PEST STATUS OF LEUCAENA PSYLLID, Heteropsylla cubana Crawford
(HOMOPTERA: PSYLLIDAE) AND BIOLOGICAL CONTROL AGENTS IN
EASTERN TANZANIA
PAULO JOHN LYIMO
A DISSERTATION SUBMITTED IN PARTIAL FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF MASTER OF ECOSYSTEMS
SCIENCE AND MANAGEMENT OF SOKOINE UNIVERSITY OF
AGRICULTURE. MOROGORO, TANZANIA.
2016
ii
EXTENDED ABSTRACT
Heteropsylla cubana has caused damaging effects to Leucaena leucocephala in Tanzania
since its outbreak in 1992. The major objectives of the study were; to determine
population density of H. cubana, mummies of T. leucaena and P. yaseeni, indigenous
predators associated with H. cubana, infestation density and shoot health of
L. leucocephala resulting from H. cubana attack in Morogoro and Tanga region. The
Point Centre Quarter method was employed to select L. leucocephala for observation of
H. cubana, mummies, indigenous predators, infestation and shoot health. R and Excel
program software were used in data analysis to obtain descriptive statistics of observed
data. The mean number of eggs, small nymphs, medium nymphs, large nymphs and adults
per 15cm terminal shoot were 14.24, 11.77, 8.78, 4.79 and 2.81 in Morogoro and 11.40,
8.16, 5.80, 3.72 and 2.42 in Tanga respectively. The population density of eggs differ
significantly among crown levels (upper, middle and lower) and not significant among
dbh classes (1-5 cm, 6-15 cm and >15 cm) in Morogoro. The situation was different in
Tanga where there was no significant difference among crown level and dbh classes. The
interaction between dbh classes and crown level was not significantly different in both
Morogoro and Tanga for eggs population density. The mean number mummies of T.
Leucaenae and P. yaseeni were 2.33 and 1.68 in Tanga and 2.64 and 2.1 in Morogoro
respectively. The dominant indigenous predators found were spiders followed by ladybird
beetles, dragonflies and lacewings for adult and regenerants L. leucocephala. The
infestation density and shoot damage were slightly high in Morogoro compared to Tanga
for adults and regenerants L. leucocephala. The study has found good shoot health and
small injury to L. leucocephala. Farmers are advised to plant L. leucocephala for various
usesas psyllid’s population is no longer a problem.
iii
DECLARATION
I, LYIMO, PAULO JOHN do hereby declare to the Senate of Sokoine University of
Agriculture that this dissertation is my own original work and it has neither been, nor
concurrently being submitted for higher degree awards in any other institution.
____________________________
PAULO J. LYIMO
_______________________
Date
(MSc. EcoSM Student)
The above declaration confirmed by;
____________________________
PROF. MAULID W. MWATAWALA
(Supervisor)
_____________________
Date
iv
COPYRIGHT
No part of this dissertation may be reproduced, stored in any retrieval system transmitted
in any form or by any means without prior written permission of the author or Sokoine
University of Agriculture in that behalf.
v
ACKNOWLEDGMENTS
I would like to express my heartfelt grateful to Almighty God for giving me strength and
good health when undertaking this study. I wish to extend my sincere gratitude to my
family for financing this study. I am tremendously indebted tomy former supervisor, late
Prof. Seif S. Madoffe of the Department of Ecosystem and Conservation, Sokoine
University
of
Agriculture
(SUA)
for
hisconstant inspiration,
patient
counsel,
encouragement, valuable guidance, efforts and readiness to assist towards quality work of
this study. I would not have been able to finish this work without his invaluable help,
comments and profound knowledge of Forest Entomology.May the soul of Prof. Seif
Madoffe rest in peace, amen.
I am very grateful to Prof. Maulid Mwatawala for supervising this dissertation after the
death of Prof. Madoffe. In particular, I thank Dr. Ezekiel Mwakalukwa, Dr. Deo Shirima,
Dr. Revocutus Petro, Mr. Charles Kilawe and Mr. Chelestino Balamafor assisting in
proposal and dissertation write-up.
I greatly appreciate the help of Christoganus John, Aika Aku, John Shesige and Yohanes
Sanga during data collection. I am thankful to Dr. Ever Mtengetifor her assistance and
guidance in the Forest Biology laboratory. I am thankful to my classmates Mr. Mganywa
Wanjala, Mr. Solomon Sembosi, Miss Mariam Gama and Mr. John Christogunus for
contributing to successful completion of this study.
I am deeply indebted to my beloved sister, Dorin Mvungi and her husband, George
Mlyuka for their inspiration and heartfelt encouragement during the study.
vi
DEDICATION
This work is dedicated to my mother, Theresia Michael and father, John Michael who laid
down foundation of my education, provided much of moral support, encouraged and
financed my education.
vii
TABLE OF CONTENTS
EXTENDED ABSTRACT ................................................................................................ ii
DECLARATION .............................................................................................................. iii
COPYRIGHT ................................................................................................................... iv
ACKNOWLEDGMENTS ................................................................................................ v
DEDICATION .................................................................................................................. vi
TABLE OF CONTENTS ............................................................................................... vii
LIST OF TABLES ............................................................................................................ x
LIST OF FIGURES ......................................................................................................... xi
LIST OF PLATES ......................................................................................................... xiii
ABBREVIATIONS AND SYMBOLS .......................................................................... xiv
DISSERTATION STRUCTURE ................................................................................... xv
CHAPTER ONE ............................................................................................................... 1
1.0
INTRODUCTION AND LITERATURE REVIEW ............................................. 1
1.1
An Overview of Exotic Forest Insect Pests in Tanzania ............................................ 1
1.1.1
Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae):
Eucalyptus chalcids ...................................................................................... 1
1.1.2
Pineus boerneri Annand (Homoptera: Adelgidae): Pine woolly aphid ......... 3
1.1.3
Cinara cupressivora Watson and Voegtlin(Lachnidae: Homoptera):
Cypress aphid ................................................................................................ 4
1.1.4
Eulachnus rileyi Williams (Homoptera: Lachnidae): Pine Needle Aphid ..... 6
1.1.5
Phoracantha semipunctata Fabricius and Phoracantha recurva Newman
(Coleoptera: Cerambycidae): Eucalyptus bark beetles .................................. 8
1.2
Study Insect: Leucaena psyllid, Heteropsylla cubana Crawford............................... 9
viii
1.2.1
Biology and ecology of H. cubana ................................................................ 9
1.2.2
Global spread and damage of H. cubana ..................................................... 11
1.2.3
Status of H. cubana in Tanzania .................................................................. 11
1.2.4
Impacts of H. cubana ................................................................................... 12
1.2.5
Control of Heteropsylla cubana................................................................... 12
1.2.5.1
Biological control......................................................................... 12
1.2.5.2
Chemical control .......................................................................... 13
1.2.5.3
Cultural methods or ecological management ............................... 13
1.2.5.4
Host Plant Resistance ................................................................... 14
1.2.5.5
Integrated Pest Management (IPM) ............................................. 14
1.3
Justification .............................................................................................................. 15
1.4
Objectives ................................................................................................................ 16
1.5
1.4.1
Overall Objective ......................................................................................... 16
1.4.2
Specific Objectives ...................................................................................... 16
Hypotheses ............................................................................................................... 17
REFERENCES ................................................................................................................. 17
CHAPTER TWO ............................................................................................................ 32
MANUSCRIPT 1 ............................................................................................................ 32
2.0
Infestation and Population Density of Leucaena psyllid, Heteropsylla cubana
(Homoptera: Psyllidae) on Leucaena leucocephala in Eastern Tanzania .................. 32
CHAPTER THREE ........................................................................................................ 60
MANUSCRIPT 2 ............................................................................................................ 60
3.0
Biological control and Parasitism of Leucaena psyllid, Heteropsylla cubana
Crawford (Homoptera: Psyllidae) in Eastern Tanzania ........................................... 60
ix
CHAPTER FOUR ........................................................................................................... 80
4.0
CONCLUSIONS AND RECOMMENDATIONS ............................................... 80
4.1
Conclusions .............................................................................................................. 80
4.2
Recommendations .................................................................................................... 80
x
LIST OF TABLES
Table 1:
Description of study areas ................................................................................ 35
Table 2:
Scores for infestation, shoot health and nymph population counts .................. 39
Table 3:
Chi- square results for association between dbh classes and
infestation density in Morogoro and Tanga regions ......................................... 45
Table 4:
Chi- square test results shows a significant difference between dbh
classes of shoot health in Morogoro and Tanga regions .................................. 47
Table 5:
Percentage of parasitization of H. cubana for adult L. leucocephala
in Morogoro and Tanga regions ....................................................................... 68
xi
LIST OF FIGURES
Figure 1:
Map of the study regions .............................................................................. 37
Figure 2:
Layout of sampling point on the study area. ................................................ 38
Figure 3:
Mean number of eggs, nymphs and adults of H. cubana for
adults L. leucocephala in Morogoro region ................................................. 41
Figure 4:
Mean number of eggs, nymphs and adults of H. cubana for
adults L. leucocephala in Tanga region........................................................ 41
Figure 5:
Mean number of eggs, nymphs and adults of H. cubana for
regenerants L. leucocephala in Morogoro and Tanga regions ..................... 42
Figure 6:
Mean trend of H. cubana life stages adults L. leucocephala in
Morogoro and Tanga regions ....................................................................... 42
Figure 7:
Nymph population counts through subjective ratings for adults
L. leucocephala in Morogoro ....................................................................... 43
Figure 8:
Nymph population counts through subjective ratings for adults
L. leucocephala in Tanga ............................................................................. 43
Figure 9:
Nymph population counts through subjective ratings for
regenerants L. leucocephala in Morogoro and Tanga regions ..................... 44
Figure 10:
Infestation frequency of H. cubana on L. leucocephala in dbh
classes in Morogoro and Tanga regions ....................................................... 45
Figure 11:
Infestation frequency of H. cubana on regenerants L.
leucocephala in Morogoro and Tanga .......................................................... 46
Figure 12:
Shoot health frequency in different dbh classes and crown parts
for adult L. leucocephala in Morogoro......................................................... 47
Figure 13:
Shoot health frequency in different dbh classes and Crown parts
for adult L. leucocephala in Tanga ............................................................... 48
xii
Figure 14:
Mean numbers of H. cubana mummies of P. yaseeni and T.
leucaenae for adult L. leucocephala in Morogoro regions........................... 66
Figure 15:
Mean number of H. cubana mummies of P. yaseeni and T.
leucaenae for adult L. leucocephala in Tanga regions ................................. 66
Figure 16:
Mean number of H. cubana mummies of Psyllaephagus yaseeni
and Tamarixia leucaenae for regenerants Leucaena
leucocephala in Morogoro and Tanga regions ............................................. 67
xiii
LIST OF PLATES
Plate 1:
Gall wasp, Leptocybe invasa............................................................................ 2
Plate 2:
1–4. One year old P. taeda seedling bearing colonies of P.
boerneri. 1, white woolly wax secreted by adults and nymphs; 2.
Apterous adult female and eggs covered with wax; 3, Apterous
adult female and egg; 4. Nymphs..................................................................... 4
Plate 3:
Cypress aphid, Cinara cuppressivora. .............................................................. 6
Plate 4:
Pine Needle Aphid, Eulachnus rileyi. .............................................................. 7
Plate 5:
Eucalyptus
bark
beetles;
(1)
Phoracantha
semipunctata
(Hoskovec 2010) and (2) Phoracantha recurva .............................................. 9
Plate 6:
Leucaena psyllid, H. cubana; (a): Eggs and Nymph, (b): Nymphs
on Leucaena, (c): Adult and (d): Adult Psyllaephagus yaseeni
Noyes, parasite of H. cubana ......................................................................... 10
xiv
ABBREVIATIONS AND SYMBOLS
ANOVA
Analysis of Variance
CABI
Centre for Agriculture and Biosciences International
cm
Centimeters
dbh
diameter at breast height
Df
Degree of freedom
EcoSM
Ecosystems Science and Management
FAO
Food and Agriculture Organization of the United Nations
FBD
Forestry and Beekeeping Division
Ha
Hectare
IPM
Integrated Pest Management
KFRI
Kenya Forestry Research Institute
m.a.s.l
metres above sea level
MNRT
Ministry of Natural Resources and Tourism
MRSEP
Morogoro Region Socio Economic Profile
NBS
National Bureau of Statistics
NFTA
Nitrogen Fixing Tree Association
SUA
Sokoine University of Agriculture
TAFORI
Tanzania Forestry Research Institute
Tsh
Tanzania Shillings
URT
United Republic of Tanzania
USA
United States of America
xv
DISSERTATION STRUCTURE
This dissertation consists of four chapters. Chapter one describes background information
on Leucaena psyllid, Heteropsylla cubana Crawford globally, Africa and in Tanzania,
problem statement and justification, objectives. Chapter two (paper one) describes
population density of H. cubana, infestation density and shoot health of Leucaena
leucocephala (Lam.) de Witresulting from H. cubana attach in Morogoro and Tanga
region. Chapter three (paper two) presents abundance of H. cubana mummies of
Tamarixia Leucaenae Boucek and Psyllaephagus yaseeni Noyes, percentage of
parasitization of H. cubana and abundance of indigenous predators in Morogoro and
Tanga regions. Chapter four consists of key areas for further studies and specific
recommendations forfarmers practice agroforestry, foresters, forest entomologists, NGOs
and government in general.
1
CHAPTER ONE
1.0
INTRODUCTION AND LITERATURE REVIEW
1.1
An Overview of Exotic Forest Insect Pests in Tanzania
Most introduced organisms, including fungi, insects and mammals, cause of major. In some
cases their impacts have been worldwide (Speight and Wainhouse, 1989). The spread of
exotic forest pests to foreign countries is mostly accidental. Many of the insects now
established in different parts of the world originated from Europe (Campbell and
Schlarbaum, 2014). Some of the early introductions into the new world, in the late
nineteenth and early twentieth centuries due to importation of European trees by the large
immigrant population to USA and Canada. Some of these insects became serious pests of
the native forests (Madoffe and Petro 2011). In Tanzania, most exotic tree species are
attacked by insects, however the intensity of attacks varies.
1.1.1
Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae): Eucalyptus
chalcids
An outbreak of the gall-forming invasive wasp, Leptocybe invasa Fisher and La Salle
(Hymenoptera: Eulophidae), commonly called blue gum chalcid (Plate 1) damage
eucalyptus plantations throughout the world (Mendel et al., 2004). It is native to Australia
and was first reported in the Middle East in 2000 and has spread to most Mediterranean
countries and many of the Eucalyptus areas in northern and Eastern Africa (Mutitu, 2003;
Mendel et al., 2004; Thu, 2004). The wasp occurs in several countries including Algeria,
Iran, Israel, Italy, Jordan, Kenya, Morocco, Spain, Syria, Turkey, Uganda and Tanzania
(Mutitu, 2003 and Petro et al., 2014). In Tanzania, L. invasa infestation was first recorded
on young Eucalyptus camaldulensis Dehnh, E. tereticornis Smith and E. grandis Hill ex
2
Maidenin Tabora and Shinyanga in early 2005. Infestation was also reported in E. grandis
clonal trial grown in Kibaha, Pwani Region and Mombo and Korogwe in Tanga Region
(Petro, 2009).
The wasp lays eggs in the petiole and midrib of leaves and stems of young shoots that
leads to gall formation, which further damages growing shoot tips and leaves of
eucalypts, resulting in quicker abscission of leaves and drying up of shoots. Severely
affected eucalypts show gnarled appearance, stunted growth, lodging, die back and
sometimes tree death (Mendel et al., 2004; Nyeko, 2005; Protasov et al., 2008; Kumari
et al., 2010). The infestation is more severe on seedlings in nurseries and young (1–3 year
old) plantations than on older trees (Nyeko, 2005). Suitable hosts of L. invasa include
several Eucalyptus species and their hybrid clones (Mendel et al., 2004; FAO, 2009; Thu
et al., 2009; Mutituet al., 2010).
Plate 1: Gall wasp, Leptocybe invasa. Source: (Rigi et al., 2014)
Leptocybe invasa infestation significantly impacted growth and biomass production in E.
grandis and E. saligna in Tanzania (Petro et al., 2014). Control measures included
application of agrochemicals and fertilizers to induce leaf formation. Suggested pest
3
management options in Kenya included quarantine, cultural control methods and Kenya
Forestry Research Institute (KEFRI) plans to initiate a biological control program as a
permanent solution (Mutitu and Mukirae, 2004).
1.1.2
Pineus boerneri Annand (Homoptera: Adelgidae): Pine woolly aphid
The Pine Woolly Aphid, Pineus boerneri Annand (Plate 2) feeds on the shoots of Pinus
species, at times causing tip dieback. The aphid occurs in Africa, Australia, Europe, New
Zealand and North and South America. This pest is native to Europe, where it damages
various species of pines. Pineus boerneri attacks 50 pine species in Africa, of which 41
species were introduced in Eastern and Southern Africa and nearly 30 species were
recorded as furnishing food for the pine woolly aphid (Madoffe, 1989). Towards the end
of 1984 nearly all pines plantations in Tanzania were infested, at different degrees of
attack (Madoffe and Day, 1995). In East Africa, planted pines are Pinus patula, P. elliottii
and P. kesiya of which P. kesiya and P. patula appear more susceptible to attack than
other pines grown (Odera, 1991). Biology, ecology and economic importance of this pest
were studied in Kenya, Zimbabwe and South Africa (Barnes et al., 1976; Zwolinski,
1989).
The commonest control method of P. boerneriis by practicing proper silviculture e.g. sites
amelioration and use of resistant pines. Biological control has also been used successfully
for example in Tanzania, native predators such as the Coccinellids sp., Chaelemens sp.,
Chilocorus sp. and Rodolia sp. Reduced aphid population in some pine plantations in the
Sao Hill, West Kilimanjaro and Meru Forest projects (Kisaka, 1990). Various exotic
predators which were evaluated for control of Pineus boerneri includesLeucopis
nigraluua, L. manii, L. tapiae, Ballia eucharis, Scymnus speciesand Tetraphleps raoi
4
Ghauri (Hemiptera: Anthocoridae). Most of these predators fed on the aphids and
suppressed the pest.
Plate 2: 1–4. One year old P. taeda seedling bearing colonies of P. boerneri. 1, white
woolly wax secreted by adults and nymphs; 2. Apterous adult female and eggs
covered with wax; 3, Apterous adult female and egg; 4. Nymphs. Source:
(Lazzari and Cardoso, 2011)
However, Kisaka (1990) reported that Tetraphleps raoi predator was not very effective as
it did not reduce population sufficiently to prevent tree mortality in contrast to Madoffe
(2006). Similarly some chemicals were reported to suppress the pest though they are
expensive and not environmentally friendly (Lazzari and Cardoso, 2011).
1.1.3
Cinara cupressivora Watson and Voegtlin (Lachnidae: Homoptera): Cypress
aphid
Cypress aphid, Cinara cuppressivora Watson and Voegtlin (Plate 3) is a significant pest
of cypress species. It is believed to have originated on Cupressus sempervirens from
5
Eastern Greece (Alleck et al., 2005). It was first recorded in Africa, from northern
Malawi in 1986. Since then it spread rapidly throughout East and southern Africa causing
significant damage. It first appeared in Kenya in 1990 and the most recent record is from
Ethiopia in 2004. Damage to hosts includes browning and defoliation, which in some
cases causes dieback and tree death (FAO, 2007). In Tanzania, symptoms of damage on
cypress trees by C. cupressivora were observed earlier in Musoma in 1986 (Murphy et
al., 1990). The C. cuppressivora is considered to be one of the most damaging introduced
insects, where it has caused extensive damages to planted cypress forests. A secondary
problem caused by aphid feeding is the copious quantities of honey dew which
encourages the growth of sooty mould. Watson et al. (1999) reported that C.
cuppressivora has seriously damaged commercial and ornamental plantings and native
stands of Cupressus, Juniperus, Widdringtonia and other Cupressaceae in Africa, Italy,
Jordan, Yemen, Mauritius and Colombia. Cinara cuppressivora caused a loss of
commercial plantations in East and South Africa and seriously affected supply of
domestic wood in the region (Ciesla, 1991).
Over 75 000 ha of C. lusitanica in Kenya, 15 000 in Tanzania and 4600 in Uganda were
infested by C. cuppressivora to variable damage levels ranging from slight to severe
(Mwangi, 2002). Therefore, it was estimated that C. cuppressivoracaused an annual loss
of growth increment worth 13.5 million USD and killed 41 million USD worth of trees in
Africa (Murphy, 1996).
Threat from this pest forced the Tanzanian Government to stop planting C. lusitanica
while most of the mature plantations were clearfelled in 1970’s and 1980’s (Madoffe,
2006). The pest can be controlled by silviculture methods e.g. thinning, proper site
6
selection and selection of resistant trees. Chemical control is only feasible on small areas
such as hedges (Madoffe and Day, 1995).
Plate 3: Cypress aphid, Cinara cuppressivora. Source: (FAO, 2007)
Classical biological control using a parasitoid, Pauesea species showed some positive
results in Kenya and Uganda (Allard et al., 1994). The parasitoid was released in early
1990’s and records showed that in the late 1990s it spread and established in northern
Tanzania (Kilimanjaro and Arusha) where C. lusitanica is widely planted. In spite of lack
of a systematic survey to evaluate the status of the pest, research showed severity of the
attack is diminishing and the Government has relaxed its ban on replanting of Cypress,
while many individuals have continued planting the species (Madoffe, 2006).
1.1.4
Eulachnus rileyi Williams (Homoptera: Lachnidae): Pine Needle Aphid
Pine Needle Aphid, Eulachnus rileyi Williams (Plate 4) attacks several species of Pinus.
Typically, this insect causes only minor damage where it has been introduced, however, it
has the potential to cause serious damage. Heavy infestations cause needles to turn yellow
and drop prematurely, resulting in growth reduction (FAO, 2007). This needle infesting
aphid of European and North America origin was for the first time discovered in Zambia,
7
Zimbabwe and South Africa in the late 1970’s but the species subsequently spread to
Tanzania, Kenya and Malawi where pines are grown (Katerere, 1984). Like the P.
boerneri, P. patula and P. elliottii seem to be particularly more susceptible. The infested
needles turn yellow and could be lost prematurely and the aphids produce copious
quantities of honeydew, which induce a cover of sooty moulds on heavily infested trees
(Madoffe, 2006). In Tanzania, the pest is found in most pine growing plantations and Sao
Hill forest plantation has the most serious attacks (Madoffe, 1989).
Plate 4: Pine Needle Aphid, Eulachnus rileyi. Source: (Goszczyński and Budzińska
2010)
However, there is no available information about the quantitative effect of the pine needle
aphid on its pine host in Tanzania, Kenya, South Africa and the actual damage to pines is
slight than that caused by the pine woolly aphid. Massawe (1991) described T. raoi as the
most important predator of Pineus species. Leucopis tapeae could also have some
prospects for management of this pest. Proper site selection, proper silvicultural practices
and use of resistant pine species could also reduce ravages from this pest.
8
1.1.5
Phoracantha semipunctata Fabricius and Phoracantha recurva Newman
(Coleoptera: Cerambycidae): Eucalyptus bark beetles
These two longicorn beetles are native to Australia and were accidentally introduced in
many parts of the world including South Africa and East Africa where Eucalyptus are
widely grown (Bubala et al., 1989). It attacks both growing trees and green logs (Annecke
and Moran, 1998). Attacks can cause considerable damage to physiologically stressed
trees sometimes killing them. Phoracantha semipunctata (Plate 5 (1)) is a serious pest in
Zimbabwe, Malawi and Zambia and to a lesser extent in Southern part of Tanzania
(Annecke and Moran, 1998).
In 1989 the beetles were widely distributed in Zambia. Out of the 54 plantations inspected
during 1980 -1983, they were present in 32 plantations corresponding to 94% of the area
of 25 000 hectares under eucalypts in Zambia (Bubala et al., 1989). All Eucalyptus
species grown in Zambia are susceptible to the attack by P. semipunctata whereby in
South Africa, host plants of Phoracantha beetles are E. grandis, E. saligna, E.
diversicolor, E. paniculata and E. maculata. Control of Phoracantha beetles includes
stripping the bark and destroying the infested branches of felled trees (Annecke and
Moran, 1998). Phoracantha semipunctata is mostly closely related to P. recurva which
has been recorded in the Northern Jarrah Forest (Wang, 1995). The two species are
distinguished by the elytra; P. semipunctata has dark reddish brown or blackish brown
elytra with the following yellowish brown markings: 1 narrow zigzag fascia at sub-base, 1
wide, more or less straight fascia just before middle and 1 oval or irregular spot on disc
before apex (Wang, 1995) (Plate 4 (1)). In comparison, the elytra of P. recurva are pale
yellow to yellowish brown with a narrow incomplete zigzag band which is reduced to a
small spot before the middle of each elytra (Plate 4 (2)). Phoracantha semipunctata does
9
not have long hairs and sensilla filiformia on each antennal segment (Faucheux, 2011), as
well as spines on the front dorsal side of hind femur, and the presence of barbs on the
backs of lower leg segments (Wang 1995).
(1)
(2)
Plate 5: Eucalyptus bark beetles; (1) Phoracantha semipunctata (Hoskovec 2010), and
(2) Phoracantha recurva (Paine et al., 2009)
In contrast, P. recurva (Plate 5 (2)) have very dense and long golden hairs arising from
the underside of each antennal segment and the hind femora with strong dense spines on
the front-dorsal side.
1.2
Study Insect: Leucaena psyllid, Heteropsylla cubana Crawford
1.2.1
Biology and ecology of H. cubana
Showler and Melcher (1995) provided a synopsis of H. cubana biology and life cycle
(Plate 6) which is somewhat variable depending upon the region and habitat. Immediately
after hatching, first-instar nymphs begin to feed gregariously near the oviposition site. As
the nymphs grow through five instars to adulthood, they colonize and feed on other
terminal portions of stems, branches and petioles of young leaves. Eggs, nymphs and
adults can be found together on shoot terminals. Each female can produce 300-500 eggs,
10
with an average of 241 eggs. Eggs are mostly laid on the upper surface of unfolded
leaflets, attached by a posterior pedicel. The incubation period for eggs seems to differ
from area to area, but it is generally 2-5 days. Heteropsylla cubana populations are
normally fluctuating quite widely over time and different levels of pest abundance occur
in different parts in the same tree, according to the differences in the growth stages of
Leucaena species. Apparently, Leucaena trees are vulnerable to high infestation of
H. cubana in the stage of producing new shoots (San Valentin, 1988). In India, the new
shoot has been usually observed by heavy infestations of up to 3000 nymphs and adults of
H. cubanaper 15 cm of terminal shoot (Nair, 2007).
(a)
(b)
(c)
(d)
Plate 6: Leucaena psyllid, H. cubana; (a): Eggs and Nymph, (b): Nymphs on Leucaena,
(c): Adult and (d): Adult Psyllaephagus yaseeni Noyes, parasite of H. cubana
(Source: CABI, 2013)
11
1.2.2
Global spread and damage of H. cubana
The first spread of H. cubana from its natural habitat was Hawaii in 1984 and later spread
to Asia in 1985 and in 1992 were noticed in the African continent, in Tanzania, Kenya,
Uganda and Burundi and by 1994 in Sudan and Zambia (Geiger et al., 1995; Ogol and
Spence, 1997; Madoffe and Petro, 2011; Ahmed et al., 2014). Most of Leucaena
plantings in Tanzania were severely damaged by H. cubana in late 1980s (Kisaka, 1994)
and continued in 2000 (Madoffe et al., 2000). Farmers in some parts of Tanzania
including Morogoro and Tabora abandoned planting Leucaena due to severe attacks.
Alternative species such as Leucaena diversiflora Schlecht, L. pallid Britton, L. collinsi
Britton, Gliricidia sepium Jacq and Calliandra calothyrsus Meisn were sought but were not
well accepted by farmers due to their limitation as a fodder (Sorensson and Brewbaker
1987; Edward et al., 2006).
1.2.3
Status of H. cubana in Tanzania
Heteropsylla cubana has been damaging L. leucocephala in Tanzania since its outbreak in
1992. Cultural, genetic and chemical controls were tried in some localised areas, however
without success (Madoffe, et al., 2000). Leucaena leucocephala is important in
maintaining soil fertility through nutrient cycling, provision of fuel wood and building
materials, fodder and in environment conservation in Tanzania (Lulandala and Hall,
1987). Leucaena is found in most part of Tanzania including Morogoro, Tanga, Tabora
and Shinyanga (Madoffe and Petro, 2011; Msangi et al., 2002). The occurrence of the
devastating H. cubana has discouraged the spread of Leucaena-based fodder production
technology since it’s outbreak on the coast of Tanzania in July-August 1992 (Madoffe
and Petro, 2011; Msangi et al., 2002). Two hymenopterous parasitoids, Tamarixia
Leucaena Boucek and Psyllaephagus yaseeni Noyes were introduced from Trinidad to
12
Tanzania in 1995 and 1996 to control H. cubana (Madoffe and Petro, 2011). Preliminary
survey in late 1990’s showed that the parasitoids were well established and were
spreading from the epicentre while there were some remarkable declines of the H. cubana
populations (Madoffe, et al., 2000; Madoffe and Petro, 2011).
1.2.4
Impacts of H. cubana
Heteropsylla cubana limited the use leucaena as a potential forage crop in Malaysia and
to a lesser extent in Australia. In Indonesia and the Philippines, Leucaena was key to the
development of more intensive, stable and sustainable farming systems for smallholder
(Napompeth, 1994; Ahmed et al., 2014). Heteropsylla cubana has also had a significant
impact on exports of leaf meal from Thailand and the Philippines. In Indonesia,
considerable economic loss was recorded on cocoa, coffee and vanilla as a result of
defoliation of Leucaena that was planted to provide shade for these crops (Napompeth,
1994).
Production losses due to H. cubana damage costed Central Queensland beef industry an
excess of $2 million per year in Australia (Mullen et al., 1998). In Morogoro region, the
average household economy loss due to H. cubana attack were estimated to be 54 125
Tanzania shillings per year for loss of pole and timber (Johansson, 1994).
1.2.5
Control of Heteropsylla cubana
1.2.5.1 Biological control
Biological control involves the use of natural enemies of a pest or disease to help keep its
numbers in check. Biological control efforts against H. cubana were successfully by
using specific natural enemies such as the predators, Curinus coeruleus and Olla v-
13
nigrum and the parasitoids, P. yaseeni and T. leucaenae in Asia-Pacific Region and
Africa (Madoffe et al., 2000; Shivankar et al., 2010; Madoffe and Petro, 2011). In
additional, several arthropod natural enemies were associated with the H. cubana, the
most dominant being spiders, lacewings, dragonflies, ladybird beetles and ants in
Tanzania (Madoffe et al., 2000).
1.2.5.2 Chemical control
Several insecticides, such as carbaryl, carbosulfan, cyhalothrin and bifenthin, have
showed equivocal results, although in some cases insecticides suppressed H. cubana
adults but spared the nymphs (CABI, 2013). Other studies indicated that some pesticides
were effective. However, the possibility of residual pesticides on leucaena fodder residues
on and financial costs discouraged pesticide use (Krishnamurthy et al., 1989; NFTA,
1988; CABI, 2013). In India, Insecticides such as endosulfan, phosalone, quinalphos and
monocrotophos (all at 0.05%), controlled H. cubana for at least two weeks and adult pest
infestations were reduced but nymph populations were unaffected (Krishnamurthy et al.,
1989; CABI, 2013). Thus, the insecticides controlled H. cubana for a short period
(Krishnamurthy et al., 1989). Chemical control is uneconomical and eliminates predators
and parasites (NFTA, 1988).
1.2.5.3 Cultural methods or ecological management
Cultural methods create conditions inhospitable for the development of damaging
numbers of pests. These include matching tree species with suitable growing sites,
intermediate harvests to maintain tree vigor and timely harvesting of plantations at
maturity (FAO, 2001). Cultural control methods are diverse and rely on a good
understanding of the pest species ecology in relation to the plant production system (Alao
14
et al., 2011). Some cultural methods, such as grazing and pruning, can be used to manage
H. cubana and should be investigated further (Soon et al., 1989). Pruning and grazing of
new Leucaena shoots preclude the use of the tree for shade estate crops. However, in one
Malaysian grazing new shoots by livestock reduced H. Cubana populations temporarily.
There are no reports of other cultural control tactics that are effective against H. cubana
(CABI, 2013).
1.2.5.4 Host Plant Resistance
Breeding aims to produce superior new genotypes by combining the desirable attributes
of 2 or more parents (Shelton, 2008). There is considerable scope for hybridisation among
Leucaena species and several naturally occurring hybrids have been reported in the native
range in Central America (Hughes, 1998). The University of Hawaii initiated a hybridbreeding program with Leucaena in the early 1980s. Since then hundreds of inter- and
intra-specific crosses were developed (Shelton, 2008). Early research with artificial
hybrids concentrated on crosses among the tetraploid accessions, L. leucocephala, L.
pallida and L. diversifolia, as these were highly cross-compatible (Sorensson and
Brewbaker 1987). Artificial interspecific F1 hybrids between L. pallida and L.
leucocephala (KX2 hybrids) have exhibited good H. cubana resistance, exceptionally
high biomass yield (the result of heterosis or hybrid vigour) and broad environmental
adaptation (Mullen et al., 2003).
1.2.5.5 Integrated Pest Management (IPM)
Integrated pest management systems combines decision-making and pest management
tools directed against a pest or pest complexes in various stages of development. IPM is
an approach for reducing the impact of insects or other pests in any ecosystem. Integrated
15
pest management was employed to control successfully H. cubana in East Africa through
use of biological methods, resistant species like L. deversiflora, L. pallida, L. collinsi,
cultural methods and alternative species such as Gliricidia and Calliandra species
(Madoffe, 2006). Similar programmes were used successful in Asia and IPM was
suggested as an essential approach for managing the H. cubana in Africa (Napompeth,
1994).
1.3
Justification
Damage caused by H. cubana was the most important the limitation in 1990s to the
productivity of L. leucocephala in Eastern Tanzania. Heteropsylla cubanacan be
controlled easily by a wide range of systemic, broad-spectrum insecticides (Barrientos
et al., 1991; Rao, 1995). However, the use of insecticides is uneconomical to small scale
farmers and poses health and environmental risks and may limit the build-up of the H.
cubana natural enemies (Ahmed et al., 2014; Heydon and Affonso, 1989).
Biological control agents may suppress H. cubana populationsin economically and
environmentally manner (Napompeth, 1994). The parasitoids, T. leucaenae Boucek
(Eulophidae) and P. yaseeni Noyes (Encyrtidae) were introduced in Tanzania to
manipulate population of H. cubana. The two parasitoids were introduced in Tabora,
Western Tanzania in February 1996 and T. leucaenae was introduced in Morogoro and
Tanga, Eastern Tanzaniain July and August 1995. However, the spread and establishment
of P. yaseeni in Morogoro and Tanga, Eastern Tanzania are not well known. Despite the
economic importance of Leucaena, the effectiveness of biological control agents for H.
cubana and the fundamental physiological ecology of the tree and H. cubana remain
poorly understood (Geiger and Andrew, 2000). In additional, little has been done to
16
identify other potential natural enemies of the H. cubanain Tanzania (Kisaka, 1994;
Madoffe et al., 2000).
A study by Madoffe et al. (2000) reported a decline of H. cubana population which was
associated with T. leucaenae and P. yaseeni. Reconnaissance surveys conducted in April,
2015 in Morogoro and Tanga showed a decline in attacks of L. leucocephala by H.
cubana. Furthermore, T. leucaenae and P. yaseeni were recorded in almost all L.
leucocephala growing areas. However, the general visual observations were not
correlated population density of both H. cubana and mummies of T. Leucaenae and P.
yaseeni. Infestation density and shoot health of L. leucocephala resulting from H. cubana
attack are also not known.
The findings from this study provide valuable information about whether the release of T.
Leucaenae and P. yaseeni has manipulated significantly population of H. cubana. The
information would form a basis for advising the farmers on whether to continue planting
L. leucocephala or look for alternative fodder and multipurpose trees.
1.4
Objectives
1.4.1
Overall Objective
To assess population density, infestation density and biological control of Heteropsylla
cubana in Leucaena leucocephala growings in Eastern Tanzania
1.4.2
i.
Specific Objectives
To establish population density of Heteropsylla cubana in Morogoro and
Tanga regions.
17
ii.
To determine abundance of mummies of Tamarixia leucaenae and
Psyllaephagus yaseeni establishment in Morogoro and Tanga regions.
iii.
To determine abundance of indigenous predators associated with Heteropsylla
cubana in Morogoro and Tanga regions.
iv.
To assess infestation density and shoot health of Leucaena leucocephala
resulting from Heteropsylla cubana attack in Morogoro and Tanga regions.
1.5
Hypotheses
Ho1:
There is low population density of Heteropsylla cubana in Morogoro and
Tanga regions.
Ho2:
There is a low mummy of Tamarixia leucaenae and Psyllaephagus yaseeni
establishment in Morogoro and Tanga regions.
HO3:
There is no indigenous predators associated with Heteropsylla cubana in
Morogoro and Tanga regions.
HO4:
There is no infestation density and shoot damage of Leucaena leucocephala
resulting from Heteropsylla cubana attack in Morogoro and Tanga regions.
REFERENCES
Ahmed, A.M., Avilés1, L.R., Sánchez, F.J., Zyoud, F. A. and Rodriguez1, M.B. (2014).
An Overview on some biotic and abiotic factors affecting the population
dynamics of Leucaena psyllid, Heteropsylla cubana Crawford (Homoptera:
Psyllidae): Contributory factors for pest management. Tropical and Subtropical
Agroecosystems 17: 437 – 446.
18
Alao, J.S., Sale, F.A. and Ojo, A.S. (2011). Problems and management of insect pests in
social forestry in Nigeria. African Journal of Agricultural Research 6 (33): 6755
– 6758.
Allard, G.B., Day, R.K., Kairo, M.T.K., Murphy, S.T. and Mutitu, E.K. (1994).
Biological control of Exotic Aphids Project. IIBC, Half yearly progress report
No. 7, Nairobi, Kenya. 113pp.
Alleck, M., Seewooruthun, S.I. and Ramlugun, D. (2005). Cypress aphid status in
Mauritius and trial releases of Pauesia juniperorum (Hymenoptera: Braconidae),
a promising biocontrol agent, Food and Agricultural Research Council, Reduit,
Mauritius. pp. 313–317.
Annecke, D.P. and Moran, V.C. (1998). Insects and Mites of Cultivated Plants in South
Africa. Vertenary Science Library, University of Pretoria. 389pp.
Austin, M.P., Williams, M.J., Hammond, A.E., Frank, J.H., Chambliss, C.G. (1996).
Psyllid population dynamics and plant resistance of leucaena selections in
Florida. Tropical Grasslands 30: 223 – 228.
Barnes, R.D., Jarvis, M.S. and Mulin, L.J. (1976). Introduction spread and control of the
pine woolly aphid, Pineus pini (L) in Rhodesia. South Africa Forestry Journal
96: 1-11.
Bray, R.A. (1994). The leucaena psyllid. In: Gutteridge R.C. and Shelton, H.M. (Eds.).
Forage Tree legumes in Tropical Agriculture. CAB International, Oxford. 283 291pp.
19
Bray, R.A. and Woodroffe, T.D. (1988). Resistance of some Leucaena species to the
Leucaena psyllid. Tropical Grasslands Journal 22: 11 – 16.
Barrientos, A., Ruiz, T.E., Febles, G., Castillo, E. and Mora, C. (1991). A note on the
utilization of three insecticides for the control of Heteropsylla cubana Crawford
(Hom: Chermidae) in Leucaena leucocephala. Cuban Journal of Agricultural
Science 25: 207 – 209.
Brewbaker, J.L. and Sorensson, C.T. (1990). New tree crops from interspecific Leucaena
hybrids. In: Janick, J. and Simon, J.E. (Eds); Advances in New Crops, Timber
Press, Portland, Oregon. 283 - 289pp.
Bubala, M., Selander, J. and Loyuyniemi, K. (1989). Forest pests and their management
in Zambia. Division of Forest Research. Forest Department. Zambia. Research
Note No 43: 23 – 25.
Burkhardt,
D.
(1986).
Nomenclatural
note
on Heteropsylla
cubana Crawford
(Homoptera: Psylloidea), a new pest in Pacific Countries. Revue suisse de
Zoologie 93(4): 1023 – 1024.
Bruzas, W.A. (1983). The Pine Woolly Aphid (Pineus pini) and Associated Insects in Pine
Plantations. Internal Report. PPRI, Department of Agriculture and Water
Supply, Pretoria. 37pp.
CABI (2013). Improving lives by solving problems in agriculture and the environment.
[http://www.cabi.org/search/?q=Leucaena+psyllid]. Site visited on 10/06/2016.
20
Campbell, F.T. and Schlarbaum, S.E. (2014). Fading Forests III: North American trees
and the threat of Exotic Pests report. Natural Resources Defense Council,
Washington, D.C. 167pp.
Castillo, A.E., Cuyagan, O.E., Fogarty, S., Shelton, H.M. (1997). Growth, psyllid
resistance and forage quality of Leucaena leucocephala, Leucaena pallida,
Leucaena diversifolia and the Fl hybrid of Leucaena leucocephala x Leucaena
pallida, Tropical Grasslands 31: 188 – 200.
Ciesla, W.M. (1991). Cypress aphid, Cinara cuppressivora: A new pest of conifers in
Eastern and Southern Africa. Plant protection Bulletin 39: 382-393.
Edward, E., Chamshama, S.A.O. and Mugasha, A.G. (2006). Growth performance of
Lesser-known
Leucaena
species/provenances at
Gairo inland
plateau,
Morogoro, Tanzania. Southern African Forestry Journal 208: 53 - 62.
FAO. (2001). Protecting plantations from pests and diseases. Report based on the work of
W. M. Ciesla. Forest Plantation Thematic Papers, Working Paper 10. Forest
Resources Development Service, Forest Resources Division. FAO, Rome. 13pp.
FAO. (2007). Overview of forest pests Kenya. Forest Health and Biosecurity Working
Papers. Rome, Italy. 26pp.
FAO. (2009). Global review of forest pests and diseases: A thematic study prepared in
the frame work of the Global Forest Resources Assessment 2005. FAO, Rome,
Italy. 222pp.
21
Faucheux, M.J. (2011). Antennal sensilla of the yellow longicorn beetle Phoracantha
recurva Newman, 1840: distribution and comparison with Phoracantha
semipunctata (Fabricius, 1775) (Coleoptera: Cerambycidae). Bulletin Institute of
Science 33(1): 19 – 29.
Geiger, C.A. and Andrew, P.G. (2000). Ecology of Heteropsylla cubana (Homoptera:
Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations, and Parasitism
in the Field. Environmental Entomology 29: 76 – 86.
Geiger, C.A., Napompeth, B. and Van Den Beldt, R.J. (1995). An update on the status of
the Leucaena psyllid in Southeast Asia. In: Shelton H.M., Piggin, C.M. and
Brewbaker, J.L. (Eds.). Leucaena: Opportunities and Limitations. Canberra:
Australian Centre for Agricultural Research. 8 – 125pp.
Goszczyński, W. and Budzińska, L. (2010). Coniferous plants in the urban greenery of
Lublin and their aphidofauna. Aphids and other hemipterous insects 16: 37 – 47.
Heydon, D. and Affonso, M. (1989). Economic review of psyllid damage on leucaena in
South East Asia and Australia. Report prepared for the Australian International
Development Assistance Bureau.
CAB International Development Service,
Wallingford, U.K. 129pp.
Hoskovec, R. (2010). Longhorned Beetles (Cerambycidae) of the West Palaearctic
region. [http://www.cerambyx.uochb.cz/cerambyx.htm] Site visited on
10/02/2016.
22
Hughes, C.E. (1998). Leucaena: A genetic resources handbook. Oxford Forestry Institute,
Tropical Forestry Paper No. 37. Oxford, UK. 274pp.
Johansson, A. (1994). Effect of Leucaena psyllid on women’s enterprises. A case of
Morogoro In: Sub Regional Workshop on Leucaena psyllid: a threat to
agroforestry in Africa. (Edited by Ciesla, M. and L. Nshubemuki), 10-14
October 1994, Dar es Salaam, Tanzania. 40 - 47pp.
Kisaka, E.Z. (1990). Special Studies on Wooly Aphids (Pineus pini) at Sao-Hill. SaoHillForest Project, Mafinga. Tanzania Forestry Research Institute, Moshi,
Tanzania. 11pp.
Katerere, Y. (1984). Biology and population dynamics of the pine needle aphid,
Eulachnus rileyi (Williams) in Zimbabwe. South Africa Forestry Journal129: 40
- 49.
Kisaka, E.Z. (1994). Incidence of forest pest in Tanzania a special reference to the
Leucaena Psyllid. In: Sub-Regional Workshop on Leucaena psyllid: a threat to
agroforestry in Africa (Edited by Ciesla, W. and L. Nshubemuki), 10-14
October 1994. Dar es Salaam, Tanzania. 236pp.
Krishnamurthy, K., Munegowda, M.R. and Rajagopal, D. (1989). Outbreak of psyllid,
Heteropsylla cubana Crawford, on Leucaena and its outlook in alley cropping in
India. Proceedings of an international workshop held January 16-21, 1989 in
Ogor, Indonesia. 17 – 24pp.
23
Kumari, K.N., Kulkarni, H., Vastrad, A.S. and Goud, K.B. (2010). Biology of
Eucalyptus
gall
wasp,
Leptocybe
invasa,
Fisher
and
LaSalle
(Hymenoptyera: Eulophidae). Karnataka Journal of Agricultural Science 23(1):211
- 212.
Larsson, S. (1989). Stressful times for the plant stress insect performance
hypothesis. Oikos 56: 277-283.
Lazzari, S. and Cardoso, J. (2011). Pineus boerneri Annand, 1928 (Hemiptera,
Adelgidae) – a new species to Brazil: morphology of eggs, nymphs and adults.
Revista Brasileira de Entomologia 55(4): 459 – 466.
Lulandala, L.L. and Hall, J.B. (1987). Fodder and wood production from Leucaena
Leucocephala intercropped with maize and beans at Mafiga, Morogoro,
Tanzania. Forest Ecology and Management 21: 109 – 117.
Madoffe, S.S. (1989). Infestation densities on the Pine woody aphid (Pineus pini) on
Pinus patula as related to site productivity at Sao- Hill Forest Plantation.
Dissertation for Award of MSc Degree at University of Dar es Salaam,
Tanzania, 141 pp.
Madoffe, S.S. (2006). Forest insect pest and their management in Tanzania. In:
Management of Selected Crop Pests in Tanzania. (Edited by Makundi, R.H,),
Tanzania Publishing House Limited, Dar es Salaam. pp. 140 – 158.
24
Madoffe, S.S. and Massawe, A. (1994). Periodicity of Leucaena psyllid infestation on
Leucaena leucocephala in Morogoro. Preliminary observation. In: Ciesla, W.
and L. Nshubemuki (eds) Proc. Workshop on Leucaena psyllid: A threat to
agroforestry in Africa. 155 - 161pp.
Madoffe, S.S. and Day, R. (1995). Plantation forest pest in Eastern Africa: present status
and management options. In: Special Issue. Management of Forest Plantation in
Tanzania; (Edited by Chamshama, S.A.O. and Idd, S.), Faculty of Forestry,
SUA, Morogoro. Forest Record No. 63:99 - 108.
Madoffe, S.S., Muhundo, L., Day, R.K. and Nshubemuki, L. (2000). The pontential of
Classical biological control against Leucaena psyllid (Heteropsylla cubana
Crawford) in Eastern Tanzania. Tanzania Journal of Agricultural Sciences 3:
113 - 122.
Madoffe, S.S., Ngoo, A.G. and Tarimo, J. (2001). The influence of induced shading in
Leucaena leucocephalla seedlings on Heteropsylla cubana. Tanzania Journal of
Forestry and Nature Conservation74: 39-51.
Madoffe, S.S. and Petro, R. (2011). Status of forest insect pests in Tanzania: Introduction,
Spread, Damage and Management Options. In: L. Nshubemuki, S.S. Madoffe,
S.A.O. Chamshama, S. Bakengesa and C. Balama. (eds). In: Preceedings of the
Workshop on Insect pests, Diseases and Soil Problems in Forest Plantation held
at the Kibaha Conference Centre, Kibaha, Tanzania, 3 to 4 February, 2011.
Tanzania Forest Research Institute, Tanzania. 2-16pp.
25
Massawe, A. (1991). A review of the pine woolly aphid, Pineus pini (L.), a pest of pine
plantations in Tanzania. In: Proceedings of a Workshop on Exotic Aphid Pests of
Conifers: A Crises in African Forestry. (Edited by Ciesla, P.M.), 3 - 6 June
1991, Kenya Forestry Research Institute, Muguga, Kenya. pp. 68 - 72.
McAuliffe, M. (2008). Investment Opportunity: New PBR Leucaena variety. A full
information package is available from Melissa McAuliffe. [http://www.
leucaena.net/pr_info_pack.pdf.] 9 /3/2015.
Mendel, Z., Protasov, A., Fisher, N. and La Sallae, J. (2004). Taxonomy and biology of
Leptocybe invasa gen and sp. n (Hymenoptera: Eulophidae), an invasive gall
inducer on Eucalyptus. Australian Journal of Entomology 43: 51–63.
Ministry of Planning, Economy and Empowerment (2006). Morogoro Region Socio
Economic Profile (MRSEP) Ministry of planning, economy and empowerment.
Dar es Salaam, Tanzania. 122pp.
Msangi, R.B., Otsyina, R. and Kusekwa, M.L. (2002). Evaluation of lesser known
Leucaena Species/Provenances and hybrids for fodder production and psyllid
tolerance at Tabora and Shinyanga, Tanzania. In: Proceedings of the Regional
Agroforestry Conference on Agroforestry Impactson livelihoods in Southern
Africa: Putting Research intoPractices. (Edited by Rao, M.R. and Kwesiga,
F.R). 20 – 24 May 2002, Aventura Resorts, Warmbaths South Africa. 181187pp.
26
Mullen, B.F., Gabunada, F., Shelton, H.M., Stur, W.W. and Napompeth, B. (1998).
Psyllid resistance in Leucaena. In: Australian Centre for International
Agricultural Research Proceedings. (Edited by Shelton, H.M., Gutteridge, R. C.,
Mullen, B.F. and R.A Bray, R.A.). Adaptation, Quality and Farming Systems
Workshop 9 – 14 February 1998. 86: 51 – 60.
Mullen, B.F and Shelton, H.M. (2003). Psyllid resistance in Leucaena.Part 2.
Quantification of production losses from psyllid damage. Agroforestry Systems
58:163 − 171.
Murphy, S.T., Abraham, Y.J., and Cross, A.E. (1990). Ecology and Economic importance
of the Aphid pests, pineus sp. and Eulachnusrileyi on exotic pine plantations in
southern and Eastern Africa. In: Workshop proceedings of exotic aphid pests of
conifers: A crisis in African forestry. (Edited by Ciesla, P. M.), 3 - 6 June 1991,
Muguga, Kenya. 51 – 62pp.
Murphy, S.T. (1996). Status and impact of invasive conifer aphid pests in Africa. In:
Proceedings of the IUFRO Symposiumon impact of diseases and insect pests in
tropical forests. (Edited by Nair, K.S.S. et al.), 23-26 November 1993, Peechi,
India. 289-297pp.
Mutitu, K.E. (2003). A pest threat to Eucalyptus species in Kenya. KEFRI Technical
Report, Kenya Forestry Research Institute, Nairobi. 12pp.
27
Mutitu, K.E., Otieno, B.O., Nyeko, P. and Ngae, G.N. (2010). Variability in the
infestation of Leptocybe invasa (Hymeneptera: Eulophidae) on commercially
grown Eucalyptus germplasm in Kenya. In: Natural Resource Management for
Improved Livelihoods. (Edited by Imo, M., Ipara, H., Etiegni, L., Mulewa, C.M.,
Muisu, F., Njiru, J.M. and Kirongo, B.B.), Moi University, School of Natural
Resource Management, Eldoret, Kenya. pp. 115–120.
Mwangi, J.G. (2002). Integrated Pest Management Model for Kenya. National Cypress
Aphid Project, Kenya. [http://www.easternarc.org/html/ipmModl] Site visited on
15/04/2016.
Nair K.S.S. (2007). Tropical Forest Insect Pests. The United States of America by
Cambridge University Press, New York. 263pp.
Napompeth, B. (1994). Leucaena psyllid in the Asia-Pacific region: implications for its
management in Africa. In: Leucaena Psyllid: a Threat to Agroforestry in Africa.
FAO Corporate Document Repository Food and Agriculture Organization of the
United Nations, Rome, Italy. pp. 1–15.
National Bureau of Statistics, NBS. (2012). Population and Housing Census: Population
Distribution by Administrative Areas. Project Report. National Bureau of
Statistics.
Nyeko, P. (2005). The cause, incidence and severity of a new gall damage on Eucalyptus
species at Oruchinga refugee settlement in Mbarara district, Uganda. Uganda
Journal of Agricultural Science 11: 47 - 50.
28
NFTA. (1988). Leucaena Psyllids - A Review of the Problem and its Solutions.
[http://factnet.winrock.org/fnrm/factnet/factpub/FACTSH/L_psyllids.html]. Site
visited on 15/07/2015.
Odera, J.A. (1991). Some Opportunities for Managing Aphid of Softwood Plantations in
Malawi. Assistance to Forestry sector Malawi. MLW/86020. ROME. 135pp.
Ogol, C. and Spence, J.R. (1997). Population density, population dynamics and impact of
the Leucaena psyllid Heteropsylla cubana Crawford in a maize-Leucaena
agroforestry system in Kenya. Insect Science and its Application 17: 183 – 92.
Paine, T.D., Dreistadt, S.H., Davis, A. and Millar, J.G. (2009). Pest Notes Publication
7425 University of California State wide Integrated Pest Management Program
Agriculture and Natural Resources. 1 - 27 pp.
Patil, N.G., Baker, P.S. and Pollard, G.V. (1993). Life histories of Psyllaephagus
yaseeni (Hymenoptera, Encyrtidae) and Tamarixia leucaenae (Hymenoptera,
Eulophidae), parasitoids of the leucaena psyllid Heteropsylla cubana.
Entomophaga 38: 565 – 577.
Petro, R. (2009). Status of pine woolly aphid (Pineus boerneri) in Sao Hill Forest
Plantation, Southern Highlands, Tanzania (Unpublished Master’s thesis).
Sokoine University of Agriculture, Morogoro, Tanzania. 36 – 57pp.
29
Petro, R., Madoffe, S.S. and Iddi, S. (2014). Infestation Density of Eucalyptus Gall Wasp,
Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae) on Five
Commercially Grown Eucalyptus Species in Tanzania, Journal of Sustainable
Forestry 33: 276 – 297.
Protasov, A., Doganlar, M., La Salle, J. and Mendel, Z. (2008). Occurrence of two local
Megastigmus sp. parasitic on the Eucalyptus gall wasp, Leptocybe invasa in Israel
and Turkey. Phytoparasitica 36(5): 449 – 459.
Rao, M.R. (1995). Leucaena psyllid in Kenya and experience with chemical control. In
Ciesla, W.M. and Nshubemuki, L. (eds) Leucaena psyllid: a threat to
agroforestry in Africa. Proceedings of a workshop held in Dar-es-Salaam,
Tanzania, 10-24 October 1994. (Rome: FAO). pp. 136 – 142.
Rigi, K., Eyidozehi, K., Jahedi, A. and Dehvairi, M. (2014). Biology, Bioecology and
behavior Eucalyptus gall wasp, Leptocybe invasa Fisher and La Salle
(Hymenoptera: Eulophidae) in Golestan Province. International Journal of
Agriculture and Crop Sciences 7 (9): 1 – 6.
San Valentin, H. (1988). Seasonal population density, distribution and host range of
psyllid infesting Ipil-ipil. [http://erdb.denr.gov.ph/enr/i4d/i4d_fo_psy.pdf.]. Site
visited on 15/04/2015.
Sharma, J.K. and Sankaran, K.V. (1988). Incidence and severity of Botryodiplodia
dieback in plantations of Albizia falcataria in Kerera, India. For Ecological
Management 24:43 – 58.
30
Shelton, H.M. (2008). Psyllid-resistant Leucaena hybrid for northern Australia. Meat and
Livestock Australia Limited, Australia. 1 – 40pp.
Shivankar, V.J. and Rao, C.N. (2010). Psyllids and Their Management. Pest Management
in Horticultural Ecosystems 16: 1 – 4.
Showler, A.T. and Melcher, J. (1995). Environmental assessment for implementation of
biological control for the Leucaena psyllid in Asia and Africa. Washington,
D.C.: U.S. Agency for International Development. 18 – 24pp.
Soon, U., Lin, T. and Chee, W. (1989). Studies on Leucaena psyllid in Malaysia. In:
Proceedings of an international workshop held January 16-21, 1989 in Ogor,
Indonesia. 28 – 39pp.
Sorensson, C. and Brewbaker, I.L. (1987). Psyllid resistance of Leucaena hybrids and
Species in Leucaena Research Report. 7 (2): 29 - 31.
Speight, M.R. and Wainhouse, D. (1989). Ecology and Management of Forest insects.
Clarendon Press. Oxford, 373pp.
Thu, P.Q. (2004). The first record of gall forming wasp associated with eucalypt
plantations in Vietnam. Science and Technological Journal of Agriculture and
Rural Development 11: 1598 - 1599.
Thu, P.Q., Dell, B. and Burgess, T.I. (2009). Susceptibility of 18 Eucalyptus species to
the gall wasp, Leptocybe invasa in the nursery and young plantations in
Vietnam. Science Asia 35: 113 - 117.
31
Wang, Q. (1995). A Taxonomic Revision of the Australian Genus Phoracantha Newman
(Coleoptera: Cerambycidae). Invertebrate Taxonomy 9: 865 – 958.
Watson, G.W., Voegtlin, D.J., Murphy, S.T. and Foottit, R.G. (1999). Biogeography of
the Cinaracupressi complex (Homoptera: Aphididae) on Cupressaceae, with
description of a pest species introduced into Africa. Bulletin of Entomological
Research. 89(3): 271 – 283.
Zwolinski, J.B. (1989). The Pine Woolly Aphid, Pineus pini (L). A pest of pines in South
Africa. South Africa Forestry Journal 151: 52 – 57.
Zwolinski, J.B. (1990). Preliminary evaluation of the impact of pine woolly aphid on
condition and growth of pines in Southern Cape. South Africa Forestry Journal
153: 22 – 26.
32
CHAPTER TWO
MANUSCRIPT 1
2.0
Infestation and Population Density of Leucaena psyllid, Heteropsylla cubana
(Homoptera: Psyllidae) on Leucaena leucocephala in Eastern Tanzania
Paulo J. Lyimo1, Maulid W. Mwatawala2 and Revocatus Petro3
1
Sokoine University of Agriculture, Department of Ecosystem and Conservation, P.O.
Box 3010, Morogoro, Tanzania,
2
Sokoine University of Agriculture, Department of Crop Science and Production, Box
3005, Morogoro, Tanzania,
3
Tanzania Forestry Research Institute, P.O. Box 45, Mafinga-Iringa, Tanzania
Abstract
The invasion of Heteropsylla cubana has restricted the utilization of the important multipurpose tree Leucaena leucocephala in Tanzania. The objectives of the study were to
determine population density of H. cubana, to assess the infestation density and shoot
health of Leucaena leucocephala resulting from psyllid attach in Morogoro and Tanga
region. The Point Centre Quarter method was employed to select Leucaena leucocephala
for observation. R and Excel program software were used in data analysis. The results of
the study showed that mean number of eggs, small nymphs, medium nymphs, large
nymphs and adults per 15cm terminal shoot were 14.24, 11.77, 8.78, 4.79 and 2.81 in
Morogoro and 11.40, 8.16, 5.80, 3.72 and 2.42 in Tanga respectively. The population
density of eggs differed significant among crown level and not significant among dbh
class in Morogoro, differently in Tanga were not significantly among crown level and
among dbh classes. The interaction between dbh classes and crown level was not
33
significant in both Morogoro and Tanga for eggs population density. There was no
significance difference of nymph and adult population density among crown level and
among dbh classes in Morogoro and Tanga. The infestation density and shoot damage
were slightly high in Morogoro compared to Tanga for both adults and regenerants L.
leucocephala. The study has found good shoot health and small injury to L. leucocephala
as a result of low population density of H. cubana. Farmers are advised to plant L.
leucocephalafor various use without any fear of H. cubana as its population is no longer a
problem.
Key words: Heteropsylla cubana, Leucaena leucocephala, Infestation density and Shoot
health
Introduction
Leucaena leucocephala (Lam.) de Witis a multipurpose tree widely grown in the tropics
(Ahmed et al., 2014; Nair, 2007). Leucaena leucocephalais highly used throughout much
of Asia and Africa as a multipurpose legume tree which provides a source of fodder,
fuelwood, shade for estate crops, reforestation, timber, erosion control and nitrogen
fixation (Napompeth, 1994). However, invasion of Leucaena psyllid, Heteropsylla
cubana Crawford limited all these benefits and it has reduce production of L.leucocephala
by 50-70% in humid regions and 20-50% in sub-humid environments (Mullen and
Shelton, 2003). Heteropsylla cubana is a tiny yellow-green insect in the family Psyllidae
of the order Homoptera. Heteropsylla cubana feeds on young growing shoots of several
plant species related to the genera Mimosa, Piptadenia and Leucaena. It is native to
Central and South America. The first spread from its natural habitatwas recorded Hawaii
in 1984 and later Asia in 1985 and East Africa in 1992 (Ahmed et al., 2014; Nair, 2007;
Madoffe and Petro, 2011). Heteropsylla cubana damages plants when both the nymphs
34
and adults suck from the developing shoots and young foliage. Heavy infestations leads to
defoliation of the plant and stop growth, although older leaves are not directly damaged
by psyllid. However, H. cubana produces sticky fluid exudates that promote growth of
sooty mould on leaves and limits photosynthesis (Shelton, 2008).
During 1986, the economic loss due to H. cubana attacks was estimated at more than 316
million USD in Indonesia. Malaysia imported over 48 000 tons of leaf meal at an
estimated cost of over 20 million USD for pig and poultry feeds due to attack of Leucaena
fodders (CABI, 2013). Also, H. cubana infestation in northern and southern Queens land
reduced Leucaena production by at least 55%. In India, over 200 000 seedlings were
destroyed by H. cubana in 1988 (CABI, 2013; Napompeth, 1994). In Tropical America,
the socio-ecological and economic impacts of H. cubana are negligible largely because L.
leucocephala is not cultivated with the same intensity as in Asia and because of
complexes of natural enemies which co-evolved with H. cubana (CABI, 2013).
Heteropsylla cubana arrived in East Africa in August 1992 and restricted the utilization
of the important multi-purpose tree L. leucocephala (Madoffe and Petro, 2011). Leucaena
leucocephala is found in many parts of Tanzania and is usually planted along farm
boundaries and in homesteads for fodder, soil fertility improvement and fuelwood
(Msangi et al., 2002). Most Leucaena stands were affected after the invasion of H.
cubana (Madoffe et al., 2000).
In planning efforts to control H. cubana through biological approachin Kenya and
Tanzania, the Asia-Pacific experience was considered the best option (Ciesla and
Nshubemuki, 1995; Madoffe and Petro, 2011). It involved biological control using two
hymenopterous parasitoids Tamarixia leucaenae Boucek and Psyllaephagus yaseeni Noyes
35
introduced from Trinidad and Tobago. They were released in Tanzania and Kenya and both
species are well established in Tanzania, have spread over large areas and they appear to be
effective against their hosts (Madoffe et al., 2000; Madoffe and Petro, 2011).
There is some reduction in H. cubana population and Leucaena shoot damage in some areas,
which could be attributed to the parasitoids (Madoffe et al., 2000). However, little is known
aboutcurrent population density of H. cubana, infestation density and shoots health of L.
leucocephala since the release of T. leucaenae, and P. yaseeni. Additionally, the
hypothesis that the decline of H. cubana population and damage in Tanzania were due to
the introduced hymenopterous parasitoids is yet to be proved (Madoffe et al., 2000;
Madoffe and Petro, 2011). Population density of H. cubana, infestation density and shoot
health of L.leucocephala were investigated. The study was based on two hypotheses that;
(1) There is a decline in population density due to release of T. leucaenae and P. yaseeni
and (2) There is a decline in infestation density and improved shoot health of L.
leucocephala due to release of T. leucaenae and P. yaseeni in Eastern Tanzania.
Materials and Methods
Description of study areas
Studies were conducted in selected sites of Morogoro and Tanga regions, as described in
Table 1 below.
Table 1: Description of study areas
Region
Morogoro
Tanga
Location name
SUA farm
Melela A
Melele B
Mlingano
Tanga dairy farm
Ziwani
Latitude
6°.822097
6°54'53.6"
6°55'84.6"
50.6667
5015'S
5º.3354
Longitude
37°.661160
37°26'0.61"
37°19'.61"
380.91667
39015
38º.5494
Altitude (m)
500.7
488.19
486.9
87.12
65.34
236.43
36
Heteropsylla cubana parasitoids were released in these sites in the 1995. Spread and
establishment of the psyllid was assessed in 1999 by Madoffe et al. (2000). Morogoro
region lies between latitude 5o 58" and 10o 0"to the South of the Equator and longitude
35o 25" and 35o 30" East of Greenwich. The region has an area of 72 939 km2and
population of 2 218 492 (MRSEP, 2006; NBS Census, 2012). Morogoro is predominantly a Miombo woodland and mountainous vegetation area. The region receives
an annual average rainfall of 600-1200 mm and average annual temperature varies
between 18oC on the mountains to 30oC in river valleys (MRSEP, 2006). Morogoro
region has mostly sandy clay loams in the topsoils and clays in subsoils.
Tanga Region is situated between 4° and 6° below the Equator and 37° to 39° 10' east of
the Greenwich Meridian. Tanga occupies a total area of 26 677 km2 with a population of
2 045 205 (NBS Census, 2012). The region is characterized by bushland, palm gardens,
village cultivations and estates (mainly sisal), natural forest and shrub thickets and open
savannah grassland with scattered trees and scrub thickets. Tanga region is characterized
by mean annual rainfall of 1200 mm and mean monthly temperatures range between 19oC
and 33oC. Tanga soils are sandy in the coastal belt, clay to loamy in the hinterland and
leached mineral laterite in the highlands (Swai et al., 2005).
37
Figure 1: Map of the study regions
Methodology
Sampling Design
The Point Centre Quarter method (PCQ) was employed to assess population of H.
cubana, incidence and damage (Marisa, 2015). Five sampling points were established in
each site; one at center and other four at the corners of site (Figure 2). Four quadrants
were established in each sampling point. Leucaena leucocephala tree and regenerants
near the sampling point at each quadrant were sampled and recorded. Leucaena
leucocephala were first grouped into two clusters of regenerants (diameter at breast
height (dbh)< 1 cm) and adult species (dbh≥ 1 cm). Adult Leucaena trees were then
38
categorized into three dbh classes i.e., (1-5 cm), (6-15 cm) and (>15 cm). Tree in each
class were then divided into three crown levels (upper, middle and lower level). Two
Leucaena trees for each dbh classes and two regenerants were sampled in each quadrant.
Figure 2: Layout of sampling point on the study area (Marisa, 2015).
Determining population numbers of H. cubana
Data were collected from 05:30-10:00 am in the morning, when adult H. cubana were
less active. One 15cm growing shoot was randomly selected and sampled from each
crown level for adult individuals (L. leucocephala with dbh≥ 1 cm) and two 15cm
growing shoot of two regenerants (L. leucocephala with dbh< 1 cm) in each quadrant. A
total of 2 160 and 240 adult individuals and regenerants L. leucocephala were sampled.
The shoots were carefully cut and put into a polythene bag (destructive sampling) and put
in a refrigerator overnight to immobilise the nymphs and adult psyllid. The collected
shoots were washed carefully with a help of brush and ethanol (70%) to a petri-dish to
remove the insects (eggs, nymphs and adults) and indigenous predators. A dissecting
microscope was used to observe when sorting and counting eggs, nymphs and adult
insects. Nymphs were then scored as small (yellow in colour, first and second instars),
39
medium (blackish in colour, third and fourth instars), or large (greenish in colour, fifth
instars).
DeterminingInfestation density and shoot health due to H. cubana
Infestation density, nymph population and shoot health of L. leucocephala were recorded
using empirical score as modified from Bray and Woodroffe, 1988 (Table 2).
Table 2: Scores for infestation, shoot health and nymph population counts
Tree infestation ratings
Nymph population score
Shoot health score
1 - No infestation
0- None
1-No damage
2 - Light infestation
1 - 1-5 nymphs
2- Slight damage
(Loss of < 25% of young Leaves)
2 - 6-30 nymphs
3 - Heavy damage
3 - Moderate infestation
3 - 31-100 nymphs
4 - Dead
(Loss of 26 to 50% of young Leaves)
4 - >100 nymphs
4 - Heavy infestation
5 - >100 nymphs extends to stem
(Loss of >75% of young Leaves)
5 - Severe infestation
(Blackening stem with total leaves loss)
Source: (Modified from Bray and Woodroffe, 1988)
Data Analysis
R version 3.2.3 and Microsoft excel computer software programs were used in data
analysis. Descriptive statistics were used to determine mean population density of H.
cubana. Two way Analysis of Variance (ANOVA) at 5% level of significance was used
to statistically test the equality of means population density differences in H. cubana and
infestation density between dbh classes and crown parts.
Results
Population density of H. cubana in Morogoro and Tanga Regions
Figures 3 and 4 show mean numbers of H. cubana individuals in Morogoro and Tanga
regions respectively. Mean numbers of eggs, small nymphs, medium nymphs, large
40
nymphs and adults per 15cm terminal shoot were 14.24, 11.77, 8.79, 4.79 and 2.81 in
Morogoro and 11.41, 8.16, 5.59, 3.73 and 2.43 in Tanga respectively. Numbers of eggs
and small nymphs were higher than the other H. cubana stages (Table 2 and 3; Figure 3
and 4). Mean numbers of larger nymphs and adults were lowest in all examined dbh
classes. The mean numbers of H. cubana in Morogoro and Tanga decreased from one
stage to another for adults L. leucocephala (Figure 6). The same population trend was
observed for regenerants L. leucocephala (Figure 5). Results showed significant
difference in number of eggs among crown levels (F=5.768, df=2, P=0.003) but not
among dbh classes (F=2.872, df=2, P=0.057) in Morogoro region. In Tanga region,
number of eggs were not significant different among crown level (F=0.061, df=2,
P=0.941) and dbh class (F=0.816, df=2, P=0.443). The interaction between DBH and
crown level was not significant different in both Morogoro (F=0.484, df= 4, P=0.748) and
Tanga (F=0.612, df= 4, P=0.654) regions.
There was no significant difference in number of small nymphs among crown levels
(F=0.367, df=2, P=0.693) and among dbh classes (F=2.317, df=2, P=0.100) in Morogoro
(Table 6). Likewise, there was no significant difference inpopulation density of small
nymphs among crown level (F=0.005, df=2, P=0.995) and among dbh class (F=0.813,
df=2, P=0.444) in Tanga region. The interaction between dbh and crown level was not
significantly different in both Morogoro (F=0.805, df=4, P=0.522) and Tanga (F=0.763,
df=4, P=0.550) for small nymph population density. The results showed no significance
difference of numbers of adult H. cubana among crown levels (F=0.235, df=2, P=0.156).
However, dbh classes had a significant effect (F=3.379, df=2, P=0.035) in Morogoro
(Table 7). In addition, there was no significance difference in number of adult H. cubana
among crown levels (F=0.235, df=2, P=0.790) and among dbh classes (F=0.813, df=2,
41
P=0.727) in Tanga (Table 8). The interaction between dbh and crown level was not
significantly different in both Morogoro (F=0.257, df=4, P=0.905) and Tanga (F=0.514,
df=4, P=0.725) regions.
20
15
10
5
Eggs
Small
Nymph
Medium
Nymph
Large
1–5
Nymph
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Crown
level
Middle
0
Lower
Population density
25
Adults
6–15 >15
Figure 3: Mean number of eggs, nymphs and adults of H. cubana for adults
Crown
level
Eggs
Small
Nymph
Medium
Nymph
Large
Nymph
1–5
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
16
14
12
10
8
6
4
2
0
Lower
Population density
L.leucocephala in Morogoro region
Adults
6–15
>15
Figure 4: Mean number of eggs, nymphs and adults of H. cubana for adults L.
leucocephala in Tanga region
42
Population density
50
40
30
20
10
0
Eggs
Small
Nymphs
Medium
Nymphs
Large
Nymphs
Adults
Morogoro
Life stage of Leucaena psyllid
Tanga
Figure 5: Mean number of eggs, nymphs and adults of H. cubana for regenerants L.
Mean number
leucocephala in Morogoro and Tanga regions
Eggs
Small Nymph
Medium
Nymph
Life stage
Figure 6:
Large Nymph
Adult
Tanga
Morogoro
Mean trend of H. cubana life stages adults L. leucocephala in Morogoro
and Tanga regions
The nymph population counts through subjective ratings (Table 1) showed most growing
shoots of adult L. leucocephala had 6–30 nymphs followed by adults with 1–5 nymphs
43
(Figure 7 and 8). Regenerants L. leucocephala had 1–5 nymphs in Morogoro and 6–30
None
1–5 nymphs
6–30
nymphs
31–100
nymphs
Nymphs population score
>100
nymphs
1–5
6–15
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Middle
Upper
50
40
30
20
10
0
Lower
Frequency
nymphsin Tanga region (Figure 9).
>100
nymphs
extends to
stem
>15
Figure 7: Nymph population counts through subjective ratings for adults L.
None
1–5
nymphs
Nymphs population score
6–30
nymphs
31–100
nymphs
>100n
nymphs
1–5
6–15
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
Lower
Upper
Middle
50
40
30
20
10
0
Lower
Frequency
leucocephala in Morogoro
>100n
nymphs
extends to
stem
>15
Figure 8: Nymph population counts through subjective ratings for adults L.
leucocephala in Tanga
44
80
Frequency
60
40
20
0
None
1–5
6–30
31–100
>100
>100
nymphs nymphs nymphs nymphs nymphs
extends
Morogoro Tangato stem
Nymphs population score
Figure 9: Nymph population counts through subjective ratings for regenerants L.
leucocephala in Morogoro and Tanga regions
Incidence of H. cubanaon L. leucocephala in Morogoro and Tanga Regions
The results revealed that there was generally slightly higher incidence of infestationin
Morogoro compared to Tanga for both adults and regenerants L. Leucocephala (Figure 10
and 11). A high proportionof adults L. leucocephala were lightly infested in all three dbh
classes in Morogoro and Tanga (Figure 10). A high proportion of regenerants of L.
leucocephala were lightly and moderately infested in Morogoro andin Tanga (Figure 10).
The results showed that there wasno significant relationship between dbh classes and
infestation density in both Morogoro and Tanga. Chi- square results for association
between dbh classes and infestation density were not significant different for adults and
regenerants L. leucocephala in Morogoro and Tanga region (Table 3).
45
Table 3:
Chi- square results for association between dbh classes and infestation
density in Morogoro and Tanga regions
Region
dbh classes
χ2 value
Df
P- value
Morogoro
1–5
20.0
16
0.220
6–15
15.0
12
0.241
>15
20.0
16
0.220
Regenerants
20.0
16
0.220
1–5
15.0
12
0.241
6–15
10.0
8
0.265
>15
15.0
12
0.241
Regenerants
15.0
12
0.241
Frequency
Tanga
70
60
50
40
30
20
10
0
1–5
6–15
>15
1–5
Morogoro
DBH
class
6–15
>15
Tanga
No infestation
Light infestation
Moderate infestation
Heavy infestation
Severe infestation
Figure 10:
Infestation frequency of H. cubana on L. leucocephala in dbh classes in
Morogoro and Tanga regions
46
80
70
Frequency
60
50
40
30
20
10
0
No infestation
Light
infestation
Infestation Rating
Moderate
infestation
Heavy
infestation
Morogoro
Severe
infestation
Tanga
Figure 11: Infestation frequency of H. cubana on regenerants L. leucocephala in
Morogoro and Tanga
Shoot Damage of L. leucocephala in Morogoro and Tanga Regions
The results showed thata high proportion of shoots of adults L. leucocephala were slightly
damaged in all three dbh classes in Morogoro and Tanga (Figures 12 and 13). The Chisquare test results shows a significant difference between dbh classes and shoot health of
adults L. leucocephala for all three dbh classes in Morogoro and Tanga regions (Table 4).
The shoot health for regenerants L. leucocephala was not significant different in
Morogoro and Tanga regions (Table 4).
47
Table 4: Chi- square test results shows a significant difference between dbh classes
of shoot health in Morogoro and Tanga regions
Region
dbh classes
χ2value
Df
Morogoro
1–5
24
6
0.001
6–15
36.0
9
0.0001
>15
36.0
9
0.0001
Regenerants
12.0
9
0.213
1–5
36.0
9
0.0001
6–15
36.0
9
0.0001
>15
36.0
9
0.0001
Regenerants
12.0
9
0.213
Tanga
P- value
Frequency
80
60
40
20
No damage
Slight damage
Heavy damage
1–5
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Middle Crown
Crown
level
Lower Crown
0
Dead
6–15
>15
Figure 12: Shoot health frequency in different dbh classes and crown parts for adult
L. leucocephala in Morogoro
No damage
Slight damage
Heavy damage
1–5
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Middle Crown
Lower Crown
Upper Crown
Crown
level
Middle Crown
80
60
40
20
0
Lower Crown
Frequency
48
Dead
6–15
>15
Figure 13: Shoot health frequency in different dbh classes and Crown parts for
adult L. leucocephala in Tanga
Discussion
During this study a low population density of H. cubana was found compared to what
was reported in other studies. In India, the new shoots were heavily infested with up to
3000 nymphs and adults per 15 cm of terminal shoot (Nair, 2007), which is very high
compared to this study found. In Australia, it was reported field collected stem tips from
all L. leucocephala individuals had H. cubana eggs of average 234±58 eggs/shoot
(Shelton, 2008).
Over 90% of samples also had approximately 75-80 younger (instars 1-2) and older
(instars 3-5) nymphs/shoot. However, the present study (in contrast to above reported
studies) were carried out in sites where T. leucaenae and P. yaseeni were introduced in
1995/1996 (Madoffe et al., 2000; Madoffe and Petro, 2011). Ahmed et al., 2014; Geiger
49
and Andrew, 2000 and Shivankar et al. (2010) reported that T.leucaenae and P.yaseeni
are one of successful biological control agentsagainst H. cubana in native and exotic
locations.
The results of this study showed that H. cubana prefers cooler climates. During the study
Morogoro had cooler climate than Tanga. Austin et al. (1996) and Castillo et al. (1997)
reported high psyllid numbers throughout the year at Southeast Queensland and upland
regions in Hawaii due to cooler climates. The current studyfound high number of egg and
small nymphs compared with medium nymphs, large nymphs and adults. Similarly,
Madoffe et al. (2000) found that small nymph populations were consistently higher than
the other two instars and larger nymphs had the lowest populations in the same studied
localities. This study found a decline in number at each life stage of H. cubana from eggs
to adults which resemble same trend reported by Madoffe et al. (2000). The lower mean
number of adult psyllid could be also due to escaping during cutting growing shoot to
polythene bags for laboratory observation. In a study, one year done by Bruzas (1983) in
South Africa, experienced higher number of eggs than nymph or adult Pineus boerneri.
The mean total numbers of H. cubana were not significantly different among dbh classes.
This is because H. cubana prefer new growing shoots and new shoots were available at
each dbh classes. In contrast, Madoffe and Petro (2011) reported a significant difference
in numbers of H. cubana between middle and old age classes but not between middle and
old age class. The difference is due to difference mode of attack by P. boerneri and H.
cubana is highly seasonal in its occurrence (Ahmed et al., 2014) and if food is available,
cool temperatures could increase the psyllid populations (Bray, 1994; Madoffe and
Massawe, 1994; Napompeth, 1994). In other studies, dry season led to tree stress and
50
made trees susceptible to even moderate psyllid population (Larsson, 1989). Other studies
showed that psyllid population was affected by temperature, moisture, humidity and
exposure to wind (Ahmed et al., 2014; Geiger and Andrew, 2000; McAuliffe, 2008) and
the ups and downs of the H. cubana populations were related to an optimum cooler
temperature range and the availability of tender shoots in Hawaii (Ahmed et al., 2014).
Generally, the mean number of H. cubana per 15cm terminal shoot in Morogoro and
Tanga for lower, middle and upper crown part were statistically insignificant which is
similar to that reported by Madoffe and Petro (2011) that the infestation by P. boerneri
between crown parts was not significant for Pinus patula and Pinus elliottii. Despite this,
there was a slightly high population density in the lower crowns, which contrasted Petro
and Madoffe (2011) who reported that middle crown part had higher total mean number
of P. boerneri, followed by lower crown part and upper crown parts.
There was slightly high infestation density in Morogoro compared to Tanga for both
adults and regenerants L. leucocephala which could be a result of high population density
of H. cubana in Morogoro compared to Tanga. Heteropsylla cubana infestations are
determined largely by the presence of nymphs and adults on the growing shoots of L.
leucocephala (CABI, 2013). The slight infestation density in Morogoro and Tanga was a
result of a role played by T. leucaenae, P. yaseeni and indigenous predators. Similarly,
Madoffe et al. (2000) and Madoffe and Petro (2011) reported the declining H. cubana
population recorded was probably due to hymenopterous parasitoids, T. leucaenae and
P.yaseeni attack. In the Asia-Pacific Region, the release of T.leucaenae and P.yaseeni
were reduced populations of H. cubana to their present low levels (Ahmed et al., 2014;
Nair, 2007). The insignificance difference between dbh classes and infestation density in
51
both Morogoro and Tanga was due to availability of growing shoots for H. cubana
feeding in each dbh class. The heavy level of shoots damage occurred in Morogoro
compared to Tanga, after that the population fluctuation in L. leucocephala. Generally,
shoot damage decreased in Morogoro and Tanga since release of parasitoids. Female
H. cubana mostly like to lay eggs on very young shoots where they are lodged between
the folds of the developing leaflets (CABI, 2013; Shelton, 2008). The regenerants
L. leucocephala have high number of suitable growing shoot compared to adults
L. leucocephala. That’s why shoot health for regenerants L. leucocephala were similar in
Morogoro and Tanga regions. These results are in agreement with Geiger and Andrew
(2000) and Chazeau et al. (1989) who reported that, H. cubana populations increased
only in the presence of young L.leucocephala leaves and new growing shoots.
Conclusion
The study investigated low H. cubana population at all life stages including eggs, small
nymphs, medium nymphs, large nymphs and adults compared to previous studies.This
could be due to role played in combination of T. leucaenae and P. yaseeni, indigenous
predators and environmental factors.The study has found good shoot health and slightly
infestation to L.leucocephala as a result of low population density of H. cubana in
Morogoro and Tanga regions.
Recommendations
Based on the results from this study and experiences from other studies, it is
recommended that; farmers should plant L. leucocephala for various uses without any
fear about H. cubana as its population is no longer a problem. Further studies should be
conducted on the status of H. cubana to other localities where the hymenopterous
52
parasitoids were not released. In addition, studies to assess the seasonal population
density of H. cubana and investigation on the effect of abiotic factors such as rainfall,
temperature, wind velocity and others on H. cubana are suggested.
References
Ahmed, A. M., Avilés1, L.R., Sánchez, F.J., Zyoud, F. A. and Rodriguez1, M. B. (2014).
An Overview on some biotic and abiotic factors affecting the population
dynamics
of
Heteropsylla
cubana
Crawford
(Homoptera:
Psyllidae):
Contributory factors for pest management. Tropical and Subtropical
Agroecosystems17: 437 – 446.
Alao, J. S., Sale, F.A. and Ojo, A.S. (2011). Problems and management of insect pests in
social forestry in Nigeria. African Journal of Agricultural Research 6 (33): 6755
– 6758.
Austin, M.P., Williams, M.J., Hammond, A.E., Frank, J.H., Chambliss, C.G. (1996).
Psyllid population dynamics and plant resistance of leucaena selections in
Florida. Tropical Grasslands 30: 223 – 228.
Bray, R.A. (1994). The Heteropsylla cubana. In: Gutteridge R. C. and Shelton, H. M.
(Eds.). Forage Tree legumes in Tropical Agriculture. CAB International,
Oxford. pp. 283 – 291.
Bray, R.A. and Woodroffe, T.D. (1988). Resistance of some Leucaena species to the
Heteropsylla cubana. Tropical Grasslands Journal 22: 11–16.
53
Brewbaker, J.L. and Sorensson, C.T. (1990). New tree crops from interspecific Leucaena
hybrids. In: Advances in New Crops (Edited by Janick, J. and Simon,
J.E.), Timber Press, Portland, Oregon. 283 – 289pp.
Burkhardt, D. (1986). Nomenclatural note on Heteropsylla cubana Crawford
(Homoptera: Psylloidea), a new pest in Pacific Countries. Revue suisse de
Zoologie 93(4): 1023 - 1024 .
Bruzas, W.A. (1983). The Pine Woolly Aphid (Pineus pini) and Associated Insects in Pine
Plantations. Internal Report. PPRI, Department of Agriculture and Water
Supply, Pretoria. 37pp.
CABI (2013). Improving lives by solving problems in agriculture and the environment.
[http://www.cabi.org/search/?q=Leucaena+psyllid]. Site visited on 10/06/2016.
Castillo, A.E., Cuyagan, O.E., Fogarty, S., Shelton, H.M. (1997). Growth, psyllid
resistance and forage quality of Leucaena leucocephala, L. pallida, L.
diversifolia and the Fl hybrid of Leucaena leucocephala x L. pallid. Tropical
Grasslands 31: 188 – 200.
Chazeau, J., Bouye, E. and Bonnet de Larborgne, L. (1989). Lutte biologique contre le
psylle Heteropsylla cubana ravageur du faux mimosa Leucaena leucocephala en
Nouvelle Calédonie. Orstom, Nouméa.
54
Edward, E., Chamshama, S.A.O. and Mugasha, A.G. (2006). Growth performance of
Lesser-known
Leucaena
species/provenances at
Gairo inland plateau,
Morogoro, Tanzania. Southern African Forestry Journal 208: 53 – 62.
FAO (2001). Protecting plantations from pests and diseases. Report based on the work of
W. M. Ciesla. Forest Plantation Thematic Papers, Working Paper 10. Forest
Resources Development Service, Forest Resources Division. FAO, Rome.
FAO. (2007). Overview of forest pests Kenya. Forest Health & Biosecurity Working
Papers. Rome, Italy. 26pp.
Geiger, C.A. and Andrew, P.G. (2000). Ecology of Heteropsylla cubana (Homoptera:
Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations, and Parasitism
in the Field. Environmental Entomology 29: 76 – 86.
Geiger, C.A., Napompeth, B. and Van Den Beldt, R.J. (1995). An update on the status of
the H. cubana in Southeast Asia. In: Shelton H.M., Piggin,
C.M. and
Brewbaker, J.L. (Eds.). Leucaena: Opportunities and Limitations. Canberra:
Australian Centre for Agricultural Research. pp. 8-125.
Hughes, C.E. (1998). Leucaena - A genetic resources handbook. Oxford Forestry
Institute, Tropical Forestry Paper No. 37. Oxford, UK. 274pp.
Johansson, A. (1994). Effect of H. cubana on women’s enterprises. A case of Morogoro
In: Sub Regional Workshop on H. cubana: a threat to agroforestry in Africa.
(Edited by Ciesla, M. and L. Nshubemuki), 10-14 October 1994, Dar es Salaam,
Tanzania. 40 - 47pp.
55
Kisaka, E.Z. (1994). Incidence of forest pest in Tanzania a special reference to the H.
cubana. In: Sub-Regional Workshop on H. cubana: a threat to agroforestry in
Africa (Edited by Ciesla, W. and L. Nshubemuki), 10-14 October 1994. Dar es
Salaam, Tanzania. 236pp.
Krishnamurthy, K., Munegowda, M.R. and Rajagopal, D. (1989). Outbreak of psyllid,
Heteropsylla cubana Crawford, on Leucaena and its outlook in alley cropping
in India. In: Proceedings of an international workshop held January 16- 21,
1989 in Ogor, Indonesia. 17 – 24pp.
Larsson, S. (1989). Stressful times for the plant stress insect performance hypothesis.
Oikos 56(2): 277 – 283.
Lulandala, L.L. and Hall, J.B. (1987). Fodder and wood production from Leucaena
Leucocephala intercropped with maize and beans at Mafiga, Morogoro,
Tanzania. Forest Ecology and Management 21: 109 – 117.
Madoffe, S.S. and Massawe, A. (1994). Periodicity of Heteropsylla cubana infestation on
Leucaena leucocephala growing in Morogoro: Preliminary observations.
In: Heteropsylla cubana "A threat to Agroforestry in Africa. (Edited by W.
Ciesla and L. Nshubemuki), Dar-es-Salaam, Tanzania.155-161pp.
Madoffe, S.S., Muhundo, L., Day, R.K. and Nshubemuki, L. (2000). The pontential of
Classical biological control against Leucaena psyllid (Heteropsylla cubana
Crawford) in Eastern Tanzania. Tanzania Journal of Agricultural Sciences 3:
113 - 122.
56
Madoffe, S.S., Ngoo, A.G. and Tarimo, J. (2001). The influence of induced shading in
Leucaena leucocephala seedlings on Heteropsylla cubana. Tanzania Journal of
Forestry and Nature Conservation 74: 39 – 51.
Madoffe, S.S and Petro, R. (2011).
Status of forest insect pests in Tanzania:
Introduction, Spread, Damage and Management Options. In: L. Nshubemuki,
S.S. Madoffe, S.A.O. Chamshama, S. Bakengesa and C. Balama. (eds).
Preceedings of the Workshop on Insect pests, Diseases and Soil Problems in
Forest Plantation held at the Kibaha Conference Centre, Kibaha, Tanzania, 3 to
4 February, 2011. Tanzania Forest Research Institute, Tanzania. 2 – 16 pp.
Marisa, H. (2015). Application of Point-Centered Quarter Method for Measurement the
Beach Crab (Ocypode spp) Density. Biological Research Journal 1: 1- 6.
Ministry of Planning, Economy and Empowerment (2006). Morogoro Region Socio
Economic Profile (MRSEP) Ministry of planning, economy and empowerment.
Dar es Salaam, Tanzania. 122pp.
McAuliffe, M. (2008). Investment Opportunity: New PBR Leucaena variety. A full
information package is available from Melissa McAuliffe. [http:// www.
leucaena. net/pr_info_pack.pdf]. Site visited on 9 /3/2015.
57
Msangi, R.B., Otsyina, R. and Kusekwa, M.L. (2002). Evaluation of lesser known
Leucaena Species/Provenances and hybrids for fodder production and psyllid
tolerance at Tabora and Shinyanga, Tanzania. In: Proceedings of theRegional
Agroforestry Conference on Agroforestry Impactson livelihoods in Southern
Africa: Putting Research into Practices. (Edited by Rao, M. R. and Kwesiga, F.
R). 20 – 24 May 2002, Aventura Resorts, Warmbaths South Africa. 181- 187pp.
Mullen, B.F., Gabunada, F., Shelton, H.M, Stur, W.W. and Napompeth, B. (1998).
Psyllid resistance in Leucaena. In: Australian Centre for International
Agricultural Research Proceedings. (Edited by Shelton, H. M., Gutteridge, R.
C., Mullen, B.F. and RA Bray, R.A.). Adaptation, Quality and Farming Systems
Workshop 9 – 14 February 1998 86: 51 – 60.
Mullen, B.F. and Shelton, H.M. (2003). Psyllid resistance in Leucaena. Part 2.
Quantification of production losses from psyllid damage. Agroforestry Systems
58:163 − 171.
Nair, K.S.S. (2007). Tropical Forest Insect Pests. The United States of America by
Cambridge University Press, New York. 263pp.
Napompeth, B. (1994). H. cubana in the Asia-Pacific region: implications for
its
management in Africa. In: H. cubana: a Threat to Agroforestry in Africa. FAO
Corporate Document Repository Food and Agriculture Organization of the
United Nations, Rome, Italy. pp. 1–15.
58
National Bureau of Statistics, NBS. (2012). Population and Housing Census: Population
Distribution by Administrative Areas. Project Report. National Bureau of
Statistics.
NFTA. (1988). H. cubanas - A Review of the Problem and its Solutions.
[http://factnet.winrock.org/fnrm/factnet/factpub/FACTSH/L_psyllids.html]. Site
visited on 15/07/2015.
Ogol, C. and Spence, J.R. (1997). Population density, population dynamics and impact of
the H. cubanaHeteropsylla cubana Crawford in a maize- Leucaena agroforestry
system in Kenya. Insect Science and its Application 17: 183 – 92.
Petro, R. (2009). Status of pine woolly aphid (Pineus boerneri) in Sao Hill Forest
Plantation, Southern Highlands, Tanzania (Unpublished Master’s thesis).
Sokoine University of Agriculture, Morogoro, Tanzania.
San Valentin, H. (1988). Seasonal population density, distribution and host range of
psyllid infesting Ipil-ipil. [http://erdb.denr.gov.ph/enr/i4d/i4d_fo_psy.pdf.]. Site
visited on 15/04/2015.
Sharma, J.K. and Sankaran, K.V. (1988). Incidence and severity of Botryodiplodia
dieback in plantations of Albizia falcataria in Kerera, India. For Ecological
Management 24: 43 – 58.
Shelton, H.M. (2008). Psyllid-resistant Leucaena hybrid for northern Australia. Meat and
Livestock Australia Limited, Austaralia. 1 – 40pp.
59
Shivankar, V.J. and Rao, C.N. (2010). Psyllids and Their Management. Pest
Management in Horticultural Ecosystems 16: 1 – 4.
Showler, A.T. and Melcher, J. (1995). Environmental assessment for implementation of
biological control for the Heteropsylla cubana in Asia and Africa. Washington,
D.C.: U.S. Agency for International Development.
Soon, U., Lin, T. and Chee, W. (1989). Studies on Heteropsylla cubana in Malaysia. In:
Proceedings of an international workshop held January 16-21, 1989 in Ogor,
Indonesia. 28 – 39pp.
Sorensson, C. and Brewbaker, I.L. (1987). Psyllid resistance of Leucaena hybrids and
Species in Leucaena Research Report 7 (2): 29 – 31.
Speight, M.R. and Wainhouse, D. (1989). Ecology and Management of Forest insects.
Clarendon Press. Oxford. 373pp.
Swai, E., Karimuribo, E., Schoonman, L., French, N., Fitzpatrick, J., Kambarage, D. and
Bryant, M. (2005). Description, socio-economic characteristics, disease
managements and mortality dynamics in smallholder's dairy production system
in coastal humid region of Tanga, Tanzania. Livestock Research for Rural
Development 17: 4 - 8.
60
CHAPTER THREE
MANUSCRIPT 2
3.0
Biological control and Parasitism of Leucaena psyllid, Heteropsylla cubana
Crawford (Homoptera: Psyllidae) in Eastern Tanzania
Paulo J. Lyimo1, Maulid W. Mwatawala2 and Ezekiel E. Mwakalukwa1
1
Sokoine University of Agriculture, Department of Ecosystem and Conservation, P.O.
Box 3010, Morogoro, Tanzania,
2
Sokoine University of Agriculture, Department of Crop Science and Production, Box
3005, Morogoro, Tanzania
Abstract
Biological control offer potential solutions against Heteropsylla cubanais economically
feasible and environmentally desirable. The objectives of the study were to quantify
abundance of mummies of Tamarixia leucaenae and Psyllaephagus yaseeni and
percentage of parasitization of H. cubana and to identify indigenous predators of the H.
cubana in Morogoro and Tanga region. The Point Centre Quarter method was employed
to select Leucaena leucocephala for observation. R and Excel program software were
used in data analysis. The mean number of H. cubana mummies of T. Leucaenae and
P. yaseeni were 2.33 and 1.68 in Tanga and 2.64 and 2.1 in Morogoro per 15cm terminal
shoot respectively. This study found rate of parasitism of small nymph and medium
nymph were 0.15% and 0.14% in Morogoro and 0.16% and 0.11% in Tanga of P. yaseeni
and T. leucaenae respectively. The dominant indigenous predators were Neoscona theisi,
Araneus inustus, Coccinella transversalis, Chilocorus circumdatus, Coelophora
inequalis, Menochilus sexmaculatus, Synonycha grandis, Harmonia sp and Chrysoperla
61
sp. This study revealed that T. Leucaenae and P. yaseeni have been established
successfully in Eastern Tanzania. The observed mean mummies was low compared to
previous studies. Farmers are advised to plant L. leucocephala for various use without any
fear about H. cubana as the introduced hymenopterous parasitoids has controlled
H. cubana population. We recommend further investigations to quantify number of
H. cubana preyed on by individual indigenous predators in Tanzania to realize whether
the indigenous predator is potential or not in controlling H. cubana.
Key words: Parasitism, Leucaena leucocephala, Tamarixia leucaenae, Psyllaephagus
yaseeni, Heteropsylla cubanaand Mummies
Introduction
Leucaena leucocephala (Lam.) de Wit is one amongst many multipurpose trees that has
been promoted for fodder production in Tanzania (Lulandala and Hall, 1987). The tree is
found in many parts of Tanzania and usually planted along farm boundaries and in
homesteads for fodder, soil fertility improvement and fuelwood (Msangi et al., 2002).
The outbreak of the devastating Leucaena psyllid, Heteropsylla cubana Crawford
discouraged the spread of leucaena based fodder production technology and many other
uses in the country. Most Leucaena stands were lowered after invasion of H. cubana
(Madoffe et al., 2000). Effort to control H. cubana via biological control in Kenya and
Tanzania, the Asia-Pacific experience was considered the best option (Ciesla and
Nshubemuki, 1995; Madoffe and Petro, 2011). Hymenopterous parasitoids Tamarixia
leucaena Boucek (Hymenoptera: Eulophidae) and Psyllaephagus yaseeni Noyes
(Hymenoptera: Encyrtidae) introduced from Trinidad and Tobago and released in Tanzania
and Kenya are well established in Tanzania, have spread over large areas and they appear to
62
being effective against their hosts (Madoffe et al., 2000; Madoffe and Petro, 2011). T.
leucaenae is a solitary ectoparasitoid that lay eggs behind the hind coxae of third or fourth
instar H. cubana nymphs (Patil et al., 1993). Oviposition by T. leucaenae appears to
inhibit further nymphal development. P. yaseeni is a solitary endoparasitoid which attacks
H. cubana instars first and second, which continue to develop until instar fifth when they
mummify (Patil et al., 1993).
Reduced H. cubana population and Leucaena shoot damage in some areas, could be
attributed to the parasitoids and indigenous predators (Madoffe et al., 2000). However, little
is known on abundance of H. cubana mummies of T.Leucaenae and P. yaseeni and
percentage of parasitization of H. cubana in Africa, including Tanzania (Geiger and
Gutierrrez, 2000). In addition, little has been done to identify the indigenous predators of
the H. cubana in Tanzania and what already reported was not at species level (Kisaka,
1994; Madoffe et al., 2000). Therefore, this study aimed at identifying and determining
the abundance of indigenous predators associated with H. cubana, abundance of H.
Cubana mummies of T. Leucaenae and P. yaseeni and percentage of parasitization of H.
cubanain Morogoro and Tanga.
The study was based on two hypotheses that: (1) There are several indigenous predators
associated with H. cubana; (2) There will be high abundance of H. cubana mummiesof T.
Leucaenae and P. Yaseeni (3) Thereis a high rate of parasitism of H. cubana. This results
from present study will be useful to agroforesters, plant protectionists, conservationists,
livestock keepers, and farmers whom have abandon planting L. leucocephala in the
country to establish and use of Leucaena for multipurpose uses such as a source of fodder,
fuelwood, shade for estate crops, reforestation, timber, erosion control and nitrogen
63
fixation. Also communities will fully understand indigenous predators associated with H.
cubana and look forward to conserve them for present and future generation.
Materials and Methods
Description of study area
Studies were conducted in selected sites of Morogoro and Tanga region, namely;
Morogoro: SUA farm, Melela A and B; Tanga: Mlingano, Tanga dairy farm and Ziwani
(Table 1).These sites were used in 1990s for the release of two H. cubana parasitoids and
later assessed for their spread and establishment (Madoffe et al., 2000). Morogoro region
lies between latitude 5o 58" and 10o 0"to the South of the Equator and longitude 35o 25"
and 35o 30" the East Greenwich with an area of 72, 939 square kilometers of the total
Tanzania mainland and population of 2218492 (MRSEP, 2006; NBS Census, 2012).
Tanga Region is situated at the extreme northeast corner of Tanzania between 4° and 6°
degrees below the Equator and 37° - 39° 10' degrees east of the Greenwich Meridian. The
region occupies an area of 26677 km2 with a population of 2045205 (NBS Census, 2012).
Sampling Design
The Point Centre Quarter method (PCQ) was employed to assess population of H. cubana
and parasitoids, damage rate and shoot health (Marisa, 2015). Five sampling points were
established in each site, where one at center and other four at the corners of site (Figure
2). In each sampling point, four quadrants were established. The adults and regenerants
L. leucocephala near sampling point at each quadrant were sampled and recorded.
L. leucocephala were grouped into two cluster of regenerants (dbh< 1 cm) and adult
species (dbh≥ 1 cm). Adult Leucaena trees were categorized into three dbh classes i.e.,
(1-5 cm), (6-15 cm) and (>15 cm) and then into three crown levels (upper, middle and
64
lower level). In each quadrant, two adults L. leucocephala for each dbh classes and two
regenerants were sampled.
Determining abundance of mummies of T. Leucaenae and P. yaseeni
Data were collected during early morning (05:30-9:00am). One 15cm growing shoot was
randomly selected and sampled from each crown level for adult species and two 15cm
growing shoot of two regenerants in each quadrant. The shoots were carefully cut into a
polythene bag (destructive sampling) and put in a refrigerator to ensure its flesh for
observation. The collected shoots were washed carefully with the help of a brush and
ethanol (70%) into a petri-dish to remove mummies of P. yaseeni and T. leucaenae. In the
Laboratory mummies of P. yaseeni and T. leucaenae were counted under a dissecting
microscope.
Determining abundance of indigenous parasitoids
The collected growing shoots were washed carefully with the help of a brush and ethanol
(70%) into a petri-dish to remove indigenous predators associated with H. cubana. The
laboratory indigenous predators were counted under magnifying hand lens for
identification of indigenous predators to species level.
Data Analysis
R version 3.2.3 and Microsoft excel computer software programs were used in data
analysis. Descriptive statistics were used to determine mean abundance of H. cubana
mummies of P. yaseeni and T. leucaenae and indigenous predators associated with H.
cubana. Analysis of Variance (ANOVA) at 5% level of significance was used to
determine whether the means abundance in H. cubana mummies of P. yaseeni and T.
65
leucaenae between dbh classes and growing sites are different. The percentages of
parasitization were calculated from mummy and 5th-instar counts using the method of
Luck et al. (1988):
Percentage parasitism = (Number of mummies /shoot)
(Correction factor) (Number of fifth instar/shoot
With
Corretation factor = 3.8
Results and discussion
Results
Abundance of Mummies of Tamarixia leucaenae and Psyllaephagus yaseeni
establishment in Morogoro and Tanga regions
The mean numbers of H. cubana mummies of P. yaseeni and T. leucaenae per 15cm
terminal shoot were 2.33 and 1.68 in Tanga and 2.64 and 2.1 in Morogoro respectively
(Table 4). Results showed that the abundance of mummies of Psyllaephagus yaseeni in
Morogoro was not statistically different among crown levels (F=1.21, df=2, P=0.298) and
among dbh classes (F=1.29, df=2, P=0.27) in Morogoro. In Tanga mean numbers of H.
cubana mummies of P. yaseeni were not significantly among crown levels (F=0.448,
df=2, P=0.639) and among dbh classes (F=1.41, df=2, P=0.246). The interaction between
dbh and crown level was not significantly different in both Morogoro (F=1.21, df= 4,
P=0.302) and Tanga (F=0.827, df= 4, P=0.51). The abundance of H. cubana mummies of
T. leucaenae were not statistically different among crown levels (F=1.28, df=2, P=0.278)
and among dbh classes (F=0.98, df=2, P=0.37) in Morogoro. In Tanga H. cubana
mummies of T. leucaenae were not significantly among crown levels (F=0.19, df=2,
66
P=0.82) and among dbh classes (F=1.227, df=2, P=0.294). The interaction between dbh
and crown level was not significantly different in both Morogoro (F=0.928, df= 4,
P=0.447) and Tanga (F=1.101, df= 4, P=0.355). There was high mean numbers of
mummies in regenerants L. leucocephala than in adult L. leucocephala for both
Mean
P. yaseeni and T. leucaenae in Morogoro and Tanga (Figure 15, 16 and 17).
5
4
3
2
1
0
Crown
level
Lower Middle Upper
Lower Middle Upper
Psyllaephagus yaseeni
Tamarixia leucaenae
1–5
6–15
>15
Figure 14: Mean numbers of H. cubana mummies of P. yaseeni and T. leucaenae for
adult L. leucocephala in Morogoro regions
4
Mean
3
2
1
0
Crown
part
Lower
Middle
Upper
Psyllaephagus yaseeni
Lower
Middle
Upper
Tamarixia leucaenae
1–5
6–15
>15
Figure 15: Mean number of H. cubana mummies of P. yaseeni and T. leucaenae for
adult L. leucocephala in Tanga regions
67
12
Mean
10
8
6
4
2
0
Psyllaephagus yaseeni
Parasitoid
Tamarixia leucaenae
Morogoro
Tanga
Figure 16: Mean number of H. cubana mummies of Psyllaephagus yaseeni and
Tamarixia leucaenae for regenerants Leucaena leucocephala in
Morogoro and Tanga regions
Abundance of indigenous predators associated with H. cubanain Morogoro and
Tanga regions
The dominant indigenous predators found were spider (Neoscona theisi and Araneus
inustus) (71.11%) of which about 60.44% observed in Tanga and 10.67% in Morogoro
(Table 6), followed by ladybird beetles (Coccinella transversalis, Chilocorus
circumdatus, Coelophora inequalis, Menochilus sexmaculatus, Synonycha grandis and
Harmonia species) (22.67%) of which 14% in Morogoro and 8.67% in Tanga, un
identified dragonfly (5.11) of which 3.67 in Morogoro and 1.33% in Tanga and lacewing
(Chrysoperla sp.) (1.11%) which was only observed in Morogoro for adult
L. leucocephala (Figure 10 and 11). The almost the same was observed for regenerants as
the predator was spider 37.02% and 22.98%, followed by ladybird beetles 15.74% and
15.74%, dragonfly 2.12% and 5.11% in Tanga and Morogoro respectively while
Lacewing 1.28% was observed in Morogoro only for regenerants L. leucocephala.
68
Parasitism Percentage of H. cubanain Morogoro and Tanga regions
The result found rate of parasitism of small nymph and medium nymph for adults
L. leucocephala were 0.15% and 0.14% in Morogoro and 0.16% and 0.11% in Tanga for
P. yaseeni and T. leucaenae respectively (Table 7). The rate of parasitism of small nymph
and medium nymph for regenerants L. leucocephala were 0.47% and 0.41% in Morogoro
and 0.47% and 0.31% in Tanga of P. yaseeni and T. leucaenae respectively.
Results showed that rate of parasitism of small nymph by P. yaseeni was not statistically
significant different among dbh classes in Morogoro (F= 0.478, df=2, P=0.621) and in
Tanga (F= 2.95, df=2, P=0.055). The rate of parasitism of medium nymphs was
significantly different among dbh classes in Tanga (F=3.07, df=2, P=0.049) but not in
Morogoro (F=0.495, df=2, P=0.610). The rate of parasitism of small nymph and medium
nymph for regenerants were high compared to adult L. leucocephala (Table 7).
Table 5: Percentage of parasitization of H. cubana for adult L. leucocephala in
Morogoro and Tanga regions
Region
dbh classes
Morogoro
1–5
6–15
>15
Mean total
1–5
6–15
>15
Mean total
Tanga
% Parasitism
Psyllaephagus yaseeni
Tamarixia leucaenae
0.16
0.14
0.16
0.13
0.13
0.16
0.15
0.14
0.18
0.12
0.14
0.09
0.12
0.08
0.16
0.11
Discussion
The study found low mean mummies compared to that reported by Madoffe et al. (2000),
which was 10 and 11 mummies per growing shoot in Tanga and Morogogro respectively.
69
The decline in mummies were due to the decline of H. cubana population as a result of
role played by P. yaseeni and T. leucaenae, indigenous predators and environmental
factors. The trend of mummies for both P.yaseeni and T. leucaenae in the three dbh
classes and localities were not different from that of H. cubana population for both
regenerants and adults L.leucocephala. The low abundance of both H. cubana and
mummies in Tanga were due to unfavourable climatic condition which does not support
H. cubana production. This concur with other studies which shows that H. cubana
population is affected by temperature, moisture, humidity and exposure to wind (Ahmed
et al., 2014; Geiger and Andrew, 2000; McAuliffe, 2008) and the ups and downs of the
psyllid populations which in turn affect mummies production are related to an optimum
cooler temperature range and the availability of tender shoots in Hawaii (Ahmed et al.,
2014).
This study found a low rate of parasitism compared to 0.23% using mummy count
reported by Geiger and Andrew (2000). The low rate of parasitism was due to few host
available for parasitism. At both localities, parasitism rates showed increased with nymph
density which was different from that of Geiger and Andrew (2000), that parasitism
increased with no density. The low parasitism rates 0.18%-0.08% (Table 3) of the H.
cubana population in this study were similar to those observed in Hawaii (Uchida et al.,
1992) and appear insufficient to suppress psyllid populations. After exposing T.leucaenae
to psyllid nymphs in quarantine, only one parasitized nymph was obtained and the entire
culture eventually perished. As a result, there was no further attempt to utilize this species
in Thailand (Napompeth, 1994). Tamarixia radiata Waters on was introduced from
Reunion to Taiwan between 1984 and 1988 for control of Diaphorina citri Kuwayama
and has caused a substantial reduction in populations of the psyllid, with up to 100%
70
parasitism recorded (Chien et al., 1989). The current study revealed that the found
indigenous predators associated with H. cubana are similar with previous studies
reported. Indeed, the study did not prove that these indigenous natural enemies were
feeding on the psyllid, consequently contributing to the declining psyllid population.
Madoffe et al. (2000) found several arthropod natural enemies living in association with
the H. cubana being spiders, ladybird beetles, ants, dragonflies and lacewings. In contrast
to this study, ants were not found in association with H. cubana. The found indigenous
predators were reported as important predators in South East Asia Pacific Region and
Central America and (Ahmed et al., 2014, Nakahara et al., 1987; McClay, 1990;
Napompeth, 1994) although there is still no quantitative evidence on the role of
indigenous predators against H. cubana (Shivankar et al., 2010).
The study by Geiger and Andrew (2000) were reported predominant coccinellid predators
at all study sites were Menochilus sexmaculatus (F.), followed by Oenopia sauzeti
Mulsant and O.kirbyi Mulsant (highland site only) and Micraspisdiscolor (F.). Coccinella
transversalis F. and Micraspis lineata (Thunberg) were occasionally observed at the
valley site. Numerous spider and dragonfly species, 4 species of ants, vespid wasps,
syrphids, reduviids, mirids, 1 Geocoris species and lacewings were also observed preying
on H. cubana, but they were not abundant. This concur with current study found in
Morogoro and Tanga.The study revealed a positive relationship and statistically
significant between population density of H. cubana and mummies of T.leucaenae and
P.yaseeni establishment in Tanga and Morogoro, which means that the high population
density of H. cubanawas related to the mummification.
71
Conclusions
This study has shown that T. leucaenae and P. yaseeni has been established successfully
in Eastern Tanzania, despite the fact that P. yaseeni were neither released in Tanga nor
Morogoro. Mummies population found lower significantly compared to what was
reported soon after the release of the T. leucaenae and P. yaseeni in 1995/1996. The
findings from the present study revealed that dominant indigenous predators of H. cubana
in Tanzania are Neoscona theisi, Araneus inustus, Coccinella transversalis, Chilocorus
circumdatus, Coelophora inequalis, Menochilus sexmaculatus, Synonycha grandis,
Harmonia species, Chrysoperla species and several unidentified dragonfly and mantispid.
Recommendations
Farmers are advised to plant L. leucocephala for various use without any fear about H.
cubana as T. leucaenae and P. yaseeni has significantly manipulate psyllid’s population.
Due to time constraint this study has not manage to assess the temporal nature of both
mummies of T. leucaenae and P. yaseeni, further investigation is recommended. Also,
other investigation should look on the effect of abiotic factors such as rainfall,
temperature, wind velocity and others onmummies of T. leucaenae and P. yaseeni. The
amount of H. cubana preyed by found indigenous predators and predator dynamics is not
well known. Further investigation should look on the interaction of indigenous predators
and H. cubana.
72
References
Ahmed, A.M., Avilés1, L.R., Sánchez, F.J., Zyoud, F.A and Rodriguez1, M.B. (2014).
An Overview on some biotic and abiotic factors affecting the population
dynamics of Leucaena psyllid, Heteropsylla cubana Crawford (Homoptera:
Psyllidae): Contributory factors for pest management. Tropical and
Subtropical Agroecosystems 17: 437 – 446.
Alao, J.S., Sale, F.A. and Ojo, A.S. (2011). Problems and management of insect pests in
social forestry in Nigeria. African Journal of Agricultural Research 6 (33):
6755 – 6758.
Austin, M.P., Williams, M.J., Hammond, A.E., Frank, J.H., Chambliss, C.G. (1996).
Psyllid population dynamics and plant resistance of leucaena selections in
Florida. Tropical Grasslands 30: 223-228.
Bray, R.A. (1994). The Heteropsylla cubana. In: Gutteridge R.C. and Shelton, H. M.
(Eds.). Forage Tree legumes in Tropical Agriculture. CAB International,
Oxford. pp. 283 -291.
Bray, R.A. and Woodroffe, T.D. (1988). Resistance of some Leucaena species to the
Heteropsylla cubana. Tropical Grasslands Journal 22: 11–16.
Brewbaker, J.L. and Sorensson, C.T. (1990). New tree crops from interspecific Leucaena
hybrids. In: Janick, J. and Simon, J.E. (Eds), Advances in New Crops, Timber
Press, Portland, Oregon. 283 – 289pp.
73
Burkhardt,
D.
(1986).
Nomenclatural
note
on Heteropsylla
cubana Crawford
(Homoptera: Psylloidea), a new pest in Pacific Countries. Revue suisse de
Zoologie 93(4): 1023 -1024.
Bruzas, W.A. (1983). The Pine Woolly Aphid (Pineus pini) and Associated Insects in Pine
Plantations. Internal Report. PPRI, Department of Agriculture and Water
Supply, Pretoria. 37pp. Castillo, A. E., Cuyagan, O. E., Fogarty, S., Shelton,
H. M. (1997). Growth, psyllid resistance and forage quality of Leucaena
leucocephala, L. pallida, L. diversifolia and the Fl hybrid of L. leucocephala x
L. pallid .Tropical Grasslands 31: 188 – 200.
Ciesla, W.M and Nshubemuki, L. (1995). Heteropsylla cubana: A threat to agroforestry
in Africa. A Proceeding of a workshop held in Dar-es-Salaam, Tanzania, 1014 October 1994, Rome FAO. 237pp.
Chien, C.C., Chiu, S.C. and Ku, S.C. (1989). Biological control of Diaphorina citrii in
Taiwan. Fruits 44: 401 – 407.
Edward, E., Chamshama, S.A.O. and Mugasha, A.G. (2006). Growth performance of
Lesser-known Leucaena species/provenances at Gairo inland plateau,
Morogoro, Tanzania. Southern African Forestry Journal 208: 53 – 62.
FAO (2001). Protecting plantations from pests and diseases. Report based on the work of
W. M. Ciesla. Forest Plantation Thematic Papers, Working Paper 10. Forest
Resources Development Service, Forest Resources Division. FAO, Rome.
34pp.
74
FAO. (2007). Overview of forest pests Kenya. Forest Health and Biosecurity Working
Papers. Rome, Italy. 26pp.
Geiger, C.A. and Andrew, P.G. (2000). Ecology of Heteropsylla cubana (Homoptera:
Psyllidae): Psyllid Damage, Tree Phenology, Thermal Relations and
Parasitism in the Field. Environmental Entomology 29: 76 – 86.
Geiger, C.A., Napompeth, B. and Van Den Beldt, R.J. (1995). An update on the status of
the Heteropsylla cubana in Southeast Asia. In: Shelton H.M., Piggin, C.M.
and Brewbaker, J.L. (Eds.). Leucaena: Opportunities and Limitations.
Canberra: Australian Centre for Agricultural Research. 8-125pp.
Hughes, C.E. (1998). Leucaena - A genetic resources handbook. Oxford Forestry
Institute, Tropical Forestry Paper No. 37. Oxford, UK. 274pp.
Kisaka, E.Z. (1994). Incidence of forest pest in Tanzania a special reference to the
Heteropsylla cubana. In: Sub-Regional Workshop on Heteropsylla cubana: a
threat to agroforestry in Africa (Edited by Ciesla, W. and L. Nshubemuki), 1014 October 1994. Dar es Salaam, Tanzania. 236pp.
Krishnamurthy, K., Munegowda, M. R. and Rajagopal, D. (1989). Outbreak of psyllid,
Heteropsylla cubana Crawford, on Leucaena and its outlook in alley cropping
in India. In: Proceedings of an international workshop held January 16-21,
1989 in Ogor, Indonesia. 17 – 24pp.
Larsson, S. (1989). Stressful times for the plant stress insect performance
hypothesis. Oikos 56: 277-283.
75
Lulandala, L.L. and Hall, J.B. (1987). Fodder and wood production from Leucaena
Leucocephala intercropped with maize and beans at Mafiga, Morogoro,
Tanzania. Forest Ecology and Management 21: 109 – 117.
Johansson, A. (1994). Effect of Heteropsylla cubanaon women’s enterprises. A case of
Morogoro In: Sub Regional Workshop on Heteropsylla cubana: a threat to
agroforestry in Africa. (Edited by Ciesla, M. and L. Nshubemuki), 10-14
October 1994, Dar es Salaam, Tanzania. 40 - 47pp.
Madoffe, S.S. and Massawe, A. (1994). Periodicity of Heteropsylla cubana
nfestation on
Leucaena leucocephala
growing in Morogoro:
Preliminary observations. In: Heteropsylla cubana "A threat to
Agroforestry in Africa. (Edited by W.Ciesla and L.Nshubemuki), Dares - Salaam, Tanzania. 155 – 161pp.
Madoffe, S.S., Muhundo, L., Day, R.K. and Nshubemuki, L. (2000). The pontential of
Classical biological control against Leucaena psyllid (Heteropsylla cubana
Crawford) in Eastern Tanzania. Tanzania Journal of Agricultural Science 3:
113 - 122.
Madoffe, S.S., Ngoo, A.G. and Tarimo, J. (2001). The influence of induced shading in
Leucaena leucocephalla seedlings on Heteropsylla cubana. Tanzania Journal
of Forestry and Nature Conservation 74: 39-51.
76
Madoffe, S.S. and Petro, R. (2011). Status of forest insect pests in Tanzania: Introduction,
Spread, Damage and Management Options. In: L. Nshubemuki, S.S. Madoffe,
S.A.O. Chamshama, S. Bakengesa and C. Balama. (eds). In: Preceedings of
the Workshop on Insect pests, Diseases and Soil Problems in Forest
Plantation held at the Kibaha Conference Centre, Kibaha, Tanzania, 3 to 4
February, 2011. Tanzania Forest Research Institute, Tanzania. 2-16pp.
Marisa, H. (2015). Application of Point-Centered Quarter Method for Measurement the
Beach Crab (Ocypode spp) Density. Biological Research Journal 1: 1- 6pp.
McAuliffe, M. (2008). Investment Opportunity: New PBR Leucaena variety. A full
information
package
is
available
from
Melissa
McAuliffe
[http://
www.leucaena.net/pr_info_pack.pdf] site visited on 9/3/2015.
Ministry of Planning, Economy and Empowerment (2006). Morogoro Region Socio
Economic
Profile
(MRSEP)
Ministry
of
planning,
economy
and
empowerment. Dar es Salaam, Tanzania. 122pp.
Msangi, R.B., Otsyina, R. and Kusekwa, M.L. (2002). Evaluation of lesser known
Leucaena Species/Provenances and hybrids for fodder production and psyllid
tolerance at Tabora and Shinyanga, Tanzania. In: Proceedings of theRegional
Agroforestry Conference on Agroforestry Impactson livelihoods in Southern
Africa: Putting Research intoPractices. (Edited by Rao, M. R. and Kwesiga,
F. R). 20 – 24 May 2002, Aventura Resorts, Warmbaths South Africa. 181187pp.
77
Mullen, B.F., Gabunada, F., Shelton, H.M, Stur, W.W. and Napompeth, B. (1998).
Psyllid resistance in Leucaena. In: Australian Centre for International
Agricultural Research Proceedings. (Edited by Shelton, H. M., Gutteridge, R.
C., Mullen, B.F. and RA Bray, R.A.). Adaptation, Quality and Farming
Systems Workshop 9 – 14 February 1998. 86: 51 – 60.
Mullen, B.F and Shelton, H.M. (2003). Psyllid resistance in Leucaena.Part 2.
Quantification of production losses from psyllid damage. Agroforestry Systems
58:163 − 171.
Nair, K.S.S. (2007). Tropical Forest Insect Pests. The United States of America by
Cambridge University Press, New York. 263pp.
Napompeth, B. (1994). Heteropsylla cubanain the Asia-Pacific region: implications for
its management in Africa. In: Heteropsylla cubana: a Threat to Agroforestry
in Africa. FAO Corporate Document Repository Food and Agriculture
Organization of the United Nations, Rome, Italy. pp. 1–15.
National Bureau of Statistics, NBS. (2012). Population and Housing Census: Population
Distribution by Administrative Areas. Project Report. National Bureau of
Statistics.
NFTA. (1988). Heteropsylla cubana - A Review of the Problem and its Solutions.
[http://factnet.winrock.org/fnrm/factnet/factpub/FACTSH/L_psyllids.html].
Site visited on 15/07/2015.
78
Ogol, C. and Spence, J. R. (1997). Abundance, population dynamics and impact of the
Leucaena psyllid, Heteropsylla cubana Crawford in a maize-Leucaena
agroforestry system in Kenya. Insect Science and its Application 17: 183 – 92.
Patil, N.G., Baker, P.S. and Pollard, G.V. (1993). Life histories of Psyllaephagus
yaseeni (Hymenoptera, Encyrtidae) and Tamarixia leucaenae (Hymenoptera,
Eulophidae), parasitoids of the Leucaena psyllid,Heteropsylla cubana.
Entomophaga 38: 565 – 577.
Petro, R. (2009). Status of pine woolly aphid (Pineus boerneri) in Sao Hill Forest
Plantation, Southern Highlands, Tanzania (Unpublished Master’s thesis).
Sokoine University of Agriculture, Morogoro, Tanzania.
San Valentin, H. (1988). Seasonal abundance, distribution and host range of psyllid
infesting
Ipil-ipil.
[http://erdb.denr.gov.ph/enr/i4d/i4d_fo_psy.pdf.]. Site
visited on 15/04/2015.
Sharma, J.K. and Sankaran, K.V. (1988). Incidence and severity of Botryodiplodia
dieback in plantations of Albizia falcataria in Kerera, India. For Ecological
Management 24: 43 – 58.
Shelton, H.M. (2008). Psyllid-resistant Leucaena hybrid for northern Australia. Meat and
Livestock Australia Limited, Australia. 1 – 40pp.
79
Shivankar, V.J. and Rao, C.N. (2010). Psyllids and Their Management. Pest Management
in Horticultural Ecosystems 16: 1 – 4.
Showler, A.T. and Melcher, J. (1995). Environmental assessment for implementation of
biological control for the Leucaena psyllid in Asia and Africa. Washington,
D.C.: U.S. Agency for International Development. 18pp.
Soon, U., Lin, T. and Chee, W. (1989). Studies on Leucaena psyllidin Malaysia.
Proceedings of an international workshop held January 16-21, 1989 in Ogor,
Indonesia. 28 – 39pp.
Sorensson, C. and Brewbaker, I.L. (1987). Psyllid resistance of Leucaena hybrids and
Species in Leucaena Research Report 7 (2): 29 – 31.
Speight, M.R. and Wainhouse, D. (1989). Ecology and Management of Forest insects.
Clarendon Press. Oxford. 373pp.
Swai, E., Karimuribo, E., Schoonman, L., French, N., Fitzpatrick, J., Kambarage, D. and
Bryant, M. (2005). Description, socio-economic characteristics, disease
managements and mortality dynamics in smallholder's dairy production
system in coastal humid region of Tanga, Tanzania. Livestock Research for
Rural Development17: 4 - 8.
Uchida, G., Beardsley, J., Reimer, N. and Wheeler, R. (1992). Comparison of Populations
of Heteropsylla cubana Crawford (Homoptera: Psyllidae) and its Parasitoids
on Seven Accessions of Leucaena (Leguminose: Mimosoideae) in Hawaii.
Hawaiian Entomological Society 31: 97 – 107.
80
CHAPTER FOUR
4.0
CONCLUSIONS AND RECOMMENDATIONS
4.1
Conclusions
Based on the findings from this study the following conclusions are made;
i.
The mean number of H. cubana population density was very low compared to
other studies due to role played in combination of Tamarixia leucaenae and
Psyllaephagus yaseeni, indigenous predators and environmental factors.
ii.
The study has found good shoot health and slightly infestation to Leucaena
leucocephala as a result of low population density of H. cubana.
iii.
This study has shown that T. Leucaenae and P. yaseeni has been established
successfully in Eastern Tanzania, despite the fact that P. yaseeni were neither
released in Tanga nor Morogoro.
iv.
The study has found low psyllid mummies compared to what was reported soon
after the release of the T. Leucaenae and P. yaseeni in 1995/1996.
4.2 Recommendations
Based on the results from this study and experiences from other studies, it is
recommended that;
i.
Farmers should now again plant L.leucocephala for various use without any fear
about H. cubana as its population is no longer a problem.
ii.
Farmers and others who practice agroforestry should conserve the found
indigenous predators in order to continue keeping in check H. cubana population
in checkfor present and future generation.
81
iii.
Further study should be conducted on what extent found indigenous predators
consume H. cubana as well as the status of H. cubana to other localities where T.
Leucaenae and P. yaseeni were not released.
iv.
Since, due to time constraint this study has not manage to assess the temporal
nature of both H. cubana, mummies of T. Leucaenae and P. yaseeni, further
investigation should look on this.
v.
Also, other investigation should look on the effect of abiotic factors such as
rainfall, temperature, wind velocity and others on both H. cubana and T.
Leucaenae, P. yaseeni as well as indigenous predators. Additionally, studies on
indigenous predators dynamics is highly recommended.
Paulo Lyimo