UNIVERSITY of CALIFORNIA RIVERSIDE Myoporum Thrips Life

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UNIVERSITY OF CALIFORNIA RIVERSIDE

Myoporum Thrips Life History, Host Preference, and Biological Control

A Dissertation submitted in partial satisfaction of the requirements for the degree of

Doctor of Philosophy

Entomology

Christopher John Shogren

December 2017

Dissertation Committee: Dr. Timothy D. Paine, Chairperson Dr. Matthew P. Daugherty Dr. Richard A. Redak

The Dissertation of Christopher John Shogren is approved:

Committee Chairperson

University of California, Riverside

Acknowledgements

I would like to express my sincere thanks to Dr. Tim Paine for his guidance and support throughout this project. Thank you to my committee members, Dr. Matt

Daugherty and Dr. Rick Redak, for their valuable advice regarding experimental design

and data analysis. The members of the Paine lab- Chris Hanlon, Colin Umeda, Rebecca

Watersworth, Gabby Martinez, Giovanna Munoz, Pamela Hsi, and Rory McDonnell-

provided assistance throughout my study an allowed me to progress with some sanity. A

big thank you to Erich Schoeller and Fatemeh Ganjisaffar, without your statistical

expertise I would never have made it this far. Thank you to D. Horton, T. Lewis, and R.

Vetter for providing assistance identifying predators. Chris Martinez and the staff at the

SCREC provided assistance with the field trial; their assistance during this project was

greatly appreciated. Thank you to my brother Charles for digging holes in the scorching

heat, and helping build fantastic cages. Thank you to Cottonwood Growers for providing

space for field trials. Financial support was received in part by the California Association

of Nurseries and Garden Centers, the Harry Scott Smith Fund, and the Robert van den

Bosch Scholarship.

In addition to the persons and organizations mentioned above, many people provided

personal support that was essential for my coming to and successfully graduating from

UCR. My friends, from life before UCR as well as those made here, are constant sources

of inspiration and gratification. Finally, I would like to express my deepest gratitude to

my family for their loving support.

Dedications

To my daughter Mia

To my family

To my friends

And

In loving memory of,

Agnes Shogren

ABSTRACT OF THE DISSERTATION

Myoporum Thrips Life History, Host Preference, and Biological Control

Christopher John Shogren

Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, December 2017 Dr. Timothy D. Paine, Chairperson

Temperature-driven development of myoporum thrips, Klambothrips myopori,

(Thysanopetra: Phlaeothripidae) was examined at seven constant temperatures (15°, 17°,

20°, 25°, 30°, 34°, and 35.5° C) on Myoporum laetum. Thrips successfully completed development to adult stage between 15 and 35.5°C. One linear and three nonlinear models were fitted to describe developmental rates of K. myopori as a function of temperature, and for estimating thermal constants and bioclimatic thresholds (Tmin, Topt and Tmax). The Briere-1 model performed best in describing the developmental rate of cumulative life stages.

Two ecological niche models, CLIMEX and Maxent, were used to predict the geographic distribution of K. myopori in its native range and globally. Overall predictions of environmental suitability differed greatly across models. The CLIMEX model accurately predicted known invasive and native localities, while the Maxent model failed to predict

the native localities and parts of the invasive range. Based on the CLIMEX model, K.

myopori has the potential to establish in many regions of the globe.

Using field studies and laboratory feeding tests, we identified Myoporum laetum and M.

‘Pacificum’ as key host plants of K. myopori. In laboratory trials, K. myopori failed to complete development on M. ‘Clean n Green’ and M. ‘Putah Creek’. For the six varieties of Myoporum tested, K. myopori damage was only observed on M. laetum and M.

‘Pacificum’. Although K. myopori can successfully colonize and reproduce on several varieties of Myoporum, they demonstrated a preference for M. laetum and M. ‘Pacificum’ in laboratory and field trials.

Using field and laboratory studies, we identified Orius spp. (Hemiptera: Anthocoridae),

Chrysoperla spp. (Neuroptera: Chrysopidae), Syrphidae, and Salticidae as possible key natural enemies of K. myopori in southern California. Laboratory studies determined the consumption rates of Orius insidiosus and Chrysoperla rufilabris at constant densities of

K. myopori and defined the functional response of the predators. Both predators consumed more 2nd instar larvae than other prey stages. O. insidious displayed a type II

functional response, while C. rufilabris displayed both type II and type III depending on

prey stage, implying the predators should be most effective at suppressing thrips

populations at lower densities.

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Table of Contents

Acknowledgements……………………………………………………………….iv

Dedications………………………………………………………………………..v

Abstract of the Dissertation………………………………………………………vi

List of Tables……………………………………………………………………...x

List of Figures…………………………………………………………………....xii

Chapter 1. Invasive Thysanoptera in California………...………………………………..1

Invasive Species and the Urban Environment…………………………………….2

Thysanoptera………………………………………………………………………8

Myoporum Thrips as a Pest……………………………………………………...11

Integrated Pest Management……………………………………………………..13

Dissertation Objectives…………………………………………………………..19

References Cited…………………………………………………………………20

Chapter 2. Predicting the Potential Invasive Range of Klambothrips myopori………...28

Introduction………………………………………………………………………29

Materials and Methods…………………………………………………………...33

Results……………………………………………………………………………38

Discussion………………………………………………………………………..41

References Cited…………………………………………………………………46

Chapter 3. Host Plant Preference and Performance of Klambothrips myopori

(Thysanoptera) in Southern California…………………………………………………..74

Introduction………………………………………………………………………75

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Materials and Methods…………………………………………………………...77

Results……………………………………………………………………………81

Discussion………………………………………………………………………..83

References Cited…………………………………………………………………87

Chapter 4. Identification of Klambothrips myopori Predator Complex………………..98

Introduction………………………………………………………………………99

Materials and Methods………………………………………………………….101

Results…………………………………………………………………………..107

Discussion………………………………………………………………………111

References Cited……………………………………………………………..…117

Chapter 5. General Conclusions……………………………………………………….141

References Cited………………………………………………………………..147

List of Tables

Table 2.1 CLIMEX parameters values for Klambothrips myopori……………………..58

Table 2.2 Development time (days) (mean ± SEM) for immature stages of Klambothrips myopori………………………………………………………………………………..…59

Table 2.3 Estimated parameters (a and b), lower developmental threshold (°C), and thermal constant (K) from linear regression……………………………………………..60

Table 2.4 Parameter estimates (±SEM) for three nonlinear development rate models for Klambothrips myopori ……………………………………………………………...... 61

Table 2.5 Summary of climate variables used in the Maxent model………………...... 63

Table 3.1 Injury rating scale for K. myopori on M. laetum……………………………...89

Table 3.2 The mean number of days (±SE) for K. myopori to complete development at 25°C……………………………………………………………………………………...90

Table 3.3 Predators collected on Myoporum varieties from surveys between August 2015 through July 2016 at the SCREC………………………………………………………...91

Table 3.4 Predators collected on Myoporum varieties from surveys between August 2015 through July 2016 at the San Jacinto site………………………………………………...92

Table 4.1 Mean annual weather variables for three collection sites from Arguez et al. (2012)………………………………………………………………………...... 121

Table 4.2 Potential predators of K. myopori collected on Myoporum laetum from surveys between June 2014 through May 2015…………………………………………………122

Table 4.3 Functional response of Orius insidiosus based on logistic regression estimate using Ne/No………………………………………………………………………...... 125

Table 4.4 Estimated type II functional response parameters ± SE (95% confidence interval) for O. insidiosus feeding on different life stages of K. myopori……………...126

Table 4.5 Functional response of Chrysoperla rufilabris based on logistic regression estimate using Ne/No……………………………………………………………………127

Table 4.6 Estimated functional response parameters ± SE (95% confidence interval) for C. rufilabris feeding on different life stages of K. myopori……………………………….128

List of Figures

Figure 2.1 Distribution map of Myoporum. Taken from Discover Life 2014…………..64

Figure 2.2 Linear and three nonlinear functions fit to the data of developmental rates (1/days) of K. myopori……………………………………………………………..…….65

Figure 2.3 Map of predicted environmental suitability for K. myopori from CLIMEX for California………………………………………………………………………………...66 Figure 2.4 Map of predicted environmental suitability for K. myopori from CLIMEX for Hawaii……………………………………………………………………………………67

Figure 2.5 Map of predicted environmental suitability for K. myopori from CLIMEX for North America…………………………………………………………………………...68 Figure 2.6 Map of predicted environmental suitability for K. myopori from CLIMEX for Australia…………………………..……………………………………………………..69 Figure 2.7 Map of predicted environmental suitability for K. myopori from CLIMEX for the world.………………………………………………………………………………...70 Figure 2.8 Map of predicted environmental suitability for K. myopori from Maxent…..71

Figure 2.9 Map of predicted environmental suitability with known localities for K. myopori in the invasive range in California……………………………………………...72

Figure 2.10 Map of predicted environmental suitability with known localities for K. myopori in the native range in Tasmania from Maxent………………………………….73

Figure 3.1 Survival distribution curves for K. myopori on four varieties of Myoporum..93

Figure 3.2 Proportion of K. myopori surviving to adulthood on different varieties of Myoporum. Bars with the same letter are not significantly different (P < 0.01)………...94

Figure 3.3 The mean number of thrips per plant over time for each collection site…….95

Figure 3.4 The mean number of predators per plant over time for each collection site...96

Figure 3.5 The mean damage score induced by K. myopori over time for each collection site………………………………………………………………………………………..97

Figure 4.1 The mean number of thrips per tree over time for each collection site…….129

xii

Figure 4.2 The mean number of natural enemies per tree over time for each collection site………………………………………………………………………………………130

Figure 4.3 Mean number (± SE) of insects per open cage at the South Coast Research and Extension Center………………………………………………………………...…131

Figure 4.4 Mean number (± SE) of thrips per cage type at the South Coast Research and Extension Center. Bars with different letters are significantly different (P > 0.05) within date……………………………………………………………………………………...132

Figure 4.5 Mean number (± SE) of insects per open cage at the San Jacinto site……..133

Figure 4.6 Mean number (± SE) of thrips per cage type at the San Jacinto site. Bars with different letters are significantly different (P > 0.05)…………………………………..134

Figure 4.7 Mean prey consumption for Orius insidiosus feeding on different life stages of Klambothrips myopori in host preference study (P<.01)……………………………135

Figure 4.8 Mean prey consumption for Chrysoperla rufilabris feeding on different life stages of Klambothrips myopori in host preference study (P<.01)…………………….136

Figure 4.9 Functional responses of O. insidiosus to different stages of K. myopori under laboratory conditions…………………………………………………………………...137

Figure 4.10 Proportion of K. myopori consumed by O. insidiosus, and logistic regression fit to the data……………………………………………………………………………138

Figure 4.11 Functional responses of C. rufilabris to different stages of K. myopori under laboratory conditions…………………………………………………………………...139

Figure 4.12 Proportion of K. myopori consumed by C. rufilabris, and logistic regression fit to the data……………………………………………………………………………140

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Chapter 1

Invasive Thysanoptera in California

Invasive species and the urban environment

Non-native species are fauna, flora or unicellular organisms that have established outside

of their native ranges and into novel habitats (Pimentel et al. 2005). The impacts of non- native species range from negligible to extremely detrimental and economically devastating. Some species are deliberately introduced into a new habitat for beneficial purposes (e.g., food, urban forestry, as pets, and biological control agents). In the United

States non-native species, such as corn, wheat, cattle, and poultry, account for more than

98% of the food system (Pimentel et al. 2005). Non-native species may also provide benefits to their new environment by providing new habitats or food resources for rare or endangered species, serving as functional substitutes for extinct taxa, providing desirable ecosystem services, and as natural enemies of pestiferous species (Schlaepfer et al. 2011).

Others are accidently introduced into new habitats, and are considered invasive if they spread rapidly, cause economic or environmental harm, or pose a threat to human health.

Invasive species can also reduce biological diversity, alter the structure and composition of native communities, act as vectors of disease, lead to the loss of ecosystem services, and in extreme cases cause the extinction of vulnerable endemic species (Simberloff et al.

2013).

An estimated 50,000 non-native species have been introduced into North America since the arrival of Europeans about 500 years ago (Pimentel et al. 2000). According to recent data, in California alone more than 17% of extant plants are exotic, greater than 35% of all freshwater fish are non-native, and more than 600 species of invertebrates are

invasive, with another 400 species having been deliberately introduced as biological control agents (Dowell and Krass 1992, Vitousek et al. 1996). Exotic species cost the

California agriculture industry billions of dollars annually in control measures and yield losses (Venette and Carey 1998). Records in California for the period 1955–1988 indicate a constant influx of non-native insects at an average of 6.1 species per year

(Dowell and Gill 1989). The continuous establishment of non-native species poses many challenges, including: identification of species that pose a high risk of becoming serious pests, monitoring for said high risk species, creation and implementation of management strategies to combat invasive species, and the costs associated with any potential management program (Simberloff et al. 2005, Buckley 2008).

With the introduction of countless invasive species, the normal functioning of an ecosystem can become altered. Plants, and more specifically, forests provide a number of ecosystem services that benefit, not only other plants and animals, but humans as well.

Ecosystem services can be defined as, but are not limited to: gas regulation, climate regulation, moderating weather extremes and their impacts, water supply and regulation, waste treatment, pollination, wildlife and biodiversity, energy use, recreation, and individual well-being and public health (Costanza et al. 1997).

Urban forests provide a variety of ecosystem services that benefit the physical environment (e.g. air and water quality), as well as the social environment (e.g. individual and community well-being) (Nowak et al. 2010). The term “urban forest” refers to all

publicly and privately owned trees within an urban area, including trees planted along

streets, in parking lots, and in manmade landscapes, as well as any remnant stands of

native forest (Nowak et al. 2010). Urban forests in the United States are estimated to

contain about 3.8 billion trees, with the tree canopy covering an estimated 27.1%

(281,000 km2) of urban areas (Nowak et al. 2002).

Trees sequester CO2 (carbon dioxide) from the atmosphere during the process of

photosynthesis, regulating the atmospheric balance of CO2 and O2. During

photosynthesis trees use light energy to convert CO2 and H2O (water) into chemical

energy, C6H12O6 (glucose) with O2 (oxygen) released into the atmosphere as a byproduct

(Reece et al. 2014). Carbon storage is defined as the amount of atmospheric carbon

stored in living plant tissue (Nowak and Crane 2002). Urban forests in the United States

have been estimated to contain 700 million metric tonnes of carbon, with a gross carbon

sequestration rate of 22.8 million tC/yr (Nowak and Crane 2002). However, the carbon

sequestered annually by urban trees in the United States is only equivalent to a given

population’s emissions over a 5-day period (Nowak and Crane 2002). Nowak and Crane

(2002) estimated the value of atmospheric carbon sequestered by urban trees in the

United States to be $14.3 billion, with an annual sequestration value of $460 million.

Urban trees, and by extension urban forests, can influence energy use in buildings by:

reducing solar heat gain through windows, walls, and roofs by shading; reducing radiant

heat gain from the surroundings by shading; reducing outside air infiltration rates by

lowering ambient wind speeds; and reducing the heat gain into building(s) by lowering ambient temperatures through evapotranspiration in summer (Heisler 1986, Akbari

2002). Akbari (2002) estimated the per-tree reduction of carbon emissions (for trees around buildings) is approximately 10–11 kg per year, which is due directly to a reduction in energy use. In a simulation by Nowak (1993) planting 10 million trees annually in energy conserving locations over a 10-year period with 100% survival rates, will result in an estimated 77 million metric tonnes of carbon being stored. This translates into 286 million tC of atmospheric carbon not being released into the atmosphere from power plants over a 50 year period. In California, McPherson et al. (2016) estimated that the annual monetary value of energy savings from the state’s 9.1 million street trees is

$101.15 million, with an average annual benefit per tree of $11.08.

The presence of urban trees and forests is also ecologically important because they function to slow the rate of precipitation reaching the ground during storms, and in turn, the corresponding infiltration rate of water into the soil. Rainwater intercepted on tree leaves and branches is temporarily stored on leaf and bark surfaces. The water eventually drips/flows off the given surfaces to the ground, or evaporates into the atmosphere, thereby reducing the overall flow of precipitation reaching the ground (Xiao and

McPherson 2002). The building of infrastructure, and removal of urban forest, alters the natural hydrological cycle. A higher proportion of rainfall becomes surface-water run-off, which results in increased peak flood discharges and degraded water quality through the pick-up of urban pollutants as the water flows over man-made surfaces (Bolund and

Hunhammar 1999). Urban runoff reduction, via the ecological services provided by urban

forests, ultimately reduces expenses for urban water runoff control and pollutant

treatment. In a study conducted in Beijing, China, Zhang et al. (2012) evaluated the economic benefits of rainwater-runoff reduction by urban green spaces. The results showed a total economic benefit, due to rainwater-runoff reduction by urban forests, of

$9.15 billion in 2009.

The urban forest is also important for individual well-being and public health. Trees make the urban environment a more aesthetic, pleasant, and emotionally satisfying place in which to live, work, and spend leisure time (Nowak et al. 2010). Ulrich (1984) showed that patients recovered faster, and with fewer complications from surgery, in a room with a view of a natural scene when compared to those without such a view. People cannot remain healthy without clean air, clean water, food, and other ecosystem services provided by the urban forest (Hartig et al. 2014). In a study on the relationship between trees and human health, Donovan et al. (2013) demonstrated a correlation between the widespread death of ash trees from the emerald ash borer (Agrilus planipennis) and an increase in mortality related to cardiovascular and lower-respiratory-tract illness.

The reduction of the Earth’s biological diversity is also a growing problem, and is broader in scope than just the extinction of species. This loss of biodiversity is of critical concern, especially given that an increasing amount of research indicates that diversity plays an important role in maintaining long-term ecosystem functioning (Dwyer et al.

1992, Alvey 2006, Balvanera et al. 2006). Biodiversity plays multiple roles in the

delivery of ecosystem services, by serving as a regulator of ecosystem processes, and in

economic terms, as a good or commodity (Mace et al. 2012). A diverse array of

organisms function together to regulate ecosystem processes including: microorganisms

involved in decomposition and nutrient cycling, primary producers creating biomass and

sequestering carbon, and predators and parasites regulating populations. Biodiversity, as

an ecosystem service, provides: food crops, allows for commercial exploitation (e.g.

pharmaceuticals), and pollination services, to name but a few. If you think of biodiversity

in the same terms as a commodity, it offers aesthetic appeal while maintaining taxonomic

diversity. The components and attributes of biodiversity, which are necessary or desirable

to retain any specific ecosystem service, will vary according to the service or good being

considered, and the processes on which it depends (Mace et al. 2012).

Insects play a huge role in maintaining ecosystem services and their biological diversity is unrivalled in the natural world. Unfortunately, an ever-increasing number of insects have become invasive pests worldwide. They have become pests of livestock, crops, other wild animals and plants, in wild lands and urban environments. Some of these insect pests are threatening the biodiversity and ecosystem services provided by urban forests, leading to a decrease in the overall ecological and commercial benefit these forests provide. In California, Ficus microcarpa and Myoporum spp. are plants widely used in urban environments as specimen trees, street trees, hedges, windbreaks, and for erosion control (Wagar and Barker 1983, Mound and Morris 2007a). While both plant

species are susceptible to damage by a small number of phytophagous insects (Lepš et al.

2001, Mound and Morris 2007a), to date these phytophagous species have not lead to the serious dieback and removal of these plants from urban landscapes. This equation has changed with the introduction of several invasive thrips species, which readily attack

Ficus microcarpa and Myoporum spp. throughout California.

Thysanoptera

Thysanoptera are minute insects which predominately occur within the temperate, tropical and sub-tropical regions of the earth (Mound 2005). The first Thysanoptera were described by De Geer under the genus Physapus in 1744 (Lewis 1997). In 1758 Linnaeus ignored this genus and assigned the four species to the new genus Thrips (Lewis 1997).

The genus was later elevated to the rank of Order, by Haliday in 1836, and given the name Thysanoptera, in reference to their fringed wings (Lewis 1997). The original description given by Linnaeus of Thrips is now used as the common name for all insects classified within the Thysanoptera.

Thysanoptera is considered the sister-group to the Hemiptera, and classified within the

Paraneoptera (Grimaldi and Engel 2005, Mound 2013). Traditionally, the thrips are classified into two suborders, Terebrantia and Tubulifera, with 14 families, of which five families are only known from fossils (Mound 2013). Of the extant families, only a single family, Phlaeothripidae, is assigned to the Tubulifera with the remaining eight,

Aeolothripidae, Fauriellidae, Heterothripidae, Melanthripidae, Merothripidae,

Stenurothripidae, Thripidae, and Uzelothripidae assigned to the Terebrantia (Mound

2013). In total, the nine families of extant thrips include 774 genera and 5938 species,

whereas fossilized thrips taxa are represented by 57 genera and 153 species distributed

across 12 families (Mound 2013). Bhatti (1988, 2006) has proposed a different

classification that recognizes the suborders Terebrantia and Tubulifera as separate Orders

with approximately 40 families. However, this classification is not widely recognized and

is not supported by molecular data (Mound and Morris 2007b, Buckman et al. 2013,

Mound 2013).

As an order, the thrips are the smallest of the winged insects, with adult body size ranging from approximately .5 to 15 mm in length (Lewis 1973). Most large species are tropical

in origin, while temperate species are usually no larger than 1 to 2 mm in size. Adults

vary in color and may appear yellow, brown, or black. Although many thrips species are

wingless, typical adults are weak fliers and bear slender wings with long marginal fringes that allow transport via wind. In the sub-order Terebrantia the wings lie parallel to each other, but in Tubulifera the wings overlap so that only one wing is completely visible

(Lewis 1973). The most remarkable feature of thrips is their asymmetrical mouthparts

(Mound and Marullo 1996). The right mandible is absent, while the left mandible is highly modified into an unarticulated stylet. The paired maxillary stylets are well developed, articulated, and join together to form a single feeding channel.

Although Thysanoptera are considered to have evolved from the same unique ancestor as

Psocoptera and Hemiptera, early in their evolution they acquired important characteristics

not found in these other Orders, including haplo-diploidy (Mound and Marullo 1996).

Female thrips develop from fertilized eggs, while males develop from unfertilized eggs.

Arrhenotoky characteristically produces unequal sex ratios, with about four times more

females than males (Moritz 1997). However, in some species males are rare or nonexistent and reproduction occurs by a form of parthenogenesis called thelytoky, where virgin females produce female offspring. Deuterotoky, where virgin females produce both male and female offspring, also occurs in some species, although rarely

(Moritz 1997). In certain species it is thought that the presence or absence of gut microbes in the parent determines the sex of the offspring (Kumm and Moritz 2008).

The life cycle of Thysanoptera is intermediate between holometabolous and hemimetabolous (Mound and Marullo 1996). The first two actively feeding instars are called larvae, and the later quiescent, non feeding stages are pupae. In the Terebrantia eggs are laid inside host tissue followed by the two larval instars, one prepupa, one pupa, and then the adult. In the Tubulifera eggs are laid on the surface of the host material, followed by two larval instars, one propupa, two pupal stages, and then the adult.

Thrips exhibit a wide diversity of life-histories, about 50% of the known species feed on fungi, approximately 40% feed on living tissues of dicotyledonous plants or grasses, and the remainder exploit mosses, ferns, gymnosperms, cycads, or are predatory (Morse and

Hoddle 2006). For thrips feeding on vascular plants the method of feeding can be variously described as puncturing the tissue and draining the cell content one at a time, piercing the epidermis and rasping the leaf tissues within, or rasping the leaf surface and sucking the sap as it exudes (Lewis 1973). Gall formation is a particular form of leaf damage that often involves considerable specificity between insect and host (Mound and

Marullo 1996). Most thrips galls are produced by the rolling, folding or wrinkling of the leaves. The structure of different galls ranges from the mere curling of the two halves of the leaf blade on either side of the midrib, like those caused by Gynaikothrips ficorum, to more pronounced rolling and folding of leaves encompassing the entire leaf bud, like those caused by Klambothrips myopori (Paine et al. 1991, Mound and Morris 2007a).

Myoporum Thrips as a Pest

Myoporum thrips (Klambothrips myopori) is an exotic insect species in the United States, causing extensive damage to plants in the genus Myoporum (Mound and Morris 2007a).

Myoporum spp. belong to the Figwort family (Scrophulariaceae) with around 32 species native in the Indo-Pacific region (Chinnock 2007). In general there is little known about this new exotic thrips species. Discovered in California in 2005 (Mound and Morris

2007a), this species was described using specimens provided to Australia’s

Commonwealth Scientific and Industrial Research Organization (CSIRO). Since its initial discovery in Orange County, K. myopori has spread to more than ten counties throughout California, and reached the island state of Hawaii in 2009 (Mound and Morris

2007a, Conant et al. 2009a). Recently, in 2011, a population of K. myopori was

discovered feeding on Myoporum insulare in Tasmania, Australia where it is thought to be the native habitat of K. myopori (Cameron and Mound 2013).

In California, Klambothrips myopori has spread rapidly to wherever Myoporum laetum is

planted and feeding causes unsightly damage (Mound and Morris 2007a). The thrips

damage is characterized by gall-like symptoms and severe distortion of new leaves.

Terminal growth is stunted and the leaf galls commonly contain the thrips population.

The drought hardiness of Myoporum, and the earlier relative resistance to insect damage

made members of this genus suitable for ornamental plantings throughout much of

California (Mound and Morris 2007a). In fact, the hardiness of Myoporum is now

leading to the plant being considered an invasive weed in some coastal areas of California

by the California Invasive Plant Council. Consequently, if the wild distribution of

Myoporum laetum expands in California, K. myopori may come to be regarded as

beneficial for its value as a biological control agent of a weed species. Documented hosts

of K. myopori include: M. laetum, M. sandwicense, Myoporum ‘Pacificum’ (‘South

Coast’), and M. insulare (Mound and Morris 2007a, Conant et al. 2009a, Cameron and

Mound 2013, Sullivan 2014).

In Hawaii, naio (Myoporum sandwicense) is a native, dominant tree species and is

regarded for its horticultural and ecological importance (Conant et al. 2009a). Naio is

one of the most important dominant tree species in some dry forests of Hawaii, such as

the mamane-naio dry forest on Mauna Kea. The mamane-naio dry forest is home to two

endangered birds, the akiapolaau (Hemignathus munroi) and the palila (Loxioides bailleui) (Scott et al. 1986). The palila is restricted to the mamane-naio dry forests on

Mauna Kea and is an obligate feeder on mamane seed pods and naio fruit (Hess et al.

2014). M. sandwicense is also an important floral resource for endemic bees in Hawaii.

Serious damage and mortality caused by myoporum thrips may be an important factor in reducing the number and diversity of native bees in Hawaii’s montane habitats

(Magnacca and King 2013).

Integrated Pest Management

Integrated pest management (IPM) is a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/benefit analyses that take into account the interest of and the impact on producers, society and the environment (Kogan 1998). Pedigo and Rice (2006) visualized

IPM as a bridge that can be crossed to avoid significant losses due to pests. The bridge is composed of a foundation arch (biological information techniques), vertical pillars

(control tactics), and a road surface (prevention of losses). The foundation arch represents the basic information and techniques that should be known in order to manage a pest species. The foundation arch, in turn, supports several pillars that represent the tactics used to manage pests, e.g. biological control, pesticide sprays, etc. Together they form a stable road to avoid economic/ecological losses to pests to various stakeholders, such as farmers and land managers.

Effective pest management strategies exploit vulnerable points of a pest’s natural biology

(Pedigo and Rice 2006). This biological information includes how individuals feed,

grow, develop, reproduce, and disperse. Population dynamics is also a crucial part of biological information that investigates the factors (natural enemies, weather, food, habitat, etc) influencing population change of a given species. For example, temperature

(weather) influences several aspects of insect development including adult size, number of larval instars, tissue morphogenesis, and sex ratio (Sehnal 1991). Mathematical models are often used to quantify the factors influencing population change and are useful for understanding population dynamics in various environments. Insect developmental rate as a function of temperature is one such model. The law of Total

Effective Temperatures states that a thermal constant must be accumulated to complete a particular developmental process. Linear models are used to explain a straight line relationship between the developmental rate of an organism and temperature (Campbell et al. 1974), while nonlinear models can describe the developmental rate across a broader temperature range and provide estimate values for the optimum temperature for

development (Lactin et al. 1995, Briere et al. 1999). The data obtained from this

biological information can then be used to estimate the best time to employ various

integrated pest management tactics (e.g. timed applications of insecticides to target

specific life stages, selecting a biological control agent with a compatible developmental

rate to that of the pest species).

The aim of an entomological IPM program is not to eradicate pest populations, but to manage them below levels that cause economics damage (Chandler et al. 2011). IPM tactics may include pesticide application(s), cultural practices (ecological management), use of resistant varieties, or implementing biological control (Kogan 1998, Pedigo and

Rice 2006, Chandler et al. 2011). Cultural control is defined as: the manipulation of the environment in order to reduce the pest population and subsequent damage it causes

(Pedigo and Rice 2006). Cultural control measures include sanitation, modification of alternative pest habitats, irrigation management, crop rotation, trap cropping, intercropping, and strip harvesting (Gurr et al. 2004, Pedigo and Rice 2006). In a study by Nicholls et al. (2000) cover crops in a northern California vineyard significantly reduced the abundance of leafhoppers and western flower thrips compared to a monoculture vineyard.

Pesticides are some of the most important chemicals used today in an effort to maintain the well-being of human populations by maintaining high levels of health, nutrition, and overall quality of surroundings (Pedigo and Rice 2006). The high efficacy, easy accessibility, and consistent performance of chemical controls make pesticides a regular component of agricultural production worldwide, and have helped give rise to new ways of growing crops (Ruberson et al. 1998, Pedigo and Rice 2006). Pesticides have been an important part of IPM programs since the concept of “integrated control” was introduced by Stern et al. (1959). Two methods for integrating chemicals into IPM programs include, using highly selective products specific to the target pest or using less specific products in

a manner or time which minimizes the effect on any beneficial organisms in the crop

(Jacobson 1997). In a study by Liburd et al. the reduced-risk chemical Spinosad, which

specifically targets insects, reduced thrips numbers in blueberries and had minimal effect

on the beneficial predator, Orius insidiosus.

Host plant resistance to pests and diseases is common in wild populations but some traits

have been lost as cultivars have been bred for maximum yield or aesthetic appearance

(Jacobson 1997, Pedigo and Rice 2006). Plant breeding programs have successfully

reintroduced genetic resistance against important pests in numerous cropping systems

including wheat, maize, rice, sorghum, alfalfa and beans (Dhaliwal and Singh 2005,

Smith 2005, Pedigo and Rice 2006, Kennedy 2008). Resistant cultivars function in many

different ways to reduce the effects of insects including: allelochemic nonpreference,

nutrition, antibiosis, and morphological characteristics that reduce their susceptibility to

the pest (Pedigo and Rice 2006). Biotechnology has also been used to develop insect-

resistant cultivars. Recombinant DNA technology greatly increases the potential array of

available resistance traits that can be bred into plants and used to obtain insect-resistant crops (Kennedy 2008). The first insect-resistant transgenic plants were produced in 1987, when genes coding for a Cry toxin of Bacillus thuringiensis Berliner were expressed in tobacco and conferred resistance to Manduca sexta L. (Lepidoptera: Sphingidae) (Vaeck et al. 1987, Kennedy 2008).

Alternatively, biological control involves the use of natural enemies to suppress pest

populations at lower densities. There are three main types of biological control: classical,

augmentation, and conservation (Bale et al. 2008). Classical biological control involves

the discovery, importation, and establishment of exotic natural enemies to control an

invasive non-native species (Van Driesche et al. 2009). Successful introductions of

natural enemies cause a shift in the system, that allows it to regain its former ecological

balance, and features stable low population densities of pests maintained by the natural

enemy population (Bellows 2001). Classical biological control often has high initial

costs, but is self- perpetuating leading to permanent control of the pest species, and

economically viable in the long term (Van Driesche 1994). Pickett et al. (1996)

estimated for every dollar spent by the State Biological Control Program and the

University of California, approximately $181 in wholesale and $245 in retail esthetic value was saved by the introduction of Encarsia inaron (Walker) (Hymenoptera:

Aphelinidae) for the control of the invasive ash whitefly Siphoninus phillyreae (Haliday)

(Hemiptera: Aleyrodidae). While classical biological control offers permanent control over large areas, the two remaining types of biological control only offer temporary pest suppression over a limited range (Bale et al. 2008).

Augmentative biological control is defined as the periodic release of natural enemies for control of a target pest, and includes inoculative releases and inundative releases (Van

Driesche et al. 2009, Van Lenteren 2012). Inoculative releases are the introduction of a small number of natural enemies early in the crop cycle with the expectation that they

will reproduce and the offspring will continue to provide control for an extended period

of time (Van Driesche et al. 2009). Inundative releases, in contrast, are the mass release of natural enemies to provide immediate control (Van Driesche et al. 2009, Van Lenteren

2012). Because augmentative biocontrol relies on commercially produced natural

enemies, it’s use is limited by cost, availability, quality, and field effectiveness of the

released species (Van Driesche et al. 2009). In a review by Collier and Van Steenwyk

(2004), augmentation reduced pest populations below target thresholds in only five out of

thirty-one cases, with an additional six cases where augmentation was not consistently

adequate, and essentially failed in 64% of cases. The review also found that in most cases

augmentative releases were more expensive than pesticide alternatives. However, a

number of studies have demonstrated augmentative releases to be efficacious and cost

effective (Moreno and Luck 1992, Trumble and Morse 1993, Collier and Van Steenwyk

2004, Stansly et al. 2005).

Conservation biological control is defined as the manipulation of cultural practices to

minimize the factors that harm beneficial species and enhances the habitat for natural

enemies already present in the field (Tscharntke et al. 2007, Van Driesche et al. 2009).

Conservation biological control is often neglected because it requires in-depth knowledge

of the ecology of natural enemies, and their associated ecological communities, for

successful implementation (Jonsson et al. 2008). Availability of shelter and non-prey

food can improve the efficacy of natural enemies and are key components of

conservation biological control programs. Useful practices may include creation of

physical refuges, provision of places for alternative hosts to live, planting flowering

plants as nectar sources, or cover crops to moderate temperature and humidity (Van

Driesche et al. 2009). Habitat management practices for conservation biological control may not only improve the efficacy of natural enemies but can also enhance other ecosystem services (Fiedler et al. 2008, Jonsson et al. 2008).

Objectives

The objectives of this project are to (1) Determine the developmental rate of Myoporum

thrips , K. myopori, (egg to adult) at different temperatures, (2) Determine the potential

host range and preference of K. myopori for different species and cultivars of Myoporum,

and (3) Investigate the predator complex of K. myopori, using various molecular

techniques, and the biology of these species to determine if they are suitable for

augmentative or conservation biological control.

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Chapter 2

Predicting the Potential Invasive Range of Klambothrips myopori

Introduction

An estimated 50,000 non-native species have been introduced into North America since the arrival of Europeans about 500 years ago (Pimentel et al. 2000). An invasive species can be defined as, an introduced species that advances without direct human assistance and threatens natural or semi-natural habitats outside its natural distribution range, causing economic, social or environmental impacts (McNeely 2001). Invasive insects can affect native biodiversity and ecosystems through direct interactions (e.g. a herbivore feeding on a native plant), or indirectly (e.g. competition for food with native species)

(Kenis et al. 2008). Pimentel et al. (2005) estimates that crop losses and control costs amount to $13.5 billion/year for invasive insects in the United States. Invasive insect herbivores can be particularly harmful to plant populations, particularly on islands, sometimes driving them to local extinction (Kenis et al. 2008).

Myoporum is a genus comprised of 30 species (Chinnock 2007). Traditionally placed in the Myoporaceae along with the genera Eremophila and Bontia, they are now considered to be a members of the Scrophulariaceae (Olmstead et al. 2001). While the greatest diversity of Myoporum is found in Australia,18 of the 30 species occur there (Chinnock

2007), the genus occurs throughout the Pacific, including New Zealand, New Guinea,

New Caledonia, Japan, China, Hawai’i, Tahiti, the Mariana and Norfolk islands, and extends westward into the Indian Ocean on the Mauritius and Rodriguez Islands (Figure

2.1) (Heenan and de Lange 2011). While most species are erect woody shrubs or small trees (e.g. M. montanum Brown), some are more prostrate in form (e.g. M. parvifolium

Brown). Myoporum are generally considered to be very hardy plants tolerant to drought,

fire, frost and grazing, and have been effectively utilized for cultural, food, medical, and

horticultural purposes (Richmond and Ghisalberti 1995).

The Australian Aboriginal culture utilized Myoporum in their hunting and battle

practices. Resins from several species (e.g. M. platycarpum Brown) were applied to twine

used to attach tomahawk heads to handles and fasten flints to spears (Richmond and

Ghisalberti 1995). The wood was used to make protective shields and woomeras (spear-

throwing sticks) (Richmond and Ghisalberti 1995). The wood of several species

including M. sandwichense Gray and M. insulare Brown, has been used for dwelling and

canoe construction (Richmond and Ghisalberti 1995). Although not a significant part of

the diet, the manna-like exudates of M. platycarpum were exploited by aboriginals in

times of famine and reported to have a sweet taste (Richmond and Ghisalberti 1995).

Myoporum was not as popular as the related genus Eremophila in traditional medicine,

but it was still widely utilized (Richmond and Ghisalberti 1994). Various species have

been used as a cure for headaches, as a laxative, a cure for venereal disease, a remedy for

toothaches, and an antidote for poisons (Brooker and Cooper 1961, Richmond and

Ghisalberti 1995). The essential oils of Myoporum, primarily furanosesquiterpenes, are known to be poisonous to livestock but also show significant insecticidal activity against leafcutting ants (Roussis and Hubert 1992), grasshoppers (Grant et al. 1980), and Pieris rapae (Guohua et al. 1999). The hardiness of Myoporum has made the genus a popular horticultural plant, and can now be found in numerous countries on every continent except Antarctica. In south western European countries such as Spain, Italy and Portugal,

trees are used as windbreaks (Richmond and Ghisalberti 1995). In California M. laetum

has been planted along 1000’s of kilometers of roadsides, and has naturalized in coastal

areas (Mound and Morris 2007a). In its native range, M. laetum has no major pest

associations (Mound and Morris 2007a). However, the closely related M. insulare

commonly supports considerable populations of thrips (Mound and Morris 2007a).

In 2005, an unidentified species of thrips was found attacking the foliage of Myoporum laetum in Orange County, California (Mound and Morris 2007a). This species has since been described as Klambothrips myopori (Thysanoptera: Phlaeothripidae) (Mound and

Morris 2007a). Within three years of discovery, K. myopori had spread over 450 miles north to San Francisco, and was discovered in Hawai’i with extensive feeding damage killing the Hawaiian native, Myoporum sandwicense (Mound and Morris 2007a, Conant et al. 2009b). In both California and Hawaii, K. myopori has spread rapidly wherever host

Myoporum is planted, causing unsightly damage characterized by gall-like symptoms and severe distortion of new leaves (Mound and Morris 2007a). Thrips populations can build up in large numbers within the folded leaves of the galls, causing terminal growth to be stunted, and in severe cases, causes branch or whole plant death (Sullivan 2014).

Invasive species, such as K. myopori, pose a threat to natural and managed ecosystems, creating a need for tools that can aid in risk assessment (Sutherst and Maywald 2005,

Venette et al. 2010). One approach is to use ecological niche models to predict the potential distribution of invasive species. This method incorporates the ecological niche concept that a species will be limited to establish only in areas that match the set of

ecological conditions in which they encounter in their native distribution (Peterson 2003,

Kumar et al. 2014). Two popular ecological niche models are CLIMEX and Maxent.

CLIMEX is a mechanistic niche model that uses a species functional traits and

physiological tolerances to predict potential distributions (Sutherst 2003, Lozier and

Mills 2011, Kumar et al. 2014). Maxent is a correlative niche model that predicts habitat

suitability by finding the probability distribution of maximum entropy (i.e. that is most

spread out, or closest to uniform), using known locality data (Phillips et al. 2006, Lozier

and Mills 2011, Kumar et al. 2014). Although the models differ in their assumptions and

modeling procedures, the comparison of the models will help elucidate the potential

distribution of K. myopori.

The objectives of this study are to: (1) determine the developmental rate of K. myopori

(egg to adult) on M. laetum at different temperatures, (2) identify global regions with

habitats suitable for K. myopori using the ecological niche modeling programs Maxent and CLIMEX, (3) develop potential distribution maps.

Materials and Methods:

Developmental rate of K. myopori

Host plants

All studies were conducted using greenhouse plant stock. All stock plants were grown for

2 years without the use of pesticides prior to taking cuttings to use in experiments.

Paternal plants were procured from various nurseries in southern California. Cuttings

were then taken from the M. laetum stock plants and rooted in individual 6.35 cm (2 ½”)

liner pots, using hormex rooting powder #8 (Brooker Chemical Company, Chatsworth,

California, USA). The soil media used was a ratio of 10:7:4, fir bark: peat moss: perlite

mixed with Osmocote 18-6-12 (Scotts Miracle-Gro Company, Marysville, Ohio, USA).

The cuttings were then placed on a mist bench, with mist every 15 minutes for 10 seconds, and bottom heat to maintain soil temperature at ~25°C. All fully rooted cuttings

used for the studies were ~20 cm in height.

Constant temperature experiment

All studies were conducted using thrips collected from a colony of K. myopori that had been reared on M. laetum in a greenhouse environment (15-35° C with ambient light and

humidity). The colony was established in the greenhouse using 100 male and 100 female

specimens collected from M. laetum on the campus of the University of California,

Riverside in 2012. A single female thrips was placed on a M. laetum cutting and enclosed

in a mesh bag. The enclosed plant/thrips was then placed in a temperature chamber

(Percival-Scientific, Iowa, USA) at one of seven constant temperatures (15°, 17°, 20°,

25°, 30°, 34°, and 35.5° C), relative humidity of ~60%, and a photoperiod of 16:8 (L:D)

hours. Groups of 30 plants were placed in each temperature chamber, with two replicates

for each temperature. Observations were made every 24 hours until thrips reached

adulthood. To measure the developmental period, after the first eggs had been laid, the

female and all eggs except one were removed. The remaining egg was then used to

determine the development of the thrips.

Development rate and models

The results of the constant temperature experiment were used to model developmental

rate (1/developmental period) from egg to adult and estimate developmental thresholds.

The relationship between temperature and development rate of K. myopori was analyzed

using one linear and three nonlinear models. In the linear model, for the most precise

estimation of K and Tmin only the linear part of the relationship between temperature and

development was used; thus, the data recorded for 35.5° C was not used. Using the

parameters estimated by the linear regression, the lower temperature threshold Tmin was

calculated by extrapolating the regression line to the temperature axis, Tmin = -a/b, and the

thermal constant (K) is the reciprocal of the slope, K = 1/b. Additionally, three nonlinear

models (Lactin et al. 1995, Briere et al. 1999) were also fit to the K. myopori development data:

The first two models were proposed by Briere et al. (1999) for modeling the influence of temperature on insects.

1/2 Briere-1: D(T) = aT(T-Tmin)(Tmax-T) (1)

1/m Briere-2: D(T) = aT(T-Tmin)(Tmax-T) (2)

The parameters are Tmin (lower temperature threshold), Tmax (upper temperature

threshold), a (equation constant) and in Briere-2, m (equation constant).

The third model was proposed by Lactin et al. (1995) as an improvement on the Logan

model (Logan et al. 1976) for modeling the insect developmental rate.

Lactin-1: D(T) = e(ρT) - e(ρTmax-(Tmax-T)/∆) (3)

The parameters ρ and ∆ are equation constants.

Statistical analyses

The parameter values of the linear and nonlinear functions were estimated using the

PROC REG and the PROC LNIN in SAS (Institute 2011). The suitability of linear and

nonlinear models was evaluated based on the Akaike information criteria (AIC)

(Burnham and Anderson 2004), with lower AIC values indicate more preferred models.

AICC was used in place of AIC due to small sample size (n/p<40):

AIC = nln(RSS/n)+2p

AICC = AIC+ 2p(p+1)/(n-p-1) where n is the number of observations, RSS is the residual sum of squares and p is the

number of parameters estimated.

Ecological niche modeling

CLIMEX

CLIMEX is a simulation model that infers the response of a species to climate from its geographical distribution and seasonal phenology (Sutherst and Maywald 1985, Sutherst

2003, Sutherst and Bourne 2009). It incorporates a hydrological model to integrate the effects of rainfall and evaporation into a moisture index (Sutherst 2003). The moisture index is then combined with a temperature response curve to produce weekly and annual

Growth Indices, which indicate the favorability of the environment for population growth

(Sutherst 2003, Hoddle 2004, Lozier and Mills 2011). The model also uses four stress indices (wet, dry, cold and hot), which estimate the survivorship during prolonged or extreme periods of adverse conditions that ultimately define the potential climatic boundaries of a species distribution (Sutherst 2003). The weekly values of each stress index are summed to annual indices that are used to generate an Ecoclimatic Index (EI), which is scaled from 0 to 100 to provide a measure of the suitability of a given environment for the persistence of a population. Locations with an EI < 10 indicate an unfavorable environment, an IE of 10-30 represents a favorable environment, and an EI >

30 is highly favorable (Sutherst 2003, Sutherst and Maywald 2005). An EI value of zero indicates a species cannot persist at that location.

The “Compare Locations” function in CLIMEX was used to develop the simulation model for K. myopori. The CliMond climatic dataset (Kriticos et al. 2012) interpolated at

10 arc minute resolution was used for modeling. The CliMond data set has long-term monthly climate means centered on 1975 for precipitation, maximum temperature, minimum temperature, and relative humidity at 0900 and 1500 hours (Webber et al.

2011, Kriticos et al. 2012, Kumar et al. 2014). Values for CLIMEX model parameters were defined based on the laboratory studies outlined above, and iteratively adjusted until the simulation model matched the known distribution of K. myopori (Table 2.1).

MaxEnt

Maxent is a maximum entropy species distribution model (Phillips et al. 2006, Lozier and

Mills 2011). Entropy in this context measures the amount of information that is contained

in a random variable (Phillips and Dudík 2008). Maxent uses presence-only locality data

to estimate a target probability distribution by finding the probability distribution of

maximum entropy (i.e., that is most spread out, or closest to uniform), subject to a set of

constraints that represent our restricted information about the true distribution and

environmental conditions (Phillips et al. 2006, Lozier and Mills 2011, Kumar et al. 2014).

Eighty percent of occurrence data was used for training the Maxent model, with the

remaining twenty percent reserved for independent validation of model performance

using the area under the receiver operating curve (AUC) statistic (Phillips et al. 2006).

Default Maxent setting was used with the “fade by clamping” option selected to

minimize model projections outside the environmental conditions of the training data.

Results

Development time

Klambothrips myopori successfully completed development from egg to adult in all temperatures evaluated (Table 2.1). The development time of K. myopori decreased until

temperature reached 34°C, above which development time began to increase. The

development time from egg to adult was longest at 15°C (85.5 ± 0.7 days) and shortest at

34°C (17.7 ± 1.8 days). The duration of immature stages and the time required to

complete the cycle from egg to adult were significantly affected by temperature (Table

2.2).

Model evaluation

The relationship between the developmental rate of K. myopori and temperature was

described using linear and nonlinear functions (Figure 2.2). The lower developmental

thresholds and thermal constants were estimated using linear regression (Table 2.3). The

lower developmental thresholds were estimated to be 11.6, 9.5, 9.5, 11.1, and 10.3 °C for

egg, 1st instar, 2nd instar, pupa, and the immature stages combined, respectively.

According to the linear regression, K. myopori requires 378.79 degree-days above the

lower threshold of 10.3 °C to complete development from egg to adult.

The estimated parameter values of the nonlinear models are presented in Table 3. The

nonlinear models provided a good fit to describe the relationship between temperature

and development rate of K. myopori (Figure 2.2, Table 2.4). The Briere-1 model showed

the lowest values of RSS and AICC (Table 2.4). It was therefore determined that the

Briere-1 model is the preferred model.

Ecological niche modeling

CLIMEX

Projections from CLIMEX recovered the known invasive range of K. myopori in

California (Figure 2.3) and Hawaii (Figure 2.4). In California, favorable environments

were predicted from the coast and into the central valley up to the Sierra Nevada

mountain range. In Hawaii, the islands of Kaua’i, O’ahu, Lan’I, and Maui are favorable

for K. myopori. The model also predicted the known invasive localities to be very

favorable environments, with a mean EI = 40.0 (27-49) versus a mean EI = 7.2 (0-36) for non-known localities in California and Hawaii. Based on the good discriminative performance in the known invasive range the model is likely to be useful for characterizing K. myopori’s potential invasive range.

In North America, the model predicts most regions in Mexico are capable of supporting

K. myopori (Figure 2.5). Within the United States, the west coast (Figures 2.5), Hawaii

(Figure 2.4) and southeastern parts (Figure 2.5) are strongly predicted to be suitable habitat. Suitable regions in Australia include Coastal Australia and Tasmania (Figure

2.6). In South America Peru, Ecuador, Colombia, Venezuela, Brazil, Paraguay and northern Argentina are favorable (Figure 2.7). In Europe the most suitable locations are along the Mediterranean coast (Figure 2.7). Suitable areas in Africa include areas south

of ~15°N, Madagascar, and the Mediterranean coast (Figure 2.7). In Asia, similar to

Africa, most locations south of ~15°N are very suitable habitat (Figure 2.7).

Maxent

The Maxent model predicts the regions around the Tropic of Cancer in North America,

Africa, and Asia as capable of supporting K. myopori populations (Figure 2.8). The model also predicts regions around the Tropic of Capricorn in South America and Africa

as favorable. Several coastal areas throughout the world are also suitable including; the

Brittany region in France, the Mediterranean coast of Libya and Egypt, coastal South

Africa, the northern coast of Australia as well as the area surrounding the Great

Australian Bight, and regions of the west coast and southern Florida of the United States.

Temperature seasonality contributed most to the model, followed by mean temperature of

the coldest quarter (Table 2.5). While projections from Maxent model recovered the

invasive range in California (Figure 2.9), it failed to adequately recover the known native

range of K. myopori in Australia (Figure 2.10). The poor performance in the native range

the model is not likely to be useful for characterizing the potential invasive range of K.

myopori.

Discussion

Invasive species are one of the leading threats to natural ecosystems and biological

diversity, and impose an enormous cost on agriculture, forestry, and other human

enterprises (Wittenberg and Cock 2001). Prevention is the most cost-effective

management strategy for invasive species (Wittenberg and Cock 2001, Bogich et al.

2008, Simberloff et al. 2013). Early detection is often crucial for determining whether

eradication of a species is feasible (Wittenberg and Cock 2001). As time since

introduction of an invasive species increases, the efficacy of management strategies

decrease and the management costs and impact of the invader increase (Simberloff et al.

2013). Predictive modeling is an important tool to help determine the potential range of

invasive species in novel geographic regions and determine those areas of greatest risk.

Once those areas of greatest risk are determined, monitoring and management programs

can be established to ensure early detection and mitigate the impact of potential invaders.

Klambothrips myopori has shown a propensity to spread rapidly and invade nonnative habitats. K. myopori is a major threat to native and ornamental plantings of Myoporum

spp. throughout the world causing gall-like symptoms, severely stunting terminal growth

and often leading to plant death (Mound and Morris 2007a, Sullivan 2014). In California

Myoporum are popular ornamentals, planted along 1,000’s of km of highway as a screen

planting, and as a groundcover for erosion control (Mound and Morris 2007a). Originally

discovered in Orange County in December of 2005, the thrips was reported in four

surrounding counties within a year. In 2008 K. myopori was discovered in the San

Francisco Bay area. However, some coastal counties with Myoporum had yet to discover

the thrips leaving a gap in populations (Cameron and Mound 2013, Sullivan 2014). By

2010 only Monterey County along the coast had yet to report the thrips (Hoddle 2013). In

surveys conducted between 2012 and 2014 K. myopori was found in 19 counties leaving

no known populations of Myoporum unaffiliated with the thrips (Shogren, personal

observation).

The relationship between insect developmental rate and temperature is critical for

understanding population dynamics (Logan et al. 1976), which establish the thermal

tolerances of a species which are used in predictive modeling. The linear model

(Campbell et al. 1974) is most commonly used for calculating the lower thermal

thresholds and thermal constants due to its ease of calculation (Damos and Savopoulou-

Soultani 2011). The rate of development of K. myopori decreased with an increase in

temperature between the ranges of 15-34°C. Linear regression estimated a lower

developmental threshold of 10.3°C, comparable to another invasive galling thrips

Gynaikothrips ficorum, which had an observed lower threshold of 12°C (Paine 1992).

This can be extrapolated to phenological models to predict the occurrence of different life stages in the field, enabling control measures to target vulnerable life stages (Wagner et al. 1984).

However, the precision of the linear model lies within a limited range of temperatures, producing unreliable predictions in extreme conditions in which the relationship is non-

linear (Logan et al. 1976, Damos and Savopoulou-Soultani 2011). For K. myopori temperatures above 34°C represent sub-optimal conditions, represented by increased development time, requiring the use of non-linear models. The Lactin model showed a relatively poorer fit to the observed data, as reflected in high RSS and AICC values. The

Briere-1 model best described the relationship between temperature and developmental rate of the pest. The model showed high goodness-of-fit for all life stages, confirmed by the low RSS and AICC values. The values of Tmin (11.9°C), Topt (32.5°C), and Tmax

(38.8°C) estimated by the Briere-1 model are representative of its current distribution.

Temperature influences thrips population dynamics due to its affects on insect developmental rate (Logan et al. 1976). During the winter months thrips populations are low, as the mean daily temperature is near the lower developmental threshold. In early spring when temperatures begin to increase, K. myopori populations increase rapidly presumably because of the increase in developmental rate. This is followed by a rapid decline in population numbers, which can be partially attributed to the influence of temperature on developmental rate, and partially to the interactions between the thrips and its host plant. Temperatures in late spring into summer can well exceed the upper developmental threshold at inland locations causing rapid population declines. K. myopori feeds on new apical growth, which is quickly stunted by thrips feeding as populations balloon in the spring. This feeding often leads to branch die back and the loss of food source for the thrips resulting in population decline.

Climate is one of the most important factors limiting species distribution (Ge et al. 2017).

Species distribution models (SDMs) are becoming popular to predict the potential

distribution of invasive species (da Silva et al. 2017). Of the two SDMs used in this study

CLIMEX outperformed Maxent in predicting the known localities of K. myopori. In

California, CLIMEX predicted favorable environments from the coast into the central valley up to the Sierra Nevada mountain range, while MAXENT restricted favorable environments to the coast. While Maxent performed well when predicting the invasion in

California, it failed to identify the invasive range in Hawaii or the native habitat in

Australia. Correlative models, like Maxent, integrate species occurrence data with spatial

environmental data to estimate the relative habitat suitability for a species (Kumar et al.

2014). The environmental data used is usually randomly picked from an entire region,

whereas the occurrence data is often biased towards easily accessible areas, possibly

leading to inaccurate models (Phillips et al. 2009). The CLIMEX model recovered the

invasive range in California as well as Hawaii, and the native range in Australia. While

CLIMEX is considered a comprehensive and reliable model (Kriticos et al. 2015), it does

have limitations. CLIMEX models are simplified to avoid the local effects of land use,

enabling them to be applied at the regional level (Sutherst 2014).

The limiting factor for both models seems to be extreme temperatures. For instance,

when focusing on the contiguous US, the extreme summer heat in the southwestern states

limited K. myopori to the coast. Extreme cold during the winter months resulted in low

suitability scores on the Midwest and Northeast. These results are expected based on the

temperature dependent models developed in this paper. Using the CLIMEX model to

assess the risk of invasion in other parts of the world, K. myopori has the potential to

invade native Myoporum spp. in the pacific and known ornamental plants throughout the

world.

In summary, we assessed linear and non-linear models to estimate the development rate of K. myopori. The linear model provided estimates for the lower temperature threshold as well the thermal constant, while the Briere-1 model best described the relationship between temperature and development rate. These models are important tools for predicting the timing of vulnerable life stages in the field to the optimal timing for implementing control measures. Using the CLIMEX model we now have a better idea of the potential invasive range of K. myopori. Suitable habitats include coastal United

States, most regions in Mexico, the majority of South America, the Mediterranean coast,

Africa south of ~15°N, Asia south of ~15°N, and coastal Australia.

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Table 2.1 CLIMEX parameters values for Klambothrips myopori

Index Parameter Value

Temperature DV0 = Lower Threshold 11.9°C

DV1 = Lower optimum temperature 20°C

DV2 = Upper optimum temperature 33.5°C

DV3 = Upper threshold 38.8°C

PDD = Number of degree-days above DV0 to complete one

generation 379°C days

Cold Stress TTCS = Temperature threshold 1.5°C

THCS = Stress accumulation rate -.005 week-1

Heat Stress TTHS = Temperature threshold 38.8°C

THHS = Stress accumulation rate .003 week-1

Dry Stress SMDS = Threshold soil moisture 0.15

HDS = Stress accumulation rate -.005 week-1

Wet Stress SMWS = Threshold soil moisture 1.5

HWS = Stress accumulation rate .001 week-1

Table 2.2 Development time (days) (mean ± SEM) for immature stages of Klambothrips myopori

Life Stage

Temperature

(°C) Egg 1st instar 2nd instar Pupal stages Cycle

15 23.0 ± 2.8a 21.5 ± 0.7a 20.0 ± 1.4a 21.0 ± 1.4a 85.5 ± 0.7a

17 19.6 ± 1.0b 19.3 ± 0.9b 16.9 ± 0.8b 17.3 ± 0.6b 73.1 ± 2.1b

20 13.3 ± 0.9c 13.0 ± 1.0c 8.6 ± 0.7c 11.4 ± 1.3c 46.2 ± 2.2c

25 5.9 ± 0.8d 5.6 ± 0.6d 5.1 ± 0.6d 4.5 ± 0.5d 21.1 ± 1.2d

30 4.9 ± .6e 5.4 ± .6d 4.0 ± .5e 4.8 ± .9df 19.1 ± 1.23e

34 4.5 ± .7e 5.3 ± 1.1de 4.0 ± .5e 3.9 ± .9e 17.7 ± 1.8f

35.5 5.4 ± 0.5de 4.7 ± 0.5e 4.2 ± 0.4e 4.5 ± 0.5def 18.8 ± 0.9ef

F value 1060.57 855.97 1140.05 659.27 3234

P <.0001 <.0001 <.0001 <.0001 <.0001

Means followed by different letters are significantly different according to ANOVA,

Tukey’s HSD test (P<0.05).

Table 2.3 Estimated parameters (a and b), lower developmental threshold (°C), and thermal constant (K) from linear

regression

2 Stage a b K (DD) Tmin (°C) r RSS AIC AICC

Egg -0.1277 0.0110 90.9918 11.6187 0.8394 0.6248 -9.5728 -5.5728

1st instar -0.0857 0.0091 110.4972 9.4696 0.7165 0.4971 -10.9441 -6.9441

2nd instar -0.1087 0.01145 87.33624 9.491703 0.8129 0.70035 -8.88761 -4.8876

60 Pupa -0.1373 0.01242 80.5153 11.05636 0.7031 0.95352 -7.03613 -3.0361

Cycle -0.0272 0.00264 378.7879 10.31818 0.8587 0.03531 -26.8121 -22.8121

RSS is the residual sum of square, AIC is the Akaike information criterion and AICC is the corrected Akaike information

criterion

Table 2.4 Parameter estimates (±SEM) for three nonlinear development rate models for Klambothrips myopori

Equations Parameters Life stage

Egg 1st instar 2nd instar Pupa Cycle

1.54E-4 1.09E-4 1.56E-4 1.62E-4 3.50E-4

Briere-1 a (7.94E-6) (1.1E-5) (8.40E-6) (1.5E-5) (1.56E-6)

13.3277 10.6359 11.4764 12.3156 11.876

Tmin (0.4909) (1.0487) (0.5777) (0.9240) (0.4620)

38.0376 40.0129 38.5876 38.565 38.7921

Tmax (0.2539) (0.7095) (0.2883) (0.5061) (0.2579)

RSS 0.6481 0.5939 0.7574 0.9999 0.0382

AIC -10.6570 -11.2688 -9.5660 -7.6222 -30.4680

AICC -2.6570 -3.2688 -1.5660 0.3778 -22.4680

2.04E -4 4.59E -12 7.6E -5 8.12E -7 2.19E -6

Briere-2 a (2.90E-5) (1.81E-10) (5.6E-5) (6.08E-6) (3.88E-6)

2.7166 0.2238 1.3068 0.4969 0.7341

m (0.5576) (0.3885) (0.4174) (0.4468) (0.2545)

12.482 14.3649 12.6957 14.7216 14.0073

Tmin (0.8830) (0.8461) (0.8664) (0.8785) (0.5093)

Tmax 36.9155 90.5792 41.3111 55.1533 48.3165

(0.5980) (102.5) (2.6738) (21.0415) (5.5741)

RSS 0.6481 0.5939 0.7574 0.9999 0.0382

AIC -8.6570 -9.2688 -7.5660 -5.6222 -28.4680

AICC 11.3430 10.7312 12.4340 14.3778 -8.4680

0.0101 0.0078 0.0105 0.0105 0.0028

Lactin ρ (3.23E-4) (3.64E-4) (3.44E-4) (5.25E-4) (8.9E-5)

39.287 38.2392 38.894 38.7755 40.1046

Tmax (0.1359) (0.1589) (0.1183) (0.1797) (0.1699)

1.48 0.7524 1.3099 1.219 1.1543

∆T (0.0903) (0.0989) (0.0832) (0.1256) (0.0661)

-1.1353 -1.0733 -1.1169 -1.1248 -1.0324

λ (0.01) (0.0115) (0.0110) (0.0169) (0.0024)

RSS 1.0814 1.0162 1.3973 1.6101 0.0692

AIC -5.0738 -5.5086 -3.2798 -2.2872 -24.3207

AICC 14.9262 14.4914 16.7202 17.7128 -4.3207

Table 2.5 Summary of climate variables used in the Maxent model

% contribution

Annual mean temp. 2.71

Mean diurnal range 0.26

Isothermality 2.23

Temp. seasonality 64.99

Max temp. warmest month 0.83

Min temp. coldest month 5.98

Temp. annual range 3.89

Mean temp. wettest quarter 0.02

Mean temp. driest quarter 0.52

Mean temp. warmest quarter 0.01

Mean temp. coldest quarter 18.57

Figure 2.1 Distribution map of Myoporum. Taken from Discover Life 2014.

Figure 2.2 Linear and three nonlinear functions fit to the data of developmental rates (1/days) of K. myopori.

Figure 2.3 Map of predicted environmental suitability for K. myopori from CLIMEX for

California 66

Figure 2.4 Map of predicted environmental suitability for K. myopori from CLIMEX for

Hawaii

Figure 2.5 Map of predicted environmental suitability for K. myopori from CLIMEX for

North America

Figure 2.6 Map of predicted environmental suitability for K. myopori from CLIMEX for

Australia

Figure 2.7 Map of predicted environmental suitability for K. myopori from CLIMEX for the World

Figure 2.8 Map of predicted environmental suitability for K. myopori from Maxent

Figure 2.9 Map of predicted environmental suitability with known localities for K. myopori in the invasive range in California

Figure 2.10 Map of predicted environmental suitability with known localities for K. myopori in the native range in Australia and Tasmania from Maxent

Chapter 3

Host Plant Preference and Performance of Klambothrips myopori (Thysanoptera) in Southern California

Introduction

Myoporum is a genus of hardy flowering plants comprised of 32 species and several

commercial cultivars. In California, there are about 10 varieties of Myoporum that are

commercially available. The drought hardiness of Myoporum, lack of suitable

replacement species, and the fact that the plants are generally pest free, has made

members of this genus popular in the horticulture trade, with several new varieties

currently in development (Mound and Morris 2007a). A new exotic species of thrips,

Klambothrips myopori Mound and Morris, has recently become a serious pest on

Myoporum laetum Forst and other members of the genus, inducing considerable leaf

deformation through its feeding activities. Since its initial discovery in Orange County,

California in 2005, K. myopori has spread to more than ten counties throughout

California and reached the island state of Hawaii in 2009 (Mound and Morris 2007a),

where it kills the indigenous M. sandwicense Gray.

Myoporum laetum was a popular, widely planted ornamental for several decades before the accidental introduction of K. myopori. Myoporum laetum was one of several drought tolerant species from New Zealand planted in ornamental settings throughout California beginning as early as the 1860s (Sullivan 2014). It was increasingly popular after the

Panama Pacific International Exposition in San Francisco in 1915, and after the publication of New Zealand Plants Suitable for North American Gardens by Leonard

Cockayne (1914) (Sullivan 2014). Due to the hardiness of M. laetum, by the early 1950’s, it was widely planted in residential landscapes throughout coastal California and along thousands of miles of highways throughout the state (Mound and Morris 2007a, Sullivan

2014). Although M. laetum is no longer a species of choice for residential or highway

plantings due to the extensive feeding damage caused by K. myopori, it still remains as a

dominant planting throughout much of California. In general, the horticulture trade has

seen an increase in the production of many drought and pest tolerant species, including

various Myoporum species and varieties.

Pedigo et al. (1986) stated that pest management decisions are often based on two

fundamental questions: can the number of feeding insects be related to specific levels of

damage, and does the level of damage cause significant levels of injury? Damage

associated with pest and injury relative to pest abundance, as well as the cost of control

and the value of the crop itself, are then used to determine an economic injury threshold.

This holds true for plants/crops grown for economic profit, but it is not easily applicable

to home landscapes where plants are grown for their aesthetic value (Raupp et al. 1992).

In such situations, aesthetic injury levels should form the basis of management decisions.

Numerous studies have demonstrated that the majority of people would discriminate/

initiate control at injury levels at or below 10% of the affected plant (Coffelt and Schultz

1990, Raupp et al. 1992, Klingeman et al. 2000). Coffelt et al. (1990) surveyed homeowners in the city of Norfolk, Virginia, regarding their requests for pesticide treatment of the orangestriped oakworm, and found 70% of requests were for trees with

1-5% defoliation. A study conducted by Klingeman et al. (2000) on consumer perceptions of injury to plant tissues caused by azalea lace bug feeding indicated 80% of consumers have a 6-10% acceptance level of pest damage. If the acceptable aesthetic injury level to the average consumer is about 10% of the affected plant, recommendations

can then be made for plants/ cultivars that are least prone to pest damage and remain

below the 10% injury threshold.

The introduction of K. myopori into California has resulted in significant damage to

established landscape plantings of Myoporum laetum It has also affected the nursery

industry in both production and sale of potential host plants. The objectives of this study are to: (1) determine the potential host range of K. myopori on different species and cultivars of Myoporum under lab and field (inland and coastal) conditions in California,

(2) assess and score the damage to each host caused by K. myopori feeding, (3) determine the host preference of K. myopori, (4) develop recommendations for cultivars least prone to feeding damage.

Materials and Methods:

Host Plants

All studies were conducted using greenhouse vegetatively propagated plant stock grown at the University of California, Riverside Agricultural Research Station in Riverside,

California. “Mother stock plants” were procured from various nurseries in southern

California. All stock plants were grown for 2 years without the use of pesticides prior to taking cuttings to use in experiments. Cuttings were taken from the Myoporum stock plants and rooted in individual 6.35 cm liner pots, using Hormex rooting powder #8

(Brooker Chemical Company, Chatsworth, California, USA). The soil media used was a ratio of 10:7:4, fir bark: peat moss: perlite mixed with Osmocote 18-6-12 (Scotts Miracle-

Gro Company, Marysville, Ohio, USA). The cuttings were then placed on a mist bench,

with mist every 15 minutes for 10 seconds, and bottom heat to maintain soil temperature at ~25° C. All fully rooted cuttings used for the studies were ~20 cm in height.

Host range of K. myopori: Lab Protocol

A study was conducted to assess plant quality of various Myoporum cultivars as potential hosts for K. myopori. All studies were conducted using thrips collected from a colony of

Klambothrips myopori that had been reared on M. laetum in a greenhouse environment

(15-35° C with ambient light and humidity). The parent colony was established using 100 male and 100 female specimens collected from M. laetum on the campus of the

University of California, Riverside. The cultivars tested as potential hosts included: M. laetum, M. laetum ‘Clean ‘n Green’, M. ‘Pacificum’, M. parvifolium, M. parvifolium

‘Pink’, and M. parvifolium ‘Putah Creek’. These varieties were selected because they are the main horticultural varieties in production in California. A single mated female thrips was placed on each Myoporum cutting using a fine paintbrush. The cuttings were then placed in individual mesh bags to completely enclose the plant and prevent the thrips from moving off the host. The enclosed cuttings were then placed in an environmental chamber (Percival-Scientific, Iowa, USA) at 25° C with a photoperiod of L16: D8 hours.

Observations were made every 24 hours to record the first oviposition, days to larval emergence, larval survival, and total development time for each stage. After the first eggs had been laid, the parental female and all but one egg were removed (N= 30). The remaining egg was allowed to hatch to determine development time for K. myopori on each variety and the survival of the offspring on each given host.

Host range of K. myopori: Field Protocol

A common garden study was conducted to examine the population dynamics and damage

of K. myopori under field conditions. Myoporum varieties were either purchased in #1

nursery containers from commercial growers, grown insecticide free, or selected from

greenhouse stock plants. Plants were approximately .5 m tall by .5 m wide at time of

planting. Potential hosts tested included: M. laetum, M. laetum ‘Clean ‘n Green’, M.

‘Pacificum’, M. parvifolium, M. parvifolium ‘Pink’, and M. parvifolium ‘Putah Creek’.

The two field locations utilized in the experiment were: the South Coast Research and

Extension Center (SCREC) in Irvine, California and a commercial grower in San Jacinto,

California. These two sites were selected due to prior knowledge of existing thrips populations, and climatic differences. Host plants were planted in May, 2015, in a randomized block design. Plants were spaced 1.4m between treatments to ensure that the plants did not touch each other, minimizing movement of thrips between treatments. Tip samples (15cm in length) were randomly collected from each cardinal direction on a monthly basis to quantify thrips population numbers and identify associated predators.

Whole plants were also rated for the level of injury induced by K. myopori (see injury ratings below). The experiment ran for 12 months. At the San Jacinto site no data were collected from December 2015- April 2016 as cold temperatures caused severe damage to host plants. Frost damage was removed from the host plants, and the host plants were allowed to recover before sampling continued.

Injury Ratings

The ratings range from 1, representing no or trace levels of thrips and damage below 5% of the total plant, to 5, representing severe infestation and damage above 20% of the total plant (Table 3.1). The “percent infestation” of each plant was measured in terms of

“percentage of tips infested” relative to the whole plant.

Statistical Analysis Survival analysis is a biostatistics method used for analyzing event occurrence data, i.e. thrips surviving to adulthood, (Marquenie et al. 2002). Kaplan-Meier distributions are stepped survivorship curves that add information as each event occurs. The survival curve can be estimated using the Kaplan-Meier estimator Ŝ(t). The estimator takes into account both censored (thrips that did not reach adulthood) and uncensored (thrips that survived to adulthood) data. The estimator can be defined as

( ) ( ) ( ) = ( ) 푟 푡푖 − 푑 푡푖 Ŝ 푡 � 푖 푡푖<푡 푟 푡 where r(ti) is the number of objects at risk, and d(ti) is the number of observed events

(Cox and Oakes 1984, Crawley 2012).

The Cox Proportional Hazards model was used to analyze the survival data. The model assumes the hazard is in the form of

( ; ) = ( ) ( )

푖 0 푖 where Zi(t) is the set of explanatory휆 variables푡 푧 휆for 푡individual푟 푡 i at time t.

The proportion of thrips surviving to adulthood among each variety was analyzed using a

generalized linear model (Team 2000). The average development time of K. myopori was

analyzed using analysis of variance (ANOVA). The number of thrips and natural enemies

collected in the garden study was log transformed to homogenize variances and

normalize data. A generalized mixed model (R Team 2000) was then used to analyze the

number of K. myopori and natural enemies on different host varieties. Mixed linear

models were used to analyze the damage induced by K. myopori on each variety (Team

2000). Due to incomplete collection data for the San Jacinto site, models were run with

SCREC and San Jacinto for the seven months in which collections overlap, and each

collection site individually.

Results:

Host range of K. myopori: Lab Study

For the six varieties of Myoporum tested, K. myopori failed to complete development on

M. ‘Clean n Green’ and M. ‘Putah Creek’ (Table 3.2). Variety had a significant effect on the mean development time (F=234.25, P<.0001). On average, K. myopori completed development in the least amount of time on M. laetum (21.1 days), followed by M. ‘Pink’

(21.6 days), M. ‘Pacificum’ (22.3 days), and M. parvifolium (23.0 days) respectively

(Table 3.2).

There were significant differences in the survival distribution curves of K. myopori on the four Myoporum varieties suitable for complete development (Figure 3.1). The lowest line is the distribution curve for M. laetum representing a higher proportion of K. myopori

have survived to adulthood during the study period. Variety had a strong effect on the

proportion of thrips reaching adulthood (χ2=39.13, df=5, P<.0001). M. laetum had the

largest proportion of thrips surviving to adulthood (1.00), followed by M. ‘Pacificum’

(0.83), M. parvifolium (0.73), and M. ‘Pink’ (0.33) respectively (Figure 3.2).

Host range of K. myopori: Field Study

Garden Study

The mean number of thrips per plant at each site is displayed in Figure 3.3. When

analyzing the overall model for both sites, variety (χ2=48.15, df=5, P<0.001), site

(χ2=5.04, df=1, P=0.025), and date (χ2=22.91, df=6, P<0.001) had a significant effect on

the number of thrips per plant. At the South Coast Research and Extension Center there

was a significant effect of variety (χ2=85.48, df=5, P<0.001) and date (χ2=42.74, df=11,

P<0.001) on the number of thrips per plant. At the San Jacinto site variety (χ2=57.50,

df=5, P<0.001) and date (χ2=39.89, df=6, P<0.001) also had a significant effect on the

number of thrips per plant.

The mean number of predators per plant at each site is displayed in Figure 3.4. For the

combined model: variety (χ2=22.28, df=5, P<0.001), site (χ2=5.34, df=1, P=0.021), and

date (χ2=23.07, df=6, P<0.001) had a significant effect on the number of predators per

plant. Predators collected at the SCREC are displayed in Table 3.3. At the SCREC there

was a significant effect of variety (χ2=21.86, df=5, P<0.001) and date (χ2=36.42, df=11,

P<0.001) on the number of predators per plant. Predators collected at the San Jacinto site

are displayed in Table 3.4. At the San Jacinto site only variety (χ2=11.50, df=5, P=0.042) had a significant effect on the number of predators per plant.

Damage Scores

For the six varieties of Myoporum tested, K. myopori damage was only observed on M. laetum and M. ‘Pacificum’ (Figure 3.5). When analyzing the overall model for both sites, variety (χ2=65.31, df=5, P<0.001) and date (χ2=24.19, df=6, P<0.001) had a significant

effect on the damage score. At the SCREC site only variety (χ2=55.68, df=5, P<0.001)

had a significant effect on the damage score. At the San Jacinto site, variety (χ2=29.31,

df=5, P<0.001) and date (χ2=15.85, df=6, P=0.015) had a significant effect.

Discussion

All insects are ecologically specialized to some extent with respect to abiotic conditions

and biotic resources (Forister et al. 2012). Phytophagous insects exhibit preferences for particular host plants but vary in the range of host plant specificity (Doederlein and Sites

1993). It is rare to find an insect that feeds indiscriminately on all the plants in its geographical range, or one that exhibits extreme monophagy (Thorsteinson 1960,

Doederlein and Sites 1993). Phytophagous insects have been classified in various ways

according to their food-plant preferences, including the crop on which they are found

(e.g. vegetable, fruit, forage, or forest insects) or according to the part of the plant injured

(e.g. foliage feeders, bark or stem borers, and gall formers) (Thorsteinson 1960).

Gall-forming thrips have been collected from a wide range of plant orders and families

(Crespi et al. 1997). They primarily attack trees and shrubs, and most species appear to be host specific (Dreger-Jauffret and Shorthouse 1992, Crespi et al. 1997). Using Mound’s

(1994) compilation of host records, which shows a given genus of gall thrips often exploits multiple plant families, Crespi et al. (1997) proposed host shifting is likely a common occurrence due to the relatively poor flight abilities of thrips and their willingness to feed on novel host plants. Crespi et al. (1997) also noted the presence of related gall thrips using related hosts may suggest cospeciation or biases in host shifting.

In laboratory studies K. myopori performed best on M. laetum. K. myopori completed

development quickest on M. laetum (21.1±.22) and had the highest survivorship (100%).

Thrips failed to complete develop on M. ‘Clean n Green’ and M. ‘Putah Creek’. One

hypothesis for the observed differences in insect development on different hosts is a

difference in host resource quality. Protein is the major nutrient required by

phytophagous insects for physiological maintenance, and is often the limiting factor for

insect development (Schoonhoven et al. 2005). In a study by Brown et al. (2002) the level

of soluble protein in host plants correlated to their susceptibility to thrips, where higher

protein levels correlated to host versus nonhost plant species. To date no analysis on the

type(s) of protein needed for thrips development has been conducted on the Myoporum

varieties used in this study, and it may be that these differences explain the different

survivorship rates seen in the experiment. Secondary metabolites of host plants can also

affect host quality for phytophagous insects. Furanoid sesquiterpene ketones, secondary

metabolites, found in Myoporum have been shown to have significant insecticidial

activity against the leafcutting ant Atta cephalotes (Roussis and Hubert 1992), they also repel mosquitoes and sandflies (Brooker and Cooper 1961), and confer immunity to attack by grasshoppers (Grant et al. 1980). It may be that the different Myoporum varieties used in the experiment sequester different secondary metabolites and this could have had an effect on thrips development.

In field studies host plant variety had a significant effect on the number of K. myopori per plant. Secondary metabolites have been demonstrated to serve as cues for host plant recognition, some of these compounds may act as positive (attractants) or negative cues

(deterrents) (Bernays 1998, Paré and Tumlinson 1999, Bruce et al. 2005, Bernays and

Chapman 2007). It is possible that among the varieties tested there are differences in recognition signals for host selection. In natural settings insects follow a sequence of behavioral responses in host selection, which include: habitat location, host location, host acceptance, and host use. In addition to behavioral cues, insects use a number of sensory cues in host selection and acceptance, including: visual, olfactory, gustatory, and tactile stimuli as well as humidity and light intensity (Bernays and Chapman 2007).

K. myopori feeds on the expanding apical leaves of its host plant, as the leaves expand the feeding damage causes the leaves to roll together and form a gall. In order for the leaves to roll together and form a gall they must be above a certain size. Varieties of Myoporum vary in leaf size. M. laetum, M. ‘Pacificum’, and M. ‘Clean N Green’ have leaves 5-10cm long, while M. parvifolium, M. ‘Pink’, and M. ‘Putah Creek’ have leaves 0.5-1.5cm long.

Across the course of the field study M. laetum (4.91±0.77) averaged the highest number

of thrips per plant, followed by M. ‘Pacificum’ (0.44±0.12), M. ‘Clean N Green’

(0.02±0.01), M. ‘Pink’ (0.01±0.01), M. ‘Putah Creek (0.007±0.00), and M. parvifolium

(0.005±0.00).

While the highest mean number of thrips corresponded to the varieties with the biggest leaves, observable feeding damage was only observed on M. laetum and M. ‘Pacificum’.

The results suggest that host suitability for K. myopori cannot be attributed to leaf size alone, but is a function of many factors that may include physical characteristics, physiological response to feeding, nutritional quality, and chemical characteristics. These differences in plant traits and host suitability should be investigated in future studies to better understand the specific traits associated with resistance to K. myopori and to improve selection for resistant cultivars.

In summary, although K. myopori can successfully colonize and reproduce on several varieties of Myoporum, they demonstrated a preference for M. laetum and M. ‘Pacificum’ in laboratory and field trials. The demonstrated host preference is also associated with enhanced thrips fitness on those hosts compared to the less preferred cultivars. The nutritional content and secondary metabolites of the tested Myoporum varieties may have effected host preference, leading to decreased colonization and overall feeding damage in certain cultivars and warrants further study. Using the aesthetic injury level of 10%, M. laetum ‘Clean ‘n Green’, M. parvifolium, M. parvifolium ‘Pink’, and M. parvifolium

‘Putah Creek’ are recommended for use in the landscape.

References Cited

Bernays, E. A. 1998. Evolution of feeding behavior in insect herbivores. Bioscience 48: 35-44.

Bernays, E. A., and R. F. Chapman. 2007. Host-plant selection by phytophagous insects, vol. 2, Springer Science & Business Media.

Brooker, S. G., and R. C. Cooper. 1961. New Zealand medicinal plants. Economic Botany 15: 1-10.

Brown, A. S. S., M. S. Simmonds, and W. M. Blaney. 2002. Relationship between nutritional composition of plant species and infestation levels of thrips. Journal of chemical ecology 28: 2399-2409.

Bruce, T. J., L. J. Wadhams, and C. M. Woodcock. 2005. Insect host location: a volatile situation. Trends in plant science 10: 269-274.

Cox, D. R., and D. Oakes. 1984. Analysis of survival data, vol. 21, CRC Press.

Crawley, M. J. 2012. The R book, John Wiley & Sons.

Crespi, B. J., a. Carmean, David A, and T. W. Chapman. 1997. Ecology and evolution of galling thrips and their allies. Annual Review of Entomology 42: 51- 71.

Dreger-Jauffret, F., and J. Shorthouse. 1992. Diversity of gall-inducing insects and their galls. Biology of insect-induced galls 295.

Forister, M., L. A. Dyer, M. Singer, J. O. Stireman, and J. Lill. 2012. Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions. Ecology 93: 981-991.

Mound, L. 1994. Thrips and gall induction: a search for patterns. Systematics association special volume 49: 131-131.

Mound, L. A., and D. C. Morris. 2007. A new thrips pest of Myoporum cultivars in California, in a new genus of leaf-galling Australian Phlaeothripidae (Thysanoptera). Zootaxa 1495: 35-45.

Paré, P. W., and J. H. Tumlinson. 1999. Plant volatiles as a defense against insect herbivores. Plant physiology 121: 325-332.

Pedigo, L. P., S. H. Hutchins, and L. G. Higley. 1986. Economic injury levels in theory and practice. Annual Review of Entomology 31: 341-368.

Raupp, M., C. Koehler, and J. Davidson. 1992. Advances in implementing integrated pest management for woody landscape plants. Annual Review of Entomology 37: 561-585.

Roussis, V., and T. D. Hubert. 1992. Total Synthesis of (+)-Myomontanone and (+)- 10,11-Didehydromyomontanone. Liebigs Annalen der Chemie 1992: 539-541.

Schoonhoven, L. M., J. J. Van Loon, and M. Dicke. 2005. Insect-plant biology, Oxford University Press on Demand.

Sullivan, J. 2014. Inadvertent biological control: an Australian thrips killing an invasive New Zealand tree in California. Biological Invasions 16: 445-453.

Team, R. C. 2000. R language definition. Vienna, Austria: R foundation for statistical computing.

Thorsteinson, A. 1960. Host selection in phytophagous insects. Annual review of entomology 5: 193-218.

Table 3.1 Injury rating scale for K. myopori on M. laetum.

Injury Thrips Population % Infestation Rating Levels of Plant 1 None - Trace <5% 2 Low 5-10% 3 Moderate 10-15% 4 High 15-20% 5 Severe >20%

Table 3.2 The mean number of days (±SE) for K. myopori to complete development at 25°C.

Mean Development Time Host Egg-Adult (days±SE)

M. laetum 21.1±.22 a

M. 'Clean n Green' Failed

M. ‘Pacificum' 22.3±.11 b

M. parvifolium 23.0±.15 c

M. ‘Pink’ 21.6±.42 ab

M. 'Putah Creek' Failed Means followed by the same letter are not significantly different (P < 0.01) using the LSMEANS/PDIFF option with a Tukey adjustment.

Table 3.3 Predators collected on Myoporum varieties from surveys between August 2015 through July 2016 at the SCREC.

Order/Family Putah Clean N Laetum Pacificum Parvifolium Creek Pink Green Araneae Salticidae 5 2 1

Coleoptera Coccinellidae 1

Diptera Syrphidae 2 4 4 1

Hemiptera Anthocoridae 60 8 4 1

Neuropetra Chrysopidae 3 1 Thysanoptera Aeolothripidae 3 1 1 4

Table 3.4 Predators collected on Myoporum varieties from surveys between August 2015 through July 2016 at the San Jacinto site.

Order/Family Putah Clean N Laetum Pacificum Parvifolium Creek Pink Green Araneae Salticidae 3

Coleoptera Coccinellidae 1

Diptera

92 Syrphidae

Hemiptera Anthocoridae 4

Neuropetra Chrysopidae Thysanoptera Aeolothripidae 1

2 χ P

Variety 39.13 <0.0001

Figure 3.1 Survival distribution curves for K. myopori on four varieties of Myoporum.

Proportion survived to adulthood 1.2 a 1 ab 0.8 b 0.6 0.4 c Prop. Survived Prop. 0.2 d d 0 Laetum Pacificum Clean N Parvifolium Pink Putah Creek Green Variety

Figure 3.2 Proportion of K. myopori surviving to adulthood on different varieties of Myoporum. Bars with the same letter are not significantly different (P < 0.01).

160 SCREC 140 120 100 Laetum 80 Pacificum 60 Parvifolium 40 Putah Creek Mean Number Number of Mean Thrips 20 Pink 0

Clean N Green 16 16 15 15 15 16 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

10 9 San Jacinto

8 7 6 Laetum 5 Pacificum 4 Parvifolium 3 Putah Creek 2 Mean Number Number of Mean Thrips 1 Pink 0

Clean N Green 16 16 15 15 16 15 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

Figure 3.3 The mean number of thrips per plant over time for each collection site.

SCREC 5

4 Laetum 3 Pacificum Parvifolium 2 Putah Creek 1

Mean Number Number of Mean Predators Pink 0

Clean N Green 16 16 15 15 15 16 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

0.6

San Jacinto 0.5

0.4 Laetum 0.3 Pacificum Parvifolium 0.2 Putah Creek 0.1

Mean Number Number of Mean Predators Pink 0

Clean N Green 16 16 15 15 15 16 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

Figure 3.4 The mean number of predators per plant over time for each collection site.

3 SCREC

2.5

2 Laetum 1.5 Pacificum Parvifolium 1 Putah Creek Mean Damage Damage Score Mean 0.5 Pink 0

Clean N Green 16 16 15 15 15 16 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

3.5 San Jacinto 3

2.5 Laetum 2 Pacificum 1.5 Parvifolium 1 Putah Creek Mean Damage Damage Score Mean 0.5 Pink 0

Clean N Green 16 16 15 15 15 16 16 15 16 16 16 15 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

Figure 3.5 The mean damage score induced by K. myopori over time for each collection site.

Chapter 4

Identification of Klambothrips myopori Predator Complex

Introduction

Klambothrips myopori Mound and Morris, the myoporum thrips, is widely distributed in

California, causing severe leaf distortion on Myoporum laetum (Mound and Morris 2007,

Cameron and Mound 2013). Since its introduction into California in 2005, K. myopori

has caused an estimated 50% decline in M. laetum populations in southern California

(Sullivan 2014). In 2009 K. myopori underwent a host shift, from M. laetum to M.

sandwichense, when it invaded Hawai’i (Cameron and Mound 2013). M. sandwichense,

locally known as naio, is highly culturally and ecologically significant (Conant et al.

2009). The endemic plant provides a unique habitat and diet component for the critically

endangered bird species, palila (Loxioides bailleui), found in the dry subalpine woodland

on Mauna Kea. Due to the ecological implications of the damage inflicted upon naio by

the myoporum thrips, interest was generated to search for the country of origin of K.

myopori, with the intention of finding possible natural enemies to be used in a classical

biological control program (Cameron and Mound 2013). Initial surveys failed to discover

any K. myopori on Myoporum laetum in the plant’s native range in New Zealand

(Cameron and Mound 2013, Sullivan 2014). Upon further inspection of the related

Myoporum insulare along coastal Tasmania and the southeast coast of Australia, K.

myopori was found causing the characteristic leaf distortion seen on other Myoporum

species in the United States (Cameron and Mound 2013).

Biological control is the action of parasites, predators, or pathogens in maintaining

another organism's population density at a lower average than would occur in their

absence (DeBach 1964). One approach to biological control has been termed “classical

biological control”, which involves the discovery, importation, and establishment of

exotic natural enemies to control an invasive non-native species (Van Driesche et al.

2009). Other types of biological control are conservation biological control and augmentation biological control. Conservation biological control is the manipulation of cultural practices to enhance natural enemies (Tscharntke et al. 2007, Van Driesche et al.

2009). In augmentation biological control, ambient natural enemy populations are typically too low to provide adequate control and require the release of additional individuals to suppress the pest population. While classical biological control involves only the use of exotic natural enemies, conservation and augmentation biological control can employ the often overlooked indigenous natural enemies (Luck et al. 1988).

In order for any type of biological program to be successful, the effectiveness of the natural enemies to be released needs to be evaluated. Luck et al. (1988) proposed six experimental designs for evaluating natural enemies; introduction and augmentation, use of cages and barriers, removal of natural enemies, prey enrichment, direct observation, and chemical evidence of natural enemy attack. Van Driesche et al. (2009) recognized four methods for evaluation of natural enemies to be used in classical biological control programs; before-and-after design (temporal design), spatial design, insecticide check method, and cage-exclusion design. Cage-exclusion experiments were employed by

Smith and De Bach (1942), and typically consists of three treatments: a closed cage, an open cage, and a no cage treatment (Van Driesche et al. 2009). Kring et al. (1985) used closed and open cages to examine the effectiveness of indigenous coccinellid predators of the introduced greenbug, Schizaphis graminum (Rondani), in Texas high plains grain

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sorghum. The experiments demonstrated the suppressive action of indigenous predators against an introduced pest.

Current management strategies of K. myopori focus on chemical and cultural control.

Limited field surveys conducted in California have revealed a diversity of indigenous predators attacking K. myopori (Sullivan 2014). Minute pirate bugs (Orius spp.) and green lacewings (Chrysoperla spp.) are encountered most often and may be good candidates for augmentative biological control due to commercial availability.

The objectives of this research component are to: (1) identify the predator complex that currently feeds upon K. myopori in California, (2) evaluate potential biological control agents, (3) and develop recommendations for use of natural enemies in augmentative biological control programs.

Materials and Methods:

Monthly Regional Survey

To determine the population densities of K. myopori present in the field, and the predators associated with them, M. laetum populations in three southern California counties were sampled on a monthly basis for 12 months. The three locations sampled were Oceanside (San Diego County), Huntington Beach (Orange County), and Hemet

(Riverside County). These three locations were selected because they represent different habitats (Table 4.1) in which the main host, M. laetum, can be found. Each site contained a minimum of 10 M. laetum at least 1.5 m in height. From each of five trees (replicates)

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randomly selected, three 15-cm branch tips (subsamples) were arbitrarily removed from various heights and directions with hand pruners. The samples were returned to the laboratory and stored at -70º C until processed. For each branch tip the number of thrips

(all life stages) and the species identification, abundance, and life stages of predators were recorded.

Separate mixed linear models were used to analyze the number of thrips and natural enemies per tree (R Team 2000). Due to incomplete collection data for Huntington

Beach, models were ran with Hemet and Oceanside for the entire 12 month collection period, and for Jan-May 2015 for all three collection sites together.

Cage Study

Cage studies were conducted at two sites in southern California: the South Coast

Research and Extension Center in Irvine and at a commercial nursery in San Jacinto.

These two sites were selected to represent the coastal (36.6 cm annual precipitation) and inland (31.6 cm annual precipitation) habitats in which K. myopori and its host M. laetum are found (Arguez et al. 2012). Myoporum laetum used in the experiment were approximately 0.5 m tall by 0.5 m wide, in #1 nursery containers. All host plants were from greenhouse stock, grown in a pest and predator free environment.

The four treatments for the study were closed-cage, open-cage, no-cage, and sentinel (no inoculated thrips, no cage). The potted plants were set out in cages with one plant per cage. The closed cages (61x46 cm with 150 x 150 micron mesh) were designed to exclude all possible predators from the host plants. Open cages were designed similar to 102

closed cages except two sides of the screening were removed to allow natural enemies access to the host plant. The no cage treatment allowed for comparison with the open cage treatment to test for possible cage effects. The sentinel treatment measured colonization rate, the number of thrips arriving during the course of the experiment.

All treatments, except sentinel, were artificially infested with K. myopori. Fifteen female adult thrips and 25 immature thrips were added to each plant and allowed to establish for one week during which time plants were caged. Once the thrips were established, the cages were removed from the sentinel treatment and the sides lifted on the open cages.

Plants were then examined two weeks after establishment. For examination, the plants were harvested and all plant and leaf matter individually bagged and brought back to the laboratory to record the densities of all insect inhabitants. The experiments were conducted as a randomized block design with five blocks. Each block consisted of one replicate of each cage treatment. The experiments were repeated three times.

For the cage studies, the number of thrips per cage was first analyzed between the open and uncaged treatments for each site (PROC GLM, SAS Institute 2011) to test for cage effects (Van Driesche et al. 2009, Butler and Trumble 2012). Analysis showed no significant (P > 0.05) cage effects therefore, data from open and uncaged treatments were pooled. The number of thrips per cage was then log transformed to homogenize variances and normalize data. Because no thrips were recovered on sentinel plants, we did not need to account for immigration in the model. The number of thrips per plant was then analyzed for each site using a mixed linear model (PROC MIXED, SAS Institute 2011).

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Prey stage preference and functional response

Based on field surveys Orius spp. and Chrysoperla spp. were identified as key natural

enemies of K. myopori. As both of these predators are available commercially (Orius insidiosus, Chrysoperla rufilabris), they were utilized to investigate host stage preference and functional response to K. myopori.

Purchased predators (Beneficial Insectary, Ca, USA), 1st or 2nd instar C. rufilabris or

adult O. insidiosus, were transferred individually into experimental arenas and starved for

24h. Experimental arenas consisted of Petri dishes with a perforated lid covered with a fine mesh (150 x 150 microns). Each arena containing an individual predator was placed in a growth chamber (25 °C, 40% RH, l6:8 L.D.) for 24 h.

In the prey stage preference test, an individual 24 h starved predator was transferred to a new arena and provided with 20 K. myopori eggs, 1st instar larvae, 2nd instar larvae,

propupa, pupa, and adults on leaf material for a total of 120 prey items. Predators were

allowed to feed on the prey items for 24 h after which the number of prey items per

predator consumed were counted. 20 replicate Petri dish arenas were established for each

of the two predator species (N=40).

In a second set of trials, to assess the functional response of the predators, individual 24 h

starved predators were exposed to densities of 2, 4, 8, 16, 32, 64, or 128 K. myopori eggs

or 1st instar larvae, 2nd instar larvae, propupa, pupa, and adults. After each 24 h, the

number of prey consumed was recorded. 20 replicate Petri dishes were established at each thrips density. (N=1680).

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Prey stage preference for each predator was first analyzed using ANOVA (SAS Institute

2011). Data was then analyzed using MANOVA to test whether the predators ate

different fractions of the various prey stages. Due to a significant difference between the

predator species, individual ANOVA’s were run for each prey stage.

Data analysis for functional response is a two-step process (Juliano 2001). In the first step, the type (shape) of functional response is determined. The most common method to determine the type of functional response is a logistic regression of proportion of prey eaten versus the initial number of prey offered:

exp ( + + + ) = 1 + exp ( + + 2 + 3 ) 푁푒 푃0 푃1푁0 푃2푁0 푃3푁0 2 3 푁0 푃0 푃1푁0 푃2푁0 푃3푁0 where Ne is the number of prey consumed, N0 is the initial prey density, (Ne/ N0) is the

probability of prey consumption, and P0, P1, P2 and P3 are the maximum likelihood

estimates of the intercept, linear, quadratic, and cubic coefficients (Juliano 2001). In Type

I responses the intercept and the linear coefficient are >0. In type II responses the linear coefficient is <0, and in type III responses the linear coefficient is >0 and the quadratic coefficient <0 (Juliano 2001). When the initial proportion of prey consumed increases with the number of prey offered, it is sufficient to identify the response as a type III. If the proportion of prey consumed declines with the number of prey offered, it is a type II response (Trexler et al. 1988, Juliano 2001). Once the functional response type is determined from the logistic regression analysis, the second step is to use nonlinear least square regression to fit the random predator equation to the data to estimate the handing

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times (Th) and attack rates (a), as the experiment was performed without prey

replacement (Rogers 1972, Juliano 2001).

For type II functional response the following model was used

Ne= N0[1-exp(a(ThNe-T))] (1)

For type III functional response the following model was used

Ne= N0{1-exp[bN0(ThNe-T)]} (2)

Where Ne is the number of prey consumed, N0 is the number of prey offered, Th is the

handling time, T is the searching time (24), and a is the attack rate (type II) or b is the

attack coefficient (type III). Nonlinear least square regression (Institute 2011) was used to

estimate the parameters of the Roger’s equation. After the parameters were estimated for

the original data (mt), the differences among values were tested for significance by estimating the variance using the jackknife technique (Meyer et al. 1986).

To calculate the jackknife pseudo-values for a the following equation was used

Mja= n * mta – (n-1)mia (3)

To calculate the jackknife pseudo-values for Th the following equation was used

MjTh= n * mTh– (n-1)miTh (4)

The mean values of jackknife pseudo-values for a and Th were then analyzed using

ANOVA (Institute 2011).

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Results

Monthly Regional Survey

Over the course of the study, a variety of natural enemies were collected on M. laetum

(Table 4.2). In total, five insect orders and five spider families were represented in the survey. The most abundant groups differed between collection sites. In Hemet, spiders,

Hemiptera, and Diptera were the most common. The most abundant predators in

Huntington Beach include Neuroptera, Diptera, and Hemiptera. In Oceanside,

Anthocoridae, Diptera, and spiders were the most abundant. Syrphid larvae, anthocorids,

Chrysoperla spp., Franklinothrips orizabensis, and one spider family (Salticidae) were all collected at each site over the duration of the survey. The coccinellid, Coccinella septempunctata, was only collected in Oceanside during the course of the survey. Several anthocorids were also only collected in Oceanside including two undescribed species of

Dasypertus (Dasypertus sp. "a" and Dasypertus sp. "b") as well as Orius insidiosus.

The mean number of thrips per tree by date and location is displayed in Figure 4.1. Thrips populations showed varying seasonal abundance, peaking in mid spring and maintaining low population numbers the rest of the year. For the sites Oceanside and Hemet in 2014-

2015, there was a significant interaction between both site (χ2=42.37, df=1, P<0.001) and date (χ2=19297.33, df=11, P<0.001), and the number of thrips per plant. For all three sites in 2015, there was a significant interaction between both site (χ2=5963.6, df=1,

P<0.001) and date (χ2=10946.5, df=4, P<0.001), and the number of thrips per plant. The mean number of natural enemies per gall is displayed in Figure 4.2. Natural enemy

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populations peaked in late spring, maintaining low population level the rest of the year.

For Oceanside and Hemet in 2014-2015, there was a significant interaction between both

site (χ2=111.17, df=1, P<0.001) and date (χ2=514.58, df=11, P<0.001), and the number of natural enemies per plant. For all three sites in 2015, there was only a significant interaction between date (χ2=62.23, df=4, P<0.001) and the number of natural enemies

per plant. There was no significant correlation between the number of thrips and natural

enemies per plant (t=0.01, df=144, P=0.86).

Cage Study

The mean number of insects per cage for the South Coast Research and Extension Center

is displayed in Figure 4.3. At the South Coast Research and Extension Center there was

no significant effect of cage treatment (F= 0.93, df=27.7, P = 0.34) or date (F= 2.52,

df=38.5, P = 0.09) on number of thrips per cage. However, when looking at the month of

November there was significantly more thrips in closed cages than open (F= 12.86,

df=14, P=0.0033) (Figure 4.4). The mean number of insects per cage for the San Jacinto

site is displayed in Figure 4.5. For the months of August and November at the San

Jacinto site no thrips survived for any treatments. For the month of October at the San

Jacinto site there was no significant difference in the number of thrips per cage treatment

(F= 0.28, df=14, P=0.61). There was no significant interaction between the number of thrips and the number of predators in open cages at the South Coast Research and

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Extension Center (F= 1.48, df=29, P = 0.23) or the San Jacinto site (F= 4.22, df=9, P =

0.07).

Prey stage preference and functional response study

Prey Stage Preference

The mean number of thrips consumed by O. insidiosus when presented with all prey life

stages is displayed in figure 4.7. There was a significant difference in O. insidiosus prey

consumption by life stage (F=103.49, df=5, P<.0001). O. insidiosus consumed more 1st instar larvae (6.10 ± .42) on average, followed by 2nd instar (4.20 ± .30), propupa (1.00 ±

.18), pupa (.45 ± .15), eggs (0.30 ± .18) and adults (0.20 ± .09). Figure 4.8 shows the

mean prey consumption of C. rufilabris feeding on different life stages of K. myopori.

There was a significant difference in C. rufilabris prey consumption by life stage

(F=282.94, df=5, P<.0001) The highest mean number of prey consumed was observed for

1st instar larvae (10.20 ± .29), followed by 2nd instar (4.90 ± .19), eggs (2.00 ± .36),

propupa (1.00 ± .15), pupa (0.60 ± .15) and adults (0.30 ± .11). When analyzing the effect

of predator species on prey consumption there was a significant effect (F=68.88, df=1,

P<.0001). C. rufilabris consumed significantly more eggs (F=18.24, df=1, P<.0001) and

1st instar (F=65.85, df=1, P<.0001) than O. insidiosus.

Functional Response

Logistic regression showed that for all prey stages the proportion of prey consumed by O. insidiosus decreased with the number of prey offered (Figure 4.10). For all prey stages

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the linear coefficients are negative (Table 4.3), suggesting a type II functional response

for all life stages. The attack rate (a) was highest for O. insidiosus feeding on 1st instar larvae (0.0881 ± .0131), followed by 2nd instar, pupa, propupa, eggs, and adults (Table

st 4.4). The handling time (Th) was shortest for eggs (1.3283 ± .2802 h), followed by 1

instar, 2nd instar, propupa, adults and pupa (Table 4.4).

Logistic regression showed that C. rufilabris differed in type of functional response

depending on the prey life stage (Figure 4.11). For eggs, 2nd instar, propupa, and pupa the

linear coefficients are negative (Table 4.5), suggesting type II functional response. For 1st

instar and adult stages the linear coefficient is positive and the quadratic coefficient is

negative (Table 4.5), suggesting type III functional response. However, the linear

coefficient is not significant for adults, constituting a weak type III functional response,

which is confirmed by the slight increase in initial proportion of prey consumed with the

number of prey offered (Figure 4.11). Based on the Rogers random-predator equation, the

highest attack rate (a) was observed for 2nd instar larvae (0.1238 ± .0145), while the

highest attack coefficient (b) was observed for 1st instar larvae (0.0205 ± .0044) (Table

st 4.6). The handling time (Th) per prey was shortest for 1 instar (0.7349 ± .0158 h),

followed by eggs, 2nd instar, propupa, pupa and adults (Table 4.6).

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Discussion

A wide variety of arthropods are known to be predators of thrips including Acari,

Anthocoridae, Araneida, Cecidomyiidae, Chrysopidae, Coccinellidae, Gryllidae,

Lygaeidae, Miridae, Nabidae, Pseudoscorpiones, Sphecidae, Staphylinidae, Syrphidae, and other Thysanoptera (Ananthakrishnan 1993, Riudavets 1995, Castañé et al. 1999).

For the predators collected during our surveys, all identified species have been known to feed upon thrips except for A. obliqua and the spider Theridion punctipes. The most abundant spider collected, Sassacus vitis, was observed by Costello et. al (1995) feeding on thrips in grape vineyards in California. In alfalfa, thrips are attacked in large numbers by C. septempunctata (Triltsch 1999). Funderburk et al. (2013) stated that species of

Anthocoridae are the most important worldwide predators of thrips. Khan and Morse

(1999) found augmentative releases of Chrysoperla spp. in citrus orchards suppressed citrus thrips levels and reduced fruit scarring. F. orizabensis is a key predator of avocado thrips in California avocado orchards (Hoddle et al. 2004). For the predators collected during our surveys only Orius tristicolor is a nonnative species, but is commonly released as a biological control agent.

Seasonal fluctuation in population density of K. myopori and associated natural enemies was observed from June 2014 to May 2015. K. myopori was found in high densities in

June 2014 and from February to April in 2015. Natural enemy populations showed similar seasonal fluctuations with high populations in June 2014 and from March to May in 2015. Environmental temperature extremes likely limited thrips populations during the winter and summer months. The lower developmental threshold of the insect is 10.3°C

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with an upper threshold of 38.7°C, similar temperatures were observed at the field

locations during the winter and summer months. Thereafter, environmental conditions

were only favorable for K. myopori during the spring months. The seasonality of K.

myopori can be exploited in augmentative biocontrol programs by releasing natural

enemies early in the year to provide control before thrips populations peak.

The cage-exclusion design has been employed extensively in evaluating natural enemies.

Butler and Trumble (2012) used exclusion cage experiments to assess the impact of

natural enemies on the potato psyllid Bactericera cockerelli in potato and American

nightshade crops. Experiments were conducted over a two week time span. Cage

treatments included closed, open and no cages. In their study significantly more psyllids

survived in closed cages than in open cages, leading to the conclusion that generalist

predators reduced psyllid population numbers. To analyze the effect of different guilds of

natural enemies of soy-bean aphids Costamagna et al. (2008) conducted cage exclusion

studies. The study used three different sized mesh screen to exclude, all natural enemies

(no-see-um netting), large predators (2mm openings), or no predators (20 cm openings).

The results of the study showed strong suppression of aphids by large generalist predators

and only slight suppression by small natural enemies.

The exclusion cage study was set up five meters from the common garden study (chapter

3) to insure an established population of thrips and natural enemies was in the immediate

vicinity. However, the data from the study failed to show consistent differences in thrips

numbers between cage treatments or a significant relationship between thrips and natural

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enemies. Populations of K. myopori peak in early spring (Figure 4.1) when host plants begin to flush. Our study was conducted during the fall months when thrips and natural enemy populations are stable but at low levels and host plants are not actively pushing new growth. During the month of August 2016, Southern California experienced a heat wave during which temperatures at the inland location exceeded 38°C (the lethal threshold of K. myopori). During the month of November 2016 the inland location experienced a frost in which the host plants used in the study experienced severe frost damage.

The natural enemies observed during the exclusion cage study were spiders (17) and lacewing larvae (2). The lack of a diverse guild of predators may be due in part to the duration of the study and/or intraguild predation. The study was conducted over periods of three weeks. The first week excluded predators from all treatments, giving predators two weeks to locate and influence thrips populations. While Butler and Trumble (2012) saw a significant decrease in pest populations within two days of initiating their study, two weeks may not have been a sufficient amount of time for our study. For our common garden study (Chapter 3) predators were not found in samples until the second month of sampling, when spiders were first observed. The following month the first lacewing and coccinillid larvae were observed. In a review by Hodge (1999) she investigated the role of spiders and implications of intraguild predation on biological control. While the review failed to form any generalized conclusions, it did discover that it is not uncommon for one-fifth of spider diets to consist of intraguild prey. The data obtained from our cage

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exclusion study is insufficient to identify whether or not natural enemies have an impact

on K. myopori survival in the field.

In a laboratory setting, the generalist predators Orius insidiosus and Chrysoperla

rufilabris showed good predation potential on K. myopori. In a prey-stage preference study both predators successfully preyed on all life stage of thrips, although they both preferred to prey on first instar thrips over other life stages when offered a choice.

Generalist predators including Chrysoperla carnea (Hoddle and Robinson 2004), Orius albidipennis (Gitonga et al. 2002), Orius insidiosus (Baez et al. 2004), Orius sp. (Kajita

1986), seem to have a preference for immature thrips over adult thrips.

In functional response studies O. insidiosus displayed an inverse density-dependent relationship between the proportion of prey consumed and the initial prey density for all prey life stages, consistent with type II functional response. C. rufilabris showed an initial increase in the proportion of prey with the number of prey offered for first instar and adult prey, consistent with a type III functional response, and displayed a type II functional response for the remaining prey life stages. O. insidiosus also displayed a type

II functional response when preying upon soybean thrips (Isenhour and Yeargan 1981).

Chrysoperla spp. often display a different type of functional response based on their life

stage (Nordlund and Morrison 1990, Kabissa et al. 1996, Hassanpour et al. 2011). Only

predators displaying a type III functional response regulate prey populations (Holling

1965) due to the long term persistence of the predator. Long term persistence of predator populations is an important part of classical and inoculative biological control programs,

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but is not as important in augmentative programs were predators are continuously released.

The parameters attack rate and handling time are used to determine the magnitude of functional responses, ex. a shorter handling time results in a steeper slope for the functional response curve (Nordlund and Morrison 1990, Ganjisaffar and Perring 2015).

In our study the handling time for O. insidiosus on eggs was shorter than other life stages.

Eggs are immobile and lack defensive mechanisms allowing predators to readily consume them. The handling time was shortest for C. rufilabris on 1st instar thrips.

During the study it was often observed that when O. insidiosus feed upon thrips eggs, the egg became stuck on the predators’ mandible, with the predator struggling to remove it increasing the handling time. The attack rate was highest for O. insidiosus feeding on 1st instar larvae (0.0881 ± .0131). However, the attack rate is much lower than other species of Orius feeding on western flower thrips. In a study by Montserrat et al. (2000) Orius majuscules had an attack rate of .688 (.059-1.318) and Orius laevigatus had an attack rate of .332 (.192-.4271) when feeding on thrips larvae. For C. rufilabris the highest attack rate was observed for 2nd instar larvae (0.1238 ± .0145), while the highest attack coefficient was observed for 1st instar larvae (0.0205 ± .0044).

The present studies set out to identify potential predators for biological control, evaluate those predators, and to potentially develop recommendations for biological control. Field sampling identified anthocorids and lacewings as good candidates for biological control.

While field studies failed to demonstrate thrips reduction due to predation, laboratory

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studies showed potential for augmentative biological control. Generally speaking, O. insidiosus and C. rufilabris consumed a higher proportion of prey at lower pest densities.

In an augmentative control program predators could be released early in the year when host plants begin to flush and thrips populations are low to provide control. Further field studies are needed to evaluate augmentative releases for control of K. myopori.

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Table 4.1 Mean annual weather variables for three collection sites from Arguez et al. (2012) Oceanside Huntington Beach Hemet Mean High Temp (°C) 18.9 22.7 27.7 Mean Low Temp (°C) 12.2 13.2 8.7 Mean Precipitation (cm) 26.1 35.4 29.7

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Table 4.2 Potential predators of K. myopori collected on Myoporum laetum from surveys between June 2014 through May 2015

Order/Family Species Hemet Huntington Beach Oceanside

Araneae

Araneidae Unidentified spp. 1

Lycosidae Unidentified spp. 2 122

Salticidae Sassacus vitis 10 11

Unidentified spp. 1 17

Theridiidae Theridion punctipes 14

Thomisidae Unidentified spp. 5 1

Unidentified 3 20

Total 19 1 65

Coleoptera

Coccinellidae Coccinella septempunctata 3

Unidentified spp. 4

Total 0 0 7

Diptera

Syrphidae Allograpta obliqua 6

Unidentified spp. 10 10 81

Total 10 10 87 123

Hemiptera

Anthocoridae Dasypertus sp. "a" 7

Dasypertus sp. "b" 1

Dasypertus spp. nymphs 5

Orius insidiosus 21

Orius tristicolor 9 4

Orius sp. "u" 20 2

Orius nymphs 2

Unidentified spp. 36 7 125

Miridae Rhinacloa forticornis 2

Total 67 7 167

Neuropetra

Chrysopidae Chrysoperla spp. 5 19 17

Total 5 19 17 124

Thysanoptera

Aeolothripidae Franklinothrips orizabensis 9 1 5

Total 9 1 5

Table 4.3 Functional response of Orius insidiosus based on logistic regression estimate using Ne/No

Prey Stage Parameters Estimates SE Chi- Sqaure P value Egg Intercept (P0) 0.2594 0.3158 0.67 0.4113 Linear (P1) -0.1428 0.0502 8.1 0.0044 Quadratic (P2) 0.00416 0.00193 4.64 0.0312 Cubic (P3) -4.00E-05 1.90E-05 3.79 0.0516 1st Instar Intercept (P0) 1.4546 0.3389 18.42 <.0001 Linear (P1) -0.1264 0.05 6.41 0.0114 Quadratic (P2) 0.00208 0.00187 1.24 0.2654 Cubic (P3) -1.00E-05 1.80E-05 0.57 0.4491 2nd Instar Intercept (P0) 1.7071 0.3422 24.88 <.0001 Linear (P1) -0.2062 0.0509 16.42 <.0001 Quadratic (P2) 0.00513 0.00191 7.23 0.0072 Cubic (P3) -4.00E-05 1.90E-05 5.38 0.0203 Propupa Intercept (P0) 0.7819 0.3161 6.12 0.0134 Linear (P1) -0.2044 0.0506 16.28 <.0001 Quadratic (P2) 0.00602 0.00195 9.49 0.0021 Cubic (P3) -6.00E-05 1.90E-05 8.01 0.0047 Pupa Intercept (P0) 1.0921 0.3232 11.42 0.0007 Linear (P1) -0.239 0.0521 21.05 <.0001 Quadratic (P2) 0.00658 0.00202 10.59 0.0011 Cubic (P3) -6.00E-05 0.00002 8.01 0.0047 Adult Intercept (P0) -0.3621 0.3315 1.19 0.2748 Linear (P1) -0.107 0.0545 3.86 0.0494 Quadratic (P2) 0.00232 0.00213 1.18 0.2778 Cubic (P3) -2.00E-05 2.10E-05 0.67 0.4148

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Table 4.4 Estimated type II functional response parameters ± SE (95% confidence interval) for O. insidiosus feeding on different life stages of K. myopori.

Prey Stage Attack rate (a) Handing time (Th) Egg 0.0173 ± .0034 e 1.3283 ± .2802 a (.0106-.0240) (.7717-1.8851) 1st Instar 0.0881 ± .0131 a 2.2836 ± .0909 b (.0620-.1141) (2.1024-2.4642) 2nd Instar 0.0710 ± .0094 b 2.5688 ± .0994 c (.0523-.0896) (2.3712-2.7663) Propupa 0.0281 ± .0042 d 2.7653 ± .1994 d (.0198-.0364) (2.3692-3.1615) Pupa 0.0341 ± .0065 c 3.7224 ± .2680 f (.0211-.0470) (3.1898-4.2549) Adult 0.0136 ± .0024 f 3.1332 ± .3776 e (.00894-.0184) (2.3826-3.8835) Means within the same column followed by the same letter are not significantly different (P < 0.01).

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Table 4.5 Functional response of Chrysoperla rufilabris based on logistic regression estimate using Ne/No

Prey Stage Parameters Estimates SE Chi- Sqaure P value Egg Intercept (P0) 1.8838 0.3472 29.44 <.0001 Linear (P1) -0.2436 0.0512 22.63 <.0001 Quadratic (P2) 0.00733 0.00191 14.76 0.0001 Cubic (P3) -7.00E-05 1.90E-05 12.88 0.0003 1st Instar Intercept (P0) 2.4183 0.8275 8.54 0.0035 Linear (P1) 0.2918 0.1414 4.26 0.039 Quadratic (P2) -0.0142 0.00544 6.81 0.0091 Cubic (P3) 0.00014 5.30E-05 6.99 0.0082 2nd Instar Intercept (P0) 4.0538 0.6433 39.71 <.0001 Linear (P1) -0.277 0.0814 11.58 0.0007 Quadratic (P2) 0.00527 0.00281 3.52 0.0606 Cubic (P3) -3.00E-05 2.60E-05 1.67 0.1967 Propupa Intercept (P0) 4.2587 0.5767 54.53 <.0001 Linear (P1) -0.4052 0.0741 29.93 <.0001 Quadratic (P2) 0.0107 0.00258 17.4 <.0001 Cubic (P3) -9.00E-05 2.40E-05 13.47 0.0002 Pupa Intercept (P0) 4.7224 0.6295 56.28 <.0001 Linear (P1) -0.4583 0.0795 33.26 <.0001 Quadratic (P2) 0.0125 0.00274 20.77 <.0001 Cubic (P3) -0.0001 2.60E-05 16.71 <.0001 Adult Intercept (P0) -0.1994 0.3047 0.43 0.5128 Linear (P1) 0.0518 0.0467 1.23 0.2678 Quadratic (P2) -0.0041 0.00179 5.26 0.0218 Cubic (P3) 4.40E-05 1.80E-05 6.22 0.0126

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Table 4.6 Estimated functional response parameters ± SE (95% confidence interval) for C. rufilabris feeding on different life stages of K. myopori.

Prey Stage Attack Rate (a) Attack Coefficient (b) Handing Time Egg 0.0419 ± .0045 1.2876 ± .0797 b (0.0330-0.0507) (1.1291-1.4460) 1st Instar 0.0205 ± .0044 0.7349 ± .0158 a (0.0117-0.0294) (0.7035-0.7664) 2nd instar 0.1238 ± .0145 1.4347 ± .0430 c (0.0949-0.1526) (1.3492-1.5203) Propupa 0.0801 ± .0084 1.4801 ± .0534 d (0.0635-0.0967) (1.374-1.5861) Pupa 0.0848 ± .0088 1.5131 ± .0514 e (0.0673-0.1022) (1.4109-1.6154) Adult 0.0085 ± .0017 3.1863 ± .1242 f (0.00516-0.0118) (2.9396-3.4331) Means within the same column followed by the same letter are not significantly different (P < 0.01).

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1400 Thrips 1200

1000

800

600 Hemet

400 Oceanside

200 Huntington Beach

Mean Number of Thrips Tree per of Thrips Number Mean 0

15 15 14 14 14 14 15 14 14 15 15 14 ------Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

Figure 4.1 The mean number of thrips per tree over time for each collection site.

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40 35 Natural Enemies 30 25

20 Hemet

Tree 15 Oceanside 10 Huntington Beach 5 0

15 15 14 14 14 14 15 14 14 15 15 14 ------Mean Number of Natural Enemies per per Enemies Natural of Number Mean Jul Jan Jun Oct Apr Sep Feb Dec Aug Nov Mar May Date

Figure 4.2 The mean number of natural enemies per tree over time for each collection site.

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3 Thrips Predators 2 Mean Number Number of Mean Insects 1

0 Aug 2016 Oct 2016 Nov 2016

Figure 4.3 Mean number (± SE) of insects per open cage at the South Coast Research and Extension Center.

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10 a per Cage per 8

Closed

K. myopori 6 Open a 4 a a a b 2 Mean Number Number of Mean 0 Aug 2016 Oct 2016 Nov 2016

Figure 4.4 Mean number (± SE) of thrips per cage type at the South Coast Research and Extension Center. Bars with different letters are significantly different (P > 0.05) within date.

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1 0.9 0.8 0.7 0.6 0.5 Thrips 0.4 Predators 0.3

Mean Number Number of Mean Insects 0.2 0.1 0 Aug 2016 Oct 2016 Nov 2016 Date

Figure 4.5 Mean number (± SE) of insects per open cage at the San Jacinto site.

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a 0.9 0.8 per cage 0.7 a 0.6 Closed

K. myopori 0.5 0.4 Open 0.3 0.2

Mean number number of Mean 0.1 0 Aug 2016 Oct 2016 Nov 2016

Figure 4.6 Mean number (± SE) of thrips per cage type at the San Jacinto site. Bars with different letters are significantly different (P > 0.05).

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7 a O. insidiosus 6

5 b 4

2 Mean Prey Prey Mean Consumption cd 1 cd cd d 0 Eggs 1st Instar 2nd Instar Propupa Pupa Adult

Figure 4.7 Mean prey consumption for Orius insidiosus feeding on different life stages of Klambothrips myopori in host preference study (P<.01).

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12 a C. rufilabris 10

6 b

Mean Prey Prey Mean Consumption c 2 c cd d 0 Eggs 1st Instar 2nd Instar Propupa Pupa Adult

Figure 4.8 Mean prey consumption for Chrysoperla rufilabris feeding on different life stages of Klambothrips myopori in host preference study (P<.01).

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Figure 4.9 Functional responses of O. insidiosus to different stages of K. myopori under laboratory conditions.

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Figure 4.10 Proportion of K. myopori consumed by O. insidiosus, and logistic regression fit to the data.

138

Figure 4.11 Functional responses of C. rufilabris to different stages of K. myopori under laboratory conditions.

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Figure 4.12 Proportion of K. myopori consumed by C. rufilabris, and logistic regression fit to the data.

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Chapter 5

Conclusion

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Myoporum thrips (Thysanoptera: Phlaeothripidae), Klambothrips myopori, poses a significant threat to ornamental and native Myoporum in its invasive range. In its invasive range of California and Hawaii, K. myopori has spread rapidly wherever host Myoporum is planted, causing unsightly damage characterized by gall-like symptoms and severe distortion of new leaves (Mound and Morris 2007). Thrips populations can build up in large numbers within the folded leaves of the galls, causing terminal growth to be stunted, and in severe cases, causes branch or whole plant death (Sullivan 2014). As relatively little is known about this thrips the goal of these studies was to gather information on its life history, host preference, and possible biological control agents in order to assist in the development of best management strategies.

Temperature-driven development of K. myopori was examined at seven constant temperatures (15°, 17°, 20°, 25°, 30°, 34°, and 35.5° C) on Myoporum laetum. Thrips successfully completed development to adult stage between 15 and 35.5°C. One linear and three nonlinear models were fitted to describe developmental rates of K. myopori as a function of temperature, and for estimating thermal constants and bioclimatic thresholds

(Tmin, Topt and Tmax). The Briere-1 model performed best in describing the developmental rate of cumulative life stages, providing values of Tmin (11.9°C), Topt

(32.5°C), and Tmax (38.8°C). According to the linear regression, K. myopori requires

378.79 degree-days above the lower threshold to complete development from egg to adult. Understanding the development of myoporum thrips will be helpful in monitoring and predicting thrips activity in order to implement management strategies at the proper

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timing. The life history data gained was also used in the creation of ecological niche models to estimate the potential invasion range of K. myopori.

Two ecological niche models, CLIMEX and Maxent (Sutherst and Maywald 1985,

Phillips et al. 2006), were used to predict the geographic distribution of K. myopori in its native range and globally. These programs use life history, temperature, and location data of the model speicies to generate maps that show environmental suitability for the model species. Overall predictions of environmental suitability differed greatly across the two models. The CLIMEX model accurately predicted known invasive and native localities, while the Maxent model failed to predict the native localities and parts of the invasive range. Based on the CLIMEX model, K. myopori has the potential to establish in many regions of the globe, including all Mediterranean climates where Myoporum is grown as an ornamental and from Asia into the Pacific islands where Myoporum is native. The predicted environmental suitability of K. myopori is much greater than its current invaded area, and it is important to understand possible management strategies to minimize its spread and impact.

Laboratory and field studies were used to identify the potential host range of K. myopori.

Both studies identified Myoporum laetum and M. ‘Pacificum’ as key host plants of myoporum thrips. In laboratory trials, K. myopori developed quickest on M. laetum, and had the greatest survival from egg to adult on M. laetum and M. ‘Pacificum’. K. myopori

failed to complete development on M. ‘Clean n Green’ and M. ‘Putah Creek’. In field

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trials host variety had a significant effect on number of thrips per plant, with M. laetum followed by M. ‘Pacificum’ having the highest average number of thrips per plant. For the six varieties of Myoporum tested, K. myopori damage was only observed on M. laetum and M. ‘Pacificum’. Although K. myopori can successfully colonize and reproduce on several varieties of Myoporum, they demonstrated a strong preference for

M. laetum and M. ‘Pacificum’.

To identify the predator complex of K. myopori field surveys were taken at three sites in southern California over the period of one year. Over the course of the study, a variety of natural enemies were collected on M. laetum. In total, five insect orders and five spider families were represented in the survey. The most abundant groups differed between collection sites. In Hemet, spiders, Hemiptera, and Diptera were the most common. The most abundant predators in Huntington Beach included Neuroptera, Diptera, and

Hemiptera. In Oceanside, Anthocoridae, Diptera, and spiders were the most abundant.

Syrphid larvae, anthocorids, Chrysoperla spp., Franklinothrips orizabensis, and one spider family (Salticidae) were all collected at each site over the duration of the survey.

Based on the field surveys, we identified Orius spp. and Chrysoperla spp. as possible key natural enemies of K. myopori. Laboratory studies were then conducted to determine the consumption rates of Orius insidiosus and Chrysoperla rufilabris at constant densities of

K. myopori and to define the functional responses of the predators. Both predators consumed more 2nd instar larvae than other prey stages. O. insidious displayed a type II functional response, while C. rufilabris displayed both type II and type III depending on

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prey stage. Generally speaking, O. insidiosus and C. rufilabris consumed a higher

proportion of prey at lower pest densities, implying in an augmentative control program

predators could be released early in the year when host plants begin to flush and thrips

populations are low in order to suppress thrips populations.

In conclusion, myoporum thrips can develop in a wide range of temperatures that allows

for the potential to establishment in many regions of the globe, including all

Mediterranean climates where Myoporum is grown as an ornamental and from Asia into the Pacific islands where Myoporum is native. Although K. myopori can successfully colonize and reproduce on several varieties of Myoporum, they demonstrated a preference for M. laetum and M. ‘Pacificum’ in laboratory and field trials. The demonstrated host preference is also associated with enhanced thrips fitness on those hosts compared to the less preferred cultivars. The nutritional content and secondary metabolites of the tested Myoporum varieties may have affected host preference, leading to decreased colonization and overall feeding damage in certain cultivars and warrants further study. Using the aesthetic injury level of 10%, M. laetum ‘Clean ‘n Green’, M. parvifolium, M. parvifolium ‘Pink’, and M. parvifolium ‘Putah Creek’ are recommended for use in the landscape. While field studies failed to demonstrate thrips reduction due to predation, laboratory studies showed potential for augmentative biological control.

Generally speaking, O. insidiosus and C. rufilabris consumed a higher proportion of prey at lower pest densities. In an augmentative control program predators could be released early in the year when host plants begin to flush and thrips populations are low to provide

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control. Further field studies are needed to evaluate augmentative releases for control of

K. myopori.

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References Cited

Mound, L. A., and D. C. Morris. 2007. A new thrips pest of Myoporum cultivars in California, in a new genus of leaf-galling Australian Phlaeothripidae (Thysanoptera). Zootaxa 1495: 35-45.

Phillips, S. J., R. P. Anderson, and R. E. Schapire. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259.

Sullivan, J. 2014. Inadvertent biological control: an Australian thrips killing an invasive New Zealand tree in California. Biological Invasions 16: 445-453.

Sutherst, R. W., and G. F. Maywald. 1985. A computerised system for matching climates in ecology. Agriculture, Ecosystems & Environment 13: 281-299.

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