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Population abundance, phenology, spatial distribution and a binominal sampling plan for Heliothrips haemorrhoidalis (Thysanoptera: Thripidae) in avocado.

Historically, the avocado crop in Chile had few pests, which were typically managed without insecticides. The value of the crop and insect pest impacts have increased recently. The area currently planted with avocado in Chile is about 36,355 hectares (Odepa 2013). Greenhouse thrips, Heliothrips haemorrhoidalis (Bouche) (Thysanoptera: Thripidae), have emerged as an economically important pest in the Valparaiso Region (Larral et al. 2008), where 60% of the Chilean avocado crop is cultivated (Odepa 2013). Feeding results in decreased plant vigor and cosmetic injury to fruit that results in rejection of fruit destined for export (Ripa et al. 2007). Goodall et al. (1987) suggested that higher plant densities favored populations of H. haemorrhoidalis. The relationship between H. haemorrhoidalis populations and damage to avocado has yet to be quantified and is not understood.

Colonies of H. haemorrhoidalis are formed on the leaves and fruits of avocado. Adults and larvae feed by piercing the epidermal tissue and sucking the cellular contents. Feeding produces russeting on leaves and fruit (Stevens et al. 1999). Russeting does not compromise the quality of the fruit pulp, but avocados are rejected for export if the total injury exceeds 1 [cm.sup.2] per fruit in Chile (Larral & Ripa 2007). It is unacceptable for premium export grade in New Zealand with injury covering more than 2 [cm.sup.2] (Stevens et al. 1999). Growers have responded by increasing pesticide use. The absence of monitoring methods, coupled with limited knowledge about pest phenology and population dynamics, has resulted in inadequate pest control with the available pesticides.

A cornerstone in developing a therapeutic control approach in an integrated pest management strategy is an understanding of pest phenology and behavior and the development of a statistically accurate sampling plan (Nyrop et al. 1999). A therapeutic management approach for greenhouse thrips in avocado can be developed and implemented with the above knowledge. Insecticide applications can be targeted to prevent damage while reducing unnecessary use with greater potential for integrating chemical, cultural, and biological control methods. The objectives of the current study were to determine the population abundance and phenology of H. haemorroidalis in avocados, to estimate the dispersion characteristics of greenhouse thrips in avocado trees and orchards, and to establish the relationships between density of H. haemorrhoidalis and percentage of leaves and fruit infested in order to develop a presence or absence (binomial) sampling plan.

Materials and Methods

Data were taken from 2 commercial, non-sprayed orchards in Quillota Province, Valparaiso Region, Chile. Each orchard was approximately 3 ha in size with mature 'Hass' avocado trees that were about 8 years old. Ten trees were randomly selected from each orchard. These were sampled about every 21 days for 2 years, from Jul 2005 to Dec 2007. Twenty fruits from below 2 m were chosen randomly on each tree and labeled using small colorful yarn tied to the base of each leaf and fruit. Marked fruits that fell during the course of the study were replaced with another that was randomly chosen. Ten mature leaves were also randomly chosen. On each marked fruit and extracted leaf, the number of H. haemorrhoidalis adults, first instars, second instars, propupae, and pupae were counted, using in the field a 3X magnification headband and in the laboratory a 50X stereoscope. The size of the fruit was measured on all sampling dates.


Means ([+ or -] SEM) on leaves and fruits were determined for larvae I, larvae II, propupae, pupae, and adults on each sample date in each field in order to determine population abundance of thrips. Taylor's power law relationships (Taylor 1984) were conducted for each H. haemorrhoidalis life stage and for life stages combined. Separate analyses were conducted for leaves and fruits in each field. Taylor's power law relates variance ([s.sup.2]) to mean (x) by the equation [s.sup.2] = a[x.sup.1], which is expressed as a linear relationship log [s.sup.2] = a + b(log x). The slopes (b) were compared to 1 using a t-test. Values of b< 1, b = 1, and b > 1 were considered representative of uniform, random, and aggregated distributions. Slopes of individual life stages were compared using the 95% confidence interval (CI). The goodness-of-fit of each relationship was evaluated by determining the coefficient of regression ([R.sup.2]).

A binominal sampling plan was developed by establishing a relationship between the total population (m) and the proportion of infested structures (leaves and fruits). This was done using variables a and b from the Taylor's power law variables in the equations of Wilson & Room (1983), where p = 1 - exp[-m(ln (a * [m.sup.(b-1)]/ (a * [m.sup.(b-1)] - 1))]. Calculation of the sample size was made for the population with a constant coefficient of variation (CV) of 25% (CV = (S/Vn)/m), which is considered acceptable in scouting programs (Southwood & Henderson 2000). The formula n = a[m.sup.b-2]/[D.sup.2] was used based on the parameters from Taylor's power law where n is the required sample size and D is the desired level of precision of 25%.



Heliothrips haemorrhoidalis formed colonies on the leaves (Fig. la, c). Populations were present on nearly all sample dates. Populations were abundant in field 2 from Aug 2005 when sampling began until Feb 2007 with the number of immatures outnumbering the number of adults on nearly all sample dates. Densities were greatest in field 2 from Feb to Oct 2006 when estimates of total thrips exceeded 1 per leaf. Populations of H. haemorrhoidalis were greatest in field 1 on all sample dates from Jan to Jul 2006 when densities exceeded 1 per leaf. Populations were very low in field 1 on all sample dates prior to and after that period.

Immature H. haemorrhoidalis outnumbered the adults on the fruits in both fields during the winter months of Jul, Aug, and Sep of 2005 (Fig. lb, d). Fruits were harvested, and new fruits were not available until Dec 2005 when adult thrips formed colonies as the new fruits developed. The abundance of the immature stages increased in both fields from the summer months of Jan, Feb, and Mar 2006 until the fall and winter months of Aug and Sep when the fruits were harvested. Colonies re-developed on the new fruits in field 2 in Nov 2006, but the numbers of immatures were less than the numbers of adults on nearly all samples dates until Nov 2007. Almost no colonies of H. haemorrhoidalis developed on the new fruits in field 1 from Nov 2006 until sampling was discontinued in Nov 2007.


Regression statistics of Taylor's power law relationships for individual sample estimates of H. haemorrhoidalis adults, pupae, and larvae on avocado leaves and fruits are shown in Tables 1 and 2, respectively. Values of the intercept a for all thrips stages in both fields ranged between 0.83 and 1.17 on leaves and between 0.48 and 1.01 on fruits. Values of the slope b for all thrips stages in both fields ranged between 1.44 and 1.53 on leaves and fruits, and each was significantly greater than 1, thereby showing that all populations were aggregated. The 95% CL of estimates of b for all stages overlapped in both fields; consequently, the degree of aggregation on leaves and fruits was similar for each thrips stage in both fields.


Because the pattern of aggregation of H. haemorrhoidalis was very similar for each life stage, Taylor's power law relationships for total adult and immature thrips were used in the Wilson & Room (1983) equation to describe the relationship between total population and the proportion of infested leaves and fruits. Figure 2 shows the relationships between population density and proportion of infested leaves and fruits using values of a and b from the Taylor's power law relationships for leaves and fruits for data pooled over fields 1 and 2. Determination of this functional relationship allows for estimating density in scouting programs without counting all inhabitants on leaves or fruits, thereby reducing the time of sampling. The proportion of infested samples was less than 0.8 for densities of about 2 thrips per leaf or fruit.

The number of presence/absence leaf and fruit samples needed to estimate density at the 25% level of precision as a function of mean density using the equation in Southwood & Henderson (2000) is shown In Figure 3. At densities of 0.5 thrips per fruit or greater, fewer than 22 samples are necessary to estimate density at the 25% level of precision.


The abundance of pests is directly associated with the phenology of the part of plant on which they feed. The abundance of thrips and their phenology has been widely studied, mainly in species infesting and causing damage in crops during the flowering period, such as Frankliniello (Thysanoptera: Thripidae) species (Northfield et al. 2008; Osekre et al. 2009; Pearsall & Myers 2000). Heliothrips haemorrhoidalis formed colonies on the leaves and fruits of avocado. They were present on the leaves of avocado at all times of the year. The adults formed colonies when the fruits were small, and the colonies increased and caused injury until the fruits were harvested. The development and abundance of the pest is associated with environmental conditions. Chhagan & Stevens (2007) determined a minimum threshold temperature of 10.1 [degrees]C for H. haemorrhoidalis. This is greater than the minimum threshold of 6.9 [degrees]C reported for Scirtothrips persea (Thysanoptera: Thripidae), another avocado pest (Hoddle 2002).

Aggregation in thrips species has been established in several publications. Wang & Shipp (2001), Parajulee et al. (2006), Salguero Navas et al. (1994), and Garcia-Mari et al. (1994) showed a significant regression in Taylor's power law for a population of Frankliniellia occidentalis (Pergande) (Thysanoptera: Thripidae) in cucumber, cotton, tomato, and strawberries with aggregation indices of about 1.5. Cho et al. (2000) described a very similar aggregation index in Thrips palmi Karny (Thysanoptera: Thripidae) in potato. These values are similar to the aggregation indices determined for H. haemorrhoidalis in this study. Worner & Chapman (2000) determined an even greater aggregation of thrips on Viburnum tinus L. (Dipsacales: Adoxaceae) with index 1.9.

Cho et al. (2000), Navarro-Campos et al. (2012), and Salguero Navas et al. (1994) observed greater aggregation of the larval thrips compared to the adult thrips. This was attributed to the reduced mobility and ability to disperse of the larvae. The pattern of aggregation was similar for all life stages of H. hemorrhoidalis on avocado. It is a colony-forming species with all life stages living in the same colony. The pattern of aggregation is expected to be similar for all life stages in colony-forming species (Southwood & Henderson 2000). This study was carried out in untreated avocado orchards. The aggregation index may differ in pesticide-treated trees (Trumble 1985).

The presence/absence census method developed by Wilson & Room (1983) to utilize Taylor's power law has been a convenient tool for integrated pest management (Kuno 1991). The relationship between the proportion of infested leaves and the mean density of the pest has been determined for different pests such as thrips, spider mites, psyllids, and white flies among others (Cho et al. 2000; Salguero Navas et al. 1994; Zalom et al. 1985; Naranjo & Flint 1995; Steiner 1990; Worner & Chapman 2000; Wang & Shipp 2001). The understanding of this relationship allows a less time-consuming monitoring and therefore less costly management of the pest (Binns & Nyrop 1992). Our results showed that H. haemorrhoidalis adults began infesting the small fruits of avocado. Injury to the fruits from feeding can be estimated to increase 0.22 [cm.sup.2] per adult per week (Stevens et al. 1999). The amount of injury of H. haemorrhoidalis that can be tolerated on exported avocado fruit is limited. Therefore, the pest must be detected at an early stage of the infestation providing the right pesticide treatment window by which a successful control is obtained avoiding additional treatments. The binomial sampling program reported here provides the monitoring parameters to estimate density with a 25% precision level before populations reach the economic threshold. This monitoring program was developed for orchards that were 2 ha in size. Observations suggested that population sizes are increased in certain areas of larger orchards perhaps due to influences such as proximity to bodies of water (P. L. and R. R., unpublished). Therefore, large orchards should be broken into smaller sections for monitoring purposes in order to further avoid treatment of the entire orchard unnecessarily.


This research was partly supported by a grant from the FONDEF DO3I1077, which is greatly appreciated. The authors also would like to thank INIA technician team, Jose Montenegro, Viviana Guajardo, and Patricia Veliz for their valuable collaboration.

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Pilar Larval (1,*), Renato Ripa (1), Joe Funderburk (3), and Eugenio Lopez (1)

(1) Centro de Entomologia Aplicada Ltda., Quillota, Chile, E-mail: (P. L); (R. R.)

(3) University of Florida, North Florida Research and Education Center, Quincy, Florida 32351, USA, E-mail: (J. F.)

(4) Facultad de Ciencias Agronomicas y de los Alimentos. Pontificia Universidad Catolica de Valparaiso, Quillota, Chile, E-mail: (E. L.)

(*) Corresponding author; E-mail:

Caption: Fig. 1. Abundance (mean [+ or -] SE) of adult and immature stages of H. hoemorrhoidolis per leaf and fruit (from sampling 10 leaves and 20 fruits of 10 sample trees) in Field 1 (a, b) and Field 2 (c, d).

Caption: Fig. 2. Relationships between the proportion of infested leaves and fruits and H. haemorrhoidalis population density using Taylor's power law indices in the Wilson & Room (1983) equation for data pooled over avocado fields 1 and 2.

Caption: Fig. 3. Relationships between the number of leaf and fruit samples needed to estimate density at the 25% precision level and the number of thrips in each part of avocado tree as determined by using the equation in Southwood & Henderson (2000) for data pooled over avocado fields 1 and 2.
Table 1. Regression statistics of Taylor's power law obtained for
different H. haemorrhoidalis life stages from random samples of 10
individual avocado leaves collected from each of 10 trees in 2 fields
located in Valparaiso Region, Chile, for all dates when the mean was
not equal to Zero.

                     Taylor's power law regression statistics
               Field 1(35 samples from 26 Jul 2005 to 12 Sep 2007;

Instar      N dates  Intercept a  Slope b          CI 95%    [R.sup.2]

Larva I     20       1.116        1.502 (***)  1.376  1.629  0.972
Larva II    19       1.007        1.470 (***)  1.351  1.589  0.976
Propupa     14       1.000        1.453 (***)  1.316  1.59   0.978
Pupa        15       1.020        1.502 (***)  1.399  1.606  0.987
Adult       29       0.830        1.455 (***)  1.355  1.556  0.970
All stages  29       1.091        1.624 (***)  1.501  1.747  0.964

            Taylor's power law regression statistics
                              FieId 2 (38 samples from 1 Aug 2005 to 10
                                               Dec 2007)
Instar      F- value  P       N dates  Intercept a  Slope        CI 95%

Larva I     624.5     0.0001  32       1.169        1 509 (***)  1.386
Larva II    680.7     0.0001  33       1.096        1.510 (***)  1.400
Propupa     535.4     0.0001  20       1.080        1.463 (***)  1.295
Pupa        981.4     0.0001  27       1.116        1.527 (***)  1.407
Adult       885.9     0.0001  35       0.89         1.436 (***)  1.276
All stages  730.7     0.0001  37       1.242        1 595 (***)  1.443

            Taylor's power law regression statistics
            FieId 2 (38 samples from 1 Aug 2005 to 10
                        Dec 2007)
Instar      CI 95%  [R.sup.2]  F-value  P

Larva I     1.632   0.954      625.5    0.0001
Larva II    1.621   0.962      780.8    0.0001
Propupa     1.631   0.949      334.7    0.0001
Pupa        1.648   0.964      676.2    0.0001
Adult       1.595   0.911      336.7    0.0001
All stages  1.748   0.928      450.5    0.0001

(***) Indicates a slope significantly greater than 1.0 at P < 0 .0001,

Table 2. Regression statistics of Taylor's power law analyses conducted
for different H. haemorrhoidalis life stages from random samples of 20
individual avocado fruits collected from each of 10 trees in 2 fields
located in Region V, Chile, for all dates when the mean was not equal
to Zero.

                    Taylor's power law regression statistics
                Field 1 (29 samples from 26 Jul 2005 to 17 Dec 2007)
Instar      N dates  Intercept a  Slope b         CI 95%     [R.sup.2]

Larva 1     17       0.907        1.374 (***)  1.281  1.466  0.985
Larva II    17       0.620        1.220 (***)  1.131  1.308  0.983
Propupa+    14       0.895        1.390 (***)  1.255  1.525  0.977
Adult       20       0.480        1 259 (***)  1.200  1.317  0.991
All stages  22       0.841        1.412 (***)  1.306  1.517  0.975

                   Taylor's power law regression statistics
                             Field 2 (29 samples from 29 Jul 2005 to 15
                                            Nov 2007)
Instar      F-value  P       N dates  Intercept a  slope        CI 95%

Larva 1     1001.1   0.0001  22       1.008        1.396 (***)  1.232
Larva II     868.4   0.0001  24       0.843        1.367 (***)  1.246
Propupa+     502.3   0.0001  21       0.936        1.404 (***)  1.196
Adult       2041.2   0.0001  29       0.530        1.212 (***)  1.095
All stages   785.3   0.0001  29       0.930        1.398 (***)  1.290

            Taylor's power law regression statistics
            Field 2 (29 samples from 29 Jul 2005 to 15 Nov 2007)
Instar      CI 95%  [R.sup.2]  F-value  P

Larva 1     1.559   0.938      317.2    0.0001
Larva II    1.488   0.960      548.5    0.0001
Propupa+    1.612   0.909      199.7    0.0001
Adult       1.329   0.941      451.5    0.0001
All stages  1.506   0.962      707.7    0.0001

(***) lndicates significantly greater than a slope of 1 at P < 0.0001
according to a t- test.

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Author:Larral, Pilar; Ripa, Renato; Funderburk, Joe; Lopez, Eugenio
Publication:Florida Entomologist
Article Type:Report
Geographic Code:3CHIL
Date:Jun 1, 2018
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