Open Access

The worldwide status of phasmids (Insecta: Phasmida) as pests of agriculture and forestry, with a generalised theory of phasmid outbreaks

Agriculture & Food Security20154:22

DOI: 10.1186/s40066-015-0040-6

Received: 29 June 2015

Accepted: 16 October 2015

Published: 1 December 2015

Abstract

Stick insects have been reported as significant phytophagous pests of agricultural and timber crops since the 1880s in North America, China, Australia and Pacific Islands. Much of the early literature comes from practical journals for farmers, and even twentieth Century reports can be problematic to locate. Unlike the plaguing Orthoptera, there has been no synthesis of the pest status of this enigmatic order of insects. This paper provides a literature synthesis of those species known to cause infestation or that are known to damage plants of economic importance; summarises historical and modern techniques for infestation management; and lists known organisms with potential for use as biological control agents. A generalised theory of outbreaks is presented and suggestions for future research efforts are made.

Keywords

Pests Infestation Agriculture Forestry

Background

The unexampled multiplication and destructiveness of this insect at Esperance farm is but one of the many illustrations of the fact, long since patent to all close students of economic entomology, that species normally harmless may suddenly become very injurious”. Riley [1]

Compared to their close relatives, the Orthoptera (sensu stricto) the Phasmida (=Phasmatodea, Phasmatoptera, Cheleutoptera) are not well known as agricultural or forest pests, despite sharing a number of key traits: large body size [2]; kentromorphism [3]; and having a widespread history of considerable damage to forests and crops [4]–[5]. The existence of kentromorphic (density-dependant) forms of some species may be homologous to the solitary and gregarious forms of the plaguing locusts. The fecundity of females is likely to be a significant factor in the scale of phasmid outbreaks—in most species, females lay several hundred eggs [6]. In addition, their wasteful eating habits [7] and their often rapid growth [8] means they consume a large quantity of vegetation [9]. Considerable efforts have been put into controlling the three species of Australian phasmid known to cause periodic infestation [10].

Phasmid outbreaks are occasionally still reported [11] although it appears that nothing from these outbreaks has yet reached the scientific literature. This work compiles the current knowledge on phasmid outbreaks and those species known to threaten economically important forests or crops, along with what little is currently known on methods for biological control. It is hoped that such a work will allow future authors to more easily place phasmid outbreaks in a worldwide scientific context and encourage their reporting in the literature, as well as providing a concise background to the importance of studying species that either parasitise or predate these insects.

This introduction provides a high-level overview of what is currently known about phasmid biology relating to their pest status. This is followed by individual accounts of pest species, and new conclusions on what causes phasmid outbreaks.

Aspects of phasmid biology potentially relevant to pest status

Kentromorphism

Density-dependent polymorphism (kentromorphism) is well studied in the members of the Acrididae (Orthoptera) colloquially known as ‘locusts’. Perhaps the best known example of kentromorphism is the two phases of Locusta migratoria [12]. In L. migratoria, the kentromorphic changes are both morphological and behavioural, creating the cryptic solitary phase and gregarious swarming phase of this species (it should be noted that intermediate forms do exist). Key [3] provides evidence of kentromorphic phases in three species of Australian phasmid known to be pests: Didymuria violescens, Podacanthus wilkinson, and Ctenomorphodes tessulatus although there is no noticeable change in activity pattern and no obvious tendency to gregariousness [13]. The solitary phases are heavily camouflaged, while the gregarious phases have aposematic colouration.

Fecundity

Phasmids generally lay a large number of eggs, so a high mortality of the egg and nymphal stages is expected. Indeed, many new phasmid hobbyists find themselves overrun after a single generation. While a number of generalist and insectivore predators attack phasmids, there are a number of phasmid egg specialist parasitoids in both the Diptera and Hymenoptera.

Foodplant choice

In general, the diet of phasmids can be considered to be polyphagous, with many species not having a unique host plant, or being capable of switching to alternative hosts if the favoured host is unavailable [14]. Blüthgen and Metzner [15] show a relationship between the age of leaf favoured and the degree of polyphagy of the phasmid, with more host-specific phasmids favouring younger leaves and vice versa. Campbell [7] agrees with this result describing host-plant preference within the genus Eucalyptus for species that feed on young foliage.

Experiences of rearing phasmids in captivity [16] and with invasive species [17] show many species are highly polyphagous.

Damage to crops

Campbell [7] reports that the Australian species Didymuria violescens and Podacanthus wilkinsoni exhibit strong negative geotaxis from the first nymphal stage—climbing trees and feeding on the growing tips of Eucalyptus. Prathapan et al. [18] report similar findings in India of Sipyloidea stigmata feeding on the terminal shoots of Piper nigrum. The damage caused is increased in the words of Campbell by “the insects’ habit of biting through the leaf near the petiole, resulting in the excision of a large part of the leaf blade. An insect may fall with the excised portion of the leaf, which it then abandons and climbs to another branchlet where it resumes feeding”.

Shepherd [19] showed that severe defoliation of Eucalyptus delegatensis by Didymuria violescens leads to significant mortality and decreased rate of increase in trunk diameter of this timber tree. Mazanec [20] showed that trunk diameter growth is decreased by moderate defoliation. Long-term effects of repeated defoliation (many phasmids have a 2-year cycle of high population density) were shown to cause high mortality and decrease in trunk diameter [21]. Subsequently, Mazanec [22] showed even a light defoliation caused significant reduction of diameter growth for two growing seasons. These findings led Readshaw and Mazanec [23] to show for timber crops that the history of outbreaks may be studied using tree rings.

Table 1 provides a list covering the species attacked by phasmids during outbreaks, as well as plants of economic importance known to be attacked by phasmids. Table 2 provides a geographic breakdown of phasmid infestations.
Table 1

Plants of economic importance attacked by Phasmids

Plant family

Plant species

Species

Locality

References

Anacardiaceae

Mangifera indica

Trachyaretaon echinatus

Philippines

[106]

  

Pharnacia magdiwang

Philippines

[106]

Araceae

Xanthosoma sagittifolia

Eubulides taylori

Philippines

[106]

Arecaceae

Cocos nucifera

Graffea crouanii

Fiji

[46, 95]

   

Tonga

[25]

   

Samoa (Upolu Island)

[93]

   

Micronesia: Pohnpei; American Samoa

[133]

   

Pacific Islands: Caroline; Marquesas; Vanuatu; New Caledonia

[134]

  

Acanthograeffea denticulata

Micronesia

[133]

  

Acanthograefeea modesta

Micronesia: Chuuk

[133]

  

Graeffea minor

Samoa

[130]

  

Graeffea lifuensis

Loyalty Islands

[102]

  

Ophicrania leveri

Solomon Islands

[26]

  

Hermarchus pythonius

Fiji

[95]

  

Graeffea seychellensis (check PSF)

Seychelles

[102]

  

Graeffea liuensis

Loyalty Islands

[102]

 

“Oil palm”

Eurycantha insularis

Papua New Guinea

Northern (Oro) Province

[114]

  

Eurycantha calcarata

Papua New Guinea

West New Britain

[112]

Burseraceae

Canarium ovatum

Pharnacia ponderosa

Philippines

[106]

Cannabaceae

Celtis sp.

Diapheromera femorata

USA: Wisconsin

[74]

Casuarinaceae

Casuarina equisetifolia

Phasmotaenia elongata

Philippines

[106]

Combretaceae

Terminalia microcarpa

Pharnacia ponderosa

Philippines

[106]

Cupressaceae

Cuprous funebris

Baculonistria alba

China: Sichuan

[117]

   

China: Yangtze River, Three Gorges Area Chongqing

Guowei [115]

Euphorbiaceae

Alueites fordii

Baculonistria alba

China: Sichuan

[117]

 

Sapium sebiferum

Baculonistria alba

China: Sichuan

[117]

Fabaceae

Robinia pseudoacacia

Diapheromera femorata

USA: Wisconsin

[74]

   

USA: New York

[66]

Fagaceae

Castanopsis fissa

Micadina yingdensis

China: Guangdong

[119]

 

Castanopsis cuspidata Castanopsis hicklii

Sinophasma maculicruralis and Sinophasma pseudomirabile

China: Guangxi Region: Bobai County

[4]

 

Cyclobalanopsis sp.

Baculonistria alba

China: Sichuan

[117]

 

Quercus liaotungensis

Ramulus chongzinense

China: Gansu Province: Chingxin and Huating Counties

[120]

 

Carpinus cordata

Ramulus chingzinense

China: Gansu Province: Chingxin and Huating Counties

[120]

 

Fagus sp.

Ramulus pingliense

China: Gansu Province: Wenxian County

[4]

Juglandaceae

Platycarya strobilacea

Baculonistria alba

China: Sichuan

[117]

 

Platycarya orientalis

Baculoinstria alba

China: Sichuan

[117]

Myrtaceae

Eucalyptus spp.

Various species are valuable timber trees (Rentz 1996)

Didymuria violescens

Australia: New South Wales, Victoria

[7, 27]

  

Podacanthus wilkinsoni

Australia

[7]

 

Psidium guajava

Trachyaretaon echinatus

Philippines

[106]

  

Rhamphosipyloidea philippa

Philippines

[106]

  

Pharnacia magdiwang

Philippines

[106]

  

Pharnacia ponderosa

Philippines

[106]

Pandanaceae

Pandanus tectorius

Graffea crouanii

Micronesia: Tonga

[25]

 

Pandanus sp.

Megacrania batesi (?)

Philippines: Capiz Province

[106]

  

Acanthograeffea denticulata

Micronesia: Marianas

[133]

Pinaceae

Pinus patula

Libethroidea inusitata

Colombia

[126]

Piperaceae

Piper nigrum

Sipyloidea stigmata

India: Western Ghats

[18]

Poaceae

Miscanthus floridulus

Graffea crouanii

Fiji

[97]

 

Zea mays

Baculonistria alba

China: Sichuan

[117]

Rosaceae

Prunus cerasus

Diapheromera femorata

USA: West Virginia

[44]

 

Prunus domestica

Ramulus pingliense

China: Gansu Province: Wenxian County

[4]

Rubiaceae

Gardenia jasminoides

Mnesilochus mindanaense

Philippines

[106]

Salicaceae

Salix heilophilia

Baculonistria alba

China: Sichuan

[117]

Sapotaceae

Palaquium sp. (?)

Lonchodes brevipes

Malay Peninsular

[135]

Solanaceae

Solanum tuberosum

Baculonistria alba

China: Sichuan

[117]

Question marks indicate potential ambiguities that are discussed in the text in the case of Phasmid species. In the case of plant species they are the likely scientific name based on vernacular names given in the reference

Table 2

Economically important plants attacked by phasmids (by geography)

Continent

Country

Locality

Host plant

Species

References

Asia

China

Guangdong Province

Castanopsis fissa

Micadina yingdensis

[119]

  

Jilin Province

Unknown

Ramulus minutidentatus

[123]

   

Tilia mandshurica

Ramulus minutidentatus

[136]

  

Shaanxi Province

Various

Ramulus pingliense

[9]

  

Gansu Province

Fagus sp.

Rosa domestica

Ramulus pingliense

[4]

  

Guangxi Autonomous Region

Castanopsis cuspidata

Castanopsis hicklii

Sinophasma maculicruralis,

Sinophasma pseudomirabile

[4]

  

Hubei Province

Orange orchards

(241 hectares, loss of over 2100 tons of fruit)

Unknown

[115]

 

India

Thenmala, Kerala, Western Ghats

Black Pepper

Piper nigrum

Sipyloidea stigmata

[18]

 

Malay Peninsular

 

“Gutta-percha”

Lonchodes brevipes

[135]

 

Philippines

 

Gabing San Fernando

Xanthosoma sagittifolia

Eubulides taylori

[106]

   

Mango

Mangifera indica

Trachyaretaon echinatus

Pharnacia magdiwang

[106]

   

Guava

Psidium guajava

Trachyaretaon echinatus

Rhamphosipyloidea philippa

Pharnacia magdiwang

[106]

   

Pandan

Pandanus sp.

Megacrania batesi (?)

[106]

   

Rosal

Gardenia jasminoides

Mnesilochus mindanaense

[106]

   

Pili

Canarium ovatum

Pharnacia ponderosa

[106]

   

Kalumpit

Terminalia microcarpa

Pharnacia ponderosa

[106]

   

Agoho

Casuarina equisetifolia

Phasmotaenia elongata

[106]

 

Solomon Islands

 

Coconut

Cocos nucifera

Ophicrania leveri

[26]

North America

USA

Wisconsin

Montmorency sour cherry

Prunus cerasus

Diapheromera femorata

[44]

  

West Virginia

Black Locust

Robinia pseudoacacia

Hackberry

Celtis sp.

Diapheromera femorata

[74]

  

New York

Black, red and chestnut-oaks

Diapheromera femorata

[65]

  

New York

Locust

Diapheromera femorata

[66]

  

Michigan

Oaks

Diapheromera femorata

[70]

  

Iowa

Hazel, oak

Diapheromera femorata

[24]

South America

Colombia

El Tambo

Pinis patula

Libethroidea inusitata

[126]

Oceania

Australia

South-East

Eucalyptus spp.

Didymuria violescens

[7]

   

Eucalyptus spp.

Podacanthus wilkinsoni

[7]

  

New South Wales

 

Anchiale austrotesselata

[48]

  

near Brisbane

 

Anchiale austrotessulata

[88]

 

Cook Islands

Atiu

Coconut

Cocos nucifera

Graeffea crouanii

[47]

 

Fiji

 

Coconut

Cocos nucifera

Graeffea crouanii

[46, 94, 95]

    

Hermarchus pythonius

[95]

   

Miscanthus floridulus

Graeffea crouanii

[97]

 

Micronesia

Tonga

Pandanus tectorius

Graffea crouanii

[25]

 

Papua New Guinea

Northern (Oro) Province, Higaturu

Northern (Oro) Province, Saiho Division (Tunana)

“Oil palm”

Eurycantha insularis

[114]

  

West New Britain, Malilimi Plantation (New Britain Palm Oil)

“Oil palm”

Eurycantha calcarata

[112]

 

Samoa

 

Cocos nucifera

Graeffea minor

[130]

 

Samoa

 

Cocos nucifera

Graeffea crouanii

[93]

Check all host plant reports are in here and vice versa

Question mark indicates potential ambiguities that are discussed in the text in the case of Phasmid species. In the case of plant species they are the likely scientific name based on vernacular names given in the reference

Infestation vs outbreak

The terminology of pest levels of phasmid varies between authors. In this work, outbreaks are considered to be a sudden increase in phasmid population, as exemplified by Diapheromera femorata in the USA and Didymuria violescens in Australia. Species which maintain fairly constant population densities that have economically important effects on crops or timber are considered to be an infestation.

Control of pest phasmids

Abiotic factors affecting phasmids in the wild

For species not capable of flight, the slow movement of the adults limits the spread of an infestation. The maximum rate of spread of Diapheromera femorata during infestation was 1/8th of a mile per year [5]. This minimal spread plus natural barriers contains the infestations, and also makes treatment much easier than it would otherwise be. Indeed, Butler [24] commented that the “extremely local character of the infestation was a curious feature”. Although in this case the insects did begin to cross a road so that “every passing carriage or motor crushed them by hundreds”.

O’Connor [25] suggests similar localisation in infestations of Graeffea crouanii on coconut in Tonga, “Normally, heavy attack by the stick insect begins in a small, localized area”. This observation was confirmed by Paine [26]: “Outbreaks seem to occur on certain islands, in certain situations, and not always very frequently, so that while over the whole range of this insect the loss of copra [the dried kernel of the coconut used to extract oil] resulting from its ravages is inconsiderable, losses to individual planters and village communities can be serious”. This slow spread is also reported for Didymuria violescens outbreaks in Australia [27].

Butler [24] recorded the males of Diapheromera femorata spreading faster than females in the United States, and opined this was due to “greater sluggishness”. This can be attributed to the greater bulk of a gravid female (both sexes of this species are apterous). The proportion of females at a distance from the focus of an infestation increased throughout the year.

Craighead [28] reports that environmental conditions may also reduce the level of infestation by Diapheromera femorata, “Under dry conditions many of the young fail to extricate themselves completely from the egg capsule and die”. The source of this is likely to be the work of Severin and Severin [29]. This is likely to be true of many temperate species that have a springtime emergence.

Predators

Bragg [30] showed that ladybirds (Coleoptera: Coccinellidae) ate young phasmids in culture conditions although there appear to be no reports of this from the wild.

Several records have been made of phasmids being predated by spiders. Robinson and Robinson [31] report a species of Eurycnema being predated by Nephila maculata. Robinson and Lubin [32] found several phasmid nymphs in the web of a species of Fecenia. Bragg [33] gives an account of the phasmid Asceles margaritatus being predated by a spider in Kinabalu National Park, Sabah. Laboratory tests confirm that phasmids are palatable to spiders [34]. The jumping spider Ascyltus pterygotes (Salticidae) was reported attacking the stick insect Graeffea crounaii by Rapp [35].

Other pests of phasmids include lizards [36]. In the old Primates gallery at the Natural History Museum, London (UK) there was a photo of a slow loris (Nycticebus coucang) feeding on a species of Eurycnema (date and location of photograph unknown).

Human usage of phasmids

Bragg [37] gives an account of the eggs of phasmids (Haaniella) being eaten by the Bideyuh tribe in Sarawak. Bragg [38] also reports the Iban tribe in Sarawak eat Haaniella echinata, not just the eggs. Stone [39] reports Extatosoma tiaratum is eaten by natives of Papua New Guinea (although as E. tiaratum is not found in this region the author probably refers to Eurycantha or Extatosoma popa). The insects eat the leaves of the sago palm, which are used as a thatching material. When the leaves are collected, any phasmids found are skewered on pointed sticks pushed from the abdomen up through the head. The insects are then spit roasted on an open fire until the legs fall off.

The hind legs of Eurycantha latro Redtenbacher, 1908 have been used as fishing hooks on Goodenough Island [40].

Non-biological control

O’Connor [25] recommends the banding of coconut palms as a defence against Graeffea crouanii, and smoking down the adult insects from the canopy. As bands were not commercial available at the time on Tonga, instructions are given for making them, “two to three parts by weight of resin are mixed with one by weight of linseed, coconut or castor oil, the oil being heated and the resin added gradually until it is all dissolved. To this may be added one ounce of technical DDT per pound of banding material”. The banding material so made is allowed to cool and painted by hand around the trunks of the palms.

The use of systemic insecticide (Monocrotophos) injected into the trunks of coconut palms has been demonstrated to be an effective method for controlling Graeffea crouanii [41, 42]. Aerial application of Malathion was considered effective in controlling an outbreak of Didymuria violescens [43].

The migration of insects from neighbouring habitats onto crops [44] means that a repeated theme in successful control of phasmid outbreaks for wingless species is the creation of barriers between host plants. Wilson [45] reports on Diapheromera femorata outbreaks in the United States: “Because the walkingstick does not fly, infestations are often localized and expand only a few hundred yards during the season. A stream or road separating parts of a stand often retards the spread of the insect. One side of such barriers can have completely denuded trees while the other might have little or no injury”. Similar advice, clearing the areas between coconut trees, is given to farmers controlling Graffea crouanii on Fiji [46] and Atui [47].

Hadlington and Hoschke [48] and Campbell [7] show that bush fires dramatically curbed the extent of a phasmid outbreak in Australia. It has been suggested [49] that phasmid eggs may survive forest fires, although in reduced numbers, so there is still potential for infestations to recur. Burning of forest may also cause a short-term spike in the phasmid density [48].

‘Smoking’ is the technique of burning palm fronds underneath infested palms to disturb the insects and cause them to fall to the ground. Reports from collectors suggest a similar effect from cigarette smoke [50] and Australian wildfires [51].

Potential for biological control

The Hymenopteran subfamilies Loboscelidiinae and Amiseginae (Chrysididae) are obligate egg parasitoids of phasmids [52]. Several hundred species are known from the American, African and Oriental regions. Later works [53] show that mimicking seeds may cause the eggs to be attractive to ants, encouraging them to take them to their nests which offer some protection from egg parasitoids. Very few associations are known between parasitoid and host [54], and it is not known how host-specific individual parasitoid species are. Severin [55] discusses the resemblance of the eggs of Diapheromera femorata to seeds, but does not conclude that this resemblance protects them from parasitoids.

Phasmophaga antennalis (Diptera: Tachinidae) appears to be a phasmid specialist feeding on several species across the United States [56, 57]. It feeds on adults, and parasitisation may be indicated by a scar on the phasmids abdomen. Perilampus hyalinus (Hymenoptera: Perilampidae) is a hyperparasitoid of phasmids via P. antennalis [57].

The adaptation of several species of phasmid to develop capitula [58] on their eggs which are attractive to ants could be an evolutionary response to the predation and parasitisation of their eggs. O’Connor [25] lists the ant Tapinoma melanocephalum as devouring the eggs of Graeffea crouanii, but it is possible the ants took the eggs to their nest. Compton and Ware [59] show that the capitula of phasmid eggs can perform the same function as the elaiosome of seeds—encouraging them to be taken, dispersed and protected by ants.

Studies by Campbell [7] looking for eggs parasitised by Cleptid wasps found that for the plaguing species Didymuria violescens and Podacanthus wilkinsoni, the level of parasitism depended on the dominant vegetation with Eucalyptus delegatensis resulting in lower levels of parasitism than Eucalyptus dalrympleana—although neither showed signs of being promising in controlling outbreaks.

The lethal parasitisation of several Bornean phasmids by mermithid larvae was demonstrated by Bragg [60]. Although the species of mermithid was not identified, it is believed the same species attacked various species of collected. Yeates and Buckley [61] also describe records of mermithid nematodes attacking phasmids.

Table 3 provides an overview of potential biological control agents.
Table 3

Potential biological control agents

Higher class.

Species

Phasmid

Notes

References

Insecta

Diptera

Tachinidae

Biomya genalis

Diapheromera femorata

Nymphs

 

[45]

 

Phasmophaga anetannalis

Diapheromera femorata

Nymphs

Phasmid consumes egg laid on foliage

[45]

 

Mycteromyiella laetifica

Graeffea leveri

nymphs/adults

Also a species of Megacrania is parasitised

[26, 137]

 

Mycteromyiella phasmatophaga

Graeffea leveri

Nymphs/adults

Probably not usual host

[26, 137]

 

Thrixion halidayanum

Leptynia hispanica

 

[138, 139]

 

Euhallidaya sverinii

Diapheromera femora

Eggs

 

[140]

Insecta

Hymenoptera

Chrysididae

Mesitiopterus kahlii

Diapheromera femorata

Eggs

Never recovered in sufficient number to be considered an important means of control

[45]

 

Cladobethylus insularis

Eurycantha insularis

Eggs

 

[114]

 

Exova tunana

Eurycantha insularis

Eggs

 

[114]

Cleptidae

Myrmecomimesis spp.

Didymuria violescens

Egg

Podacanthus wilkinsoni

Egg

 

[7]

 

Myrmecomimesis sp.

Anchiale austotesselata

 

[48]

  

Ctenomorphodes tessulatus

egg

305 emerged from a field collected sample of 11,694

[88]

 

Myrmecomimesis nigripedicel

Ctenomorphodes tessulatus

Egg

At much lower density than M. striata

[88]

 

Myrmecomimesis rubrifemur

Graeffea crouanii

In Australia attacks Anchiale austrotesselata. Unsuccessfully introduced to Fiji.

[99]

 

Loboscelidia sp.

Anchiale austrotesselata

 

[48]

 

Loboscelidia sp.

Ctenomorphodes tessulatus

Only 6 from sample of 11,694 eggs

[88]

Eupelmidae

Paranastatus nigricutellatus Eady, 1956

Paranastatus verticalis Eady, 1956

Graffea crouanii

eggs

Controls up to 50 % of eggs. Seems effective on Fiji but not western Samoa [100]

[46, 101, 141]

 

Anastatus (Anastatus) eurycanthae Gibson, 2012

Eurycantha calcarata

eggs

 

[112]

 

Anastatus gratidiae Risbec, 1951

Gratidia sp.

 

[142]

Formicidae

Tapinoma melanocephalum

Graeffea crouanii

Eggs

 

[25, 143]

 

Pheidole megacephala

Graeffea crouanii

Eggs

 

[143]

Mecoptera

Bittacidae

Harpobittacus sp.

Anchiale austrotesselata

 

[48]

Aves

Gymnorhina tibicen

Graeffea crouanii

 

Paine [26] from Hinckley (unpublished)

 

Acridotheres tristis

Graeffea crouanii

 

[47]

Mammalia

Rattus exulans

Graeffea crouanii

All instars and eggs

 

[144]

 

Rattus rattus

Graeffea crouanii

all instars and eggs

 

[143]

Fungus

Deuteromycetes

Hyohomycetaceae

Beauveria bassiana

Unknown

Used in China to control infesting phasmids

[115]

This table shows host-specific parasites and specific examples of wild predators. Laboratory studies of generalist predators (e.g. [145]) and non-economically important generalist insectivores (e.g. Hamilton and Pollack 1961) are not included

Monitoring

Campbell [7] gives two methods for monitoring phasmids in outbreak proportions. The first is to count eggs in a sample area of soil under the canopy and scale up to an acre taking account of the proportion of canopy cover (adult insects of the species studied are canopy dwellers). The second method (to estimate numbers of nymphs and adults) was to catch the frass using suspended traps and dry it to constant mass before calculating the frass fall per hour. Both methods were deemed satisfactory for estimating populations.

A solved problem?

While phasmid outbreaks can be efficiently controlled using injected or aerially applied insecticides, a deeper understanding of the causes of phasmid outbreaks (Table 4) will allow for more targeted control and mitigation, perhaps without resorting to the use of insecticides. The problem faced is similar to that faced in controlling the pest Orthoptera [62].
Table 4

Comparison of phasmid species known to outbreak

Species

Host plants

Eggs laid

Body length

Life cycle

Diapheromera femorata

Young nymphs on low growing plants: beaked hazel, rose, juneberry, sweetfern, blueberry, strawberry. older nymphs/adults: black oaks, basswood, wild cherry and less preferred: quaking aspen, paper birch, hickory, locust, apple, chestnut [45].

150

3 per day [45]

2.5″–3.5″ [45]

Eggs hatch May/June, Adulthood late July/August, mating a week later, egg lying until October. In north of range eggs double diapause and there are two broods, further south eggs hatch year following oviposition [45]

Didymuria violescens

Various species of Eucalyptus (see species report)

200

1–5 per day [27]

357 (mated) 401 (virgin)

([146] laboratory)

Approx 3″ [27]

Egg hatches in spring (October–December) after 6–18 month diapause. Five nymphal stages from 1 to 3 weeks each [27]

Podacanthus wilkinsoni

Various species of Eucalyptus

 

120 mm [85]

Eggs remain dormant until spring, or spring the following year. Insects mature the same year they emerge from the egg

Accounts of phasmids attacking economically important plants

Species where the only literature record is a foodplant association are not discussed further, details are given in the preceding tables. A partial list of synonyms is given—synonyms not used in publications in the References are ignored. Taxonomic names have been checked and updated using the Phasmida SpeciesFile [63].

Species accounts

Diapheromera femorata (Say, 1824)

= Spectrum femoratum Say, 1824 [64]

This species is widespread in the United States east of the Rocky Mountains [28], but rarely in levels likely to cause concern.

Riley [1] reports an unusual number of this species feeding on rose bushes and other shrubs while he was lecturing at Cornell University (Ithaca, NY, USA). Riley’s report goes on to describe the earliest documented infestations of this species, also in New York State, starting in 1874. Reproductions from two letters ([65, 66]) to the American Agriculturalist are given in [67].

Ferrisborough (1874) reports a case of the insects attacking locust (Robinia pseudoacacia) used to “furnish the farm with posts and stakes” in New York State [68]. The insects entirely stripped the trees of their leaves every second year. Over a period of 15 years, the increasing infestation resulted in nearly all of the locust being killed, and the insects spreading to nearby native trees.

Snow’s account [69] from Yates County, New York is perhaps the earliest one with which we have the most complete history of infestation. The site of the infestation was Esperance Farm [1]. The insects attacked second-growth plantations of white oak and hickory, as well as his peach orchard. The first signs of infestation were described in his report: “I noticed about August 15th, in the reservation of young timber, mostly white oak and hickory, a few trees having the appearance of being burned just enough to kill the leaves. On closer investigation I found many of these insects devouring the leaves”.

The American Agriculturist [65] continues the reporting of the infestation on Snow’s land. The reported case in 1874 develops until the phasmids “appeared in such numbers as to denude of their foliage … some 25 acres”. After a year of relatively little damage in 1876, the infestation returned: “the trees on some 30 acres were stripped of their leaves. So thorough was the work of these insects, that from a distance the woods appeared as if a fire had gone through them”. The destruction caused by the insects continued until they were stopped by frost, and resulted in many dead branches. The numbers during an infestation “are almost beyond comprehension: they cluster upon a limb or fence-rail so thickly that they pile up upon one another, and one cannot enter the wood where they are, without having numbers on his clothing”.

A response to the American Agriculturalist request [66] reports a similar story from Conklin from Cumberland County, Pennsylvania. The insects had been seen on his land for 40 years, but 10 years previously (circa 1877) had reached infestation densities. “In this instance … these insects denuded a row of locust trees that formed the shelter on the northwest side of a peach orchard. For half a dozen rods from this locust row the peach trees were also stripped of their leaves”.

Riley, as the Entomologist of the US Commission for Agriculture, continued his investigation [1] reporting that “the underbrush was also very effectually cleaned of its foliage”. Riley continued to investigate the pest phasmid, calculating that captive females were capable of laying “upwards of a hundred” eggs.

Butler [24] records an infestation in predominantly oak woodland in the area around Peterson, Iowa (USA). They spread from the forest to an orchard where “they infested particularly one tree of early apples, devouring nearly all the leaves; on a single twig six inches in length I counted sixteen clustered together and they were equally numerous over the entire tree”. Butler goes on to describe the effect of the infestation on his family, “The woods had become forbidden ground to us; if one was sufficiently brave to start through them, the walking-sticks fell to the ground from every tree in such numbers to sound like hail”.

The largest reported outbreak of D. femorata is from Ogemaw County, Michigan (USA), where several smaller infestations merged in the autumn of 1936 to cover approximately 2500 acres [70]. All of the infestations were in second-growth stands of oak. The insects were first discovered in the area in 1921 and first caused major defoliation in 1928. During 1931, no adults were found but the density of eggs in leaf litter was measured at 36.5 per square foot. In 1932, the largest Michigan report was 1600 acres south of Grayling. The same infestation was mapped in 1936 and covered upwards of 1900 acres. Graham reports that “without exception these outbreaks are located in the same type of forest… these hills were formerly covered, for the most part, with a forest of white and Norway pine mixed with apsen, oak, cherry, and, in places, paper birch”. The prevailing forestry management of the time, following logging and repeated burning, allowed mature oaks to dominate and caused the phasmid infestation. The rate of defoliation observed by Graham shows that “trees may be completely stripped by the middle of July, but usually this stage occurs much later”. Graham also notes that the large infestations seem to be created by the merging of smaller ones, commenting that “the original foci are sometimes easily located by an examination of the condition of the trees, especially when years of infestation have been followed by the death of the favourite host trees”.

Many subsequent authors state that this species is capable of causing infestations within the continental United States and giving the areas more likely to have infestations as the “Lake States” [71] or south of a line drawn between southern Nebraska and Delaware [45, 72] but few detailed reports can be traced in the literature. Wilson [45] while not giving details of individual infestations does detail the effect on trees infested with this species “The entire leaf blade, except the basal parts of the stout veins, is consumed. During heavy outbreaks large stands are often completely denuded. Trees may be defoliated two times in the same season in some outbreaks. Three or four heavy infestations are usually sufficient to cause some branch mortality”. Helfer [73] describes walking through an infested area; “Eggs and faecal pellets are dropped to the ground in great numbers, producing a pattering sound, like rain, accompanied by a peculiar seething sound of thousands of jaws chewing the leaves”. Over 100 eggs per square foot of ground have been recorded in severe infestations [45].

Oatman [44] describes a 1959 request from a Door County, Wisconsin cherry grower asking for advice on chemical control of this species. Interestingly, their main concern was not damage to the crop but the unwillingness of contracted Jamaican labour to work in infested areas due to superstitions relating to the insects. The infestation increased through 1960 until in 1961, “within seconds after a person stopped under or near a tree, walkingsticks dropped onto and crawled upon his body so that even to an experienced entomologist it was an uncomfortable, creepy feeling”.

An ‘Event Notification Report’ from the Smithsonian Institution’s Centre for Short-Lived Phenomena (25 September 1973; [74]) details: “Millions of walking sticks, Diapheromera femorata, have infested an area in the Knobley Mountains about 3–4 miles from Keyser, West Virginia. When the infestation was first observed on 7 September, five acres (0.04 km2) of black locust and hackberry trees had been affected. At present 10 acres of these trees have been completely defoliated and the trees and ground are covered with these insects”.

Natural control might include the wasp Mesitiopterus kahliix which has been recovered from eggs of this species [45]. Wilson also reports two parasitic flies that attack the nymphs, Biomya genalis and Phasmophaga antennalis the later being interesting as the phasmid is parasitised by eating eggs the fly has laid on the foliage. Wilson again reports that birds including crows and robins concentrated in heavily infested areas and feed on the insects. Riley [1] reports that turkeys and chickens feed upon nymphs while they remain close to the ground, and that various species of Heteroptera feed on nymphs and adults (Arma spinosa, Poisus cynicus and Acholla multispinosa). Graham [70] reports robins and crows feeding on the insects with “large flocks of these birds … observed day after day on each of the major infestations. Although the birds were numerous, the insects were so much more so that the effect on the walking-stick population seemed insignificant”.

The first recommended chemical treatment was Paris Green Water [copper(II) acetate triarsenite in aqueous solution] [1], for treatment of young nymphs near ground level. Riley’s preferred method was destruction of eggs, either by digging and turning them into the ground, or by burning over the dead leaves during winter. Graham [70] views replanting of native trees as the preferred method of control, and advises against burning: “It should be remembered … that forest fires have been responsible for setting the stage for walking-stick outbreaks by killing out all tree growth except that of the oaks”. The use of calcium arsenate, either by spraying or dusting is also recommended “where the presence of the insects becomes objectionable”. Wilson [45] recommended the use of DDT application in the later half of July for control, or a barrier strip 100ft wide sprayed with lead arsenate at 4 pounds per 100 gallons of water per acre to prevent infestation from neighbouring areas. A revised edition of the publication [72] states “As this publication goes to press, there are no chemical insecticides registered for use in control of the walkingstick”.

Rivers et al. [75] showed that the venom of Nasonia vitripennis (Hymenoptera: Pteromalidae) was tolerated by adults of Diapheromera femorata.

Didymuria violescens (Leach, 1814)

= Phasma violescens Leach, 1814

This Australian species feeds on various species of Eucalyptus, preferring E. robertsoni, Eucalyptus radiata, E. dives, E. dalrympleana, E. maculosa, E. viminalis and E. bicostata. Other eucalypts are less favoured but also used as hosts, including the economically valuable alliances where E. delegatensis (alpine ash) or E. regnans (mountain ash) dominate [27]. The species can be uni-voltine or semi-voltine depending on environmental conditions, achieved through one of two stages of diapause in the egg stage [76, 77].

Outbreaks have been recorded in State Forests around Nundle (Nundle, Hanging Rock, Tomalla, Nowendoc and Tuggolo State Forests), Jenolan (Jenolan and Konangaroo State Forests) and the southern highlands of New South Wales (Bago State Forest) and Victoria (Mt Bogong, Mt Stabley, Mt Pinnibar).

The outbreak in the Nundle area started in the summer of 1949–50. The outbreak continued 2 years later and in the summer of 1951–1952 extensive defoliation occurred, followed by a sudden, but temporary, reduction in phasmid numbers over extensive areas. In the Tuggolo State Forest, extensive defoliation occurred in the 1955–1956 season and most of the remaining forested area (except for areas burnt late in 1957) in the 1957–1958 season. In the Jenolan area, large numbers of trees were killed over thousand of acres [7]. A widespread fire in the summer of 1957 in this area also destroyed large numbers of phasmids.

In the Nundle and Jenolan areas, two species of phasmid, D. violescens and P. wilkinsoni, occur in plague numbers, though the latter is probably responsible for the greater part of the defoliation. In the southern highlands area, violescens alone is involved. Adults of P.  wilkinsoni are most abundant during the even numbered years and those of D. violescens during the odd numbered years.

Population densities of D. violescens were noticed to be higher than usual in the areas infested by Podacanthus wilkinsoni from 1947 to 1948 onwards. The dating of the first major outbreak was confirmed using tree ring data [23] to occur in 1951 rather than in 1953 as stated by previous authors. This outbreak occurred outside of the range of Podacanthus wilkinsoni. Infestations continued every year until 1962–1963 [27]. No defoliation was reported by 1967 [23].

Newman and Endacott [43] report on the treatment of an infestation in the catchment area of the Kiewa Hydro-electric scheme, Victoria. Defoliation by phasmids was first noted in this area in 1956–1957 with subsequent infestation levels in 1958–59. Treatment was required as death of the forest in the catchment area could reduce the stability of soil on mountain slopes which are stabilised by tree roots, increase the risk of forest fire and ‘draw adverse comment from a community which is making increasing use of the area for recreation’. Control was with Malathion with 4.5 oz of active ingredient in 3 gallons of light diesel fuel per acre. Delivery was by helicopter. Spraying was at a time after the majority of the insects had hatched and before oviposition to reduce negative effects on the Hymenopteran egg parasites of the phasmids. The frass-fall method used by Campbell [7] was used to determine the effectiveness of treatment, which was determined to be highly successful.

The pattern of infestation [27] does not involve long-range dispersal. In the initial stages, the insects increase in density, sporadically getting to densities that cause severe defoliation in small groups of trees, generally at elevations of 2000–4000 ft on ridge tops and Western facing slopes. Two years later the next generation, the areas of severe infestation expand to several square miles, and occasionally joining. In following generations, areas around the original epicentres may be completely defoliated. During the decline of an outbreak, severe defoliation becomes diffuse, then patchy until only small pockets of high phasmid density are left, which generally fail to persist. The decline of outbreaks is demonstrated by Readshaw to be due to an increased predation and parasitisation of the egg stage as outbreaks progress. The lack of Chrysid (Hymenoptera) parasites in the alpine conditions where outbreaks occur is postulated to be a reason why these populations of D. violescens are prone to outbreak.

In 1963, Didymuria violescens defoliated 650 square miles of Eucalyptus forest, an event deemed serious not only for direct negative effects of tree growth and survival but also the potential threat this might cause to the stability and efficiency of important water catchments [27, 43].

Although present in mountain and coastal forest throughout New South Wales and Victoria, large outbreaks are confined to “the inland slopes of the Great Dividing Range, between Canberra, A.C.T., and west Gippsland, Victoria. Typically, outbreaks occur at elevations between 2000 and 4000 ft in forests with tall trees, an almost continuous canopy, and a shrubby understory containing a sprinkling of sapling eucalypts. The forest floor usually comprises a loosely packed layer of undecomposed litter and varying amounts of grass and herbaceous vegetation” [20]. In the areas where this species reaches plague proportions, this species has a two-yearly life cycle apart from populations in the Mt Warning area [7]. In some stands, 80 % of trees were killed after two severe defoliations in alternate years [21].

A further outbreak [78] at the Corin Dam (nera Canberra) was initially suspected to be fire damage but was revealed to be an outbreak of this species in 1988. It was likely to have started in the wet and cool summer of 1983–1984. Very small nymphs travelling on air currents are considered as a means of an outbreak spreading.

Males of this species fly sporadically from elevated positions and can travel a significant distance over their lifetime. Females do not fly but can glide short distances. This can lead to differential dispersal between males and females [7]. The spread of this species is thus slow, and might be the cause of outbreaks occurring predominantly in areas where the tree canopy is largely continuous.

Some natural control may be achieved by Indomyrmex ants and the birds Colluricincla harmonica and Cinclosoma punctatum [27]. The bird Strepera graculina is considered to be an important predator of this species [79].

Podacanthus wilkinsoni Macleay, 1882 [80]

= Didymuria violescens nymph sensu Froggatt (1923)*

*Froggatt confuses Didymuria violescens as the nymphs of Podacanthus wilkinsoni. See [7].

The first report of this species causing infestation is from Mr C. S. Wilkinson (in [80]) and is the first report of pest phasmids in Australia (nr Binda Caves, Westmoreland). Macleay speculates that phasmids may be the cause for other large areas of eucalypt deaths in the vicinity of Australian colonies. Further reports of mass defoliation from Murphy’s Creek, nr Walcha, New South Wales were made by Oliff [81] and Froggatt [82] states that continued every alternate year. The common name of ‘Ringbarker’ comes from the similar effect on trees as ringbarking (removing a complete ring of bark around the tree to cause death—a technique used by foresters to thin woodland).

The species can be uni-voltine or semi-voltine depending on environmental conditions, achieved through one of two stages of diapause in the egg stage [76]. In the areas where this species reaches plague proportions, this species has a two-yearly lifecycle [7].

A note in the Proceedings of the Linnean Society of New South Wales [83] reports Mr Froggatt “showed a series of specimens of the gregarious phasmids Podacanthus wilkinsoni Macleay, showing remarkable colouration varying from deep green to bright red. There were hundreds of thousands of these stick insects crawling over the scrub about 20 miles east of Glen Innes, where these were taken in the middle of March”. Whether the insects were correctly identified in this instance is unknown.

Outbreaks that began in the cool summer of 1947–1948 in New South Wales (Nundle and Jenolan) continued every second summer until 1959–1960 when the outbreak suddenly declined. Hadlington (in [84]) reports that these forests were being converted to Pinus radiata which is not susceptible to attack.

Campbell [7] reports a 1957 study of soil egg density of areas completely defoliated by this species estimating densities of over 1,200,000 eggs per acre. Studying the viability of these eggs suggested a maximum population of over 350,000 phasmid per acre (50,000 per acre is considered enough for serious defoliation). Severe fires in late 1957 were shown to have a dramatic effect in reducing the phasmid outbreak.

Elliott et al. [85] “has causes periodic, ever defoliation in the highland forests of south–eastern Australia. It os distributed from Northern New South Wales down to areas south west of Sydney. Several species of eucalypts are acceptable hosts and E. radiata, E. robertsonii, E. dives, E. viminalis, E. huberiana, E. dalrympleana, E. stellulata and E. Pauciflora are favoured species”.

Anchiale austrotessalata (Brock and Hasenpusch, 2007) [86]

= Ctenomorphodes tessulatus Gray, 1835 [87]

Unlike Didymuria violescens and Podacanthus wilkinsoni which have been known to reach plague densities since at least 1880, the first record of this Australian species causing infestation is in 1956 [48]. High-density populations were reported from Toonumbar, Wedding Bells, Tanban, Ingalba and Colombatti State Forests.

While many species of trees were eaten (Syncarpia, Acacia, Casuarina), there is preference for Eucalyptus species. E. maculata that had been completely defoliated were found adjacent to E. microcorys with intact crowns. The areas of forest with pest levels of phasmids consisted of E. punctata, E. triantha, E. paniculata, E. maculata, E. gummifera, Syncarpia laurifolia. These regions consistently had an understory of Casuarina torulosa and E. microcorys [48].

The species can be uni-voltine or semi-voltine depending on environmental conditions, achieved through one of two stages of diapause in the egg stage [76]. Laboratory studies showed females could lay up to 900 eggs over a period of 5 months [48].

Heather (1965) studied the egg parasites of this species from Slacks Creek State Forest Reserve (near Brisbane) where this species had been ‘varying to plague proportions’ in recent years [88]. The mortality of first instar nymphs was found to increase in dry conditions [48].

Further outbreaks in coastal Queensland between 1974 and 1976 caused extensive tree damage and some tree fatality [89, 90].

Graeffea crouanii (Le Guillou, 1841)

= Bacillus crouanii Le Guillou, 1841 [91]

= Graeffea coccophaga (Newport, 1844) [92]

= Graeffia coccophaga incorrect subsequent spelling of genus by Hopkins [93]

= Graeffia coccophagus incorrect subsequent spelling by Simmonds [94]

Unlike the early reports of Diapheromera femorata that are in their own way poetic, the earliest reports of Graeffea crouanii are short and terse, perhaps due to them being reported by visiting and stationed entomologists rather than the landowners directly. Veitch and Greenwood [95] list the species “as being of some considerable importance” on the cocoanut[sic], Cocos nucifera on Fiji. The eggs of this species have been shown to survive floating in seawater [96] so could potentially disperse among islands naturally.

Hopkins [93] spent 2 years on Samoa working on filariasis for the London School of Hygiene and Tropical Medicine with P.A. Buxton, studying agricultural pests that came their way, admitting their “observations make no claim to completeness, they are perhaps worthy of publication in view of the scarcity of records from this group of islands”. G. crouanii was found to be “a serious pest of coconuts in some districts, entirely stripping the leaves and leaving only the mid-ribs. They are almost entirely nocturnal in their habits and may easily be collected on the smaller trees by searching for them with a lantern at night”.

Simmonds [94] reports from Fiji: “One of the periodic occurrences of damage by stick insects (Graffea coccophagus) was reported in May, this time from the Macuata coast”.

O’Connor [25] reports an outbreak of this species on Tonga and reports additional foodplants of Pandanus tectorius (used as food, thatch and in the manufacture of mats and baskets) and Miscanthus japonicus (=Miscanthus floridulus, incorrectly reported as a rush—correctly reported as grass in Lever [97]—edible). The outbreak was on Fofoa island, Vavau, with the infestation covering 50 of 180 acres. Hundreds of coconut palms had been killed by the feeding activity of the phasmid and “many more were stripped, except for a few stunted and distorted central fronds, and the remainder retained about half or a third of their normal foliage”. O’Connor visited in April–May 1949 at the end of the outbreak.

Paine [26] gives details of an outbreak on the island of Taveuni (Fiji group) which “began to reach serious dimensions in 1958, and by April 1959 100 acres of coconuts were affected. By the end of 1961 the outbreak had extended over 500 acres in which the older fronds were at least 50 per cent defoliated and nearly 400 palms had been killed”.

This species was introduced to the island of Atiu (Cook Islands) by the ancient Polynesians. Reports from the 1800s from missionaries and visitors noted it could be extremely common and was capable of destroying groups of Coconut Palms [47]. The Common Myna bird (Acridotheres tristis), also introduced to the island, is an effective predator of the insect introduced to the island to control the phasmid [98]. Populations of the insect increased in response to plans enacted to first control (May 2009) then eradicate (November 2010) the Myna population. Paine (1968) lists predation from “turkeys, domestic fowl and Australian Magpie (Gymnorhina tibicen) will attack Graffea on the ground (Hinckley, unpublished) and the Mantid Tenodera aridifolia (Stoll) on coconut leaves (Singh, unpublished)”. Singh’s unpublished report to the Director of the Department of Agriculture, Fiji also states that an introduced toad, Bufo marinus, is not considered an effective predator.

O’Connor [25] found that the eggs of caged stick insects were devoured overnight by the “minute and rapidly moving” ant Tapinoma melanocephalum, although it is possible the eggs were just carried to their nest and not consumed. The Fijian Ministry of Primary Industries recommends a number of biological and mechanical methods of controlling G. crouanii in Fiji [46]. Recommended biological controls are the egg parasite wasps Paranastatus nigriscutellatus Eady, 1956 and P. verticalis Eady, 1956. Paine (1968) gives the level of parasitism by these species from unpublished reports from Hinckley (10 %) and Pillai (52 %).

Paine [26] also reports of an unsuccessful attempt to control this species by establishing populations of the tachinids Mycteromyiella letifica and M. phasmatophaga. One of the tachinid flies (Diptera) thought to control Graeffea leveri, Mycteromyiella laetifica on the Solomon Islands were imported to Fiji to try and control this species. 960 puparia were shipped, with half used for experiments and the remainder released on Taveuni. The fly could be reared in lab conditions but not maintained in culture [99]. No evidence was found for persistence in the wild of those released. Waterhouse and Norris [100] suggest a reason for the limited control exerted by these predators is that the maggots can feed inside and emerge from larger hosts without damaging vital organs. Similarly, the hymenopteran Myrmecomimesis rubrifemur from eggs of Anchiale austrotessulata could not be bred on this species.

Biological control is more effective when combined with using cattle, goats or sheep to clear weeds around the base of infected trees to expose eggs to sun and other predators (including poultry). Crooker [101] and Lever [102] report high levels of infestation in farms with dense ground cover in Tonga, while Singh (1981) reports plantations almost free from infestation with little ground cover. The effect of desiccation on reducing the survival of eggs was discussed by Rapp [35]. Inter-cropping with non-host plants such as Theobroma cacao or Colocasia esculenta may help reduce damage to coconuts by up to 90 %.

O’Connor [25] gives a recipe for making sticky bands using “two or three parts by weight of resin are mixed with one part by weight of linseed, coconut or castor oil, the oil being heated and the resin added gradually until it is all dissolved”. The recommendation of adding DDT to the banding mixture is no longer applicable. The banding mixture is applied around the trunk of the palm to trap nymphs climbing the trunk. Debris from the floor of the plantation piled near the palms and set on fire removes insects from the coconut crown, and these too are caught on the band as they climb the tree.

Deesh, Swamy and Khan [103] summarise the problems of chemical control of this species. The problems relate to the high crown of the adult trees (circa 25 m above the ground) which makes physical application of insecticide difficult, and mist sprays can only reach heights of around 12 m. Aerial application is effective [104] but expensive [96]. Chemical control is effective when the crowns are reachable [105]. Injection of systematic insecticides is possible and routinely used [41] although fungal infection via the bored holes in the trunk can kill the tree [42].

Graeffea leveri (Günther, 1937)

= Ophicrania leveri Günther, 1937

This species feeds on coconut palms. In the Solomon Islands (except Savo), flies of the Tachinid genus Mycteromyiella prey on nymphs of this species and it may be due to the lack of Mycteromyiella on Savo that this island is the only one to get major infestations of this phasmid [102].

Mycteromyiella laetifica attacks Graeffea leveri and a species of Megacrania at all nymphal stages and as adults. Generally, only one egg is oviposited on each phasmid, but more (up to 7) is not uncommon. The eggs are laid externally, and those laid on more heavily chitinised sections of the host have significantly increased mortality. Most hosts died within 5 days of parasite emergence—although some went on to successfully reproduce [26].

Parasitised hosts were shipped to Fiji in 1963–1964 in an effort to establish this species as a parasite of Graeffea crouanii. Mycteromyiella phasmatophaga also attacks Graeffea leveri although its usual host is likely to be Sipyloidea poeciloptera. Again usually only one egg is oviposited on each phasmid, although one specimen had 9 parasite eggs.

Megacrania batesii Kirby, 1896

This species is thought [106] to be the culprit of an “unusually high population of an undetermined stick insect that infested pandan plants that are used for mat-weaving in Capiz Province on Panay Island [Philippines]”.

Carausius morosus (Sinéty, 1901)

This species has been introduced accidentally on a number of occasions. Generally, it is not considered a pest, but an outbreak in the San Diego (California, USA) area was a cause of concern for a number of years. A project to record hostplants of the species in San Diego Zoo [17] showed the species to be widely polyphagous. The species is now regarded as a pest in the local area [107]. Headrick and Wilen [108] summarise the history of this invasive species in the area: “the precise time of its establishment in California is unknown; the first official finding occurred in San Diego County in 1991 and shortly thereafter in San Luis Obispo County. There has been an increase in homeowner reports of walking stick damage in the last 10 years along the Central and Southern coasts of the state”.

Due to its popularity as both a pet and laboratory animal, there have been several other unintentional introductions of this species. Its spread in the Azores is discussed by Borges et al. [109]. Brock [110] confirms the identity of a non-native species in the Cape Suburbs, South Africa, as C. morosus, where it seems to have become a minor garden pest. “One lady had telephoned him, distressed that pest control people had recently killed all the adults on ivy (often mentioned as a foodplant), but she now had lots of nymphs”. The species does not currently appear to be a pest after accidental introduction to Madeira [111].

Eurycantha calcarata Lucas, 1869

Gibson et al. [112] refer to this species as an important pest of oil palm in Papua New Guinea and a Eupelmid (Hymenoptera) egg parasite they are rearing in the laboratory for field studies.

Eurycantha insularis Lucas, 1869

Outbreaks of this species in Oro Province, Papua New Guinea have been treated by the organophosphate insecticide monocrotophos [113]. Kimsey et al. [114] describe two new Amisegine wasps (Hymenoptera: Chrysididae) as egg parasites of this species, reared from eggs collected from infested oil palms.

Sipyloidea stigmata Redtenbacher, 1908

Reported to be an increasing pest of Piper nigrum (Black Pepper) [18] and reaching economically important levels in Thenmala and Kulathupuzha, India where it has a preference for eating tender leaves on plagiotropic stems of the vine.

Baculonistria alba (Chen and He, 1990) [2, 115]

= Baculum alba Chen and He, 1990 [116]

= Phobaeticus sichuanensis Cai and Liu, 1993 [117]

A 1986 infestation of this species destroyed several hundred hectares of forest in Wushan County and Zhongxian County (Sichuan Province) through 1986, with densities of several hundred individuals per tree [4].

Another infestation of 800 hectares happened in the Three Gorges area of the Yangtze River green-shelter, in March–April 2005. Around 40 hectares of trees were killed and defoliation was predominantly restricted to Cupressus funebris. The infestation reached an average density of 120 individuals per tree, and was controlled in early May by the application of insecticide. Reported with photographs of defoliation by Xiang Guowie [115].

This species has a 3-year life cycle [116].

Micadina yingdensis Chen and He, 1992 [118]

= Micadina yingdeensis incorrect subsequent spelling [119]

Around 2000 hectares of Castanopsis ifs were damaged by this species in Guangdong Province, China during 1989, around 400 hectares of trees were killed. The next year nearly 3000 hectares in the same region were infested, with the area of destroyed trees (50,000 m3 of timber valued at $560,000) reaching 850 hectares. The density reached more than 450 specimens on a 2–3-year-old tree with less than 100 leaves, more than 1000 insects were found on a 6–7-year-old tree with a crown diameter of <1.5 m3 [119].

This species is unusual as it may be up to tri-voltine [115].

Ramulus chongxinense (Chen and He, 1991) [120]

= Baculum chongxinense Chen and He, 1991 [121]

In Gansu Province (Chongxin and Huatin Counties), China this species attacked over 20 species in 1998, with the infestation covering over 2600 hectares (2,100 hectares were destroyed) at densities estimated as 1000–5000 individuals per plant. Quercus liaotungensis and Carpinus cordata were the most affected species. The infestation recurred on a two-year cycle.

Ramulus minutidentatus (Chen and He, 1994) [122]

= Baculum minutidentatum Chen and He, 1994 [123]

This species defoliated several areas of forest in Yongji County (Jinlin Province) in 1991, killing all younger trees and making older trees dry and withered (Xu and Zhang, 1994 from Hennemann et al., 2008). Infestation occurred 1998–2001 in Tonghua (Jinlin Province) where 2000–5000 insects per tree (Tilia mandshurica) were found, along with a leaf-litter egg density of 1000–3000/m2. This species has a three-year life cycle ([124] in [115]).

Ramulus pingliense (Chen and He, 1991) [4]

= Baculum pingliense Chen and He, 1991 [121]

This species reached damaging levels in Ankang (Shaanxi Province) during 1985. The insects are long lived and individuals can eat remarkable quantities of both young and old foliage. (Ji et al. 2000 in Hennemann et al. 2008). July 1985 saw this species, along with R. intersulcatus which caused less damage, infest forests and gardens in Pingli (Shaanxi Province), the total area was 1400 hectares, including 360 hectares of crops and over 1000 hectares of forest.

Chen [4] reports considerable damage by this species affecting 2,000 hectares of forest and plantation, including Fagus sp. and Prunus domestica in Gansu Province.

This species is uni-voltine [115].

Sinophasma brevipenne Günther, 1940 [125]

Zeng et al. (2002 in [115]) report up to 500 of these insects infesting the crowns of trees in Guiyang (Guizhou Province) in 1983, with many trees in the centre of the city being completely defoliated.

Sinophasma maculicruralis Chen, 1986

Sinophasma pseudomirabile Chen and Chen, 1996

Chen [4] reports both species have been known to cause regular harm in the Guangxi Autonomous Region. In 1984, the population density reached 2000–5000 individuals per tree. Hundreds of hectares of Castanopsis cuspidata and C. hicklii were almost totally defoliated. S. maculicruralis is uni-voltine [115].

Libethroidea inusitata Hebard, 1919

This species has been known to cause damage to Pinus patula in Colombia, where up to 80 hectares were destroyed in 1992–3 [126].

Conclusions and remarks

Theory of phasmid outbreak release

Readshaw [27] proposed a theory for the occurrence of phasmid outbreaks based on a study of Didymuria violescens. Campbell [127] also summarised conditions that make an outbreak likely. The theory presented here combines these two theories and provides supporting evidence from other outbreaks reported in this paper. Several of the criteria suggested by Readshaw are rejected, at least for a general theory, through comparison to North American infestations.

Rejected criteria:
  1. 1.

    Periodicity

    Readshaw [27] puts emphasis on the semi-voltine life cycle of Didymuria violescens as being important to sustaining infestation, giving the trees a year to recover between outbreaks. The uni-voltine life cycle of Diapheromera femorata, and the up to tri-voltine Micadina yingdensis show that alternating years of low and high density are not critical in creating or sustaining an outbreak.

     
  2. 2.

    Kentromorphism

    While kentromorphism is important in the plague locusts, it appears not to be crucial in phasmid outbreaks, only being present in the Australian species that cause periodic infestation. It seems likely this is an evolutionary response to naturally occurring outbreaks caused by forest fires, whereas the other species cause infestation as a response to recent human modification of their environment.

     
Accepted criteria:
  1. 1.

    Habitat disturbance

    Readshaw [27] requires outbreaks to be infrequent. This point is expanded upon by Campbell [127] as ‘Freedom from Catastrophe’ and ‘Forest Stand Conditions’. In Australia, the criterion is a period of absence of forest fire or other catastrophe (between 10 and 80 years). The condition of forest is also a factor in the Michigan and other infestations of Diapheromera femorata where younger second-growth forest was closely linked to high phasmid densities. The introduction of the phasmid may itself be the disturbance, such as the case of Carausius morosus in San Diego [17], and potentially some introductions of Graeffea corona onto new islands [100].

     
  2. 2.

    Inability of predators and parasitoids to contain infestation

    When phasmids occur at normal population densities, the equilibrium is maintained by a number of predators and parasitoids. During an outbreak the phasmid population increases to a level where these natural enemies are incapable of controlling their numbers. Readshaw [27] used the periodicity criterion to explain why these species did not also increase significantly inline with the phasmid population. Given the rejection of this criterion, it seems likely that the inability of these species to control the phasmid population is in fact due to the ‘Habitat disturbance’ criterion: rapid ecological disturbance has either removed or temporarily reduced the population of phasmid predators and parasitoids.

     
  3. 3.

    High fecundity

    Readshaw [27] required a “relatively rapid and massive development around epicentres of high density” for infestations to occur and expand. The species known to cause infestation are known to be highly fecund, all laying in excess of 100 eggs over their lifetime. This high level of reproduction suggests that phasmids in general are heavily predated and/or parasitised. The absence of these enemies is likely therefore to cause a rapid, continued, increase in their abundance until predation/parasitisation is restored, the forest is destroyed through defoliation, or a catastrophic event such as a forest fire. Neumann [6] demonstrated that crowding and food shortage reduced fecundity of females of Didymuria violescens in laboratory conditions.

     
  4. 4.

    Slow migration

    Phasmids are generally slow moving insects, and the species known to cause periodic infestation are known to migrate slowly from the epicentres. In the case of Diapheromera femorata, even a road has been known to create a break between infested and non-infested areas. In the conditions of an outbreak, this slow migration causes the population density to rise significantly generation-on-generation. Readshaw [27] suggests that localised outbreaks may cause further outbreaks by acting as foci for predators and allowing other areas to reach outbreak density. While Readshaw suggests bird predation may act to produce this effect, Campbell [127] notes that birds have been known to completely control early outbreaks of phasmids.

     

Geographic remarks

While recent decades have seen major phasmid outbreaks, there are still many questions that are unanswered in this aspect of phasmid biology. First, while some Australian species have kentromorphic phases no American species are known to. This strongly suggests a long history of outbreaks in Australia and thus an entirely natural cause of outbreaks. So far nobody has reported kentromorphic morphological or behavioural changes in Diapheromera femorata, the sole species prone to infestation levels in the USA or any of the Chinese phasmid fauna.

Further work

The method of Hadlington and Hoschke [48] for measuring damage by these insects (measuring the dry weight of faeces and fallen foliage as a result of feeding) applied to laboratory cultures of these insects could provide baseline data for the severity of infestations for different species.

The study of historical infestations, even when they are ongoing, could be improved using the tree ring technique of Readshaw and Mazanec [23]—and could help the study of the current regular infestations in China and elsewhere. While dendrochronology had been thought impractical for work on Eucalypts, a new body of work shows that it is possible [128].

As the author of the American Agriculturist [65] closed their work, I hope this summary will encourage further work on the importance of phasmids and I would welcome any references that I have overlooked.

Here is an opportunity for [an entomologist] to do useful work—in tracing the habits of this insect, and in suggesting the means for staying its progress. We call attention to this case in the hope of calling out information. If any readers have knowledge of similar ravages, or any experience in the destruction of the insects, we hope they will communicate it”. Anon. [65]

Declarations

Acknowledgements

Hannah Theodorou started work on collecting data for this work. Harriet Campbell-Longley (Natural History Museum Library) provided a great deal of assistance with a great deal of patience. Goulven Keineg (Natural History Museum Library) managed to trace a number of difficult references. Sara Pinzon Navarro (CSIRO) and Graeme Lloyd (Macquarie University) helped to locate number of hard-to-find articles on the Australian species covered here.

Philippa Richardson (University College London) very kindly checked the completed manuscript. Two anonymous reviewers made useful corrections and suggestions.

Competing interests

The author declares that he has no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Life Sciences, Natural History Museum

References

  1. Riley CV. Report of the Entomologist: the thick-thighed walking-stick. In: LeDuc, editor. Annual Report of the Commissioner of Agriculture for the Year 1878. Washington: Government Printing Office; 1879.Google Scholar
  2. Hennemann FH, Conle OV. Revision of Oriental Phasmatodea: the tribe Pharnaciini Günther, 1953, including the description of the world’s longest insect, and a survey of the family Phasmatidae Gray, 1835 with keys to the subfamilies and tribes (Phasmatodea: ‘Anareolatae’: Phasmati. Zootaxa. 2008;1906:316.Google Scholar
  3. Key KHL. Kentromorphic phases in three species of Phasmatodea. Aust J Zool. 1957;5(3):247–84.View ArticleGoogle Scholar
  4. Chen S. The present research situation and future advice of stick insect in China. For Pest Dis. 1994;3:38–40.Google Scholar
  5. Graham SA. The walking stick as a forest defoliator. Michigan Sch. For. Conserv. Circ. 1957;3.Google Scholar
  6. Neumann FG. Egg production, adult longevity and mortality of the stick insect Didymuria violescens (Leach) (Phasmatodea: Phasmatidae) inhabiting mountain Ash Forest in Victoria. J Aust Entomol Soc. 1976;15:183–90.View ArticleGoogle Scholar
  7. Campbell KG. Preliminary studies in population estimation of two species of stick insect (Phasmatidae: Phasmatodea) occurring in plague numbers in highland forests of south-east Australia. Proc Linn Soc N South Wales. 1960;85(3):121–41.Google Scholar
  8. Boucher S, Varady-Szabo H. Effects of different diets on the survival, longevity and growth of the Annam stick insect, Medauroidea extradentata (Phasmatodea: Phasmatidae). J Orthoptera Res. 2005; 14(1):115–18.Google Scholar
  9. Ji H, Luo X, Li W, He Z. Baculum pingliense Chen et He—its capacity of food taking and excreting faeces. Sichuan J Zool. 2000;19(5):6–8.Google Scholar
  10. Neumann FG. Regulation and usage of insecticides in Australian forestry from the mid-1960s to 1990. Aust For. 1992;55:48–64.Google Scholar
  11. Baker”EW. In the News: Stick insects destroy 24 ha of forest. 2011. http://invertdiary.ebaker.me.uk/2011/06/in-news-stick-insects-destroy-24ha-of.html.
  12. Uvarov BP. A revision of the genus Locusta, L. (=Pachytylus, Fieb.) with a New Theory as to the periodicity and migrations of locusts. Bull Entomol Res. 1921;12(2):135–63.View ArticleGoogle Scholar
  13. Rentz DC. Grasshopper Country. UNSW Press; 1996.Google Scholar
  14. Blüthgen N, Metzner A, Ruf D. Food plant selection by stick insects (Phasmida) in a Bornean rain forest. J Trop Ecol. 2006;22(01):35.View ArticleGoogle Scholar
  15. Blüthgen N, Metzner A. Contrasting leaf age preferences of specialist and generalist stick insects (Phasmida). Oikos. 2007;116(June):1853–62.View ArticleGoogle Scholar
  16. Phasmid Study Group. Phasmid Study Group Culture List. 2015. http://phasmid-study-group.org/specieslist.
  17. Baker E. Carausius morosus introduced in San Diego. figshare. 2015. doi:10.6084/m9.figshare.1304202.
  18. Prathapan KD, Anith KN, Faizal MH, Lekha M, Dhanya MK. A report on Sipyloidea stigmata Redtenbacher (Diapheromeridae: Necrosciinae) as the first phasmid crop pest in India and its redescription. Zootaxa. 2008;1959:58–64.Google Scholar
  19. Shepherd KR. Defoliation of Mountain Ash, E. delegatensis, by Phasmids. 1957.Google Scholar
  20. Z. Mazanec. The effect of defoliation by Didymuria Violescens (Phasmatidae) on the growth of Alpine Ash. Aust For. 1966;30:125–30.Google Scholar
  21. Mazanec Z. Mortality and diameter growth in Mountain Ash defoliated by phasmatids. Aust For. 1967;31:221–23.Google Scholar
  22. Mazanec Z. Influence of defoliation by the phasmatid Didymuria violescens on seasonal diameter growth and the pattern of growth rings in Alpine Ash. Aust For. 1968;32:3–14.Google Scholar
  23. Readshaw JL, Mazanec Z. Use of growth rings to determine past phasmatid defoliations of Alpine Ash Forests. Aust For. 1969;33:29–36.Google Scholar
  24. Butler H. An unusual occurrence of walking-sticks. J Econ Entomol. 1914;7:299.Google Scholar
  25. O’Connor BA. Some insect pests of Tonga. Agric J. 1949;20(2).Google Scholar
  26. Paine RW. Investigations for the biological control in Fiji of the Coconut Stick-insect Graeffea crouanii (Le Guillou). Bull Agric Res. 1968;57(4).Google Scholar
  27. Readshaw JL. A theory of phasmatid outbreak release. Aust J Zool. 1965;13(475–490).Google Scholar
  28. Craighead FC. Insect enemies of eastern forests. US Dep. Agric. Misc. Publ. 1950;657.Google Scholar
  29. Severin HHP, Severin HC. 1910. The effect of moisture and dryness on the emergence from the egg of the walking-stick Diapheromera femorata Say. J Econ Entomol. 1910;3:479–81.Google Scholar
  30. Bragg PE. Phasmids eaten by ladybirds. Bull Amat Entomol Soc 50:253.Google Scholar
  31. Robinson MH, Robinson B. Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithson Contrib Zool. 1973;149:1–76.View ArticleGoogle Scholar
  32. Robinson BMH, Lubin YD. Specialists and generalists: the ecology and behavior of some web-building spiders from Papua New Guinea. Pac Insects. 1979;21(2):133–64.Google Scholar
  33. Bragg PE. Phasmids and cockroaches as prey of spiders and mantids. Bull Amat Entomol Soc. 1990;51:19–20.Google Scholar
  34. Nentwig W. Stick insects (Phasmida) as prey of spiders: size, palatability and defence mechanisms in feeding tests. Oecologia. 1990;82(4):446–9.View ArticleGoogle Scholar
  35. Rapp G. Eggs of the stick insect Graeffea crouanii Le Guillou (Orthoptera, Phasmidae). Mortality after exposure to natural enemies and high temperature. J Appl Entomol. 1995;119:89–91.View ArticleGoogle Scholar
  36. Hamilton WJ, Pollac JA. The food of some lizards from Fort Benning, Georgia. Herpetologica. 1961;17(2):99–106.Google Scholar
  37. Bragg PE. Phasmida and coleoptera as food. Bull Amat Entomol Soc. 1989;49:157–8.Google Scholar
  38. Bragg PE. Phasmids of Borneo. Kota Kinabalu: Natural History Publications (Borneo); 2001.Google Scholar
  39. Stone JLS. Keeping and breeding butterflies and other exotica. 1992.Google Scholar
  40. Balfour H. Note on a New kind of Fish-hook from GoodenoughIsland, d’Entrecasteaux Group, New Guinea. Man. 1915;15:9–10.View ArticleGoogle Scholar
  41. Anonymous. Fiji Department of Agriculture. Report for the year 1969. 1970.Google Scholar
  42. Dharmaraju E. Trunk injections with systematic insecticides for the control of the coconut stick insect Graeffea crouanii (Le Guillou). Alafua Agric Bull. 1977;2(2):6–7.Google Scholar
  43. Newman RL, Endacottt ND. The control of a phasmatid insect plague in the forested catchment of the Kiewa Hydro-Electric Scheme. Aust For. 1962;26:6–21.Google Scholar
  44. Oatman ER. Walkingsticks: an unusual pest on Sour Cherry. J Econ Entomol. 1965;58:588–9.View ArticleGoogle Scholar
  45. WLF. Walkingstick. For Pest Leafl. 1964;82.Google Scholar
  46. Swamy BN, Deesh AD. Management of coconut stick insect—Graeffea crouanii (Le Guillou) in Fiji. Tech Bull Minist Prim Ind. 2012.Google Scholar
  47. McCormack G. The common Myna and the coconut Stick-insect on Atiu. 2013.Google Scholar
  48. Hadlington P, Hoschke F. Observations on the ecology of the Phasmatid Ctenomorphodes tessulata (Gray). Proc Linn Soc N South Wales. 1959;84(2):146–59.Google Scholar
  49. Sandoval CP. Persistence of a walking-stick population (Phasmatoptera: Timematoidea) after a wildfire. Southwest Nat. 2001;45(2):123–7.View ArticleGoogle Scholar
  50. Langlois F, Lelong P. Une nouvelle methode de chasse: La douche froide! Le Monde des Phasmes. 1992;20:6–7.Google Scholar
  51. Lowe L, Brock PD. A new (hot) method of collecting stick insects in Australia. Phasmid Stud. 1994;4(1):2–3.Google Scholar
  52. Kimsey LS, Bohart RM. The Chrysidid Wasps of The World. Oxford University Press. 1990.Google Scholar
  53. Compton SG, Ware AB. Ants disperse the Elaiosome-bearing eggs of an african stick insect. Psyche A J Entomol. 1991;98:207–13.Google Scholar
  54. Krombein KV. Biosystematic studies of Ceylonese Wasps, XI: a monograph of the Amiseginae and Loboscelidiinae (Hymenoptera: Chrysididae). Smithson Contrib Zool. 1983;(376).Google Scholar
  55. Severin HHP. A study on the structure of the egg of the walking-stick diapheromera femorata say; and the biological significance of the resemblance of phasmid eggs to seeds. Ann Entomol Soc Am. 1910;3(2):83–92.View ArticleGoogle Scholar
  56. Tilgner EH, McHugh JV. First record of parasitism of Manomera tenuescens Scudder (Phasmida: Heteronemiidae) by Phasmophaga antennalis Townsend (Diptera: Tachinidae). Entomol News. 1999;110:151–2.Google Scholar
  57. Pitts JP, Tilgner EH, Dalusky MJ. New host records for Perilamprus hyalinus (Hymenoptera: Perilampidae) and Phasmophaga antennalis (Diptera: Tachinidae). J Entomol Sci. 2002;37(1):128–9.Google Scholar
  58. Sellick JTC. The capitula of phasmid eggs: an update with a review of the current state of phasmid ootaxonomy. Zool J Linn Soc. 1988;93:273–82.View ArticleGoogle Scholar
  59. Compton SG, Ware AB. Ants disperse the elaiosome-bearing eggs of an african stick insect. Psyche (Stuttg). 1991;98(May):207–13.View ArticleGoogle Scholar
  60. Bragg PE. Parasites of phasmida. Entomology. 1993;112(l):37–42.Google Scholar
  61. Yeates GW, Buckley TR. First records of mermithid nematodes (Nematoda: Mermithidae) parasitising stick insects (Insecta: Phasmatodea). N Zeal J Zool. 2009;36(1):35–9.View ArticleGoogle Scholar
  62. Jago N. The world-wide magnitude of orthoptera as pests. J Orthoptera Res. 1998;1998(7):117–24.View ArticleGoogle Scholar
  63. Brock PD. Phasmida species file online. 2015. http://phasmida.speciesfile.org. Accessed 01 June 2015.
  64. Say T. Long expedition. 1824;2:297.Google Scholar
  65. Anonymous. A new enemy to our forest trees. Am Agric. 1887;36(6):219.Google Scholar
  66. Anonymous. The walkingstick again. Am Agric. 1887;36(8):302.Google Scholar
  67. Baker E. Phasmid infestations reported in American Agriculturist. Invertebrate Diaries. 2015. http://invertdiary.ebaker.me.uk/2015/02/phasmid-infestations-reproted-in.html.
  68. Ferrisburgh RER. Letter. New Yorker; 1874.Google Scholar
  69. Snow GC. Letter. New York Wkly Trib; 1874.Google Scholar
  70. Graham SA. The walking stick as a forest defoliator. University Michigan Sch. For. Conserv. Circ. 1937;3.Google Scholar
  71. USDA Forest Service. Insects of eastern forests. USDA Misc. Publ. 1985;1175.Google Scholar
  72. Wilson LF. Walkingstick. For Pest Leafl. 1971;82(Revise).Google Scholar
  73. Helfer JR. How to know the grasshoppers and allies. Dover Publications; 1963.Google Scholar
  74. Centre for Short-Lived Phenomena. Knobley Mountain Walking Stick Infestation; 1973.Google Scholar
  75. Rivers DB, Hink WF, Denlinger DL. Toxicity of the venom from Nasonia vitripennis (Hymenoptera: Pteromalidae) towards fly hosts, nontarget insects, different developmental stages, and cultured insect cells. Toxicon. 1993;31(6):755–65.View ArticlePubMedGoogle Scholar
  76. Hadlington P, Shipp E. Diapause and Parthenogenesis in the eggs of three species of Phamsatodea. Proc Linn Soc N South Wales. 1961;86:268–79.Google Scholar
  77. Readshaw JL, Bedford GO. Development of the egg of the stick insect didymuria violescens with particular reference to diapause. Aust J Entomol. 1971;19:141–58.Google Scholar
  78. Readshaw JL. Phasmatid outbreaks revisiting. Aust J Zool. 1990;38:343.View ArticleGoogle Scholar
  79. Readshaw JL. The distribution, abundance and seasonal movements of the pied currawong, Sterpera graculina (Shaw), an important bird predator of phasmatidae. Aust J Zool. 1968;16:37–47.View ArticleGoogle Scholar
  80. Macleay WJ. On a species of Phasmatidae destructive to Eucalypti. Proc Linn Soc N South Wales. 1882;6(3):538.Google Scholar
  81. Oliff S. Entomological notes. Agric Gaz N South Wales. 1891;2(6):350–1.Google Scholar
  82. Froggatt WW. Notes on stick or leaf insects with an account of Podacanthus wilkinsoni, as a Forest Pest, and the Spiny Leaf Insect, Extatosoma tiaratum, in the Orchard. Agric Gaz N South Wales. 1905;16(6):515–20.Google Scholar
  83. Anonymous. Notes and exhibits. Proc Linn Soc N South Wales. 1906;31(2):261.Google Scholar
  84. Neumann FG, Marks GC. A synopsis of important pests and diseases in Australian forests and forest nurseries. Aust For. 1976;39:83–102.Google Scholar
  85. Elliott HJ, Ohmart CP, Wylie RF. Insect Pests of Australian Forests. Reed International Books Australia Pty; 1998.Google Scholar
  86. Brock PD, Hasenpusch J. Studies on the Australian stick insects (Phasmida), including a checklist of species and bibliography. Zootaxa. 2007;1570:3–84.Google Scholar
  87. Gray GR. Synopsis of the species of insect belonging to the family Phamsidae; 1835.Google Scholar
  88. Heather JR. Occurrence of Cleptidae (Hymenoptera) Parasites in Eggs of Ctenomorphodes tessellatus (Gray) (Phasmida) in Queensland. J Entomol Soc Queensl. 1965;4:86–7.View ArticleGoogle Scholar
  89. Wylie FR, Yule RA. Tree death and decline in native vegetation of south-east Queensland. Tech Pap Queensl Dep For. 1979;19.Google Scholar
  90. Wylie FR, Bevege DI. Status of Eucalyptus dieback in Queensland. Tech Pap Queensl Dep For. 1980;20.Google Scholar
  91. Le Guillou JC. Revue zoologique Sociaetae Cuvierienne; 1840.Google Scholar
  92. Newport G. On the reproduction of lost parts in Myriapoda and Insecta. Philos Trans R Soc Lond. 1844;134:283–94.View ArticleGoogle Scholar
  93. Hopkins GHE. Pests of Economic Plants in Samoa and other Island Groups. Bull Entomol Res. 1927;18(1):23–32.View ArticleGoogle Scholar
  94. Simmonds HW. Entomology division—annual report, 1935; 1936.Google Scholar
  95. Veitch R, Greenwood W. The food plants or hosts of some fijian insects. Proc Linn Soc N South Wales. 1921;46:505–17.Google Scholar
  96. Swaine G. The coconut stick insect Graeffea crouanii Le Guillou. Oleagineux. 1969;24(2):75–7.Google Scholar
  97. Lever RJAW. Insect pests of some economic crops in Fiji. Bull Entomol Res. 1947;38(1):137–43.Google Scholar
  98. Heptonstall REA. The distribution and abundance of Myna Birds (Acridotheres tristis) and Rimatara Lorikeets (Vini kuhlii) on Atiu, Cook Islands. Submitted in accordance with the requirements for the degree of Masters of Science M.Sc. Biodiversity and Conservation (p. 52); 2010.Google Scholar
  99. Rao VP. Biological control of pests in Fiji. Commonw Inst Biol Control Misc Publ. 1971;2.Google Scholar
  100. Waterhouse DF, Norris KR. Biological Control: Pacific Prospects. Melbourne: Inkata Press; 1987.Google Scholar
  101. Crooker PS. Final report of the research officer entomologist. Government Experimental Farm Vaini, Tonga; 1979.Google Scholar
  102. Lever RJAW. Pests of the coconut palm. Rome; 1969.Google Scholar
  103. Deesh AD, Swamy BN, Khan MGM. Distribution of coconut stick insect, Graeffea crouanii and its parasitoids in selected islands of Fiji. Fiji Agric J. 2013;53(1):18–24.Google Scholar
  104. O’Connor BA. Aerial spraying of coconut palms to control stick insect Graeffea crouanii Le Guillou. Fiji Agric J. 1959;29:138–41.Google Scholar
  105. Swaine G. Agricultural Zoology in Fiji. London: Her Majesty’s Stationery Office; 1971.Google Scholar
  106. Lit IL, Eusebio OL. A new species of the genus Pharnacia (Phasmatodea: Phasmatidae: Phasmatinae: Pharnaciini) on Mango Trees in SIbuyan Island with Notes on Stick Insects Found on Agricultural Crops. Philipp Agric Sci. 2008;91:115–22.Google Scholar
  107. Arakelian G. Indian stick insect (Carausius morosus). Pest Bull Los Angeles Cty Dep Agric Comm; 2015.Google Scholar
  108. Headrick DH, Wilen CA. Indian walking stick. Univ Calif Pest Notes. 2011;74157.Google Scholar
  109. Borges PAV, Reut M, da Ponte NB, Quartau JA, Fletcher M, Sousa AB, Pollet M, Soares AO, Marcelino JAP, Rego C, Carodoso P. New records of exotic spiders and insects to the Azores, and new data on recently introduced species. Arquipelago. 2013;30:57–70.Google Scholar
  110. Brock PD. New records of alien stick-insects. Phasmid Stud. 1998;7:39–40.Google Scholar
  111. Aguiar AMF, Pombo DA, Gonçalves YM. Identification, rearing, and distribution of stick insects of Madeira Island: an example of raising biodiversity awareness. J Insect Sci. 2014;14(49):1–13.View ArticleGoogle Scholar
  112. Gibson GAP, Dewhurst CF, Makai S. Nomenclatural changes in Anastatus Motschulsky and the description of Anastatus eurycanthae Gibson n. sp. (eupelmidae: Eupelminae), an egg parasitoid of Eurycantha calcarata Lucas (Phasmida: Phamsatidae) from Papua New Guinea. Zootaxa. 2012;3419:53–61.Google Scholar
  113. OPRA,. Annual report of the Papua New Guinea Oil Palm Research Association; 1989.Google Scholar
  114. Kimsey L, Dewhurst C, Nyaure S. New species of egg parasites from the Oil Palm Stick Insect (Eurycantha insularis) in Papua New Guinea (Hymenoptera, Chrysididae, Phasmatodea, Phasmatidae). J Hymenopt Res. 2013;30(2013):19–28.View ArticleGoogle Scholar
  115. Hennemann FH, Conle OV, Zhang W. Catalogue of the Stick and Leaf-insects (Phasmatodea) of China, with a faunistic analysis, review of recent ecological and biological studies and bibliography (Insecta: Orthoptera: Phamsatodea). Zootaxa; 2008.Google Scholar
  116. Chen S, He Y. Baculum album—a new walking stick injurious to forests in Sichuan. J Beijing For Univ. 1990;12(4):54–6.Google Scholar
  117. Cai B, Liu SL. A news species of Phobaeticus from China. Acta Entomol Sin. 1993;36(4):469–71.Google Scholar
  118. Chen S, He Y. Micadina yingdensis new species: a new walking stick injurious forest pest from Guangdong Province. For Res. 1992;5(2):209.Google Scholar
  119. Chen S, Xu S. A study in the biological characteristics and control of Micadina yingdeensis. For Res. 1994;7(2):187–92.Google Scholar
  120. Li X, Bing XX, Chen S, Li H. Study on the bionomics and control of Baculum chongxinense. Sci Silvae Sin. 2002;38(6):159–63.Google Scholar
  121. Chen S, He Y. Three new species of Baculum attacking forest from China (Phasmida: Phasmatidae). Sci Silvae Sin. 1991;27(3):229–33.Google Scholar
  122. Otte D, Brock PD. Phasmida species file. Catalog of stick and leaf insects of the world. CafePress; 2005.Google Scholar
  123. Xu S, Zhang H. Biological characteristics of Baculum minutidentatum. Jilin For Sci Technol. 1994;2:21–3.Google Scholar
  124. Chen S, He Y. Two new species of the genus Baculum from China (Phasmatodea: Phasmatidae: Heteronemiidae). Acta Entomol Sin. 1994;37(2):196–8.Google Scholar
  125. Hennemann FH, Conle OV. Studies on New Guinean giant stick-insects of the tribe Stephanacridini Günther, 1953, with the descriptions of a new genus and three new species of Stephanacris Redtenbacher, 1908 (Phasmatodea: ‘Anareolatae’). Zootaxa. 2006;1283:1–24.Google Scholar
  126. Madrigal CA. Los Fasmidos como plaga potencial de le reforestacion en Colombia. Ponencia para el Simposo sobre Plages Forestales. XXIV Congresso Sociedad Colombiana de Entomologia. 1997. p. 225–40.Google Scholar
  127. Campbell KG. Factors limiting the distribution and abundance of the three species of phasmatids (Phasmatodea: Phasmatidae) which occur in plague numbers in forests of South-Eastern Australia. J Entomol Soc Aust (New South Wales). 1974;8:3–6.Google Scholar
  128. Brookhouse M. Eucalypt dendrochronology: past, present and potential. Aust J Bot. 2006;54:435–49.View ArticleGoogle Scholar
  129. Packard AS. 5th report of the United states Entomological Commission. Washington; 1890.Google Scholar
  130. Swezey OH. Notes on insect pests in Samoa. Proc Haw Ent Soc. 1924;5(3):385–93.Google Scholar
  131. Arment C. Stick insects of the Continental United States and Canada: species and early studies. Landsville: Coachwhip Publications; 2006.Google Scholar
  132. Noyes JS. Universal Chalcidoidea Database. 2015. http://www.nhm.ac.uk/chalcidoids.
  133. Muniappan R. Pests of coconut and their natural enemies in Micronesia. Micronesia. 2002;6:105–10.Google Scholar
  134. Mariau D. The fauna of oil palm and coconut. Insect and mite pests and their natural enemies. Montpellier: CIRAD; 2001.Google Scholar
  135. Dammerman The. Agricultural Zoology of the Malay Archipelago: The animals injurious and beneficial to agriculture, horticulture and forestry in the Malay Peninsular, The Dutch East Indies and The Philippines. Amsterdam: J. H. de Bussy Ltd.; 1929.Google Scholar
  136. Wang G, Zhou C. Occurrence and control of Baculum minuidentatum. For Pest Dis. 2003;22(6):31–3.Google Scholar
  137. Crosskey R. A new species of Mycteromyiella (Diptera: Tachinidae) parasitic on Ophicrania leveri Günther (Phasmida: Phasmatidae) in the Solomon Islands. Bull Entomol Res. 1968:525–532.Google Scholar
  138. Pantel J. Sur la larve de Thrixion halidayanum Rond. insecte diptere de la tribu des Tachininae, parasite de Leptynia hispanica Bol. insecte orthoptere de la famille des phasmidae. Stades larvaires et biologie. Comptes rendus des seances l’academie des Sci Paris. 1897;124:472–74.Google Scholar
  139. Lelong P. Thrixion halidayanum (Rond.) parasite de Leptynia hispanica (Bol.). Le Monde des Phasmes. 1989;5:19–22.Google Scholar
  140. Walton WR. A new tachinid parasite of Diapheromera femorata Say. Proc Entomol Soc Wash. 1914;16:129–32.Google Scholar
  141. Uili S. Agricultural development in Tokelu. Alafua Agric Bull. 1980;5:23–5.Google Scholar
  142. Risbec J. Les Chalcidoides de l’Afrique occidentale francaise. Mem l’Institute Fr d’Afrique Noire Ifan-Dakar. 1951;13:172.Google Scholar
  143. Rapp G. Eggs of the stick insect Graeffea crouanii Le Guillou (Orthoptera, Phamsidae). Mortality after exposure to natural enemies and high temperature. J Appl Entomol. 1995;119:89–91.View ArticleGoogle Scholar
  144. Rapp G. Coconut stick insect Graeffea crouanii (Orthoptera: Phasmida), Coconut flat moth Agonozena argaula (Lepidoptera: Agonoxenidae). Studies on pest status, biology, ecological control carried out int he kingdom of Tonga, South Pacific. Stuttgart: Hohenheim; 1989.Google Scholar
  145. Shelomi M. Phasmid eggs do not survive digestion by Quails and Chickens. J. Orthoptera Res. 2011;20(2):159–62.View ArticleGoogle Scholar
  146. Neumann FG. Egg production, adult longevity and mortality of the stick insect. 1976:183–190.Google Scholar

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