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Biological performance ofDiclidophlebia smithi (Hemiptera:Psyllidae), a potential biocontrolagent for the invasive weed MiconiacalvescensElisangela Gomes Fidelis de Morais a , Marcelo Coutinho Picançoa , Robert Weingart Barreto b , Nilson Rodrigues Silva a & MateusRibeiro Campos aa Department of Animal Biologyb Department of Fitopathology, Federal University of Viçosa,36570-000, Viçosa, Minas Gerais, CEP, 36570-000, BrazilPublished online: 14 Dec 2009.
To cite this article: Elisangela Gomes Fidelis de Morais , Marcelo Coutinho Picanço ,Robert Weingart Barreto , Nilson Rodrigues Silva & Mateus Ribeiro Campos (2010) Biologicalperformance of Diclidophlebia smithi (Hemiptera: Psyllidae), a potential biocontrol agent forthe invasive weed Miconia calvescens , Biocontrol Science and Technology, 20:1, 107-116, DOI:10.1080/09583150903428711
To link to this article: http://dx.doi.org/10.1080/09583150903428711
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RESEARCH ARTICLE
Biological performance of Diclidophlebia smithi (Hemiptera: Psyllidae),a potential biocontrol agent for the invasive weed Miconia calvescens
Elisangela Gomes Fidelis de Moraisa,*, Marcelo Coutinho Picancoa,
Robert Weingart Barretob, Nilson Rodrigues Silvaa and
Mateus Ribeiro Camposa
aDepartment of Animal Biology, and bDepartment of Fitopathology, Federal University ofVicosa, 36570-000, Vicosa, Minas Gerais, CEP 36570-000, Brazil
(Received 31 March 2009; returned 19 May 2009; accepted 20 October 2009)
Diclidophlebia smithi Burckhardt, Morais and Picanco (Hemiptera: Psyllidae) is apromising biological control agent of Miconia calvescens DC. (Melastomataceae),a neotropical invasive weed in forest ecosystems in French Polynesia and Hawaiiand a threat in Australia, where it was also introduced. A study on thereproductive performance of D. smithi under laboratory conditions through lifeexpectancy and fertility tables is presented. Results indicated that this psyllid hasa high reproductive capacity (R0�1 and rm�0) and a short life cycle (46�47 days)and can have up to nine generations per year. The critical period of its life cycle isduring the nymphal stage which is clearly inadequate for field introductions. Thebest age for introducing D. smithi against M. calvescens is the 4th day of the adultstage. D. smithi is easily mass-reared and has a short life cycle and a highreproductive capacity, which are desirable characteristics for a biological controlagent.
Keywords: psyllid; weed; life tables; mass-rearing; Melastomataceae
Introduction
Miconia calvescens DC. (Melastomataceae) (common names: ‘cancer vert’ and velvet
tree) is among the world’s worst invasive species (International Union for
Conservation of Nature 2008). Invasion by this plant is a threat to several humid
forests ecosystems throughout the world, but impact has been particularly severe on
oceanic islands, such as French Polynesia (Gagne, Loope, Medeiros, and Anderson
1992; Meyer 1996; Medeiros, Loope, Conant, and Mcelvaney 1997), and Hawaii,
(Csurhes 1997). M. calvescens is native to humid tropical forests of Central and
South America, where it is not considered a weed. It is neither abundant nor
common, due to competition with other plant species and heavy damage from its
natural enemies, mainly arthropods and plant pathogens. Numerous insect species
feeding on this plant were found during systematic surveys in selected areas in Brazil
(Picanco et al. 2005; Seixas, Barreto, and Killgore 2007).
Classical biological control is probably the only sustainable way of controlling
these invasive populations. Preliminary surveys of arthropods attacking
*Corresponding author. Email: [email protected]
ISSN 0958-3157 print/ISSN 1360-0478 online
# 2010 Taylor & Francis
DOI: 10.1080/09583150903428711
http://www.informaworld.com
Biocontrol Science and Technology,
Vol. 20, No. 1, 2010, 107�116
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M. calvescens were conducted in Brazil, Costa Rica and Trinidad from 1993 to 1995
and several arthropods and pathogens were collected and illustrated. Robert
Burkhart, Hawaii Department of Agriculture’s exploratory entomologist involved
in the surveys, was pessimistic about the potential of the many arthropods he found
as biocontrol agents (C. Smith, personal communication) and attention was then
concentrated on the exploitation of pathogens. In 1995, a search for M. calvescens
pathogens native to the neotropics was initialiated. Selected areas in Brazil, Costa
Rica and Ecuador were surveyed and numerous pathogens were found, including a
phytoplasm, two species of nematodes Ditylenchus and one oomycete Pythium sp.
(Seixas, Barreto, and Matsuoka 2002; Seixas, Barreto, Freitas, Maffia, and Monteiro
2004; Seixas et al. 2007).Until recently, only one natural enemy has been released for a classical biological
control of M. calvescens. The fungus Colletotrichum gloeosporioides f. sp. miconiae
was introduced into Hawaii in 1997 (Killgore, Sugiyama, and Barreto 1997) and into
French Polynesia in 2001, contributing to the control of miconia to some extent
(particularly in French Polynesia) (Meyer, Taputuarai, and Killgore 2007). There-
fore, it is now clear that additional agents will be required to provide an effective
control of this weed.
In the early 2000s, there was renewed interest in arthropod natural enemies of
miconia and more intensive surveys were performed both in Brazil (Burckhardt,
Morais, and Picanco 2006) and in Costa Rica. Coincidentally, among the numerous
insect species collected on miconia in both countries were two closely related species
of psyllids: Diclidophlebia smithi Burckhardt, Morais and Picanco (Hemiptera:
Psyllidae) in Brazil (Burckhardt et al. 2006) and D. lucens Burckhardt, Hanson and
Madrigal in Costa Rica (Burckhardt, Hanson, and Madrigal 2005). Psyllid species
initially were regarded as among the most promising agents to be used against this
weed (Picanco et al. 2005; Burckhardt et al. 2006).
Diclidophlebia smithi is a new species recently described by Burckhardt et al.
(2006) and then selected for further studies. This psyllid is a member of the possibly
monophyletic species group associated with Melastomataceae and appears to be
widely distributed in south-eastern Brazil. Specificity tests demonstrate that D.
smithi is unable to develop on any of the Melastomataceae species: Clidemia
capitellata, C. hirta, Miconia mendoncaii, M. albicans, M. ibaguenscens, Leandra
lacunosa, Ossala confertiflora, Tibouchina granulosa and T. moricandiana. In
addition, D. smithi colonies were found on plants neighboring M. calvescens plants
in the forests of Dionısio, Guaraciaba and Vicosa. This species was found in
Dionısio, Guaraciaba and Vicosa (state of Minas Gerais) and also in Mangaratiba
and Ilha Grande � Angra dos Reis (state of Rio de Janeiro) (Burckhardt et al. 2006).
After an insect has been identified as a potential biological control agent, life
history studies are necessary (Harley and Forno 1992). Life tables are used as tools
for evaluating a potential biological control agent. From life history studies it is
possible to elucidate the development, survival and fertility patterns of the insects.
Constructing life tables is an important aid for understanding the insect’s population
dynamics. They also provide data on a population’s mortality and survival rates.
Fertility life tables provide a way to express, in numeric form, the main
characteristics of the specific mortality for each age (Rabinovich 1978), and the
reproductive capacity of a population (Price 1997). From life tables, it is possible to
108 E.G.F. de Morais et al.
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determine the best age for introducing a natural enemy and the critical periods in its
life cycle.
This paper includes part of the results of the investigation conducted with
D. smithi in Brazil and focuses on the reproductive performance of this psyllidthrough life expectancy and fertility tables.
Materials and methods
Life and fertility life table data of D. smithi were obtained during two generations,
the first was from September 3 to October 20, 2005 and the second was from July 24
to September 8, 2006. Studies were performed in a rearing room of the ‘Laboratorio
de Manejo Integrado de Pragas’ of the Universidade Federal de Vicosa. During theexperiments, air temperature, relative humidity and photoperiod were not controlled
but were monitored daily. Although the environment in rearing room was not
controlled, it did not vary much. The rearing room was under natural light and the
photoperiod was calculated using an equation that relates sun declination and
latitude (Smithsonian Institution 1963). Mean environmental conditions during the
first generation of studies were: 20.490.38C, relative humidity 77.391.2% and
photoperiod 12.190.04 h light. For the second generation they were: 17.690.38C,
relative humidity 7991.0% and photoperiod 11.390.03 h light.Twenty pairs of day-old D. smithi were placed on five M. calvescens seedlings
(four pairs per seedling). These seedlings were 80�100 cm tall and were from seeds
which were collected in the field and germinated in a box with sand. When seedlings
were more or less 10 cm tall, they were transplanted to pots full of soil with a
capacity of five liters. Before transplanting, each pot received 50 g of 4-14-8 mineral
fertilizer (N-P-K) and these seedlings were irrigated daily.
Adults of D. smithi were obtained from nymphs collected from the field and
maintained on M. calvescens seedlings until adult emergence. The number of eggs,females and males were counted daily and the hatching rate was also evaluated.
Thirty emergent nymphs were individually transferred with a thin brush to buds
collected from mature M. calvescens plants in the field. These buds were maintained
with their petioles immersed in glass dishes containing 100 mL of water distiled. The
majority of these buds remained in good condition throughout the study but in case
a bud senesced; nymphs were transferred to fresh organs. The instar of each nymph
and their survival were recorded daily. The eggs and the nymphs of first and second
instars were counted with the aid of a hand magnifying glass at 10� magnification.Instar development was determined by the presence of exuviae, nymphal
coloration (usually yellow after ecdysis) and size (data given in Burckhardt et al.
2006). Young adults were sexed and sex ratio was determined. Females and males
were easily separated because females have a visible ovipositor on the end of
abdomen and are larger.
Life expectancy and fertility life tables
Life expectancy tables were constructed from the survival data, according to the
methods described by Southwood and Henderson (2000) and Price (1997). Graphs
of life expectancy (ex) and mortality (100qx) over time (days) for each life cycle
studied were prepared with the life expectancy tables.
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Fertility tables were constructed according to the procedure described by
Southwood and Henderson (2000) and Price (1997). Regression analysis of survival
and reproductive rate over time (days) were made separately for both life cycles.
Results
Generation time (T) of D. smithi was 37.69 days during the first generation and
35.54 days in the second. The time necessary for the population, starting from adults,
to double in number was 9.75 days in the first generation and 7.86 in the second
(Table 1).
Table 1. Diclidophlebia smithi (Hemiptera: Psyllidae) fertility life table in the first and second
generations, in Vicosa (state of Minas Gerais, Brazil).
Stage x lx mx mxlx xmxlx
First life cycle
Egg
0 1.00 0.00 0.00 0.00
3 1.00 0.00 0.00 0.00
6 1.00 0.00 0.00 0.00
8 1.00 0.00 0.00 0.00
First instar9 0.87 0.00 0.00 0.00
11 0.78 0.00 0.00 0.00
Second instar12 0.73 0.00 0.00 0.00
14 0.73 0.00 0.00 0.00
Third instar15 0.70 0.00 0.00 0.00
18 0.67 0.00 0.00 0.00
Fourth instar19 0.67 0.00 0.00 0.00
22 0.50 0.00 0.00 0.00
25 0.37 0.00 0.00 0.00
Fifth instar26 0.37 0.00 0.00 0.00
30 0.37 0.00 0.00 0.00
Adult
31 0.37 0.00 0.00 0.00
33 0.37 0.69 0.25 8.38
34 0.37 3.08 1.13 38.36
37 0.37 6.92 2.54 93.92
39 0.37 4.00 1.47 57.20
42 0.37 0.85 0.31 13.03
45 0.33 0.17 0.06 2.54
47 0.07 0.00 0.00 0.00
GRR�39.78, R0�14.58, T�37.69 days, DT�9.75 days, rm�0.07 and l�1.07
Second life cycle
Egg0 1.00 0.00 0.00 0.00
3 1.00 0.00 0.00 0.00
7 1.00 0.00 0.00 0.00
First instar8 1.00 0.00 0.00 0.00
11 0.80 0.00 0.00 0.00
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Diclidophlebia smithi began to lay eggs at 33 days of age in the first generation
and at 31 days in second generation. The gross reproductive rate (GRR) was higher
in the second generation (47.46 females/female) as compared to the first (39.78
females/female). Net reproductive rate (R0), which represents how much the
population increased during a generation, was also higher in the second generation
(22.97) compared to the first (14.58) (Table 1).
The intrinsic (rm) and finite rates of increase (l) were 0.07 and 1.07 during the
first generation and 0.09 and 1.09 in the second, respectively. These values of l�1
indicate the population was increasing. In other words, it means that the birth rate
was higher than the death rate in the population (Table 1).The survival curve of D. smithi had four phases in both generatons. The first
phase occurred during the egg stage and began at the first instar, when there was no
mortality observed. This phase lasted until the 8th day in the first generation and 9th
day in the second. Mortality between the first and second phases was due to the
failure of egg eclosion (8%). The second phase corresponded to the first, second,
third and fourth instars, when survival rate was 37% of individuals in the first
generation (lx�2.5�0.32x�0.02x2�0.0004x3, R2�0.98, F�262.6, pB0.0001)
and 53% in the second (lx�1.95�0.16x�0.07x2�0.0001x3, R2�0.96, F�92.96,
pB0.0001). This phase lasted from the 8th to the 25th day in the first generation and
from the 9th to the 23rd day in the second. The third phase corresponded to the fifth
instar and half the adult stage, when mortality was zero. This phase lasted from the
Table 1. (Continued).
Stage x lx mx mxlx xmxlx
Second instar12 0.80 0.00 0.00 0.00
14 0.72 0.00 0.00 0.00
Third instar15 0.72 0.00 0.00 0.00
18 0.58 0.00 0.00 0.00
Fourth instar19 0.56 0.00 0.00 0.00
22 0.54 0.00 0.00 0.00
Fifth instar23 0.52 0.00 0.00 0.00
26 0.52 0.00 0.00 0.00
28 0.52 0.00 0.00 0.00
Adult
29 0.52 0.00 0.00 0.00
31 0.52 0.20 0.10 3.22
32 0.52 4.00 2.08 66.56
35 0.52 8.00 4.16 145.60
38 0.48 5.00 2.40 91.20
41 0.20 1.00 0.20 8.20
43 0.14 0.46 0.06 2.75
46 0.04 0.00 0.00 0.00
GRR�47.46, R0�22.97, T�35.54 days, DT�7.86 days, rm�0.09 and l�1.09
x�Age (days). Lx�Number of surviving females in the beginning of each x. mx�Number of femaleprogeny per female in interval of age x. GRR� Gross reproductiverate. R0�Net reproductive rate.T�Generation time (days). DT� Necessary time for the population to double in number of individuals(days). rm�Intrinsic rate of increase. l�Finite rate of increase.
Biocontrol Science and Technology 111
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25th to 44th day in first generation and from the 23rd to 37th day in the second. The
fourth round corresponded to the end of the adult stage, when after the 44th day in
the first generation (lx�4.8�0.1x, R2�0.97, F�84.4, pB0.0027) and the 37th day
in the second generation (lx�8.85�0.36x�0.04x2, R2�0.97, F�154.21, pB
0.0001) all individuals died (Figure 1).Oviposition by female D. smithi in the first generation commenced on the
31st day and finished on the 45th day, with the highest oviposition on the 37th
day (/mx�6:43e(�0:5((x�37:11)=2:39)2); R2�0.91, F�68.27, pB0.0001). In the second
Figure 1. Survival rate (lx) and cumulative number of female eggs.female�1 day�1 (mx) of
Diclidophlebia smithi (Hemiptera: Psyllidae) during its first (A) and second generations (B).
Vicosa, Minas Gerais State, Brazil.
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generation, oviposition occurred from the 29th to 45th day and the highest
egg deposition was on the 35th day (/mx�6:73e(�0:5((x�35:41)=2:89)2); R2�0.90,
F�31.35, pB0.0001). Survival curves and reproduction rate intercepted
on the 34th day in the first generation and the 32nd day in the second generation.
This corresponded to the fourth day after adult emergence in both generations
(Figure 2).
Diclidophlebia smithi exhibited its highest mortality during the fourth instar in
both generations, and this is considered as the critical period (Figure 2).
Figure 2. Life expectancy (ex) and mortality (100qx) of Diclidophlebia smithi (Hemiptera:
Psyllidae) during its first (A) and second generations (B). Vicosa, Minas Gerais State, Brazil.
Biocontrol Science and Technology 113
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Discussion
Life table parameters obtained in this study provide useful information on the
biology and the biocontrol potential of the psyllid D. smithi. Reproductive
parameters obtained from both fertility life tables of D. smithi (R0�1 and rm�0)
showed that this species has a high potential for population growth in areas of
intended introduction for biological control of M. calvescens. This psyllid can
increase its population size 110�147 times during a year. Time necessary for the
population to double in number (DT) also indicated that even in milder seasons, this
psyllid can produce up to nine generations within a year. Other studies have shown
the reproductive capacity of psyllids generally is extremely high (e.g., Mehrnejad
2001; Mehrnejad and Copland 2005; Center et al. 2006), which is a positive factor
that can lead to success in weed biological control. The high reproductive potential is
also a cause of difficulty for control of pest psyllids (e.g., Mehrnejad 2001). The high
reproductive capacity of psyllids has contributed to success of this insect group in
biological control of weeds (e.g., Center et al. 2006; Shaw, Bryner, and Tanner 2009).
As the rate of population increase is considered the main determinant in the
establishment and invasion success of a biological control agent (Crawley 1986),
these results show that D. smithi may have a great chance to establish in new areas.
These biological parameters were obtained during cool temperatures (at 17�218C), therefore, the performance of D. smithi could be better at higher temperatures,
since the optimum temperature range for psyllids is betwewen 22 and 288C (Kapatos
and Stratopoulou 1999; Liu and Tsai 2000; Fung and Chen 2006). In Hawaii for
example, air temperatures are cool the entire year, with a median of 258C during the
summer and 228C in winter. It is therefore probable that D. smithi will establish easily
in these areas.
Our results identify the nymphal stage as a critical phase with high mortality.
This information should be useful for evaluating the potential for mass-rearing and
anticipating the potential population growth in the field (Southwood and Henderson
2000; Diaz, Overholt, Cuda, Pratt, and Fox 2008).
The best time for releasing an insect is another aspect to be considered in
biocontrol programs. Releases should be conducted when the insect exhibits high
dispersal and reproductive capacity and also at a stage of low mortality. The
intersection point of fertility (mx) and survival rate (lx) curves provides a good
indicator of the best time for agent release in the field. Therefore, the best age for
introduction of D. smithi for controlling M. calvescens should then be 4-day-old
adults, because at this stage females have a high reproductive rate, are mature, able to
fly and mortality is also low. Eggs laid have a high hatching rate, which will then
produce a large number of nymphs. Center et al. (2006) demonstrated that the psyllid
Boreioglycaspis melaleucae has a high dispersion capacity in the field, with a rate
ranging of 10 km/year. Therefore, as D. smithi has a high reproductive capacity, it is
possible that this species will establish in introduced areas.
Although mass-rearing is not a critical issue for the use of D. smithi as a
biocontrol agent (since the approach here is not inundative but instead classical), this
insect is easy to rear. Mass rearing is essential for the host range tests in quarantine.
The methodology for raising this psyllid was very simple and low cost, and a single
miconia seedling can produce a great number of psyllids (Morais, personal
observation).
114 E.G.F. de Morais et al.
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In summary, D. smithi exhibited a high biotic potential with a short life cycle and
can be easily mass-reared. These characteristics are very favorable for this psyllid as a
potential biological control agent for M. calvescens.
Acknowledgements
This study was supported by USGS BRD Pacific Island Ecosystem Research Centre, NationalPark Service, the Research Corporation of Hawaii and the Conselho Nacional deDesenvolvimento Cientıfico e Tecnologico (CNPq). Dr C. Smith (RCUH, University ofHawaii) is thanked for his continuous support and encouragement. We also thank JeffreyRyan Oar, from Oregon State University, for the English revision of the text.
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