Open Access
Translator Disclaimer
1 January 2014 Seasonal Dynamics of the Flower Head Infestation of Smallanthus maculatus by Two Nonfrugivorous Tephritids
José F. Dzul-Cauich, Vicente Hernández-Ortiz, Victor Parra-Tabla, Victor Rico-Gray
Author Affiliations +
Abstract

Seasonal dynamics of the capitula infested by Dictyotrypeta sp. and Rhynencina spilogaster (Steyskal) (Diptera: Tephritidae) was evaluated throughout the flowering cycle of their host plant the sunflower, Smallanthus maculatus (Cavanilles) Robinson (Asterales: Asteraceae). In central Veracruz, Mexico, along 16 consecutive weeks, a total of 1,017 mature capitula were collected, recording the presence and abundance of immature stages (larvae and pupae) and their related parasitoids. Both fly species were present throughout the entire season, with overall Infestation of 51.5% of the capitula examined. However, Dictyotrypeta sp. infested 11.3%, representing about one-fifth of them, and R. spilogaster was most abundant infesting four times as many capitula (42.9%), whereas both species were found together in only 2.6% of the capitula examined. Based on the temporal occurrence of larvae and pupae into flower heads as well as their associated parasitoids and times of emergence, Dictyotrypeta sp. had two yearly generations, and It seems that the second generation could enter a seasonal diapause; in contrast, R. spilogaster was a univoltine species that entered diapause that lasted until the next year.

Fruit flies of the subfamily Tephritinae (Diptera: Tephritidae) are widely distributed in temperate and subtropical regions of the world; however, most studies of their biology and ecology have been focused on Nearctic species inhabiting northern temperate regions (Headrick and Goeden 1998). On the contrary, few studies have documented the relationship between nonfrugivorous tephritids and their host plants in Neotropical species, in many cases, recording the first biological data and the findings of new taxa (Prado et al. 2002, 2004; Almeida et al. 2006; Norrbom and Prado 2006; Norrbom et al. 2010).

In the central region of Veracruz, Mexico, an undescribed species of Dictyotrypeta and Rhynencina spilogaster (Steyskal) (Diptera: Tephritidae) were found feeding on the capitula of Smallanthus maculatus (Cavanilles) Robinson (Asterales: Asteraceae) (V.H.O., unpublished data). The genus Dictyotrypeta comprises six species of exclusive Neotropical distribution stretching from Mexico to Argentina, with the recent inclusion of two further species, Tetreuaresta crenulata (Wulp) and Baryplegma incisa Wulp (Norrbom et al. 1998, 2010). The limited biological data available indicate that Dictyotrypeta atacta (Hendel) feeds on the capitula of Lessingianthus, Proteopsis, and Trichogonia (Asteraceae) in Brazil (Prado et al. 2002), whereas Dictyotrypeta incisa has been reared from the capitula of S. maculatus and Smallanthus riparius (Kunth) Harold Robinson in Mexico and Guatemala (Norrbom et al. 2010). The genus Rhynencina contains four Neotropical and one Nearctic species (Norrbom et al. 1998). The biology of these species is also poorly understood, as only the host plant of Rhynencina emphanes (Steyskal) is known, as these develop on Espeletia sp. flowers in Colombia (Freidberg and Norrbom 2000); likewise, Rhynencina longirostris Johnson feeds on Smallanthus uvedalius (L.) Mackenzie ex Small in North America, whose biology has already been studied (Steck and Sutton 2000, Steck et al. 2003).

The presence of Tephritinae species on their host plants is influenced by several characteristics, for instance, plant height, flowering time, and spatial host abundance (Walton et al. 1990, Rivero-Lynch and Jones 1993, Fondriest and Price 1996, Williams et al. 2001, Walker et al. 2008), in addition to climatic features as precipitation and temperature (Solbreck and Sillén-Tullberg 1986, Milton 1995). Some authors have reported significant differences in the levels of parasitism under natural conditions, suggesting that parasitism rates may be associated with host range and the particular biology of each fly species involved (Duan and Messing 1998, Alyokhin and Messing 2003, Knio et al. 2007, Edwards et al. 2009). Especially, seasonal variation during flowering season and development time of capitula may influence their rates of infestation and life cycles (English-Loeb and Karban 1992, Alyokhin et al. 2002, Woods et al. 2008, Duguma et al. 2009). However, in most of the studies, flower head infestation throughout continuous seasonal cycle has not been assessed, which allows monitoring temporal changes on infestation patterns. The aim of this study was to assess the seasonal dynamics of infestation yielded by Dictyotrypeta sp. and R. spilogaster on the capitula of S. maculatus, as well as recording the occurrence of natural parasitism along its entire flowering season, in a coffee-growing region of central Mexico.

Materials and Methods

Study Area. The study sites were located in the montane cloud forest in the central region of Veracruz. Currently, this kind of vegetation occurs as a fragmented community, composed of natural forest patches and secondary growth species, particularly as a result of the presence of shaded coffee plantations and grasslands (Williams-Linera 2007). Field work was conducted from August to November 2008, in the neighboring towns of Coatepec (19° 27′ N, 96° 06′ W; 1,252 m altitude) and Teocelo (19° 23′ N, 96° 58′ W; 1,218 m altitude), both with similar climatic conditions. Highest rainfall occurred in June (571.5 mm), and the driest month was March (24.2 mm). The highest average temperature occurred in May (24.9°C), while the lowest was recorded in November (18.3°C) (CONAGUA 2008) (Fig. 1).

Fig. 1.

Climatic conditions of monthly rainfall (mm) and average temperatures (°C) in the studied locality during the yearly cycle January–December 2008.

f01_01.jpg

The Host Plant. S. maculatus is a Mesoamerican plant that occurs throughout extensive areas of Mexico, including the state of Veracruz, but its range goes as far as Panama. It is a herbaceous perennial, 1 to 2 m height (exceptionally reaching up to 5 m), with flower heads ranging from 1 to 2 cm in width, found growing in groups or panicles and rarely solitary (McVaugh 1984, Villaseñor and Espinosa 1998, Rzedowski 2001). Previous observations in the study area showed that S. maculatus grows in open disturbed areas, on roadsides, and coffee plantations, appearing in irregular groups from a few individuals up to several dozens of them, with a flowering cycle starting from July–August stretching to November–December (V.H.O., unpublished data).

Flower Head Sampling. During the flowering season of the host plant, 16 weekly collections of mature capitula were done, characterized by their ligulate and disc flowers dry, and by the presence of peripheral mature achenes. Assessing the extent of flower head infestation, collections were random among plants, and sample size was determined by the abundance and availability of mature capitula. Each time, the analyzed samples were obtained from different groups of plants, because S. maculatus is a weed periodically removed by coffee growers. Samples were placed in fine mesh bags and transported to the laboratory, where they were separated and placed in plastic chambers of 250 ml with adequate ventilation, and all information was recorded in a data matrix. Every week, each capitulum and its mature achenes were carefully dissected under the stereomicroscope, to detect and quantify the presence of immature stages. Part of the larvae and pupae sampled were kept in rearing chambers until emergence of adults. Identification of the specimens was done with reference to the characteristic damage into the achenes or receptacle, and by the size and color of pupae. Voucher adult specimens were pinned and deposited in the Entomological Collection of the Instituto de Ecología (IEXA), whereas botanical specimens were placed at the Herbarium of the Instituto de Ecología (XAL), both of these housing Instituto de Ecología A.C. (INECOL) institutional collections (Xalapa, Mexico).

Statistical Analysis. To evaluate the weekly proportion of infested capitula, linear regression of arcsine-transformed data (arcsin √proportion) were performed; because flower head production exhibited a lot of variation along the sampling period, a correction factor was applied as follows: CF = √1–n/N, where n is the weekly sample size and N the population size sampled (Zar 2010). Mean of individuals per sample within capitula was estimated by linear regression analysis (including polynomial of second and third order), and likelihood-ratio tests were used for comparisons of these models (Crawley 2007). Possible relationships between some of the dependent variables along the seasonal cycle (e.g., density of individuals per capitulum and fly species, and number of individuals per fly species) were assessed using Spearman's rank correlations. All tests were performed using the R program (Development Core Team 2011).

Results

During the annual flowering cycle of S. maculatus, 16 weekly samples accounted for 1,017 of mature capitula. Infestations by two species occurred throughout the entire season, occupying 51.5% of the flower heads. However, Dictyotrypeta sp. infested 11.3%, representing about one-fifth of all infested capitula; whereas R. spilogaster resulted more abundant infesting four times as many capitula (42.8%), and both species were found together in only 2.6% of the capitula examined (Table 1).

Seasonality. The accumulated infestation by Dictyotrypeta sp. showed differences in terms of abundance, presenting low rates of infested capitula (13.9%) during the first half of the cycle (August–September), with a notable increase in the second half (October–November), occupying 86.1% of them. On the other hand, in R. spilogaster, the highest infestations occurred during the first half of the season (64.2%), decreasing in the second half to 35.8% (Fig. 2). The linear regression analysis showed that the capitula infested by Dictyotrypeta sp. increased significantly toward the end of the season (R 2 = 0.28, F1,14 = 5.55, P = 0.033), contrasting with a decrease in the infestation by R. spilogaster, which also proved to be significant (R 2 = 0.34, F1,14 = 7.45, P = 0.016) to the end of the flowering cycle (Fig. 3).

Average density of individuals per capitulum infested by R. spilogaster was 2.83 individuals per capitulum (± 1.8 SD), the most frequent ratio was 2–3 specimens observed in 41.5% of cases, a single specimen in 28.7%, 4–6 specimens in 25%, and 7–10 specimens in only 4.8% of the capitula. High densities of individuals (≥ 3 individuals per capitula) mainly occurred through September and early October. In contrast, lower densities were observed starting August and extending from late October to November. Comparisons of the rate of individuals observed throughout the flowering season, using the third-order polynomial regression analysis, showed significant differences (R 2 = 0.55, F3,12 = 4.98, P = 0.017; Fig. 4), and these infestation rates were positively correlated with increases in the capitula infested (Spearman's rank correlation, ρ = 0.70, P = 0.001).

Table 1.

Capitula infested by two tephritid species throughout the flowering season of S. maculatus

t01_01.gif

Fig. 2.

Proportion of the capitula infested by Dictyotrypeta sp. and Rhynencina spilogaster along the flowering season of S. maculatus.

f02_01.jpg

Meanwhile, the average density of Dictyotrypeta sp. individuals was 1.40 individuals per capitulum (± 0.7 SD); thus, most of the capitula was accounted to be infested by a single specimen in 68.7% of cases, two specimens in 23.5%, and 3–5 specimens in only 7.8% of the capitula. However, tested comparisons of the rate of individuals inside the capitula throughout the flowering season neither showed a correlation (P> 0.1; Fig. 4) nor was there a correlation between average of individuals and the number of capitula infested (Spearman's rank correlation, ρ = 0.31, P = 0.12).

Immature Stages and Infestation. Total infestation by Dictyotrypeta sp. was represented by 162 specimens (larvae 15.4%, pupae 84.6%), and correlation analysis showed that individual abundance increased significantly toward the second half of the season (Spearman's rank correlation, ρ = 0.51, P = 0.019). Larvae were absent from the initial two-thirds of the season, appearing later into this period; meanwhile, pupae were observed throughout the entire cycle, with the highest abundance focused in the second half (Fig. 5A). Both larvae and pupae were found mostly within the mature achenes (82.7%), but they were also discovered inside the receptacle (17.3%). Achenes infested by larvae of this species showed a typical damage, indicated by an orifice covered with waste from feeding, while damage to the receptacle was recognized by the presence of galleries that lead toward an achene.

R. spilogaster was recorded by a total of 1,234 individuals, without significant variations along the entire season (Spearman's rank correlation, δ = -0.41, P = 0.055). In this case, most individuals recovered were larvae (80.2%) appearing throughout the flowering period, while pupae accounted for only 19.8% of the specimens, especially observed in the early weeks of the flowering season (Fig. 5B). Larvae and pupae were found exclusively within the mature achenes without apparent traces of infestation, so its presence was detected just dissecting each one of them.

Parasitism. To assess natural parasitism in Dictyotrypeta sp., 118 pupae were kept alive in emergence chambers. Here, 22 adult flies were obtained in a rate of emergence of 15.7 days (± 3.1 SD), while from remaining pupae 88 Hymenopteran parasitoids were recovered, representing 74.6% of parasitism in the sample. All parasitoid specimens belong to five species from the families Figitidae sp. 1 (48) and Pteromalidae sp. 1 (37), followed by three species of Eupelmidae (1), Eurytomidae (1), and Eulophidae (3), respectively. The average times of emergence were as follows: Figitidae sp. 1 = 79.7 days (± 35.4 SD) and Pteromalidae sp. 1 = 50.9 days (± 34.3 SD), while emergence times of the single specimens of Eulophidae, Eupelmidae, and Eurytomidae ranged from 15 to 19 days (Fig. 6A). All parasitoids were reared from a single puparium, excluding the three Eulophid specimens that showed a gregarious parasitism.

Fig. 3.

Correlation analysis of the proportion of capitula infested by two Tephritinae species throughout the flowering cycle of S. maculatus (August–November 2008).

f03_01.jpg

Fig. 4.

Analysis of the density of tephritid individuals infesting the capitula of S. maculatus (August–November 2008): mean of individuals observed in R. spilogaster showed significant differences (P < 0.05).

f04_01.jpg

Likewise, 135 puparia of R. spilogaster were kept in the emergence chambers, and 69 of them remained alive for 303.9 days (± 71.2 SD), whereas 66 parasitoids of Pteromalidae sp. 2 emerged from the other puparia, which came into diapause because adults lasted for 303 days (± 134.2 SD) after collection, and accounted for 48.9% of parasitism in the sample (Fig. 6B).

Discussion

Insects that share food resources follow two survival strategies, either an avoidance strategy or maximizing their competitiveness (Zwölfer 1979). In Tephritinae infesting a single host, phenomena of interspecific competition have been reported, but there are also evidences of avoidance strategies during the seasonality of the host (Michaelis 1986, Straw 1989a, Knio et al. 2001, Story 2002, Holt and Zwölfer 2007). Results of this study showed differences in temporary patterns of infestation by Dictyotrypeta sp. and R. spilogaster, suggesting distinct strategies of resource exploitation, as only 2.6% of the capitula were simultaneously occupied by two species.

The flowering season of the host offered a constant resource supply for both tephritids; however, R. spilogaster presented populations approximately four times larger than Dictyotrypeta sp. These results can be related to the particular biology of each species, because the mature larvae of the former are small-size specimens, and each individual feeds exclusively on a single achene. Although the larvae of the latter are twice as large, their food requirements are greater, and therefore, it was found in the achenes and in the receptacle. The habit of feeding in the receptacle is a facultative mode of resource exploitation, and it may provide additional nutrients for continued development within the capitulum (Knio et al. 2001).

Fig. 5.

Abundance of larvae and pupae recovered from 16 samples along flowering season of S. maculatus in central Veracruz, México: (A) Dictyotrypeta sp. and (B) R. spilogaster.

f05_01.jpg

The average density of 1.4 individuals observed in Dictyotrypeta sp. suggests that females usually lay 1–2 eggs per capitulum and probably do so during its early development, because damage was always observed in the center of the receptacle, and in most of the cases, a later transferral took place to the achene. Low densities per capitulum indicated a small clutch size as a strategy to maximize the probability that offspring found enough food resources for development, but it may also indicate the existence of a marking pheromone after oviposition, which would be recognized by conspecific females (Straw 1989b; Pittara and Katsoyanos 1990; Lalonde and Roitberg 1992a, b). In the case of R. spilogaster, the average density of 2.8 individuals per capitulum suggests that females made multiple ovipositions, depositing a single egg in each achene, which provides enough resources for individual development, whereas an increase in the density of individuals per capitulum was correlated with population growth along the season.

In Dictyotrypeta sp., only pupae were found at the beginning of the season, suggesting that oviposition may occur during the early development of the capitula. However, to the end of the season (S10–S16), larvae also appeared, indicating a second generation of this species. From the start of the season, some adults emerged in an average time of 15 days (range 9–22), whereas during the second half of the season, the two most abundant parasitoid species emerged in an elapsed time of 50–79 days, suggesting that second generation could enter diapause. Contrastingly, R. spilogaster is clearly a univoltine species with a long life cycle that entered diapause, because larvae as pupae were present throughout the entire season, and larvae were represented by 80.2% of the specimens, while 19.8% were pupae remaining viable for up to 303 days on average. Nearly identical times of emerged parasitoids were also recorded. Similar observations were done in the North American sister species, R. longirostris that breeds in the capitula of S. uvedalius, showing that flies and parasitoids exhibited a single annual generation (Steck et al. 2003).

Mature achenes per capitulum produced by S. maculatus were estimated in 13.03 (± 2.4 SD; N = 276), so the total number of damaged achenes by two tephritids was 20.6% (Dictyotrypeta sp. 2.02% and R. spilogaster 18.6%). It means that nearly one-fifth of the seeds were predated, which represents a relatively low impact on the reproductive success of the host plant. However, the damage to the receptacle by the former species may have an indirect effect on the seed production, because studies on other receptacle feeders, such as Chaetostomella cylindrica and Terellia colon, suggest that they may restrict the flow of nutrients, reducing the fitness and weight of healthy seeds (Kinkorová and Mícková 2006, Koprdova and Martínková 2006).

Fig. 6.

Parasitoids recovered and times of emergence in two Tephritinae species: (A) Figitidae sp. 1 and Pteromalidae sp. 1, parasites of Dictyotrypeta sp. and (B) Pteromalidae sp. 2, parasite of R. spilogaster.

f06_01.jpg

There are evidences of high spatial and temporal variability in predispersal seed predation by insect herbivores (Kolb et al. 2007, Abdala-Roberts et al. 2010). Moreover, the action of the natural parasitism found in some Tephritinae species used for control of weeds could also exert a reduction in their effectiveness, limiting their establishment and impact as agents for biological control (Marshall et al. 2004, Edwards et al. 2009).

Results of multiple interactions between these tephritids and their parasitoids were restricted to single-year sampling at a single locality. Further research on several cycles and localities are required to make generalizations of these assertions. Multiple interspecific interactions may also affect whether there is a reduction or an increase in seed predation (Lamp and McCarty 1982, Groenteman et al. 2007, Tonkel and Piper 2009). Moreover, species of Coleoptera and Lepidoptera were observed either in the achenes, the receptacle, or both, whose trophic interactions are being assessed as a whole (V.H.O., unpublished data). This will provide a comprehensive view of the impact of these herbivores on the reproductive success of the host plant.

Acknowledgments

This research is part of the thesis of master of science degree of the senior author (J.D.C.) at the INECOL, México, under the advisory of V.H.O. J.D.C. thanks the National Council for Science and Technology (CONACyT, México) for the scholarship provided for carrying out postgraduate studies (Ref: no. 212521), as well as the monthly stipend for academic residency (Ref: Inecol SP/CAP/10-106). This is a contribution to the project Insect—Plant Interactions supported with funds of the INECOL (Ref: VHO-10128).

References Cited

1.

L. Abdala-Roberts , V. Parra-Tabla , C. Díaz-Castelazo , L. Salinas-Peba , and G. H. Delfín . 2010. Spatial variation in the strength of a trophic cascade involving Ruellia nudiflora (Acanthaceae), an insect seed predator and associated parasitoid fauna in Mexico. Biotropica 42: 180–187. Google Scholar

2.

A. M. Almeida , C. R. Fonseca , P. I. Prado , M. Almeida-Neto , S. Diniz , U. Kubota , M. R. Braun , L. G. Raimundo , L. A. Anjos , T. G. Mendonça , et al. 2006. Assemblages of endophagous insects on Asteraceae in São Paulo Cerrados. Neotrop. Entomol. 35: 458–468. Google Scholar

3.

A. V. Alyokhin , and R. H. Messing . 2003. Parasitism of Hawaiian non-frugivorous fruit flies (Diptera: Tephritidae) by an exotic parasitoid, Eurytoma tephritidis Fullaway (Hymenoptera: Eurytomidae). Proc. Hawaiian Entomol. Soc. 36: 29–37. Google Scholar

4.

A. V. Alyokhin , R. H. Messing , and J. J. Duan . 2002. Infestation of Elephantopus mollis (Asteraceae) flowerheads by Tetreuaresta obscuriventris (Diptera: Tephritidae) on Kauai, Hawaiian islands. Entomol. News 113: 247–252. Google Scholar

5.

(CONAGUA) Comisión Nacional del Agua. 2008. Weather information provided by the National Water Commission. Organismo Cuenca Golfo-Centro, Xalapa, Veracruz, México. Google Scholar

6.

M. J. Crawley 2007. The R book. John Wiley, West Sussex, England. Google Scholar

7.

Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria, ( http://www.R-project.org) (accessed 22 June 2011, version 2.13.0). Google Scholar

8.

J. J. Duan , and R. H. Messing . 1998. Effect of Tetrastichus giffardianus (Hymenoptera: Eulophidae) on nontarget flowerhead-feeding tephritids (Diptera: Tephritidae). Environ. Entomol. 27: 1022–1028. Google Scholar

9.

D. Duguma , T. J. Kring , and R. N. Wiedenmann . 2009. Seasonal dynamics of Urophora quadrifasciata on spotted knapweed in the Arkansas Ozarks. Can. Entomol. 141: 70–79. Google Scholar

10.

P. B. Edwards , R. J. Adair , R. H. Holtkamp , W. J. Wanjura , A. S. Bruzzese , and R. I. Forrester . 2009. Impact of the biological control agent Mesoclanis polana (Tephritidae) on bitou bush (Chrysanthemoides monilifera subsp. rotundata) in eastern Australia. Bull. Entomol. Res. 99: 51–63. Google Scholar

11.

G. M. English-Loeb , and R. Karban . 1992. Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae). Oecologia 89: 588–595. Google Scholar

12.

S. M. Fondriest , and P. W. Price . 1996. Oviposition site resource quantity and larval establishment for Orellia occidentalis (Diptera: Tephritidae) on Cirsium wheeleri. Environ. Entomol. 25: 321–326. Google Scholar

13.

A. Freidberg , and A. L. Norrbom . 2000. A generic reclassification and phylogeny of the tribe Myopitini (Tephritinae), pp. 581–627. In M. Aluja and A. L. Norrbom (eds.), Fruit flies (tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, Florida, U.S.A. Google Scholar

14.

R. Groenteman , D. Kelly , S. V. Fowler , and G. W. Bourdôt . 2007. Interactions between nodding thistle seed predators. New Zeal. Plant Prot. 60: 152–157. Google Scholar

15.

D. Headrick , and R. D. Goeden . 1998. The biology of nonfrugivorous tephritid fruit flies. Ann. Rev. Entomol. 43: 217–241. Google Scholar

16.

C. Holt , and H. Zwölfer . 2007. Life history and behaviour of Terellia longicauda (Meigen), a highly specialised tephritid of the woolly thistle, Cirsium eriophorum. Stud. Dipterol. 14: 331–340. Google Scholar

17.

J. Kinkorová , and M. Mícková . 2006. Life history of the European tephritid fly Chaetostomella cylindrica (Diptera: Tephritidae) and its possible use as a biocontrol agent in the USA. Proc. Entomol. Soc. Wash. 108: 51–61. Google Scholar

18.

K. M. Knio , R. D. Goeden , and D. H. Headrick . 2001. Resource utilization in the sibling species Trupanea nigricornis (Coquillett), a polyphage, and the narrowly oligophagous T. bisetosa (Coquillett) (Diptera: Tephritidae) in Southern California. Proc. Entomol. Soc. Wash. 103: 946–961. Google Scholar

19.

K. M. Knio , D. Goeden , and D. H. Headrick . 2007. Natural enemies of the cryptic and sympatric species, Trupanea nigricornis (Coquillett), a polyphage, and the narrowly oligophagous T. bisetosa (Coquillett) (Diptera: Tephritidae). Proc. Entomol. Soc. Wash. 109: 187–197. Google Scholar

20.

A. Kolb , J. Ehrlén , and O. Eriksson . 2007. Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspect. Plant Ecol. Evol. Syst. 9: 79–100. Google Scholar

21.

S. Koprdova , and Z. Martínková . 2006. Pre-dispersal predation and seed damage of Centaurea scabiosa L. (Asteraceae). J. Plant Dis. Prot. 20: 305–308. Google Scholar

22.

R. G. Lalonde , and B. D. Roitberg . 1992a. Field studies of seed predation in an introduced weedy thistle. Oikos 65: 363–370. Google Scholar

23.

R. G. Lalonde , and B. D. Roitberg . 1992b. Host selection behavior of a thistle-feeding fly: choices and consequences. Oecologia 90: 534–539. Google Scholar

24.

W. O. Lamp , and M. K. McCarty . 1982. Biology of predispersal seed predators of platte thistle, Cirsium canescens. J. Kansas Entomol. Soc. 55: 305–316. Google Scholar

25.

J. M. Marshall , R. A. Burks , and A. J. Storer . 2004. First host record for Pteromalus cardui (Hymenoptera: Pteromalidae) on Urophora quadrifasciata (Diptera: Tephritidae) in spotted knapweed (Centaurea biebersteinii, Asteraceae) in Michigan, U.S. A. Entomol. News 115: 273–278. Google Scholar

26.

R. McVaugh 1984. Polymnia. Flora Novo-Galiciana: a descriptive account of the vascular plants of western Mexico. The University of Michigan Press. Ann Arbor, Michigan, U.S.A. Google Scholar

27.

H. Michaelis 1986. Competition of Urophora stylata F. and Terellia serratulae L. (Dipt. Tephritidae) in the flowerheads of Cirsium vulgare, pp. 191–199. In M. Mangel (ed.), Pest control: operations and systems analysis in fruit fly management. Springer-Verlag, Berlin, Heidelberg, New York. Google Scholar

28.

S. J. Milton 1995. Effects of rain, sheep and tephritid flies on seed production of two arid Karoo shrubs in South Africa. J. Appl. Ecol. 32: 137–144. Google Scholar

29.

A. L. Norrbom , and P. I. Prado . 2006. New genera and host plant records of Asteraceae-feeding Tephritidae (Diptera) from Brazil. Zootaxa 1139: 1–17. Google Scholar

30.

A. L. Norrbom , L. E. Carroll , F. C. Thompson , I. M. White , and A. Freidberg . 1998. Systematic database of names, pp. 65–251. In F. C. Thompson (ed.), Fruit fly expert identification system and systematic information database. Backhuys Publishers, Leiden, Netherlands. Google Scholar

31.

A. L. Norrbom , B. D. Sutton , G. J. Steck , and J. Monzón . 2010. New genera, species and host plant records of Nearctic and Neotropical Tephritidae (Diptera). Zootaxa 2398: 1–65. Google Scholar

32.

I. S. Pittara , and B. I. Katsoyannos . 1990. Evidence for a host-marking pheromone in Chaetorellia australis. Entomol. Exp. Appl. 54: 287–295. Google Scholar

33.

P. I. Prado , T. M. Lewinsohn , A. M. Almeida , A. L. Norrbom , B. D. Buys , A. C. Macedo , and M. B. Lopes . 2002. The fauna of Tephritidae (Diptera) from capitula of Asteraceae in Brazil. Proc. Entomol. Soc. Wash. 104: 1007–1028. Google Scholar

34.

P. L. Prado , A. L. Norrbom , and T. M. Lewinsohn . 2004. New species of Tomoplagia Coquillett (Diptera: Tephritidae) from capitula of Asteraceae in Brazil. Neotrop. Entomol. 33: 189–211. Google Scholar

35.

A. P. Rivero-Lynch , and T. H. Jones . 1993. The choice of oviposition site by Terellia ruficauda on Cirsium palustre. Acta Oecol. 14: 643–651. Google Scholar

36.

J. Rzedowski 2001. Compositae, pp. 764–975. In G. Calderón and J. Rzedowski (eds.), Flora fanerogámica del Valle de México, segunda edición. Instituto de Ecología AC y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Pátzcuaro, México. Google Scholar

37.

C. Solbreck , and B. Sillén-Tullberg . 1986. Seed production and seed predation in a patchy and time-varying environment. Dynamics of a milkweedtephritid fly system. Oecologia 71: 51–58. Google Scholar

38.

G. J. Steck , and B. D. Sutton . 2000. New records for Tephritidae (Diptera) in Great Smoky Mountains National Park. Insecta Mundi 14: 256. Google Scholar

39.

G. J. Steck , B. D. Sutton , and D. Defoe . 2003. Biology of Rhynencina longirostris Johnson (Diptera: Tephritidae). Proc. Entomol. Soc. Wash. 105: 542–547. Google Scholar

40.

J. Story 2002. Spotted knapweed, pp. 169–180. In F. V. Driesche, B. Blossey, M. Hoodle, S. Lyon, and R. Reardon (eds.), Biological control of invasive plants in the eastern United States. United States Department of Agriculture, Forest Service Publication, Morgantown, West Virginia, U.S.A. Google Scholar

41.

N. A. Straw 1989a. The timing of oviposition and larval growth by two tephritid fly species in relation to host-plant development. Ecol. Entomol. 14: 443–454. Google Scholar

42.

N. A. Straw 1989b. Evidence for an oviposition-deterring pheromone in Tephritis bardanae (Schrank) (Diptera: Tephritidae). Oecologia 78: 121–130. Google Scholar

43.

K. C. Tonkel , and G. L. Piper . 2009. Patterns in resource partitioning by insect biological control agents of yellow starthistle (Centaurea solstitialis L.) in Washington. Northwest Sci. 83: 16–24. Google Scholar

44.

J. L. Villaseñor , and F. J. Espinosa . 1998. Catálogo de Malezas de México. Universidad Nacional Autónoma de México and Fondo de Cultura Económica. México D.F., México. Google Scholar

45.

M. Walker , S. E. Hartley , and T. H. Jones . 2008. The relative importance of resource and natural enemies in determining herbivore abundance: thistles, tephritids and parasitoids. J. Anim. Ecol. 77: 1063–1071. Google Scholar

46.

R. Walton , A. E. Weis , and J. P. Lichter . 1990. Oviposition behavior and response to plant height by Eurosta solidaginis Fith (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 83: 509–514. Google Scholar

47.

I. S. Williams , T. H. Jones , and S. E. Hartley . 2001. The role of resources and natural enemies in determining the distribution of an insect herbivore population. Ecol. Entomol. 26: 204–211. Google Scholar

48.

G. Williams-Linera 2007. El bosque de niebla del centro de Veracruz: ecología, historia y destino en tiempos de fragmentación y cambio climático. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad e Instituto de Ecología AC, Xalapa, México. Google Scholar

49.

D. M. Woods , M. J. Pitcairn , D. B. Joley , and C. E. Turner . 2008. Seasonal phenology and impact of Urophora sirunaseva on yellow starthistle seed production in California. Biol. Control 47: 172–179. Google Scholar

50.

J. H. Zar 2010. Biostatistical analysis, 5th ed. Prentice Hall, Upper Saddle River, New Jersey, U.S.A. Google Scholar

51.

H. Zwölfer 1979. Strategies and counter-strategies in insect population systems competing for space and food in flower heads and plant galls. Fortschr. Zool. 25: 331–353. Google Scholar
© The Author 2014. Published by Oxford University Press on behalf of the Entomological Society of America.
José F. Dzul-Cauich, Vicente Hernández-Ortiz, Victor Parra-Tabla, and Victor Rico-Gray "Seasonal Dynamics of the Flower Head Infestation of Smallanthus maculatus by Two Nonfrugivorous Tephritids," Journal of Insect Science 14(189), 1-7, (1 January 2014). https://doi.org/10.1093/jisesa/ieu051
Received: 19 October 2012; Accepted: 22 February 2013; Published: 1 January 2014
JOURNAL ARTICLE
7 PAGES


Share
SHARE
KEYWORDS
Asteraceae
immature stage
parasitoid
Tephritinae
trophic interaction
RIGHTS & PERMISSIONS
Get copyright permission
Back to Top