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Assessing the effect of plant surface on the predatory ability 

of Orius vicinus: A potential biological control agent of the 

tomato-potato psyllid (Bactericera cockerelli) 

 

 

A thesis presented in partial fulfilment of the  

requirements for the degree of 

 

 

 

 

Master of Science  

in 

Zoology 

 

 

at Massey University, Palmerston North,  

New Zealand 

 

 

 

 

Abel Gamarra Landa 

2019 

  



ii 

 

  



iii 

 

Abstract 

 

The tomato-potato psyllid (TPP), Bactericera cockerelli (Sulc), is a pest to solanaceous 

crops (e.g. potato, tomato, peppers, and eggplant) and is associated with economically 

important plant diseases. Subsequently, chemical control is the preferred management 

option. However, chemical reliance is associated with a host of issues. The development 

of biological control methods is vital to implementing Integrated Pest Management 

(IPM) programs as an alternative to broad-spectrum insecticide usage. The predatory 

bug Orius vicinus (Ribaut) is a potential biological control agent that is capable of 

consuming all nymphal life stages of TPP. 

 

In order to be a commercially viable management option, potential biological control 

agents of TPP have to cope with the different morphological plant features of the pest’s 

wide range of host plants. Tomato and capsicum plant surfaces were selected as the 

experimental surfaces for my thesis because they differ significantly in their substrate 

morphology. Tomato plant surfaces can be a hostile environment for potential 

biological control agents due to the negative effect tomato trichomes have on their 

foraging performance. Alternatively, because capsicum plant surfaces are virtually void 

of trichomes they appear to be more suitable for effective biological control agent 

deployment. 

 

I exposed the predatory bug to a variety of TPP nymph densities (10, 20, 30 and 40 

individuals) in order to determine the functional response of O. vicinus. Furthermore, 

the predatory bug was exposed to all five TPP nymphal stages simultaneously. The 

predatory performance of O. vicinus was also assessed on experimental arenas varying 

in complexity (leaflet vs. small plant environments). The functional response was 

determined to be Type II on both plant surfaces. Nymph consumption at higher prey 

densities (30 and 40 nymphs) was significantly greater on capsicum than on tomato. 

Nymph consumption at lower prey densities (10 and 20 nymphs) was only significantly 

greater on capsicum when the complexity of the experimental arena increased from 

leaflet to small plant. The influence of O. vicinus in nymph dispersal was also assessed. 

My results revealed that the presence of O. vicinus increased the dispersal of nymphs to 

lower leaf surfaces and that nymph dispersal was significantly greater on capsicum than 

on tomato. 



iv 

 

 

TPP nymph size preference by O. vicinus was determined in my study. I established that 

the predatory bug is capable of killing all nymphal stages. My study strongly indicated 

that the predatory bug is more likely to target and consume medium (3
rd

 instars) and 

large nymphs (4
th

 and 5
th

 instars) over small nymphs (1
st
 and 2

nd
 instars). I investigated 

the behaviour of O. vicinus adults and TPP nymphs during their interactions via video 

recordings. The predatory bug spent a significantly greater amount of time investigating 

TPP nymphs on capsicum than on tomato. There was significantly higher number of 

attacks recorded on capsicum. The greater killing percentage on tomato suggests that 

the defensive capabilities of TPP nymphs appear to have been negatively affected by the 

tomato substrate. 

 

The results from my study indicate that augmentative releases of O. vicinus, in the 

presence of smaller TPP nymphs, could be a viable biological control option on 

capsicum plants. However, the predatory bug will likely struggle if deployed on tomato 

plants. Future studies should be conducted in settings such as open field or glasshouses 

using multiple predatory bugs in the presence of susceptible life stages to assess 

augmentative release efficiency. 

 

Keywords: Biological control, tomato-potato psyllid (TPP), Bactericera cockerelli, 

Orius vicinus, functional response, prey preference, plant surface morphology, 

capsicum, tomato. 

  



v 

 

Acknowledgements 

 

This thesis would not have been possible without the input and support from many 

people. Firstly, I must thank my supervisors Professor Murray Potter and Professor 

Qiao Wang. They have shown much patience and understanding over the years as I 

juggled full time work and thesis requirements. Their input, guidance and 

encouragement have been valuable and appreciated. I must also thoroughly thank Dr 

Xiong Zhao He, who provided vital statistical analysis expertise and was always on 

hand to assist me in any way he could. 

 

I would also like to thank the following people who provided vital assistance in some 

capacity during my thesis. They virtually kept my thesis alive at times. Mike Sim from 

Bioforce for providing Orius vicinus individuals for my colony. Robin Gardner-Gee 

from Plant and Food Research for providing TPP individuals for my colony. Steve Ray 

and the staff at the Massey University Plant Growth Unit, for providing vital assistance 

and maintenance of my experimental plants. Paul Barrett for assisting with any 

technical issues with the temperature control rooms and providing equipment when 

needed.  

 

I would also like to thank Diwas Khatri for kindly lending me his video camera for my 

experiment. Jen Buxton for helping transport plants from the PGU to my lab and 

Geneva Whitlow–Waa for maintaining my plants alive while I was away from campus. 

My mother Cynthia Landa and her partner Neil Hawes for providing much appreciated 

dinners during the experimental phase of my thesis. Finally, the long journey of this 

thesis would not have been possible without the love and understanding of my lovely 

partner Laura Volp. 

  



vi 

 

  



vii 

 

Table of Contents 

 

Abstract iii 

Acknowledgements  v 

Table of Contents  vii 

List of Figures  ix 

List of Tables xi 

 

Chapter 1: Introduction  1 

1.1 Overview 1 

1.2 Tomato-potato psyllid (TPP) 3 

 1.2.1 Distribution 3 

 1.2.2 Life history 5 

  1.2.2.1 Life stages 5 

 1.2.3 Diseases associated with TPP 7 

  1.2.3.1 Psyllid yellows 7 

  1.2.3.2 Candidatus Liberibacter 8 

 1.2.4 TPP management strategies 10 

  1.2.4.1 Monitoring TPP 10 

  1.2.4.2 Insecticides 10 

   1.2.4.2.1 Biorational insecticides 13 

  1.2.4.3 Biological control 13 

   1.2.4.3.1 Entomopathogenic fungi 14 

   1.2.4.3.2 Parasitoids 14 

   1.2.4.3.3 Predators 16 

1.3 Genus: Orius 19 

 1.3.1 Orius vicinus 20 

1.4 The effect of morphological plant traits on biological control agents 22 

 1.4.1 Assesment of experimental plant surfaces 25 

  1.4.1.1 Tomato plant surfaces 25 

  1.4.1.1 Capsicum plant surfaces 27 

1.5 Aims and objectives 28 

 

Chapter 2: The effect of host plant substrate on the biological control potential  

of Orius vicinus (Ribaut) on Bactericera cockerelli (Sulc) nymphs  31 

2.1Abstract  31 

2.2 Introduction  31 

2.3 Material and Methods  34 

 2.3.1 Experimental plants  34 

 2.3.2 Insect colonies 35 

 2.3.3 Experimental design  35 

  2.3.3.1 Leaflet experimental arena  35 

  2.3.3.2 Plant experimental arena  37 

 2.3.4 Data analysis  38 

  2.3.4.1 Leaflet experimental arena  38 

  2.3.4.2 Plant experimental arena  41 

2.4 Results  42 

 2.4.1 Leaflet experimental arena 42 

 2.4.2 Plant experimental arena 49 



viii 

 

2.5 Discussion 51 

 

Chapter 3: The effect of host plant substrate on the behaviour of Orius vicinus 

(Ribaut) and Bactericera cockerelli (Sulc) nymphs  55 

3.1 Abstract  55 

3.2 Introduction  55 

3.3 Material and Methods  57 

 3.3.1 Experimental plants  57 

 3.3.2 Insect colonies 58 

 3.3.3 Experimental design  58 

 3.3.4 Data analysis  61 

3.4 Results  62 

3.5 Discussion  66 

 

Chapter 4: Conclusion  71 

4.1 Objectives and outcomes  71 

 4.1.1 Objective 1  71 

 4.1.2 Objective 2  72 

 4.1.3 Objective 3  72 

 4.1.4 Objective 4  72 

4.2 Future research  73 

4.3 Final summary  74 

 

References  75  



ix 

 

List of Figures 

 

Figure 1.1: TPP life stages: egg attached to capsicum leaflet (left); fifth instar TPP 

nymph on tomato leaflet (middle); and adult TPP on tomato leaflet (right).................6  

 

Figure 1.2: Adult O. vicinus probing a TPP nymph on capsicum surface (left) and O. 

vicinus nymph on tomato surface (right).......................................................................21 

 

Figure 2.1: Adult O. vicinus on smooth surfaced capsicum (left) and hairy surfaced 

tomato (right) leaves......................................................................................................35 

 

Figure 2.2: Petri dish containing the raised tomato leaflet uncovered (left) and covered 

with jar with ventilation holes (right)............................................................................36 

 

Figure 2.3: Uncovered (left) and covered (right) small capsicum plant with all but one 

leaflet removed..............................................................................................................38 

 

Figure 2.4: Estimated percentage of TPP nymphs located on the upper surface of 

capsicum (C) and tomato (T) leaflets after 24 h in the presence (+) and absence (-) of O. 

vicinus at different prey densities..................................................................................43 

 

Figure 2.5: Percentage of TPP nymphs consumed by O. vicinus on the upper surface of 

capsicum and tomato leaflets after 24 h. For each density or mean, columns with 

different letters are significantly different (Kruskal-Wallis Test: P < 0.05)................. 44 

 

Figure 2.6: Percentage of TPP nymphs consumed by O. vicinus on capsicum and 

tomato leaflets after 24 h. For each density or mean, columns with different letters are 

significantly different (ANOVA: P < 0.05)...................................................................44 

 

Figure 2.7: Type II functional response of O. vicinus on capsicum and tomato leaflet 

surfaces: (A) number of TPP nymphs consumed, and (B) percentage of TPP nymphs 

consumed.......................................................................................................................46  

 

Figure 2.8: TPP density (TPPD: 10, 20, 30 and 40 nymphs) and size index (TPPSI: 

small (1), medium (2), and large (3) nymphs) affecting the rate of TPP consumed 

(ROTPPC) by O. vicinus: (A) Capsicum, ROTTPC = 0.0148 – 0.0014TPPD + 

0.3814TPPSI – 0.0992TPPSI
2
 (R

2
 = 0.1185, F3,236= 10.57, P < 0.0001); (B) Tomato, 

ROTTPC = 0.0459 – 0.0039TTPD + 0.3209TPPSI – 0.0733TPPSI
2
 (R

2
 = 0.1562, F3,236 

= 14.57, P < 0.0001)..................................................................................................... 48  

 

Figure 2.9: Percentage of TPP nymphs located on the upper leaf surface of capsicum 

and tomato plants after 24 h. Columns with different letters are significantly different 

(Kruskal-Wallis Test: P < 0.05).................................................................................... 49 

 

Figure 2.10: Percentage of TPP nymphs consumed by O. vicinus on the upper leaflet 

surface of capsicum and tomato plants after 24 h. Columns with different letters are 

significantly different (Kruskal-Wallis Test: P < 0.05)................................................ 50 

 

 



x 

 

Figure 2.11: Percentage of TPP nymphs consumed by O. vicinus on capsicum and 

tomato experimental arenas after 24 h at the prey density of 10 individuals. Columns 

with different upper case letters indicate significant differences between experimental 

arenas within host plants and columns with different lower case letters indicate 

significant differences between host plants  (ANOVA: P < 0.05).................................50 

 

Figure 2.12: Hairless capsicum stem surface (left) and hairy tomato stem surface 

(right).............................................................................................................................53 

 

Figure 3.1: Adult TPP on smooth surfaced capsicum (left) and hairy surfaced tomato 

(right) leaves..................................................................................................................58 

 

Figure 3.2: Capsicum leaflet sitting on blutack balls surrounded by water within Petri 

dish (right). Aerial view of Petri dish within plastic cylinder containing capsicum leaflet 

(left)...............................................................................................................................59 

 

Figure 3.3: TPP nymphs on tomato surface: (1) first instar, (2) second instar, (3) third 

instar, (4) fourth instar, and (5) fifth instar....................................................................60 

 

Figure 3.4: The mean number of seconds spent by O. vicinus performing the observed 

behaviours on tomato and capsicum surfaces during the 1 h observation period (Wal = 

Walking; Sea = Searching; Sta = Stationary; Gro = Grooming; Ori = Orienteering; Inv = 

Investigating; Att = Attacking; Con = Consuming; Oth = Other). For each behaviour, 

columns with a different letter are significantly different (ANOVA: P < 0.05).......... 62 

 

Figure 3.5: Adult O. vicinus probing large sized TPP nymph (left) and adult O. vicinus 

consuming medium sized TPP nymph (right)...............................................................69 
 

  



xi 

 

List of Tables 

 

Table 2.1: Logistic regression analysis of functional response of O. vicinus to TPP 

densities.........................................................................................................................45 

 

Table 2.2: Searching efficiency (a, h
-1

) and handling time (Th, h) parameters (P) for 

Type II functional response of O. vicinus to TPP nymph density on Capsicum (C) and 

Tomato (T) plants..........................................................................................................47  

 

Table 3.1: Behavioural parameters for adult O. vicinus...............................................60 

 

Table 3.2: Behavioural parameters for TPP nymphs....................................................61 

 

Table 3.3: The mean (±SE) number of predator-prey encounters and number of 

predator attacks observed on capsicum and tomato surfaces........................................63 

 

Table 3.4: The mean (±SE) percentage of attacks resulting in kills observed on 

capsicum and tomato surfaces...................................................................................... 63 

 

Table 3.5: The probability (±SE) of O. vicinus initiating an encounter with TPP nymphs 

based on their size on capsicum, tomato, and combined (capsicum and tomato) 

surfaces..........................................................................................................................64 

 

Table 3.6: The probability (±SE) of O. vicinus initiating an attack during an encounter 

with TPP nymph based on their size on capsicum, tomato, and combined (capsicum and 

tomato) surfaces.............................................................................................................64 

 

Table 3.7: The probability (±SE) of O. vicinus killing a TPP nymph during an attack 

based on their size on capsicum, tomato, and combined (capsicum and tomato) 

surfaces..........................................................................................................................65 

 

Table 3.8: The probability (±SE) of TPP nymph performing defensive behaviours 

during an encounter with O. vicinus based on their size on capsicum, tomato, and 

combined (capsicum and tomato) surfaces....................................................................66 

 

Table 3.9: The probability (±SE) of TPP nymph performing defensive escape 

behaviours during an encounter with O. vicinus based on their size on capsicum 

surfaces..........................................................................................................................66 

 

 

 

  



xii 

 

  



1 

 

Chapter 1: Introduction  

 

1.1 Overview 

 

Integrated Pest Management (IPM) combines biological, cultural and chemical tactics to 

reduce pest populations to economically tolerable levels whenever they reach an 

economic threshold (Tang & Cheke, 2008). IPM programs incorporate economic injury 

levels, economic thresholds, field monitoring and record keeping, to make pest 

management decisions (Tang & Cheke, 2008). Studies have revealed that IPM programs 

are more effective than relying solely on chemical control, which is associated with a 

host of issues such as environmental damage, development of insecticide resistance and 

secondary pest problems (Symondson et al., 2002; Tang & Cheke, 2008; Van Lenteren, 

2012b).  Biological control is a key aspect of the IPM paradigm, and can be defined as 

the exploitation of the ability of an organism to reduce the population density of another 

organism (Symondson et al., 2002; Van Lenteren, 2012b).  

 

Biological control can be broken down into the following types: natural, conservation, 

classical, and augmentative (Van Lenteren, 2012b). Natural biological control can be 

defined as the reduction of pest organisms by their natural enemies without human 

intervention (Van Lenteren, 2012b). Conservation biological control occurs when 

human intervention protects and stimulates the performance of naturally occurring 

biological control agents (Van Lenteren, 2012b). Classical biological control involves 

introduction of agents from an exploration area (usually the area of origin of the 

targeted pest) and their release in the areas where the targeted pest has become a 

problem (Van Lenteren, 2012b). Augmentative biological control is the mass-rearing 

and mass release of biological control agents with the purpose of immediately 

controlling a pest population (Van Lenteren, 2012b). Augmentative control can be an 

environmentally and economically sound alternative to chemical pest control in certain 

areas of agriculture such as greenhouses (particularly those that use bees for pollination) 

(Van Lenteren, 2012b). Biological control agents used in augmentative control 

programs can be either indigenous or exotic. However, there are costs associated with 

the importation and release of exotics due to the required environmental assessment of 

their impact and subsequent registration (Van Lenteren, 2012b). Therefore finding ways 



2 

 

to augment the efficacy of indigenous or established exotic natural enemies is usually 

the primary option when a new pest is found (Van Lenteren, 2012b). 

 

Arthropods used as biological control agents generally come from four taxonomic 

groups: Hymenoptera, Acari, Coleoptera and Heteroptera (Van Lenteren, 2012b). A 

review of multiple biological control studies by Stiling and Cornelissen (2005) found 

that the majority of biological control agents were generalists whose efficacy tended to 

be higher than specialists. However, the capability of generalists to affect non-target 

organisms has to be taken into consideration when assessing their potential as biological 

control agents (Stiling & Cornelissen, 2005). The majority of studies on biological 

control agents reviewed by Stiling and Cornelissen (2005) focused on their 

effectiveness while other areas of interest included their feeding or oviposition 

behaviour and the biotic effects on the target and/or the agents (e.g. tri-trophic 

interactions). The success of biological control programs is primarily determined by 

economic criteria, so potential biological control agents are either deemed to be a 

potential success or a failure based on their performance in totally or partially 

controlling a pest population (Stiling & Cornelissen, 2005).  

 

In this chapter, I review literature relevant to my studies. I start with a review of the 

distribution, life history, history as a recognised plant pest, and potential methods of 

control of the tomato-potato psyllid (TPP), Bactericera cockerelli (Sulc) (Hemiptera: 

Triozidae). I then review the literature on Orius vicinus (Ribaut) (Heteroptera: 

Anthocoridae) which is a potential biological control agent for TPP, and the effects that 

plant morphological traits (e.g., foliar pubescence, glandular trichomes, waxy leaf 

surface, and plant architecture) can have on the performance efficiency and behaviour 

of biological control agents. I have placed particular focus on tomato and capsicum 

because they provide the experimental surfaces I used here. I selected these plants 

because they are important crops grown in glasshouses and because they differ 

significantly in their substrate morphology. Finally, I then outline my aim and 

objectives for this thesis.  

 

  



3 

 

1.2 Tomato-potato psyllid (TPP) 

 

TPP was first described as Trioza cockerelli by Karel Sulc in 1909 (Butler & Trumble, 

2012a; Horton et al., 2016). In 1911 TPP was reassigned from the genus Trioza to 

Paratrioza (Butler & Trumble, 2012a). The genus Paratrioza was subsequently 

synonymized with the genus Bactericera in 1997, which also led to TPP changing 

families from Psyllidae to Triozidae (Burckhard & Lauterer, 1997; Butler & Trumble, 

2012a). TPP is also commonly known as either the potato psyllid or the tomato psyllid 

(Abdullah, 2008). 

 

TPP nymphs and adults are phloem-feeders that are capable of feeding on all plant 

surfaces (leaves, stems, petioles) (Butler & Trumble, 2012a). TPP infestations have 

been associated with outbreaks of economically important plant diseases (Butler & 

Trumble, 2012a). TPP can also affect crops via honeydew accumulation (insect faeces) 

which can result in sooty mould that can compromise the structure of the plant and may 

impose an economic cost due to fruit requiring cleaning or being downgraded (Prager et 

al., 2016). TPP infestations have the potential to inflict significant economic losses to 

solanaceous crops (e.g. potato, tomato, peppers, and eggplant) in North America, 

Central America, and New Zealand (Burckhard & Lauterer, 1997; Teulon et al., 2009; 

Butler & Trumble, 2012a; Munyaneza, 2012). Currently, the combination of chemical 

solutions and the implementation of cultural control methods such as removal of 

alternative breeding hosts is the standard control strategy for TPP outbreaks (Butler & 

Trumble, 2012a). Threshold benchmarks for IPM programs have been proposed, 

developed and deployed (Goolsby et al., 2007; Butler et al., 2011; Walker et al., 2015a; 

Prager et al., 2016). 

 

1.2.1 Distribution 

 

TPP is believed to be indigenous to the southwestern USA and northern Mexico 

(Goolsby et al., 2007). They are currently found throughout North and Central America, 

including USA (Arizona, California, Colorado, Idaho, Kansas, Minnesota, Montana, 

Nebraska, Nevada, New Mexico, North and South Dakota, Oklahoma, Oregon, Texas, 

Utah, Washington, and Wyoming), Canada (Alberta, British Columbia, Ontario, 

Saskatchewan), Mexico, Guatemala, Honduras, Nicaragua and New Zealand 



4 

 

(Burckhard & Lauterer, 1997; Gooslby et al., 2007; Butler & Trumble, 2012a;  

Munyaneza, 2012; Horton et al., 2015). TPP and their associated diseases were reported 

on Norfolk Island in 2014 and there are concerns it could reach mainland Australia or 

Tasmania via accidental importation or natural dispersals via airflow from New Zealand 

(Walker et al., 2015b). Californian capsicums infested with live TPP nymphs are 

rejected in high numbers by border authorities in Hawaii (Walker et al., 2015b). Costa 

Rica temporarily banned all imports of potato from Nicaragua once TPP and its 

associated diseases were discovered. These highlight the threat of this pest to the trade 

of a country (Munyaneza, 2012). 

 

Through the use of mitochondrial DNA (mtDNA), researchers have discovered four 

distinct TPP haplotypes within the United States which have been identified as central, 

western, northwestern and southwestern due to their presence in these regions 

(Munyaneza, 2015). These haplotypes may potentially differ in their capability to 

develop and reproduce on various host plants; transmit diseases; their overwintering 

capabilities; and magnitude of dispersal (Munyaneza, 2015). Previous genetic studies 

had suggested that TPP populations in North America belonged to two groups, one from 

western United States (invasive type) and the other from central United States and 

eastern Mexico (native type) (Liu et al, 2006a; Liu & Trumble, 2007). TPP that invaded 

New Zealand were believed to have come from the western North American range, in 

other words the “invasive” type rather than the “native” type (Walker et al., 2015b). 

 

The invasion of TPP into New Zealand may have occurred in the summer of 2005-2006 

(Teulon et al., 2009; Butler & Trumble, 2012a). However, the entry pathway remains 

unclear with the most likely scenario being accidental introduction from the western 

United States via smuggled primary host plant material into the Auckland region 

(Teulon et al., 2009; Thomas et al., 2011). TPP populations were established in both the 

North and South Islands of New Zealand by 2009 (Teulon et al., 2009; Thomas et al., 

2011). Widespread distribution is believed to have been achieved by a combination of 

natural dispersal (e.g. movement from infested crops to nearby crops) and human-

meditated dispersal (e.g. infested host plant material and inanimate objects) (Teulon et 

al., 2009). The affected indoor and outdoor crops included capsicum, tomato, tamarillo 

and potato (Teulon et al., 2009). TPP infestations and associated diseases resulted in 

IPM systems within the New Zealand vegetable sector being severely affected due to 



5 

 

increased usage of non-selective chemicals (Teulon & Hill, 2015). Furthermore the 

export certification of certain crops was momentarily lost (Teulon & Hill, 2015). 

 

1.2.2 Life history 

 

TPP have a host plant range that exceeds 20 plant families and they are capable of 

completing development on over 40 host species (Butler & Trumble, 2012a). Plant 

species from the family Solanaceae appear to be the preferred host plants; however, 

reproduction and development have also been recorded on species from the family 

Convolvulaceae including sweet potato (Butler & Trumble, 2012a; Munyaneza, 2012; 

Diaz-Montano & Trumble, 2013). TPP behaviours (including feeding, jumping and leaf 

abandonment); life parameters (including developmental rates and survivorship); and 

nymphal densities have been shown to vary between host plants species and even host 

plant cultivars (Liu & Trumble, 2004; Liu & Trumble, 2005; Goolsby et al., 2007; Yang 

& Liu, 2009; Yang et al., 2010b; Yang et al., 2013; Thinakaran et al., 2015a; 

Thinakaran et al., 2015b). The vast host range of TPP complicates the control of this 

pest due to the different susceptibilities each host plant has to TPP and its associated 

diseases (Prager et al., 2016). TPP nymphs (particularly from the northwestern 

haplotype) have the capability of overwintering on certain host plants (e.g. bittersweet 

nightshade) which are generally outside of agricultural crops, making management 

difficult (Goolsby et al., 2007; Butler & Trumble, 2012a; Munyaneza, 2015; Horton et 

al., 2015). Non-crop hosts can act as reservoir hosts which allow for future invasions 

into crop hosts (Thinakaran et al., 2015a). Despite the overwintering potential of TPP, 

the main mechanism for TPP presence in agricultural crops is believed to be their 

capacity to migrate long distances via air currents (Goolsby et al., 2007; Butler & 

Trumble, 2012a).  

 

1.2.2.1 Life stages 

 

TPP pass through hemimetabolous metamorphosis and their development is temperature 

dependent (Butler & Trumble, 2012a). The optimal laboratory temperature for survival, 

development and oviposition is believed to be 26.7°C, and these life history parameters 

begin to be negatively affected when temperatures rise beyond 32.2°C (Butler & 

Trumble, 2012a). Sustained temperatures above 38°C are lethal for eggs and nymphs 



6 

 

(Butler & Trumble, 2012a). Depending on the temperature, a single generation can be 

completed within three to five weeks (Munyaneza, 2012). Under ideal climatic 

conditions the rapid development cycle of TPP and the early reproductive capability of 

females allow for rapid population growth which tends to contain overlapping TPP 

generations within a growing season (Liu & Trumble, 2005; Lacey et al., 2009; Butler 

et al., 2011; Butler & Trumble, 2012a; Munyaneza, 2012). In countries and regions such 

as Mexico and Central America where temperature remains ideal for this species, 

regardless of the season, and where host plants are always available, it is possible for 

TPP to reproduce and develop throughout the year (Munyaneza, 2012). 

 

TPP eggs (Figure 1.1) are yellow, oval shaped, 0.3 mm in length, 0.1 mm in width and 

are attached to the plant surface (generally the leaves) via a 0.2 mm long stalk (Butler & 

Trumble, 2012a). The egg stage can take anywhere between 3 to 15 days and there is a 

1:1 sex ratio (Yang & Liu, 2009; Yang et al., 2010b; Butler & Trumble, 2012a; Yang et 

al., 2013). The nymph stage (Figure 1.1) consists of five instars, whose length of 

development may vary depending on host plant and field/laboratory conditions (Yang & 

Liu, 2009; Yang et al., 2010b; Yang et al., 2013). Host plants can influence the 

development of life stages with progression from egg to adult under laboratory 

conditions taking 18.7, 19.6, 24.1 and 26.1 days on tomato, potato, eggplant and 

capsicum, respectively (Yang & Liu, 2009; Yang et al., 2010b; Yang et al., 2013). 

Transitions from egg to adult have been found to take longer in field conditions (Yang 

et al., 2010b; Yang et al., 2013).  

 

  
Figure 1.1: TPP life stages: egg attached to capsicum leaflet (left); fifth instar TPP 

nymph on tomato leaflet (middle), and adult TPP on tomato leaflet (right). 

 

TPP adults (Figure 1.1) generally emerge with pale green or light amber in colour, 

eventually darkening to reach their brown/dark green adult coloration (Butler & 

Trumble, 2012a). Adult length ranges from 1.3mm to 1.9mm (Liu & Trumble, 2007; 



7 

 

Butler & Trumble, 2012a). They can live between 16 and 97 days (Yang & Liu, 2009; 

Yang et al., 2010b; Butler & Trumble, 2012a; Yang et al., 2013).  Females produce a 

pheromone that attracts males (Guedot et al., 2010). Adults are capable of reaching 

reproductive maturity within 48 hours from emergence (Guedot et al., 2012). The pre-

oviposition period (covering emergence to first egg oviposition) for females can range 

from 5.9 to 8 days (Abdullah, 2008). Females have the capability to oviposit between 5 

to 50 eggs over a 24 hour period (Butler & Trumble, 2012a). Furthermore, females have 

the ability to oviposit in excess of 1400 eggs in their lifetime (Liu & Trumble, 2005; 

Thinakaran et al., 2015a). In open field conditions females prefer potato and tomato to 

pepper, eggplant and silverleaf nightshade for oviposition (Thinakaran et al. 2015b).  

However, such preferences do not occur in laboratory conditions where adults prefer 

larger host plants regardless of species (Thinakaran et al., 2015b). Prager et al. (2014) 

suggest that TPP have host plant preferences influenced by haplotype.  

 

The spatial distribution of TPP adults within crops varies among host plants (Henne et 

al., 2010b; Butler & Trumble, 2012c; Prager et al., 2013c; Prager et al., 2014). TPP 

nymphs on potato tended to distribute themselves on the underside of leaves, but, on 

capsicum no such leaf side preference was found (Butler & Trumble, 2012c; Prager et 

al., 2013c). TPP were found primarily in the upper two thirds on both potato and 

capsicum plants (Butler & Trumble, 2012c; Prager et al., 2013c). These spatial 

distribution differences highlight the importance of developing sampling plans for 

specific crops (Prager et al., 2014). Adults are active dispersers and are capable of 

covering extensive distances within crops and therefore infesting multiple plants at 

relative rapid frequencies (Henne et al., 2010b). Alternatively, Thinakaran et al. (2015b) 

reported that TPP movement after landing was minimal. 

 

1.2.3 Diseases associated with TPP 

 

1.2.3.1 Psyllid yellows 

 

TPP was first classified as a pest of agricultural crops following an outbreak of an 

unidentified disease on potato crops in the late 1920s which was later attributed to the 

feeding behaviour of TPP nymphs and named ‘Psyllid Yellows’ (PY) (Butler & 

Trumble, 2012a). PY infects the entire plant which leads to reduction in growth, 



8 

 

erectness of new foliage, chlorosis of leaves, thickened internodes, aerial tubers, 

premature senescence and eventually plant death (Liu & Trumble, 2006; Butler & 

Trumble, 2012a). The nymphal stages of TPP are attributed as the main culprits in the 

proliferation of PY (Liu & Trumble, 2006; Butler & Trumble, 2012a). Symptoms 

appear at low and high nymph densities (Liu & Trumble, 2006; Butler & Trumble, 

2012a). The presence of crystalline honeydew produced by nymphs can be used as an 

indicator of TPP infestation (Abdullah, 2008). Adults do not appear to be as capable as 

nymphs in producing PY (Butler & Trumble, 2012a). Recovery from PY can potentially 

occur in potato and tomato plants if nymphs are removed within 10 days of infestation 

(Liu et al, 2006b; Butler & Trumble, 2012a). Therefore, PY is likely the result of an 

unidentified toxin rather than a pathogenic microorganism (Butler et al., 2012a; Prager 

et al., 2016).  

 

1.2.3.2 Candidatus Liberibacter  

 

The disease ‘Zebra chip’ (ZC) was first documented in the early 1990’s on potato crops 

in Mexico and later discovered in Texas and other American states (Munyaneza et al., 

2007b; Munyaneza et al., 2007b). ZC outbreaks in Mexico and the USA have resulted 

in massive economic losses (Munyaneza et al., 2007b). ZC is named after the dark 

brown streaks that appear in chips towards the end of the processing stage (Munyaneza 

et al., 2007b). ZC symptoms are similar to other TPP caused diseases (e.g. PY) 

(Munyaneza et al., 2007b). However, differences between PY and ZC symptoms have 

also been recognized (Secor et al., 2009). The exact cause of ZC went largely 

undetermined until observations made in the mid 2000’s correlated the abundance of 

TPP individuals with ZC infected potato crops in Mexico and the USA (Munyaneza et 

al., 2007b). ZC has now been documented throughout most of the known range of TPP 

including New Zealand (Secor and Rivera-Varas, 2004; Liefting et al., 2008; Henne et 

al., 2010a).  

 

While TPP was identified as the transmitting vector of ZC to solanaceous species, the 

causal agent of ZC was undetermined until 2008 when a phloem- limited, Gram 

negative, unculturable bacteria from the Alphaproteobacteria group named Candidatus 

Liberibacter psyllaurous (syn. Ca. L. solanacearum) was identified (Munyaneza et al., 

2007a; Hansen et al., 2008; Liefting et al., 2008; Munyaneza et al., 2008; Gao et al., 



9 

 

2009; Liefting et al., 2009a; Munyaneza et al., 2009d; Munyaneza, 2010; Munyaneza, 

2015). Hansen et al. (2008) proposed that a new bacteria species of the genus 

Candidatus Liberibacter, which the authors termed Ca. L. psyllaurous, was capable of 

infecting solanaceous plants and was vectored by TPP. About the same time, a 

previously undescribed disease was discovered in New Zealand solanaceous crops 

(capsicum, Cape gooseberry, tamarillo, tomato and potato) and ultimately revealed to be 

a new species of the Candidatus Liberibacter genus which was named Candidatus 

Liberibacter solanacearum (Liefting et al., 2008; Liefting et al., 2009a; Liefting et al., 

2009b). Further studies established that Ca. L. psyllaurous and Ca. L. solanacearum 

(referenced as CLs from this point on) were the same bacterium (Crosslin & Bester, 

2009; Munyaneza et al., 2009a,b,c; Secor et al., 2009; Wen et al., 2009; Crosslin et al., 

2010; French-Monar, 2010; Munyaneza, 2015). While CLs infections result in ZC 

disease in potatoes, the outcome of the infection in tomatoes, peppers/capsicums and 

eggplants is vein greening disease (Prager et al., 2016). Convolvulaceae species such as 

sweet potato and bindweed appear to be suitable hosts for TPP but not for CLs 

(Munyaneza, 2012).  

 

It has now been established that not all TPP colonies carry CLs (Henne et al., 2010a; 

Henne et al., 2010b). Temperatures below 17°C slow but do not prevent the 

development of CLs while temperatures above 32°C are known to be detrimental to CLs 

(Munyaneza et al., 2012). The heat sensitivity of CLs could explain the presence of this 

bacterium in certain countries and regions (Munyaneza et al., 2012). CLs can be 

transmitted vertically however the ratio of transmission through the different TPP life 

stages appears to be influenced by the host plant, e.g. greater on potato reared TPP than 

on tomato reared TPP (Hansen et al., 2008).  The bacterium is generally horizontally 

transmitted throughout crops by TPP feeding on infected plants and propagating the 

disease to healthy plants (Munyaneza, 2015). CLs are believed to be transmitted to the 

plant by nymphs and adults during phloem salivation, meaning that both life stages have 

to be controlled (Butler et al., 2012; Page-Weir et al., 2011; Echegaray et al., 2016). 

Adults were reported as being more efficient vectors than nymphs at transmitting CLs to 

plants (Buchman et al., 2011). The transmission of CLs to tomato and potato plants by 

an individual can range between less than 10 minutes to 6 hours; generally 

transmissions to susceptible plants will be achieved after one week of exposure to 

infected TPP (Hansen et al., 2008; Yang et al., 2010a; Munyaneza, 2010; Butler et al., 



10 

 

2011; Jorgensen et al., 2013; Prager et al., 2013a; Munyaneza, 2015). The latent period 

of the bacterium in TPP is roughly two weeks when feeding has occurred on infected 

potato plants, however it is shorter when feeding has occurred on infected tomato plants 

potentially due to the greater CLs titer in tomato than potato (Munyaneza, 2015).  

 

1.2.4 TPP management strategies 

 

1.2.4.1 Monitoring TPP 

 

Early detection of TPP invasions via ‘direct’ and/or ‘indirect’ sampling techniques 

increases the probability of implementing management decisions to eradicate/control 

TPP prior to population establishment and propagation of associated diseases and also 

assists in the development of economic action thresholds by confirming the efficacy of 

controls, trends of infestations and population dynamics of secondary pests and natural 

enemies (Al-Jabr & Cranshaw, 2007; Goolsby et al., 2007; Walker et al., 2011; Martini 

et al., 2012; Yen et al., 2013; Walker et al., 2013; Yen et al., 2013; Echegaray et al., 

2016). A study by Walker et al. (2011) on unsprayed potato crops in Pukekohe revealed 

that early season crops could avoid being damaged by TPP infestations and confirmed 

that sticky traps were a good indicator of crop infestation. Furthermore, Walker et al. 

(2013) developed a sub-sampling method of plants and recommended that crop scouting 

protocols for TPP infestations be based on sampling 100 middle leaves of 50 randomly 

selected plants. In order to mitigate the risk of TPP incursions into Australia an ongoing 

surveillance program using yellow sticky traps was initiated in 2011 in various locations 

around Tasmania, Victoria, South Australia and Queensland (Walker et al., 2015b).  

 

1.2.4.2 Insecticides 

 

Economic pressures on farmers to control TPP invasions immediately, because of their 

high reproductive rates and the threat posed by the suite of associated diseases that they 

carry, has led to insecticide applications being the most widely used TPP management 

strategy in the majority of affected regions (Goolsby et al., 2007; Yang et al., 2010a; 

Butler et al., 2011; Ail-Catzim., et al 2012; Butler & Trumble, 2012a; Munyaneza, 

2012; Mauchline & Stannard, 2013; Granados-Echegoyen et al., 2015; Munyaneza, 

2015; Prager et al., 2016; Villanueva et al., 2016). TPP management is complicated 



11 

 

because pathogens may be transmitted to the plant at the same time as insecticides are 

ingested by the insect (Liu & Trumble, 2004; Prager et al., 2013a). TPP death after toxic 

consumption generally takes longer than the time required by a TPP individual to 

transmit the pathogen to the plant (Yang et al., 2010a; Butler et al., 2011; Jorgensen et 

al., 2013; Prager et al., 2013a; Munyaneza, 2015). Prager et al. (2013a) proposed that 

ZC symptoms were found in their field study despite low TPP pressure and significant 

effects of insecticide treatments because 100% mortality was not achieved and enough 

TPP survived to transmit the bacteria. This outcome highlights the difficulty of 

managing diseases that can be passed on by relative few individuals (Prager et al., 

2013a).  

 

A variety of studies have focused on the immediate knockdown and residual effects of 

products on TPP nymphs and adults (Berry et al., 2009; Gharalari et al., 2009; Page-

Weir et al., 2011). The effectiveness of an insecticide may vary depending on the life 

stage that has been targeted; chemicals that control adults may not be effective against 

eggs and nymphs and vice versa while others can affect all life stages (Page Weir et al., 

2011; Butler & Trumble, 2012a; Prager et al 2013a; Prager et al., 2013b ;Munyaneza, 

2015; Echegaray et al., 2016). Insecticides will also affect TPP behaviours such as 

feeding, probing, cleaning, resting and walking in different ways (Butler et al., 2011; 

Butler et al., 2012). TPP reproduction can also be affected (Echegaray et al., 2016). 

Insecticides can reduced bacterium transmission by repelling TPP or inhibiting them 

feeding, but non-target effects and resistance have also been reported (Liu & Trumble, 

2007; Berry et al., 2009; Butler et al., 2011; Butler et al., 2012; Liu et al., 2012; Prager 

et al 2013a; Prager et al 2013b; Cerna et al.,2012; Ail-Catzim et al., 2015; Martinez et 

al., 2015).   

 

Resistance to insecticides by TPP has been linked to how long and how often certain 

insecticides have been used in the affected regions (Liu & Trumble, 2007; Prager et al., 

2013a; Chavez et al., 2015; Prager et al., 2016). The potential of TPP populations to 

develop resistance to commonly used chemicals could be mitigated with the 

introduction of newer insecticides with distinct modes of action (Echegaray et al., 

2016). The perception of ineffective TPP control via insecticides has also been proposed 

to be due to unsatisfactory spray coverage, faulty calibration and ineffective equipment 

rather than chemical resistance (Chavez et al., 2015). The application method of 



12 

 

insecticides can cause differences in mortality (Gharalari et al., 2009; Prager et al., 

2016). Good coverage of plant surfaces is vital for effective results due to TPP adults 

and nymphs regularly distributing themselves to the underside of leaves (Munyaneza, 

2015). 

 

The management of TPP is usually conducted via the calendar based rotation of a small 

group of insecticides (Goolsby et al., 2007; Liu & Trumble, 2007; Yang et al., 2010a; 

Butler et al., 2011; Guenthner et al., 2012; Prager et al., 2013a; Echegaray et al., 2016). 

Rotation of treatments with different modes of action serves as a tool for insecticide 

resistance management strategy and maximises the impact of natural enemies by 

deploying the more selective products earlier in the season (Gharalari et al., 2009; 

Anderson et al., 2013; Wright et al., 2015; Prager et al., 2016). TPP commercial 

insecticide programs in Northern New Zealand typically involve a greater number of 

applications in comparison to Southern New Zealand programs due to lower TPP 

pressure down South (Wright et al., 2015). Following consistent results over six 

growing seasons in the Pukekohe region Walker et al. (2015a) reported that insecticides 

are not required before the end of December. The New Zealand potato industry has 

taken the recommendation from Walker et al. (2015) onboard and growers are now 

saving up to 10 insecticide sprays per season in early potato crops and using more 

selective insecticides to minimize effects on natural enemies. 

 

Anderson et al. (2013) proposed that intense insecticide programmes do not guarantee 

the elimination of ZC risk and they are economically unsustainable. The arrival of TPP 

into New Zealand disrupted IPM practices for affected solanaceous crops due to the 

incompatibility of the majority of registered TPP controlling insecticides with existing 

IPM management plans (Berry et al., 2009; Mauchline & Stannard 2013). Similarly, 

dramatic increases in TPP populations resulted in pesticide usage increases and 

disruption of low-input IPM strategies of California and Baja California (Mexico) 

tomato crops (Liu & Trumble., 2004). Furthermore, growers in potato growing regions 

in Texas grew their crops without the use of insecticides prior to the appearance of ZC 

(Guenthner et al., 2012). Subsequently, growers via trial and error attempted to narrow 

down effective insecticides against TPP that were also least disruptive against beneficial 

species (Guenthner et al., 2012). Despite the use of multiple applications of insecticides 

with varied modes of action, yield and quality losses remain a problem for the affected 



13 

 

industries (Guenthner et al., 2012). Organic productions affected by TPP find that 

compatible insecticides are not abundant and those that are compatible may not provide 

effective protection on their own (Villanueva et al., 2016). Organic productions may 

require alternative host plants in order to increase numbers of natural enemies with 

assistance from the use of organic insecticides (Villanueva et al., 2016). 

 

1.2.4.2.1 Biorational insecticides 

 

The use of biorational insecticides (e.g. soaps/detergents, essential oils, mineral oils and 

botanical extracts, wettable sulphur, etc. ) is seen as an approach to maintain a 

sustainable TPP IPM program (Lacey et al., 2009; Yang et al., 2010a; Lacey et al., 

2011; Diaz Montano & Trumble, 2012; Jorgensen et al., 2013; Granados-Echegoyen et 

al., 2015; Wright et al., 2015). These environmentally sensitive products tend to be 

active against targeted pest population but also relatively harmless to non-target 

organisms which will allow the conservation and augmentation of biological control 

agents and will avoid the use of broad-spectrum insecticides (Yang et al., 2010a; Lacey 

et al., 2011; Diaz Montano & Trumble, 2012; Jorgensen et al., 2013). Phytotoxicity is a 

potential adverse effect of biorational insecticides (Yang et al., 2010a; Jorgensen et al., 

2013). Biorational products alone might be incapable of being a commercially viable 

option (Wright et al., 2015). However, mixing biorational insecticides with different 

traditional effective pesticides can possibly delay the development of resistance and 

increase their efficacy (Yang et al., 2010a). 

 

1.2.4.3 Biological control 

 

The reliance of broad-spectrum insecticides can be expensive, environmentally 

damaging, susceptible to resistance and lethal to natural enemies (Butler et al., 2011; 

Chavez et al., 2015; Granados-Echegoyen et al., 2015; Munyaneza, 2015; Pineda et al., 

2016). Concerns with chemical control dependency and potential resistance suggest 

there is a need to find alternative solutions (Butler et al., 2011; Chavez et al., 2015; 

Munyaneza, 2015; Prager et al., 2016). The use of biological control agents in 

conjunction with selective insecticide programs and other control methods is a 

prospective solution to deal with the overuse of chemical controls (Symondson et al., 

2002; Van Lenteren, 2012b; Prager et al., 2016). TPP has known natural enemies but 



14 

 

the number of studies on potential biological control agents acting on TPP is fairly 

limited and therefore the number of commercially available biological control agents 

exclusive to this pest are non-existent (Munyaneza, 2015; Prager et al., 2016). Most 

commercially available biological control agents are usually marketed towards other 

pest species that cause issues in similar host plants such as whiteflies, leafminers, thrips, 

aphids and spider mites (Prager et al., 2016; Bioforce Limited, 2014). 

 

1.2.4.3.1 Entomopathogenic fungi 

 

Fungi are an effective entomopathogen of Hemiptera due to their ability to penetrate the 

integument of the insect and not rely on uptake via the piercing and sucking mouthparts 

(Lacey et al., 2009). Furthermore, their insecticidal activity is usually host specific and 

can often complement predators and parasitoids (Lacey et al., 2011; Mauchline & 

Stannard, 2013). Commercially available fungi have been trialled on TPP adults and 

nymphs in the laboratory and greenhouses with varied success (Lacey et al., 2009; 

Lacey et al., 2011; Mauchline & Stannard, 2013; Tamayo-Mejía et al., 2014). 

Environmental factors are vital to entomopathogenic fungi success in field 

environments particularly in areas where temperatures and relative humidity 

percentages can fluctuate outside the range of ideal conditions for fungal germination 

and infection (Lacey et al., 2009; Lacey et al., 2011). Ultraviolet radiation inactivated 

conidia and was identified as the principal limiting factor of residual activity in 

entomopathogenic fungus applications (Lacey et al., 2011). The development of greater 

effective delivery systems such as spraying technology that efficiently targets the lower 

sides of leaves was proposed by Lacey et al. (2011) as a means to extend the viability of 

conidia and improve residual activity. Mauchline and Stannard (2013) emphasised the 

importance of timing spray applications of entomopathgens to periods when 

greenhouses are at an ideal temperature in order to maximise effectiveness.  

 

1.2.4.3.2 Parasitoids 

 

The North American parasitoid Tamarixia triozae (Burks) (Hymenoptera: Eolophidae) 

has been observed parasitizing TPP nymphs in Mexico and USA field environments 

(Rojas et al., 2015; Castillo Carrillo et al., 2016). Mexican T. triozae were imported to 

containment into New Zealand and subsequently granted release approval by the New 



15 

 

Zealand Environmental Protection Agency to manage TPP (Workman & Whiteman, 

2009; Environmental Protection Authority, 2016). A variety of studies have been 

performed on the T. triozae-TPP interactions (Martinez et al., 2015; Rojas et al., 2015; 

Yang et al., 2015; Hernández-Moreno et al., 2017). Yang et al. (2015) reported that T. 

triozae significantly preferred to parasitize larger (fourth and fifth) instar stages over 

smaller instar stages, potentially due to their greater nutritional content which would 

increase development and ensure lower mortality rates. When female parasitoids were 

deployed in, densities greater than one their searching efficiency was greatly reduced 

(Yang et al., 2015). Rojas et al. (2015) raised the issue that T. triozae is not known to 

target TPP adults that are largely responsible for the infection of plants with ZC disease. 

Nevertheless, T. triozae was deemed to have the potential to be used in augmentative 

TPP control programs on tomato and bell pepper (Rojas et al., 2015; Yang et al., 2015). 

The combination of T. triozae and entomopathogenic fungi against TPP nymphs has 

been tested with results revealing that the combination was more effective if the fungus 

is applied after the parasidoid has parasitized the target rather than before (Tamayo-

Mejía et al., 2015; Tamayo-Mejía et al., 2016). 

 

The susceptibility of T. triozae to broad spectrum insecticides has led to low parasitism 

levels being reported in the field (Liu et al., 2012; Martinez et al., 2015; Rojas et al., 

2015). However, a variety of insecticides have been identified by Liu et al. (2012) as 

being likely to be IPM compatible with T. triozae. Morales et al. (2015) recommended 

that the application of selective insecticides may be most effective when the parasitoid 

is in its pupal stage since this is the least susceptible stage. The apparent sensitivity of 

the parasitoid towards the tested insecticides in a laboratory environment led Martinez 

et al. (2015) to propose that the combination of these tools in a TPP IPM program must 

be evaluated further in a field environment. Liu et al. (2012) concluded that unlike 

parasitoids reared and tested in cages, vials or dishes, T. triozae on a plant can 

potentially escape the effects of detrimental insecticides by finding refuge in non-

contaminated sections of the plant or via insecticide residue degradation due to rainfall. 

Therefore, laboratory results should not be extrapolated immediately to commercial 

crop level although they do provide an insight of the potential effects they may have on 

the parasitoid. 

 



16 

 

1.2.4.3.3 Predators 

 

Augmentative releases of the parasitoid T. triozae are expensive to deploy due to the 

large numbers required; furthermore, they generally target larger TPP instars, limiting 

the impact on disease transmission by smaller TPP instars (Rojas et al., 2015; Calvo et 

al., 2016). T. triozae was tested in combination with Dicyphus hesperus Knight 

(Heteroptera: Miridae) on a variety of TPP life stages and the predatory mirid reportedly 

preferred to prey on unparasitized nymphs rather than parasitized nymphs (de Lourdes 

Ramírez-Ahuja et al., 2017). The simultaneous release of D. hesperus and T. triozae 

was summarised by de Lourdes Ramírez-Ahuja et al. (2017) as having the potential to 

succeed because each agent targets different TPP life stages but further research into 

their relationship was required before this interaction can be fully implemented. A 

variety of studies have been conducted on predatory mirids predating on TPP adults and 

nymphs (Martinez et al., 2014; Calvo et al., 2016; Pineda et al., 2016). D. hesperus and 

Engytatus varians (Distant) (Heteroptera: Miridae) were proposed as potential TPP 

predators to be deployed in IPM programs (Martinez et al., 2014; Calvo et al., 2016; 

Pineda et al., 2016). However, precaution is required prior to release because predatory 

mirids have the capability to injure plants (Martinez et al., 2014; Calvo et al., 2016; 

Pineda et al., 2016). 

 

The potential of coccinelid species as biological control agents of TPP have also been 

tested with varying results. For example, O’Connell et al. (2012) tested TPP nymph 

consumption by Cryptolaemus montrouzieri Mulsant, Cleobora mellyi Mulsant, and 

Scymnus loewii Mulsant on potato and tomato leaflets. The authors reported that C. 

mellyi consumed the greatest number of nymphs while S. loewii consumed the least. 

The research into the biological control potential of C. mellyi was advanced further by 

Pugh et al. (2015) who investigated TPP consumption in the presence of green peach 

aphids, potato aphids and whiteflies. The authors reported that no prey preference was 

found between the aphid species and TPP. However, there was a significant preference 

of TPP over whiteflies. TPP numbers in potato plants significantly decreased in the 

presence of C. mellyi which subsequently increased the production of tubers by the 

plants.  

 



17 

 

Ail-Catzim et al. (2012) reported that the third larval stage of Chrysoperla carnea 

(Stephens) (Neuroptera: Chrysopidae) was likely to be successful in augmentative 

biological control programs of TPP nymphs. Cerna et al. (2012) identified insecticides 

that were highly toxic towards C. carnea and therefore deemed to be impractical for 

their implementation in a joint biological/chemical TPP control program. However, the 

authors also proposed abamectin and endosulfan as candidates for integration with C. 

carnae releases due to their high toxicity towards TPP and low toxicity towards C. 

carnae. Similarly, Ail-Catzim et al. (2015) proposed that abamectin could be employed 

in cooperation with C. carnae in an IPM system. Interestingly, unlike Cerna et al. 

(2012), biefenthrin was not discarded by Ail-Catzim et al. (2015) and was also proposed 

to use in an IPM system. Like Cerna et al. (2012), profenofos and imidacloprid were 

also found to be highly toxic and discarded as an IPM option. 

 

Xu and Zhang (2015) proposed the predatory mite Amblydromalus limonicus Garman & 

McGregor (Acari: Phytoseiidae) as a potential biological control agent of TPP due to its 

capacity to consume and reproduce on a diet of TPP eggs, first, second and third instar 

nymphs and psyllid-produced honeydew and also be commercially mass reared. 

Villanueva et al. (2016) reported that adult Amblyseius largoensis (Muma) (Acari: 

Phytoseiidae) consumed TPP eggs on potato leaf disk. Furthermore, the predatory mite 

was observed in non-experimental settings predating on TPP nymphs. The authors also 

identified two further phytoseiid mites Typhlodromips near tennesseensis 

(Mesostigmata: Phytoseiidae), and Typhlodromalus near peregrinues (Mesostigmata: 

Phytoseiidae) as potential biological control agents for TPP but predatory tests were not 

conducted. Geary et al. (2016) reported that Anystis baccarum L. (Trombidiformes: 

Anystidae) was capable of attacking and killing large TPP nymphs but proposed that the 

predatory mite was potentially more suited to attack the egg and smaller nymphal stages 

of TPP despite not investigating these life stages in their study. Furthermore, the authors 

reported that the predatory mite appeared to be distracted by the presence of psyllid-

produced honeydew leading them to occasionally feed and be satiated on these sugars, 

leaving the prey alone. 

 

A TPP monitoring study on Pukekohe region potato crops by Walker et al. (2011) 

revealed that the brown lacewing Micromus tasmaniae (Walker) (Neuroptera: 

Hemerobiidae) and the small hover fly Melanostoma fasciatum (Macquart) (Diptera: 



18 

 

Syrphidae) were the most abundant predators. The study also revealed the presence of 

other predators such as Pacific damsel bug Nabis kinbergii Reuter (Hemiptera: 

Nabidae), 11-spotted ladybird Coccinella undecimpunctata L. (Coleoptera: 

Coccinellidae), and large spotted ladybird Harmonia conformis (Boisduval) 

(Coleoptera: Coccinellidae). Based on their presence in potato crops, MacDonald et al. 

(2015) investigated the potential of M. tasmaniae, M. fasciatum, N. kinbergii, C. 

undecimpunctata, and H. conformis as TPP biological control agents. All the tested 

predator life stages consumed all of the TPP life stages offered. However, the tested 

predators did not show any preference for TPP over Myzus persicae Sulzer (Hemiptera, 

Aphididae). The authors concluded that M. tasmaniae and M. fasciatum have the 

potential to be effective natural enemies of TPP in crop IPM programs that implement 

the use of selective insecticides and emphasise the use of conservation biological 

control methods.  

 

The biological control potential of Orius tristicolor (White) (Hemiptera: 

Anthocoridae) to control TPP in capsicum, tomato and potato Southern Californian 

crops was investigated by Butler and Trumble (2012b) during a two-year study which 

combined field study with laboratory feeding tests. O. tristicolor was categorized as a 

potential biological control agent due to its presence on the affected crops (particularly 

capsicum and tomato) and its ability to attack TPP nymph stages. A subsequent study 

by Castillo Carrillo et al. (2016) on the abundance of predatory arthropods on 

bittersweet nightshade, a non-crop host of TPP, found that O. tristicolor was one of the 

most abundant generalist predator species found. Tran (2012) investigated the biological 

control potential of O. vicinus to control TPP in New Zealand. The predatory bug 

consumed a greater number of egg and smaller nymphal stages in comparison to larger 

nymphal stages. The predatory bug preferably consumed thrip nymphs over TPP 

nymphs; however, it continued consuming TPP in the presence of its preferred prey. 

Tran (2012) concluded that further studies were required to assess the true impact of O. 

vicinus on TPP populations. Tran (2012) identified plant architecture and/or traits as 

potential factors that may affect the predatory behaviour of O. vicinus. Therefore, 

assesing the predatory bug on crops with variying morphological plant traits will 

provide further insight into their practical usefulness. Particularly, considering the 

potential of TPP to inflict economic losses to a wide variety of solanaceous crops, 

which vary in morphological traits.    



19 

 

1.3 Genus: Orius 

 

Species from the genus Orius (Hemiptera: Anthocoridae) are commonly known as 

minute pirate bugs or flower bugs (Lattin, 1999; Horton, 2008). There are roughly 70 

described Orius species that are geographically widespread (found in Oriental, 

Ethiopian, Palaertic, and Neotropical regions) occupying both natural and disturbed 

habitats (Horton, 2008). Orius spp. attack and consume small soft-bodied arthropods 

from a variety of taxonomic groups (e.g. thrips, scales, aphids, psyllids, and eggs/small 

larvae of Lepidoptera, Coleoptera, and Diptera) (Lattin, 1999; Horton, 2008; Gomez-

Polo et al., 2013). Consumption of prey is achieved via their piercing-sucking 

mouthparts, which are in the form of a slender beak/labium (Horton, 2008). Orius spp. 

can also supplement their diet with pollen, which means that they can potentially 

maintain themselves on this food source when prey populations are low (Lattin, 1999; 

Horton, 2008; Gomez-Polo et al., 2013). However, their ability to ingest plant juices 

means that they are also susceptible to systemic insecticide ingestion from root treated 

plants (Funderburk et al., 2000; Horton, 2008). Nevertheless, several studies have 

identified compatible insecticides that can be implemented concurrently with Orius spp. 

in IPM programs (Funderburk et al., 2000; Funderburk et al., 2013; Srivastava et al., 

2014).  

 

The colonization of crops by Orius spp. can occur without human intervention (Veres et 

al., 2012). However, various Orius spp. are produced by commercial insectaries for 

augmentative biological control programs against economically important pests in 

annual/perennial row crops, greenhouses and ornamental plants environments (Horton, 

2008; Bonte & De Clercq, 2011; Veres et al., 2012). An augmentative biological control 

programs reviewed by van Lenteren (2012b) found that Orius spp. were used in 9 out of 

20 programs involving heteropteran species. Control programs using O. laevigatus 

(Fieber) were implemented in 15 to 20 countries worldwide (van Lenteren, 2012b). 

Furthermore, control programs involving O. laevigatus and O. insidiosus (Say) were 

reported to have sold anywhere between a hundred thousand to a million individuals per 

week (van Lenteren, 2012b). The majority of studies on this family are generally 

focused around economically important arthropod pests (Horton. 2008). The predatory 

performance of Orius spp. has been trialled on a variety of plants (cucumber, sweet 

pepper, eggplant, sweet corn, lima bean, French bean, soy bean, tomato, cabbage, wild 



20 

 

grape, strawberry, potato, roses, sweet potato) with a variety of economically important 

pests (thrips, spider mites, whiteflies, aphids, Lepidoptera larvae and eggs) (Chambers 

et al., 1993; Coll & Ridgway, 1995; Eigenbrode et al., 1995; Eigenbrode et al., 1996; 

Coll et al., 1997; Brown et al., 1999; Zsellér & Kiss, 1999; Norton et al., 2001; Gitonga 

et al., 2002; Shipp & Wang., 2003; Rutledge & O’Neil, 2005; Economou et al, 2006; 

Hamdan & Abu-Awad, 2007; Chow et al., 2008; Madadi et al., 2008; Lundgren et al., 

2009; Chow et al., 2010; Dai et al., 2010; Jalalizand et al., 2011; El-Basha et al., 2012;  

Fathi, 2014).   

 

1.3.1 Orius vicinus 

 

O. vicinus is widely distributed in the Palaearctic region (particularly in Europe) 

(Lariviere & Wearing, 1994). It has subsequently been found in western North America 

(British Columbia, Oregon and Washington) since the 1930s but had previously been 

misidentified as O. minutus (Linnaeus) (Lewis & Lattin, 2010). Despite its vast 

Northern Hemisphere range its presence in the Southern Hemisphere was unknown until 

the early 1990s when Lariviere and Wearing (1994) recorded their existence on 

chemically untreated apple trees in the central Otago region. How and when O. vicinus 

became established in New Zealand remains unknown but it may have arrived earlier 

than the 1990s but its susceptibility to insecticides may explain why it failed to establish 

on commercial orchards (Lariviere & Wearing, 1994).  

 

The development of O. vicinus from egg to adult will generally take two months 

(Lariviere & Wearing, 1994).  The predatory bug will pass through five nymphal stages 

(Figure 1.2) which will generally take 16 to 18 days at 25C° (Lariviere & Wearing, 

1994). Adults (Figure 1.2) are relatively small and will reach a length between 2.0-2.6 

mm (Lariviere & Wearing, 1994). The predatory bug has two to three generations per 

year within their European range (Wearing & Attfield, 2002). Research in New Zealand 

indicates that there are usually two generations per year with a potential third generation 

being possible during warm seasons (Wearing & Attfield, 2002). Females from the 

second generation overwinter after mating (Wearing & Attfield, 2002).  

 



21 

 

 
Figure 1.2: Adult O. vicinus probing a TPP nymph on capsicum surface (left) and O. 

vicinus nymph on tomato surface (right). 

 

The predatory bug from the Palaearctic region is generally found in fruit trees 

(particularly apple trees of the Beauty of Boskoop variety, a preference that might be 

substrate related) and herbaceous plants (e.g. Chenopodium and Herecleum) (Lariviere 

& Wearing, 1994). It was also collected from a variety of North American plants by 

Lewis and Lattin. (2010), implying a vast host range in this region. O. vicinus in its 

natural environments in the Palaearctic region largely targeted aphids, mites, thrips and 

scale insects (Lariviere & Wearing, 1994; Wearing & Colhoun, 1999; Lewis & Lattin, 

2010). North American potential prey consisted of bark lice, psyllids, thrips, aphids and 

leafhoppers (Lewis & Lattin, 2010). The diet of the predatory bug in New Zealand has 

been observed to include mites, thrips and leafhoppers (Lariviere & Wearing, 1994; 

Wearing & Colhoun, 1999). 

  

O. vicinus survives on a variety of prey species and a pollen-specific diet in the 

laboratory (Heitmans et al. 1986).  Within a New Zealand context, Wearing and 

Colhoun (1999) studied the development and adult size of O. vicinus on the mites 

Aculus schlechtandali (Nalepa) (Prostigmata: Eriophyidae), Panonychus ulmi (Koch) 

(Trombidiformes: Tetranychidae), and Tetranychus urticae Koch (Acari: 

Tetranychidae), the larvae of the New Zealand flower thrip Thrips obscuratus 

(Crawford) (Thysanoptera: Thripidae) and the apple leaf curling midge Dasineura mali 

(Bouche) (Diptera: Cecidomyiidae). The authors found that the predatory bug fed and 

completed their development on all prey species. The fastest development time and 

largest adult size were recorded for the predatory bugs that fed on T. obscuratus and the 



22 

 

slowest development and smallest adult size were recorded for predatory bugs fed with 

A. schlechtandali. 

 

Within a biological control context, O. vicinus has previously been identified as having 

the potential to provide control against phytophageous mites (Heitmans et al, 1986). 

Wearing and Lariviere (1994) also raised the possibility that they could be mass reared 

and released in greenhouses. Furthermore, Wearing and Lariviere (1994) proposed the 

deployment of the predatory bug to act as a biological control agent in New Zealand 

apple and stonefruit orchards. The implementation of integrated organic production 

systems in New Zealand orchards with their use of selective insecticides or alternative 

pest management methods such as mating disruption further increased its suitability as a 

biological control agent (Walker et al., 1997; Walker et al., 1998; Wearing & Colhoun, 

1999). A study by Wearing et al. (2010) monitored the woolly apple aphid Eriosoma 

lanigerum (Hausmann) (Hemiptera: Aphididae) and its natural enemies on apple 

orchards between 1994 and 2000 as pest management transitioned from conventional 

fruit production (broad spectrum insecticide usage) to integrated fruit production 

(biological and cultural control along with selective insecticide usage). O. vicinus were 

either absent if organophosphate insecticides were applied or in low numbers if 

lufenuron (a chitin synthesis inhibitor) was sprayed. However, a significant greater 

number of O. vicinus were found in trees sprayed with the selective insecticide 

tebufenozide (Wearing et al., 2010). These results coincide with a study by van de Veire 

et al. (2002) who tested the effects of 22 pesticides on O. laevigatus and catalogued 

tebufenozide as harmless while also suggesting that lufenuron should not be used in 

conjunction with the predatory bug.  

 

1.4 The effect of morphological plant traits on biological control agents 

 

The assessment of a potential biological control agent on a targeted pest must consider 

the effect that the morphological traits of the host plant may have. These traits have the 

capacity to affect the pest control efficiency of the biological control agents by 

impeding their movement, reducing their attachment efficiency and providing refugia 

that allow prey to be completely or partially inaccessible (Clark & Messina, 1998; 

Cortesero et al., 2000; Reynolds & Cuddington, 2012a; Reynolds & Cuddington, 

2012b).  



23 

 

 

The gross morphology of plants (e.g., overall size, macroscopic shape and connectivity 

between plant parts) can affect the foraging success of predators and parasitoids 

(Reynolds & Cuddington, 2012a). Cloyd and Sadof (2000) investigated how plant 

height, leaf surface area, number of leaves and number of branches impacted the attack 

rate of the parasitoid Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae) on 

various densities of the citrus mealybug, Planococcus citri Risso (Hemiptera: 

Pseudococcidae). The authors found that the plant height and number of leaves of 

Solenostemon scutellarioides (L.) Codd (Lamiales: Lamiaceae) negatively affected the 

searching efficiency of the parasitic wasp. Gingras et al. (2002) suggests that the 

reliance of the parasitoid Trichogramma evanescens Westwood (Hymenoptera: 

Trichogrammatidae) on locomotion over chemical cues and flying to locate the eggs of 

Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) explains the decrease in their host 

finding ability and parasitism rate when plant structure connectivity increased (greater 

number of stems, secondary stems, leaves and buds resulted in more plant connections). 

Similarly, Gingras et al. (2008) found that T. turkestanica Meyer  located more E. 

kuehniella eggs on simple (less plant connections) than on complex (greater plant 

connections) plant structures. The authors suggest that increases in connections also 

increase the number of pathways and directions a parasitoid can take which lessens host 

finding efficiency. This effect has been shown in the performance of parasitoids on 

cabbage, Brussels sprouts and broccoli (Gingras et al, 2003). 

 

Like parasitoids, predators that rely on locomotion as their primary method of searching 

for prey are also susceptible to the effects of plant morphology. Legrand and Barbosa 

(2003) reported that the predation rates of Coccinella septempunctata Linnaeus on pea 

aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), decreased on structurally 

more complex hosts (complexity was determined by the number of branch nodes). 

However, Karaeiva and Sahakian (1990) found contrasting results when they reported 

that C. septempunctata had greater success capturing A. pisum on leafless mutant pea 

plants (with greater junctions) than on normal leafy pea plants (with less junctions). The 

predator falling off the slippery leaf surfaces was proposed by Karaeiva and Sahakian 

(1990) as the reason for greater success in the leafless plant. Similarly, Reynolds and 

Cuddington (2012a) found consumption rates on A. pisum for a similar predator 

Harmonia axyridis Pallas (Coleoptera: Coccinellidae), and dissimilar predator C. 



24 

 

carnea increased in highly branched pea plants and decreased in leafier and less 

branched pea plants. Different searching strategies and/or consumption capacities were 

proposed by Reynolds and Cuddington (2012a) as potential reasons why their results 

differed from Legrand and Barbosa (2003). Prey distribution was also proposed as a 

reason for the disparity in results. Karaeiva and Sahakian (1990) and Legrand and 

Barbosa (2003) used the same predator but differed in prey distribution (patchy 

distribution vs. roughly uniform distribution). Reynolds and Cuddington (2012a) 

concluded that partial refugia in leafier morphologies could make prey inaccessible to 

predators and would explain the lower consumption they and Kareiva and Sahakian 

(1990) reported. 

 

Enemy free spaces can be found in plants that provide refugia for prey to become 

inaccessible to predators. Clark and Messina (1998) proposed that predation rates of the 

fourteen-spotted ladybird, Propylea quatuordecimpunctacta (L), on the Russian wheat 

aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), were greater on Indian 

ricegrass than on crested wheatgrass due to the available refugia in the latter being large 

enough to allow aphids to find shelter but small enough to deny access to the predator. 

In comparison the refugia available on Indian ricegrass was relatively small and only 

allowed a certain number of aphids to be completely inaccessible to the predator, which 

left the majority of available aphids exposed to the predator. 

 

Gassman and Hare (2005) tested four natural enemies of the leaf feeding beetle Lema 

daturaphila Kogan and Goeden (Coleoptera: Chrysomelidae) and the piercing-sucking 

mirid bug Tupiocoris notatus Distant (Hemiptera: Miridae) on Jimsonweed which 

exhibits two trichome phenotypes: a velvety phenotype (surface is densely covered with 

short non-glandular trichomes) and a sticky phenotype (surface is less densely covered 

with glandular trichomes that secrete glucose esters and aliphatic acids). Natural 

enemies were less effective on sticky surfaces due to their movement being hampered 

and the authors hypothesized that the negative impact of glandular trichomes on 

predators might have led to certain herbivores specializing on these plants due to the 

enemy free space they provided. 

 

Eigenbrode et al. (1996) tested the mobility and predation rates of adult Hippodamia 

convergens Guerrin-Menneville (Coleoptera: Coccinellidae), adult O. insidiosus, and 



25 

 

larval C. carnea on larval populations of the diamondback moth Plutella xylostella (L.) 

(Lepidoptera: Plutellidae) on two cabbage surfaces (normal-wax and glossy) which 

differed in the amount of crystallized waxes (wax bloom) found on their surfaces.  The 

authors found that predators were less mobile and spent more time grooming on the 

normal-wax surfaces (extensive wax bloom) due to reduced traction/attachment.  

Furthermore, the greater number of prey encounters on glossy surfaces (no wax bloom) 

was attributed to predators experiencing less mobility impediments which increased 

searching efficiency and thus emphasised a link between mobility and predation.  

 

Fathi (2014) investigated the predation rates of O. minutus on T. urticae on potato 

cultivars that differed in leaf trichome densities. The authors found that the predation 

rates of O. minutus were significantly higher on the cultivar with the lowest trichome 

density. Furthermore, there was no difference in predation rates between the two 

cultivars with high trichome density. Similarly, Jalalizand et al. (2011) also focused on 

T. urticae predation (via functional response) but using Orius niger niger (Hemiptera: 

Anthocoridae) on cucumber (high trichome density) and strawberry (low trichome 

density) leafs. The predator handling time was highest and searching efficiency was 

lowest on cucumber, while the maximum number of prey attacked by the predator was 

highest on strawberry. The authors attributed this result to the mechanical effect that 

cucumber trichomes had on the movement and subsequent encounter rate of the 

predator. Krips et al. (1999) reported that Phytoseiulus persimilis Athias-Henriot (Acari: 

Phytoseiidae) moved faster on the gerbera cultivar surface with the lowest trichome 

density. Furthermore, the effect of leaf hair density on predation of T. urticate eggs by 

the predatory mite was only significant at low prey densities with no effect at high prey 

densities. 

 

1.4.1 Assessment of experimental plant surfaces  

 

1.4.1.1 Tomato plant surfaces 

 

There are host plant structures that are either partially or completely unsuitable for 

either predators or parasitoids to maintain pest populations below economic threshold 

levels. The literature suggests that the stems and foliage of tomato plants can be a 

hostile environment for potential biological control agents due to the negative effect 



26 

 

tomato non-glandular and glandular trichomes have on the foraging performance of the 

predator/parasitoid (De Clercq et al, 2000; Kennedy, 2003; Shipp & Wang, 2003; 

Economou et al, 2006; Koller et al 2007).  

 

Cédola et al. (2001) found that Neoseiulus californicus McGregor (Acari: Phytoseiidae) 

predating on the two-spotted spider mite, T. urticae, exhibited poor predatory 

performance when tested on two tomato hybrids with different glandular trichome 

densities. De Clerq et al. (2000) reported that the foraging efficiency of Podisus 

nigrispinus Say (Heteroptera: Pentatomidae) on various densities of the beet armyworm 

Spodoptera exigua Hubner (Lepidoptera: Noctuidae) was lowest on tomato surfaces in 

comparison to other tested host plant surfaces. Verheggen et al. (2009) reported that 

larvae Episyrphus balteatus De Geer (Diptera: Syrphidae) predating on M. persicae 

moved significantly slower on the stems of tomato in comparison to other tested plant 

surfaces. Furthermore, a significantly greater number of predators were recorded falling 

off the stem surface of tomato. The authors from these studies concluded that tomato 

surfaces impeded efficient locomotion. 

 

O’Connell et al. (2012) tested TPP nymph consumption by Coccinellid species on 

tomato and potato plant surfaces. Adults and fourth instar larvae of C. mellyi consumed 

the greatest number of TPP nymphs on both plant surfaces and showed no difference in 

performance between plant surfaces. However, S. loewii adults performed poorly on 

tomato surfaces. Behavioural observation results on tomato leaflets revealed that the 

smaller S. loewii spent more time grooming and less time searching for prey while the 

opposite occurred for the larger C. mellyi. The authors concluded that C. mellyi had a 

morphological advantage over S. loewii due to their larger size, which enabled greater 

consumption capacity and reduced the effect of tomato trichomes on their mobility.  

 

The searching behaviour of highly mobile predators like Orius spp. may be influenced 

by the plant surface in which they are released (Coll et al., 1997). The walking speed of 

adult O. insidiosus was found by Coll et al. (1997) to be significantly slower on tomato 

surfaces than on plant surfaces with lower trichome densities. The authors conducted 

simulated searching efficiency tests (by overlapping the information gathered from prey 

distribution maps and predator walking paths) and the results indicated that at low prey 

densities the rate of encounters would be lowest on tomato surfaces. The activity of O. 



27 

 

niger Wolff was tested by Economou et al. (2006) on different varieties of tomato 

cultivars which differed in trichome density. The authors found that the predatory bug 

spent more time grooming and less time moving on the cultivar with the greatest 

trichome density. Furthermore, Shipp and Wang (2003) tested the effectiveness of 

augmentative releases of the predatory bug O. insidiosus on greenhouse tomatoes 

infested with Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) and 

found that it failed to reduce the pest to acceptable non-economic loss densities. 

Monitoring of population densities revealed that O. insidiosus failed to establish on 

tomato crops. A number of dead O. insidiosus nymphs were found tangled on the 

glandular hairs of tomato stems, implying that establishment failure could be related to 

the impact of tomato surfaces. Alternatively, Hamdan and Abu-Awad (2007) reported 

that O. laevigatus consumed significantly more tobacco whitefly larvae Bemisia 

tabacion (Gennadius) (Hemiptera: Aleyrodidae) on the leaf discs of tomato than on 

eggplant. It is important to highlight that both tomato and eggplant leaf surfaces are 

densely covered with trichomes (Kennedy, 2003; Madadi et al., 2008) and that a plant 

surface with lower trichome densities was not tested in this study. 

 

1.4.1.2 Capsicum plant surfaces 

 

Sweet pepper/capsicum surfaces appear to have greater suitability for predators and 

parasitoids that rely on locomotion to search for prey and hosts. As demonstrated by 

Hernández-Moreno et al. (2017) who found that T. triozae consumed more TPP nymphs 

on capsicum plants than on tomato plants, attributing this result to the effects of tomato 

trichomes. Furthermore, Madadi et al. (2007) found that the handling time of Neoseiulus 

cucumeris (Oudemans) (Acari: Phytoseiidae) predating on onion thrips Thrips tabaci 

(Lindeman) (Thysan: Thripidae) was lowest on capsicum than on plant surfaces with 

greater trichome densities. Choudhury and Copland (2003) found that when the 

parasitoid wasp Anagarus atomus Linnaeus (Hymenoptera: Mymaridae) was exposed to 

the glasshouse leafhopper, Hauptidia maroccana Melichar (Hemiptera, Cicadellidae)  

they moved fastest on sweet pepper surfaces in comparison to other plant surfaces that 

ranged in greater trichome densities. Similarly, Sütterlin and van Lenteren (1997) 

reported that Encarsia formosa Gahan (Hymenoptera: Aphelinidae) recorded faster 

walking speeds on capsicum in comparison to tomato leaves. These studies highlighted 

https://www.google.co.nz/search?q=Aphelinidae&stick=H4sIAAAAAAAAAONgVuLUz9U3SKksMC5fxMrtWJCRmpOZl5mSmAoAT2C6fhsAAAA&sa=X&ved=2ahUKEwj96ZysmMrgAhUaTn0KHV3KBBMQmxMoATAVegQIBRAV


28 

 

the relationship between trichome density and movement (a key component of 

searching success).  

 

Despite their apparent suitability for predators and parasitoids, the surfaces of 

capsicum/peppers can deleteriously affect their predation/paratisim rates. Abdala-

Roberts et al. (2014) investigated the abundance of the predatory mite Amblyseius 

swirskii Athias-Henriot (Mesostigmata: Phytoseiidae) and their predation rates of thrips 

Frankliniella cephalica Crawford DL (Thysanoptera: Thripidae) on 17 different pepper 

(Capsicum annuum Linnaeus) varieties that varied in flower number, pollen production 

and leaf trichome density. Greater A. swirskii densities were reported on varieties with 

an intermediate trichome density. High trichome densities appeared to interfere with A. 

swirskii foraging and influenced the low abundance of the predator on these varieties. 

The authors concluded that this trait may incur an ecological cost to the host plant by 

reducing indirect defences and potentially benefiting pests. Leaf surface hairiness could 

be taken as an indicator that predators/parasitoids may struggle to effectively control a 

pest population, however, this may not always be the case. Kheradpir et al. (2008) 

found that consumption of spider mites T. urticae by the predacious thrips Scolothrips 

longicornis Priesner (Thysanoptera: Thripidae) was highest on the hairier tomato 

surface than on the hairless/smoother capsicum surface. The authors suggested that the 

capsicum surface was too slippery for effective traction which affected the movement of 

the predator. 

 

Despite of the unsuitability of sweet pepper/capsicum plant surfaces in certain predator-

prey interactions they do appear to be suitable for effective Orius spp. predation. As 

demonstrated by O. albidipennis (Reuter) on leaf discs (Madadi et al., 2008) and small 

plants (Madadi et al., 2009). Furthermore, Van de Veire and Degheele (1992) reported 

that O. niger contributed to the population decline of Western flower thrip in Belgian 

sweet pepper glasshouse crops.  

  

1.5 Aims and objectives 

 

The aim of this thesis was to investigate how the morphological structures of plant 

surfaces (hairy tomato vs. non-hairy capsicum) can influence the predatory behaviour 

and efficiency of a potential biological control agent (O. vicinus) on an economically 



29 

 

important pest (TPP) that affects a variety of host plants. The objectives of this thesis 

were to: 

 

1. Determine the effects of plant surface morphology on the TPP nymph 

consumption capacity of O. vicinus (Chapter 2). 

2. Assess how the surface structure influences the dispersal of TPP nymphs in the 

presence and absence of O. vicinus (Chapter 2). 

3. Determine the TPP nymph size preference of O. vicinus (Chapter 2 and Chapter 

3).  

4. Investigate the behaviour of O. vicinus and the defensive behaviours (fight or 

flight) of TPP nymphs during predator-prey encounters on morphologically 

dissimilar surfaces (Chapter 3). 

 

  



30 

 

  



31 

 

Chapter 2: The effect of host plant substrate on the biological control potential of 

Orius vicinus (Ribaut) on Bactericera cockerelli (Sulc) nymphs.  

 

2.1 Abstract 

 

Broad-spectrum insecticides are the preferred option for managing invasions to 

solanaceous crops by the tomato-potato psyllid (TPP) Bactericera cockerelli (Sulc). 

However, chemical reliance is associated with a host of issues. Therefore, the 

development of alternative management options such as biological control is vital for 

implementing future Integrated Pest Management (IPM) programs. This chapter 

investigates the biological control potential of Orius vicinus (Ribaut) adults acting on 

TPP nymphs on morphologically distinct plant surfaces (tomato versus capsicum). The 

functional response of adult O. vicinus simultaneously exposed to all TPP nymphal 

stages was determined to be Type II on both plant surfaces. The handling time (Th) was 

significantly longer and the searching efficiency (a) was slightly greater on tomato in 

comparison to capsicum. Nymph consumption at higher prey densities (30 and 40 

nymphs) was significantly greater on capsicum than on tomato. Nymph consumption at 

lower prey densities (10 and 20 nymphs) was only significantly greater on capsicum 

when the complexity of the experimental arena was increased from leaflet to small 

plant. The presence of O. vicinus increased the dispersal of nymphs to lower leaf 

surfaces. Nymph dispersal was significantly greater on capsicum than on tomato. O. 

vicinus was capable of attacking and killing all nymphal stages. The predatory bug 

significantly preferred medium sized nymphs on both surfaces.  

 

2.2 Introduction 

 

The economic impact of tomato-potato psyllid (TPP) Bactericera cockerelli (Sulc) 

invasions to solanaceous crops has led to chemical control being the preferred 

management option (Liu & Trumble, 2004; Goolsby et al., 2007; Berry et al., 2009; 

Yang et al., 2010a; Ail-Catzim., et al 2012; Butler & Trumble, 2012a). However, broad-

spectrum insecticide usage can be expensive, can cause environmental contamination, 

and can lead to secondary pest outbreaks due to natural enemies being removed (Van 

Lenteren & Woets, 1988; Butler et al., 2011). Furthermore, dependency on chemical 



32 

 

control may lead to chemical resistance (Goolsby et al., 2007; Gharalari et al., 2009; 

Butler et al., 2011; Cerna et al., 2012; Liu et al., 2012; Martinez et al., 2015; 

Munyaneza, 2015; Barrios-Diaz et al., 2016; Calvo et al., 2016; Prager et al., 2016). 

Therefore, integrated pest management (IPM) that incorporates biological control 

methods along with target-specific pesticides and cultural control methods is a 

prospective long term alternative to broad-spectrum insecticide usage (Liu et al., 2006b; 

Liu et al., 2012; Martinez et al., 2015; Calvo et al., 2016; Prager et al., 2016).  

 

Butler and Trumble (2012b) identified Orius tristicolor (White) (Hemiptera: 

Anthocoridae) as a potential TPP biological control agent in Southern California 

solanaceous crops. The predatory bug has also been found on bittersweet nightshade 

(Solanum dulcamara L), a key non-crop host of TPP (Castillo Carrillo et al., 2016). 

Certain species from the Orius genus (Hemiptera: Heteroptera: Anthocoridae) are mass-

produced by commercial insectaries for use in augmentative biological control programs 

that target economically important pests (Horton, 2008; Colomer et al., 2011; Veres et 

al., 2012; van Lenteren, 2012b; van Lenteren et al., 2017). Commercial insectaries in 

New Zealand are now mass-producing Orius vicinus (Ribaut) (Heteroptera: 

Anthocoridae) as a biological control agent of various insect pests (e.g. thrips, aphids 

and spider mites) (Bioforce Limited, 2014). The predatory bug has been observed 

preying on mites, aphids, thrips, psyllids, leafhoppers and scale insects (Lariviere & 

Wearing, 1994; Wearing & Colhoun, 1999, Wearing & Attfield, 2002; Lewis & Lattin, 

2010; Wearing et al., 2010). Tran’s (2012) functional response study found that O. 

vicinus was capable of consuming TPP nymphs (particularly smaller nymphs), 

suggesting that the predator may have potential for augmentative release programs for 

TPP management. 

 

The failure of arthropod predators to manage pest densities below economic thresholds 

has been linked to prey densities rapidly increasing and overwhelming the functional 

response of the predator (O’Neil, 1997). The functional response describes the 

relationship between prey density and the number of prey consumed by a predator. The 

functional response of a predator will generally fit one of the following three types of 

mathematical models: Type I (linear), Type II (convex) or Type III (sigmoid) (Holling, 

1959; Hassell et al., 1977; Colton, 1987; O’Neil, 1997; Gitonga et al., 2002; Lester & 

Harmsen, 2002; Stewart et al., 2002; Xiao & Fadamiro, 2010). Type II responses are 



33 

 

most commonly observed among arthropod predators and are characterized by the 

proportion of prey consumed monotonically declining with increasing prey density 

(Holling, 1959; Beddington 1975; Hassell et al., 1977; O’Neil, 1989; Gitonga et al., 

2002; Stewart et al., 2002; Pervez, 2005; Timms et al., 2008; Xiao & Fadamiro, 2010). 

Type III responses are typically associated with efficient biological control agents 

(Fernández-arhex & Corley, 2003; Xiao & Fadamiro, 2010). However, potential 

biological control agents that exhibit Type II responses on targeted pests have been 

identified (De Clercq et al., 2000; Badii et al., 2004; Timms et al., 2008). The functional 

response can be broken down into two components: (1) the searching efficiency, which 

includes aspects of the encounter rate, strike rate and capture efficiency, and (2) the 

handling time, which includes the effects of recognition, pursuit, capture, ingestion and 

digestion of prey (Holling, 1959; Thompsom, 1975; Spitze, 1985; El Basha et al., 2012).  

 

Functional response and other predatory assessment studies are generally performed in 

laboratory settings in order to control the experimental arena (Symondson et al., 2002; 

Timms et al., 2008). Laboratory studies tend to test predators on homogeneous prey 

populations (Schenk & Bacher, 2002). Subsequently, predation on different instars is 

investigated separately and the results are generally characterized with different output 

values (e.g. attack rate and handling time). However, arthropod species undergo 

considerable changes in size during their lifecycle, which inevitably results in the 

coexistence of multiple size classes of targeted prey and biological control agents 

(McArdle & Lawton, 1979; Colton, 1987; Lester & Harmsen, 2002; Rudolf, 2008). 

Furthermore, predators are typically exposed to artificial environments (i.e. high prey 

density on a Petri dish with limited or no plant component presence) that generally fail 

to emulate host plant environments where prey can be harder to access/capture (e.g. 

leaf/stem texture can influence the searching behaviour of predators and the 

distribution/dispersal of prey) (Hassell et al., 1977; Everson, 1980; Carter et al., 1984; 

O’ Neil, 1989; Coll et al., 1997; O’Neil, 1997; Messina & Hanks, 1998; Stewart et al., 

2002; Mahdian et al., 2007; Davidson et al., 2016).  

 

The host plant plays a pivotal role in predator/prey interactions and thus the 

morphological characteristics of host plants (e.g. substrate) could influence the 

predatory performance of a biological control agent in the field (Hassell et al., 1977; 

Everson, 1980; Cortesero et al., 2000; De Clercq et al., 2000; Mahdian et al., 2007; 



34 

 

Timms et al., 2008). The interactions between plant, pest, potential biological agent and 

environment need to be understood in order to formulate and establish an effective 

biological control program that fits within the IPM paradigm (De Clerq et al., 2000). 

Furthermore, biological control agents may have to cope with different morphological 

plant features in order to be a commercially viable management option against pest 

species that infest a wide range of host plants (Skirvin & Williams, 1999). Therefore, 

results gained in laboratory environments should be assessed with caution and 

experimental environments should incorporate as much naturalistic attributes as 

possible if these are to be used in assessing the true potential of a biological control 

agent (Everson, 1980; Messina & Hanks, 1998; Stewart et al., 2002; Kumar & Mishra, 

2014). 

 

The aim of this study was to investigate the biological control potential of O. vicinus on 

TPP nymphs, with  four  objectives: (1) to investigate the effect of the morphological 

structures of the host plant (smooth surfaced capsicum vs. hairy surfaced tomato) on the 

predatory performance of O. vicinus, (2) to assess the effect of the host plant on TPP 

nymph movement in both the presence and absence of O. vicinus, (3) to test TPP nymph 

size preference by O. vicinus, and (4) to compare predatory performance of O. vicinus 

on experimental arenas varying in complexity.  

 

2.3 Material and Methods 

 

2.3.1 Experimental plants  

 

Tomato (Solanum lycopersicum cv. Moneymaker) and capsicum (Capsicum annuum cv. 

California Wonder) plants (Figure 2.1) were grown at the Plant Growth Unit (PGU), 

Massey University, Palmerston North. Seeds were obtained from Egmont 

Seed Company Ltd, New Plymouth. The experimental plants were chosen due to the 

impact TPP has on their respective industries and their known differences in leaf surface 

trichome density (Sutterlin & van Lenteren, 1997; Madadi et al., 2007). When plants 

were five weeks old, they were transferred to a 25°C controlled temperature room with 

a photoperiod of 16:8 h (L:D). 

 



35 

 

 
Figure 2.1: Adult O. vicinus on smooth surfaced capsicum (left) and hairy surfaced 

tomato (right) leaves. 

 

2.3.2 Insect colonies 

 

TPP nymphs were obtained from a Plant and Food Research, colony and reared on 

tomato (S. lycopersicum cv. Moneymaker) and capsicum (C. annuum cv. California 

Wonder) plants in Massey University, Palmerston North. O. vicinus were obtained as 4
th

 

or 5
th

 stage nymphs from Bioforce Ltd, Auckland. The predators were reared in plastic 

containers (length: 15 cm, height: 9 cm, width: 7 cm) with mesh-covered holes. TPP 

nymphs were provided as prey on capsicum or tomato leaflets attached to a tube filled 

with water. Leaflets were replaced daily to ensure constant supply of nymphs to the 

predators. The leaflets with O. vicinus eggs were placed in separate containers in order 

to ensure the completion of the predatory bug lifecycle. Due to time constraints, adults 

were not assessed separately by sex in this study. TPP and O. vicinus colonies were 

maintained in a 25C° controlled temperature room with a photoperiod of 16:8 h (L:D). 

All experiments were carried out under this environmental condition. All insects used in 

the experiments completed their lifecycle in the experimental environment.  

 

2.3.3 Experimental design 

 

2.3.3.1 Leaflet experimental arena: O. vicinus TPP consumption, functional response, 

prey size preference and TPP movement in absence or presence of a predator 

 

The leaflet experimental arena consisted of a Petri dish (diameter: 85 mm, depth: 12 

mm) covered by a plastic jar (diameter: 85 mm, height: 100 mm) containing ventilation 

holes on its sides covered with mesh. A capsicum or tomato leaflet was raised off the 



36 

 

base of the Petri dish by an entomological pin (height: 38 mm) and a plastic vial 

(height: 40 mm) filled with water. The pin and vial were held in place by small balls of 

blutack
® 

(Figure 2.2). The purpose of raising the leaflet from the surface of the Petri 

dish was to isolate the predator and prey on the leaflet surfaces and to allow predator-

prey interactions to take place on upper and lower leaflet surfaces as they would in a 

natural setting.  

 

 
Figure 2.2: Petri dish containing the raised tomato leaflet uncovered (left) and covered 

with jar with ventilation holes (right). 

 

Prey densities used in this experiment comprised of nymphs at different developmental 

stages: 20% small sized (1
st
 and 2

nd
 instars), 40% medium sized (3

rd
 instar), and 40%