Nickel uptake by Flacourtiaceae of New Caledonia

Transcription

1 : Froc. R. Soc. Lofid. B 05, 869 (979) printed in Great Britain Nickel uptake by Flacourtiaceae of New Caledonia BY. JAPFRÉ?, w. KERSEN~, R. R. BROOES$ AND R. D. REEVES$?Cente ORSO, Noud, New Caledonia $Department of Chemistvy, Biochemistry and Biophysics, assey niversity, Palmerston North, New Z&nd (Communicated by R. E. F. atth, F.R.S. - Received October 978) Herbarium and field specimens (over 00) of all of the Flacourtiaceae of New Caledonia were analysed for nickel in order to identify hyperaccumulators (> 000 pg/g dry mass) and to assess nickel accumulation in relation to the evolutionary status of nickel plants of New Caledonia. One hyperaccumulator mas identified in the genus Lasio- Chlamys, ten among Xybm, one among Casearia and seven among Homlium. Although these HomaZium nickel plants had previously been. recorded, fresh data for these and other Hmlium are presented. he remarkable tolerance of Flacourtiaceae to ultrabasic rocks is shown by the fact that 75 yo of the species are found on such substrates. he number of hyperaccumulators was greatest in the genera Xybsma and Homalium. he Flacourtiaceae are among the most primitive of all angiosperms and in common with other primitive hyperaccumulators, contain nickel as a complex with citric acid. he only advanced New Caledonian nickel plant (Psychotria douarrei) has most of its nickel bound with ligands other than citric acid, a feature of other advanced hyperaccumulators. It is postulated that nickel complexing with citric acid may be a primitive character. ost of the New Caledonian nickel plants belong to the order Violales of subclass Dilleniidae. It is suggested that hyperaccumulation of nickel is an evolutionary character which occurs in long-indisturbed floras such as that of New Caledonia.. INRODCION Althoûgh the nickel content of plants not growing over ultrabasic or other nickeliferous rocks is usually less than pg/g (dry mass), significantly higher levels (0-00 j.tg/g) are found in serpentine floras. Occasionally plants are found with nickel. concentrations in the range pg/g ( %). Such planta have been termed hy~zracc~m~lators of nickel (Brooks et al. 977). his classification is concerned only wi%h the nickel concentration in the plant and does not substitute for more specifk (though potentially confusing) terms indicating relatidns. between plants and their substrates (see, for example, Duvigneaud & Denaeyer-De-Smet 96). It also does not imply that all individuals of a given species will necessarily contain > 000 pg/g nickel. -- v - \-

2 , I Jaffré Italy by inguzzi & Vergnano (98), another 70 such species (including a further species of Alyssum) have been reported. he largest number of hyperaccumulator species, all in the genus Alyssum, occurs in the Eastern editerranean (Brooks & Radford 978, Brooks et al. 979). Five nickel plants hitve been discovered in Southeast Asia (Brooks & Wither 977; Wither & Brooks 977) and ABLE. LIS OF COOPERAING HERBARLA ' ' institution abbreviation country France uséum National d'histoire Naturelle, Paris P Netherlands Rijksherbarium, Leiden L New Caledonia Centre ORSO, Noh& NO Switzerland Institut für Systematische Botanik, Zürich z nited Kingdom Royal Botanic Garden, Edinburgh E Royal Botanic Gardens, Kew K one in Western Australia (Severne& Brooks 97; Cole 97). wo hyperaccumulators have been reported from Africa (Wild 970, 97), but no species from he Americas has yet been found. he remaining 8 hyperaccumulators are confined to New Caledonia and include seven species of Homalium (Jaffé& Schmid I 97, Brooks et al. 97, 977)~ two Hybanthus (Jaffré & Schmid 97), seven Geissois (Jaffr6 & Schmid 97; Jaffré et az. 979), one Psychotria (Jaffré & Schmid 97)~ and one Sebertia (Jaffré et al. 976). In terms of density of occurrence and generic diversity, the hyperaccumulators of New Caledonia are unique. he de.i-elopment of so many species and genera of nickel-tolerant plants in New Caledonia probably results from two main factors : the relatively large area of ultrabasic rocks upon the island (i.e. one third of its km) and the isolation of New Caledonia from continental masses and a subsequent development of a flora with 80 % endemism at the species level. Sleumer (97) has recognized 5 species and genera among the Flacourtiaceae of New Caledonia and-the Loyalty Islands. hey- include Lasiochlamys ( species), Xybosm (8 species), Casearia (6 species) and Homalium (6 species). Because investigations among most of the New Caledonia Homalium species have already revealed the existence of seven hyperaccumulators (Ja&é & Schmid 97; Brooks et al. 97, 977), it would obviously be of interest to examine the whole of the Homalium genus in the island as well as other genera of Flacourtiaceae within New Caledonia, in the expectation of discovering fixther nickel plants 5 a family well represented in New Caledonia. he data would be of additional significance for attempting to explain more fully, the reasons for the concentration of so many hyperaccumulators upon this island. he results of such a surv'ey are presented in this paper. ;.-.I -. _ I _--I_ p.-.

3 Nickel uptake by Plucou&aceae of New Caledonia 87. AERIAL AND EHODS (a) Plants sampled Plant material was supplied from the herbaria listed in table. Over 00 specimens of all the 5 species listed by Sleumer (97) were analysed for nickel. hese species are listed in table together with the number analysed. (b) Analytical procedures Dried leaf samples with an average mass of about 0.0 g (about em) were placed in 5 cms borosilicate test-tubes and ignited at 500 "C in a muffle furnace. he ash in each tube was then dissolved in ems of HCl. he solutions were analysed for nickel by atomic absorption spectrophotometry. Automatic corrections for non-atomic absorption were made using a hydrogen continuum lamp. All concentration data were expressed on a dry mass basis. Although analytical data were presented to three significant figures, there was an approximately 0 % intraleaf, and 0 % interleaf variability in the nickel content of a given herbarium specimen. Although this variation was appreciable, it was far less than the interspecific variations of the nickel contents of the plants and can therefore be considered as relatively unimportant. Since both nickel and chromium are present in comparable concentrations in New Caledonian soils (Jaffré et al. g7), and since chromium uptake by plants is usually very slight, the chromium content of samples high in nickel was used as an index of possible contamination because dried herbarium material is impossible t.0 wash. Specimens with chromium contents exceeding 0 pg/g were therefore assumed to be contaminated and were reject.ed. On occasions, plants may accumulate significant amounts of chromium. here was therefore the possibility that some of the rejected specimens were ignored unwarrant-edly. However since only three or four specimens were in fact, rejected, this possibility does not affect the data to any significant degree. I. RESLS AXD DISCSSION Nickel concentrations exceeding 000 pg/g (dry ma.ss) mere found in one species of Lasiochlamys, ten of Xylosma, one of Casearia and seven of Homalium. Concentration data are shown in table. his table also includes information on the type of substrate and on the collection localities. Collection localities are coded in table and are shown in full in figure. As far as possible 'type' material (including types, isotypes, holotypes and lectotypes) was used. In all cases, the planits represented type material and authenticated specimens originally studied by Sleumer (97) in his revision of the family (numbers indicated in table ). he use of such material ensured a minimum of misidentifications (a common problem with herbarium specimens). he relatively large number of specimens of Homalium

4 w ABLE. NICKEL CONCENRAIONS (pg/g DRY ASS) IN HE,FLACORIACEAE OF NEW ALIDONIA species () L. koghienkis (Guillaumin) Sleumer () L. pltuta Sleumert () L. coriacea Sleumer () L. pseudocoriacea Sleiimer (6) L. rivularis Sleumer (6) L. trichoslemna (Guillaumin) Sleumer (7) L. fusciculata (Guillaumin) Sleumer (8) L. cordijolics Sleumer (9) L. hiirlimcsnnii (Guillaumin) Sleumer (0) L. grossecrenatu Sleumer () L. reticulata (Schlechter) Pax & Hoffman () L.?jeliana Sleumer () L. planchonelluefolka (Guillaumin) Sleumer number,; li { f; mean Ni range Genus I.siochla?,tys substrate. u N N N N collection locatio? (see figure i) 8, 9, 9, 7, a 0 9 G. G, 7, 8,, -. authenticated material analysed s (5) s () s () *r s () S s (5),

5 able (cont.) () X. otbiculutum (J. R. & G. Forster) G. Forster () X. pinisulare Guillaumint () X. pancheri Guillaumint () X. dothioenae Guillaumint (5) X. vincentii Guillaumint (6) X. capillipes Chilhumin (7) X. nervosum Guillaumin (8) X. serpentinum Sleumert (9) X. lancgozium* Sleumer (0) X. giguntifolium Sleumer ( ) X. inuequinervium Sleumer () X. bernardiunum Sleumor () X. boulindue Sleumert () X. kuulenae Sleumert (5) X. confusum Guillaumint (6) X. molestum Sleumert (7) X. tuberacuhtum Sleumert ( 8) X. Zifuunum Guillaumin Genua Xylosma ' GOO - NJ N N 0, 0 u, 5, 9, 6, 50, 65 8, 9, 5,, 6, 7, 9 8, 8, 0,,, 6, 57, 58, , 7, 5 5, 7, 8 iou Genus Casearia () C puberula Guillaumin, () C. coriifoolia Lescot & Sleumer () C. kaalemis Lescot & Sleumer () C. deplunchei Sleumer (5) C. ifu.ana DBniker (6) C. me&hx" Sprengel? ,, 6, 7, 7,, 7, 6

6 () H. serratum Guillaumin () H. buxifolium Dliniker () H. kanaliense (Vieillard) Briquett () H. rubiginosum (Vieillard) Warburg (5) H. austrocaledonicunt Seomannt (6) H. deplanchei (Vieillard) Warburg? (7) H. decurrens (Vieillard) Briquet (8) H. rubrocostatum Sleumer (9) H. guillainii (Vieilard)t Briquet (0) H. francii GuiIlaumint () H. intermedium (Vieillard) Briquet () H. rivulare (Vieillard) Briquet () H. mathieuanttm (Vioilard)t () H. justnposituin Sloumor (5) H. polyskzchyum (Vieillard) Briquet F able (cont.) Genus iomalium F- IGO ci N N 0, 55, 58 59, 7 7 9,0 F, 7, 55, 66, , 8 6, 7 (6) H. le-ratiomm Guillaumin 6 7, 8, 9 t Hyperaccumulator status. S, Including specimens (number in parentlieses) examined by Sleutnor (I 97) ;, authenticated material including types, isotypos, holotypes or lectotypes;, ultrabasic rocks; N, non-ultrabasic rocks; Bf, ultrabasic and othor rocks. 9, 9 a, ew Co O

7 .i/-. Nickel uptake by Flacourtiaceae of New Caledonia 9 ka?zu.liense (8) and H. guillainii (7) represented mainly material collected by 'the authors in the field. he seven hyperaccumulators in the genus Homalium (table ) have previously been reported bjr. Jaffré 6: Schmid (97), and Brooks et. al. (97,977), but the present data include many more specimens (60 instead of 6) and encompass all sixteen species (instead of ). Data for Lusioch,laanzys, Xylosma and Casearia are entirely new. \$ES BELEPf ) I Piotrv dc5 Lacs ;l 'e v,,<?: FIGRE. ap of New Caledonia showing areas of ultrabasic rocks. mbers adjacent to place-names are referred to in table. ', he Flacourtiaceae of New Caledonia have an inordinate tolerance of ultrabasic substrates. About 75 % of all species are found on ultrabasic rocks and 5 yo are found on non-ultrabasic substrates. At least half of the species are exclusive to ultrabasics. his distribution is remarkable since ultrabasic rocks cover only one third of New Caledonia. he proportion of hyperaccumulators is greatest among the Xyosm.a (0 out of 8) an$ Honzalium (7 out of 6) species. Even among the remaining species of these genera, nickel uptake is very high. here are three species of Lasiochlanzys with nickel contents in the range pg/g (an upper limit for most serpentine species, and four species of Xylosma, two of Casearia and four of Homalium in the same Category. Even among plants growing on supposedly non-ultrabasic substrates, nickel lerels arc surprisingly high. Such examples are L. trichostemona

8 9. Jaffré (9 pg/g), L. grossecrenata (6 pg/g) and H. rivulare (5 pg/g). However in some cases, these non-ultrabasic soils consist of alluvia derived originally from the weathering of ultrabasic rocks and which still retain an appreciable nickel content. he presence of so many hyperaccumulators (9 out of 5 species) in a single family raises interesting questions as to the mechanisms whereby nickel is not only tolerated, but is also accumulated by the New Caledonian plants. Phytochemical studies on : Sebertia acuminata, Ceissois puinosa., Hybanthus awtrocaledonicus, Hybanth,u.s inledonicu.a, and species of Homalium, have shown a strong correlation between levels of nickel and of citric acid in leaves (Lee et al. 978). Lee et a. (977) have isolated a citrate complex of nickel from Sebertia acuminata, Hybanthus austrocal edonic us, Hybant hus caledonicus, Homalium francii, H omalium guillainii, und Homaliunt ka,naliense. here is no reason to doubt that the other hyperaccumulators of nickel among the Homalium and probably in the other genera of the Flaoourtiaceae also have their nickel completed with citric acid. From studies on seven of the New Caledonian hyperaccumulators it is apparent that with a single exception, most of the nickel is bound with citric acid. In the-,case of Psych.otrin doumrei (Rubieceo;e), however, only a small part of the nickel is bound to citric acid. he remainder is present as a relatively, low molecular weight cationic complex of unknown composition (Kelly et al. 975). All the New Caledonian plants with nickel-citrate complexes are members of primitive families. he advancement index as defined by Sporne (969) is as follows for each family : Flacourtiaceae (Lasiochlamys, Xylosma, Casearia, Hmalium) -, Cunoniaceae (Geissois) -, Violaceae (Hybanthus) -, Sapotaceae (Sebertia.) -, Rubiaceae (Psychotria) he advancement index (based on morphological characters) extends from (most primitive) to O0 (most advanced). It is clear that the advanced Psychotria dowtrrei is distinguished from all other, New Caledonian hyperaccumulators by its behaviour in complexing nickel mainly with a ligand or ligands other than citric acid. It is postulated therefore that nickel complexing with citric acid may be a primitive character of hyperaccumulators, reaching its highest development in the Flacourtiaceae, one of the most primitive of a. the angiosperms (Sporne 969). he postulate that nickel accumulation via citric acid complexing is a primitive character is strengthened by the findings of Lee et al. (978) who showed that advanced hyperaccumulators of the family Cruciferae (advancement index 6) complexed their nickel with malic acid rather than citric acid. he same finding was originally made for A. bertolonii by Pelosi et al. (976). It is appropriate now to consider the taxonomic classification (Cronquist 968) of the Flacourtiaceae and other New Caledonian families and genera of hyperaccumulators of nickel. With the exception of the advanced Psychotria (subclass Asteridae, order Rubiales) and the primitive Geissois (subclass Rosidae, order Cunoniae), all other New Caledonian nickel plants belong to subclass Dillenidae and the orders Ebenales (Sapotaceae) and Violales (Flacourtiaceae and Violaceae).

9 Nickel uptake by Placourtiaceae of New Caledonia 9 he occurrence of nnmerous nickel-accumulating species in the order Violales is not confined to New Caledonia. Brooks & Wither (977) discovered hyperaccumulation of nickel in the South-East Asian Rinorea bengale?tsis (Violaceae) and Severne % Brooks (97) discovered this character in the West-Australian species Hybanthus Joribundus (see also Cole 97). Within subclass Dilleniidae are also to be found (number of hyperaccumulating species in parentheses) the genera Alyssum (5 species), Phnchnelh ( species), Sebertia ( species), and richspermum ( species), though only one of these is found in New Caledonia (S. acuminata). he distribution of nickel plants among a very few subclasses and orders of the primitive agnoliatae is highly unusual. It is aiso probable that hyperaccumulation of nickel is an evolutionary character which reaches its greatest development in relatively undisturbed floras such as that of New Caledonia. any questions still remain unanswered, particularly in the phytochemistry a,nd plant physiology of these species. Further work is needed to account for the Iimited uptake of nickel by t.he large number of non-accumulators found in ultrabasic areas, and to explain the detailed mechanisms of uptake and translocation of nickel in hyperaccumulator species. Such uptake mechanisms are also of interest to workers in the field of nickel extraction and refining, since there is an obvious benefit in being able to emulate technologically, the low-energy extraction of nickel by plants. I he authors would like to express their warm thanks to the institutions listed in table and to the following individuals: Dr N. Hallé (P), Professor C. Kalkman, hlr A. K. Groenewegen, Dr H. Sleumer (L), he Director (NO), Professor K.. Kramer (Z), he Director (E), he Director (K). s,. REFERENCES Brooks, R. R., Lee, J. & Jaffré,. 97 Some New Zealand and New Caledonian plant accumulators of nickel. J. Ecol. 6, Brooks, R. R., Lee, J., Reeves, R. D. & Jaffré,. 977 Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J. geochem. Explor. 7, Brooks, R. R., orrison, R. S., Reeves, R. D., Dudley,. R. & Akman, Y. 979 Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc. R. Soc. Lod. B 0, 870. Brooks,'R. R. & Radford, C. C. 978 Nickel accumulation by European species of the genus Alyssum. Proc. R. Soc. Land. B 00, 7-. Brooks, R. R. & Wither, E. D. 977 Nickel accumulation by Rinorea bengalensit? (Wall.) O.K. J. geochem. Explor. 7, Cole,.. I 97 Geobotahical arid biogeochemical investigations in the sclerophyllus woodland and scrub associations of the Eastern Goldfields area of Western Australia, with particular reference to the role of Hybanthece$oribundus (Lindl.) F. uell. as nickel indicator and accumulator plant. J. appl. Ecol. 0, Cronquist, A 968 he evolution and classificatwn of jzowe7in.g plants, Boston: Houghton iffiin. Duvigneaud, P. & Denaeyer-De Smat, S. 96 Flore et végétation du cuivre au Katanga. Bull. Soc. r. Bot. Belg. 96, 06. Jaffré,., Brooks, R. R., Lee, J. & Reeves, R. D. 976 Sebertia acuminata: a nickel-accumulating plant from New Caledonia. Science, N.Y. 9,

10 9 '. Jaffré Jaffré,., Brooks, R. R. & row, J Hyperaccumulation of nickel by Geissois species. PI. Soil (in the press). Jaffré,., Latham,. 6: Quantin, P. 97 Les sols des mmsqs miniers de Nouvelle Calédonie. et leur relation avec la végklation. Nouméa: Spec. Rep. O.R.S..O.. Jaffré,. & Schmid,. 97 Accumulation du nickel par une Rubiade de Nouvelle Calédonie: Psychotria douamei (G. Beauvisage) Däniker. C. r. hebd. Séanc. Ad. Sci. Paris 78, Kelly, P. C., Brooks, R. R., Dilli, S. t Jaffré,. 975 Preliminary observations on the ecology and plant chemistry of some nickel-accumulating plants from New Caledonia. Proc.R. Soc. Lod. B 89, Lee, J., Reeves, R. D., Brooks, R. R. & Jaffré,. 977 Isolation and identification of a citrato complex of nickel from nickel-accumulating plants. Phytochemistry 6, Lee, J. Reeves, R. D., Brooks, R. R. 6: Jaffré,. 978 he relation between nickel and citric acid in some nickel-accumulating plants. Phytocbemistrg 7, ïnguzzi, C. & Vergnano, O. 98 I contenuto di nichel nelle ceneri di Alyssum bertolonii Desv. emorie Soc. tosc. Sci. nut. A 55, Pelosi, P., Fiorentini, R. & Galoppini, C. 976 On the nature of nickel complexes in Alyssum bertolonii Desv. II. Agric. biol. Chem. 0, 6-6. Severne, B. C. t Brooks, R. R. 97 A nickel-accumulating plant from Western Australia. Planta. 0, 9-9. Sleumer, H. 97 A concise revision of the Flecourtiaceae of New Caledonia and the Loyalty Islands. B lum, -7. Sporne, K. R. 969 he ovule as an indicator of evolutionary status in angiosperms. New Phytol. 68, Wild, H. 970 he vegetat<ion of nickel-bearing soils. Kirkia (suppl. to vol. 7), pp. -6. Wild, H. 97 Indigenous plants and chromium in Rhodesia, Kirkiu 9, -. Wither, E. D. & Brooks, R. R. 977 Hyperaccumulation of nickel by gome plants of S. E. Asia J. geockem. Explor. 8,