(Insecta, Thysanoptera) on the Mediterranean Oak, Quercus Ro Tundifolia L

Miscel.lania Zooloaica 22.1 (1999) 11

Seasonal abundance and biology of sporophagous thrips and notes on other thrips (Insecta, Thysanoptera) on the Mediterranean oak, Quercus ro tundifolia L. in Navarra (N Spain)

A. Goldarazena & L. A. Mound

Goldarazena, A. & Mound, L. A,, 1999. Seasonal abundance and biology of sporophagous thrips and notes on other thrips (Insecta, Thysanoptera) on the Mediterranean oak, Quercus rotundifolia L. in Navarra (N Spain). Misc. Zool., 22.1: 11-19.

Seasonal abundance and biology of sporophagous thrips and notes on other thrips (Insecta, Thysanoptera) on the Mediterranean oak, Quercus rotundifolia L. N, Navarra (NSpa~w-This paper records the seasonal abundance of four species of sporophagous thrips collected on the Mediterra- nean oak, Quercus rotundifolia L., in the Mediterranean area of Navarra (N Spain). The life cycles of Cornpsothrips albosignatus (Reuter), Priesneriella clavicornis (Knechtel); Megalothrips bonannii Uzel and Cryptohrips n~grbes(Reuter) are reported, and notes given about habitat specificity and wing development. Notes about host specific Terebrantia thrips of the Mediterranean oak are also reported.

Key words: Thysanoptera, Tubulifera, Seasonal abundance, Life cycle, Sporophagous thrips, Quercus rotundifolia.

(Rebut: 28 VI1 98; Acceptació condicional: 2 11 99; Acc. definitiva: 15 111 99)

A. Goldarazena'lJ, Depto. de Zoología y Ecología, Fac. de Ciencias, Univ de Navarra, 31080 Pamplona- Iruña, Navarra-Nafarroa, España (Spain): L. A. Mo~nd(~),British Museurn Natural History, Dept. of Entornology, Crornwell Road, SW75BD London, Inglaterra (England).

e-mail: [email protected] (2) e-mail: [email protected]

ISSN: 021 1-6529 O 1999 Museu de Zoologia 12 Goldarazena & Mound lntroduction tervals throughout 1997 and January 1998. Samples were taken from branches of Few reports have been published on the Quercus rotundifolia L. by beating dead seasonal dynamics and habitat specificity of branches, with or without dried leaves, and sporophagous thrips (Thysanoptera, Phlaeo- also live branches with lichens, over a plastic thripidae, Idolothripinae), although such dish of about 40 cm in diameter. A bar data is of significant interest for the under- 20 cm steel bar was used for beating. The standing of their biology and life cycle. specirnens were stored in vials containing Most of the taxonornic literature on thrips AGA (60% ethanol 10 parts, glycerol 1 part, in Spain involves species'description and lo- acetic acid 1 part), and examined with a cality records (BERZOSA,1983, 1988, 1990; phase contrast microscope in semipermanent TITSCHACK,1976) wifh little precise biological slide preparations made with Hoyer's information and only for pest species has mountant and sealed with commercial var- the seasonal dynamics and biology been nish. Recognition of the biological stages studied in depth in this country (LACASA was carried out under a stereomicroscope. PLASENCIA,1987, 1988; LACASAPLASENCIA et al., Three oak trees and microhabitats cho- 1988, 1990; BIELZAet al., 1996a, 1996b). In sen for sarnpling are described in Results. Navarra, the host plants and distribution of Samples were taken monthly during 1997, Terebrantia and Tubulifera have been re- and each microhabitat was beaten for 20 ported (GOLDARAZENA& MOUND, 1998, 1999; rninutes each time. Thrips were also ex- GOLDARAZENAet al., 1998, in press) and the tracted from leaf litter of Q. rotundifolia ecology and life cycle of ectoparasitic en- with a Berles-Tullgren funnel. The pop- emies of thrips in the Basque Country have ulations of sporophagous thrips and their been investigated (ZHANG& GOLDARAZENA,microhabitats were detected previously dur- 1996; GOLDARAZENAet al., 1997; GOLDARAZENAing faunistic studies carried out in a six- & ZHANG,1998). This lack of biological in- year survey of the Mediterranean area of formation contrasts with the detailed ob- Navarra (GOLDARAZENA,1996). servations on the behaviour of some fun- gus feeding Phlaeothripines in North America (CRESPI,1986a, 1990) and in Eng- Results land (CRESPI,1986b). However, the recent book by LEWIS(1997), particularly the chap- The richness of thrip habitats in the ter on biological diversity (MOUND,1977), Mediterranean oak indicates the scarcity of biological inforrna- tion on thrips other than a few pest spe- The Mediterranean oak, Q. rotundifolia L., is cies. The purpose of this article is to record one of the most representative tree species observations on the seasonal abundance in the Mediterranean area of Spain. Four and life cycle of sporophagous thrips asso- sporophagous thrips were found, living in ciated with Quercus trees in central and three different rnicrohabitats on branches of southern Navarra, and to determine their this tree, but other thrip species feed on the precise habitats within the oak trees they flowers and foliage or are predators. occupy. Throughout the study, many Thripidae were also collected from Q. Dead fallen branches with dried leaves rotundifolia, living in the flowers and feeding either on pollen and flower tissues or One collection site consisted of four large predating on other thrips. These collections branches which had fallen on the ground. are summarised in table 1. The leaves were attacked by a brown fun- gus throughout the year. The large Idolo- thripine species, Megalothrips bonannii Uzel, Material and methods was found in this habitat.

The study sites were located in a Mediterra- Leafless dead fallen branches nean forest in Tafalla (Navarra, N Spain). Field collections were made at rnonthly in- At the second site, several dead branches were Miscel.lania Zoologica 22.1 (1999)

Table 1. Thrips associated with the Mediterranean oak Quercus rotundifolia L.: F. Flowers; L. Leaves. Db. Dead branches with or without leaves; B. Branches with lichens. Trips asociados con la encima Mediterránea Quercus rotundifolia L.: F: Flores; L. Hojas; Db. Ramas muertas con o sin hojas; B. Ramas con líquenes.

Thrip family 1 species F L Db B Thripidae Thrips minutissimus Linnaeus + Thrips tabaci Lindeman + + Thrips angusticeps Uzel + + Oxythrips quercicola Bagnall + Oxythrips ulmifoliorum (Ha l iday) + Drepanothrips reuteri Uzel + Aeolothripidae Aeolothrips melaleucus Haliday + Aeolothrips gloriosus Bagnall + Phlaeothripidae Megalothrips bonnanii Uzel + Priesneriella clavicornis (Knechtel) + Cryptothrips nigripes (Reuter) +

completely covered by a black microscopic fun- The four species studied belong to the gus throughout the year. Cryptothripsnigripes Subfarnily ldolothripinae Bagnall. A revised (Reuter) and Priesneriella clavicornis (Knechtel) classification of this subfamily (MOUND& PALMER, were found in this habitat. 1983) recognised a world total of 600 species in 78 genera, two tribes and nine Live branches partially covered with lichens subtribes. ldolothripines have broad maxil- lary stylets, which forrn a tube through which The third site was an oak tree with branches whole fungal spores are ingested into their covered with different species of lichens. bodies. Presumably the Mediterranean oak Compsothrips albosignatus (Reuter), one of and their rnicrohabitats mentioned above the largest thrips in Europe, was collected in provide optimal conditions of temperature this habitat. and hurnidity for the development of the particular fungi on which these thrips feed. Flowers of Quercus rotundifolia

Many species of Thripidae were collected in Seasonal abundance of the sporophagous I the flowers of the Mediterranean oak dur- thrips- ing 1991-98, but only the species listed in table 1 breed on this plant. Their larvae feed The seasonal abundance of Compsothrips on pollen, and or leaves, or preying on albosignatus is indicated in fig 1. Fernales, other thrips associated with this tree. males and larvae were collected throughout 14 Goldarazena & Mound

Fernales -c Males

ABCD EFGHIJKLM Dates

on branches of Quercus . 51V 1997; E. 10V 1997; F. 20 VI 1997; G. 15 VI1 1997; H. 3 Vlll 1997; 1. 6 IX 1997; J. 2 X 1997; K. 30 XI 1997; L. 20 XII 1997; M. 25 1 1998. Abundancia estaciona1 de Compsothrips albosiqnatus- en las ramas de Quercus rotundif olia. (Para las abreviaturas.de las fe

the year from January 1997 to January 1998. populations of Compsothrips maroccanus The maximum number of specimens on the Priesner were collected under the rhizoma- branches was found in late June, and the tous grasses Lygeum spartium and Lavandula minimum in mid-July. The sharp decrease in latifolia. However, this thrip species seems to the thrip population from late June to be restricted to these habitats, and was not 15 July, was probably due to the high sum- found on Quercus trees in Navarra at any mer temperatures during this fortnight. The time. All the specimens were apterous. thrip fauna extracted with a Berlese funnel The seasonal abundance of Cryptothrips from three 5 kg samples of leaf litter col- nigripes (Reuter) is shown in figure 2. All life lected under the tree during August is pre- stages were collected in small numbers sented in table 2. The number of Co. throughout the sampling period. The great- albosignatus specimens collected from leaf est number of specimens was taken in late litter is similar to the number captured on June, and the minimum in January and Feb- the tree in late June. The thrips presumably ruary. Although most specimens collected were migrate from the branches to the cooler and apterous, macropterous females were col- more humid leaf litter under the trees in lected from March to August and represented response to the high summer temperatures. 30% of the total females captured (fig. 3). The thrips were also found in the litter dur- The only males found in these samples were ing late July. From August to November the macopterous. Natural enemies of this species number of thrips captured on the branches were not observed. The presence of increased, but it decreased again in Decem- macropterous and apterous females in late ber. All the specimens collected were apter- winter to summer suggests that the winged ous. The males varied between 0.25-0.74% females disperse and colonise new habitats of the population during the sampling pe- whilst the wingless females feed and breed in riod (table 3). the old sites. The male population during the In the same forest as the oak trees, large sampling period was between 0.20-0.71 %. Miscel•lània Zoològica 22.1 (1999) 15

Table 2. Thrip fauna extracted between July and August with the Berlese funnel from the soil under the tree of Quercus rotundifolia where the sampling of Compsothrips albosignatus was made. Fauna de tisanópteros extraída entre julio y agosto con el embudo de Berlese del suelo bajo la encina donde se realizó el muestreo de Compsothrips albosignatus.

Sample 1 Sample 2 Sample 3 Thrip family /species 15 VII 1997 3 VIII 1997 20 VIII 1997 Thripidae Thrips minutissimus Linnaeus 22 15 8 Thrips tabaci Lindeman 6 0 2 Chirothríps manicatus (Haliday) 43 28 2 Aptinothrips elegans Priesner 56 41 23 Aptinothrips rufus (Haliday) 19 9 10 Dendrothrips saltator Uzel 3 0 1 Aeolothripidae Aeolothrips intermedius Bagnall Phlaeothripidae Cephalothrips coxalis Bagnall 8 7 2 Cephalothrips monílícornís (Reuter) 28 35 12 Haplothríps setíger (Príesner) 6 1 0 Compsothrips albosignatus (Reuter) 87 73 59 Amphibolothrips marginatus (Buffa) 3 0 1 Weight of the sample (kg) 5.300 5.225 5.289

Table 3. Total number of specimens, sex ratio and variation of the percentage of males during the sampling in trees of Quercus rotundifolia. Número total de ejemplares, sex ratio y variación del porcentaje de machos a lo largo del muestreo en los boles de Quercus rotundifolia.

C. albosignatus C. nigripes M. bonanníí P clavicornis Total number of females 342 47 342 345 Total number of males 191 12 145 178 Sex ratio 1:2 1:3 1:2.5 1:2 Proportion of males 0.25-0.74 0.20-0.71 0.08-0.39 0.33-0.69 16 Goldarazena & Mound

7- Females w - Males

ABCDEFGHIJKLM Dates

Fig. 2. Seasonal abundance of Cryptothri Quercus rotundifolia. (For abbreviations see fig. 1.) Abundancia estaciona1 de Cryptothrips Quercus rotundifolia. (Para las abreviaturas ver fig. 1.

The seasonal abundance of Priesneriella clavicornis (Knechtel) is shown in figure 4. Females, males and larvae were collected throughout the year. The maximum number of specimens was captured in late June and the minimum number from January to March. All the specimens taken were apterous. They were found on dead branches of Q. rotundifolia, and none were found in leaf litter samples. The males made up between 0.33-0.69% of the population during the sampling period. The seasonal abundance of Megalothrips bonannii Uzel is shown in figure 5. Females, males and larvae were collected throughout the sampling period, but the maximum number of adults was taken in late May and Apterous U Macropterous June. A few pupal specimens were collected from May to August. The population of adults increased suddenly from February to March and decreased in winter. Qnly macropterous adults were collected, and the male popula- Fig. 3. Wing development in the female tion varied between 0.08-0.39%. Two natural populations of Cryptothrips nigripes. enemies of M. bonannii were found in this Desarrollo alar oblacionesde population (GOLDARAZENAet al., 1997). The hembras de Cr ectoparisitic mite A. dactylidium rnoundi Goldarazena et al. feeds on the eggs of these Miscel,lania Zoologica 22.1 (1999) 17

45 T Females

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 t ABCD EFGHI JKLM Dates

Fig. 4. Seasonal abundance of Priesneriella clavicornis on dead branches of Quercus rotundifolia. (For abbreviations see fig. 1.) Abundancia estaciona1 de Priesneriella clavic rotundifolia. (Para las abreviaturas ver fig. 1.)

60 -t Females

2 50 Q --

ABCDEFGHI JKLM Dates Goldarazena & Mound thrips and on the haemolymph of the adults. Acknowledgements The seasonal abundance of this mite and a revision of the genus Adactylidium is pres- We thank Prof. Dr. Jordana from the ently under study. A new species of Universidad de Navarra, Dr. zur Strassen from Thripastichus (Hymenoptera, Eulophidae) the Forschungsinstitut und Naturmuseum was found attacking the second instar lar- Senckenberg, Prof. Dr. Marullo from the Uni- vae of M. bonannii (GOLDARAZENA& LOOMANS, versity of Basillicata, Prof. Dr. Lacasa from the in press). Departamento de Protección Vegetal de Murcia, C.R.1.A and Prof. Dr. Berzosa from the Universidad Complutense for providing in- Resumen formation and much encouragement. This paper was funded by the Research Plan of Abundancia estacional y biología de trips The University of Navarra (PIUNA). We also esporófagos y notas sobre otros trips (Insecta, thank Dr. S. Nakahara (Unites States Depart- Thysanoptera) de la encina Mediterránea, ment of Agriculture, Maryland, USA) who gave Quercus rotundifolia Linneo en Navarra (N helpful information and comments on the España) original manuscript during the senior author's stay in Maryland. The senior author received En este trabajo se estudia la abundancia a grant from the Department of Education of estacional de cuatro especies de tisanópteros the Government of Navarra where the sam- esporófagos capturados en la encina pling was made. We are also very grateful to mediterránea, Quercus rotundifolia L., en la the reviewers whose useful comments have región mediterránea de Navarra (N España). helped to improve the original manuscript. Se ha estudiado la distribución estacional de Compsothrips albosignatus (Reuter) (fig. l), Cryptothrips nigripes (Reuter) (fig. Ref erences 2), Priesneriella clavicornis (Knechtel) (f ig. 4), Megalothrips bonannii Uzel (fig. 5) y a BERZOSA,J., 1983. Tisanópteros de la Sierra de lo largo del año 1997 y se aportan datos Guadarrama IV. Phlaeothripidae Uzel, sobre la especificidad del hábitat en el que 1895. Graellsia, 39: 127-137. se encuentran estos trips en la encina, sobre - 1988. Karnyothrips americanus (Hood, la variación en la proporción de machos 1912) en la Península Ibérica (Thysa- respecto a las hembras a lo largo del noptera: Phlaeothripidae). Boln. Asoc. muestre0 (tabla 3) y la evolución en el Esp. Ent., 12: 137-141. desarrollo alar de las especies mencionadas - 1990. Nuevos datos sobre el género (fig. 3). Así mismo se citan las especies de Allothrips Hood, 1908 (Thysanoptera: tisanópteros Terebrantia que son específicos Phlaeothripidae) Redia, 73(2): 355-363. de las flores y las hojas de la encina BIELZA,P., TORRESVILA, L. M. & LACASAPLASENCIA, mediterránea en Navarra, como resultado A., 1996a Incidencia cuantitativa y cuali- de la prospección faunística realizada du- tativa de Haplothrips tritici Kurd. (Thysanop- rante los años 1993-1995 (tabla 1). tera: Phlaeothripidae) en la producción de Los tisanópteros esporófagos, pertene- trigo. Bol. San. Veg. Plagas, 22(2): 277-288. cientes a la subfamilia Idolothripinae, han - 1996b. Efecto del laboreo en la supervi- sido encontrados en tres tipos de micro- vencia de las larvas invernantes de hábitas: a. Ramas muertas caídas que por- Haplothrips tritici Kurd. (Thysanoptera: tan hojas secas, b. Ramas muertas caídas sin Phlaeothripidae). Bol. San. Veg. Plagas, hojas; c. Ramas vivas cubiertas parcialmente 22(2): 289-296. de líquenes. Se describen las dinámicas CRESPI,B. J., 1986a. Size assesment and alter- estacionales, la propoción de machos y native fighting tactics in Elaphrothrips hembras para las especies esporófagas men- tuberculatus (Insecta: Thysanoptera). cionadas en el párrafo anterior y se comen- Anim. Behav., 34: 1.324-1.335. ta la posible migración de Co. albosignatus - 1986b. Territoriality and fighting in a co- desde la encina al suelo durante la estación lonial thrips, Hoplothrips pedicularius, and más calurosa del verano (fig. 1, tabla 2). sexual dimorphism in Thysanoptera. Ecol. Miscel.lania Zoologica 22.1 (1999) 19

Entomol., 11 : 119-1 30. larvae (Acari: Erythraeidae) ectoparasitic - 1990. Subsociality and female reproduc- on Thrips trehernei (Thysanoptera: tive success in a rnycophagous thrips: an Thripidae) in the Basque Country (Spain). observational and experimental analysis. Syst. Appl. Acarol., 3: 125-129. J. lnsect Behav., 3: 61-74. LACASAPLASENCIA, A., 1987. Un trips de recien- GOLDARAZENA,A., 1996. Contribución al te introducción en Europa, nueva plaga conocimiento de los tisanópteros de en los cultivos hortícolas y frutales espa- Navarra (Insecta, Thysanoptera). Tesis doc- ñoles. Agrishell, 37: 4-8. toral, Universidad de Navarra. - 1988. Los tisanópteros en horticultura: su GOLDARAZENA,A., JORDANA, R. & ZHANG,Z.-Z., implicación parasitaria. Tercer Symposium 1997. Adactylidium moundi and A. Nacional de Agroquímicos, Sevilla: 33-52. costarricensis, two new species of Acaro- LACASAPWSENCIA, A. & MARTINEZ,M. C., 1988. phenacidae (Acari: Tarsonemida) parasitic Notas sobre la biografía de Hercinothrips on Thysanoptera. Internat. J. Acarol. femoralis Reuter (Thysanoptera: Thripidae) 23(4): 261-268. potencial plaga en las plantas ornamenta- GOLDARAZENA,A. & LOOMANS,A. M. (in press). les. Bol. San. Veg., Plagas, 14: 67-75. Natural enemies of Thysanoptera in LACASAPLASENCIA, A,, MARTINEZ,M. C. & ALLIAGA, Navarre (Northern Spain): an introduc- J., 1990. Los trips en los frutales de hueso tion. Sixth Internat. Symposium of del Sureste español: su implicación para- Thysanoptera, 1988 Antalya, Turkey sitaria y ecología. Bol. San. Veg., Plagas, GOLDARAZENA,A. & MOUND,L. A,, 1998. In- 16: 425-426. troducción a la fauna de los Tisanóp- LEWIS,T., 1997. Thrips as crop pests. Ed. CAB teros (CI. Insecta: 0. Thysanoptera) de International, Wallingford, England. Navarra-Nafarroa, sus plantas hospeda- MOUND,L. A,, 1997. Biological diversity. In: doras y su distribución. I Suborden Thrips as crop pests: 197-215 (T. Lewis, Terebrantia. Est. Mus. Cienc. Nat. de Ed.). Ed. CAB International, Wallingford, Álava, 12: 167-202. England. - 1999. Hindsiothrips from Spain with the MOUND,L. A. & PALMER,J., 1983. The generic first record of Tylothrips osborni (Hinds) and tribal classification of spore-feeding from Europe (Thysanoptera, Phlaeo- Thysanoptera (Phlaeothripidae: Idolo- thripidae). Entomol. Month. Mag., 134: thripinae). Bull. Brit. Mus. Nat. Hist., 3 19-324. 46(1): 1-174. GOLDARAZENA,A,, MOUND, L. A. & JORDANA, R. TITSCHACK,E., 1976. Verzeichnis der bis jetzt (in press). lntroduction to the thrips fauna aus dem spanischem territorum bekannt of Navarre (CI. Insecta: 0. Thysanoptera), gewordenen tubuliferen thysanopteren. with their host-plants and distribution. Dtsch. Entomol. Z., 23: 131-152 Suborder Tubulifera. Sixth Internat. Sym- ZHANG,Z.-2. & GOLDARAZENA,A., 1996. posium of Thysanoptera, 1998 Antalya, Abrolophus and Grandjeanella larvae Turkey. (Acari: Erythraeidae) ectoparasitic on thrips GOLDARAZENA,A. & ZHANG,Z.-Z., 1998. Seasonal (Thysanoptera: Thripidae). Syst. Appl. abundance of Abrolophus neobrevicollis Acarol., 1: 127-144.