with cut grassland (Morris and Rispin 1987). Among other turf scarab beetles,

European chafer, Rhizotrogus majalis Razoumowsky, grubs were more common in pastures mowed during the female beetles’ oviposition flights than in grass that was not mowed (Gyrisco et al. 1954).

Reduced abundance of predators caused by insecticide application may also cause an increase in the density of some turf pest insects. Insecticide treatment before or during oviposition periods of adult scarab beetles interferes with predation on their eggs and grubs and incurs high populations of white grubs (Terry et al. 1993).

Scarab beetles in turfgrass are affected by soil moisture, texture and pH. May or June beetles, Phyllophaga crim'ta Burmeister, flights and oviposition are closely tied to

41 rainfall (Gaylor and Frankie 1979). Another scarab turf pest, the southern masked

chafer (Cyclocephala immaculata Olivier) does not lay eggs in dry soil (Potter 1983).

Choice and non-choice tests with Japanese beetle, Popilliajapom'ca‘ Newman, and rose

chafer, Macrodactylus subspinosus (F.), show that both scarabs lay more eggs in moist

soil, up to field capacity, and that rose chafer has no ovipositional preference for soil textures and Japanese beetle avoids oviposition into pure sand (Allsopp et al. 1992). In the only report of a pH effect on scarabs in turfgrass, the masked chafer (Cyclocephala

sp.) is adversely affected by low pH (Potter et al. 1996).

Previous observations that A. spretulus adults were consistently found to be 2 to

4 times more abundant in the fairway than in the rough may partially explain the higher density of A. spretulus grubs in the fairway (Smitley et a1. 1998). This may reflect the

female’s preference of the fairway to rough for an oviposition site. The objectives of this study are to determine how mowing height and soil moisture affect the colonization

and ovipositional preference of A. spretulus adult beetles.

Materials and Methods

Mowing Height Experiment. Turfgrass modules were established and

maintained in a greenhouse (Fig. 1). The average air temperature was 278°C in June

and 294°C in July 1999. Perennial ryegrass (Lolium perenne L.) was seeded into 40 plastic pots (15 by 15 cm) filled with loamy sand soil (85.9% sand, 9.9% silt, 4.2% clay, and a pH of 6.5) in March. The grass was irrigated daily and fertilized weekly with 0.8

g/liter of 20:20:20 N:P:K. The grass was clipped by hand twice each wk. Turf maintained as fairway was cut to a height of 1.5 cm while turf maintained as rough was cut to a height of 5.0 cm.

42 Ten experimental modules were made from 40 square pots filled with turf.

Each module consisted of two fairway pots and two rough pots bound tightly together

(Fig. 1). The rims of each pot that faced the inside of a module were cut down to the level of the soil surface. Thus A. spretulus adults could move around all four grass sections but they could not easily leave the module.

A. spretulus adults were easily found on the surface of golf course greens in

Michigan in early June. We collected them at Royal Scot Golf Course, Lansing, MI.

Forty beetles were introduced into each module. After beetles were released, each module was covered with a fine-net cage (30 by 30 by 50 cm). The cage was removed briefly each time we watered or clipped grass. These plots were maintained for two months after beetles were released. At the end of the experiment, each section of all modules was torn apart and examined for A. spretulus grubs.

Numbers of grubs in the 2 fairway sections were combined and those in the 2 rough sections per module were combined. These numbers of grubs were square root transformed before analysis. Means of grubs found in the fairway were compared to those in the rough using a PROC MIXED statement in SAS software (SAS Institute

1990)

Soil Moisture and Mowing Height Experiment. Seven different experiments were conducted from August to September 1999 and May to July 2000 in a growth chamber. All A. spretulus adults were collected at Royal Scot Golf Course, Lansing, MI

as previously described. Adult beetles captured in the fall of 1999 were newly emerged,

while the beetles collected in the spring and summer of 2000 had already survived the

previous winter. The growth chamber was set at 25°C and 60% relative humidity with a

photo period of 12:12 (lightzdark).

43 Turf cores (2 cm diameter and 4 cm deep) were taken fi'om annual bluegrass

(Poa annua raptans L.) fairway and rough at the Hancock Turfgrass Research Center,

East Lansing, MI. The fairway was maintained at a mowing height of 1.5 cm with 1.5 cm thatch while the rough was maintained at a mowing height of 5.0 cm with 3.0 cm thatch. No insecticides were applied in 1999 or 2000. The soil of this area was

Owosso-Marlette sandy loam with a pH of 7 .5.

Turf cores were placed into pots of steam-sterilized loamy sand soil (87.4% sand,

9.3% silt, 3.4% clay, and 7.1 pH). The bulk density of this loamy sand was 1.41 g/cm3 and the saturation point was calculated to be 46% water by volume. The wilting point (-

1.5 MPa) was estimated to be approximately 6% water by volume, using the general relationship between soil moisture and soil texture (Brady and Wei] 1999).

To achieve the desired soil moisture levels, we added the amount of water determined as a percent by volume into the soil (Fig 2). Soil moisture in the prepared turf arenas was stabilized for 24 h before A. spretulus adults were released. Each turf arena was enclosed within a pin-holed transparent plastic bag after beetles were added.

In a preliminary experiment, this transparent plastic bag was effective for maintaining soil moisture. After one wk, soil moisture levels were within 2% of the original level.

In the first experiment, two fairway and two rough cores were placed in each of ten round plastic pots (10 cm diameter and 15 cm deep) (Fig. 2A). Soil was maintained at the same moisture level (17% water by volume). Fifteen A. spretulus adults were released in each arena on 19 August 1999. One wk later, we pulled out the turf columns and counted adult beetles, eggs and first instars with a dissecting microscope.

In experiments 2 and 3, two different soil moisture levels were created to give A. spretulus adults a choice for colonization and oviposition (Fig 2B). Soils containing 9%

44 and 23% water by volume were prepared. A round plastic pot was divided in the middle by an impermeable plastic sheet. Half of the pot was filled with dry soil (9% water by volume) and the other half with wet soil (23% water by volume). One fairway core and one rough core were implanted into each half of the pot. Fifteen A. spretulus adult beetles were released into each of ten arenas on 24 August 1999 (experiment 2). A wk later, we pulled out the turf cores and counted adults, eggs and first instars with a dissecting microscope. Experiment 3 was conducted with the same methods on 4

September] 999.

In experiments 4 to 7, four different soil moisture levels were created to test A. spretulus preferences for 8%, 13%, 20% or 26% soil moisture by volume (Fig. 2C).

Each arena consisted of four 10 by 10 by 10 cm square plastic pots, tightly pushed together without any gap between pots. The inside rims of the four pots were cut down to the soil surface level to allow beetles free movement. One fairway and one rough core were put in each pot. A total of six plots were set up, including one control that was used for monitoring soil moisture levels. Control pots were weighed each day and water was added to all pots, as needed in the control pots. Twenty A. spretulus adults were released in each arena. The arenas were examined one wk later for adults, eggs and first instars. From late May through mid July, four different experiments were sequentially conducted.

If eggs were detected in turf cores, the top 5 cm of soil in each pot was also examined for eggs. Eggs were isolated from soil samples with a semi-automatic elutriator (Byrd et al. 1976) and sugar floatation (Jenkins 1964), which are used to extract nematodes, fungi or insect eggs from soil. The soil samples were filtered through 850 um coarse and then 75 um fine steel screens by an elutn'ator. Eggs and debris mixtures

45 caught in the fine screen were centrifuged in a 2 mol sugar solution and then in pure water. The eggs floating on the supernatant of the pure water were collected and counted with a dissecting microscope.

Colonization preference of A. spretulus adults was determined from the proportion of recovered adults to the total number of adults introduced into each turf arena. These percentage data were arcsine square root transformed before analysis.

Each arena was considered as a block. The first experiment was statistically tested as a randomized complete block model by a single factorial analysis of variance (AN OVA) using a SAS PROC MIXED procedure. The remaining experiments were analyzed as a spit block model. In this model, the effect of time was nested with the block, and mowing height was considered as the split effect for each moisture level. The effects of time, mowing height and soil moisture were tested by a three-factorial AN OVA. The recovery of adults was compared between the fairway and rough or among different soil moisture levels by a least squares means (LSMEAN S) option with PROC MIXED. The numbers of eggs and first instars isolated from turf cores were square root transformed before analysis. The effects of time, soil moisture and mowing height were tested by a three-factorial ANOVA.

Results

Mowing Height Experiment. A mean of 1.8 grubs was found in two fairway sections and a mean of 1.6 grubs was found in two rough sections of each module.

Grub occurrence was not different among the fairway and rough sections (P = 0.92).

We found few survived A. spretulus adults at the end of our experiment.

Soil Moisture and Mowing Height Experiment. In experiment 1, mowing

46 height did not affect colonization by A. spretulus adults. Similar numbers of beetles were recovered in the fairway and rough (Table 1).

In experiments 2 and 3, block and mowing height did not impact the colonization behavior of adult beetles. However, more beetles selected turf cores in wet soil than in dry soil, regardless of block and mowing height (Table 2).

In experiments 4 to 7, the recovery of beetles was also not different among blocks or between the fairway and rough. Adult colonization was again significantly different among four different soil moisture levels (Table 2). Adults consistently preferred wet soil to dry soil (Table 2). Multiple comparisons by the least square means test showed that more beetles colonized soils containing 3 13% water by volume than 8% (P 5 0.001), while their responses were not different among the three moisture levels 3 13% (P =

0.41) (Table 1).

Over 50% of the released adult beetles were recovered after one wk in experiments 1 to 3 where each plot was 78.5 cmz. Only 28-46% of the beetles were recovered in experiments 4 to 7 where each plot was 400 cm2. As the size of the turf arena increases, fewer beetles were recovered. In experiment 7 conducted on 10 July

2000, only 5.7% of the recovered beetles were alive. In the other experiments, over

87% of the recovered beetles survived (Table 3).

In experiments 1 to 4, using adult beetles collected in August, early September and mid May, we did not find any A. spretulus eggs or first instars. Meanwhile, we found eggs in experiments 5 and 6 and first instars in experiments 6 and 7. A total of

114 eggs and 172 first instars were isolated in these three experiments. The number of of eggs and grubs in experiment 6 initiated on 15 June comprised 82% of the total eggs and first instar grubs found in all 7 experiments.

47 When eggs and grubs were found, time was a significant factor (P < 0.01).

When statistical analysis was run with the numbers of eggs and first instars collected from experiments 5,6 and 7, there was a significant mowing height effect (P < 0.05) but no moisture effect (P = 0.56) on oviposition.

Egg separation by the elutriator and sugar floatation was effective for isolating A. spretulus eggs from soil. In a control run of this process with known numbers of corn rootworm eggs, approximately 70% were recovered. We tested the soil fiom experiment 6 where the ovipositional activity was the highest, to determine how many eggs were deposited in the surrounding soil instead of in turf cores. Only 8 eggs and 2

first instars were separated from a total of 20 100-ml soil samples.

Discussion

Soil moisture is an important factor for some soil-ovipositing insects like the bean leaf beetle (Cerotoma trifilrcata (Forster)) (Marrone and Stinner 1983), and the southern corn rootworm (Diabrotica undecimpunctata howardi Barber) (Brust and House

1990). In loamy sand soil, moist soil (from -0.1 to -1.0 MPa) is preferred for oviposition by the southern corn rootworm and been leaf beetle and their ovipositional activity is kept maintaining up to saturated soil moisture. However, the least oviposition by both beetles occurs in the oven dry soil.

In our research, soil moisture was important for A. spretulus colonization of turf regardless of whether turfgrass was cut at fairway height or rough height. Adults preferred to inhabit turf cores placed in soil containing 3 13% water by volume to soil containing less than 9% water. They, however, did not discriminate among the three levels of soil moisture from 13% to 26%. We expect that the behavior of A. spretulus

48 adults will be affected on golf courses in areas where the irrigation system does not reach.

This agrees with the observation of Smitley et al. (1998) where A. spretulus adults were

scarce in the dry rough where irrigation coverage did not extend.

Only A. spretulus adults collected in June and early July oviposited in our growth chamber experiments. In these 3 experiments, eggs and grubs were found in all four soil moisture levels. More eggs and grubs were found in rough turf than in fairway turf cores. However, not enough data were available to determine the ovipositional preference of A. spretulus adults because 82% of all eggs and first instars came from a single experiment (experiment 6).

Thatch in perennial ryegrass turf taken fi'om the rough area of the Hancock

Turfgrass Research Center is 2-fold thicker than in the fairway turf cores. The soil moisture effect on A. spretulus adults may be confounded with mowing height and thatch in our turf arena experiment because organic matter has a greater water holding capacity than any other soil texture. The high water holding capacity of thatch may attract adults and perhaps induce their oviposition in our turf arena.

A. spretulus grub infestation is more common in fairways than roughs of golf courses (V ittum 1995, Smitley et al. 1998). Golf course roughs with high mowing height tend to accumulate more thatch than fairways (Beard et al. 1978, Sheannan 1980,

Dunn et al. 1981). The spatial distribution of A. spretulus grubs in golf courses does not

agree with our observations that A. spretulus adults homogeneously colonized fairway

and rough cores at the same moisture levels in our growth chamber experiments and

infestation of grubs was similar in the fairway and rough turf in greenhouse experiments.

However, under the field conditions, roughs are likely to be drier than fairways because

irrigation is targeted to fairways with some overlap into roughs. Even if the same

49 amount of water is applied, roughs tend to consume more soil water and become drier

than fairways (Madison and Hagan 1962, Shearman 1984, Morhard and Schulz 1998).

Therefore, A. spretulus females may be attractive to golf course fairways for their

oviposition.

We did not test the survival of A. spretulus eggs and grubs in the fairway and

rough. However, it is known that the eggs and larvae of some scarab beetles do not

survive well under dry soil conditions (Potter 1983). While golf course fairways are not

expected to become dry enough to affect the survival of A. spretulus, this may be a factor

in roughs where irrigation does not reach. The development of Japanese beetle (Popillia japom'ca Newman) and masked chafer (Cyclocephala sp.) was delayed and their body

weight decreased in tall turf compared with short turf (Potter et al. 1996). Higher

activity of natural predators in the rough compared with the fairway may increase the

mortality of eggs and grubs in the rough (Smitley et al. 1998, Rothwell and Smitley

1999). Also A. spretulus grubs tend to be more highly infected by Bacillus sp. in roughs

than fairways (Rothwell and Smitley 1999). Eventually, the survival of A. spretulus

eggs and grubs in golf course roughs may be lower than in the fairway.

Oviposition of A. spretulus adults collected between August 1999 and July 2000,

adds some key information about their life cycle in MI. Newly emerged adults in

August and September did not oviposit. Overwintered adults also did not show

ovipositional activity until early June, even though beetles become active on golf courses

as early as 1 May. All of the eggs were deposited between 31 May and 10 July. The

survival of adults plummeted from 90% in June to 6% in mid July, indicating that few

individuals from the overwintered generation survive after mid July. This high

mortality in mid July is coincident with reduced flight activity of A. spretulus adults at

50 this time (Johanningsmeier 1999). Their flight activity decreased to almost no detectable level from 26 June to 31 July in 1992 and from 28 June to 9 August in 1993.

Flight resumed after mid August, presumably by the new generation. This field data about the flight of A. spretulus adults and our laboratory data about their oviposition and mortality support observations that A. spretulus is univoltine in MI.

A partial second generation was speculated in MI because of field observations of A. spretulus grubs, pupae and callow adults in mid September (V ittum 1995, Smitley et al. 1998). However, in our study, newly emerged adults in late summer did not oviposit but the ovipositional activity of overwintered adults extended to mid July. Second instars of A. spretulus were observed in MI from 6 to 26 July 1993 (Johanningsmeier

1999). The oviposition in mid July by the overwintered generation may cause the delayed occurrence of A. spretulus grubs in early September. To determine the importance of a partial second generation in M1 will require monitoring A. spretulus grubs for several years.

51 Reference Cited

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Econ. Entomol. 85: 2194-2200.

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Brady, N. C., and R. R. Wei]. 1999. The nature and properties of soils. Prentice Hall,

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Brust, G. E., and G. J. House. 1990. Influence of soil texture, soil moisture, organic cover, and weeds on oviposition preference of southern corn rootworm (Coleoptera:

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Byrd, D. W., Jr., K. R. Barker, H. Ferris, C. J. Nusbaum, W. E. Griffin, R. H. Small, and C. A. Stone. 1976. Two semi-automatic elutriators for extracting nematodes and certain fungi from soil. J. Nematol. 8: 206-212.

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52 Gyrisco, G. G., W. H. Whitcomb, R. H. Burrage, C. Logothetis, and H. H. Schwardt.

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Madison, J. H., and R. M. Hagan. 1962. Extraction of soil moisture by Merion bluegrass (Poa pratensis L. 'Merion') turf, as affected by irrigation frequency, mowing height, and other cultural operations. Agron. J. 54: 157-160.

Marrone, P. G., and R. E. Stinner. 1983. Effects of soil moisture and texture on oviposition preference of the bean leaf beetle, Cerotoma trifllrcata (Forster) (Coleoptera:

Coccinellldae). Environ. Entomol. 12: 426-427.

Morhard, J., and H. Schulz. 1998. EinfluB von Artenzusammensetzung, Schnitthiihe und Bewéisserungsart auf den Wasserverbrauch von Intensivrasen. Rasen. Turf. Gazon.

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affect root-feeding white grubs (Coleoptera: Scarabaeidae) in turfgrass. J. Econ. Entomol.

89: 156-164.

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spretulus, Aphodius granarius (Coleoptera: Scarabaeidae), and predaceous insects across

golf course fairways and roughs. Environ. Entomol. 27: 1336-1349.

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arthropods and predation on Japanese beetle (Coleoptera: Scarabaeidae) eggs and fall

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55 Figure Captions

Fig.1. Module consisting of two fairway pots and two rough pots in our greenhouse experiment.

Fig.2. Turf arenas consisting of fairway turf cores and rough turf cores placed into soils having different moisture levels: one moisture level (A), two moisture levels (B) and four moisture levels (C).

56 Table 1. Percentage of A. spretulus adult beetles recovered from the total number of released beetles.

‘ — EXllverIrllentfiI MOW'”9 Soil moisture (% by volume)

series height 8-9 13-14 17-20 23-26

1 Fairway -— — 26.7 1 5.1 —

Rough — — 30.7 1 2.8 _-

2_3 Fairway 14.9 1 2.2a — — 21.3 1 2.7b

Rough 9.7 1 2.1a — — 27.2 1 3.6b

4_7 Fainlvay 2.1 1 0.8a 5.3 1 1.2b 4.6 1 0.8b 4.3 1 1.0b Rough 3.3 1 0.6a 4.3 3; 0% 4.6 11.0b 6.1 11.1b Means 1 SE within a row followed by the same letter are not significantly different (P = 0.05; LSMEANS statement in SAS MIXED).

57 Table 2. Factorial ANOVA for testing the effects of time, block, soil moisture, and mowing height on the colonization of A. spretulus adults.

Exp Source of variation F df P

1 Block 0.39 9, 9 0.91 Mowing height 0.46 1, 9 0.51 2-3 Time 0.37 1, 18 0.55 Block 0.61 9, 18 0.77 Moisture 18.36 1, 18 0.0004” Mowing height 0.10 1, 18 0.75 Time (Block)a 0.10 9, 18 0.10 Time X Moisture 0.31 1, 18 0.02* Time X Mowing height 0.39 1, 18 0.02* Moisture X Mowing height 3.34 1, 18 0009" Time X Moisture X Mowing height 10.33 1, 18 0.005“ 4-7 Time 0.69 3, 16 003* Block 2.01 4, 16 0.14 Moisture 4.33 3, 48 0.009**

Mowing height 2.18 1, 16 0.16 Time (Block) 1.87 12, 16 0.12 Time X Moisture 1.35 9, 48 0.24 Time X Mowing height 5.32 3, 16 0.01** Moisture X Mowing height 1.18 3, 48 0.33 Time X Moisture X Mowing I'Eght 2.00 9, 48 0.06

P-values followed by one or two asterisks are significant at the 5% or

1% confidence level, respectively.

aBlock effect was nested with time effect.

58 1.0 00 7 0 +

70 5.7 35.0

July with 1.5 Exp 17 00 1.8 6 + 11.9

58 89.7

29.0 introduced June 7.2 4.6 Exp

22 arenas 00 0.6 5 0 1

92 91.3

46.0 turf

June 1.2 Exp

6

from beetles.

00 . 4 0 0

56 94.5 28.0

May

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MI adults Exp

27

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99 total

3 Lanisng, 0

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103 95.2 68.8

Sep

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99

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116 93.6 77.3

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0 0 A.

86

spretulus

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Table

t*I'otal °Percentage

“Percentage spretulus Eggs“ First

Life Adults

Adutsb

Adults A.

59 |4— 15cm —->|

Fainlvay Inner rim

Fairway . Outer rlm

60 O Fairway :2 cm

— 6 Rough a [:1 17% soil moisture a

23% soil moisture I: 9% soil moisture

_26% soil moisture : o ‘__ moisture a - 20% soil » . ' '1» ' [:113% soil moisture o (I a [:3 8% soil moisture

61 Appendix 1

Record of Deposition of Voucher Specimens"

The specimens listed on the following sheet(s) have been deposited in the named museum(s) as samples of those species or other taxa, which were used in this research. Voucher recognition labels bearing the Voucher No. have been attached or included in fluid-preserved specimens.

Voucher No.: 2000-07

Title of thesis or dissertation (or other research projects): PREDATION, SOIL MOISTURE AND MOWING HEIGHT AS POTENTIAL FACTORS IN THE SKEWED DISTRIBUTION OF ATAENI US SPERET UL US (COLEOPTERA: SCARABAEIDAE) ON GOLF COURSE FAIRWAYS AND ROUGHS

Museum(s) where deposited and abbreviations for table on following sheets:

Entomology Museum, Michigan State University (MSU)

Other Museums:

Investigator’s Name(s) (typed) Young-Ki Jo

Date 12/15/00

*Reference: Yoshirnoto, C. M. 1978. Voucher Specimens for Entomology in North America. Bull. Entomol. Soc. Amer. 24: 141-42.

Deposit as follows: Original: Include as Appendix 1 in ribbon copy of thesis or dissertation.

Copies: Include as Appendix 1 in copies of thesis or dissertation. Museum(s) files. Research project files.

This form is available fiom and the Voucher No. is assigned by the Curator, Michigan State University Entomology Museum.

62 Appendix 1.1

Voucher Specimen Data

Page 1 of LPages

Museum where deposited (D U

MSU MSU MSU MSU E MSU MSU MSU

Other

l0 of. Adults 6‘

Adults 9

31//5’/Wc>0

for

/ Number Pupae

Nymphs

University Larvae

specimens

Date Eggs State

listed

,.

/ Michigan

above

or

2000-07

Muse

MI

y the

the

No

Center

Center

Center

Center

Center

Center

Center

in

,

collected

Lansing,

2000

2000

2000

2000

2000

2000 2000

Received

deposit

Voucher

Research

Research

Research

Research

Research

Research

Research

June

June

June

June

June

June

June

Course,

MI,

MI,

MI,

MI,

MI,

specimens

MI,

MI,

Golf

for

deposited

Turfgrass

Turfgrass

Turfgrass

Turfgrass

Turfgrass

Turfgrass

Turfgrass

Scot

2000

data

and

Lansing,

Lansing,

Lansing,

Lansing,

Lansing,

Lansing,

Lansing,

June

Hancock

East

East

Hancock

East

Hancock

East

Hancock

East

Hancock

East

Hancock

East

Hancock

Royal

Label used

5/00

(typed)

12/1

(Say)

necessary)

(Gravenhorst)

(Say)

abricius)

if

(Say)

(F

Stephens

(Haldeman)

Name(s)

(Schrank)

taxon

sheets

Jo

comma

ochropezus

other

carbonan’us

cognatus

sphaen'collis

aflinus

spretulus

or

impuncticollis

additional

Investigators Date Younfli

Stenolophus

Stenolophus

Philonthus Philonthus (Use Harpalus

Species

Apocellus Amara Ataenius

63

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