Assessment of the potential for integration of avian conservation with modern agricultural production

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Assessment of the potential for integration of avian conservation with modern agricultural production
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Wildlife Ecology and Conservation thesis, Ph.D   ( lcsh )
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Includes bibliographical references.
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by Gregory Alan Jones.
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ASSESSMENT OF THE POTENTIAL FOR INTEGRATION OF AVIAN
CONSERVATION WITH MODERN AGRICULTURAL PRODUCTION















BY

GREGORY ALAN JONES


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE
UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA




























Copyright 2003

by

Gregory Alan Jones















ACKNOWLEDGMENTS

Funding for my research was provided by the Florida FIRST initiative of

the University of Florida's Institute of Food and Agricultural Sciences, the

Organic Farming Research Foundation, The Eastern Bird Banding Association,

The North American Bluebird Society, and the University of Florida's

Department of Wildlife Ecology and Conservation.

I am truly grateful for the collaborative assistance of the following

researchers: Dr. Kathryn Sieving, Dr. Michael Avery, Dr. Robert Meagher, Dr.

Kenneth Buhr, and Dr. Jennifer Gillett. I thank Dr. Avery, Kandy Rocca, and all

of the staff members at the USDA Denver Wildlife Research Center's Florida

Field Station, Gainesville, Florida, for use of their facilities, birds and their help in

conducting experiments. I also thank Dr. Meagher, Charlie Dillard and all of the

staff members at the USDA-ARS Insect Behavior & Biocontrol Unit, Gainesville,

Florida, for the help and provision of experimental materials. I thank the

following research assistants: Matt Reetz, Leonard Santisteban, and Kat Smith. I

thank the WEC staff members Caprice McRea, Monica Lindberg, Delores

Tillman, Laura Hayes, and Sam Jones for their kind help and friendship over the

past years.

A very special thank you goes to the members of my supervisory

committee for their guidance and support during pursuit of my degree: Dr.









Kathryn Sieving (Chair), Dr. George Tanner, Dr. Michael Avery, Dr. Douglas

Levey, and Dr. E. Jane Luzar. I will always be grateful for Dr. Sieving's

commitment, encouragement, and patience as I struggled through the process of

developing a research program and seeing it through to completion. I appreciate

the special attention and help provided to me by all of these people, each in their

own way over the years. I have very much enjoyed working with each of these

fine individuals.

I wish to relate my appreciation to Dean Jimmy Cheek and Associate

Dean E. Jane Luzar for providing me the opportunity to work with the students

and faculty in the College of Agricultural and Life Science's Honors Program. It

has been a great privilege and learning experience to be able to interact with the

brightest and the best of the college's students. I have been very fortunate to be

able to work and learn from some of the top teaching staff in the college as well in

this program. I am very grateful for these people's support over the past few

years.

I greatly appreciate the logistic cooperation of the following extension

agents Gary Brinen, Austin Tilton, David Denkins, Jacque Bremen, Marvin,

Anthony Drew, and David Holmes. I would also like to thank Marty Mesh and

the Florida Certified Organic Growers and Consumers, Inc. for their assistance.

The cooperation and participation of the following producers is gratefully

acknowledged as well: Larry and Greg Rogers, the Hauffler Brothers, Don King,

Andy Mulberry, W. K. Bagwell, Dennis Short, Kathy and Marvin Graham, Lois

Milton, Tommy Simmons, Bill Ogle, Bill Allen, Rosalie Koenig, Charles









Lybrand, Donald Appelbaum, Ed Parker, Charles Andrews, Joe Durando, Paul

Morris, Archer Christian, Cynthia Conolly, and Bikram Singh.

I would especially like to thank my fellow colleagues in Dr. Sieving's lab

for their fellowship over the years. Their reviews, sharing of ideas, and guidance

has truly been an important factor in the success of my graduate program. I have

enjoyed their friendship while I have been at the university and hope to continue

to be close to them in the future. Thanks Tom, Marcela, John, Traci, Matt, Mike

and Ivan.

Finally, I thank my wife Leigh and my two sons Ben and Zach for their

love, support and patience. I know I have not always been easy to live with,

especially at times when I was frustrated or stressed during the past few years. I

could not have achieved my academic or career goals without them. I love you

all. I also appreciate the love and support provided to me and my family by my

parents and especially my mother-in-law Jamie Schnabel.
















TABLE OF CONTENTS


Page

ACKNOWLEDGMENTS ............................... ... ........... iii

ABSTRACT .. ................................. ........... ............. viii

CHAPTERS

1 INTRODUCTION .................... ................... ............ 1

Economic Ornithology The First Attempt to Integrate Bird
Conservation and Agricultural Production ............................. 2
Effects of Agricultural Practices on Avian Populations ................. 4
Birds as Predators in Agroecosystems ..................................... 8
Examples of Experimental Work Investigating the Impact of
Birds on Insect Populations in Modem Agroecosystems ............ 10
Natural Systems Agriculture or Ecoagriculture .......................... 12
Research Needs ......................... ...... ........ .... 16
Conclusion ............ ............................... ... ........ 17

2 AVIAN BIODIVERSITY AND FUNCTIONAL INSECTIVORY
ON NORTH-CENTRAL FLORIDA FARMLANDS .............. 19

Introduction ...................... ................ ... ...... ..... ....... 19
M methods .............. ............... ........... ............... 23
Results ................ .... ...... ... ....... ...... 30
Discussion ................ ....................... .... .. .. 40

3 INTERCROPPING WITH SUNFLOWERS TO CREATE LOCAL
REFUGIA FOR AVIAN PREDATORS OF ARTHROPOD PESTS 50

Introduction ......................... .... ................... 50
M ethods .................. .... ............................ ..... 54
Results .................................................................. ...... 61
Discussion ......... ..... ..... ......................... ........ 76
Conclusion ..................... .................... .......... 82









4 PARASITIZED AND NON-PARASITIZED PREY SELECTIVITY
OF INSECTIVOROUS BIRDS: POTENTIAL FOR
AUGMENTATION OF CLASSICAL BIOCONTROL ............ 84

Introduction .............. ..................... ........ 84
M methods .......... .... ..... .............. ......... ........... 87
R results ............... .. ............. .. ........ ....... .... ... 95
Discussion ..................... ................ .. ...... .......... 96
Conclusion ............. ............. .................... 100

5 SUMMARY AND FUTURE RESEARCH NEEDS ................... 102

Summary ................ ...................... ................ .. 102
Future Research Needs ..... .................... ...... ............ 106
Conclusion ................... .. .. ........... .... .... ............ 107


LITERATURE CITED ................... ... ........ ..... ....... 109

APPENDICES

A BIRD SPECIES OBSERVED DURING CENSUS SURVEYS
IN NORTH-CENTRAL FLORIDA FARMLANDS ...... 128

B BIRD SPECIES OBSERVED ON ORGANIC FARMLANDS
OF NORTH-CENTRAL FLORIDA ....................... 133

C BENEFICIAL INSECTS OCCURRING ON SUNFLOWER
AND CROP VEGETATION ............................. 138


BIOGRAPHICAL SKETCH .................................... ............. 140














Abstract of Dissertation Presented to the Graduate School
Of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy

ASSESSMENT OF THE POTENTIAL FOR INTEGRATION OF AVIAN
CONSERVATION WITH MODERN AGRICULTURAL PRODUCTION

By

Gregory Alan Jones

December 2003

Chair: Kathryn E. Sieving, Associate Professor
Major Department: Wildlife Ecology and Conservation


The overall goal of my research was to assess the potential for integrating

bird conservation on farmlands while enhancing production goals through

augmentation of insect pest control. Working on selected conventional and

organic farms in North-central Florida my study objectives were to: 1) assess

habitat characteristics on and adjacent to farms influencing avian species diversity

and insect-foraging activity, and to identify 'functional insectivores' on these

farms, 2) determine the effectiveness of sunflower intercrops as refugia for both

insectivorous birds and beneficial insects in cropped fields, and as tools to

enhance insect-foraging by birds in cropped areas, and 3) test the hypothesis that

insectivorous birds can potentially augment pest control programs involving

hymenopteran parasitoid predators, via preference for unparasitized over

parasitized prey.









Using a combination of bird surveys and focal foraging observations over

2 years, I determined that bird diversity in cropped and non-cropped habitats on

farms varied in the following ways: a) vegetation type in field borders

significantly influenced species richness per census point (F5,30 = 3.5, P = 0.013)

and in field borders (F5.30 = 3.8, P = 0.009), b) mixed crops generated

significantly greater bird densities per point (F,3o = 7.4, P = 0.011) and in cropped

fields (Fi,30 = 8.2, P = 0.008), and c) foraging activity and abundance of

functional insectivores were greatest in mixed crops (F1,29= 4.2, P = 0.051). In a

replicated, controlled field experiment I determined that intercropping rows of

sunflowers significantly increased densities of birds (F2," = 43.33, p< 0.001),

numbers of individuals (F.,, = 59.84, p < 0.001), and foraging time by individual

insectivores in crops (F,,,9 = 51.93, p < 0.001). Visual observations and stomach

samples confirmed that birds consumed economically important pest insects. In

experimental feeding trials, blackbirds exhibited no preference between

parasitized and non-parasitized lepidopteran larvae of similar body size (Wo =

139, p = 0.69) but a significant preference for larger non-parasitized prey (Wo =

248, p < 0.001). My study suggests that farmlands can be managed to enhance

wild bird populations and the potential that birds could augment pest control

programs in modem agricultural operations.















CHAPTER 1
INTRODUCTION


The relationship of birds to agricultural activities in the temperate zones of the

Northern Hemisphere has long been of interest to ornithologists both in the United

States and in Europe. Early naturalists published numerous papers describing careful

observations and thoughtful consideration of the relation of birds to crop production.

During its existence, multiple reports produced by the Section for Economic

Ornithology within the federal Department of Agriculture confirmed the utility of

birds as destroyers of pest insects, often recommending their classification as highly

beneficial to agriculture. However, with the advent of farm mechanization, synthetic

chemical pesticides, and the intensification of agricultural production, focus upon the

positive impact birds may have on agriculture waned and research interest regarding

the detrimental effect agriculture has on avian populations increased. Currently

ornithologists have suggested that change in agricultural practices and landscape

structure over the past few decades have reduced the occurrence of farmland habitat

elements many farmland species had traditionally utilized (O'Conner and Boone

1990, Freemark 1995, McLaughlin and Mineau 1995).

Rodenhouse et al. (1995) believe that agriculture has had a greater impact on

the status of Neotropical migratory birds than any other human activity. Additionally,

their review also shows that conservation measures benefiting avian species in









agricultural landscapes will be acceptable to farmers if management

recommendations have neutral or positive effects on food production. Sufficient

evidence has accumulated from studies in forest, grassland, orchard, and row

cropping systems that offers sufficient evidence that insectivorous birds may be of

economic value by enhancing production through predation of pest insects. Due to

this potential ecological role of birds in agroecosystems, several reviewers of past

work, including McFarlane (1976), Jackson (1979), and Kirk et al. (1996), suggest

birds should be considered as components of modem biological pest management

schemes. However, despite potential values of birds on farms, the theory and practice

of enhancing these native natural enemies by providing habitat for them within

cropping systems has been relatively neglected.

Ornithologists have an opportunity to propose management recommendations

favoring avian conservation within agricultural production systems by working within

interdisciplinary teams developing modem sustainable or natural systems agriculture

(Rodenhouse et al. 1995). As agricultural producers recognize the importance of a

structurally and biologically diverse fanned environment, ornithologists can institute

the resurrection of quality avian habitat within agroecosystems. Enlightened

management of farmlands can satisfy the needs of agriculture and numerous avian

species while providing mutual benefits (Rodenhouse et al. 1995).



Economic Ornithology The First Attempt to Integrate Bird Conservation
and Agricultural Production

Early naturalists in this country, such as Alexander Wilson, James Audubon,

and even Benjamin Franklin, became interested in bird behavior and made references









to the purely economic phases of bird life. Their writings repeatedly relate the value

of different species as destroyers of insects. After 1850, various researchers

interested in agriculture published numerous papers in agricultural journals and in

reports of agricultural and horticultural societies that described careful observations

and thoughtful considerations of the relation of birds to crop production (reviewed by

Weed and Dearborn 1935). Needless to say, these publications generated a great deal

of discussion as to the true utility of birds, because some bird species had long been

considered agricultural pests.

One of the results of the organization of the American Ornithologist's Union

(AOU; circa 1883) was the impetus it gave to the study of bird's food habits to

resolve questions of their utility as pest predators and the desirability of legislation

permitting the destruction of species popularly considered pests. At the request of the

AOU and researchers within the Department of Agriculture, congress appropriated

monies to establish a Section for Economic Ornithology (SEO) within the Division of

Entomology of the federal Department of Agriculture (McAtee 1933). The section

was responsible for the promotion of economic ornithology (or the study of the

interrelation of birds and agriculture), the investigation of avian food habits, the

investigation of both resident and migratory birds in relation to both insects and

plants, and publish reports thereon (McAtee, 1933, Weed and Dearborn 1935).

Research emphasis at this time consisted of the examination of the contents of

bird stomachs, together with observations of birds in the field. Multiple reports

produced by the SEO confirmed the utility of birds as destroyers of pest insects and

as important weed seed predators. Reports of this nature submitted to the USDA's









administrators often concluded that birds feed largely upon pest insects and should be

classified among the species highly beneficial to agriculture. The section later

developed into the original Biological Survey, and research of this kind continued

until the early 1930s (Weed and Dearborn 1935, Kirk et al. 1996). However, with the

advent of synthetic chemical pesticides in the 1940's, little work in this field has been

done (Kirk et al. 1996). Currently, avian research performed by the USDA focuses,

for the most part, upon control of crop damage by birds. While focus upon the

positive impact birds may have upon agriculture waned, research interest regarding

the detrimental effects agriculture has had on birds has increased since the 1940s.



Effects of Agricultural Practices on Avian Populations

Agricultural development since the 1700s has dramatically altered or

eliminated the natural landscape of the continental United States. Forests originally

covered about one-half of this region of North America, 40% was covered in

grasslands, and the remaining area was arid and barren (Cochrane 1993). Between

1790 and 1890, 300 million acres of virgin forests were cleared and an equal amount

of grasslands were plowed. Agriculture today comprises the largest landuse class

encompassing over 50% of the arable land area of the contiguous 48 states (USDA

1998). Currently, of the 1.9 billion acres of land in the U. S., some 350 400 million

acres are under intensive crop cultivation with approximately another 200 million

acres of marginal land at the ready to be put into this practice should prices warrant

its use (Cochrane 1993). While the conversion of natural landscapes to

agroecosystems in Europe occurred much earlier in history, this alteration took place









steadily across several centuries, and agricultural lands now comprise 41% of the land

area of the 15 countries of the European Union (Pain and Dixon 1997).

Agricultural practices on farmlands have changed drastically over the past 150

years. The concept of farm mechanization was widely accepted in the 1850s,

characterized by the use of cultivators, mowing machines, and reapers (Cochrane

1993). From this point farm machines evolved rapidly; increasing in size and

efficiency and incorporating both steam and then internal combustion power.

Increased size and efficiency of farm machinery in the post World War 2 years

allowed for the expansion of field size and homogenization in farmland structure.

During the period from 1935 to 1970, while the acreage of land under cultivation did

not change the number of farms declined from 6.8 million to 3 million via corporate

consolidation concomitantly with an intensification of production per unit area

(Cochrane 1993). This same phenomenon occurred in post World War 2 Europe

including increased field sizes, reductions or elimination of boundary features, and an

overall change in agricultural landscape structure (Pain and Dixon 1997).

Many researchers here in the U.S. have suggested that changes in agricultural

practices over the past few decades have reduced the favorability of agricultural

landscapes for foraging and nesting by many native and migrant species (Best 1986,

O'Conner and Boone 1990, Wamer 1992, Bollinger and Gavin 1992). The once

heterogeneous landscape found in agroecosystems composed ofwoodlots, ponds,

shelterbelts, wooded hedgerows and fencerows, and other such landscape elements

provided for an abundance and diversity of bird species. However, these landscapes

have become increasingly homogenized through the removal, fragmentation, and









isolation of these elements upon which many species had come to depend (O'Conner

and Boone 1990). For example, Gawlick and Bildstein (1990) attribute the decline of

Loggerhead Shrikes to loss of their preferred edge habitat in farm landscapes. This

same sentiment has been voiced by researchers in Europe relating that increased

specialization has reduced the prevalence of mixed farming and the habitat mosaics

inherent to traditional types of farming (O'Conner and Shrubb 1986, Baillie et al.

1997). Groppali (1993) related the percentage of eradication of tree rows and hedges

to expand cultivated parcels within his study area near Cremona, Italy, was 33% and

36% respectively over a 9-year period, 1980-1989. In these parcels where tree rows

and hedges had been removed, species diversity and numbers of nesting pairs of birds

were significantly reduced. In Britain, Baillie et al. (1997) found that more farmland

birds are declining than increasing, and more importantly, specialist farmland species

are declining more than generalists due to loss of preferred farmland habitat.

Within the U.S., resident and migratory landbird passerines, represented by

over 200 different species, constitute over 70% of the bird species that feed, roost, or

breed on agricultural lands (Rodenhouse et al. 1993). Most landbirds utilizing crop

fields and edges are Neotropical migrants, and agricultural practices have been

implicated in the decline of at least nine of these species currently listed as threatened

or endangered. Studies in U.S. farm landscapes have found the majority of bird

species utilizing agricultural lands are found in uncultivated areas. Highest species

richness and abundance have been documented in those areas with greatest vegetative

structure, including woody shrubs and trees. Avian richness and abundance are often

lower in grassed edge, and lowest in row cropped fields (Shalaway 1985, Best et al.









1990, Camp 1990). Therefore there appears to be a strong correlation between

decreasing species richness and abundance and decreasing structural diversity in farm

systems. Similar results have been obtained in European studies (Baillie et al. 1997).

Production practices associated with agricultural intensification are also

problematic for birds utilizing agricultural landscapes. Intensive agricultural

practices include greater working of the land with quick rotations or relay cropping,

cover crops replacing fallow rotations, increased livestock densities, and use of high

yielding cultivars requiring greater or more frequent fertilization and irrigation

(O'Connor and Boone 1990). Rodenhouse et al. (1993) indicated that Breeding Bird

Survey abundances of many bird species in agricultural landscapes have exhibited

significant negative associations with specific crops between 1973-1989, suggesting

detrimental cropping practices are being employed. Multiple quick crop rotations

within a year, or relay cropping, increases the frequency of disturbance during avian

breeding potentially causing direct injury to adults and nestlings. Injury and nest

destruction by farm machinery can occur during field preparation, planting, crop

management, and harvest operations. Individuals can also be harmed indirectly

through the application of herbicides and insecticides that alter vegetation structure

and the insect food base within and immediately surrounding cultivated parcels

(O'Conner and Boone 1990, Rodenhouse et al. 1993). In their publication Birds in

Europe, Tucker and Heath's (1994) analysis of the major threats to birds listed as

species of conservation concern showed that agricultural intensification affects more

species than any other threat.









Birds as Predators in Agroecosystems

While the detrimental effects of modem agriculture on birds has received

much attention, the importance of wild bird management to enhance the productivity

and sustainability of agriculture, or to maintain ecological integrity and biodiversity

in agroecosystems, has not been thoroughly investigated (Rodenhouse et al. 1993,

Kirk et al. 1996). Rodenhouse et al. (1993) suggest that the development of lower

input sustainable agriculture and acceptance of integrated pest management (IPM)

programs may offer opportunities for greater avian conservation in agroecosystems.

Most importantly, management of uncultivated habitats (where birds may thrive) to

preserve natural enemies of agricultural pests will become a central part of pest

management planning in IPM (Rosen et al. 1996). The conservation value for bird

species utilizing low-input agricultural landscapes will be realized through the

reestablishment of habitat (i.e. Woodlots, windbreaks, complex hedgerows, etc.) and

an increase in food resources enhancing both their survival and reproductive success.

Rodenhouse et al. (1995) believe that the key to acceptance of conservation measures

that benefit avian species in agricultural landscapes is that management

recommendations do not interfere with, and hopefully enhance, production. Here lies

an important opportunity for ornithologists. By illustrating that birds may be of

economic value by enhancing production through predation of pest insects, farmers

could be encouraged to consider providing habitat for these species in their cropping

systems and farm landscapes.

Studies relating individual pest species to individual bird species or groups of

species offer sufficient evidence that birds can and should be considered as an









important component of modem biological pest management schemes (Jackson

1979). Birds are important predators of many destructive forest insects and play an

important role in suppressing phytophagous insect populations in forest ecosystems

(reviewed by Takekawa et al. 1982, McFarlane 1986, Price 1987). Moreover, via

numerical and functional responses to insect outbreaks in North America birds are

potentially decreasing insect outbreak frequency and severity (Holling 1988, Dahlston

et al. 1990, Holmes 1990). Limitation of phytophagous insect biomass in these

systems may have an important effect upon primary productivity within forest

systems. For example, Marquis and Whelan (1994) have demonstrated that exclusion

of insectivorous birds from foraging on phytophagous pests of white oak in Missouri

significantly reduces long-term primary productivity of individual trees. Over several

years, trees harboring insectivorous birds had greater leaf area and stem elongation

than did trees where birds were excluded or in trees that were sprayed with

insecticide. Conceivably, birds utilizing agricultural areas could provide similar

biomass reduction and productivity benefits, which could be realized through

appropriate management practices (Rodenhouse et al. 1995, Kirk et al. 1996).

Over the past 10 years, field entomologists and agronomists have increasingly

recognized that conservation of natural enemies via management of non-cropped

habitats that support them is important to effective and successful biological control

in agricultural systems (Rosen et al. 1996). However, despite its demonstrated value,

the theory and practice of enhancing native natural enemies as integral components of

agroecosystems has been relatively neglected (Picket and Bugg 1998). If a low-input

productive balance is to be restored within agroecosystems, farmers must recognize









and make use of natural control of insect pests by providing for the needs of all

potential predators of pest insect within these systems. As was recognized long ago

by economic ornithologists, most birds that traditionally utilize agricultural areas may

be of great economic value by providing biological stability in agroecosystems.

Conservation of beneficial insectivorous birds through habitat enhancement on farms

could result in significant economic benefits to agricultural production by reducing

pest control costs and improve sustainability through reduced reliance upon persistent

toxic agrochemicals.



Examples of Experimental Work Investigating the Impact of Birds
on Insect Populations in Modern Agroecosystems

Since 1950, several studies have focused upon 2 pests of field crops, corn

borers and grasshoppers, utilizing exclosures to compare insect populations protected

from bird predation (Kirk et al. 1996). Both Floyd et al. (1971, 1969) and Black et al.

(1970) reported significantly lower survival of overwintering corn borer larvae found

in corn stalks exposed to bird predation compared to those present within exclosures.

As overwinter losses were normally low due to other factors, they concluded these

were destroyed via predation by birds [such as Northern Flickers (Colaptes auratus)]

observed feeding on corn stalks. Numbers of larvae removed compared with the

numbers remaining in infested stalks where birds had been excluded ranged from

45% to over 80% in these studies. Quiring and Timmins (1988) found similar results

of reduced corn borer larvae overwinter survival due to predation by American Crows

(Corvus brachyrhynchos) in southwestern Ontario, Canada. Additionally, corn borer









larvae removal was found to be greatest in those fields nearest one of the largest

known crow roosts in the region.

Exclusion studies of bird predation impact upon grasshoppers in rangeland

systems (frequently grasslands are interspersed with row cropping fields) have

produced mixed results. While Belovsky et al. (1990) determined birds had a minor

impact on grasshopper populations, other studies indicated that birds do affect

grasshopper densities and species richness. Joern (1986) concluded that avian

predation can have a significant impact on grasshopper populations through biomass

reduction and reduction of species diversity. Modeling this, Kirk et al. (1996)

estimated that a grasshopper-eating passerine family unit could consume 3.7 kg of

grasshopper biomass, or approximately 149,000 individuals per breeding season. In a

grassland system of Northwest China, numbers of breeding Rosy Starlings (Sturnus

roses) were increased after human made nesting sites with shrubby cover and water

were added (Olkowski and Zhang 1998). Researchers determined grasshopper

numbers were reduced from 42 to 2.3 per m2 within a 500 m radius around artificial

nesting structures by the end of the birds' breeding season (Chen 1986, Olkowski and

Zhang 1998).

Two recent exclosure studies have evaluated the impact of bird predation on

foliage arthropods in coffee plantations and lepidopteran pests in an orchard system.

Greenberg et al. (2000) found birds reduced the abundance of large arthropods on

coffee plants by 64-80%, compared to that those found on plants where birds were

excluded, depending on the coffee system type (shade or sun coffee). A significant

reduction in leaf damage to coffee plants was associated with this reduction in









arthropod biomass in both coffee systems. Mols and Visser (2002) found that

caterpillar damage levels to apples in orchards decreased with increased periods of

foraging by great tits (Parus major). Overall damage to apples by caterpillars was

reduced by measurable amounts improving yield, number of apples per tree,

compared to trees where great tits were excluded.

Both McFarlane (1976) and Kirk et al. (1996) conclude that strong

experimental evidence in forest and grassland systems suggests avian predation could

suppress crop insect pest populations at medium or low infestation levels,

representing an important ecological in agroecosystems would compliment integrated

pest management plans. While birds alone may not "regulate" insect pest

populations, combined with other forms of pest management, they promise to play an

important ecological role in agroecosystems (Kirk et al. 1996). Sympathetic

management is needed to stem the decline of farmland birds and enable them to

assume a mutualistic role with agricultural production.



Natural Systems Agriculture or Ecoagriculture

Agricultural modernization largely contradicts ecological principles.

Consequently modem, or "conventional", agroecosystems are inherently unstable,

plagued by recurrent pest outbreaks, pollution of water systems, soil erosion,

salinization, and other undesirable environmental and social costs (Altieri 1994).

Modem agriculture emphasizes artificial single species monocultures, requiring

constant human intervention to suppress ecological succession and maintain

productivity (Swift and Anderson 1993). Additionally, simplification of species









composition of biological communities both reduces their stability and results in

increased susceptibility of that community to invasion by undesirable species (Elton

1958, Crawley 1987). Therefore, conventional agriculture exists in a metastable

equilibrium regulated by enormous inputs of energy (Harwood 1990) and human

activity (Gliessman 1987). The inherent self-regulation of populations within natural

biotic communities is lost when humans modify community interactions and disrupt

coevolutionary processes (Tumbull 1969). Inherent limitations of species populations

within natural communities is a desirable attribute to incorporate into synthetic

agroecosystems (Tumbull 1969) and, in particular, enhancement of predator-prey

relationships characteristic of natural systems has a pivotal role to play in the

evolution of agriculture towards more environmentally sustainable systems in this

century (Atkinson and McKinlay 1997).

An ecosystem approach to agriculture emphasizes management of

agroecosystems in such a manner that sufficient food production will be sustainable

and of high quality with minimal environmental disturbance (Colby 1990, McNeely

and Scherr 2003). Utilizing this approach, it is believed that a multitude of beneficial

ecological processes can be incorporated into agroecosystems (Soule and Piper 1992).

The central idea for "ecological agriculture" is that the structures of native biological

communities are the most appropriate structural models for agriculture. Such

communities have developed and endured in particular environments as a result of

centuries of evolutionary selection for ecosystem function (The Land Institute 1999,

McNeely and Scherr 2003). Agricultural systems that are modeled after natural

ecosystems should exhibit many functional attributes and processes that stabilize









natural systems, including vegetation adapted to the local climate, closed nutrient

cycling, effective resource partitioning, soil preservation, and biological methods of

crop protection (Soule and Piper 1992). Therefore, by mimicking the local natural

vegetation structure of native biological communities, farmers can emulate a whole

package of patterns and processes that have developed over an evolutionary time

frame exhibited by these ecological systems. Additionally, rather than perfecting one

crop at a time, this holistic ecological perspective to agricultural production suggests

seeking out a collection of plants and animals that work well together. It is this

perspective of natural systems agriculture that provides a great opportunity for avian

conservation.

The potential exists to manage farm habitats to attract selected desirable

species in greater numbers in order to create a stable guild of insect predators, capable

of rapid aggregation to high density "hot spots" of colonizing pests, and capable of

switching to pest species from alternative foods (Helenius 1998). Methodologies that

promote the abundance and diversity of pest insect predators will not only

significantly contribute to non-chemical based crop protection but also provide

beneficial consequences in conserving biological diversity in agricultural landscapes.

Habitat management to enhance biological control of arthropod pests can provide

various environmental requisites to pest insect enemies (such as birds) including

modified climate, protective cover, nesting habitat, and supplementary foods (Pickett

and Bugg 1998). Colonization, dispersal by diffusion, and foraging movements of

beneficial predators can be influenced through habitat modifications within cropping

systems (Helenius 1998). For example, weedy vegetation strips within fields could









be arranged in such a way as to provide refuge and increase interspersion of foraging

predators within large cropped areas (Nentwig 1998). Modifying agricultural

landscapes, or "farmscaping," by adding features such as hedgerows, field margins,

shelterbelts, and roadside and watercourse plantings using native trees, shrubs,

perennial grasses, and herbaceous and annual broadleaf species can attract and sustain

beneficial arthropod pest predators (Bugg et al. 1998).

Ornithologists have an opportunity to propose management recommendations

favoring avian conservation within agricultural production systems by working within

interdisciplinary teams developing modem sustainable or ecoagriculture. The largely

unexplored diversity of avian insect predators that could be included in natural

biological regimes offers numerous possibilities for their use in cropping systems.

Birds of conservation concern, both resident and migratory, can benefit from

cropping systems and farmland habitat structure created to enhance insectivorous bird

use of agroecosystems. Through this effort, many habitat features and the structural

complexity once found within agricultural landscapes supporting avian species in the

past would be reintroduced. As agricultural producers recognize the importance of a

structurally and biologically diverse farmed environment, ornithologists can institute

the resurrection of quality avian habitat within agroecosystems. With enlightened

management of farmlands both the needs of agriculture and numerous avian species,

as well as other wildlife, can be satisfied and mutually beneficial (Rodenhouse et al.

1995).









Research Needs

Before we can propose that agricultural producers can truly employ birds in

pest management schemes we must not only know the relationship between insect

pests and avian species, we must have an understanding of the functional role birds

currently play in modem agroecosystems. With this understanding, management

recommendations for biological control enhancement can be developed by

manipulating populations of avian species identified as potentially beneficial

currently existing in, or that could be attracted to, these systems. Rodenhouse et al.

(1995) state that future research should focus upon identifying farmland structures

and agricultural practices that create and sustain avian populations. They explain that

studies of annual breeding productivity and survival of birds nesting in fields and

edges are few, potential source areas that may require protection or expansion have

not been identified, and the values of specific landscape elements and combinations

of elements have not been determined for agroecosystems. Therefore, they believe

that both field-scale and landscape scale studies need to be performed and integrated.

Kirk et al. (1996) believe that a consideration of birds should be part of any

economic cost/benefit assessment related to pest control programs and farm

landscapes should be managed with them in mind. They state that more

multidisciplinary studies are needed to examine: (1) the abundance and availability of

birds relative to various insect pest species, (2) avian diets and foraging habits to

determine quantitatively the site-specific level of predation on invertebrate pest

species compared to other arthropods, (3) integration of birds with other natural insect

enemies, and (4) management of farmland landscapes in ways that best augment









natural control of insect pests. Wratten et al. (1998) indicate the potential for the

expansion of research exploiting ecological knowledge in farmland management is

promising. They suggest that a better understanding is needed of 3 related processes:

(1) the spatial scale dynamics of beneficial insect predators on farmland, (2) the

potential negative effects of insect predator refugia, and (3) the mechanisms involved

in the functioning of within-field and border refugia for the enhancement of natural

enemies of insect pests in agroecosystems.



Conclusion

Ornithologists have suggested that change in agricultural practices and

landscape structure over the past few decades have reduced the favorability of

farmland habitat elements many farmland species had traditionally utilized.

Agricultural landscapes have become increasingly homogeneous through the

removal, fragmentation, and isolation of these elements upon which many species had

come to depend. Intensification of agriculture, resulting in changes in production

practices, has also been cited as being problematic for birds utilizing agricultural

landscapes. Direct injury to individuals and nest destruction can be caused by farm

machinery during cropping operations. Individuals may also be harmed indirectly

through the application of agrochemicals. Holistic ecological perspectives to

agricultural production of both sustainable and natural systems agriculture provide an

opportunity to promote the inclusion of suitable habitat in agricultural lands for avian

species. Farm habitats can be managed to attract desirable insect pest predator

species in greater numbers contributing to non-chemical based crop protection as well









as improve conservation of biological diversity in agricultural landscapes. Migratory

and resident species of conservation concern will also benefit from farm structure and

management created to enhance avian presence in agroecosystems.

Recommendations developed by the ornithological community integrating the

body of information defining the problems faced by farmland birds with research

illuminating the functional role birds play in these systems, can potentially reverse

agricultural practice-induced avian population declines. Aldo Leopold stated,


In its extreme form it [agriculture] is humanly desolate and economically
unstable. These extremes will someday die of their own too much, not
because they are bad for wildlife, but because they are bad for farmers.
When that day comes, the farmer will be asking us how to enrich the wildlife
of his community. (Leopold 1945, page 168)

As imperatives for agricultural shift from the single goal of increasing production per

acre to environmentally sustainable systems, an excellent opportunity exists to match

the aspirations of farmers with needs of birds of conservation concern.















CHAPTER 2
AVIAN BIODIVERSITY AND FUNCTIONAL INSECTIVORY ON NORTH-
CENTRAL FLORIDA FARMLANDS


Introduction

Although agroecosystems do not support the biodiversity of natural landscapes

they replace, under the right circumstances they can provide diverse ecological functions

in addition to habitat for wild species. In regions where urbanization is rampant (e.g.,

Florida) farmlands are often the only ecological buffer between natural ecosystems and

suburban sprawl (Evans and McGuire 1996, McNeeley and Scherr 2002). Reflecting

growing public concerns over scientific reports of agriculture's negative effects on

human and ecosystem health (e.g., Parsons et al. 2000) during the past decades, policy

makers have been responding with incentives to modify grower operations to reduce

negative environmental impacts and increase ecological values of farmlands (Ikard 1996,

D'Souza and Ikerd 1996). For example, USDA programs like SARE (Sustainable

Agriculture Research and Education) promote development of sustainable agricultural

practices through research partnerships between farmers and scientists

(http://www.sare.org/htdocs/sare/about.html). Additionally, the Farm Bill of 2002

provides farmers monetary incentives for conservation of soil, water, air, and biodiversity

(Farm Security and Rural Investment Act of 2002). Signs of change toward ecological

agriculture include an increase of 10% per year in US farmland acreage under certified

organic management (USDA 1996, 2000, 2001a). With the public, policy makers, and









farmers increasingly involved in exploring alternative agriculture, the need for research to

integrate production of ecological services, native biodiversity, and healthy foods is also

intensifying (Rodenhouse et al. 1995, McNeeley and Scherr 2002).

Wildlife conservation is a natural partner in cultivating ecological agriculture

(Vandermeer and Perfecto 1997, McNeeley and Scherr 2002), yet this partnership is

weak because conventional food production practices that are detrimental to biodiversity

still dominate, and because research has not been satisfying demands for information for

ecologically-oriented farm operations (Hess 1991, Alston and Reding 1998, Jacobson et

al. 2003). Habitat destruction for agricultural expansion remains the single most

important cause of biodiversity impoverishment the world over (Vitousek et al. 1997),

and if native biotas are to survive the coming decades of human population expansion,

agricultural production lands must improve their biodiversity-holding capacity (Pimental

et al. 1992, Hobbs and Norton 1996). Indications are that alternative agriculture practices

encourage native wildlife and protect ecosystem services better than conventional

production agriculture (Warburton and Klimstra 1984, Pimental et al. 1992, Uri et al.

1999, McNeely and Scheer 2002), in part because sustainable farming generates

heterogeneous vegetative environments with features (hedge rows, shelter belts, mixed

cropping systems, and plantings that host natural enemies of pest species; O'Conner and

Boone 1992) that encompass many recognized values for both wildlife and people (e.g.,

wild flowers, pollinators, and game; Daily 1997a). Conventional agriculture, however,

still dominates human landscapes in the developed world, to the detriment of native

biodiversity. For example in the U.S., over 200 native species of resident and migratory

birds feed, roost, or breed on agricultural lands (Rodenhouse et al. 1993), but many of









their populations decline by 50% or more where expansive monocropping systems with

short rotation periods, heavy chemical inputs, and intensive mechanization reign

(O'Conner and Shrubb 1986, Rodenhouse et al 1993, Freemark 1995, McLaughlin and

Mineau 1995; bird declines in Europe see, Pain and Dixon 1997, Pain and Pienkowski

1997, Ormerod and Watkinson 2000).

Ecological research on farmlands would help the shift to ecologically sustainable

agriculture, but research to foster ecological integrity on farms is scarce (Cochrane 1993,

McNeely and Scheer 2002), despite numerous encouraging factors: 1) considerable

public interest, 2) diverse ecological values of farmlands, 3) an enormous area on the

earth's surface in which to work (950 million acres in the U.S.; USDA 1999), 4) global

biodiversity conservation needs to prioritize farmlands, because current parks and

reserves are insufficient and, 5) farmlands are relatively easy to restore to native

ecosystems (Askins 2000, McNeely and Scheer 2002). One reason for lack of interest in

conservation research in agroecosystems is that agriculture is a business and ecologists

have largely failed to show how biodiversity conservation and ecological functionality

can realize economic benefits for growers (Daily 1997b, McNeely and Scheer 2002). A

priority area of interest to growers has always been pest control. Whereas bio-control

programs focus primarily on invertebrate predators on pests, little work has been done to

integrate vertebrate species into row crop agricultural systems. In this study I assessed

the potential that native bird species could serve as effective predators of pests. I

examined factors influencing avian species diversity on North-central Florida farmlands

and, in particular, factors that increased insect-eating activity by wild birds in cropped

fields. Goals for this study were two-fold: 1) to assess overall avian biodiversity (species









richness and densities) on a selection of conventional and certified organic farms, and

identify farm characteristics (management and vegetative structural features) correlated

with bird diversity, and 2) to identify 'functional insectivores' among the bird species

utilizing farmlands (or, those species that we observed to feed frequently on insect prey

in cropped fields), and to identify farm characteristics (management and vegetative

structural features) correlated with the densities of functional insectivores in cropped

fields.

Study Design

Certified organic farming is defined as crop production without the use of most

conventional pesticides, synthetic fertilizers, sewage sludge, or bio-engineered food

plants (USDA 2002). Other works have shown that both birds and insect biomass can be

higher on organic, or low input, than conventional farms (birds: Christensen et al. 1996,

Chamberlain et al. 1999, Freemark and Kirk 2001, Beecher et al. 2002; insects:

Dritschillo and Wanner 1980, Hald and Reddersen 1990, Brooks et al. 1995, O'Leske et

al. 1997, Feber et al. 1997 & 1998). Therefore, in this investigation of factors affecting

bird diversity, abundance, and insect foraging paired sampling sites were selected on both

organic and conventional farms. In addition to censusing the bird community over 2

years (2000 and 2001), extensive foraging observations were conducted on individual

birds in cropped areas, and both field scale features (crop type, field border vegetation)

and type of matrix adjacent to each sampled field were characterized as predictors of both

bird diversity and foraging activity on the two farm types. I define functional

insectivores as bird species that were observed most commonly feeding on insect prey

taken from crop vegetation. All of my study species have been classified in the literature









according to well-established foraging guilds (e.g., frugivore, insectivore, omnivore)

based on their most typical or average annual diet composition across the US (De Graaf

et al. 1985). However, many birds' diets vary with season, and both typical frugivores

and omnivores can be highly insectivorous during breeding efforts (Beal et al. 1941,

Martin et al. 1951, Ehrlich et al. 1988). Therefore, rather than using 'typical' dietary

guilds to classify how birds might be interacting with insect pests, I wanted to know

which species were frequently out in fields eating insects during the spring growing

seasons on the farms studied. The most abundant of these insect-foraging species were

designated as functional insectivores or those most likely to consume insect biomass

with positive economic outcomes for farming operations.


Methods

Research Site Selection

With the aid of University of Florida Cooperative Extension agents, and following

farmer participation in surveys (see Jacobsen et al. 2003), local producers were contacted

to obtain permission for conducting research on their properties. A total of 30 census

points were established on certified organic farms during April of 2000, and a paired

reference site for each of these points on a nearby conventional farm was established (n =

60 total points, 10 organic and 10 conventional farm properties) in an effort to match crop

types, habitat structure, field border types, and matrix vegetation where possible (after

Rogers and Freemark 1991, Christensen et al. 1996, Chamberlain 1999). In 2001, one of

the organic farms sampled in 2000 was not planted, thus 5 fewer points were used in the

second year of the study. The 20 farm properties ranged in size from 4 to 104 ha located

within Alachua, Gilchrist, Marion, and Jefferson Counties of North-central Florida.









Patterns of Bird Diversity

Census surveys

Surveys were used to estimate bird species richness and density in cropped and

non-cropped habitats on farms. Birds were censused utilizing point count methods

described in Bibby et al. (1992) with modifications recommended by Freemark and

Rogers (1995) to suit agricultural landscapes. Sampling points of 50 m radius (fixed)

were situated on the border of cropped fields with non-cropped areas (Figure 2-1).

Census points were at least 200 m apart if they occurred on any single farm management

unit. All points were sampled a minimum of 4 times between 25 April and June 30 in

both 2000 and 2001, and order of visitation to sites in the pair (organic vs. conventional)

and the order of points visited on each farm management unit were reversed each visit.

Censuses were conducted between dawn and 1100 EST on fair weather days. All birds

seen or heard within the 50 m fixed-radius during a 10 min period were recorded.

Registrations were recorded and mapped onto two 1800 semi-circles (in the cropped field

and the un-cropped area after Freemark and Rogers 1995; Figure 2-1). By marking the

locations of individuals and noting their movements on maps this minimized the potential

of double counting individuals during counts. By censusing in this manner, I quantified

bird occurrences, both within cropped areas close to field edges and in adjacent non-

cropped habitats.

I began counting 2-3 minutes after arriving at each station. Birds occurring

outside of the circles or flying overhead were noted (see below) but excluded from point

count data, with one exception; I considered swallows or purple martins flying low (< 10

m above vegetation) over fields to be 'using' them (since they are likely to be foraging on















































Figure 2-1. Aerial view of a farm site in Alachua Co. illustrating 50 m radius point count
circle positioned on the edge of a cropped field where cropped field and field border
habitat type were characterized. Matrix type adjacent to each field was characterized
within a 200 m radius semicircle at each census point (after Freemark and Kirk 2001).









insects; see Boutin et al. 1999). Birds flushed within a count circle as an observer

approached or left a station were counted if they were not otherwise recorded during the

count period. If a flock was encountered, it was followed after the end of the sampling

period (if needed) to determine its composition and size. Because sampling occurred

during the breeding seasons only, singing males observed repeatedly during counts were

assumed to be paired breeders and were counted as two individuals (after Bibby et al.

1992). Walk-abouts were conducted in cropped and non-cropped areas on each farm unit

following point counts (Freemark and Rogers 1995). Only species not noted during the

formal point counts were recorded during walk-abouts.

Habitat classification: field-scale features and adjacent matrix type

Habitat characteristics associated with each census point were assessed at field

edges and in surrounding matrix (Figure 2-1; refer to Table 2-1). Field scale

characteristics of the farms were classified within each 50 m census point and included

whole-farm management type (certified organic or conventional), crop diversity (mixed

or mono crops), and field border habitat types (see Table 2-1). Matrix types that

dominated the immediate area adjacent to fields sampled were characterized within a 200

m (6.3 ha) radius semi-circle adjacent to the cropped field edge (see Freemark and Kirk

2001, Figure 2-1, Table 2-1). The dominant matrix type was identified as the one habitat

type covering the largest area within the 200 m semi-circle. Area of each matrix type

was measured within the semicircle plot utilizing ESRI ArcView software and the Xtools

extension package (Oregon Dept. of Forestry 2001) and 1999 digital ortho quarter-quad

aerial photos obtained from the Florida Department of Environmental Protection. Of the









Table 2-1. Predictor and response variables used in analyses. The representative scale of
measurement for each predictor variable is indicated in column 3. See text for clarification.


Variable Categories Scale
Predictor Variables
Year 2000
2001
Farm type Conventional Whole Farm
Organic Whole farm
Crop Mono 50 m radius census plot
Diversity Mixed 50 m radius census plot
Border type Crop 50 m radius census plot
Hardwood 50 m radius census plot
Hedge 50 m radius census plot


Pasture 50 m radius census plot
Suburb 50 m radius census plot
Pine 50 m radius census plot
plantation
Matrix type Crop 200 m radius semicircle
Hardwood 200 m radius semicircle
Pasture 200 m radius semicircle
Suburb 200 m radius semicircle
Pine 200 m radius semicircle
plantation
Response Variables
Density 50 m radius census plot


Species richness 50 m radius census plot Total # of species counted
Insect-foraging observed ** 50 m radius census plot Categorical (yes / no)
* 3 measures taken: whole point count circle, crop half, and field border half of circle.
** Only in crop half of point count circle.


Definition


Time (2 levels) included as
repeated measure in analyses
Conventional management
Certified organic management
Single crop species in field
2 or more crop species in field
Cultivated field in production
Broad-leaved trees > 5 m tall
Linear strip of woody
vegetation
Improved grassland: grazed
Residential development
Slash pine trees > 5 m tall


Cultivated field in production
Broad-leaved trees > 5 m tall
Improved grassland: grazed
Residential development
Slash pine trees > 5 m tall




Mean # of birds / ha









five matrix types (Table 2-1), the mean coverage for each primary matrix type was never

less than 62% (max 90%) of the 200 m radius semi-circle.

Determination of functional insectivores

In order to identify those species exhibiting the greatest potential as arthropod

pest predators in cropping systems a minimum of two 1-hour ad libitum foraging

observation sessions per census point were conducted during each of the two breeding

seasons (Robinson and Holmes 1982, Rodenhouse and Best 1994). Observations were

taken within the cropped portions of the 50 m fixed-radius point count circles. Foraging

data included identification of species observed to take invertebrate prey from crop

vegetation. Birds were determined to be insect foragers if they perched on, or flew low

over, crop vegetation while taking insect prey at least one successful prey capture had

to be observed for a bird to be designated as a forager. I then selected functional

insectivores, or those species most likely to have an impact on insect pests in cropped

areas, in the following manner from among the species documented to be taking insects

in cropped fields the ten species were picked that also occurred in the greatest densities in

the cropped areas (from point counts). The factors (field and matrix characteristics;

Table 2-1) associated with the highest recorded densities of the ten functional

insectivores were then assessed in cropped fields that were sampled (see Data Analysis).

Data Analysis

Bird diversity

Because of my initial expectation that farm management would influence avian

biodiversity, avifaunal differences between the organic and conventional farm sites

sampled was broadly assessed, including species lists, comparisons of total species









counts with Breeding Bird Survey data and Audubon Society occurrence data from

Alachua County (where most of the farms were located). Total species counts for each

farm were determined by totaling the number of species detected on point counts, species

noted inside cropped areas but outside the fixed radius during point counts, and species

detected during search surveys (walk-abouts for 30 min).

In order to determine how field and matrix characteristics influenced bird species

richness and density only point count data was used and analyzed in the following way.

The number of individuals and species counted in each circle was averaged over all

counts done in each circle in each year. Count data by crop versus field border portions

of each count circle were also separated out. Thus, for each count circle the following 6

response variables were derived: mean number of species per count circle, mean number

of species in the field border vegetation, mean number of species in crop vegetation;

mean density of birds per count circle (standardized to # of birds / ha), mean density of

birds / ha of field border, and mean density of birds / ha of crop. The three density

variables and the three richness variables were submitted to two separate repeated

measures multivariate analysis of variance (RM-MANOVA) with the following predictor

variables: year (as the repeated measure), farm type, crop diversity, border type, and

matrix type (Table 2-1).

Functional insectivory

Finally, to understand what farm-scale habitat features might influence

insectivory in cropped fields a univariate repeated measures analysis of variance

(RMANOVA) model was applied with the same predictor variables as above, and density

of birds (ten functional insectivore species only) detected only in the crop half of count









circles as the response variable.



Results

Bird Species Richness on Organic versus Conventional Farms

In statistical models of factors influencing species richness, farm management

(organic versus conventional) was never a significant predictor. However, on average,

more bird species were observed on (and unique to) organic than conventionally managed

farms (Figure 2-2, see Appendix A). A total of 64 different bird species were recorded in

point count censuses during the first field season (1 May 30 June 2000). Sixty species

were observed in or near organic crops, 49 in or near conventional fields, 45 were

common to both farm types, 4 were unique to conventional and 15 to organic systems.

Seventy-four species were counted in 2001 (25 April 30 June). Sixty-six of these

species were observed in or near organic and 58 in or near conventionally managed

fields, 52 species were common to both farm types, and 6 were unique to conventional

systems, and 14 to organic systems (see Appendix A). Together, the species observed

using farmscapes of North-central Florida represented 82 % of resident and migratory

landbird species listed as breeders in Alachua County (where most of our samples were

taken; Alachua Audubon Society 2003) and nearly all of those species noted in recent

Breeding Bird Surveys along the two routes monitored in the same county (USGS 2001a,

USGS 2001b; FFWCC 2003; Figure 2-2). I observed 24 listed species on organic farms

(18 state listed, 6 federally listed), and 18 listed species on conventional farms (14 state, 4

federal; see Appendix A). Of the five farms with the most bird species, 3 were organic

and 2 conventional. Finally, all 10 of the functional insectivore species (abundant insect-










100



90-



) 80-
C.
0
S70
E

60


50


40
6 ) o o
o Jo C
0 0 0 0





Figure 2-2. Number of landbird species known to breed in Alachua County, FL (Alachua
County Audubon Society 2003) and species documented on the two Breeding Bird
Survey routes (# 25013 and 25113; USGS 2001a, USGS b, Florida Fish and Wildlife
Conservation Commission 2003) compared to the number of species observed in organic
and conventionally managed farmlands of north-central Florida during the breeding
seasons of 2000 and 2001 (1 May 30 June, 25 April 30 June, respectively).









eating species observed in cropped areas) were observed in both organic and

conventional fields (see below).

Factors Influencing Bird Community Structure

Species richness

A RM-MANOVA model was constructed in the following way: year (2 levels) as

the repeated measure; mean number of species per point, per crop half, and per border

half of point count circles as response variables; farm type, crop diversity, field border

type, adjacent matrix type as categorical predictors; all main effects and 2-way

interactions were specified using Type III sum of squares. No within-subjects contrasts

(year effects) were significant (at alpha = 0.05), and only field border type had a

significant influence on species richness (per point; F5,30 = 3.5, P = 0.013, and field

border half of the count circle; F5,30 = 3.8, P = 0.009; see Figure 2-3 caption for multiple

comparison tests).

Bird density variation

Using the same RM-MANOVA model as above, with three different response

variables (mean densities of birds per point, per crop, and per border half of count

circles), again no effects of year were found, and only crop diversity significantly

influenced bird densities (per point; F1,30 = 7.4, P = 0.011, and per crop half of the count

circle; Fi,30 = 8.2, P = 0.008); fields with more than one crop type had higher bird

densities (Figure 2-4). All other factors and interaction terms were non-significant. I

noted that the two most abundant species sampled were Northern Cardinal and Northern

Mockingbird. Since these two species numerically dominated the data, and both are

known to be edge and disturbance associated (Ehrlich et al. 1988, Derrickson and

















12-






8-







41






0-
crop hardwood


hedge


* Per Point
* In Crop


pasture pineplan suburb


Field Border Type



Figure 2-3. Mean number of species detected per point, and in crop half of point count
circles (both years averaged). Error bars = 1 SE. Multiple comparisons tests (LSD)
indicate the following: hardwood and hedge borders generated significantly more species
per point than crop, pasture, or pine plantation borders (P < 0.03); hardwood borders
generated more species in crops than all other border types except hedges (P < 0.05), and
hedge borders generated more species in crops than pasture and pine plantation (P <
0.03).


0

0
.0


E
z
E
10
B










* Per Point
U In Crop


"""-


I II
mono
Crop Diversity


Figure 2-4. Mean densities of birds (all species) detected per point, and per crop half of
point (years combined) in mono-cropped and poly-cropped fields. Error bars = 1 SE.


mix
mix









Breitwisch 1992, Halkin and Linville 1999), I decided to re-run this analysis without

them to get insights about abundance variation of species with other kinds of habitat

associations. The same RM-MANOVA model was re-applied and again found no effects

of year but significant effects of crop diversity on densities of birds in crops (FI,29 = 10.5,

P = 0.003; higher densities in mixed crops). Border vegetation type was also found to

significantly affect densities per point (F5,29 = 3.8, P = 0.01) and in the crop (F5,29 = 4.1, P

= 0.006; see Figure 2-5 caption for multiple comparison tests), and there was a significant

interaction between adjacent matrix and field border vegetation types on bird densities in

the crop (F6.29 = 2.5, P = 0.044; Figure 2-6). Given that I did not have all combinations of

border and matrix types represented in my point count sampling, multiple comparisons

could not be run on the interaction. However, of the combinations sampled, the greatest

numbers of birds were observed in crops that were bordered by hardwood with adjacent

pine plantation matrix, bordered by hedge with adjacent hardwood, pasture, or pine

matrix, and in fields with pasture in both border and adjacent matrix (Figure 2-6).

Foraging activity in cropped fields: functional insectivory

After completing 2 h of foraging observations at each of the 60 census points each

year, I focused further sampling in each year on the 30 points with the most foraging

activity observed during the first two 1 h sessions (an additional 2 h of sampling at each of

30 points in each year for a total of 360 hours of foraging observations in cropped fields).

Of the 49 species of birds observed in or near conventionally managed crops during the

2000 breeding season, 14 species (29%) foraged in crop vegetation, and 23 of 60 (38%)

species on organic farms foraged in crop vegetation (see Appendix A). In 2001, 20 of 58

(35%) species on conventional and 36 of 66 species (55%) on organic farms actively















* Per Point
* In Crop


8-



V



a T
c


S2-






crop hardwood
crop hardwood


pineplan suburb


Field Border Type


Figure 2-5. Excluding Northern Cardinals and Northern Mockingbirds, mean densities of
all birds per point, and per crop half of point count circles, by field border type (years
combined). Error bars = 1 SE. Multiple comparisons tests (LSD) revealed the following
(P < 0.03): hardwood borders generated higher densities per point than all types except
hedge, and hedge generated higher densities per point than crop, pasture and pine
plantation. No multiple comparisons among border types for bird densities in crop half
of count circles were significant (although the main effect was).














12- Matrix Type
Scrop
11 hardwood
pasture
S 10 pineplan
,c *suburb
U 8--

17-

o 6-

5-

o 4

2-

I I


crop hardwood hedge pasture pineplan suburb

Field Border Type

Figure 2-6. Excluding Northern Cardinals and Northern Mockingbirds, mean bird
densities in crops given different combinations of field border vegetation type and
adjacent matrix vegetation type. Error bars = 1 SE.









foraged in cropped areas. In both seasons I noted that foraging activity was most common

in cropped areas with perching structures from which birds could survey for potential food

items. Densities of the ten functional insectivore species were significantly greater in the

crop half of census points that contained numerous perching structures (t = 6.13, p < 0.001,

N = 60). This was true whether the perch was manmade (e.g. an elevated sprinkler head)

or vegetative (e.g. sunflower or corn stalks) regardless of farm management type.

Of the ten functional insectivore species identified, only 4 are usually classified as

insectivores, one as a carnivore, and 5 of the ten species are normally considered

omnivores (De Graaf et al. 1985, see Appendix A), although all are known to be

insectivorous during the breeding season (Beal et al. 1941, Martin et al. 1951, Ehrlich et

al. 1988). Individuals of these species were observed to capture insects from crop

vegetation and either eat them immediately or carry them into adjacent matrix,

presumably to feed young. The two most abundant of the functional insectivores

(Northem Cardinals and Northern Mockingbirds; Figure 2-7) were also the most

abundant species overall (see above). Using a RM-ANOVA model (using the same

predictor variables and model structure as in the community structure analysis, above),

but only one response variable (mean densities of these ten species in cropped half of

count circles), no effect of year was found, and the only significant main effect was crop

diversity -mixed crop areas had more functional insectivores than monocrops (F.,29=

4.2, P = 0.051; Figure 2-8).












0.8 -



0.6

0

= 0.4 -



S0.2 -



0.0
blgr eabl inbu noca oror
brth gcfl losh nomo suta
Species

Figure 2-7. Mean densities of the ten functional insectivores observed in crop half of
census points. Species codes: blgr = Blue Grosbeak, brth = Brown Thrasher, eabl =
Eastern Bluebird, gcfl = Great Crested Flycatcher, inbu = Indigo Bunting, losh =
Loggerhead Shrike, noca = Northern Cardinal, nomo = Northern Mockingbird, oror =
Orchard Oriole, suta = Summer Tanager. Error bars = 1 SE.












A 5- I Crop Diversity
/ mixed
o0
> monocrop
15 4-


S-3-
to



4- 2

1-


I i
2000 2001
Year

Figure 2-8. Mean density often functional insectivores in fields with I (mono) or more
than 1 (mixed) type of crop planted, by year. Error bars = 1 SE.









Discussion

Avian Diversity on North-central Florida Farmlands

Avian species richness at census points (whole point and border half of count

circle) was strongly influenced by field border types, with hardwood forest and hedge

borders harboring the greatest diversity (Figure 2-3). This finding confirms the general

pattern that structurally complex windbreaks, hedgerows and field borders support more

complex farmland bird communities than conventional 'clean-farming' practices that

suppress non-crop vegetation (e.g. Osborne 1984, Green et al. 1994, Parish et al. 1994 &

1995, Chamberlain and Wilson 2000). Data analyses did not reveal any other field-scale

features or matrix types causing significant variation in the number of bird species

visiting the crop half of our point count circles. This is likely to be because the majority

of species attracted to habitats in fragmented farmscapes also utilize fields (see Appendix

A) and those few that do not utilize open fields are those that rarely come to the ground

(e.g., great homed owl, cedar waxwing, red-eyed vireo) or that have behavioral

limitations on entering open areas (e.g., Sieving et al. 1996).

Densities (species combined) of birds, however, varied significantly (among point

counts and in crop half of point counts) with border and matrix vegetation type and with

crop type. With or without Northern Cardinals and Northern Mockingbirds included in

the analysis, fields with mixed crops attracted greater numbers of individuals than mono-

crop fields (Figure 2-4), and when the two common generalist species were removed,

border and matrix habitat type also significantly affected bird densities in the crops and in

point count circles (Figure 2-5). Thus, removal of mockingbirds and cardinals was

important because as habitat generalists, their numerical dominance in our data could









have masked the responses of most species to the farmscape features we considered (see

Best et al. 1995). Hardwood and hedge field borders increased bird densities per point

(Figure 2-5; as they did number of species), and although it appears that hardwoods,

hedge, and pasture generated the highest densities in crops (Figure 2-5), the lack of

significant contrasts was probably due to: 1) the low densities of birds once the two most

abundant were removed and, 2) the significant interactions between border type and

adjacent matrix type.

Findings of this study support tentative generalizations emerging from larger scale

(landscape) analyses of bird distributions that have found blocks of hardwoods or natural

grassland adjacent to cropped areas tend to generate the highest bird diversity on

farmlands (Best et al. 1995 and 2001, Kirk et al. 2001), and that total area and

juxtaposition of vegetative cover types comprising recognizable farmscape elements

(field borders, windbreaks, etc.) largely determine bird densities in agroecosystems

(Freemark et al. 1993, Rodenhouse et al. 1993). Thus, this study emphasizes that, both,

the dominant vegetative communities in landscapes where farms and farm fields are

imbedded and the spatial configuration of habitat on farms determine bird species

diversity on farms. Farmers seeking to manage bird diversity do not have control over

landscape context (once a farm is purchased). But these results suggest that schemes to

design on-farm habitats (crops, field borders, and location of planted fields with respect

to adjacent matrix types) to influence bird diversity could be effective, very flexible, and

accommodate different classes of birds (i.e. woodland, grassland, edge, generalist

species) and, therefore, be excellent tools for avian conservation in agroecosystems (see

below).









Bird Diversity on Organic versus Conventional Farms of North-central Florida

In apparent contradiction with other studies in North America (Freemark and Kirk

2001, Beecher et al. 2002) and Europe (Christensen et al. 1996, Chamberlain et al. 1999)

that documented significantly greater bird diversity associated with organic farming

practices, I detected only slight enrichment of bird diversity in organic versus

conventional farming systems of North-central Florida. In fact, most species that could

be expected in North-central Florida during the breeding season were observed utilizing

the farmscapes I studied, regardless of farm management (Figure 2-2). This contradiction

derives from differences in cropping practices on the farms studied by others, and in the

scale at which studies were conducted. In the other studies, birds were surveyed

primarily in farms with mono-cropped fields mixed crops were uncommon and

variables similar to our 'crop type' predictor were not incorporated into analyses. As an

a prior variable in analysis models, crop diversity proved to be a very strong predictor of

bird density. Since both conventional and organic farmers in my sample employed mixed

and mono crops, differences in bird occurrence generated by chemical applications may

have been insignificant by comparison. Moreover, both organic and conventional farms

in North-central Florida are relatively small (10 out of 16 were less than 10 ha) compared

to farms used in other studies that spanned a considerable size range (from a minimum of

10 -40 ha to much larger). North-central Florida is still largely forested, and because

farms were relatively small, most farm fields were close (or adjacent) to significant areas

of hardwood forest the habitat that generated the highest farm-bird diversity in this

study. The current landscape is likely to represent a 'patch mosaic' of diverse habitat

types long recognized as essential for the maintenance of bird (and other) species on









farmlands (birds; O'Conner and Boone 1992, Best et al. 1995: plants; Freemark et al.

2002: moths; Ricketts et al. 2001: ants; Perfecto and Vandermeer 2002). Thus, I

speculate that in farming regions with larger farms (and larger farm fields), where sources

of birds are more distant and mixed cropping is less frequent, organic farm practices may

be more important in determining species diversity than in landscapes with small-scale

farms and a diverse habitat mosaic.

Functional Insectivory in Cropped Fields

I found that birds were willing to utilize cropped fields to forage at most census

points regardless of crop type or management. However, in both years, fields planted

with polycultures attracted the greatest densities of the ten functional insectivore species,

compared to monocropped fields, regardless of other factors (Figure 2-8). The most

attractive fields in this study had vegetable and cut flower intercrops, followed by

multiple vegetable crops, and monocropped systems had the fewest birds; monocropped

watermelon was the least attractive crop. These results are similar to those of Robbins et

al. (1992), Rodenhouse and Best (1994), and Stallman and Best (1996) where avian

diversity, abundance, and foraging activity were strongly associated with increased

structural complexity of vegetation in cropped fields. In general, birds can rapidly assess

within-habitat variation in food availability (Fretwell and Lucus 1970, Hutto 1985) and

will quickly recruit to feed in food-rich patches. Since insect species richness and

diversity increase with vegetation diversity in cropped fields (Elliott et al. 1998) and are

greater in polyculture verses monoculture systems (reviewed by Andow 1991), the

increased functional insectivore foraging activity 1 observed in mixed crops verses

monocultures was probably driven by variation in arthropod prey resources (though I did









not quantify this). Because organic fields tend to support greater arthropod diversity and

density (Dritschillo and Wanner 1980, Hald and Reddersen 1990, Brooks et al. 1995,

O'Leske et al. 1997, Feber et al. 1997 & 1998), and because high bird diversity in organic

fields has been linked to richer arthropod foods (Brea et al. 1988), the lack of a

significant difference in bird diversity between organic and convention fields in this study

suggests that polyculture cropping in conventional systems also results in an overall

greater arthropod diversity and abundance (Paoletti et al. 1992, Stary and Pike 1999).

One important determination I made during this study is that without watching

what birds eat when they are in fields, farmers and researchers alike may mistake the

roles that different species play. Because a few birds can be significant pests in

agroecosystems, eating sprouted plants, seed crops, and ripening fruits (Weed and

Dearborn 1935, Beal et al. 1941, Dolbeer 1990, Rodenhouse et al. 1993), this role is often

the first one ascribed to any birds observed in cropped areas. In this study I observed

abundant insectivory and only isolated instances of fruit damage (by mockingbirds on

strawberries) by birds in my study fields. But while many of the species observed to take

insects are normally classified as insectivores, several of the functional insectivores are

not. The Northern Cardinal is usually classified as an omnivore (De Graaf et al. 1985)

and popularly known as a seed-eater because it frequents backyard bird feeders. Yet the

cardinal was the most abundant functional insectivore in this study. They made longer

foraging bouts and took more insects than other species, and either immediately

consumed them or carried them into nearby field margins (presumably to feed young).

Two other species typically classified as omnivores (or popularly thought of as

granivores), blue grosbeaks and indigo buntings, were also among the functional









insectivores (top ten most common species in cropped fields taking insect prey; see

Appendix A, Figure 2-7) and caused no crop damage during our observations. Clearly,

these species are omnivores when the diet is summarized over an entire year. But

because many omnivores and primarily granivorous species become highly insectivorous

during the breeding season to support their energetic needs and those of their nestlings

(Beal et al. 1941, Martin et al. 1951, Ehrlich et al. 1988), I advocate the utility of

'functional insectivore' in the context of farm birds. If the seasonality of bird diets is

emphasized, then farmers and conservationists alike can make more careful, and more

accurate, assessments of the potential positive and negative interactions birds can have

with cropping systems.

In conclusion, I found a large number of insectivorous bird species utilize cropped

fields of North-central Florida (see Appendix A), and direct observations during foraging

bouts indicated that most of these species were actively capturing insect prey from crop

vegetation. Insectivorous birds exhibit numerical and functional responses to insect

outbreaks in North American forest systems, potentially decreasing pest outbreak

frequency and severity (Holling 1988, Dahlston et al. 1990, Holmes 1990). This work

supports the general assessment that the ecological role of birds, as insect predators in

agroecosystems, is likely to realize enhanced production and economic values to farmers.

Moreover this work, in light of the current dearth of studies attempting to document

economic and production benefits of natural pest control agents, begs for further

investigation of avian insectivory as a component of pest management schemes that are

consistent with ecologically sound agriculture (Jackson 1979, McFarlane 1986 and Kirk

et al. 1996).









Conservation Implications

Increased awareness of the functional role that insectivorous species may have in

cropping systems could further encourage producers to engage in avian conservation

efforts on their lands. Recent surveys of farmers in North-central Florida indicated they

were supportive of increasing populations of certain bird species if it would benefit their

production efforts (i.e. insectivorous birds that may eat insect crop pests; Jacobson et al.

2003). Encouragingly, an overwhelming majority of farmers surveyed believed birds

could help lower insect populations on their farms (91%). Most farmers also indicated

that they would like to attract such birds to their farms (85%), and over a third of these

farmers were already engaged in attracting birds to their farms (Jacobson et al. 2003).

Additionally, since farmers in Florida have expressed great interest in conservation of

birds if they can aid in control of insect pests (without causing crop damage; Jacobson et

al. 2003), the potential for integrating bird conservation with farm production is

encouraging, particularly if more research is devoted to assessing realized benefits to

farmers. This work suggests that functional insectivory in fields can be encouraged at the

farm scale (by land-owners) by planting polycultures in fields adjacent to blocks (matrix)

of hardwood and pine forest with structurally complex field borders (hardwood, hedge)

between the matrix and the crop. It was also observed that insect eating birds heavily

utilized elevated perch structures (irrigation pipes, sprinkler heads, wire fence posts,

trellises, and natural structures such as sunflowers, cornstalks, bushes, and trees).

Though I did not characterize these effects, perches to enhance bird activity in disturbed

areas appears to be effective in many systems (Holl 1998). My next steps are to pursue









an understanding of economic benefits of on-farm manipulations of functional

insectivores.

While farmers cannot readily manipulate the relative abundance of land cover and

land use at the landscape scale surrounding their farms, it is quite clear that farms in

landscapes with greater proportions of their original native habitats will be able to attract

more birds, in part because larger pools of species and individuals are supported in such

landscapes. It is also apparent that such landscapes generate complex mosaics at the farm

scale, unlike regions with large (corporate) conventional fanning operations adjacent to

one another. Because most recent studies of bird diversity on farms in the U.S. have

occurred in expansive conventional systems of the Midwest (see Best et al. 1995, Best et

al. 1997, Beecher et al. 2002) and California (see Elphick and Oring 1998, Bird et al.

2000), where there is little habitat (and impoverished avifaunas that often cause crop

damage), and because such conventional corporate farms comprise most acreage in

agricultural use, the current view of integrating birds and agriculture is somewhat

pessimistic (Peterjohn 2003). Numerically, mostfarms in the US are small to medium

sized traditional operations occurring in landscapes with a mosaic of crop and non-crop

habitat elements (ERS-USDA 2003), like the farms in this study. A recent national study

found the average small farm devotes 17% of its land to forest patches compared to 5%

on large farms, and allocates nearly twice the acreage to soil improvement efforts such as

cover crops (D'Souza and Ikerd 1996). Additionally, non-cropped acreage or acreage set

aside for conservation purposes is substantial among small farms in the U.S. For

example small family farm operators controlled 85% of acres enrolled in the

Conservation Reserve Program as of 1998 (USDA 2001b). Given that many of the small









farms surveyed in North-central Florida appear to provide suitable habitat for a diversity

of species, and that these farmers' attitudes toward avian conservation are positive, I

argue that the prevailing negative view of agriculture as a partner in biodiversity

conservation is counter-productive. Large-scale conventional farming operations that

dominate large regions and comprise the majority of farmed areas in the US are, indeed,

devastating to birds and native biodiversity in general. But studies, including mine,

indicate that most farms (the smaller operations in diverse landscapes) already support

significant avian (and other) biodiversity, in part, because most farmers are open to

fostering such conservation goals. Therefore, I am encouraged that the potential to alter

agriculture in positive ways is tremendous. Policies are in place that provide monetary

and other incentives (i.e. 2002 Farm Bill conservation programs), and most stakeholders

are apparently open to possibilities (Jacobson et al. 2003), and the kind of research

needed to establish an economic basis for more ecologically sound agriculture is known

(McNeely and Scheer 2003).















CHAPTER 3
INTERCROPPING WITH SUNFLOWERS TO CREATE LOCAL
REFUGIA FOR AVIAN PREDATORS OF ARTHROPOD PESTS

Introduction

Innovative crop protection, through enhancement of predator-prey

relationships characteristic of natural systems, has a pivotal role to play in the

evolution of agriculture towards environmentally sustainable systems (Atkinson and

McKinlay 1997). Methodologies that promote pest insect predators (e.g., birds, bats,

wasps, beetles) on farms can augment both non-chemical crop protection and

conservation of biological diversity in agricultural landscapes. Although the value of

native insectivorous animals as predators in agroecosystems was once widely

recognized and promoted by scientists and farmers, research on potentially beneficial

species inhabiting agroecosystems was largely abandoned in 20"h Century North

America due to the pervasive use of pesticides and related technologies. As sectors

of the agricultural industry explore lower input systems (e.g., organic farming, natural

systems agriculture; Colby 1990) to reduce destructive impacts on human health

(www.epa.gov/pesticides/citizens/riskassess.htm) and ecosystem functions (Altieri

1994), research focused on designing farming systems that emulate more complex

ecosystems is urgently needed. Efficient and sustainable agro-ecosystems will

support ecosystem functions and species composition that reflect local biotic and

abiotic conditions (Soule and Piper 1992, McNeely and Scherr 2003). Thus, research









on sustainable and ecologically sophisticated agriculture should develop designs

appropriate for local conditions and sets of species, in addition to general principles

of agroecosystem function and management (Lewis et al. 1997).

Biological control by natural enemies has been the most successful and

promising alternative to unilateral reliance on chemical pesticides (Hoy 1992, Zalom

et al. 1992), and is considered to be the 'backbone' of integrated pest management

schemes (Rosen et al. 1996). The economic value of biological control methods

included in integrated pest management (IPM) programs may be considerable over

long time periods. For example, a study of citrus production in the San Joaquin

Valley of California indicated substantial savings of pesticide and energy costs could

be realized by growers utilizing IPM methodologies (Flint 1992). Biological control

methods that promote native pest insect predators for non-chemical crop protection,

by their nature, also contribute to conservation of biological diversity in agricultural

landscapes (The Soil Association 2000).

Habitat Management for Predators in Agroecosystems

Habitat management to enhance biological control refers to the establishment

of environmental conditions amenable to natural enemies that increase and sustain

their populations and improve their effectiveness in controlling pests (Pickett and

Bugg 1998). Population processes such as colonization / dispersal and foraging

movements of predators can be influenced by habitat modifications (Helenius 1998).

On farms, such dynamics of natural enemy populations can be altered through

management of within-field strips, cover crops, field margins, hedgerows, fencerows,

windbreaks, irrigation and drainage ditches, and roadside margins. For example,









Nentwig (1998) found that sown weed strips within cropped areas increased

arthropod enemy abundance and activity in crops, via greater effective dispersal into

the interior of expansive fields. Moreover, predation rates on pest species were

higher near the sown strips. Others have recognized the potential importance of

predator refugia within farmed areas for pest control and call for better understanding

of the mechanisms underlying refugium design and function for managing natural

enemies (Schoenig et al. 1998, Wratten et al. 1998).

Clearly, agroecological infrastructure (e.g., the landscape context and within-

field structure of cropped areas) affects the maintenance and activity of predators at

the scale of individual fields, and the conservation of predator diversity (richness and

abundance) requires consideration of both favorable and unfavorable habitat aspects

when designing predator-friendly agroecosystems (Booij and Noorlander 1992,

Wratten et al. 1998). For example, studies of abundances and foraging activities of

insectivorous birds in cropped systems (reviewed by Kirk et al. 1996) suggest that

bird use of crops for foraging depends not only on food abundance, but also upon

vegetation cover and microclimate in the field (Rodenhouse and Best 1994) and upon

habitat composition in the surrounding landscape (see Chapter 2).

Objectives

This study investigates the effect of within-field habitat structure upon the

abundance and foraging activity of insectivorous birds in cropping systems where all

features are under the direct control of farmers. The occurrence, densities, and

foraging activities of insectivorous birds in cropped fields are significantly higher in

those having the greatest diversity of vegetation (polycultures vs. monocultures; see









Chapter 2). Therefore, the overall objective of this study was to examine the effect of

sunflowers (Helianthus annuus) within cropped fields as refugia for birds. I tested

the hypothesis that sunflower rows included in a cropping system would increase the

occurrence, density, and foraging activity of insectivorous birds in cropped fields.

Additionally, I varied the density of sunflower rows per unit-area to determine its

influence on bird behavior and distribution in cropped fields. I conducted

observational assessments of foraging activity budgets of insectivorous bird species

utilizing cropped fields with sunflower rows compared to control plots. Using visual

observations I attempted to verify if birds were consuming economically important

pest insects. Forced regurgitation gut samples were collected from a few birds

captured in mist nets after they foraged in crop vegetation to aid in this verification.

Insects found within regurgitate samples were identified to order and family.

The addition of sunflowers to attract beneficial insects into cropping systems

has been described in several extension fact sheets (Univ. of Florida Extension

Circular 563, Univ. of Rhode Island Landscape Horticulture Factsheet, Univ. of

Maine Coop Extension Bulletin # 7150) and gardening publications (Long 1993,

Starcher 1995, Turton 1998). However, one concern with adding non-crop vegetation

strips within cropped fields is that this treatment may attract and increase the

abundance of pest insects to the crops (Bugg and Pickett 1998). Therefore, I also

performed a limited survey of the insect fauna found in sunflower treatment plots to

establish a partial listing and the relative occurrences of both beneficial and pest

arthropods found on sunflower and nearby crop vegetation (sensu Henn et al. 1997

and the UF Coop. Ext. Service Insect Identification Sheets SPSET 5 1997).









Methods

Research Site Selection

Growers were identified in North-central Florida during the fall of 2001 and

permission was obtained to conduct research activities on their properties. All

participating farms were under certified organic management as designated by the

Florida Organic Growers Association (Florida Certified Organic Growers and

Consumers, Inc., PO Box 12311 Gainesville, FL 32604) and most are now USDA

Organic certified.

Experimental Design

Four organic growers were asked to incorporate rows of multi-branched open-

pollinating varieties of sunflowers into their cropped acreage at the earliest planting

dates during their spring summer growing seasons 2002 and 2003. These multi-

branched sunflowers have been observed to provide foraging, roosting, and even

nesting micro-habitat for many species of insectivorous birds in two organic farms

that already incorporate them extensively for cut flower production (Jones

unpublished data). Vegetable crops grown in the experimental blocks chosen for the

study included polycultures of kale, collard greens, yellow and zucchini squash,

tomatoes, green beans, cucumbers, and sweet corn. Only two of the farm sites had

entire fields dedicated to a single crop type (sweet corn).

A total of 18, 4-hectare blocks were available for the study 8 of which

received sunflower row treatment while the other 10 served as controls within the

farm sites. This unbalanced arrangement of 8 treatment and 10 control blocks was

necessary to ensure that each farm contained at least 1 control and treatment block, to









pair crop types in treatment and control blocks as much as possible, and to allow the

incorporation of sunflower rows into blocks in such a way as to minimize their impact

on each farmer's production regime. Treatment blocks were divided among farms

that ranged in size from 8 ha to 80 ha in size with 2 blocks in the smallest farm, 4

blocks in each of 2 farms that were 20 ha in size, and 8 blocks in the largest farm. A

randomized block design was incorporated into the 4-hectare plots with sunflower

row treatments at varying densities of 0, 1, or 2 rows per 0.4 ha. All sunflower rows

consisted of Im-wide rows of plants at a density of 9 plants per square meter and

were interspersed between, and parallel with, production rows (Figure 3-1). In all

blocks that had sunflower rows placed in them the rows were centered in roughly

rectangular fields, planted in strips that would not otherwise have had crop

vegetation, and were approximately 100 m in length (Figure 3-2).

Sunflower rows were maintained throughout the spring growing season as other crops

were planted, harvested, and rotated through each farm's production area. Treatment

blocks were assigned different treatments during the second field season (either 1, 2

or no rows/0.4 ha of sunflowers) to control for differences in the border habitat types

that were adjacent to each treatment block. This was important since border habitat

types significantly affect the numbers of birds available to venture into cropped

fields. Avian occurrence and abundance in field borders varied significantly from site

to site being greatly influenced by the vegetation composition of the field border (see

Chapter 2).
















































Figure 3-1. Multi-branching sunflower varieties were planted at 1 or 2 rows per 0.4
ha between vegetable rows to attract birds and beneficial insects into cropped fields.
A row of sunflowers is shown here planted in a non-production strip containing
irrigation sprinklers between rows of tomatoes.















































100 m


Figure 3-2. Typical layout of treatment and control blocks at a 20 ha farm site. A
randomized block design was incorporated into the 4-hectare plots with sunflower
row treatments at varying densities of 0, 1, or 2 rows per 0.4 ha. All sunflower rows
consisted of Im-wide rows of plants at a density of 9 plants per square meter and
were interspersed between, and parallel with, production rows. In all blocks that had
sunflower rows placed in them the rows were centered in roughly rectangular fields,
planted in strips that would not otherwise have had crop vegetation, and were
approximately 100 m in length.









Bird Sampling

Birds were censused and their foraging activities quantified throughout the 2

growing periods from 1 April 15 June 2002 and 2003. Birds were censused 6 times

in each treatment and control block utilizing standard point count methods (Bibby et

al. 1992) modified as described by Freemark and Rogers (1995) for censusing in

croplands. All census points were located at least 200 m from each other when

occurring within the same farm management unit. Point counts were conducted

between dawn and 1000 EST on fair weather days. All birds seen or heard within a

50 m fixed-radius from each census point during a ten-minute period were recorded.

Observations began 2-3 minutes after 1 arrived at each point count station. Birds

flying over sample areas were excluded, except swallows or martins if they were

feeding on aerial invertebrates directly over crop vegetation (see Boutin et al. 1999).

Utilizing mapping data sheets (marking exact locations of individuals and their

movements) minimized duplicate records. Both species numbers and bird densities

were averaged across samples at each point. Univariate analyses were performed to

compare bird densities within the treatment and control blocks to determine

sunflower row treatment effects upon bird response variables among experimental

plots for the study (Zar 1999).

Point count circles used to assess bird species occurrence and density were

located on the edges of fields centered to the ends (1 sunflower row plots) or between

(2 sunflower row plots) sunflower rows in treatment blocks, V2 in the field and /2 in

the field border vegetation (Figure 3-2). For comparisons among treatments and

control blocks, only birds detected in the crop half of count circles were used in









assessing species occurrence and density. Count circle radii extended V2 the length of

the sunflower rows, and were therefore sufficient to detect sunflower effects on birds.

Half of each count circle was located in the field border vegetation for two reasons.

First, standing in the border provided some cover to reduce the conspicuousness of

the observer (and minimize effects on bird behavior in the crop). Second, all census

points in this study were censused in the 2 years previous to this study and those data

were used to assess variation in bird abundances in cropped field blocks among years

and treatments.

Foraging Surveys

Observations of foraging behavior were made during six, I-hour scan

sampling sessions (Martin and Bateson 1993) at each treatment plot spread over the

study period. Avian species observed to forage in crop vegetation and the time spent

in foraging bouts were noted. Birds were considered foraging if they were observed

to be making their way through or on crop vegetation and actively scanning or

probing that vegetation for prey items (as opposed to being perched and resting,

singing, or grooming etc.). Any successful capture of an insect prey item was noted

and an attempt was made to visually identify those insects being consumed by

foraging birds. Use of sunflower plants by foraging species was described. The

degree that inclusion of sunflower rows increased foraging activity in surrounding

crop vegetation was determined by univariate analysis of variance comparing

differences in mean numbers of birds and duration of foraging bouts among treatment

blocks. Regression analysis was used to examine the relationship between foraging

activity and growth of sunflower plants through each growing season (Zar 1999).









Gut Content Surveys

An attempt was made to identify insects eaten by insectivorous birds within

the test plots through gut content analysis. Birds were captured directly after foraging

in crop vegetation utilizing mist-netting techniques within treatment plots. A partial

sample of each bird's stomach contents was collected via a non-lethal forced

regurgitation (Prys-Jones et al. 1974). After capture, birds were administered an oral

emetic consisting of a 0.1 cm3 of 1% solution of antimony potassium tartrate per 10 g

of body mass and placed in a darkened holding cage lined with wax paper. Within 2

- 3 minutes, most birds regurgitated pellets of partially digested insects that were then

collected and preserved in alcohol for identification. Birds were then released at

point of capture after a short rest period and an examination for any signs of stress.

Samples obtained in this way are highly correlated with total crop and stomach

contents of collected birds (Rosenburg and Cooper 1990).

Insect Surveys

Insects were sampled a minimum of 3 times in 10 randomly chosen 1 m2

quadrats within sunflower rows and in 10 randomly chosen locations in crop

vegetation a minimum of 10 m distant from the sunflower rows within treatment

blocks during the growing season 2002. During 2003 insects were again sampled a

minimum of 3 times in 10 randomly chosen 1 m2 quadrats within sunflower rows, 10

quadrats in crop vegetation at 1 m, and 10 quadrats at 10 m distant from the

sunflower rows. Insects were sampled utilizing a standard scouting technique in each

quadrat counting the numbers of individuals found per 1 m2 of crop vegetation (after

Morris 1960, Southwood 1978). Insects observed were identified to family level and









relative abundances noted. Using Henn et al. (1997) and the UF Coop. Ext. Service

Insect Identification Sheets SPSET 5 (1997), I classified insects as beneficiall" or as

crop pests. Then, I compared the occurrence and number of individuals per m2

beneficial and pest insects found upon sunflower plants and crop vegetation (at 2

distances away from sunflowers in year 2) during the two growing periods (Zar

1999).



Results

Bird Species Occurrence and Densities

A total of 68 species were observed utilizing cropped areas of the treatment

and control blocks or their bordering habitats (within 50 m of field edges; see

Appendix B). Of these 68 species observed within the blocks, 62 species (91%) were

observed in the border habitat while 49 species (72%) were observed in the cropped

areas themselves; 5 of which were only observed in the cropped fields. Mean

densities of birds occurring in the cropped areas of the treatment and control blocks

varied significantly from year to year during the study and from the two years (2000

and 2001) previous to the study (2.9 birds/ha in 2003, 3.3 birds/ha in 2002, 4.3

birds/ha in 2001, and 1.8 birds/ha in 2000; F,3.34 = 2.74, p = 0.04). During the study

cropped areas with sunflower treatments of one row and two rows per 0.4 ha

exhibited significantly greater mean densities of birds than did control plots (3.5 3.5,

5.8 4.5, and 0.9 1.8 birds/ha respectively; F2.20 = 43.33, p< 0.001). This difference

was apparent with the addition of just a single row of sunflowers per 0.4 ha (Figure 3-

3). Differences in bird densities between treatment and control blocks were greatest









in 2003 (2-way ANOVA Year x treatment F,2, = 4.41, p = 0.013) during which

blocks having 2 sunflower rows per 0.4 ha exhibited a 206% greater mean density of

birds than did 1 row and a 1500% greater mean density of birds than did control plots

(Figure 3-3). Mean bird densities occurring in cropped areas were not significantly

different among these same blocks in the two years previous to this study (2000: F.5,

=.843, p = 0.436; 2001: F253 = 1.41, p = 0.254).

Foraging Behavior

Foraging observations during the 2 growing seasons indicated that the presence of

sunflower rows significantly increased the presence and activity of insectivorous

birds in vegetable or row-crops compared to control blocks. Mean number of

individual birds foraging per hour in cropped areas was significantly greater in those

blocks with sunflower rows versus control blocks, 0.7 0.1 and 1.7 0.1 individuals

per hour respectively (Fj.1 = 59.84, p < 0.001; Figure 3-4). Mean foraging activity

per hour in cropped areas was also significantly greater in those blocks with

sunflower rows versus controls, 0.06 1.01 hr and 0.24 .02 hr respectively (F1.i =

51.93, p < 0.001; Figure 3-5). This difference in foraging activity was consistent

each year as treatment plots were rotated among the 18 experimental plots. Mean

time birds spent foraging in crop vegetation significantly increased over the course of

each growing season as both sunflowers and crop vegetation matured (F,. = 9.13, p =

0.003). Birds were found to be attracted to and utilize sunflower plants as perches by

the time they were 0.6 m tall. As sunflowers increased in stature through the growing

season, birds were observed to increasingly utilize sunflower plants as cover and

perch sites from which they would forage into crop vegetation (Figure 3-6).















: ar
8.00 2002
2003
.5
*E 6.00


4.00 -
r &
c 2.00


0.00 -


Control


I
Sunflower
(1 row / acre)


I
Sunflower
(2 row / acre)


Figure 3-3. Sunflower treatment plots exhibited significantly greater mean densities
of birds in the cropped fields than control plots during both spring growing seasons
(F2.o = 43.33, p< 0.001), and especially in 2003 (2-way ANOVA Year x treatment
F2,20 = 4.41, p= 0.013). This difference was apparent with the addition of just a
single row of sunflowers per 0.4 ha increasing mean density nearly 4 times that of
control plots. Error bars = 1 SE.












year
SU 2002
'i*r 2003
S1.50 -
o







S o0.50 -



0.00 -
Control Sunflower




Figure 3-4. Mean number of individual birds foraging in cropped areas was
significantly greater in those plots with sunflower treatments in both growing seasons
2002 and 2003 (FI.t96 = 59.84, p < 0.001). Error bars = 1 SE.













ear
2002
2003

0.20"
I..


I-

". 0.10-
C




0.00 0 ......--...-

Control Sunflower



Figure 3-5. Mean foraging time (proportion of 1 hour observation session) in cropped
areas was significantly greater in those plots with sunflower treatments in both
growing seasons 2002 and 2003 (F,,x = 51.93, p < 0.001). Error bars = 1 SE.
















































Figure 3-6. As sunflowers increased in stature, birds were observed to increasingly
utilize sunflower plants as cover and perch sites from which they would forage into
crop vegetation. An Eastern Kingbird (Tyrannus tyrannus) surveys crop vegetation
from a sunflower perch looking for prey.









During the 216 hours of foraging observations made during the study period a

total of 428 foraging bouts were observed. The species most often observed to forage

in crops for insects included 2 resident species Northern Cardinals (Cardinalis

cardinalis) and Eastern Bluebirds (Sialia sialis), and two migrants, Blue Grosbeaks

(Guiraca caerulea), and Indigo Buntings (Passerina cyanea)(see Appendix B).

These four species accounted for 63% of the foraging bouts observed and 65% of the

time birds were observed to forage in the treatment and control blocks during the

study (Figure 3-7). Northern Cardinals were the most prevalent foragers throughout

each growing season accounting for more than 1/3 of the foraging bouts observed.

Eastern Bluebirds were also common foragers accounting for 8.6% of the foraging

bouts observed. Blue Grosbeaks and Indigo Buntings became common foragers (7%

and 9% of foraging bouts observed respectively) as they returned from wintering

grounds several weeks into the two growing seasons. Small flocks of species that

winter in North-central Florida such as Western Palm Warblers (Dendroica

palmarum) and Yellow-rumped Warblers (Dendroica coronata) were observed

foraging in cropped areas during the first few weeks of each growing season.

In approximately 10% of the foraging bouts I was able to identify an insect

prey item that had been captured. Two of the most common prey identified were

lepidopteran larvae and grasshoppers. Inspections of crop vegetation after bouts, in

spots where birds had foraged, allowed further confirmation of likely prey species

being consumed. Insects most prevalent in inspected foraging sites included Green

Stink Bugs (Acrosternum hilare), Imported Cabbageworm (Pieris rapae Linnaeus),

and numerous Dipterans (Figure 3-8).











a. Foraging bouts


BLGR
70%
COGD



I -







" : : ,


b. Foraging time


BLGR










INBU
8.7%


Figure 3-7. Species-specific proportion of foraging bouts (a.) and time spent foraging
per hour (b.) of birds observed during 216 hours of observation in sunflower and
control blocks during the 2002 and 2003 spring growing seasons. Northern Cardinals
(Cardinalis cardinalis), Eastern Bluebirds (Sialia sialis), Blue Grosbeaks (Guiraca
caerulea), and Indigo Buntings (Passerina cyanea) accounted for 63% of the foraging
bouts observed and 65% of the time birds were observed to forage in the treatment
and control blocks during the study. See Appendix B for complete list of those
species observed foraging in crops.


YRWA
47%
WPWA
68%






NOCA
38.3%


Other














NOCA
35.7%















































Figure 3-8. Birds foraging in crop vegetation were observed to consume numerous
lepidopteran larvae as well as grasshoppers and beetles. Insects consumed by birds
included Green Stink Bugs (Acrosternum hilare), Imported Cabbageworm (Pieris
rapae Linnaeus), and numerous Dipterans.









Insects were taken directly from crop vegetation and either consumed on the spot or

carried into nearby field border habitat (presumably to be consumed there or to feed

to young). A total of 20 birds observed to forage for insects in crop vegetation (10

Northern Cardinals, 3 Blue Grosbeaks, 6 Indigo Buntings, and 1 Summer Tanager)

were captured immediately after foraging. Regurgitated gut samples obtained from

12 of these captured birds confirmed that economically important pest insects were

consumed such as leaf-chewing caterpillars and grasshoppers (Figures 3-9). Remains

of beneficial insects were not evident in these gut samples.

Beneficial and Pest Insect Occurrence

Beneficial insects were attracted to sunflower plants by the time they reached

0.15 m in height. Beneficial insects observed on sunflowers and nearby crop

vegetation (within 1m of sunflowers) included arthropod predators, parasitic wasps,

and important pollinators representing 30 different families (Appendix C). The most

commonly occurring beneficial insects observed on sunflowers were Big-eyed Bugs

(Geocoris ssp.), Honey Bees (Apis mellifera), Green Lynx Spiders (Peucetia

viridans), Ants (Formicidae), and Sphecid Wasps (Sphecidae). The most commonly

occurring beneficial insects observed on nearby crop vegetation were Green Lynx

Spiders (Peucetia viridans), Lady Beetles (Coccinellidae), Big-eyed Bugs (Geocoris

ssp.), Predatory Stink Bugs (Pentatomidae), and Assassin Bugs (Reduviidae). The

occurrence of beneficial insects was significantly greater on sunflower vegetation

than on crop vegetation greater than 10 m distant from sunflowers in both 2002 (Fl.16

= 11.78, p = 0.003; Figure 3-10) and 2003 (Fi.6 = 12.94, p = 0.002; Figure 3-11).

While crop vegetation 10 m distant from sunflowers harbored significantly fewer





















































Figure 3-9. Gut content samples obtained from birds captured after foraging in crop
vegetation confirmed that economically important pest insects were consumed such
as leaf-chewing caterpillars. The intestinal tracts and other internal organs of
numerous caterpillars were identifiable in most stomach samples.









While crop vegetation 10 m distant from sunflowers harbored significantly fewer

beneficial insects, this difference in occurrence in sunflower and crop vegetation was

not seen in crop vegetation directly adjacent to sunflowers (within Im) when this was

assessed during the 2003 growing period (F,22 = 2.29, p = 0.144; Figure 3-11).

Pest insects representing 12 different arthropod families were found on

sunflowers and nearby crop vegetation. The most commonly occurring pest insects

were Green Stink Bugs (Acrosternum hilare), Corn Flea Beetles (Chaetocnema

pulicaria, Chrysomelidae) and Imported Cabbageworm larvae (Pieris rapae -

Linnaeus) respectively. The occurrence of pest insects on sunflower and crop

vegetation greater than 10 m distant from sunflowers did not significantly differ in

2002 (F1,16 = 0.12, p = 0.74; Figure 3-12) but did significantly differ in 2003 (F,16 =

14.7, p = 0.001; Figure 3-13). Greater mean numbers of pest insects per meter were

observed on sunflower vegetation than on crop vegetation greater than 10 m distant

from sunflowers (2.5 individuals / m2 vs. 0.2 individuals / m2 respectively). This

same difference was found on crop vegetation within 1 m of sunflowers as well in

2003 (2.5 individuals / m2 vs. 0.5 individuals / m2 respectively, F1,22 = 13.4, p =

0.001; Figure 3-13).













6.0-


4.0-


0.0--


Crop Vegetation


Sunflowers


Figure 3-10. Occurrence of beneficial insects was significantly greater on sunflower
vegetation than on crop vegetation during the 2002 growing
season (F,.,, = 11.78, p = 0.003). Error bars = 1 SE.

















M 3.0"
CE

2.0-

Eo

1.0-



Distant Adjacent Sunflowers






Figure 3-11. The occurrence of beneficial insects was significantly greater on
sunflower vegetation than on crop vegetation more than 10 m distant from
sunflowers in 2003 (F1.,6 = 12.94, p = 0.002). Occurrence of beneficial insects on
crop vegetation directly adjacent to sunflowers (within Im) did not significantly
differ from that found on sunflower vegetation (F,2, = 2.29, p = 0.144).
Error bars = 1 SE.















2.50-



2.00-



2 1.50-



O0 1.00-
E


0.50-




Crop Vegetation Sunflowers



Figure 3-12. Occurrence of pest insects on sunflower and crop vegetation greater
than 10 m distant from sunflowers did not significantly differ in 2002 (F.6 = 0.12,
p = 0.74). Error bars = 1 SE.











3.00 -




S 2.00 -

c E
-0


E 1.00-




0.00-
Distant Adjacent Sunflowers



Figure 3-13. Occurrence of pest insects on sunflower and crop vegetation greater
than 10 m distant from sunflowers significantly differed in 2003 (F,,, = 14.7, p =
0.001). Greater mean numbers of pest insects per meter were observed on sunflower
vegetation than on crop vegetation greater than 10 m distant from sunflowers (2.5
individuals / m2 vs. 0.2 individuals / m2 respectively). This same difference was
found on crop vegetation within I m of sunflowers as well (2.5 individuals / m2 vs.
0.5 individuals / m2 respectively, F,,, = 13.4, p = 0.001)









Discussion

Avian Abundance and Foraging Activity

In this study 1 tested the hypothesis that cropped fields with sunflower rows

incorporated into the cropping system would exhibit greater bird densities. My

results support this hypothesis. Those fields with even one row of sunflowers per 0.4

ha exhibited significantly greater bird densities than those without, regardless of crop

type or crop diversity. While an additional increase in density was seen with an

additional row of sunflowers, it appears that a single row may be enough to make

cropped areas more attractive for bird use. A single row of sunflowers added to a

field increased bird densities and foraging time spent by those birds nearly 4 times

that seen in control blocks. Therefore the addition of a single sunflower row may

provide the added structural vegetation to make a cropped field attractive for bird use

in those systems where their presence could possibly provide a benefit. However,

additional work needs to document and quantify the impact this increase in bird

density has on insect populations in crops and crop production.

In this study I also tested the hypothesis that foraging activity would be

increased in crop vegetation with the presence of sunflower rows. Results of my

foraging observations support this hypothesis since foraging activity was 4 times

greater in crops with sunflower rows. Previous studies suggest foraging activities of

insectivorous birds in cropped systems depends upon vegetation cover and

microclimate in the field (Rodenhouse and Best 1994, and reviewed by Kirk et al.

1996). Birds were found to begin to utilize sunflower vegetation as soon as the plants

were able to support perching and provide some cover (Figure 3-14).
















































Figure 3-14. Birds were found to begin to utilize sunflower vegetation as soon as the
plants were able to support them as a perch and begin to provide some cover. Once
sunflowers reached a height of at least 24", birds were observed to fly in to the fields
and first land on the sunflowers before venturing into nearby crop vegetation. A
Palm Warbler (Dendroica palmarum) is shown perched on a sunflower while
foraging for insects in nearby rows of kale.









Once sunflowers reached a height of at least 0.6 m, birds were observed to fly in to

the fields and, first, land on the sunflowers before venturing into nearby crop

vegetation. Several studies have confirmed the strong relationship between hedgerow

presence and composition, and avian presence and community structure in

agricultural landscapes (see O' Connor 1984, MacDonald and Johnson 1995).

Therefore in those fields in which birds may provide a benefit as insect predators, the

addition of sunflowers into the cropping system may be an effective and temporary

habitat modification.

I observed birds actively pursuing and consuming economically important

pest insects gleaned from crop vegetation. The value of utilizing naturally occurring

enemies cannot be overemphasized within organic farming systems and IPM

programs (Rosen et al. 1996). Insectivorous birds are naturally occurring components

of agroecosystems and their feeding activities in and around cropped areas may be of

great economic value. Birds are both mobile enough to recruit readily to high-density

food patches in their home ranges, and are capable of complex prey-switching and

specialization behaviors (McFarlane 1976, Kirk et al. 1996). Due to these

characteristics birds are potentially important components of biological control

regimes, provided they increase the natural mortality of agricultural arthropod pests

without adversely affecting other natural enemies and the crops themselves

(McFarlane 1976, Kirk et al. 1996).

As pest predators, birds may provide both numerical and functional responses

to prey availability over short time periods and large areas (Holling 1988, Dahlston et

al. 1990, Holmes 1990) potentially stabilizing pest communities in agroecosystems,









augmenting the activities of other classes of predators with different characteristics

(Price 1987, Rosen et al. 1996, Helenius 1998). Since birds responded to the

presence of sunflower rows after they reached a certain height, timing of planting of

these rows will be critical to maximize the benefit of attracted insect predators to

crops. Sunflower plantings should proceed that of other crop vegetation by several

weeks to allow their establishment and potential attraction of beneficial predators

before crops, and any associated pests, reach critical growth stages. Optimally,

potential suppression of pest insects will occur if an adequate predator base is present

before pests colonize crop vegetation and their populations grow to economically

damaging levels (Price 1987, Rosen et al. 1996, Helenius 1998).

Most bird damage to crops in the U.S. occurs to grain and small sized fruit

crops appear to be worse in certain regional locations, certain cropping system

designs, and in crops bred for very early or late season harvests (reviewed by

Rodenhouse et al. 1995). Several bird species are known to cause considerable

damage to crops, especially flocking species such as Red-winged Blackbirds

(Agelaiusphoeniceus) and Cedar Waxwings (Bombycilla cedrorum). During my 4

years of observations of birds in cropping systems I observed very little damage to

vegetable crops by birds. During the spring growing season of 2001, North-central

Florida experienced severe drought conditions. In this season I observed watermelon

damage cause by American Crows (Corvus brachyrhyncos) presumably to obtain

water. In all 4 years, 2000 2003, I also observed a limited amount of strawberry

damage caused by Northern Mockingbirds (Mimuspolyglottos). During this study

participating farmers reported that they did not experience any increase in bird









damage due to attracting more birds into their cropping systems with sunflower

plantings. I did not observe any of the 3 most problematic species mentioned above

utilizing sunflowers (blackbirds, crows, or waxwings) or being attracted to plots with

sunflower rows over the study period.

In a recent survey of Florida farmers, bird damage to crops was reported by

32.9% of the survey participants primarily indicating damage to watermelon or corn

by crows (Jacobsen et al. 2003). However only 11.8% reported the need to utilize

bird control methods to limit damage. In some cases proper "farmscaping" cannot

only increase the presence of beneficial organisms, but may reduce the presence or

abundance of problematic species in cropping systems as well. Farmscaping is

defined as a whole-farm, ecological approach to pest management through selective

placement of hedgerows, insectiary plants, cover crops, and water reservoirs to attract

and support populations of beneficial organisms such as insects, bats, and birds of

prey (http://attra.ncat.org/attra-pub/PDF/farmscaping.pdf). Research in farmscaping

to maximize beneficial organisms and limit pests is ongoing to identify and develop

such management strategies (Pickett and Bugg 1988, Bommarco and Ekbom 2000).

Beneficial and Pest Insect Occurrence

Insect sampling efforts revealed that sunflowers did indeed attract and play

host to numerous beneficial insects as has been described in numerous publications

(Henn et al. 1997, UF Coop. Ext. Service Insect Identification Sheets SPSET 5 1997).

Sunflower plants were found to attract predaceous insects almost immediately after

establishment. Parasitoids and pollinators were attracted as soon as these plants

began to produce flowers. These same beneficial insects were found to also occur on








crop vegetation but in lower numbers. It has been found in several studies that

providing predator refugia within cropping systems via strip crops or uncultivated

corridors can result in the migration of predatory insects into adjacent crops (see

Johanowicz and Mitchell 2000, Mensah 1999, Nentwig 1998, Schoenig et al. 1998,

Wratten et al. 1998, Rodenhouse et al. 1992). In the 2003 growing season I modified

the sampling methodology in an attempt to determine whether beneficial insects

attracted to the sunflowers may have been moving out from the sunflowers into

adjacent crop vegetation. Results indicated that crop vegetation 10 m distant from

sunflowers harbored significantly fewer beneficial insects than did that within 1 m.

Moreover, crop vegetation within 1 m of sunflowers exhibited nearly the same

abundance and diversity of beneficial insects as did the sunflowers themselves.

Further study is required to fully describe the distances key beneficial insects move

from sunflowers and the impact these beneficial insects have on crop pests.



Conclusion

Bird populations and avian community structure are known to respond

differently to the distribution of cropped and non-cropped landscape elements and the

distribution, relative cover classes, and juxtaposition of agricultural landscape

elements in agroecosystems (Freemark et al. 1993, Rodenhouse et al. 1993). Intrinsic

habitat qualities such as food resources or shelter availability play important roles in

habitat selection by birds (Bairlein 1983, Martin and Karr 1986, Moore et al. 1995).

Moreover, habitat complexity resulting from a mix of different plant species,

percentages of vegetative cover and variations in the size, distribution, and









juxtaposition of plant assemblages will influence the local diversity of bird species

(James 1971). The addition of structurally diverse vegetation strips within cropped

fields appears to attract and provide cover for birds utilizing adjacent non-crop

habitats. In so doing the probability that these highly insectivorous animals may

provide an economic benefit to producers is greatly increased. In return, the creation

of suitable habitat within cropping systems may aid in the conservation of all avian

species within agroecosystems. Within the discipline of conservation biology there is

increasing recognition that protected reserves alone will not be sufficient to conserve

biodiversity in the long term; therefore, methods of integrating conservation and

productive use must be achieved (Hobbs and Norton 1996). This study contributes to

a better understanding of the effects of vegetative structure and crop species

composition on farm-bird community structure, with more general applications to

implementation of environmentally sensitive agriculture.















CHAPTER 4
PARASITIZED AND NON-PARASITIZED PREY SELECTIVITY OF
INSECTIVOROUS BIRDS: POTENTIAL FOR AUGMENTATION OF
CLASSICAL BIOCONTROL


Introduction

Biological control by natural enemies is the most successful and promising

alternative to unilateral reliance on chemical pesticides in low input cropping systems

(Rosen et al. 1996). Classical biological control programs often rely on releasing

introduced (non-native) parasitoids to reduce exotic pest populations (DeBach and

Rosenl991), where host specificity is emphasized using parasitoids or predators of

targeted pest arthropods. While a majority of biological control research has focused

upon "specialist" enemies for individual agricultural pests, the strategy of enhancing

these efforts by increasing "background mortality" (see Beddington et al. 1978) through

assemblages of native generalist predators also shows promise in crop management

schemes (Helenius 1998). Such augmentation of classical biological control programs

will require sustained availability of large numbers of inexpensive, high quality, naturally

occurring predators (Hoy 1992). Multiple natural enemies in a system are understood to

provide a shifting temporal and spatial mosaic of predation rates across multiple prey,

dampening variability in the systemic predator-prey dynamic (Rabb 1971). Thus

augmentation of classical biological control measures involves efforts to enhance the

presence of naturally occurring enemies of pest arthropods in agroecosystems.









Over the past 2 decades, field entomologists and agronomists have increasingly

recognized that the conservation of natural enemies via the management of non-cropped

habitats that support them is important to effective and successful biological control in

agricultural systems (Rosen et al. 1996). However, little work has been done looking at

avian insect predators in modem cropping systems to fill this role of augmenting other

control measures. One particularly important potential mechanism whereby birds might

stabilize and augment pest control is consumption of individual prey that escape mortality

from other agents of biological control. In systems where introduced or native

parasitoids are supported via provision of critical habitat (e.g., insectiary plantings) rather

than through repeated releases onto fields, parasitism rates undergo fluctuations due to

parasitoid population lags (Bugg and Pickett 1998). In such systems birds could function

to stabilize and maintain sufficient pest mortality rates given their abilities to respond

functionally to changes in prey abundance (McFarlane 1976). While this scenario

reasonably explains how birds could effectively augment arthropod pest mortality

induced by parasitoids typically employed in classical biological control regimes

(McFarlane 1976, Kirk et al. 1996), its generality, practicality, and economic efficiency

have not been assessed for any agroecosystem.

Bruns (1959) stated that birds would be of value as insect predators in a system

only if they increase the effectiveness of control by taking insects over and above those

that would normally have been destroyed by other agents. Several studies have

demonstrated that birds select and consume non-parasitized insects suggesting that bird

predation may be additive to the mortality caused by parasitoids (Sloan and Simmons

1973, Schlichter 1978). Sloan and Simmons (1973) reported that hymenopterous









parasitized jack pine budworm (Choristoneura pinus Bechstein) larvae and pupae were

unanimously rejected by foraging chipping sparrows (Spizella passerina). Similarly,

Schlicter (1978) reported that black-capped chickadees (Parus atricapillus) largely

avoided foraging upon galls on Canada goldenrod (Solidago canadensis) that had been

parasitized by mordellid beetle (Mordellistena unicolor) larvae to extract gall fly

(Eurosta solidaginis) larvae. Therefore it appears that birds have the ability to

distinguish prey that have been damaged or may be compromised by a parasite and avoid

such prey.

Previous observations have confirmed that many birds occurring in cropped fields

of North-central Florida actively forage for and consume caterpillars in crop vegetation

(see Chapters 2 and 3). Fall armyworms [Lepidoptera: Noctuidae, Spodopterafrugiperda

(J. E. Smith)] are important pests in vegetable and row crops (Johnson and Sprenkel

1996) and are often subjected to biological control using cultured parasitoids (R.

Meagher, USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology

(CMAVE), Gainesville, FL, pers. comm., Johnson and Sprenkel 1996). Parasitoids are

insects whose eggs are deposited on another arthropod (usually an insect) host, its larvae,

or in the host's egg. The resultant larvae develop by feeding upon the bodies of the host

resulting in the host's death (Godfray 1994).

In this study I addressed whether birds would consume armyworms that had been

parasitized or avoid such prey. I tested the hypothesis that birds prefer to forage upon

non-parasitized armyworm prey via captive feeding trials where birds were also offered

prey parasitized by Euplectrus wasp larvae. In both studies where birds avoided prey, it

was suggested that visual cues were utilized to distinguish between prey types (Sloan and









Simmons 1973, Schlichter 1978). Parasitoids can be divided into two classes by the

feeding behavior of their larvae. Endoparasitoid larvae feed from, and develop within,

the body of their host. Ectoparasitoid larvae develop while externally attached to the host

feeding with mouthparts buried into the host's body (Godfray 1994). Larvae of the genus

Euplectrus are gregarious (more than one parasitoid larvae per host) external parasites of

lepidopteran larvae. Euplectrus larvae remain attached to the exoskeleton and feed on the

dorsum of their host, which is often still able to move freely about (Figure 4-1). Once the

Euplectrus larvae mature they move below the emaciated host to pupate, spinning silk

from the host's Malpighian tubes which hold the host down and separate the larvae from

each other (Grissell and Schauff 1997). Therefore, Euplectrus served as a good

representative of commonly occurring ectoparasitoids whose larvae develop on the

external surface of their host that could be visually identified by a bird.



Methods

Research Facilities and Test Species

Feeding trials were conducted in an aviary at the USDA National Wildlife

Research Center's Florida Field Station, Gainesville, Florida. Red-winged blackbirds

(Agelaius phoeniceus) captured in agricultural settings and housed at the field station

were utilized as a test insectivorous species. This species was chosen due to the fact that

individuals of this species commonly occur in agricultural landscapes (Ehrlich et al.

1988, Dolbeer 1990) and have been previously examined for their predatory impact on

insect pest populations in crops (Bendell et al. 1981). Birds were presented parasitized

and non-parasitized fall armyworms provided by the USDA- ARS CMAVE, Gainesville,









FL. Parasitized armyworm larvae were those that had been exposed to and carried larvae

of the Eulophid parasitoid species Euplectrus plathypenae (Howard). This

Hymenopteran species commonly occurs in Florida and has been investigated for its

biological control value (R. Meagher, USDA-ARS, Center for Medical, Agricultural and

Veterinary Entomology (CMAVE), Gainesville, FL, pers. comm.).

Paired Feeding Trials With Non-parasitized Larvae

The first set of feeding trials performed with non-parasitized prey test if the

captive birds would feed upon fall armyworms, and I determined their baseline

consumption given this food item. Only those birds willing to readily eat armyworms

were utilized for subsequent tests. Additionally, since birds have exhibited prey size

selectivity when presented a choice (Krebs et al.1977, Davies 1977, Zach 1979) an

assessment was made whether birds exhibited a feeding preference for different instar

sizes of these caterpillars. Maintenance food was removed by 0700 EST and 1-2 hrs later

birds were presented with a plastic cup divided into two chambers (Figure 4-2). In the

first protests, 10 armyworms of equal size were simultaneously presented in the cup's

chambers and birds were allowed to forage undisturbed for '/2 hour (Figure 4-3). The

propensity of each bird to eat the armyworms, the chamber location (left or right side of

cup) the larvae were chosen from, and the time it took for the bird to consume all 10

larvae were noted. In these tests, as well as all that followed in this study, a bird would

not be given a subsequent test presentation until at least 1 hour had passed.

In the second set of tests, those birds that had exhibited a willingness to eat

armyworms in the first tests were simultaneously presented 10 larvae of two different

instar sizes, 5 large (5th instar, 26.1 + 3.0 SD mm, n = 28) vs. 5 small (2"d or 3rd instar,

















































Figure 4-1. Euplectrus plathypenae Howard (Hymenoptera: Eulophidae) larvae attached
to an armyworm (Spodoptera ssp.) larvae host.















































Figure 4-2. Prey item presentation cup placed in test cage with a red-winged blackbird
(Agelaius Phoeniceus) foraging for a food item. The presentation cup contained a center
divider partitioning the cup into two chambers. A red line painted on the exterior of the
cup allowed observers to easily determine which chamber a food item was taken from.





















-4,:


v
:i4:



1 J
S,. .r. ~." 4 '
i' .. ..,






I'.

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Figure 4-3. In multiple trials, birds were offered fall armyworms [Spodopterafrugiperda
(J. E. Smith)] of similar body size in each of the presentation cup's chambers.




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