POPULATION DYNAMICS OF Aphis gossypii IN COTTON:

LABORATORY STUDIES AND FIELD VALIDATION

by

ANAND P. SAPKOTA, B.E.

A THESIS

IN

ENTOMOLOGY

Submitted to the Graduate Faculty

of Texas Tech University in Partial Fulfillment of the Requirements for

the Degree of

MASTER OF SCIENCE

Approved

Chairperson of the Corrtmittee

Accepted

Dean of the Graduate School

December, 2004

ACKNOWLEDGEMENTS

I am extremely grateful to my major professor and chairperson of my committee.

Dr. Megha N. Parajulee. for his guidance throughout my graduate studies. His untiring

help, encouragement and high standards allowed me to complete my research and report

the results in this thesis in a manner in which 1 can take pride. 1 am extremely grateful to

him for providing me the opportunity to pursue my M.S. degree.

I thank Dr. Dana O. Porter and Dr. Chad S. Davis for serving on my thesis

committee and for their valuable guidance in the preparation of this thesis. This thesis

would not have been completed without the enormous help from Mark D. Amold. He

helped "franslate" my language to what is in this thesis. I owe you a lot, Mark!

I express my sincere appreciation to Stanley C. Carroll for his help with anything

I ever needed in my research and to my colleagues R. B. Shrestha, Andy Cranmer, and

Latha Bommireddy for their help and friendship. I am indebted to R. B. Shrestha for data

analyses. I am grateful to Lanthia Jones and Will Keeling for their assistance in

constmcting the aphid cages and for counting aphid nymphs for me when my busy

schedule did not allow me to do it myself. I also express sincere thanks to Ajaya Khadka

for his help in typing some of the data tables.

My heartfelt thanks go to my loving wife, Tara Sapkota, for her patience and

affection, and for taking care of our yovmg children, Ashis and Asmita, back home in

Nepal during my graduate studies in the United States. I am ever gratefiil to my parents,

mother in-law, my family members, and relatives who encouraged me to study abroad,

and supported my family back home during my absence.

11

TABLE OF CONTENTS

ACKNOWLEDGEMENTS ii

LIST OF TABLES v

LIST OF FIGURES yi

CHAPTER

I. INTRODUCTION AND LITERATURE REVIEW 1

1.1 Description 4

1.2 Life Cycle 5

1.3 Damage to Cotton 6

1.4 Pest Activity 8

1.5 Objectives and Rationale 9

1.6 Literature Cited 11

II. EFFECT OF CONSTANT TEMPERATURES ON DEVELOPMENT AND REPRODUCTION OF THE COTTON APHID IN THE LABORATORY 15

2.1 Introduction 15

2.2 Materials and Methods 17

2.3 Data Analysis 19

2.4 Results and Discussion 20

2.5 Literature Cited 32

ill

III. DEVELOPMENT AND REPRODUCTION OF COTTON

APHIDS IN THE FIELD 34

3.1 Introduction 34

3.2 Materials and Methods 36

3.3 Data Analysis 37

3.4 Results and Discussion 38

3.5 Literature Cited 44

VITA 46

IV

LIST OF TABLES

2.1. Calendar of cotton planting, fertilization and transferal of potted cotton plants to growth chambers for the cotton aphid life history study, 2003 26

2.2. Instar-specific and total nymphal development duration (±SEM) of .4. gossypii at six constant temperatures in the laboratory, 2003 27

2.3. Life history parameters (±SEM) of A. gossypii at six constant temperatures in the laboratory, 2003 28

2.4. Life history characteristics (±SEM) of A. gossypii at six constant temperatures in the laboratory, Lubbock, Texas, 2003 29

LIST OF FIGURES

2.1. Daily survivorship and fecundity schedules of cotton aphids held at six constant temperatures in the laboratory 30

2.2. Daily survivorship and fecundity schedules of cotton aphids held at six constant temperatures in the laboratory, comparing all temperature-dependant responses in a single overlaid graph for each life history parameter 31

3.1. Daily average survivorship of cotton aphids in the field, Lubbock, Texas, 2003 41

3.2. Daily average fecundity of cotton aphids in the field, Lubbock, Texas, 2003 41

3.3. Average cumulative (lifetime) fecundity of cotton aphids in the field, Lubbock, Texas, 2003 42

3.4. Daily average temperature under the surface of cotton leaves next to caged cotton aphids used in a life table study, Lubbock, Texas, 2003 43

vi

CHAPTER I

INTRODUCTION AND LITERATURE REVIEW

The worid's human population is increasing at a fast pace. By contrast,

availability of agricultural land is shrinking. The more the human population increases,

the more agricultural products are needed. If we fail to control crop damage by insect

pests, we cannot expect crop production to fulfill the needs of the increasing population.

The United States is the single largest consumer market for cotton in the world, using

more than 20% of cotton produced worldwide (Worsham 2002). The United States is the

second largest cotton producer in the world, producing 17.2 million of bales in 2000

(Anonymous 2004). In total, there are seventeen U.S. states that grow cotton, extending

in a belt along the southem United States, from Virginia to California. Texas is a major

cotton producing state, producing an average of 4.5 million bales of cotton annually. The

Texas High Plains is the most intensive cotton-growing region in the world, producing an

average of 2.7 million bales (59% of Texas) of cotton annually.

In 2003, 2.4 million acres of cotton were planted in the Texas High Plains

(Williams 2004). Blackshear and Johnson (2001) reported that total cotton acreage in the

Texas High Plains region has varied little from 1995 to 1999, fluctiiating between 3.4 and

3.8 million acres. Blackshear and Johnson (2001) further stated that due to varying

weather conditions and biotic factors, total cotton production was more variable, ranging

from 2.6 to 3.4 milhon bales per year from 1995 to 1999. A 20-year average (1984-2003)

cotton production statistic indicates that approximately 25.6 % of United States cotton is

produced in Texas, whereas 59% of Texas cotton is produced in the High Plains region

(Plains Cotton Growers, Inc., personal communication). Five-year average (1996-2001)

statistics indicate that 7 to 9% of yield was lost annually to cotton arthropod pests across

die United States, while average annual yield losses in Texas ranged from 8 to 16%.

During the same period, the Texas High Plains lost 6-9% of the annual yield to arthropod

pests. In 2002, Texas losses equaled 2.1% of potential bales in the United States, third

highest among the cotton growing states (Williams 2003). There are many factors that

reduce cotton yield. Among the most significant factors are pest insects of which the

cotton aphid is one of the most significant in Texas High Plains cotton.

The cotton aphid. Aphis gossypii Glover (Homoptera: Aphididae) is the most

common agricultural insect pest in the Texas High Plains and reduces yield and quality of

cotton. Based on economic impact, the cotton aphid was the sixth and seventh ranked

pest of cotton in the United States in 2002 and 2003, respectively (Williams 2003, 2004).

Cotton aphids are small, slow moving insects that usually feed on the undersurface of the

cotton leaf. The aphid has piercing-sucking mouthparts that are used to suck sap from the

plant. Cotton aphids are not only responsible for reducing cotton yields and quality

through feeding damage, but also excrete waste in the form of a sticky substance called

honeydew. Molds develop on honeydew, and as a result, plant leaves may become

twisted and wilted. Honeydew can also reduce yield and the quality of cotton fibers.

Honeydew that falls onto exposed lint in open bolls causes serious problems at the textile

mill (Slosser at el. 1989, Leser et al. 1992). During the spinning process sugars in the

honeydew on contaminated lint accumulate on machinery and interfere with the

processing. Sand particles trapped by the honeydew abrade and cause premature wear to

machine parts. Growers may receive reduced prices for their lint if honeydew

contamination is detected. Sticky lint was a severe problem in the Texas High Plains

cotton industry in 1995 (Lloyd 1997). The concem over sticky lint was so strong that it

prompted research to investigate the use of sprinkler irrigation systems to wash aphid

honeydew sugars from lint under emergency conditions (Amold et al. 2002).

Paddock (1919) reported that the cotton aphid was a pest in Texas cotton in 1916.

Outbreaks of the cotton aphid have indicated that it has the potential to be a serious pest

of cotton in any season (Akey and Butler 1989). In the Texas High Plains, widespread

cotton aphid infestations are considered to be an intermittent problem, and in most years

the cotton aphid is a secondary pest (Leser 1994). In some years, widespread aphid

outbreaks have been severe, making the aphid an economically significant pest (Leser et

al. 1992). Leser et al. (1992) stated that the cotton aphid became an increasingly

important pest of cotton in West Texas beginning in the mid-1980s. The cotton aphid

was regarded as the number one cotton pest in 1991 in the Southwestem United States

(Hardee and Herzog 1992, Head 1992). Use of pyrethroid insecticides to control other

cotton pests often resulted in increased aphid infestations, conmionly referred to as

••flare-ups" (Kidd 1995, Kidd and Rummel 1997). Among several factors affecting

cotton aphid severity in cotton, high nitrogen and water availability levels have been

shown to enhance aphid growth and development (Allen et al. 1992, Slosser et al. 2001).

However, it is unlikely that Texas High Plains producers would have the luxury of using

excess nitrogen and water in their cotton production systems due to scarcity of water, low

rainfall, and the high price of nitrogen. Nevertheless, the effect of the combination of

nifrogen application rate and water use should not be ignored in cotton aphid

management. Rummel et al. (1995) and Parajulee et al. (2002) noted that the plant stand

density affects the severity of cotton aphid infestations. These authors further stated that

cotton aphid infestations are more severe in areas of thin stand density and in skip-row

planting pattems.

It is difficult to forecast the potential density of aphid populations in the field due

to the lack of knowledge about aphid population growth parameters. Parajulee et al.

(2003) pointed out that currently, there are no accurate methods of predicting the density

to which a cotton aphid population will develop in a cotton field. The objective of the

present study was to describe the life history parameters of cotton aphids in the laboratory

as well as in the field, and examine the relationship between field and laboratory

generated life history parameters and population dynamics.

1.1 Description

Cotton aphids are small, soft-bodied and slow moving yellowish or dark green

insects. The adult cotton aphid varies in color from light to dark green and has dark

siphunculi (Slosser et al. 1989). At high temperattires and in crowded environments,

adult aphids are pale yellow in color (Blackman and Eastop 1985). The length of an

aduh cotton aphid is approximately two millimeters, and the insects are pear shaped.

There are both winged and wingless asexual adult aphids that can be seen in the Texas

High Plains cotton field. Alate cotton aphids have well-developed and larger compound

eyes as compared to the apterae (Miyazaki 1987). Ebert and Cartwright (1997) stated

that first-instar cotton aphids have four segments in the antenna, whereas second-instar

nymphs have five segments. Ebert and Cartwright (1997) further stated that there is not

much visible difference between second and third instars with the exception that the

second instars have developing wings and third instars have small wing pads. Fourth

instars have developing wings that are distinctly visible. Third instars have no setae, and

fourth instars have setae on the margin of the genital plate (Ebert and Cartwright 1997).

1.2 Life Cycle

The cotton aphid life cycle in the Texas High Plains is complex, and there has

been difficulty in completely describing it (Kring 1972, Parajulee et al. 2003). Many

species of aphid females reproduce asexually in a process called parthenogenetic

reproduction. In parthenogenetic reproduction, adult females give birth to live nymphs.

Parthenogenetic reproduction does not involve gene recombination like sexual

reproduction, so offspring are clones of the mother. Slosser et al. (1989) reported that

most of the cotton aphids seen in the United States cotton belt are females, and males are

seldom seen. Some aphids reproduce sexually and exhibit a holocyclic stage. In most

cases A. gossypii reproduces asexually with either alate or apterous females (Ebert and

Cartwright 1997). However, altemation of sexual and parthenogenetic reproduction

(cyclic parthenogenesis) commonly occurs in aphids (Dixon 1987).

Kidd (1995) stated that the role of reproductive male cotton aphids might be to

mate with oviparous females to produce eggs that are able to overwinter. It is believed

that male cotton aphids are produced late in the season for this very reason-sexual

reproduction with oviparious female and production of eggs that can survive the winter

(Parajulee et al. 2003). In the cotton belt region in spring, female cotton aphids give birth

to live nymphs, and generally all progeny develop into wingless females. Parajulee et al.

(2003) noted that the peak aphid population in the Texas High Plains occurs during mid-

August. Parajulee et al. (2003) further noted that a holocyclic life cycle of cotton aphids

likely exists in the Texas High Plains, although no ovipare were found in their study.

1.3 Damage to Cotton

Cotton aphids are a serious pest of cotton throughout the world. Rummel et al.

(1995) stated that prior to 1975, infestations of the cotton aphid were not serious in Texas

High Plains cotton. Rummel et al. (1995) further stated that the first major cotton aphid

outbreak in the Texas High Plains occurred during July and August of 1975. The cotton

aphid outbreak of 1975 was intense, widespread, and uniform (Rummel 1975). In the

cotton season of 1989, it was difficult to control cotton aphids in West Texas due to

resistance to previously effective insecticides (Allen et al. 1990). In a study to confirm

the effects of pyrethroid insecticides on cotton aphid infestation development,

applications of cyhalothrin were made to cotton aphid infested plots (Kidd et al. 1996).

In pyrethroid treated plots, aphid populations rapidly increased, and significant yield loss

was observed (Kidd et al. 1996). In another study, cyhalothrin stimulated and increased

the cotton aphid population (Slosser et al. 2001). Rummel et al. (1995) noted that the

insecticide resistance of cotton aphids was confirmed in 1991.

Cotton aphids usually feed on the undersides of leaves by sucking liquid from

phloem tissue, but they also infest cotton terminals, usually during the early colonization

stage or late in the season when leaves are less favorable feeding sites. The aphid draws

sap from the phloem tissue by using its piercing-sucking mouthparts. Direct feeding of

cotton aphids causes a general reduction in plant vigor that can reduce lint yield.

Similarly, honeydew excreted by cotton aphids may serve as a medium for fungi,

the most common of which is known as black sooty mold. This fiingus may cover

substantial portions of leaves and inhibit photosynthesis, reducing plant vigor and

inhibiting proper plant growth. The amount of honeydew produced by aphids in the 1̂ '

instar is significantly higher than that of other instars (Henneberry et al. 2000). Slosser

and Parajulee (2002) documented a threshold of 11 aphids per leaf that will cause sticky

lint when bolls are open. This threshold is similar to the threshold of 10 aphids per leaf

suggested for California by Rosenheim et al. (1995).

Cotton aphids feed on undersurface of leaves, which can cause crinkling and

cupping of leaves, reducing growth and resulting in stunted seedlings. Slosser et al.

(1989) reported that distortion of cotton leaves and stunted growth of small plants is clear

evidence of the plant injury due to cotton aphid. Honeydew lowers the quality and grade

of the lint. As a result, growers receive lower prices for lint that has been judged to be

sticky.

1.4 Pest Activity

The cotton aphid was known as a serious pest of cotton in 1854 in South Carolina

(Slosser et al.l989). Prior to 1975, cotton aphid infestations were not serious, and the

aphid was not regarded as a pest in the Texas High Plains (Rummel et al. 1995).

Rummel et al. (1995) further stated that after 1975, cotton aphids became an annual pest

in Texas High Plains cotton. The cotton aphid was first reported as a pest of melon in

Texas in 1892, and was recognized as a cotton pest in 1916 (Paddock 1919).

Slosser et al. (1989) stated that after using calcium arsenate to control the boll

weevil, cotton aphids became an increasingly noticeable problem in the southem United

States. In the 1980s, cotton aphids appeared as a significant problem in west Texas

(Leser et al. 1992). The cotton aphid became a major pest of cotton in 1991 in Texas

(Head 1992). The abundance of most aphids is due to their high reproductive rate and

overlapping generations (Dixon 1998). Parthenogenetic reproduction allows the

overlappmg generations and a higher rate of population increase (Dixon 1987). The peak

activity of cotton aphids occurs in mid or late August in the Texas High Plains, and the

duration of this activity is temporally short (Parajulee et al. 2003). Cotton aphid

population increases between mid-August and mid-September can be very rapid,

particularly if synthetic pyrethroid applications are made to control other pests such as

bollworms (Kidd and Rummel 1997, Slosser et al. 2001). The Texas High Plains has

great potential for natural control of cotton pests (including the cotton aphid) by

arthropod predators and parasitoids, which in some cases could be used to reduce

unnecessary usage of insecticides (Amold 1999). Increased nitrogen in leaves, high leaf

moisture and skip-row planting pattems have been shown to increase numbers of cotton

aphids (Slosser et al. 1992, 1997, 1998; Parajulee et al. 2002). Cotton aphid infestations

are becoming problematic in most years. Nevertheless, aphid populations have been

generally maintained at a secondary pest levels by the action of biological control agents

in west Texas cotton (Parajulee et al. 1997, Parajulee and Slosser 1999).

1.5 Objectives and Rationale

The cotton aphid is a common pest of cotton in the Texas High Plains. In some

years, cotton aphid infestations are considered an occasional or secondary problem (Leser

1994), whereas in other years, widespread outbreaks occur and the aphid becomes a

serious, significant pest (Leser et al. 1992). Rummel et al. (1995) reported that in 1991 a

widespread cotton aphid infestation occurred across the Texas High Plains similar to that

of 1975. In the 1989 outbreak, insecticide resistance was observed throughout West

Texas and aphid control became more difficuh, requiring higher rates of previously

effective insecticides (Allen et al. 1990). In 1991, there were more losses in cotton due to

aphid infestations than due to any other pests in the United States (Head 1992). Wang

and Tsai (2000) stated that without a thorough understanding of pest biology and

population dynamics, reliable predictions of impending pest populations and the

development of pest management strategies to counter these infestations are impossible

to achieve. Many studies have examined aphid population growth in relation to

temperattire (Graham 1959, Messenger 1964, Campbell et al. 1974, Komazaki 1982,

Nowierski et al. 1983, Kersting et al. 1999, Xia et al. 1999, Wang and Tsai 2000).

Currently no accurate methods exist to predict the population density, to which

cotton aphids will develop in cotton fields (Kidd and Rummel 1997, Parajulee et al.

2003). The lack of understanding of cotton aphid population grov^h parameters is one

factor that hampers the development of such a method. Hence, it is essential to know the

population growth parameters of cotton aphids in the field, as well as in the laboratory.

There are no studies documenting simultaneous experiments quantifying cotton aphid life

history parameters at constant temperatures, using actual cotton plants in the laboratory

and at fluctuating temperatures in the field. In this study, experiments were conducted in

the summer of 2003 in order to acquire more detailed data on aphid population dynamics.

The objective of this study was to describe the life history parameters of the cotton aphid

in the laboratory and in the field.

10

[ .6 Literature Cited

Akey, D. H., and G. D. Butler. 1989. Developmental rates and fecundity of apterous Aphis gossypii on seedlings of Gossypium hirsutum. Southwest. Entomol. 14: 295-299.

Allen. C. T., W. L. Multer, and V. Lucero. 1990. Seasonal changes in cotton aphid susceptibility to insecticides in west Texas cotton, pp. 287-290. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Allen, C. T., D. E. Stevenson, C. W. Roberts, R. R. Minzenmayer, T. W. Fuchs, A. Z. Mathies. P A. Glogoza, G. W. Jones, and M. G. Hichey. 1992. Development of cotton aphid populations on several different cotton varieties in west Texas, pp. 831-833. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Anonymous. 2004. World of cotton. National Cotton Council of America web page http://www.cotton.org/econ/world/index.cfm July 13, 2004.

Amold, M. D. 1999. Natural mortality of the bollworm in Texas High Plains cotton. M.S. thesis, Texas Tech University, Lubbock, TX.

Amold, M. D., D. R. Rummel, J. P. Bordovsky, J. E. Slosser, and S. C. Carroll. 2002. Use of the center pivot irrigations system for reduction of cotton aphid sugars on cotton lint. Southwest. Entomol. 27: 11-19.

Blackman, R. L., and V. F. Eastop. 1985. Aphids on the Worid's Crops: An identification guide. Wiley and Sons, Inc., New York.

Blackshear, J., and P. Johnson. 2001. Profitability of cotton production in the Texas High Plains, pp. 241-244. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez, and M. Mackauer. 1974. Temperature requirements of some aphids and their parasites. J. Appl. Ecol. 11: 431-438.

Dixon, A. E.G. 1998. Aphid Ecology. Chapman and Hall, Inc., New York.

Dixon, A. F. G. 1987. Evolution and adaptive significance of cyclical parthenogenesis in aphids, pp. 289-297. In A. K. Minks and P. Harrewijn [eds], Worid Crop Pests:

11

Aphids, their bilogy, natural enemies and control, vol. 2A. Elsevier, Amsterdam, The Netherlands.

Ebert, T. A. and B. Cartwright. 1997. Biology and ecology of Aphis gossypii Glover (Homoptera: Aphididae). Southwest. Entomol. 22: 115-153.

Graham, H. M. 1959. Effects of temperature and humidity on the biology of Therioaphis maculata (Buckton). Univ. Calif Publ. Entomol. 16: 47-80.

Hardee, D. D. and G. A. Herzog. 1992. 45"" annual conference reports on cotton insect research and control, pp. 626-644. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Head, R. B. 1992. Cotton insect losses 1991, pp. 621-623. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Henneberry, T. J., L. Forlow Jech, T. de la Torre, and D. L. Hendrix. 2000. Cotton aphid (Homoptera: Aphididae) biology, honeydew production, sugar quality and quantity, and relationships to sticky cotton. Southwest. Entomol. 25: 161-174.

Kidd, P. W. 1995. Impact of insect predators and a pyrethroid insecticide on field populations of the cotton aphid. Aphis gossypii Glover, in Texas High Plains cotton. M. S. thesis, Texas Tech University, Lubbock TX.

Kidd, P. W. and, D. R. Rummel. 1997. Effect of insect predators and a pyrethroid insecticide on cotton aphid. Aphis gossypii Glover, population density. Southwest. Entomol. 22: 381-393.

Kidd, P- W.. D. R. Rummel, and H. G. Thorvilson. 1996. Effect of cyhalothrin on field populations of the cotton aphid, Aphis gossypii Glover, in the Texas High Plains. Southwest. Entomol.21: 293-301.

Komazaki, S. 1982. Effects of constant temperatures on population growth of three aphid species, Toxoptera citricida (Kirkaldy), Aphis citricola Van der Groot and Aphis gossypii Glover (Homoptera: Aphididae) on citms. Appl. Entomol. Zool. 17:75-81.

Kring, J. B. 1972. Flight behavior of aphids. Annu. Rev. Entomol. 17: 461-492.

Kersting, U., S. Satar, and N. Uygun. 1999. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Homoptera. Aphididae) reared on Gossypium hirsutum L. J. Appl. Entomol. 123: 23-27.

12

Leser, J. F., C. T. Allen, and T. W. Fuchs. 1992. Cotton aphid infestation in west Texas: A growing management problem, pp. 823-827. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Leser, J. F. 1994. Management of cotton aphids: Texas style, pp. 137-141. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Lloyd, M. 1997. Sticky cotton gums up mills. Cotton Farming. 41: 14-16.

Miyazaki. M. 1987. Morphology of aphids, pp. 1-25. In A. K. Minks and P. Harrewijn [eds.]. World crop pests: Aphids, their biology, natural enemies, and control. Volume 2A. Elsvier, Amsterdam, The Netherlands.

Messenger, P. S. 1964. The influence of rhythmically fluctuating temperatures on the development and reproduction of the spotted alfalfa aphid, Therioaphis maculata. J. Econ. Entomol. 57: 71-76.

Nowierski, R. M., A. P. Gutierrez, and J. S. Yaninek. 1983. Estimation of thermal thresholds and age-specific life table parameters for the walnut aphid (Homoptera: Aphididae) under field conditions. Environ. Entomol. 12: 680-686.

Parajulee, M. N., P. W. Kidd, D. R. Rummel, and W. P. Morrison. 2003. Aerial movements of the cotton aphid. Aphis gossypii Glover (Homoptera: Aphididae), and discovery of male morphs in the Texas High Plains. Southwest. Entomol. 28: 241-247.

Parajulee, M. N., J. E. Slosser, and D. G. Bordovsky. 2002. Planting pattems affecting the abundance of cotton aphids and banded winged whiteflies in dryland cotton. In Proc. Beltwide Cotton Conf., Nat. Cotton Council of Amer., Memphis, TN.

Parajulee, M. N., and J. E. Slosser. 1999. Evaluation of potential relay strip crops for predator enhancement in Texas cotton. Int. J. of Pest Manage. 45: 275-286.

Parajulee, M. N., R. Montandon, and J. E. Slosser. 1997. Relay intercropping to enhance abundance of insect predators of cotton aphid (Aphis gossypii Glover) in Texas cotton. Int. J. Pest Manage. 43: 227-232.

Paddock, F. B. 1919. The cotton or melon louse. Tex. Agric. Exp. Stn. Bull. 257.

Rosenheim, J. A., K. J. Fuson, and L. D. Godfrey. 1995. Cotton aphid biology, pesticide resistance, and management in the San Joaquin Valley, pp. 97-101. In D. J. Herber and D. A. Richter [eds.], Proc. Beltwide Cotton Res. Conf., Nat. Cotton Council of Amer. Memphis, TN.

Rummel, D. R. 1975. Focus on entomology. Tex. Agric. Ext. Ser. Newsletter. 14: 7.

13

Rummel, D. R., M. D. Amold, J. E. Slosser, K. C. Neece, and W. E. Pinchak. 1995. Cultural factors influencing the abundance of Aphis gossypii Glover in Texas High Plains cotton. Southwest. Entomol. 20: 396-406.

Slosser, J. E., W. E. Pinchak, and D. R. Rummel. 1989. A review of known and potential factors affecting the population dynamics of the cotton aphid. Southwest. Entomol. 14: 302-313.

Slosser, J. E., W. E. Pinchak, and W. A. Frank. 1992. Effect of planting date on cotton aphid and banded winged whitefly populations in dryland cotton. Southwest Entomol. 17: 89-100.

Slosser, J. E., G. B. Idol, D. R. Rummel, and W. E. Pinchak. 1997. Influence of plant maturity and application timing of dicrotophos for control of cotton aphid. Soutiiwest. Entomol. 22: 207-215.

Slosser, J. E., W. E. Pinchak, and D. R. Rummel. 1998. Biotic and abiotic regulation of Aphis gossypii Glover in west Texas dryland cotton. Southwest. Entomol. 23: 31-65.

Slosser, J. E., M. N. Parajulee, G. B. Idol, and D. R. Rummel. 2001. Cotton aphid response to irrigation and crop chemicals. Southwest. Entomol. 26: 1-13.

Slosser, J. E., and M. N. Parajulee. 2002. Relationship between numbers of cotton aphids per leaf and sticky lint. In Proc. Beltwide Cotton Conf., Nat. Cotton Council of Amer., Memphis, TN.

Williams, M. R. 2003. Cotton insect losses 2002. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Williams, M. R. 2004. Cotton insect losses 2003. /« Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Wang, J. J., and J. H. Tsai. 2000. Effect of temperature on biology of Aphis spiraecola. Ann. Entomol. Soc. Amer. 93: 874-883.

Worsham, J. B. 2002. Cotton incorporated activity report 2001. In Proc. Beltwide Cotton Conf., Nat. Cotton Council of Amer., Memphis, TN.

Xia, J. Y., W. Van der Werf, and R. Rabbinge. 1999. Influence of temperattire on bionomics of cotton aphid. Aphis gossypii, on cotton. Entomol. Exp. Appl. 90: 25-35.

14

CHAPTER II

EFFECT OF CONSTANT TEMPERATURES ON

DEVELOPMENT AND REPRODUCTION

OF THE COTTON APHID IN

THE LABORATORY

2.1 Introduction

The cotton aphid is a polyphagous pest infesting various crops throughout the

world. The development, survivorship, and reproduction of the cotton aphid are strongly

influenced by temperature and quality of food. The speed of physiological development

and rate of reproduction of the aphid increase as the temperature increases to an upper

limit. At extreme low and high temperatures, developmental rate and reproduction rate

of the cotton aphid are reduced. Kersting et al. (1999) reported that the developmental

rate for different stages of A. gossypii increased linearly as temperature increased within

the range of 15 to 30 *̂ C. Both food quality and temperature play a distinct role in cotton

aphid population increase. Developmental rates and fecundity of apterous A. gossypii on

cotton seedlings at different temperatures and a photoperiod of 18:6 (L: D) were studied

by Akey and Butler (1989). Many studies have been conducted examining the

relationship between different constant temperatures and aphid development including

the effects of temperature and humidity on the biology of Therioaphis maculata

(Buckton) (Graham 1959); the influence of rhythmically fluctuating temperatures on the

development and reproduction of the spotted alfalfa aphid (Messenger 1964); temperature

15

requirements of some aphids and their parasites (Campbell et al. 1974); estimation of

thermal thresholds and age-specific life table parameters for the walnut aphid under field

conditions (Nowierski 1983); and influence of temperature and daylength on population

development of ^. gossypii (Aldyhim and Khalil 1993). The effect of temperature on

population growth of the cotton aphid on Gossypium hirsutum L. was studied by Kersting

et al. (1999) in Turkey and Xia et al. (1999) in China. Xia et al. (1999) stated that

environmental conditions, especially temperature, affect the population growth of the

aphid. Wang and Tsai (2000) studied the effect of temperature on the biology of A.

spiraecola in Florida. Similar studies on other aphids include: Ma et al. (2004) (rose

grain aphid), Weathersbee et al. (2004) (brovm citms aphid), and Morgan et al. (2001)

(pea aphid).

Developmental time of aphids decreases as temperature increases up to an upper

limit. Above this limit, development and fecundity slow down. Insects are poikilotherms

and cannot regulate their body temperature. The development and reproduction of aphids

depend on the temperature of the surrounding environment. Wang and Tsai (2000) stated

that pest population prediction systems and management strategies depend on a broad

understanding of the pest's biology and population dynamics. The objective of this study

was to generate comprehensive life history parameters across a temperature range (10-35

° C) in a standard rearing environment in the laboratory.

16

2.2 Materials and Methods

Cotton plants used in laboratory studies were grown to the eight tme-leaf stage in

a greenhouse at the Texas Agricultural Experiment Station (TAES) in Lubbock, TX.

During the periods the plants were in the greenhouse, the temperature was maintained at

26.7 '̂ C. Evaporative cooling, gas heating, and an automated shade cloth system

maintained a relatively constant temperature during the periods of germination and

growth.

Seeds of the commercial cotton cultivar Paymaster 2326 RR (PM 2326 RR) were

planted at weekly intervals for eight weeks. Three seeds were planted in each of 125

plastic pots (10.16 cm X 10.16 cm x 10.16 cm) beginning 28 May 2003. The growing

medium was a standard potting soil (SB 300 Professional Growing Mix, Simgrow

Company, Bellevue, WA). After germination, seedlings were thinned to one dominant

seedling per pot. All pots were manually watered daily. Miracle-Grow (Scott's

Miracle-Grow Products, OH) fertilizer was applied once weekly for three consecutive

weeks. A solution of one tablespoon of Miracle-Grow to one gallon of water was used.

Table 2.1 presents the timeline of cotton planting, fertilizer applications, and plant

fransfer to growth chambers for the life history study.

At the 8 tme-leaf stage, plants were brought to the laboratory. Twelve plants

were placed into each of six growth chambers (Model 818, Precision, Winchester, VA)

that were set to maintain six constant temperatures: 10, 15, 20, 25, 30 and 35 C. The

photoperiods in all growth chambers were held constant at 14:10 (L: D) h. The growth

chambers had a capacity of 0.5 m^ (interior dimensions 51 cm x 69 cm x 145 cm), and a

17

temperature control range of+/- 0.1 "C. One day prior to transferring the cotton plants to

the growth chamber, adult cotton aphids were placed on the undersurface of detached

fourth and fifth true cotton leaves and placed in petri dishes (15 cm diameter x 2.5 cm

depth) to harvest newly emerged nymphs for the study. Moist filter papers were provided

in each petri dish to prevent the leaves from drying.

Twelve cotton plants were transferred to each of the six growth chambers.

Newly emerged aphid nymphs (<24 h old) were transferred individually to the underside

of the 4"̂ and 5"̂ mainstem leaves (from the top of the plant) of each cotton plant in the

growth chamber using a camel's hair bmsh, with a total of 24 aphids per temperature

freatment. Aphid fransfer was done with great care to minimize the potential injury to the

young aphids. Individual aphids were confined to a section of leaf using clear plastic,

hinged boxes as cages (catalog # 203, Alpha Rho Inc., Fitchburg, MA) immediately after

they were placed on the leaf. Spring-loaded stainless steel hair clips (L «& N Sales and

Marketing, Hatboro, PA) were re-shaped to fit over the clear plastic cages and were used

to hold cages tightly closed and securely attached to leaves. A 1.25 cm diameter hole

was drilled in the bottom of each plastic cage and perforated muslin cloth was hot-glued

over the hole to provide ventilation to the cage interior while preventing escape of aphids.

Rearing plants were replaced once a week to standardize the host plant quality across

temperature treatments.

Individual nymphs were observed every 24 h, and nymphal duration and mortality

were recorded until they reached adulthood. Aduh aphids were observed daily and newly

18

bom offspring were counted and removed until the last individual from each treatment

died.

2.3 Data Analysis

The following life history parameters of cotton aphids held at constant

temperatures of 10, 15, 20, 25, 30 and 35 "C were quantified: instar-specific and total

nymphal durations, age-specific survivorship, age-specific fecundity, gross reproductive

rate, net reproductive rate, finite rate of increase, doubling time, and intrinsic rate of

population increase. The life history parameters were calculated by using the methods

described by Andrewartha and Birch (1954). In this analysis, the first day of the test

aphid's life was set as the first pivotal age with age divided into increments of one day.

The intrinsic rate of increase (r) was determined by iteratively solving the Euler equation

as given below.

le-'^l.m.^i

Where x is the age in days (including immature stages), r is the intrinsic rate of

increase, 4 is the proportion of individuals alive at time x of an original cohort (including

immature mortality). The variable m^ is the mean number of offspring produced per

surviving aphid during the age interval x (1 day). The life table parameters, gross

reproduction rate (GRR=Im^), net reproductive rate (Ro= Il^m^c), finite rate of increase

(k=e'), mean generation time (GT=lnRo/r), and doubling time (DT=ln2/r) were calculated

using the methods described by Andrewarth and Birch (1954).

19

After computing the intrinsic rate of increase (r) for the original data (r^//), the

Jackknife method (Meyer et al. 1986) was used to estimate the standard error of the

calculated life table statistics. Life history parameters were analyzed using a general

linear model with temperature as a source of variation (SAS Institute 2003). Least

squares means were compared using Fisher's Protected LSD (SAS Institute 2003).

Developmental threshold temperatures were calculated using regression analyses of

development rate (1/development duration) on temperature for each instar and for total

nymphal development.

2.4 Results and Discussion

Instar-specific and total nymphal developmental durations for aphids at the six

constant temperatures are presented in Table 2.2. For first, second, third, and fourth

instars, the developmental duration ranged from 5.58 to 1.11, 6.32 to 1.00, 6.47 to 1.13,

and 6.74 to 1.10 days, respectively, for aphids held at 10, 15, 20, 25, 30 and 35 °C. Total

nymphal duration to reach adulthood ranged from 25.11 d (10 ''C) to 4.38 d (30 °C).

With the exception of first instar nymphs, the shortest instar-specific developmental

durations were exhibited by aphids at 25 °C (1.10 d, fourth instar) or 30 °C (1.00 d,

second instar, and 1.13 d, third instar). The shortest total nymphal duration was observed

at 30 °C (4.38 d). A general rise in developmental duration was observed from 30 to 35

°C for total nymphal duration, and for all immature stages except first instar, where the

difference was numerically very small (0.02). None of the differences in developmental

durations between 30 and 35 °C were statistically significant.

20

As with previous studies, general aphid developmental time shortened with rising

temperature, to an upper limit after which the developmental duration increased. Results

of this study indicated that the developmental duration for all immature stages is shortest

at 25 or 30 °C, and total nymphal duration is shortest at 30 °C. These results are in

agreement with those of Xia et al. (1999) and Kersting et al. (1999). At 35 °C, a

numerical rise in developmental duration was observed for all immature stages (except

first instar) as compared to 30 °C. These differences were not statistically significant, but

the fact that they were observed for second, third and fourth instars and for the total

nymphal duration indicates that the upper temperature limit above which aphid

development will slow may occur between 30 and 35 °C.

Developmental duration of aphids (all instars and in the total) held at 10 °C and

15 °C were significantly different from each other and from that of the aphids held at the

higher temperatures (Table 2.2). With the exception of second instars, at higher

temperatures of 20 to 35 °C, a general pattern was evident that the number of significant

differences between developmental durations of aphids held at the different constant

temperatures became fewer as the aphid moved from one instar to the next. For first

instars, developmental durations at 30 and 35 °C were not significantly different, while

third and fourth instars had no significant differences in developmental durations between

25, 30 and 35, and 20, 25, 30 and 35 °C, respectively.

The clean statistical breaks between developmental durations of all immature

stages of aphids held at 10 and 15 °C (Table 2.2) indicate that at lower temperattires, all

immature aphid stages (f' to 4* instars) are affected similarly by temperattire changes.

21

However, at higher temperatures (20 to 35 °C), a general progressive lack of significant

differences in developmental durations as aphids molted to later instars indicates a

smaller influence of increasing temperature on larger aphid immatures. Developmental

threshold temperatures were calculated to be 6.3, 6.7, 5.9, 5.9, and 6.26 "C for 1'', 2"**, 3"*,

and 4 instars and for total nymphal development, respectively.

Survivorship and fecundity of test aphids held at the six constant temperatures are

presented in Figures 2.1-2.2. In viewing the survivorship curves (4) for aphids held at

the six constant temperatures, a general trend is evident (Figures 2.1-2.2). As

temperature increased, survivorship progressively fell more precipitously, indicating

increasing aphid mortality at a younger age. At 10, 15, 20, 25, 30 and 35 °C, aphid

survivorship dropped below 80% at 39, 29, 33, 21, 20, and 14 days of life, respectively.

At the same temperatures, aphid survivorship dropped below 20% at 52, 51, 47, 44, 38,

and 17 days of life, also respectively. The drop in survivorship was particularly sharp at

35 °C, dropping from 94% on the 12* day of life to 17% on the 17'̂ day of life, a period

of five days. Fecundity curves (Figures 2.1-2.2) also showed an obvious pattern. Number

of days elapsed until first deposition of progeny decreased progressively and sharply at

temperattires 10 (26 d) to 15 (14 d) to 20 °C (8 d), then stabilized at five days for 25, 30

and 35 °C.

Selected life table parameters are presented in Tables 2.3 and 2.4. The average

ages reached by female aphids before production of first progeny decreased sharply as

temperattire increased from 10 (29.69 d) to 15 (16.56 d) to 20 °C (9.00 d), before

stabilizing between six and seven days for temperatures 25, 30, and 35 °C (Table 2.3).

22

The pre-reproductive rate of aphids (time between reaching adulthood and producing

progeny) ranged from 2.84 d at 10 °C to 0.78 d at 35 °C with a low of 0.65 d at 25 °C.

Average longevity of test aphids also declined as temperature increased, with a sharp

decline observed at 35 °C. Average lifetime fecundity of females rose from a low of 7.9

progeny at 10 °C to a peak of 53.1 progeny at 30 °C, and then declined sharply to 13.9

progeny at 35 °C (Table 2.3).

Gross reproductive rate (GRR) an indicator of lifetime fecundity, ranged from 9.8

for aphids held at 10 °C to 58.9 for aphids held at 30 °C (Table 2.4). A general rise in

GRR was observed with rising temperature to 30 °C, but GRR declined sharply from 30

to 35 °C (-41.6) and was significantly lower than the GRRs of aphids held at all other

temperatures except 10 °C (Table 2.4). The same pattem was observed for net

reproductive rate (Ro), which incorporates fecundity and survivorship. Finite rate of

growth (X), which combines fecimdity, survivorship and longevity that indicates whether

a population is increasing or decreasing (<l=decreasing, >l=increasing, l=stable), also

showed a general increase with increasing temperature, but peaked at 25 °C (1.45516).

Interestingly, X was higher at 35 than 30°C, but this difference was numerically very

small and not significant. Doubling time (DT) exhibited much the same pattem as X as

far as advancement of aphid development (unlike X,, a lower DT resuhs in faster aphid

population development), with the best DT of 1.88 at 25 °C. The DTs at the highest

temperattires of 30 (2.26 d) and 35 °C (2.20 d) were relatively low, particularly when

compared to 10 and 15 °C (Table 2.4).

23

Life history parameters calculated for this study that measure the onset and level

of fecundity of cotton aphids rose with rising temperature to an upper limit. At lower

temperatures, the onset of reproduction was delayed and the level of lifetime fecundity

was lower. This upper temperature limit appears to be between 30 and 35 °C. At 35 °C

temperature onset of reproduction was not delayed, but lifetime fecundity was

significantly lower than at the more moderate temperatures. The finite rate of growth (X)

of aphids held at 35 °C was relatively high and the doubling time (DT) was relatively low

when compared to the aphids held at the lower temperatures (Table 2.4). However, this

was offset by the higher mortality (lower survivorship. Figures 2.1-2.2) of aphids held at

the higher temperature.

Results of this study indicate that 25 to 30 °C is the optimum temperature range

for cotton aphid development, reproduction and population increase. At 30 °C the

lifetime fecundity of female aphids was the highest of all temperatures tested. However,

at 30 °C, the survivorship curve (Figures 2.1-2.2) had a steeper decline from the 15 to

the 45* day of life indicating higher mortality in this time period. At 25 °C, the finite

rate of growth (k) was highest and the doubling time (DT) was shortest of all the

temperatures tested (Table 2.4). The lower mortality suffered by aphids at 25 °C

(compared to 30 °C) very likely is the cause of the rise in these parameters. Finite rate of

growth (X) and doubling time (DT) are the more important parameters describing

population increase.

24

As a result, the optimum temperature is probably closer to 25 °C. The results of

this study agree with previous studies that the optimum aphid development temperature

(held constant) in a laboratory study is 25 to 30 °C, and provide affirmation for the

previous research (Akey and Butler 1989, Xia et al. 1999, Kersting et al. 1999).

25

Table 2.1. Calendar of cotton planting, fertilization and transferal of potted cotton plants to growth chambers for the cotton aphid life history study, 2003.

Batch p. . Fertilization Plants transferred to No. *' 1 2 3 growth chambers

1.

2.

->

4.

5.

6.

7.

8.

05-28

06-04

06-11

06-18

06-25

07-02

07-09

07-15

06-04

06-11

06-18

06-25

07-02

07-09

07-15

07-22

06-11

06-18

06-25

07-02

07-09

07-15

07-22

07-29

06-18

06-25

07-02

07-09

07-15

07-22

07-29

08-05

07-10

07-16

07-24

07-31

08-09

08-16

08-24

08-31

For each plant, fertilizer applications were made at weekly intervals; the plants were transferred to the growth chambers at about six weeks (8 tme-leaf stage).

26

Table 2.2. Instar-specific and total nymphal development duration days (±SEM) of ^. gossypii at six constant temperatures in the laboratory, 2003.

Stage 1̂ '̂C iT^'c 20 "C 25 "C 30"''C 35"''C F P~

5.58a 3.56b 2.28c 1.60d 1.13e l . l le instarl (±o.l4) (±0.14) (±0.10) (±0.11) (±0.07) (±0.08)

- „ 6.32a 3.55b 1.50c 1.40c l.OOd 1.21cd instar 11 ^^^ ^^^ ^^^^^^ ^^^^^2) (±0.11) (±0.00) (±0.10) ^'^'^ "'""^

- ^ , „ 6.47a 3.15b 1.61c 1.15d 1.13d 1.18d . , „ „ .^^^, Instar III ^̂ ^̂ ̂ 2) (±0.11) (±0.12) (±0.11) (±0.07) (±0.10) ^^^'^ ^^'^^^

6.74a 3.25b 1.50c 1.10c 1.13c 1.28c ^^ ^ <0.001 Instar IV ^^^^^^ ^^^ 25) (±0.12) (±0.07) (±0.07) (±0.16)

Total 25.11a 13.50b 6.89c 5.25d 4.38d 4.53d ^^. . ^^ Q^, duration (±0.37) (±0.36) (±0.38) (±0.36) (±0.32) (±0.37)

Means within a row, followed by the same letter, are not significantly different (i'<0.05; LSD)

27

Table 2.3. Life history parameters (±SEM) of A. gossypii at six constant temperatures in the laboratory, 2003.

Stage 10°C 15°C 20 °C 25 "C 30 "C 35 °C

Pre-reproductive 2.84a 1.79b 1.11c 0.65c 0.83c 0.78c Period (d) (±0.34) (±0.18) (±0.08) (±0.11) (±0.08) (±0.13) ^^'^ ^^"^^^

Age of aduh at ^^^^^ ^^^^^ ^ first reproduction ^^^33^ ^^^3^^ ^^^3^^ ^^^3^^ ^^^^^^ ^^^ 3^^ 829.9 <0.001

Lifetime fecundity 7.89d 28.50c 43.94b 44.75b 53.08a 13.94d per female (±2.54) (±2.47) (±2.61) (±2.47) (±2.26) (±2.61) 54.79 <0.001

T .. iA^ 43.32a 40.80a 39.39a 29.65b 28.21b 14.22c -^ ,„ ^^„, Longevity (d) ^^^.28) (±2.22) (±2.34) (±2.22) (±2.03) (±2.34) ^2.49 <0.001

Sample size (n) 19 20 18 20 24 18

Means within a row, followed by the same letter, are not significantly different (P<0.05; LSD).

28

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29

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0.8 -

0.6 -

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0.2 -

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A A — 1 — 1 — 1 — 1 — f ^ — 1 — 1 -

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0.8 -

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0.8 -

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4.0

3.5

3.0

2.5

2.0

1.5

1.0

0.5

0.0

0 5 10 15 20 25 30 35 40 45 50 55 60 0 5 10 15 20 25 30 35 40 45 50 55 60

Age of Aphid (days)

Figure 2.1. Daily survivorship (L) and fecundity (mx) schedules of cotton aphids held at six constant temperatures in the laboratory.

30

X l - i o >

3 in "3 3 O o a o

0 5 10 15 20 25 30 35 40 45 50 55 60

Age (days)

ar

Fecu

ndi

Dai

ly

4.5 -

4.0-

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2.5 -

2.0-

1.5 -

1.0-

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/ \ ^*

—ii-i—U-\—1^

Fecundity 10 °C 15 °C 20 °C 25 °C 30 °C 35 °C

A A ^ 10 15 20 25 30 35 40 45 50 55 60

Age (days)

Figure 2 2 Daily survivorship and fecundity schedules of cotton aphids held at six constant temperatures in the laboratory, comparing all temperattire-dependant responses in a single overlaid graph for each life history.

31

2.5 Literature Cited

Akey, D. H., and G. D. Butler Jr. 1989. Developmental rates and fecundity of apterous Aphis gossypii on seedling of Gossypium hirsutum. Southwest. Entomol. 14: 295-229.

Aldyhim, Y. N., and A. F. Khalil. 1993. Influence of temperature and daylength on population development of Aphis gossypii on Cucurbita pepo. Entomol. Exp. Appl. 67: 167-172.

Andrewartiia, H. G. and L. C. Birch. 1954. The distribution and abundance of animals. University of Chicago Press, Chicago, IL.

Campbell, A.. B. D. Frazer, N. Gilbert, A. P. Gutierrez, and M. Mackauer. 1974. Temperature requirements of some aphids and their parasites. J. Appl. Ecol. 11: 431-438.

Graham, H. M. 1959. Effects of temperature and humidity on the biology of Therioaphis maculata (Buckton). Univ. Calif Publ. Entomol. 16: 47-80.

Kersting, U., S. Satar, and N. Uygun. 1999. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Homoptera: Aphididae) reared on Gossypium hirsutum L. J. Appl. Entomol. 123: 23-27.

Ma, C. S., B. Hau, and H. Poehling. 2004. Effects of pattem and timing of high temperature exposure on reproduction of the rose grain aphid, Metopolophium dirhodum. Entomol. Exp. Appl. 110: 1-65.

Messenger, P S. 1964. The influence of rhythmically fluctuating temperatures on the development and reproduction of the spotted alfalfa aphid, Therioaphis maculata. J. Econ. Entomol. 57: 71-76.

Meyer, J. S., C. G. higersoU, L. L. McDonald, and M. S. Boyce. 1986. Estimating uncertainty in population growth rates: Jackknife vs. bootstrap techniques. Ecology 67: 1156-1166.

Morgan, D., K. F. A. Walters, and J. N. Aegerter. 2001. Effects of temperature and cuhivar on pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) life history. Bull. Entomol. Res. 91: 47-52.

Nowierski, R. M., A. P. Gutierrez, and J. S. Yaninek. 1983. Estimation of thermal thresholds and age-specific life table parameters for the walnut aphid (Homoptera: Aphididae) under field conditions. Environ. Entomol. 12: 680-686.

SAS histitute. 2003. SAS/STAT user's guide, SAS Instittite, Cary, NC.

32

Wang, J. J., and J. H. Tsai. 2000. Effect of temperature on biology of Aphis spiraecola. Ann. Entomol. Soc. Amer. 93: 874-883.

Weathersbee, A. A., C. L. Mckenzie, and Y. Q Tang. 2004. Host plant and temperature effects on Lysiphlebus testaceipes (Hymenoptera: Aphididae), a native parasitoid of the exotic brown citrus aphid (Hemiptera: Aphididae). Ann. Entomol. Soc. Amer. 97: 476-480.

Xia, J. Y.. W. Van der Werf, and R. Rabbinge. 1999. Influence of temperature on bionomics of cotton aphid. Aphis gossypii, on cotton. Entomol. Exp. Appl. 90: 25-35.

33

CHAPTER III

DEVELOPMENT AND REPRODUCTION OF

COTTON APHIDS IN THE FIELD

3.1 Introduction

There are 17 cotton-growing states in the United States. In these States, there are

more than 14 million acres of land devoted to cotton production, and an average of 17

million bales of cotton are produced annually (Anonymous 2004). Williams (2004)

reported that in 2003, there were 5.6 million acres of cotton planted in Texas with 2.24

million of the acreage in the Texas High Plains. Arthropods are the most serious group of

pests that reduce cotton yield in the Texas High Plains. In 2003, Texas High Plains

growers lost 43,561 bales of cotton valued at 12.54 million dollars to arthropod pests.

(Williams 2004). Among the arthropod pests of cotton, the cotton aphid was ranked the

seventh most economically important pest in the United States in 2003.

The cotton aphid. Aphis gossypii Glover (Homoptera: Aphididae), is a common

and in some years devastating pest of cotton, Gossypium hirsutum L., in the Texas High

Plains. In the Texas High Plains, the cotton aphid is an occasional or secondary pest of

cotton in most years (Leser et al. 1994), while in other years; aphids can develop

widespread populations and can become a serious and economically significant pest

(Leser et al. 1992). Parajulee et al. (2003) reported that though there has been no

documentation, it is believed that large, widespread cotton aphid outbreaks in the Texas

High Plains take place due to aerial immigration from a more southem location.

34

Many studies have been conducted to examine the effect of environmental,

cultural, and plant condition factors on cotton aphid population development. Cotton

aphid peak populations occurred in August, which was related to high temperature, and

peak aphid numbers were correlated with solar radiation, day length and percentage of

nitrogen in the cotton leaves (Slosser et al. 1998). Slosser et al. (1998) frirther

documented that abiotic and biotic factors and their interactions regulated the average

population density of aphids during August. The application of cyhalothrin caused rapid

increases in cotton aphid population densities resulting in significant loss of cotton yield

(Kidd et al. 1996, Slosser et al. 2001). In a laboratory study conducted in China, Xia et

al. (1999) studied effects of temperature on the development and fecundity of cotton

aphids at different temperatures. A similar study was conducted by Kersting et al.

(1999), which studied the effect of temperature on development rate, and fecundity of

cotton aphids on cotton leaves in Turkey. In Arizona, Akey and Butler (1989) conducted

a study to examine aphid developmental rate and fecundity on cotton plants kept at

constant temperatures in modified growth chambers. During the period of a major cotton

infestation, higher numbers of cotton aphids were found on cotton plants in conventional

cultivation plots than on those mulched with wheat straw (Rummel et al. 1995). Rummel

et al. (1995) further reported that reflectance ratio of the mulched soil surface was higher

than that of bare soil. This sttidy shows the influence of light on aphid population

development in the field. The objective of this study was to conduct a comprehensive

field life table sttidy in a fluctuating temperature regime to validate laboratory life table

data.

35

3.2 Materials and Methods

The study was conducted at the fexas Agricultural Experiment Station farm at

Lubbock, Texas during the summer of 2003. Experimental plots were planted to the

cotton cultivar Paymaster 2326 (PM 2326 RR) on 14 May 2003 at 40" row spacing.

Land and crop management followed standard procedures recommended for fiirrow-

irrigated cotton in the Texas High Plains. Cotton plants were fertilized with 80-0-0 (N-P-

K) lbs/acre.

On 18 July 2003. 30 newly bom aphid nymphs were individually placed on the

underside of fifth mainstem node cotton leaves (one aphid per fifth leaf per plant and

number of plants were 30). Leaves were located at the fifth node down from the top of

the plant. Square T'xT'x '/a", clear plastic boxes with hinged tops (Alpha Rho Catalog #

203, Alpha Rho Inc. Fitchburg, MA) were used to confine the aphid nymphs. A half-inch

diameter hole was drilled in the bottom of each plastic cage and perforated muslin cloth

was hot-glued over the hole in order to allow ventilation and prevent the escape of test

aphids. A camel's hair bmsh was used to transfer aphid nymphs to the leaves, and

extreme caution was taken to avoid injury to the young aphids. Plastic cages were

deployed on the leaves using modified hair clips (L & N Sales and Marketing, Hatboro,

PA). Test aphids were transferred to the new fifth leaf when the plant produced a new

leaf to standardize the leaf nutritional quality among test insects. Aphids were monitored

every 24 hours and the developmental stage, fecundity, and mortality were recorded.

During the reproductive stage of test aphids, newly bom aphids were counted and

recorded, then removed daily until the last aphid from the hand placed cohort died.

36

3.3 Data Analv.sis

The following life history parameters were quantified: instar-specific and total

developmental period, age-specific surviyorship and fecundity, gross reproductive rate,

net reproductive rate, finite rate of increase, doubling time, and intrinsic rate of increase.

The life history parameters were calculated by using the methods described by

Andrewartha and Birch (1954). In this analysis, the first day in the life of the nymph was

set as the first pivotal age and age increments were set to one day. The intrinsic rate of

increase (r) was determined by iteratively solving the Euler equation as given below.

Ze^Xm^^i

Where x is the age in days (including immature stages), r is the intrinsic rate of

increase, Ix is the proportion of individuals alive at time x of an original cohort (including

immature mortality). The variable m^ is the mean number of offspring produced per

surviving aphid during the age interval x (Iday). The life table parameters gross

reproduction rate (GRR=Zmx), net reproductive rate (Ro= H^mx), finite rate of increase

(A=e'', a discrete form of the intrinsic rate of increase), and doubling time (DT=ln2/r)

were calculated using the methods described by Andrewarth and Birch (1954). After

computing the intrinsic rate of increase (r) for the original data (rati), the Jackknife

method (Meyer et al. 1986) was used to estimate the standard error of the calculated life

table statistics.

In order to monitor the actual temperatures that aphids were experiencing in the

field, two, four-probe HOBO® weather dataloggers (model H08-006-04, Onset Computer

Corp., Bourne, MA) were installed in the cotton field. The two dataloggers were

installed on two separate plants, with probes placed at four identical locations on each

37

plant. Temperature probes were installed on the undersurface of cotton leaves at the fifth

node from the top of the plant. Degree-days were computed above a developmental

threshold of 6.26 C. The development threshold was obtained by regressing temperature

against the inverse of nymphal development time measured in the Chapter II Laboratory

Study, then solving the resulting model for the x intercept (y=0).

3.4 Results and Discussion

Instar-specific nymphal developmental duration did not significantly vary among

instars. Nymphal durations consisted of 38, 48, 37, and 34 degree-days above a

development threshold of 6.26 °C for first, second, third, and fourth instars, respectively.

Cotton aphid mortality began at 448 degree-days (20 days from birth) and ended when

the last aphid died at 907 degree-days (46 days from birth) (Figure 3.1). Average

longevity was 31.4 calendar days and 674-degree days. Xia et al. (1999) reported a

developmental threshold of 7.1 °C from a laboratory study and estimated aphid longevity

to be approximately 275 degree-days. Aphid survivorship in this study was more than

two times that of the survivorship reported by Xia et al. (1999). Though the development

threshold in this study was lower than that used by Xia et al. (1999), causing faster

accumulation of degree-days, the size of the increase in survivorship in this study greatly

overshadows any influence due to this factor. Kersting et al. (1999) reported a

developmental threshold of 6.2 °C, and an average survivorship period of 25.2 d

(calendar days) at 25-30 °C, over 20% lower than in this study. Both of the previous

studies were conducted in the laboratory and used excised leaves in Petri dishes for their

rearing substrate. The present study was conducted in the field and used living plants as

38

the rearing substrate. Results of the present study indicate that cotton aphids exhibit

better survivorship in their natural habitat (cotton plants in the field) than in the

laboratory. One reason for the large difference between this and the previous studies may

be the fact that aphids utilized the turgor pressure of the living plants to aid in intake of

plant fluids, and excised leaves may not provide the level of nutrition as compared to

living plant leaves.

Aphid reproduction began at 140 degree-days (6 days from birth) and the daily

fecundity peaked at 241 degree-days (12 days from birth); reproduction ceased at 740

degree-days (35 days from birth) (Figure 3.2). Cotton aphids produced an average of 63

offspring in a 30-day average reproductive lifespan (Figure 3.3). Because survivorship

was 100% when 80% of reproduction had been completed (day 19) (Figures 3.1 and 3.2),

the net reproductive rate was only slightly lower than the gross reproductive rate. The

gross reproductive rate, net reproductive rate, finite rate of increase, intrinsic rate of

growth and doubling time were 62.24, 59.06, 1.4326, 0.35971 and 1.94 respectively. Xia

et al. (1999) reported gross and net reproductive rates of 28.3 and 24.4, respectively, at 25

°C. In the present study, although the field temperature fluctuated during the study

period, degree-days accumulated by caged aphids remained between 20 to 25 degree-

days per day when 95% of reproduction was occurring (27 days) with average daily

temperature of 28.1 °C (Figure 3.4). Data reported from laboratory studies indicated that

aphids showed the best fecundity on cotton seedlings in the laboratory at 25-27 °C (Akey

and Butler 1989), a temperature range only slightiy lower than average temperatures

during July-August in the Texas High Plains (Figure 3.4). In the laboratory sttidy

(Chapter II), gross and net reproductive rates, and intrinsic rate of growth were 50.5,

39

44.8, and 0.37403 at 25 °C. and 58.9. 53.1, and 0.31218 at 30 °C, both respectively (Table

2.4). Aphid fecundity in our field study was higher than that reported in previous studies.

As proposed for survivorship, poorer nutritional quality of plants or the use of excised

leaves, as rearing substrates in these studies may have been a factor in influencing

fecundity. However, in our lab study, aphids were caged on living plants in the growth

chamber, indicating that some other factor may also be influencing survivorship and

fecunditN of aphids. Effects of other factors such as solar radiation or humidity on cotton

aphids in the field should be investigated in fiiture studies.

In summary, the present field study revealed that the gross reproductive rate

(GRR) was higher in the field (62.24) compared with that in the laboratory (highest lab

GRR among the six different constant temperatures was 58.9), with the finite rate of

increase (X.) of 1.43263. This indicates that cotton aphids exhibit higher developmental

and growth rates in their natural habitat compared to growth chambers. Nutrition may be

one reason for this difference. But future research should specifically address this factor

and other potentially influential factors such as solar radiation, daily fluctuations in field

temperatures, humidity, air condhion and movement (natural vs. growth chamber), and

other factors.

40

0 10 20 30 40

Aphid Age (Days from Birth)

50

Figure 3.1. Daily average survivorship of cotton aphids in the field, Lubbock, Texas, 2003.

O u

s s

0 10 20 30 40

Aphid Age (Days from Birth)

50

Figure 3.2. Daily average fecundity of cotton aphids in the field, Lubbock, Texas, 2003.

41

w) 60

0 10 20 30 40 50

Aphid Age (Days from Birth)

Figure 3.3. Average cumulative (lifetime) fecundity of cotton aphids in the field, Lubbock, Texas, 2003.

42

35

s h. 4>

a a a> H 0̂ &£ R u a> >

<

30

25

20

15

16-Jiil 31-Jul 15-Aiig 30-Aug

Sample Date

Figure 3.4. Daily average temperature ( "C ) under the surface of cotton leaves next to caged cotton aphids used in a life table study, Lubbock, Texas, 2003. The dashed line indicates the average daily temperature when 95% reproduction was occurring.

43

3.5 Literature Cited

Akey, D. H., and G. D. Butler. 1989. Developmental rates and fecundity of apterous Aphis gossypii on seedlings of Gossypium hirsutum. Southwest. Entomol. 14: 295-299.

Andrewartha, H. G. and, L. C. Birch. 1954. The Distribution and Abundance of Animals. University of Chicago Press, Chicago, IL.

AnonvTnous. 2004. The world of cotton. National Cotton Council of America web page http://www.cotton.org/econ/world/index.cfm.

Kersting, U., S. Satar, and N. Uygun. 1999. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Homoptera: Aphididae) reared on Gossypium hirsutum L. J. Appl. Entomol. 123: 23-27.

Kidd, P. W.. D. R. Rummel, and H. G. Thorvilson. 1996. Effect of cyhalothrin on field populations of the cotton aphid. Aphis gossypii Glover, in the Texas High Plains. Southwest. Entomol.21: 293-301.

Leser, J. F., C. T. Allen, and T. W. Fuchs. 1992. Cotton aphid infestations in west Texas: A growing management problem, pp. 823-827. In Proc. Beltwide Cotton Conferences, Nat. Cotton Council of Amer., Memphis, TN.

Leser, J. F. 1994. Management of cotton aphids: Texas style, pp. 137-141. /n Proc. Beltwide Cotton Conferences, Nat. Cotton Council of Amer., Memphis, TN.

Meyer, J. S., C. G. IngersoU, L. L. McDonald, and M. S. Boyce. 1986. Estimating uncertainty in population growth rates: Jackknife vs. bootstrap techniques. Ecology 67: 1156-1166.

Parajulee, M. N., P. W. Kidd, D. R. Rummel, and W. P. Morrison. 2003. Aerial movements of the cotton aphid. Aphis gossypii Glover (Homoptera: Aphididae), and discovery of male morphs in the Texas High Plains. Southwest. Entomol. 28: 241-247.

Rummel, D. R., M. D. Amold, J. E. Slosser, K. C. Neece, and W. E. Pinchak. 1995. Cultural factors influencing the abundance of Aphis gossypii Glover in Texas High Plains cotton. Southwest. Entomol. 20: 396-406.

Slosser, J. E., W. E. Pinchak, and D. R. Rummel. 1998. Biotic and abiotic regulation of Aphis gossypii Glover in west Texas dryland cotton. Southwest. Entomol. 23: 31-65.

44

Slosser, J. E., M. N. Parajulee. G. B. Idol, and D. R. Rummel. 2001. Cotton aphid response to irrigation and crop chemicals. Southwest. Entomol. 26: 1-13.

Williams, M. R. 2004. Cotton insect losses-2002. In Proc. Beltwide Cotton Conf, Nat. Cotton Council of Amer., Memphis, TN.

Xia, J. Y., W. van der Werf, and R. Rabbinge. 1999. Influence of temperature on bionomics of cotton aphid. Aphis gossypii, on cotton. Entomol. Exp. Appl. 90: 25-35.

45

VITA

Anand P. Sapkota was bom on April 10, 1965 in Bharatpur Chitwan, Nepal. He

completed an associate degree in Civil Engineering from the Tribhuvan University,

Kathmandu, Nepal in 1985. He then joined a Civil Engineering Consulting firm in

Kathmandu as a junior engineer and served from 1986-1989. He was then deployed to

the department of irrigation at the Ministry of Water Resources in Kathmandu, Nepal in

1989. He received a four-year study leave from this job, and completed his bachelor's

degree in Civil Engineering from the Tribhuvan University in 2000. He became a

registered Engineer of the Nepal Engineering Council in 2001. Though his

undergraduate fraining was in engineering discipline, he accepted an opportunity to

pursue an M.S. degree in Entomology at Texas Tech University in Spring 2003. During

his M.S. program he was awarded a West Texas Agricultural Chemicals Institute

Scholarship and the Harold and Mary Dregne Graduate Scholarship. His wife, 12-year

old son Ashish and 9-year old daughter Asmita resided in Nepal during his graduate

study in the United States.

46

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