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14 June 2019 Interference and Exploitation Competition between Frankliniella occidentalis and F. intonsa (Thysanoptera: Thripidae) in Laboratory Assays
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Abstract

Recently, the native species Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae) has been found to be regionally dominant over its invasive congener Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in Korea. To understand the variation in patterns of occurrence in the field, the effect of competition on the biological attributes of the 2 thrips species was assessed in the laboratory. In a behavioral study, the effect of inter- and intraspecific competition in honey or pollen feeding was observed in a glass-slide arena, and we found both reproduction and longevity to be more reduced in F. occidentalis than in F. intonsa by competition. However, the extent of feeding marks on bean leaves made by both species (in competition) was not significantly different from that made by each species separately, except in the case of the F. intonsa larvae. In an experiment on potted bean plants, competition caused a greater reduction in numbers of F. occidentalis progeny than that of F. intonsa progeny. In behavioral observations, guarding and feeding times of adult F. intonsa were 8.5 and 1.5 times longer on honey, and 42.8 and 1.3 times longer on pollen than F. occidentalis, respectively. However, in intraspecific competition, none of the behavioral parameters in pollen feeding showed significant differences in either species, except for the “confronting” behavior. In conclusion, both interference and exploitation competition exist between the 2 thrips species, and in laboratory studies F. intonsa was more persistent, not only at feeding and guarding food sources, especially in the adult stage, but also in displaying higher reproduction and longevity. These may be the underlying mechanisms for the asymmetrical pattern of occurrence of the 2 thrips in the field.

Frankliniella occidentalis (Pergande) and Frankliniella intonsa (Trybom) (both Thysanoptera: Thripidae) are sympatric thrips species found on many flowering plants, making them important agricultural pests (Murai 1988; Atakan et al. 1999). Thrips damage plants directly by sucking plant cell contents, and indirectly by transmitting tospovi-ruses such as tomato spotted wilt virus and impatiens necrotic spot virus, causing significant economic losses worldwide (Lewis 1997). Frankliniella occidentalis is an invasive species in Korea, where it has spread throughout Korea since its first appearance on Jeju Island in 1993, whereas F. intonsa is a native species, and widely distributed in the Palearctic and part of the Oriental regions. Frankliniella intonsa has itself invaded both North America (Nakahara & Foottit 2007) and New Zealand (Teulon & Nielsen 2005). In Korea, no consistent pattern has been observed regarding the occurrence of these 2 thrips (Table 1). However, the native F. intonsa has recently been found to be regionally dominant in Korea, although the invasive F. occidentalis is generally considered to be the more common thrips (Table 1). Our preliminary laboratory assays (unpublished) indicate that interspecific competition occurs between these 2 species.

Table 1.

The pattern of relative occurrence of Frankliniella occidentalis (FO) and Frankliniella intonsa (FI) in fields and greenhouses in Korea.

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Interspecific competition can be an important factor in determining insect population size and structure. Under interspecific competition, individuals of 1 species will suffer resource restriction due to the presence of individuals from the other species. Interspecific competition is often highly asymmetrical, with the consequences differing between the 2 species. Interspecific competition also can be a factor determining geographic ranges of thrips (van Rijn et al. 1995; Kirk & Terry 2003; Deligeorgidis et al. 2006). In European greenhouses, F. occidentalis replaced Thrips tabaci Lindeman (Thysanoptera: Thripidae), but van Rijn et al. (1995) suggested that F. occidentalis is the superior competitor, because they could find no differences in other potential explanations, including the intrinsic rate of increase, net reproductive time, or development time. In contrast to outcomes in European greenhouses, F. occidentalis has failed to establish as the dominant species in the eastern US, despite repeated accidental introductions (Kirk & Terry 2003). Paini et al. (2008) demonstrated that F. occidentalis larvae are competitively inferior to the congeneric Frankliniella tritici (Fitch) (Thysanoptera: Thripidae), a species endemic to most of the eastern US. The authors speculated that interspecific larval competition between F. occidentalis and F. tritici possibly contributes to the biotic resistance limiting the spread of F. occidentalis in the eastern US. Therefore, interspecific competition is an important factor that should be considered when assessing any invasive lspecies' spread and success, but there is no information available on the competition between F. occidentalis and F. intonsa. In this study, we conducted both biological and behavioral studies to explain the different pattern of occurrence in the field between these 2 anthophilous thrips in recent yr.

Materials and Methods

INSECT REARING

Collections of F. occidentalis and F. intonsa were made from a strawberry greenhouse in 2012, in Songcheon, Andong, South Korea, and thrips were reared in plastic containers (24 cm L × 17 cm W × 8 cm H) containing 8 excised, rooted (on water-soaked cotton) red kidney bean (Phaseolus vulgaris L.; Fabaceae) stems with cotyledonous leaves. A mixture of pure honey and pine pollen was streaked along the principal vein of each leaf using a fine brush. For ventilation, two 6 cm diam holes were cut in the lid of each container, and the holes were covered with thrips-proof fabric (196 mesh count, Saatilene Hi-tech, Zurich Co., Como, Italy). The containers were kept at 24 °C and 16: 8 h (L: D) photoperiod in a growth chamber, and water was added when needed. To initiate new generations, 30 newly emerged adult thrips were transferred to a new plastic container with the same food sources as needed.

EFFECT OF INTERSPECIFIC COMPETITION ON REPRODUCTION

Unmated adult females (< 24 h old) were used for this experiment. A leaf cage arena was constructed of cotton with a 0.7 cm diam hole attached to a red kidney bean leaf. The cotton with the hole was covered with thrips-proof fabric. A mixture of honey and pollen was provided inside the arenas, inside of which we placed either 1 individual of 1 of the 2 thrips or a single pair of thrips, with 1 individual of each species. Thrips were kept in the leaf cages for 24 h at 28 °C in an incubator, after which adults were removed. The leaf arena exposed to thrips was detached, placed on water-soaked cotton, and examined daily for larval hatch and adult emergence.

EFFECT OF INTERSPECIFIC COMPETITION ON LONGEVITY

We assessed the effect of competition on adult longevity using Eppendorf tubes (2 mL) as an experimental arena. In these tubes, we placed either a single 1-d-old individual of 1 of 2 species or 1 pair (1 female of each species). A 4 mm diam hole was made in the cap, then covered with thrips-proof fabric. As a food source, we placed a fresh leaf disc (5 mm L × 2 mm W) of red kidney bean on water-soaked cotton, and a drop of mixed honey and pollen on the inside the tube. Leaf discs were changed daily. Each treatment was replicated 10 times. The experiment was conducted inside a growth chamber at 30 °C, 70–75% RH, and a 16: 8 h (L: D) photoperiod, and data were recorded daily until all adults died.

EFFECT OF INTERSPECIFIC COMPETITION ON EXTENT OF LEAF FEEDING

Female adults (< 24 h old) and second instar larvae (48 h old after molt from the first instar) were used to measure feeding activity on kidney bean leaves in a leaf-cage arena. For both life stages (adults or larvae), 1 individual of 1 of the 2 species or a pair of thrips (1 individual each from the 2 species) were kept in an arena, which was made of a cotton pad with a 5 mm diam hole space placed over the bean leaf. A piece of thrips-proof fabric was attached to the arena using a clip to fix the cotton ring to the leaf, and the arena was kept at 24 °C in an incubator after adding sufficient water to the bean plant to keep the plant fresh during the experimental period. Adults were removed after 24 h, and feeding marks on the leaf were photographed under a dissecting microscope (10×) with a digital camera (DS-Fi 1, Nikon Corporation, Kanagawa, Japan). Sigma Scan Pro (SPSS Science, Chicago, Illinois, USA) was then used to measure the area of leaf with thrips damage.

DEMONSTRATION OF INTERSPECIFIC COMPETITION ON POTTED BEAN PLANTS

Interspecific competition between F. occidentalis and F. intonsa on whole plants was demonstrated using a cylindrical cage (30 cm H × 16 cm D), with 1 end covered by thrips-proof fabric, that covered a potted red kidney bean plant with 2 cotyledonous leaves. Ten females and 5 males (all 5–7 d old) of either 1 or both of the test species were released into test cages, which were then held at 28 °C in an incubator. The 3 treatments, each with 10 replicates, included in the experiment were (i) F. occidentalis only, (ii) F. intonsa only, and (iii) F. occidentalis and F. intonsa together. Data were first recorded from 14 d after treatments and continued up to 7 d. For easier collection, each plant was placed under a fluorescent light, causing thrips to aggregate at the top of the cylinder, where they were collected using an aspirator into a centrifuge tube (about 50 mL). Species and sex were identified under the dissecting microscope. Mean generation time was calculated as the date of introduction of thrips to the cylindrical cage until the date of adult emergence in the next generation.

BEHAVIORAL OBSERVATIONS ON INTERSPECIFIC ADULT COMPETITION

For this experiment, we used an experimental arena formed by 2 microscope glass slides sandwiched together (Lim et al. 2001), after inserting a flattened piece of cotton (1.5 cm L × 1.5 cm W × 0.2 cm H) with an internal hole (5 mm diam) between the 2 slides as a spacer. A droplet of honey or a lump of powdered pine pollen were placed in the center of the arena as a food source. Unmated, unfed females of F. occidentalis and F. intonsa (< 1 d old) were paired in an arena, and replicated 20 times for each food source (honey or pollen). Thrips behaviors were observed for 20 min, and were classified into categories as follows: (1) confrontation (when 2 thrips face each other without any movement); (2) food guarding (when either F. occidentalis or F. intonsa remain very close to food, sometimes feeding and sometimes quiescent); (3) feeding (when an individual stood still with its forelegs apart, antennae still, usually nodding its head up and down, and probing with its mandible); (4) wandering (random movement); and (5) resting (no movement of any body parts). Data were recorded either as number of events observed (for confrontation) or number of s when the thrips were engaged in a particular behavior (all other behaviors).

BEHAVIORAL OBSERVATIONS ON INTERSPECIFIC IMMATURE COMPETITION

The same procedures and treatments were used to observe the behavior of second instar larvae (< 48 h old after molting from the first instar) of the 2 species of thrips. Each arena contained 2 individuals, i.e., 1 of each test species. There were 30 and 20 replications for honey and pollen as a food source, respectively. Behavioral parameters, including confrontation, food guarding, feeding, wandering, and resting also were measured as mentioned above.

BEHAVIORAL OBSERVATIONS ON INTRASPECIFIC ADULT COMPETITION

The same procedures as above were used to observe intraspecific behavioral parameters to assess the effects within each thrips species of intraspecies competition of adults. A total of 10 and 15 pairs of individuals were observed for F. occidentalis and F. intonsa, respectively, when honey was provided as a food source, whereas 20 pairs of individual F. occidentalis or F. intonsa were replicated on pollen. Behavioral parameters, including confrontation, food guarding, feeding, wandering, and resting also were measured as mentioned above. The value of each individual in each parameter in each species was averaged and used for further analysis.

STATISTICAL ANALYSIS

All data analyses were performed in SPSS (SPSS Inc., Chicago, Illinois, USA). Before analysis, all data sets were tested for normality using a Kolmogorov-Smirnov test (P < 0.05), and a Levene test was applied to test the data for homogeneity of variance using SPSS version 22. A nonparametric 2-way ANOVA was used according to Scheirer et al. (1976) if data did not meet the assumptions of parametric ANOVA and could not be adequately transformed. Pairwise comparisons were performed using the nonparametric Mann-Whitney U test (P < 0.05).

Results

EFFECTS OF INTERSPECIFIC ADULT COMPETITION ON REPRODUCTION

We found a significant difference in progeny production between the 2 species. In competition, the number of progeny were reduced by 79.0% in F. occidentalis and 43.0% in F. intonsa (species H = 18.249; df = 1; P < 0.001; competition H = 39.649; df = 1; P < 0.001; species × competition H = 2.051; df = 1; P = 0.099) (Fig. 1).

EFFECTS OF INTERSPECIFIC ADULT COMPETITION ON LONGEVITY

There also were significant effects of competition on adult longevity. Frankliniella intonsa lived 1.22 times longer than F. occidentalis when not in competition, but this increased to 1.58 times when in competition with F. occidentalis. Under competition conditions, the longevity of both species was reduced compared to when there was no competition. Longevity under competition was reduced by 41.0% and 23.0% for F. occidentalis and F. intonsa, respectively (species H = 17.210; df = 1; P < 0.001; competition H = 29.512; df = 1; P < 0.001; species × competition H = 6.981; df = 1; P = 0.005) (Fig. 2).

Fig. 1.

Effect of competition between Frankliniella occidentalis (FO) and Frankliniella intonsa (FI) on progeny production (mean + SE) in a leaf cage (hole covered with thrips-proof fabric in 0.7 cm diam cage).

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Fig. 2.

Effect of competition between Frankliniella occidentalis (FO) and Frankliniella intonsa (FI) on adult longevity (mean d + SE) in a micro-tube arena (2 mL capacity).

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EFFECTS OF INTERSPECIFIC ADULT AND IMMATURE COMPETITION ON AREA OF LEAF FEEDING

We found significant differences in the area of leaf feeding between the 2 life stages, i.e., adult and larvae, and between the interspecific competition and no-competition treatments (life stage H = 16.400; df = 1; P < 0.001; competition H = 11.035; df = 2; P < 0.002). However, no significance was found in the interaction of species and competition (H = 1.295; df = 2; P = 0.262). In both adults and larvae of the 2 thrips species, the area of feeding damage on leaves made by 1 individual of either species of F. occidentalis or F. intonsa alone (without competition) was not significantly different than that made by 2 individuals (1 each from the 2 species, in competition) as determined by post-hoc t-tests, except in the case of F. intonsa larvae (F. occidentalis adults t = 0.995; df = 18; P = 0.333; F. intonsa adults t = 1.940; df = 18; P = 0.068; F. occidentalis larvae t = 0.974; df = 18; P = 0.343; F. intonsa larvae t = 2.671; df = 18; P = 0.016) (Fig. 3). Also, when we summed the areas of feeding made by 1 individual from each species without competition, they were not significantly different from that made by 2 individuals (1 each from the 2 species) in competition (adults t = 1.607; df = 18; P = 0.126; larvae t = 1.306; df = 18; P = 0.208 in a post-hoc t-test) (Fig. 3).

EFFECTS OF INTERSPECIFIC COMPETITION ON PROGENY PRODUCTION ON POTTED BEAN PLANTS

There were significant effects on progeny production in terms of both male offspring (species: H = 9.414; df = 1; P = 0.001; competition: H = 17.488; df = 1; P < 0.001; species × competition: H = 19.240; df = 1; P < 0.001) and female offspring (species: H = 16.182; df = 1; P < 0.001; competition: H = 24.444; df = 1; P < 0.001; species × competition: H = 0.085; df = 1; P = 1.308) under competition in the cylindrical cage experiment. When in a competitive environment, the number of F. occidentalis male progeny produced was significantly reduced (by 85.8%), whereas numbers of F. intonsa male progeny produced were significantly increased (by 15.9%) (Fig. 4). When under competition, female progeny numbers were significantly reduced by 45.3 and 49.9% in F. occidentalis and F. intonsa, respectively (Fig. 4). Competition had no significant effect on male generation time in either F. occidentalis or F. intonsa (species: H = 0.074; df = 1; P = 1.416; competition: H = 0.088; df = 1; P = 1.288; species × competition: H = 0.088; df = 1; P = 1.288) (Fig. 5). However, competition significantly reduced the female generation time in both F. occidentalis and F. intonsa (species: H = 7.245; df = 1; P = 0.004; competition: H = 8.927; df = 1; P = 0.002; species × competition: H = 2.195; df = 1; P = 0.090) (Fig. 5).

Fig. 3.

Effect of competition between Frankliniella occidentalis (FO) and Frankliniella intonsa (FI) on leaf feeding in a leaf cage.

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Fig. 4.

Number (mean + SE) of next generation thrips progeny produced by Frankliniella occidentalis (FO) or Frankliniella intonsa (FI) female adult under competitive conditions in a cylindrical cage arena.

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INTERSPECIFIC BEHAVIOR OF ADULT FEMALES FEEDING ON HONEY

Frankliniella occidentalis and F. intonsa adult females showed different feeding behavior when provided with honey as the only food source. Significant differences between the species were observed in food guarding, feeding, and wandering (Table 2). Frankliniella intonsa guarded the honey 8.5 times longer (U = 128.500; P = 0.017) and fed 1.5 times longer (U = 127.000; P = 0.048) than did F. occidentalis. Also, F. intonsa wandered 40.4% as much as F. occidentalis (U = 107.000; P = 0.012). There were no significant differences in resting behavior between the 2 species (U = 158.500; P = 0.257).

Fig. 5.

Generation time (mean d + SE) of males and females of Frankliniella occidentalis (FO) and Frankliniella intonsa (FI) reproducing in a cylindrical cage arena.

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INTERSPECIFIC BEHAVIOR OF ADULT FEMALES FEEDING ON POLLEN

There was also a significant difference in food guarding behavior when pine pollen was provided as a food source (Table 2). Frankliniella intonsa guarded the pollen 42.8 times longer (U = 75.500; P = 0.000) than F. occidentalis (Table 2). No significant difference was found between species in feeding (U = 150.500; P = 0.180) or resting time (U = 152.500; P = 0.196). Frankliniella intonsa wandered only 39.8% as long as F. occidentalis (U = 95.500; P = 0.005).

INTERSPECIFIC BEHAVIOR OF IMMATURES FEEDING ON HONEY

Food guarding, feeding, and wandering times differed significantly between immature stages of the 2 species (Table 3). Frankliniella intonsa guarded 14.5 times longer (U = 344.000; P = 0.012), fed on honey only 32.2% as long as F. occidentalis (U = 252.500; P = 0.003), and wandered 1.78 times longer (U = 234.000; P = 0.001) than F. occidentalis. Resting time was not different between the species (U = 368.000; P = 0.223).

INTERSPECIFIC BEHAVIOR OF IMMATURES FEEDING ON POLLEN

None of the behaviors, i.e., food guarding (U = 180.500; P = 0.311), feeding (U = 165.500; P = 0.343), wandering (U = 169.000; P = 0.402), or resting (U = 195.500; P = 0.903) were significantly different between immature stages of the 2 species when feeding on pollen (Table 3).

INTRASPECIFIC BEHAVIOR OF ADULT FEMALES FED HONEY

Frankliniella occidentalis females engaged in 2.5 times more bouts of confrontation (U = 39.500; P = 0.044) than F. intonsa (Table 4). Frankliniella intonsa guarded honey 4.7 times longer than F. occidentalis (U = 50.500; P = 0.047). None of the other behaviors were significantly different between females of the 2 species feeding on honey (feeding U = 70.000; P = 0.782; wandering U = 62.000; P = 0.471; resting U = 57.000; P = 0.316).

INTRASPECIFIC BEHAVIOR OF ADULT FEMALES FED POLLEN

Among females provided with pollen, none of the behaviors measured showed any significant differences between species except for bouts of confrontation. No significant differences were found for other behaviors (food guarding U = 180.000; P = 0.152; feeding U = 188.500; P = 0.756; wandering U = 162.500; P = 0.310; resting U = 159.000; P = 0.257) (Table 4). Frankliniella occidentalis engaged in 2.6 times more bouts of confrontation (U = 90.500; P = 0.002) than did F. intonsa.

Discussion

Interspecific competition refers to competition for limiting resources such as food, nutrients, space, mates, or nesting sites between 2 or more species (Begon et al. 1996). Interspecific competition often negatively affects inferior species by reducing their population and growth rates, which in turn influences the population dynamics of both the superior and inferior species (Booth & Murray 2008). The competition can be either direct interference (contest) competition or indirect exploitative (scramble) competition. In interference competition, 1 conspecific or heterospecific organism prevents other organisms from using the resource, whereas organisms use up a limited resource in exploitation competition (Nicholson 1954). Interference competition includes direct killing, aggressive displacement behavior, and the production of chemicals (deterrents and pheromones) that hinder colonization, feeding, or oviposition (Kaplan and Denno 2007). On the other hand, exploitative competition includes resource depletion with severe consequences for most or all of the competing individuals, resulting in high density-dependent mortality and reproductive failure, drastic population crashes, and unstable population dynamics (Nicholson 1954). This study confirms that both interference and exploitation competition may occur between the 2 flower thrips F. occidentalis and F. intonsa, and F. intonsa seems to be a superior competitor to F. occidentalis. Adult F. intonsa guarded both honey and pollen longer, and fed longer on honey than F. occidentalis, and this dynamic may have led to lower reproduction and longevity in F. occidentalis than in F. intonsa in leaf cage and micro-tube arena experiments, respectively. These behaviors also may be the underlying reason for the competitive dominance of F. intonsa under field conditions. Adult F. intonsa may consume more food due to its higher reproductive activity compared to F. occidentalis. Ullah and Lim (2015) found that F. intonsa produced 46% more offspring per female than did F. occidentalis under fluctuating temperatures. As Murai (1988) reported, pollen feeding increases the number of eggs produced by F. intonsa, and therefore nutrients ingested during the adult stage might affect certain life table parameters, such as fecundity. This relationship between the populations of F. occidentalis and F. intonsa could be an example of the more general situation in which populations subjected to interference competition benefit from competition with another species. Food guarding is described here for the first time in thrips, although mate guarding has been documented in phlaeothripid thrips (Mound 1991; Tsuchida & Ohguchi 1998; Morris et al. 2002; Ullah & Lim 2015).

Table 2.

Interspecific behavior between Frankliniella occidentalis and Frankliniella intonsa female adults when either honey or pollen was provided as food in an experimental arena. Confronting behavior (mean ± SE) was recorded as number of confrontation bouts, but duration (mean s ± SE) was recorded for all other behaviors.

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Resource guarding has been studied extensively in different insect taxa. Social insects have a division of labor in which individuals specialize in reproduction, feeding, or guarding. Many terrestrial hemipterans exhibit maternal guarding behavior of eggs and young nymphs (Eickwort 1981). Eberhard (1975) found a pentatomid bug defending her eggs against the scelionid egg parasitoid. In dung beetles, male beetles guard dung balls while the female excavates sites for oviposition (Kanta 2013). Guarding behavior also has been observed in a female earwig, cockroaches, crickets, bugs, web spinners, and book lice (Kanta 2013).

Table 3.

Interspecific behavioral observation between Frankliniella occidentalis and Frankliniella intonsa larvae when either honey or pollen was provided as food in an experimental arena. Confronting behavior (mean ± SE) was recorded as number of confrontation bouts, but duration (mean s ± SE) was recorded for all other behaviors.

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Interestingly, the greater guarding behavior of F. intonsa larvae did not translate into more food consumed. On pollen, no statistical difference was found in any of the other parameters we assessed in the presence of competition. Although the underlying mechanism responsible for the asymmetry in competitive dominance between adult and larval stages is not known, larvae of F. occidentalis did better in competition with F. intonsa than did adults. Although F. occidentalis larvae did not guard food resources to any great extent, they fed on honey for a longer period of time than did larvae of F. intonsa (Table 3). Sometimes, confrontation also occurred close to a food source, and such behavior was especially severe on pollen among both adults and larvae. However, we observed that F. occidentalis larvae did not abandon a honey source when confronted by F. intonsa larvae, but rather made quick forays into the food. The reason for the more frequent confrontation on pollen than on honey can be explained by the fact that pollen is an important food source for thrips. Pollen is known to enhance survival and fecundity, and shorten development time (Abdullah et al. 2001), although pollen from different plant species varies in nutritional value (Lundgren 2009).

Interspecific competition of insects is 1 component of the biotic resistance of ecosystems (Northfield et al. 2011), and is affected by the availability of resources. Thus, the impact of invasive species may be reduced through competitive interactions with native species (Levine et al. 2004). In this study, we found that adults of the invasive F. occidentalis were inferior competitors to adults of the native F. intonsa on both food sources tested, and this competitive asymmetry may lead to the exclusion of F. occidentalis from some areas. Similar results were found by Paini et al. (2008), who showed that the native F. tritici is competitively superior to the invasive F. occidentalis in the eastern states of the US. In contrast, Northfield et al. (2011) reported that F. occidentalis is competitively superior to Frankliniella bispinosa (Morgan) (Thysanoptera: Thripidae), a common thrips in southern Florida, and suggested this greater competitive ability of F. occidentalis was a cause of its invasiveness. Increasing densities of F. occidentalis lowered the average reproductive success of F. bispinosa females, which may have caused F. occidentalis to be the better competitor (Northfield et al. 2011). Nevertheless, competition can be affected by other external factors, such as weather condition and insecticide application, and pesticide-mediated interspecific competition has recently been reported between local and invasive thrips species in China (Zhao et al. 2017).

Table 4.

Intraspecific behavioral observation between Frankliniella occidentalis and Frankliniella intonsa female adults when either honey or pollen was provided as food in an experimental arena. Confronting behavior (mean ± SE) was recorded as number of confrontation bouts, but duration (mean s ± SE) was recorded for all other behaviors.

t04_322.gif

Interspecific competition also can be important in other insects, such as the competitive superiority of the invasive mosquito Aedes albopictus (Skuse) (Diptera: Culicidae) over several native species, which appears to have aided the spread of this invasive pest (Levine 2004). Likewise, the invasive fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae) has extirpated many native ant species in the southeastern US due to the former lspecies' superiority in both resource exploitation and aggressiveness. Based on both empirical evidence and model prediction, Amarasekare (2002) suggested that successful invasive species should be superior at both exploitation and interference competition. Thus, our study suggests that the native F. intonsa provide resistance to invasion by F. occidentalis, because the invasive thrips is inferior at both interference and exploitation in the adult stage, although not in the larval stage. In interspecific competition, adult F. intonsa guarded the honey 6.3 times and pollen 71.3 times longer than in intraspecific competition, suggesting that it performs better in the presence of the opponent species F. occidentalis on both food sources, relative to competition from its own species.

In conclusion, when native F. intonsa in the adult or larval stage feed on honey, they are better at exploitation and interference competition than the invasive F. occidentalis. However, when the larval stages feed on pollen, this difference was not always observed between the 2 species. Interspecific competition between the 2 thrips species may be 1 of the underlying mechanisms explaining patterns of occurrence in the field. If the factors affecting the spread of invasive species can be better understood, invasions might be better predicted and pest management programs could be improved (Yasuda et al. 2004).

Acknowledgments

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry, and Fisheries through the Advanced Production Technology Development Program, funded by the Ministry of Agriculture, Food, and Rural Affairs (116089-03).

References Cited

1.

Abdullah AA, Zhang Z, Masters GJ, McNeill S. 2001. Euseius finlandicus (Acari: Phytoseiidae) as a potential biocontrol agent against Tetranychus urticae (Acari: Tetranychidae): life history and feeding habits on three different types of food.Experimental and Applied Acarology25: 833–847. Google Scholar

2.

Amarasekare P. 2002. Interference competition and species coexistence.Proceedings of the Royal Society of London B: Biological Sciences269: 2541–2550. Google Scholar

3.

Atakan E, Uygur S, Özgür AF. 1999. The weed host species of flower thrips, Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae).The Journal of Turkish Weed Science2: 32–38. Google Scholar

4.

Begon M, Harper JL, Townsend CR. 1996. Ecology: Individuals, Populations, and Communities.3rd edition.Blackwell Science Ltd., Cambridge, Massachusetts, USA. Google Scholar

5.

Booth DJ, Murray BR. 2008. Coexistence, pp. 664–668 In Jorgensen SE, Fath BD [eds.], Population Dynamics. Vol. 1, Encyclopedia of Ecology.Elsevier, Amsterdam, The Netherlands. Google Scholar

6.

Deligeorgidis PN, Ipsilandis CG, Vaiopoulou M, Deligeorgidis NP, Stavridis DG, Sidiropoulos G. 2006. The competitive relation between Frankliniella occidentalis and Thrips tabaci: the impact on life-cycle and longevity.Journal of Entomology3: 143–148. Google Scholar

7.

Eberhard MJW. 1975. The evolution of social behavior by kin selection.The Quarterly Review of Biology50: 1–33. Google Scholar

8.

Eickwort GC. 1981. Presocial insects, pp. 223–224 In Hermann HR [ed.], Social Insects. Vol. II.Academic Press, New York, USA. Google Scholar

9.

Kanta S. 2013. A Text Book of Insect Studies.Lulu Press Inc., Raleigh, North Carolina, USA. Google Scholar

10.

Kaplan I, Denno RF. 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory.Ecology Letters10: 977–994. Google Scholar

11.

Kirk WDJ, Terry LI. 2003. The spread of the western flower thrips Frankliniella occidentalis (Pergande).Agricultural Forest Entomology5: 301–310. Google Scholar

12.

Kwon OH, Jang KS, Won JG, Hwang JE, Jeon SG, Kwon TY. 2013. Seasonal occurrence and damage of major pests on red pepper in Northern Gyeongbuk Province.Proceeding of Biannual (Spring) Symposium of the Korean Society of Applied Entomology, p. 131. (Korean title and abstract.) Google Scholar

13.

Levine JM, Adler PB, Yelenik SG. 2004. A meta-analysis of biotic resistance to exotic plant invasions.Ecology Letters7: 975–989. Google Scholar

14.

Lewis T. 1997. Pest thrips in perspective, pp. 1–4 In Lewis T [ed.], Thrips as Crop Pests.CAB International, Wallingford, United Kingdom. Google Scholar

15.

Lim UT, Mainali BP. 2009. Optimum density of chrysanthemum flower model traps to reduce infestations of Frankliniella intonsa (Thysanoptera: Thripidae) on greenhouse strawberry.Crop Protection28: 1098–1100. Google Scholar

16.

Lim UT, Van Driesche RG, Heinz KM. 2001. Biological attributes of the nematode, Thripinema nicklewoodii, a potential biological control agent of western flower thrips.Biological Control22: 300–306. Google Scholar

17.

Lundgren JG. 2009. Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae.Biological Control51: 294–305. Google Scholar

18.

Mainali BP, Lim UT. 2008. Evaluation of chrysanthemum flower model trap to attract two Frankliniella thrips (Thysanoptera: Thripidae).Journal of Asia-Pacific Entomology11: 171–174. Google Scholar

19.

Mainali BP, Lim UT. 2010. Circular yellow sticky trap with black background enhances attraction of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae).Applied Entomology and Zoology45: 207–213. Google Scholar

20.

Moon HC, Cho IK, Im JR, Goh BR, Kim DH, Hwang CY. 2006. Seasonal occurrence and damage by thrips on open red pepper in Jeonbuk Province.Korean Journal of Applied Entomology45: 9–13. Google Scholar

21.

Morris DC, Schwarz MP, Crespi BJ. 2002. Pleometrosis in phyllode-glueing thrips (Thysanoptera: Phlaeothripidae) on Australian Acacia.Biological Journal of the Linnean Society75: 467–474. Google Scholar

22.

Mound L. 1991. Secondary sexual character variation in male Actinothrips species (Insecta: Thysanoptera), and its probable significance in fighting behaviour.Journal of Natural History25: 933–943. Google Scholar

23.

Murai T. 1988. Studies on the ecology and control of flower thrips, Frankliniella intonsa (Trybom).Bulletin of the Shimane Agricultural Experiment Station23: 1–73. Google Scholar

24.

Nakahara S, Foottit RG. 2007. Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae), an invasive insect in North America.Proceedings of the Entomological Society of Washington109: 733–734. Google Scholar

25.

Nicholson AJ. 1954. An outline of the dynamics of animal populations.Australian Journal of Zoology2: 9–65. Google Scholar

26.

Northfield TD, Paini DR, Reitz SR, Funderburk JE. 2011. Within plant interspecific competition does not limit the highly invasive thrips, Frankliniella occidentalis in Florida.Ecological Entomology36: 181–187. Google Scholar

27.

Paini DR, Funderburk JE, Reitz SR. 2008. Competitive exclusion of a worldwide invasive pest by a native. Quantifying competition between two phytophagous insects on two host plant species.Journal of Animal Ecology77: 184–190. Google Scholar

28.

Scheirer CJ, Ray WS, Hare N. 1976. The analysis of ranked data derived from completely randomized factorial designs.Biometrics32: 429–436. Google Scholar

29.

Teulon DAJ, Nielsen MC. 2005. Distribution of western (glasshouse strain) and intonsa flower thrips in New Zealand.New Zealand Plant Protection58: 208–212. Google Scholar

30.

Tsuchida K, Ohguchi S. 1998. Male mating behavior and female-biased sex ratio of the Japanese gall-forming thrips Ponticulothrips diospyrosi (Thysanoptera: Phlaeothripidae).Annals of the Entomological Society of America91: 27–32. Google Scholar

31.

Ullah MS, Lim UT. 2015. Life history characteristics of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae) in constant and fluctuating temperatures.Journal of Economic Entomology108: 1000–1009. Google Scholar

32.

van Rijn PCJ, Mollema C, Steenhuis-Broers GM. 1995. Comparative life history studies of Frankliniella occidentalis and Thrips tabaci (Thysanoptera: Thripidae) on cucumber.Bulletin of Entomological Research85: 285–297. Google Scholar

33.

Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T. 2004. Asymmetric larval interactions between introduced and indigenous ladybirds in North America.Oecologia141: 722–731. Google Scholar

34.

Zhao X, Reitz SR, Yuan H, Lei Z, Paini DR, Gao Y. 2017. Pesticide-mediated interspecific competition between local and invasive thrips pests.Scientific Reports7: 40512. https://doi.org/10.1038/srep40512 Google Scholar
Mohammad Mosharof Hossain Bhuyain and Un Taek Lim "Interference and Exploitation Competition between Frankliniella occidentalis and F. intonsa (Thysanoptera: Thripidae) in Laboratory Assays," Florida Entomologist 102(2), 322-328, (14 June 2019). https://doi.org/10.1653/024.102.0206
Published: 14 June 2019
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