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Ecology, Behavior and Bionomics Geographical Transition Zone of Solenopsis Fire Ants (Hymenoptera: Formicidae) and Pseudacteon Fly Parasitoids (Diptera: Phoridae) in the State of São Paulo, Brazil MA Pesquero1, AMPM Dias2 1Univ Estadual de Goiás, UnU de Morrinhos, Morrinhos, GO, Brasil 2Univ Federal de São Carlos, Depto de Ecologia e Biologia Evolutiva, São Carlos, SP, Brasil

Keywords Abstract Host selection, community, biological control Solenopsis saevissima (Smith) and Solenopsis invicta Buren are Correspondence Marcos A Pesquero, Rua 14, nº 625, Jardim América, Morrinhos, 75650-000, GO, Brasil; thePseudacteon most abundant and widely distributed fire ants in Brazil. The [email protected] occurrence of the two fire ant species and of their parasitoids spp. is described for a climatic and phytophysiognomicS Edited by Fernando L Cônsoli – ESALQ/USP transitionsaevissima area in the state of São Paulo. Both fire ant species have awhile parapatric S invicta distribution, apparently determined by the climate: . Received 07 February 2011 and accepted 12 between the predominates latitudes 21 ºinS andthe north 23º part of São Paulo (Aw climate), July 2011 . in the south (Cfa climate). A sympatricS saevissima area is observed in the north and with S invicta S. Two different communities of parasitic decapitating flies wereº58’S associated 47º with . . in the south, with a sympatric area in the municipalityPseudacteon of São Carlos (21 53’W).P The litoralis possible causes ofP curvatusthis biogeographic Ppattern wasmanni are discussed. P Preferencepradei tests with P obtusus flies challengeS thesaevissima association ofP dentiger. Borgmeier, P disneyi. Pesquero Borgmeier, and P .lenkoi Schmitz, . BorgmeierS invicta and . Borgmeier with . , and . Borgmeier, . . Borgmeier & Prado with . . Introduction et al et al 1997)

Banks 1987, Campiolo 1994, Morrison hasSolenopsis also been saevissimademonstrated (Smith) to be and important S invicta inBuren species are ofPrevious Pseudacteon research has resulted in considerable knowledge composition of local communities. Solenopsis about theet altaxonomy and etgeographic al distribution saevissima . decapitating flies in South America the most common fire ants species in Brazil. (Patrock 2009, Plowes 2009). Due to the high occupies a large central area whereet the al species richness of fire ants and the natural occurrence BrazilianSolenopsis savannah invicta dominates, extending to the north, of parasitoids in South America, the host specificity is northeast and southeast regions of Brazil (Ross an importantet al aspect to be consideredet al when selecting 2010). also has a wide distribution, natural enemies for fire ant biological control in the US including Paraguay, a great extension in Bolivia, in (Vazquez 2004, Folgarait et al 2005b). Moreover,et northeastern Argentina, north of UruguayS invicta and a north-and S althe ecological differentiation amonget alparasitoid specieset al saevissimasouth band of Brazil that goes from the state of Rondônia such as daily activityet al (Pesquero 1996, Folgarait to the state of Rio Grande do Sul. Both . . 2007a), attack place (Pesquero 1993, Orr are parapatric in Brazil, with known zones of Neotrop1997, Folgarait Entomol 40(6): 647-6522007b) © and 2011 host Sociedade size Entomológica(Williams & do Brasilcontact in the states of Mato Grosso do Sul, São Paulo and647 Geographical Transition Zone of Solenopsis Fire Ants and Pseudacteon Fly Parasitoids Pesquero & Dias

Paraná (Porter et al et al 47º et al 1992,Pseudacteon MacKay 1994, Shoemaker 53’W). The region has transition characteristics of the 2006). Brazilian savanna and the Atlantic Forest (Fig 1a), and is S saevissimaOf the 36 described and S invicta species that parasitize located between the two main climatic zones according to fire ants in the Neotropical region, 19 are associated withet the Köppen’s classification, “Aw” to the north and “Cfa” to al. . in South America, and 16 are the south of the state (Fig 1b). Two pasture areas (0.2 ha) listed as common to both species of fire ants (Patrock 5-10 km apart, located near toSolenopsi a river, streams and Pseudacteon or lake were 2009). However, 11P of borgmeieri these species have P ranges cultellatus that demarcated in each municipality to estimate the richness are mostly limited P nudicornis to one species or another. P solenopsidis Only five and abundance of species of . species of parasitoids P tricuspis ( . Schmitz, . All colonies found in the areas were disturbed with the Borgmeier, . Borgmeier, . et aid of a small shovel to encourage the exit of ants and to alSchmitz and . Borgmeier) haveP nudicornis ranges thatP attract the parasitoids. cultellatusbroadly overlapP with tricuspis both fire ant species (Patrock A sample of fire ant workers was removed from 2009). Furthermore, the oviscape of . , . each colony for species identification (Trager 1991). , and . shows intraspecific variation Flies were collected during the first seven hours from describe(Porter & the Pesquero occurrence 2001), of Pseudacteon suggesting the occurrence of sunrise, a period that includes the peak of activity of all populations in process of reproductive isolation. Here we the species found in the wider region (Pesquero 1997). parasitoid species Flies that approached the colonies andºC) washovered used over to store fire and their fire ant hosts in a transition zone between two ant workers in attack mode (Porter 1998) were collected different describedPseudacteon communities for SBrazil saevissima (Pesquero and with an aspirator. A cooler (circa 12 S1997). invicta We have also conducted tests to determine the Solenopsisthe flies prior and to Pseudacteon species identification were retained (Porter by the& Pesquero authors preference of species for . 2001) with a hand lens (20x). Voucher specimens of . in the field. Material and Methods and deposited in the Museu deS Zoologia, invicta Universidadeand another deas SSão saevissima Paulo, state of São Paulo, Brazil. One colony identified as . º º . , collectedet alin Anhembi and Sales Oliveira, Field work was carriedº outº in six municipalities situatedº respectively, were separated from soil particles by 7inº the state of São Paulo: Anhembiº º(AN: 22 47’S, 48 7’W), flotation (Jouvenaz 1977), transferred to white 21Itirapinaº (IT:º 22 24’S, 47 54’W), São Carlos (SC: 21º 58’S, plastic trays (35 x 40 x 10 cm) coated internally with 53’W), Rincão (RI: 21 35’S, 47 57’W), Barrinha (BA: Fluon (ACG Chemicals Americas Incorporation, Bayonne, 12’S, 48 10’W) and Sales Oliveira (SO: 20 52’S, NJ) and feda with insects, water and sugar water during Floresta estacional semidecidual Cerrado Floresta ombrófila densa Cerrado - floresta estacional semidecidual Cerrado - floresta ombrófila densa Floresta ombrófila mista

0 100 km Brazil Af b Aw SO Am BA Cwa RI Cwb SC Cfa IT Cfb AN 0 500 km

(1988)Fig 1 a) Vegetationapud types of the state of São Paulo, Brazil according to IBGE Siqueira & Durigan (2007). b)et Climatic al classifications for the state of São Paulo, Brazil according 648 Neotrop Entomol 40(6): 647-652 © 2011to Rolim Sociedade (2007).Entomológica do Brasil Pesquero & Dias Geographical Transition Zone of Solenopsis Fire Ants and Pseudacteon Fly Parasitoids

associated with S saevissima the study. These trays of fire ants were used in the host northern community with nine species (5.11 ± 0.32, n = 6)S chooseselection between assays. theIn each nest samplingof S saevissima place a ortest S ofinvicta host invicta . Pseudacteon, and a southern community choice was established, where the parasitoid flies could with eight species (4.68 ± 0.84, n = 4) associated with . . . Pseudacteon (Fig 2). A mixturetricuspis of P nudicornis andspecies P solenopsidis of the two simultaneously. communities (13 species, 9 ± 0, n = 2) was observed inP Trays were 10 m apart one from another to reduce borgmeieriSC. , . . mutual interference in the attraction of parasitoids, and occurred in territories of both species of fire ants, and . were transferred to another distant point 50 m from in the southern occurred community only in wereSC associated P wasmanni with a single the previous one at 1h intervals. The flies captured Punidentified tricuspis P fire litoralis ant species. and P The pradei most abundant species were stored and identified as described previously and the northern were P cultellatus P. affinis Schmitz, released beforePseudacteon dusk. Rates of attack, parasitoidSolenopsis pupation P. disneyi , . P fowleri. PesqueroBorgmeier, and P dentiger and in and emergence were not observed. Data on the preference . , . Borgmeier, of species of for the two species of . Pesquero, . . was analyzed by Wilcoxon matched pairs test with the BorgmeierPseudacteon (Table 1). Systat program (Systat Incorporation 2010). A total of 106 males and 195 females belongingPseudacteon to 14 Results species of were observedSolenopsis on the two trays of fire ants (Table 2). The two communities of flies recognized the dominant species at simultaneouslythe sampling sites attracted (z = 3.29, to the n colonies= 14, P of< 0.001).S invicta In and an A total of 84 colonies of fire ants with estimates Solenopsis of Sanalysis saevissima restricted (P affinis to theP speciesdisney P of dentiger parasitoidsP tricuspis that wereP saevissimadensities varying was dominant between in 10 the and sites 70 tocolonies/ha the north (38.2of SC pradei and P wasmanni . ± 6.44, n = 12) was found at the sampling sites. S invicta . . , . , . , . , . . ), the preference for the local host (RI, BA, SO), with 92% of the 27S saevissima colonies, while colonies . were ant remained significant (z = 2.20, n = 6, P < 0.03). was dominant in the sites to the south ofS SCinvicta (IT, AN), colonies with Discussion 70% of the 20 colonies. Only . found below IT to theS south, invicta and only . S saevissima were found above RI to the north. In SC, 27% of the 37 colonies belonged to . and 38% to . , The average density of fireS invictaant colonies (30 ± 37in andthe region55 ± 8 with 19% having ambiguous characteristics between both (38.18 ± 6.44, n=12) was intermediate if compared species and six colonies seemed to belong to two other bywith Porter the values et al found for . Solenopsis saevissima and offire Pseudacteon ants species. colonies/ha)S invicta in surveys carried out in South America PseudacteonA total of 186 unidentified males and 398 females (1992, 1997). º24’ and 21º were collected. Fifteen species of . had a narrowS saevissima latitudinal in sympatricthe state of band Paraná in were observed in the whole sampling sites. the study region situated between 22 35’S. Two communities of parasitoids were recognized: a However, records of .

lenkoi SO disneyi cultellatus BA affinis fowleri dentiger RI tricuspis borgmeieri solenopsidis SC nudicornis litoralis IT wasmanni obtusus AN pradei curvatus

Pseudacteon

N Fig 2 Distribution of spp. southaccording communities to sampling are sites associated in the statewith 0 100 Solenopsisof São Paulo, saevissima Brazil. Theand northSolenopsis and km invicta São Carlos were found at sites both to the , respectively. The species around

Pseudacteon Pseudacteon on the trays of Solenopsis invicta and Solenopsis saevissima whereTable 1Solenopsis Abundance invicta of species in selected Table 2 Abundance of wheremunicipalities Solenopsis in thesaevissima state of São Paulo, Brazil. IT+AN = sites in all sampling sites (AN, predominates. RI+BA+SO = sites IT, SC, RI, BA, SO) in the stateFire of an Sãot sp ePaulo,cies Brazil. Pseudacteon Total predominates. SC = site where S. saevissima S. invicta bothPseu speciesdacteon of fire antsIT+ AareN similarlySC abundant.RI+BA+SO Total Northern community Southern community aﬃnis 6 2 8 curvatus 1 6 7 cultellatus 36 0 36 litoralis 26 5 31 dentiger 14 1 15 nudicornis 1 2 3 disneyi 7 1 8 obtusus1 12 6 18 fowleri 10 0 10 pradei 24 2 26 lenkoi 6 0 6 solenopsidis 2 1 3 nudicornis 3 0 3 tricuspis 28 9 37 tricuspis1 2 0 2 wasmanni 16 42 58 Males 38 8 46 Northern community Southern community aﬃnis 10 8 18 curvatus 0 1 1 borgmeieri 5 5 litoralis 0 26 26 cultellatus 61 36 97 obtusus1 0 12 12 dentiger 5 14 19 pradei 4 20 24 disneyi 24 13 37 tricuspis 4 24 28 fowleri 17 10 27 wasmanni 1 15 16 lenkoi 6 6 Males 3 68 71 nudicornis 3 3 Total 134 178 312 solenopsidis 1 1 1 tricuspis1 2 2 Total 110 195 93 398 These biotypes are smaller and have distinctive morphological differences when compared to type specimens. 1 (Cacaterra et al Pseudacteon These biotypes are smaller and have distinctive morphological differences when compared to type specimens. 2008). antsThe of S species saevissima of observed here represent S invicta territory 75% of all known species of this group associated with fire expand its distributionet al area by approximately 420 km to . group in South America. The southern the south of the study region into the . Scommunity invicta corresponded to flies previously described (Shoemaker 2006). It is possible that the climatic for the region of Rio Claro (SP) (22°24’S, 47°33’W) onS annualconditions rainfall are (circa a limiting 1500 mmfactor3 to the distribution of saevissima. , while the northern community correspondedP tricuspis these ants, although the two zones have similar average andto flies P nudicornis found in Goiânia found in (GO) the territories (16°42’S, 49°15’W)of S saevissima on . ). In the north area of the and S invicta (Pesquero 1997). Populations of . state of São Paulo, characterizing the climate “Aw”, the . . temperature,et al potential evaporation and hydricS deficiency invicta in . havePseudacteon the biotypes affinispreviously and describedP cultellatus for are higher than those of the south “Cfa” climate areaet the state of Goiás and São Paulo, respectively (Porter & al(Rolim 2007). However, the occurrence of . andPesquero P curvatus 2001). . lower latitudes (Porto Velhoº 8°36’S, 63°54’W) (Lofgren were identified as the biotypes found in the state of Goiás, northern 1975) and occurrence the high of latitudinal S invicta overlap betweenet al 1975) the twoand . Borgmeier in the state of São Paulo (Porter thefire mostant species southern (circa occurrence 17 of difference of S saevissima between the most & Pesquero 2001). et al . ) (Lofgren The territories of the two communities studied here . (Shoemaker were abruptly interrupted in São Carlos (SC), indicating dominance 2006) require abilities more of S studies,invicta including examination of strong environment changes. Three non-exclusive competitive exclusion. The high recruitment response and hypotheses may contribute to this geographic distribution . reinforce this hypothesis 650 Neotroppattern. Entomol 40(6):The first647-652 hypothesis © 2011 Sociedade is that Entomológica parasitoids docan Brasil be Pesquero & Dias Geographical Transition Zone of Solenopsis Fire Ants and Pseudacteon Fly Parasitoids

invicta and S saevissima Pseudacteon Pseudacteonspecies specific to the fire ants and, therefore, follow the . , and between communities of distribution of their host. Although the development of parasitoid flies supported by these ants in flies on non-host fire ants species is possible Brazil. The distribution of parasitoid flies seems to be under laboratoryet al conditions, theet alapproach and attack determined by host specificity,Pseudacteon while (Pesquero fire ants distribution 1997) and rates are reduced compared with local fire ant species dominanceseems to result of Solenopsis from climatic (Calcaterra influence. et al 2008)However, indicate data (Folgarait 2002, Folgarait 2005b). Ecological on change of niche of and behavioral factors are considered as so or more important as physiological and taxonomic limitations that interespecific competition must also be taken into in the determination of the host range in other groups consideration in the inquiry of this phenomenon. of parasitoids (Whitfield & Wagner 1988, Morehead & Acknowledgments Feener Jr 2000, Stireman & Singer 2003). Although the reduced number of fire ant species ofcolonies the Pseudacteon (n = 1) can underestimate intercolonial variation, assays for host selectionP demonstratedaffinis P dentiger the preference P disneyi Nivaldo D Oliveira assisted during field collections. Rafael P pradei P tricuspis flyand communities P wasmanni werefor the attracted local fire by F Juliano (UEG - UnU Morrinhos) and two anonymous ants species. However, . , . , . P, reviewers of the manuscript provided a number of helpful tricuspis. ,and. P disneyi . suggestions. This study was supported by a research the two fireSolenopsis ants species (Table 2). Of these parasitoids, . assistantship provided by FAPESP. et al 2005); P. pradei haveand Pregional wasmanni biotypes occur and in attackareas References different species (Pesquero 1997, Calcaterra . et al . P affinis and P dentiger having an association with more than one fire ant host Solenopsis invicta seem to be limited to the distribution area of S saevissima Calcaterra LA, Livore JP, Delgado A, Briano JA (2008) Ecological species (Patrock 2009), but . . et al dominance of the red imported fire ant, , in its . native range. Oecologia 156: 411-421. between(Pesquero the 1997, northern Patrock and the southern 2009). areas can enforce In our second hypothesis, the climatic differences CalcaterraPseudacteon LA, Porter SD, Briano JA (2005) Distribution and abundance of fire ant decapitating flies (Diptera: Phoridae: important physiological restrictions regarding to body ) in three regions of southern South America. Ann et al (2005a) Entomol Soc Am 98: 85-95. temperature and water balance for these small insects (Porter & Gates 1969). Indeed, Folgarait Campiolo S, Pesquero MA,Solenopsis Fowler HGsaevissima (1994) Size-selective offound Pseudacteon a significant association between climatic variables oviposition by phorid (Diptera: Phoridae) parasitoids on (mainly temperature and precipitation) and groupings workers of the fire ant, (Hymenoptera: Formicidae). Etologia 4: 85-86. species in South America. However, Pseudacteon the limiting factors for the regional climatic variations Folgarait PJ, Bruzzone OA, Patrock RJW, Gilbert LE (2002) ofcan Pseudacteon be overcome by acclimatization of these species. Developmental rates and host specificity for Evaluating the period of daily activity of two communities parasitoids (Diptera: Phoridae) of fire ants (Hymenoptera: in places with different climates in Brazil, Formicidae) in Argentina. J Econ Entomol 95: 1151-1158. (2005a) Pesquero (1997) reported that the majority of species Folgarait PJ, Bruzzone OA, Porter SD, Pesquero MA, Gilbert LE in the community located in tropical climate with dry Biogeography and macroecology of phorid flies that winters had crepuscular activity, while those species attack fire ants in southeastern Brazil and Argentina. J Biogeogr situated in humid climate with hot summers were active 32: 353-367. during the warmest hours of the day. Pseudacteon obtusus FolgaraitSolenopsis PJ, invicta Chirino and MG, Solenopsis Patrock richteri RJW, Gilbert LE (2005b) In our last hypothesis, we assume that communities Development of (Diptera: Phoridae) on incan communities be saturated, of making Pseudacteon difficult the introduction of a fire ants (Hymenoptera: new species (Ricklefs 1987). This subject is little explored Formicidae). Environ Entomol 34: 308-316. , but the predominance Folgaraita Solenopsis PJ, Patrock RJW, Gilbert LE (2007a) The influence of (84%) of local assemblies with a lower richness (upet toal ambient conditions and space on the phenological patterns of four species) as compared with the richness observed phorid guild in an arid environment. Biol Control for regional assemblies in South America (Patrock 42: 262-273. 2009), and the convergence of structure between two regional communities in Brazil (Pesquero 1997) suggest Folgarait PJ, Patrock RJW, Gilbert LE (2007b) Associations of fire ant phorids and microhabitats. Environ Entomol 36: 731-742. the role of competition in the community structure of Solenopsis these insects. S Jouvenaz DP, Allen GE, Banks WA, Wojcik DP (1977) A survey for This study represents the first register of geographic pathogens in fire ants, spp., in the Southeastern United transitionNeotrop Entomol zone 40(6): between 647-652 populations © 2011 Sociedade of Entomológicafire ants .do BrasilStates. Fla Entomol 60: 275-279. 651 Geographical Transition Zone of Solenopsis Fire Ants and Pseudacteon Fly Parasitoids Pesquero & Dias

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