Memoranda Soc.Fauna Flora Fennica80:49-68. 2004 Influenceof species,sex, age and food on the accumulation of toxic cadmium and someessential metals in AuchenorrhynchousHomoptera PekkaNuorteva, Martin Lodenius,Sumio Nagasawa*, Esa Tulisalo & Sirkka-LiisaNuorteva Nuorteva,P., Lodenius, M., Tulisalo,E, & Nuorteva,s.-L., Department o.f'Limnologt,and Environmental st:ienc'e,Hel.sinki Llniversity, PB 65, FI-000r4 Hetsinki IJniversitv\ Itlagttsawa,5.,I9-45 Utoosaka,Shimizu 421-0873, Japan occurrenceof toxiccd andthe essential, partly antagonistic metals Fe,zn,Mn andcu in the Homopteransuborderluc'henorrhynchawas studicd through AAS analyscs.22 spe- ciesfrom 5 familieswere analysed through 2 | 7 samplesincluding 4360 specimens.The main materialwas from theunpolluted Finnish SW archipelago,and was complerncnted with cicadas(cic'adidae) from a city gardenin Shimizu,Japan, and with leaflroppers (Tvphlocybidue)from parksof Helsinkicity, Finland. The lowestadult levels (below 0.2 I ppm) were found in the mesophyll-feedingTyphlocybidae, the highestlevels in the xy- lem-feedingcicadidae and,Cerc:opidcte. Avcrages as high as 5.5 and 3.6 ppm ppm/dwt occurredin Meimuna opali/bra andPhilaenus ,spuntarius respectively. A clear sexdiffer- enceexisted rn the cd levelsof cir:adidae(males 1.20-1 1.0 ppm; females0.06-0.51 ppm). The oppositesituation was presentfor two cercopidand two cicadellidspecies. During development,the Cd-levelsof Cicadettidaereached peak concentrationsin adults,typically in hemimetabolousinsects. In xylem-feedtngCerc.opitlae the peaklcvel occurred,howeveq at the end of thelarval stage and was extremely high (up to 30 3g ppm in total,33 ppm in Malpighiantubules and 180ppm in theintestine). The necessary repro- duction saving cd decreasein adults was accelerared,in Aphropl'roraalni througha changeof hostplant species. The Cd levclsin variousspecies of food plantsmirrored it- selfclearly in thelarvae of Philaenusspumarius. The high Cd levelsin cercopidlarvae re- flecteditself in the sphecidwasp Argvrcstes; mystaceolts. 1. Introduction asthe functions ofthe entirelife-supporting global machinery.Anomalous metal accumulationsand Mining and industrycontinuously transfer metals ecophysiologicaldisrurbances in variousorgan- from the interior of rocks to thc biosphere.Acid isms have beendescribed in thousandsof scien- raln suppoftsthe transformationof metalsinto a tific papers.Adequate evidence does, however, bioavailablefbrrn. Elevatcd levcls of bioavailable coveronly a f'ewsystematic groups of organisms. metalsin the biospherehave the potentialto dis- In fact, systematicalcategories with tensof thou- turb theecophysiology of living organismsas well sandsof species,have been studied very superfi- ciallyor notat all. ' Prof.Sumio Nagasawa died on November2, 2004 The insufficientlystudied groups include the 80, 2004 50 l,luortevaet al. 'Memoranda Soc.Fauna Flora Fennica (1987) detected insect order Homoptera, consisting of more than when Stary and Kubiznakova ants,which consume 40,000species, all with piercing-suckingmouth- highmetal levels in redwood maximal metal levels parls. Within this large order too, the existing aphidhoneydew They noted had freshly collecteo metal evidenceis distributedunevenly. Practically in such ant workers which (- the honeydew) of aphids no evidence exists for the suborder Auche- the liquid excrements to the nest.This obser- norrhyncha consisting of 30,000 species.All andwere on their way back and expanded availableevidence is concentratedto a coupleof vation has later been conltrmed of severalauthors (Mar- superfamilies in the smaller suborder Stenor- upon through the studies rhyncha(consistingof about10,000 species). This tin 2000). to produce such huge restrictedevidence does, however, illustrate some Aphids are really able that it is capable basicfeatures which arevalid for the metalbiology amountsof Cd-loadedhoneydew of red wood antsto the of the whole order. to elevatethe hugebiomass highestlevel among forest animals (Y1,,-Mononen et al. 1989,Nuorteva 1990, 1999,Maavara et al' kind of situationhas de- 1.1.Metal biology in Homopteran suborder 1994,Martin 2000).This red wood ants are really Stenorrhyncha veloped because the strong honeydew consumers.More than 90% of food consistsof honeydew I .I .l . Meralsin PsYllids the red wood ant's (Rosengrenand Sundstrom1991). lt is possibleto inpact of this Cd trans- Among psyllids,Al, Fe, Ni, Mn, Cu,Zn, Cd and understandthe tremendous considersthat the ant bio- Hg levelshave been determined in 14 out of about fer process,when one exceedthat of 1,000 existing species(Glowacka et al. 1997)' massmay under optimal conditions (Holldobler and Wil- Generally psyllids accumulate low amounts of all other forest invertebrates metals,but their metal burdensincrease with age' son 1990). (Migula et al' 1993, Exuvia were importantfor the eliminationof Al, It hasbeen demonstrated Martin and Nuorteva Ni and Mn, larval wax for Al, Cu and Ni. ln pol- 1997, Maavara er a1.1994, 1997,Martin et a1.1999,Martin luted areas Psyllopsisfrarini eliminated large 1997, Rabitsch coloniesdoes resist high amountsof Al, Fe, Cu and Cd with honeydew' 2000) that red wood ant physiologicaltoler- This way of metalelimination was lessimportant Cd load by aid of 1) a normal social tolerancesystem in speciesliving in unpollutedsites. Biomagnifi- ance system,2) a special in the feeding cation of metal levels from food plants to psyllids basedon negativebioaccumulation inhibition (expressedas the concentrationfactor) was low for chain (including partial metal transfer mandibularglands) and Mn, Al and Ni (cf: 0.56-1.08),but high for the by the postpharyngealand compensatemortality' toxicCd (cf: 5.86). 3) a supercolonysystem to However, when anthropogenic environmental pollution elevatesthe Cd level in ants ten-fold systemsdoes not l.1.2. Metals in aphidsand their honeydew ower the normal, the tolerance more protect the ant colonies. This results to de- - a danger lor ants cline of ant populations,which may in turn endan- red wood antscontrol ef- Of the2,000 aphid species, tentative analyses extst ger foresthealth because ofseveralspecies offor- for only 6. Their Cd levelsare not very high: 0'04 fectivelythe populations ppm in the pemphigid Pachypappa populi estpest insects. (Nuortevaet Soltanpour1997), 0.3-0.6 ppm in the others(Nuorteva et al. 2001).The corresponding aspollution damage levels for Cu are9 andg-25 ppm and for Zn 6l and I . I .3. The role of aphids 220 1,010ppm, resPectivelY. exacerbators Superficialconsideration of such low levels a simpletoxicologi- gives an impression of minimal influence of Metal pollutionin biotais not of certainorganisms aphidson thebiotic metalcirculation. Such an im- cal problem where the health limits are sur- pressionis, however,elroneous. This was found deterioratesbecause their tolerance MemorandaSoc. Fauna Flora Fennica80. 2004 . Nuortevaet al. 5l passed.In many cases,the pollutantsonly de- the first visible phaseof a gradualforest decline creasethe pestresistance ofplants. In suchcases, process(Carle 1968, Carle and Pontivy 1968, herbivoresact as pollution damageexacerbators. Villemant 1981,Walther et a. 1984,White 1984, ln general, plant suitability for aphids in- FrihrerI 987,Nuorteva 1990). Although pollution creasesthrough elevated flow of amino acids in damageaggravation by insectpests is well docu- the sieve tubes from which most aphids imbibe mented, it has rarely been taken into account by their food. Becauseamino acids are the mostnec- environmentalists(\luorteva 1997,Nuortevaet al. essarydietary ingredientsfor the parthenogeneti- t999,2001). cally reproducingand rapidly growing aphids,any kind of amino acid elevations are beneficial for them. Regularly, aphids benefit from amino acic 1.2 Biological background for metal mobilizations in spring and autumn. In addition, circulation in the Homopteran suborder aminoacid mobilizations released in thehost plant Auchenorrhyncha by stressand diseaseare beneficial for aphids. On this way air pollution stresswith SO' NO, Someprinciples of thepollution biology observec and acid mist elevates aphid populations on in the Homopteran suborder Stenorrhynchamay roadsides(Walther et al. 1984,Braun and Fliicki- be valid when one tries to understandthe Cd bio- ger 1985, Bolsinger and Fliickiger 1984, 1987, logy in the suborder Auchenorrhyncha, where 1989), on agricultural crops (Dohmen 1985, metal pollution biology is practically unknown Culliney and Pimentel 1986, Wanington 1987, Because considerable differences exists in the Warringtonet al.1987, Houlden et al. 1990,1991) bionomics between the two suborders,one may and on forest trees(Villemant 1981,Braun and also expect some dissimilarities in the pollution Fliickiger 1989,Wanington and Whittaker 1990, biology.Some dissimilarities are described below: Holopainenet al.1991, 1995, l99l Neuvonenet One essentialdifference is the much more ac- al. 1992,Holopainen and Oksanen1995). tive locomotion (umping, running and flying) of SO, hasbeen noted to more clearly affect aphid the auchenorrhlmchousHomoptera (Fritzsche et performancethan O, and N0, (Holopainen et al. al. 1972).Consequently, substantial proporlion of 1995, 1997, Holopainenand Kcissi 1998,Kainu- the dietary sugarsis neededto cover the energy lainenet al. 2000).Elevation of aphidpopulations loss, which results in a more diluted honeydew at roadsidesmay thus be more due to host plant (Schefer-Immel1957, Mitsuhashi and Koyama stressthan use ofNO, asa nitrogen source(Viskari 1969,197 t, 1975). & al. 2000a).Moreover,