Acta Agronómica

Introduction

Within the Tarsonemidae family P. latus is considered the most important pest of citrus in the tropics and in other regions of the world (Gerson, 1992). This Tarsonemidae, known as "broad mite", has a wide geographical distribution and a considerable number of host plants in tropical areas (Gerson, 1992). According to Peña & Campbell (2005), in temperate and subtropical regions, attacks plants under screenhouse conditions, and according to Rogers, Stansly, Childers, Mccoy & Nigg (2010), also attacks other citrus species such as lemon and lime. In this sense, P. latus disperses through wind, the transportation of infected plant tissues, by natural contact of plant foliage, and through foretic relationship with insects (Palevsky, Soroker, Weintrub, Mansour, Abo-Moch & Gerson, 2001). On the other hand, Ochoa, Aguilar & Vargas (1991), and Rogers, Stansly, Childers, Mccoy & Nigg (2010), consider that P. latus is the most important pest in lemons in some areas of the Caribbean.

On leaves, damage is characterized by malformation of growing tissues, including leaves, shoots and flowers. The mite injects toxic saliva causing twisted, hardened and distorted growth in the plant terminal buds (Rogers, Stansly, Childers, Mccoy & Nigg, 2010). When populations are high, infested leaves bend and turn to coppery and purple color. Damage on citrus fruit occasionally occurs on the shaded side and can go unnoticed; however, if the attack is severe, there can be discoloration and fruit drop. Fruit areas which are infested, have a burnt appearance and rough texture. Furthermore, there may be a lifting of the epidermis superficial layer, which remains to the fruit surface a silver-gray thin film (Rogers, Stansly, Childers, Mccoy & Nigg, 2010).

In fact, in a previous work, Peña & Bullock (1994), found that the attack of the mite reduces leaf area and water content in limes and sweet oranges in citrus-growing areas in Florida. Peña (1990), found in artificial infestations on lime fruits in laboratory, smaller than 2.5 cm in diameter, the mite population have allowed an increasing in few days after infestation. In screenhouse conditions, damage occurred between 10 and 14 days, and in the field conditions, between 9 and 15 days after infestation.

Colombia has a low market share of orange export. This situation is associated with, among other limiting factors, damages caused by pests such as mites, which are a serious problem in fruit crops (Ochoa, Aguilar, & Vargas, 1991). In Colombia, P. latus, was reported in 1971 on citrus (Zuluaga, 1971).

Recently, Mesa & Rodríguez (2012), reported the presence of this mite in Valencia orange in Antioquia, Caldas, Quindío, Risaralda and Valle del Cauca-Colombia, where P. latus is the responsible of losses between 37-40% on fruit quality. Given the negative impact of P. latus in the citrus production in Colombia, this study was conducted as a first step in developing an IPM program for broad mite control with the objectives of (1) determining its main biological and behavioral aspects and (2) to study the P. latus damage in different Valencia orange plant organs.

Materials and methods

Results

Life cycle and developmental stages

It was already expected that P. latus would sucessfully develop from eggs to adults when fed on valencia orange, which takes 3.2 days. The average duration of incubation period was 1.7 days and the larval stage lasted 0.9 days. The quiescent nymph "pupa" lasted 0.6 days; in fact, the immature survival was 95% (Table 1). Sex ratio (female: male) was 2.4:1.

Table 1: Mean duration (days ± S.E.M.) of the immature stages of P. latus on Valencia orange young leaves at 25 ± 5°C, 70 ± 5% RH and 12:12 (L : D) photoperiod

Reproductive, longevity, fecundity periods and life table parameters

P. latus males starts their reproductive activity in search of a pupa stage of development, which they raise with the help of their last pair of legs, which is fixed with the male genital papilla to their body, in turn, is a posterior extreme and it is loaded as they walk until the adult female emergence. In general, P. latus female, requires a pre-oviposition period of 1.3 days. However, preoviposition of P. latus is almost immediately after emerging. Average duration of oviposition period is relatively short (7 days). The survival period (l_x) follows a normal curve in which young P. latus female survival is very high, in the case of the fecundity, most egg production peak occurs in the first and second day of the P. latus female life (Figure 1).

Figure 1: Survivorship (l x ) and fecundity (m x ) curves of P. latus on Valencia orange young leaves at 25 + 5°C, 70 + 5% RH and 12H:12H (L:D) photoperiod. Error bars represent mean standard error.

On average, the longevity of P. latus female was 9.6 days (Table 2).

Table 2: Life table parameters for P. latus reared on Valencia orange young leaves at 25 + 5oC, 70 + 5% RH and 12:12 (L:D) photoperiod

In this study, P. latus produced 39.0 eggs.female^-1, which is equivalent to 3.1 eggs.female^-1 per day. Conversely, P. latus showed a net reproductive rate (R_o) of 93.3, an intrinsic rate of natural increase (r_m) of 1.2, a finite multiplication rate (λ) of 3.7, a generation time (T) of 0.6 and a doubling time (TD) of 3.4 days, respectively (Table 2).

Damage of P. latus in young leaves

First damage signs caused by P. latus on newly developed Valencia orange shoots are characterized by a change in the epidermis color tone, which loses brightness and becomes opaque, giving the impression of being dehydrated. Therefore, leaves twist or curl along their edges, starting from the base to the apex, at this point the highest feeding and oviposition activities of females occurs. As time passes, damage is more noticeable and the leaf color turns into a brown spot that starts mainly on the mid-rib. If damage is severe, the shoot drops off (Figure 2).

Figure 2: Damage caused in Valencia orange shoots by P. latus: A, B, D and E. Tissue distortion, twisting or curling towards its back, sheaf of leaves tanning. C. Intervenal yellowing. F. Leaf drop. G. Healthy shoot.

No differences were found between days of appearance of first symptoms (F=13.5; df=3; P<0.30) and leaf drop (F= 31.8; df=3; P<0.25) according to the level of infestation of P. latus in Valencia orange shoots (Table 3). These symptoms occurred between 7.0 and 11.8 days after infestation.

Table 3: Days of appearance of first damage symptoms and newly developed leaf drop in Valencia orange young leaves affected by three infestation levels of P. latus under screen house conditions at 25°C and 70% R.H in Palmira Valle del Cauca, Colombia

¹ Values within a column followed by same letters are not significantly different (P <0.05, ANOVA, L.S.D. test).

Damage of P. latus in young fruit

First signs of damage caused by P. latus on Valencia orange fruits with a diameter between 0.1-0.3 cm, are characterized by a change in the epidermis color tone, which loses brightness and becomes opaque. Later, there are parallel scissions that start at the base of the fruit, giving the impression of tissue dehydration. The highest feeding and oviposition activity of the females takes place in this area. Over time, damage is more noticeable and it becomes a brown spot at the base of the fruit (Figure 3).

In the case of fruits with larger diameter (1.0-3.0 cm), damage is characterized by the change in the epidermis coloration, which becomes whitish and opaque, with mummified appearance; this damage may, initially, occupy small areas, but as time passes, can cover all the fruit (Figure 3).

There were differences between days of appearance of first symptoms (F= 8.5; df= 2; P<0.0001) and fruits drop (F= 8.6; df= 2; P<0.0006) according to the level of infestation of P. latus females and the infested structure type (Table 4).

Figure 3: Damage symptoms at 25oC and 70% R.H in Palmira-Valle del Cauca, Colombia caused by P. latus in Valencia orange fruits with a diameter between 0.1-0.3 cm (age: 9.5 days after flowering) and 1.0-3.0 cm (60 days after flowering): A: Healthy small fruit; B: damage caused by 15 females after 7 days of infestation on small fruit; C: Damage caused by 30 females after 24 hours of infestation on small fruit; D: Healthy large fruit E: Damage caused by 15 females after 7 days of infestation on large fruit; F: Damage caused by 30 female after 24 hours of infestation on large fruit.

Table 4: Days of appearance of first damage symptoms and drop of Valencia orange fruits affected by two infestation levels of P. latus females under screenhouse conditions (25oC and 70% R.H) in Palmira-Valle del Cauca, Colombia.

¹ Values within a column followed by same letters are not significantly different (P <0.05, ANOVA, L.S.D. test).

In fact, in that small fruits (0.1 - 0.3 cm in diameter) infested with 15 and 30 females of P. latus show earlier symptoms of damage and abscission of structure than those fruits infested with five females, in which damage and fruit drop occur 8.6-19.3 days after infestation, respectively.

In the case of fruits, 1.0-3.0 cm diameter with infestation levels of 15 females, the first symptoms of damage and subsequent collapse of the structure occur 14.5-18.1 days after initial infestation, if the level of infestation increases to 30 females, the first symptoms of damage and the collapse of the structure occurs significantly faster, 3.0 and 13.5 days, respectively.

Discussion

In this study, morphological characteristics of P. latus adults were similar to those observed by Ochoa, Aguilar & Vargas (1991), P. latus eggs are oval, whitish with the chorion covered by longitudinal rows of white tubercles, occupying about half the female body (Norton, Kethley, Johnston & O'Connor, 1993). The pupa stage corresponds to a quiescent phase, which develops in the larval cuticle. This developmental stage is also known as "pharate female" or quiescent nymph (Norton, Kethley, Johnston & O'Connor, 1993). Duration of the egg stage was, on average, 1.7 days, equivalent to more than half the time of the mite full development cycle, being similar to findings of Vieira & Chiavegato (1999), and Ferreira, Oliveira, Haji & Gondim (2006), in plants of C. limon (2.2 days) and grapevine (3.9 days), respectively.

Total life cycle of P. latus was 3.2 days (Table 1), which coincides with the observations of Vieira & Chiavegato (1999), who worked with young fruits of C. limon under weather conditions of 27.2 ± 0.5 °C and 68.2 ± 1.2% RH.

Similar to those in this study (25 ± 5 °C, 70 + 5% RH and 12:12 L:D h photoperiod) and Vieira & Chiavegato (1999), at 27°C and 67.6% RH and an identical photoperiod. High survival (>90%), high percentage of adult females compared to males (2.4:1) and short development time (3.2 days) are characteristics of this species which ensure its survival in different stages of development.

Figure 1, shows the cohort survival, which follows a normal curve in which immature and young P. latus female survival is very high, a fact that guarantees a stable population in terms of the age distribution and permanent reproduction and multiplication expectations. Under the conditions of this study (25 + 5 °C, 70 + 5% RH and 12:12 L:D photoperiod) a preoviposition period of 1.3 days was registered (Table 2), a similar value to those recorded by Vieira & Chiavegato (1999), in cotton leaves (1.1 days ) and lemon young fruits (0.9 days). However, in hosts plants such as grapevine, where had achieved preoviposition periods of 0.3 days (Ferreira, Oliveira, Haji & Gondim, 2006). Oviposition period lasted, on average, 7 days and was similar to that found by Vieira & Chiavegato (1999), (6.8 days on young lemon fruits). After oviposition, females can live up to 0.8 additional days, on average. However, on grapevine crops this average could extend up to 1.1 days (Ferreira, Oliveira, Haji & Gondim, 2006).

In this study, P. latus longevity on leaves of the Valencia orange was 9.6 days, these results are comparable in variability to the report by Vieira & Chiavegato (1999), in young lemon fruits. However, longevities of 13.6 days in cotton (Vieira & Chiavegato, 1999) and of 15.8 days in grapevine (Ferreira, Oliveira, Haji & Gondim, 2006), have been recorded.

Observed fecundity was 39 eggs.female^-1, 3.1 eggs per P. latus female per day. In a previous research work carried out by Vieira & Chiavegato (1999), with other hosts plants of the genus Citrus, maintained at 27°C, specifically with Sicilian lemon (C. limon), found fecundities of 24.9 and 58.9 eggs per P. latus female, respectively, which shows that this host is very suitable for P. latus population development and have allowed a possible explanation why there are so high populations of the pest in this crop.

Under the conditions of this experiment, the species generation growth rate was 120% (Table 2), which is difficult to find in another species. Results show that indicators of its life table (R _o =93.3, r_m=1.2, λ=3.7, T= 0.6 and TD= 3.4 days) were higher compared with those achieved by Ferreira, Oliveira, Haji & Gondim (2006), in grapevine (R _o= 30.12, r_m=0.314, T=10.81 and λ=1.37).

Symptoms described in this study for the attack of P. latus on young leaves of Valencia orange (Figure 2), confirms findings of Jeppson, Keifer, & Baker (1975), who described a variety of symptoms and specific reactions due to the possible toxin that P. latus injects. According to these researchers, some of the symptoms are confused with viral diseases, herbicides or stress problems due to Magnesium deficiency. The most significant damages occur on the plants growing points where the tissues are turgid (Jeppson, Keifer, & Baker, 1975).

According to the results of the experiments on newly developed shoots (Table 3), independent of the number of mites, the first symptoms of damage occurred between 7 and 8.5 days after infestation.

Nevertheless, the fall of the structures occurred between 11.8 and 14.6 days, which indicates damage severity on young tissues, up to the point that infestations of five P. latus females can cause shoots drop in a short time, which is concordance to Gerson (1992).

In the present study, we found that damage symptoms from the attack of P. latus in some host plants may occur very quickly, suggesting that few mites are sufficient to cause damage. In fact, symptoms of damage caused by P. latus on Valencia orange fruits with diameters between 0.1 - 0.3 cm, which were characterized by the change in the epidermis tone and the blackening appearance at the fruit base (Figure 3), which is consistent with the findings of Peña (1990), in lime fruits. Initial symptoms of damage and fruit drop occur first in fruits with diameter between 0.1 - 0.3 cm (Table 4); especially with 15 and 30 females.

With these population levels, in less than 3 days, the impact of P. latus on fruit drop is observed, which occurs 7-8 days after the attack. These results provides more accurate and reliable estimates of the first stages of fruit formation (0.1- 0.3 cm) are very sensitive to the mite attack and confirm findings of Brown & Jones (1983), and Peña (1990), who worked with lime fruits, found that P. latus prefers those with small diameters. De acuerdo con Jeppson, Keifer & Baker (1975), who indicates mite preference for young tissues and indicate that P. latus populations in field conditions, should be evaluated at this phenological stage, in order to establish action thresholds.

In the case of fruits with larger diameter (between 1.0 - 3.0 cm), was only found a change in the epidermis coloration, which became whitish and opaque (Figure 3).

In this phenological fruit stage with the evaluated levels of infestation as an extension in the time of appearance of damage symptoms and fall of the fruit, are listed in Table 4, which confirms the reports of Jeppson, Keifer & Baker (1975), these researchers found that mites cannot feed on old and fibrous tissues.

Results obtained in this study, provides more important information to explain how a mite with such a very short life cycle, high oviposition rate and huge biotic potential causes such severe damage so quickly in both young tissues and shoots and in newly formed fruits. If we keep in mind is considered that young shoots and fruits with diameters between 0.1-0.3 cm, and infestations of 5 and 15 mites can present damage in 8.6 and 2.8 days, respectively, it is clear that P. latus is a pest in Valencia oranges as recorded by Mesa & Rodríguez (2012), for this citrus-producing areas in Colombia.

In the past, Bassett (1981), considers that the presence of a small number of individuals of P. latus is sufficient to cause economic damage in the host plant; results of this study provide basic information on the establishment of action thresholds against P. latus.

Given these concerns, the biological parameters of the mite and plant structures most affected by control measures at the appropriate timing in field conditions, which had achieved the first steps in establishing IPM strategies for mites in this crop.

For the first time in Colombia, establishing artificial infestation trials with P. latus on Valencia orange organs, with results that approximate the density of this mite found under true field conditions. However, is still necessary to determine the population densities levels of P. latus that justify control, taking into account observations by Peña (1990), on density variations of P. latus in the crop associated with the presence of natural enemies, inter specific competition with other species of mites such as Phyllocoptruta oleivora Ashmead (Acari: Eriophyidae) and environmental conditions.