The Mineral Nutrition of Bromeliaceae Author(s): D. H. Benzing and A. Renfrow Reviewed work(s): Source: Botanical Gazette, Vol.

135, No. 4 (Dec., 1974), pp. 281-288 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2474221 . Accessed: 15/10/2012 14:20
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135(4):281-288.1974. GAZ. BOT.

THE MINERALNUTRITION OF BROMELIACEAE

D. H. BENZING AND A. RENFROW Oberlin College, Oberlin, Ohio 44074 ABSTRACT Bromeliaceae exhihits a uriderange of habitat preferences, ranging from mesic terrestrial to arid epiphytic Much of this diversity is facilitated by adaptations which aid salt procurement and increase mineral use efficiency in the forest canopy. Three major nutritional strategies exist in the family: the one emDloyed by numerous terrestrial species of subfamilies Bromelioideae and Pitcairnioideae seems to differ very little from that serving many rooted terrestrials in other families- the tank and atmospheric strategies, however are based on much more specialized nutritional modes which are derived from the former. Each is dependent on a broad constellation of structural and functional features involving many parts of the plant hody and all phases of the life cycle. Tank nutrition is most effective on moist sites, while the atmospheric forms are adapted to drier, less fertile situations. Relationships among these nutritional strategies and the major taxonomic units of Bromeliaceae are proposed.

Materialandmethods Introduction inplantandothermaterial of elements suband analyses All epiphytism pronounced Because of its on wet digestedsamplesaccording stantial ecological importance in many New World wereperformed tropical and subtropical communities, Bromeliaceae to methods previously described (BENZING and . 197 1C) has attracted the attention of various kinds of RENFROW stemflowreportedin table 1 were reports of the Among Collections years. many biologists for collarsattachednear the generated by these workers are several designed to made using polyurethane elucidate the diverse adaptations which underlie the base of the trunkfollowingthe methodsof LIKENS werefilteredto remove unusual habitat preferences of many bromeliads and EATON(1970). Samples collection. after immediately 1948; particulates PITTENDRIGH 1913; PICADO 1904; (e.g., WIEZ 1971a, 1971b; BENZING The data in table 4 were obtained by dipping and RENFROW BENZING specimensfor 5 min each day for 1973). These studies document the existence of field-collected 2 X 1-5 unique combinations of functional and structural 120 days in a nutrientsolutioncontaining and S. P, Na, X, Mg, K, Ca, of concentrations counter M effectively specializationsin the family which the aridity and sterility of the epiphytic biotope and The salts used to makeup this solutionwereCaCl2, was accommodate these plants to the diverse levels of MgS04, NH4Cl,NaCl, and KCl. Phosphorus Sampleswere maintainedon illumination encountered within the forest canopy. providedvia HaPO4. in a growth Many of the significant details of these adaptations stainlesssteel traysbetweentreatments 1,500 of approximately illumination roomproviding remain unknown, however. were mainLeast understood but among the most important ft-c for 14 h each day. Temperatures of these adaptive features are those which relate to tainedbetween20 and 23 C. Each value represents the mineral nutrition of the epiphytic members of the averageand standarderrorof determinations the family. Bromeliaceae and just a few other made on six to nine rootless whole rosettes of or five to six clustersof rosettes circinafa families occupy what appear to be some of the most Tillandsia mineral-deficientenvironments inhabitated by vas- of T. usneoides.Each sample was carefully discular plants. The existence of so few major taxa in memberedand washed in distilled water before the drier (and probably least fertile) canopies sug- dlgestlon. proThe details of certain other e.xperimental gests that, along with other capabilities, bromeliads in the bod- of this report. areprovided and plants of similar habitat preferences possess cedures unusually effective mechanisms for accumulating Resultsand discussion mineral salts from dilute sources and that they can or to To a plant lackinga capacityfor parasitism utilize these limited substrates with vers high one unableto interceptand extractnutrientsfrom efficiency. particulatespassing This reportrepresentsan attempt to identify those litter and other mineral-rich aspects of epiphytic bromeliads which permit them througha tree crown, the forest canop) is quite to scavenge efficientls and utilize with great economv sterile.On all but the morehumidsites the surfaces withinthe forestprofileare nutrient salts from sources other than a mineral soil. availablefor anchorage andimmediately during e.xcept dr>, and bare tlsually Considerations of the evolutionary relationships to most Compared precipitation. of periods following in operating strategies ecological major the among mineral soils, these substrata provide rninimuna Bromeliaceaeare also made.
. .

281

Quercuslaetis Taxodiumdtstichum ............. .............

11 9.56 7 28.1 + 1.46 + 11.3 4.37 2.73 ++ 1.17 0.49 2.48 5.57+ + 0.33 2.540.98 2.47++0.21 0.58 3.01 8.17 + +0.28 1.88 0.68 0.422+ + 0.083 0.054

282

BOTANICALGAZETTE

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opportunities for the procurement of nutrient salts. Therefore, among other capacities, epiphytes on bark surfaces devoid of a moist nutritive mantle of organic debris and living organisms either must be able to generate their own soil by impounding, adjacent to their absorbing organs, appropriate substances from the environment which will decompose and yield dissolved nutrients or must be able to extract sufficient quantities of dissolved salt from the dilute fluids that briefly pass over the plant while rain is falling. These natural solutions, designated "fallthrough" or "stemflow," depending on the path followed through the canopy to the forest floor, are invariably enriched with solutes leached from plant tissues or washed from the atmosphere (TUKEY1970). The fertility of these fluids is determined by many factors including the relative leachability of mineral elements from a particular plant tissue, the time of year, the vigor of the host and the proximity of a marine habitat. Rarely, however, are such macronutrients as K, N, or P present in these solutions in concentrationsexceeding a few parts per million. A number of accounts have been published which provide some insight into the chemical makeup of rainfall as it passes through a forest profile (e.g., CURTIS 1946; TAMM 1951; MCCOLL 1970). Unfortunately, few of the analyses reported were performed on waters collected from trees supporting vascular epiphytes. The composition of stemflow recovered from several trees hosting bromeliad and orchid epiphytes in south Florida is presented in table 1. Note that the concentrations of all the elements which were monitored are low, but phosphorus is always the most dilute. These values are not substantially differentfrom those established for other woody plants in temperate and other tropical regions; they suggest that plants dependingon these solutions for the major portion of their mineralneeds have access to far smaller supplies of salts than most terrestrialspecies growing in soil. Constraints in addition to the low availability of nutrients per se may interferewith salt accumulation by many bromeliads and other extreme epiphytes. As is the case with most drought-enduring angiosperms, a low surface-to-volume ratio is maintained

by many bromeliads. Through this small interphase between plant and environment, which so efifectively reduces transpiration, must pass all the mineral nutrients required for growth and reproduction. Furthermore, the absorption of solutes is restricted to those brief intervals when the epidermallayers of the specimen are wetted with solutions containing nutrient materials. One of the major barriers to successful epiphytism, then, is the problem of securing enough nutrient salts in the forest canopy to support acceptable rates of growth and adequate reproductive output. Three ecological strategies exist in Bromeliaceae; two facilitate very distinct and efifective modes of epiphytism, and the third is operational in Pitcairnioideae,a predominantlyterrestrialgroupwhich, judging by its floral and vegetative structures, is the most primitive of the three bromeliad subfamilies (fig. 1). The nutrition of the pitcairnioids, as well as their general ecological strategy, probably most closely approximates that of the family prototype. Rooted terrestrials also occur in substantially epiphytic Bromelioideae. Although rare in Pitcairnioideae, tank rosettes are found in all three subfamilies, while atmospheric types are restricted to Tillandsioideae. Figure 1 also depicts the probable phylogenetic relationshipsamong the three subfamiliesand the three ecological strategies of Bromeliaceae. The details of this proposedscheme will become apparent as the discussion continues. Among the ecologically more advanced elements of Bromeliaceae (the epiphytes), the conventional division of labor between root and shoot systems has been altered markedly. In addition to serving its usual role as the site of photosynthesis and sexual reproduction, the shoot has assumed the additional task of salt and moisture procurementfor the entire plant body. Depending on the species and the severity of its preferred habitat, the root system is reduced in extent and modified in function for attachment rather than absorption. Some bromeliads occupying the driest sites may have little or no root development as adults (PITTENDRIGH 1948). Two features of the shoot, the occurrenceof tank leaves and the presence of absorbingtrichomes, have been unusually important in the attainment of

TABLE 1
MINERAL COMPOSITION OF STEMFLOW COLLECTED FROM TREES WHICH HOST ORCHID AND BRONIELIAD EPIPHYTES No . o F IND IVIDUA L z SAMPLED CONCENTRATION (ppm) OF ELEMENTS Ca K Mg N Na P

TREESPE CIE s

NOTE.-Samples were collected during a thunderstorm December 1, 1971, from trees in the University of South Florida Ecological Preserve.

1974]

BENZING & RENFROW MINERAL NUTRITION OF BROMELIACEAE

283

epiphytism in this family. Each in its most advanced the nutrients needed to attain fairly large size and to expression is associated with a dififerentnutritional produce sizable crops of fruit and seed within a few mode. The more widespread tank strategy is well years after germination. The extent of the mineral suited to wet sites, while the second mode, which supply present at a given time within the tanks of and Guzmaniamonosfachia appears to rely very heavily on the foliar trichome, adult Catopsisfloriburzda from south Florida is illustrated in table 2. Among is most adaptive on drier locations. Impoundments capable of intercepting and hold- tank species, both are small; yet the quantities of ing moisture and debris are found in several families, several impounded nutrients such as nitrogen are but none is more effective in creating a soil substitute relatively sizable in both. To what degree the relative or is more important to the survival of the plant than proportions of each element in these tanks had been the tank rosette of Bromeliaceae. The overlapping altered by the rosette prior to sampling is unclear. inflated leaf bases and channeled blades create a Relatively high nitrogen levels (as opposed to such series of watertight catchments which, in humid elements as K and P) may result because this climates, may maintain permanent pools of fresh nutrient is more slowly reduced to a soluble form water serving a great variety of invertebrate and from the decomposingvegetation which makes up the vertebrate terrestrialand aquatic organisms (PICADO bulk of the solids in the tank. No doubt some 1913; LAESSLE 1961). Several investigations have elements are absorbedpreferentially. Some measure of just how rapidly salts maST acillustrated the effectiveness of the tank microcosm as a source of mineral nutrients and moisture for the cumulate in the leaf axils of a tank rosette is ilrosette (PICADO 1913; BENZING 1970b). Apparently lustrated in table 3. In this experiment, urine sample the surfaces of the leaf bases are sufiiciently perme- bottles were attached upright to tree limbs in a able to permit the shoot to obtain from its tanks all well-drainedoak stand and in a nearb- swamp about

FrG.1. The proposed relationships amongthe nutritional strategiesof Bromeliaceae and its threesubfamilies

284

BOTANICAL GAZETTE

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1 mile north of Tampa, Florida. All were left debris and moisture. At first these crude tanks may undisturbed fromSeptember 7, 1971to July 100 1972. have been exploited by the root system. Later, with To a degree,each samplecan be compared to the further refinements of the tanks, foliar absorption singleaxil of an averageto largebromeliad rosette, prevailed and epiphytism developed. Comparable since the volume and apertureof a urine sample stages in this evolutionary sequence can be found bottle are of comparable size. Again, differences among extant species of Bromelia and other genera among samplesexisted in the total amountsand of Bromelioideae. relativequantitiesof all six elementsassayed.As in j More equivocal is the proposed evolution of tank real tankst phosphoruslevels were consistently epiphytism in Tillandsioideae from a xerophytic, lowest.These differences in salt accumulation indi- nonimpounding, terrestrial ancestrv. Considerable cate that nutritional factorsmay affectsite quality evidence suggests that mesophytic tank forms rather for tank species and that such phenomenacould than nonimpoundingxerophytes (atmospherics)posplay an importantrole in determining where in- sess the primitive growth form, water balance dividualspecimens becomeestablished and succeed mechanisms, and mineral nutrition in the subfamily in the canopt,-. (BENZING and RENEROW 1971a, 1971b). The origin and BURT1970) may Tankleavesarecharacteristic of numerous genera of the latter type (BENZING in Bromelioideae and of some species of the pit- have taken place in a neotenous fashion (fig. 1). In cairnioid genusBrocchinia,and occurin everygenus any case, the tank habit as well as epiphytism itself of Tillandsioideae(fig. 1); but the evolutionary appears to have originated independently in each status of the impounding rosettein each subfamily subfamily. The mineral nutrition of the so-called air plants or remains undetermined.PITTENDRIGH (1948) has suggested a very plausible explanationfor the atmospheric bromeliads has generated much comsimultaneousdevelopmentof tank nutrition and ment but little data over the years since these plants epiphytism in Bromelioideae. According to this were first discovered by European explorers. Attheory, the bromeliad prototypewas a terrestrial mospheric bromeliads rely on an ecological strategy form adaptedto arid conditions;nutritionalinde- which seems to be predicated on a very highly pendence froma substratum was attainedas its leaf specialized mineral nutrient and water economy. baseswereprogressively modified to collectairborne Because their roots are reduced to an attachment
TABLE 2

TOTAL QUANTITIES OF SIX ELEMENTS IN LIQUID AND DEBRIS IMPOUNDED BY THREE ROSETTES EACH OF IMMATURE CATOPSIS FLORIBUNDA AND GUZMANIA MONOSTACHIA OVEN-DRY a WEIGHT (g) OF TANK CONTENT s oF 1 ROSETTE

ELEMENT (mg) PERGRAM DREWEIGHT Ca 13.3 13.3 13.8 18.3 10.1 13.0 K 0.55 0.57 0.28 0.60 0.43 3.01 Mg 0.62 1.07 0.81 0.80 0.46 1.17 N 14.4 22.1 18.7 12.6 15.7 14.2 Na 0.30 0.21 0.22 0.27 0.16 0.76 P 0.77 0.95 0.78 0.74 0.71 0.64

Catopsisfloribnda Guzmania monostachia

5.99 3.23 3.07 11.0 7.25 11.5

NOTE.-Samples were collected in southern Florida July 9-10, 1972. aAt 85 C for 24h. TABLE 3

ELEMENTS ^ACCUMULATED IN URINE SAMPLE BOTTLES (mg/BOTTLE) MAINTAINED IN CROWNS OF FOREST TREES NEAR TAMPA, FLORIDA, SEPTEMBER 7 1971-JULY 10, 1972 Sample no.

Tree species

Ca 5.36 5.74 11 .7 2.00

K 3.54 1.34 1.76 0

Mg 0.81 1.09 2.72 0.20

N 27.2 7.19 15.6 3.20

Na 2.43 0.84 3.68 0.30

P 3.23 0.41 1.46 0.28

1. . . . . .
2. . . . . . 3. . . . . .

4. . . . . .

Querc1fs virginiana (upland) Q. nigra (swamp) Q. nigra (swamp) Q. Zaevis(up]and)

NOTE.-The entire contents of each bottle were included in the analysis.

1974]

BENZING & RENFROW MINERAL NUTRITION OF BROMELIACEAE

285

role or are missing altogetherin the adult and andBromelioideae attainthe samestageof maturity becauseno tanks are presentat any growthstage, and often reachmuchlargersize in half that time. these plants must derive all of their nutrientsalts Liberal applicationsof fertilizersand water plus directly from rainfall, fallthrough,and stemflow. various quantities of sunlight fail appreciablyto Not only are they usually unable to create and acceleratethe growthof these plants in the greenmaintain a soil substitute, but these species are house. Unlike many plants from relativelyfertile poorly equippedto absorb salts which might be environments, andmorelike mostothersadaptedto availableon the barksurface.A possibleexception soils of low fertility, these epiphytesseem to have may be the myrmecophytic species,as theseplants ratherlimitedabilitiesto improveyield in response may be operatingmore like tank forms than like to increased mineral nutrientand moisture supplies. atmospherics (BENZING 1970a). An appropriate growth habit coupled with the In contrast to atmospheric forms,tankbromeliads regularproductionof offshootscan also increase are restricted to communities whereimpoundments mineralnutrienteconomy.It is probablyno coincican be frequentlyreplenished with moisture.High dencethat extremeepiphytism in Bromeliaceae and humidity and frequent rains are deleterious to otherepiphytic taxasuchas Orchidaceae is frequentatmospherics, however,since the moistureheld by ly associatedwith monocarpicor relativelysmall the peltate trichomes againstthe shoot retardsgas polycarpicshoots exhibiting determinategrowth. exchange(BENZING and RENFROW 197l b). Within Oldercolonies of suchplantsare typicallycomposed the subfamily only two generaof six, Tillandsia and of successivegenerations of asexualoffshootsthat closely relatedVriesea, are involvedin this unique individuallyremainalive several years after their ecologicalstrategy.The remainder are tank forms reproductive roleis terminated. Analysis of Tillandsia circinata coloniesin Floridasuggeststhat elements (fig. 1). Mineral nutrition consistsof two somewhat exclu- such as K, P, and N are effectivelymobilized from sivephases, procurement andutilization. Adaptations postfruiting shootsand areusedagainin subsequent which enhanceprocurement as well as phenomena generationsof offshoots (BENZING and RENFROW whichincrease mineral use efficiency will be favored 1971c).Whetherthese epiphytescan mobilizemost in sterilelocationssuchas the forestcanopyas long of the K, P, and N fromsenescingtissues,and thus as their presencedoes not overly antagonizesome reserve unusuallylarge fractionsof their modest other vital function of the plant. Some of these pools of these elements for future seed crops by possibleadaptations are listed in the Appendix.A recycling via asexual reproduction,is unknown. discussion of theseand the evidence, if any, for their Apparently certain bogplantsareunusually effective existence in Bromeliaceae is presented below. in mobilizing at leastN andP priorto leafabscission, Becausethe mineralneeds of all plants are inti- andthiscapacitymayrepresent an effectual response mately linkedto biomassproduction, growthrates to the extremeinfertilityof theiracidicsubstratum are particularly importantin environments of low (SMALL 1972). fertility. All plants must accumulateprescribed The partitioningof resourcesbetween a plant's species-specific amounts of each essential mineral sexual and asexual reproductive efforts can have elementif optimumfunctionis to be achieved.A greatecological significance (HARPER 1967).A plant specieswhoserateof biomass production is inherent- employinga reproductive strategy which features ly slowpresumably has moretimeto accumulate the the allocation of smallfractionsof a scarcenutrient requisite solutesfor growthand reproduction thana to seed production while most of its supplyof this morevigorous one. Fast-growing speciesare usually elementis reserved for the moredependable producadaptedto fertilehabitatsand employan ecological tion of offshoots is bettersuitedto succeedin sterile strategy predicatedon the rapid attainment of habitats (as long as sufficient dispersaland genetic maturityor large size and the productionof sub- recombination are accomplishedto maintain the stantial masses of reproductive material.On less species) than are those plants which allot greater fertile sites these same individualsoften develop proportions of theirnutrient pool to seedproduction. debilitating deficiencies, lose competitiveabilitS,or Althoughthe expenditure of mineralsinvolved in fail to maintain the necessarylevels of vigor or sexualreproduction is not knownfor any bromeliad, reproduction to persist(MONTGOMERY 1912;BRAD- mostatmospherics produce relatively fewsmallseeds, SHAW 1969;GOODMAN 1969). while tank tillandsioids, particularly the few which Atmospheric bromeliads mature muchmoreslowls typically fail to produceoffshoots,generatemany tend than terrestrial and tank bromeliads. Atmospheric moreseedsof aboutthe samesize. Bromelioids tillandsiascommonlyrequire4 or more 5 ears to to ripennumerous, muchlarger,seeds.Pitcairnioids reachfirstflowering fromseed, whereas mesophytic often producesmallseeds,but the numberstend to terrestrials and many tank formsin this subfamily be large.Unlikemanytankandterrestrial forms,the

A. Aechmea Catopsis C Pitcairnia T. G. Bromelia Vriesea foribunda paniculigera monostachia baltrisiana usneoides pruinosa circinata nudicaulis splendens karatas berteroniana spTillandsioideae ........................... ........................... ........................... ........................... ........................... ........................... ........................... ........................... ........................... .......................

Bromelioideae Tillandsioideae Pitcairnioideae Tillandsioideae Tillandsioideae Tillandsioideae Tillandsioideae Bromelioideae Bromelioideae Tillandsioideae Florida Jamaica Dominica Florida Florida Florida Jamaica Florida Trinidad Trinidad 1 Jamaica 1.. 19 150.70 0.26 0.83 0.67 0.51 0.73 2 0.34 1 0.38 0.36 .0.40 .59 48 0.48 1.70 0.34 1.03 0.50 0.32 1.94 1.94 1.43 0. 0.72 0. 0.18 14 0.24 0.0.15 18 0.14 0.29 0.20 0.12 0 14 1.0.81 0.73 0.36 0.54 0.60 .36 0.82 0.34 67 0.57 0.89 1.140. 0.044 0.32 0.38 0.41 0.10 0.81 0.55 0.65 0.48 0.18 0.55 064

0. 0.091 0.060 0.095 0.035 0.075 0.042 0.085 0.058 0.057 0.012 0.029 068

286

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total reproductiveoutput each season from atmospherics represents a very small fractionof the total biomassandprobably only a smallpart of the total mineralresource of the parentat the time of fruit dehiscence. Providingthe necessary mobilities exist, the nutrients remaining in a postfruiting shoot (perhaps the bulk present before the seeds are dispersed) couldbe usedto generate successive crops of seed and the vegetativetissuenecessaryto ripen them. In environmentssuch as xerophyticones where relativelyfew growingseasons provide the optimumconditionsrequiredfor seed germination andseedling establishment, the generation of sizable seed cropsincorporating large portionsof a slowly accumulated mineral wouldbe disadvantageous. By prolonging the expenditure of a limitedresource over many seasons,the probability that a few of even a smalltotalnumber of seedswillbe dispersed at times coincident with conditions favoring germination and establishment is increased. All plant organs are permeableto mineralnutrients, and salts may be absorbedas well as lost throughthe surfacesof most, if not al], healthy stemsandleaves.However, the shootsof someplants seem to be more resistantto leachingthan others (TUKEY1970). Epiphyteswouldbe well servedby adaptations whichretardleaching. To date,no informationon leachingis availablefor Bromeliaceae or any othergroupof epiphytes. As indicated by the largeconcentrations of certain mineralswhich must be presentin some plants to prevent the appearanceof deficiencysymptoms, numerousfield crops and other plants adapted to fertilehabitatsmaintainhigh nutrientdemands per unit of biomassproduced. Othersfrommoresterile
TABLE ELEMENTAL COMPOSITION OF LEAF BLADE ALL THREE TISSUES

sites may requiresmallerquantitiesof the same nutrientsto generateequivalentweights of tissue (WUENSCHER and GERLOFF 1971). On a dry or a fresh weight basis, the mineralcomposition of the leaves of field-collected bromeliads of normalsize and vigor for their type correlates with the availability of nutrientsto thoseplants in theirpreferred habitats.Judgingfromthe smallquantities(table4) of several macronutrients in the leaves of these healthy field specimens,atmospherics requirethe smallestquantities of K, P, and N per unit of living leaf tissuefornormal functionamongthe nutritional types in Bromeliaceae.The quantities of these macronutrients in the leavesof both tankformsand rooted terrestrials tend to be substantiallylarger and are comparable to the levelsreported in similar tissuesof terrestrial species frommanyotherfamilies. Elements suchas CaandMg seemto be less affected by habitatpreference. Sodiumcomposition is much higherin tank and atmospheric epiphytes.Conceivably,Na maybe replacing someof the K requirement in thesemorespecialized forms.All thesecollections weremadefromplantswellremoved in mostcases, by severalkilometers from the salt spray zone of the marineshoreline, so that they can be considered freeof salts accumulated directlyfromsea water. Plants able to exploit a supplemental sourceof nutrientsare likely to be better adapted to sites wherethe usualsuppliesof salts are dilute than are other species lacking the same capacity. Tank nutrition,variousformsof parasitism, and myrmecophilyare all feasibleways of increasing access to salts in a forestcanopywherethe barksurfacesare sterileand usuallydry. Unliketank epiphytism and parasitism,the nutritionalsignificance of myrme4 (<7O OF DRY WEIGHT) STRATEGIES FIELD-COLLECTED FROM

SPECIES

REPRESENTING

NUTRITIONAL Collection locality

IN BROMELIACEAE

Ecological strategy and species Rooted terrestrials:

Subfamily

Ca

Mg

Na

Pitcairnia bromeliafolia........................... Pitcairnioideae

Tank epiphytes:

Jamaica

1.06

1.02

0.14

1.37

0.036

0.084

Guzmania lingulata ........................... Tillandsia anceps ...........................

Atmospheric epiphytes:

Tillandsioideae Tillandsioideae

Trinidacl Trinidad

0.44 0.39

1.59 1.06

0.25 0.14

0.88 0.85

0.19 0.26

0.063 0.044

NOTE.-Each sample consisted of leaf blade tissues collected from two or more mature leaves taken from one or more healthy rosettes. Values for each species are based on three or more separate samples.

After treatment...............

1.142 | 0.045 0.334 + 0.022

1974]

BENZING & RENFROW- MINERAL NUTRITION OF BROMELIACEAE

287

TABLE 5 cophilyremainsunclear;but ant-plantassociations occur in severalgenerain both Bromeliaceae and TOTALN AND P CONTENTOFFIELD-COLLECTED Orchidaceae, as well as in epiphyticspeciesof AsTILLANDSIA CIRCINATA AND T. USNEOIDE.S SHOOTS BEFORE AND AFTERTRE;ATMENT clepiadaceae, Rubiaceae, and otherfamilies(WHEEWITH NUTRIENTSOLUTION LER 1942;BENZING 1970a). Because the root system is reducedor absent, COMPOSITION (X0 OF DRY WEIGHT) atmospherics and probablymany tank formsmust rely on theirshootsto absorbminerals. Despite the N P ability of the foliar surfacesof virtuallyall higher plantsto absorb somesalts, compared to the typical Tillantlsia circinata: Before treatment ................. 0. 436 + 0. 019 0. 0185 + 0. 001 root system most leaves and stems are poorly After treatment ................. 1 .395 + 0. 118 0.383 + 0. 064 adaptedfor salt uptake.Amongatmospherics, how- T. usneoides: ever,the necessary foliarpermeability to compensate Before treatment . . . . . 0. 743 + 0 . 082 0 . 0184 + 0 . 001 7 for the absence of an absorbing root systemand the often transitory contactbetweenabsorbing surfaces and nutrientsolutionsseemsto be providedby the presenceof unique absorbingtrichomeson most intervalsof time is illustratedin experiments on surfacesof the shoot (SCHIMPER 1888; MEZ1904; Tillandsia circinata and T. usneoides. When fieldBENZING and BURT 1970) . collectedplants were derootedand immersedin a All bromeliads but one possessfoliartrichomes of nutrient solutioncontaining macronutrients and Na one kind or another (TOMLINSON 1969). In most at 2 X 1-5 M for about 5 min each day, N and P instances this appendage has a complex multicellular were taken up at a rate whichincreased the initial peltate structure including a disk of dead cells sublevels of each nutrientsubstantially after 120 days tendedby a stalkof livingones.The stalkpenetrates (table 5). During this period,P accumulation was the epidermis andapparently servesas a conduitfor greatest, with a 20-fold increase in the case of T. wateror solutesfromthe environment to the mesocircinata. Apparently both species can effect luxury phyll in many taxa. Membersof Tillandsioideae since the quantitiesof each element exhibit the most specialized of these organs (MEZ accumulation, sequestered far exceededthose required for growth 1904;TIETZE 1906;DOLZMANN 1964;BENZING and during the period of treatment. The adaptive sigBURT 1970).Whenthe trichome coveris dense,as it nificance of luxuryconsumption amongplantsfrom alwaysis amongatmospherics, up to 5.0<7o or more environments wherenutrientsmay of the foliarsurfacemay be occupiedby the stalks sterileterrestrial be available for only limited periods each growing of theseuniqueabsorbing appendages (BENZING and season has been recognized by others (SNAYDON and BURT1970). Tank and terrestrialbromeliads,in BRADSHAW1962; JEF]?REY1964; RORISON 1969). contrast,usuallyfeaturea sparsertrichomecover, the low availabilityof P in the forest and the bromelioid and pitcairnioid(membersof Considering canopy, the great avidityfor this particular element Bromelioideae andPitcairnioideae, respectively) disexpressed in these two species takes on added tal stalkcellsareoftensmaller. Usuallyno morethan slgnl: lcance. l.O'Wo of the leaf blade surfaceis occupiedby the The detailsof the mechanisms whichunderlie the trichome stalksin thesespecies. considerable ecological diversity of Bromeliaceae and The remarkable water-absorbing capacityof the the unusual tolerances to environmental tillandsioid trichome has been appreciated for some in particular extremes of certain of its most specialized members time, but the role this appendageplays in salt remainincompletely known.It is at this point quite absorption throughout the familyis less clear (MEZ clear, however,that distinctlydifferentand some1904;Aso 1909;BENZING and BURT 1970).Recent times unusualmodes of mineralprocurement and experiments employinglabelednutrients(BENZING utilizationand differentdemandsfor nutrientsalts and BURT 1970; BENZING 1973) indicate that the are operativein the familyand that these patterns leaves of atmospherics are capableof accumulating of function are associatedwith specificecological much larger quantitiesof Ca, P, and Zn during strategies, habitat preferences,and characteristic short periodsof contact with dilute nutrientsolu- root and shootmorphologies. tions than comparable preparations of blade tissue fromtankandterrestrial bromeliads. Directevidence Acknowledgments of the involvement of the trichome in salt accumula- This workwas madepossibleby NationalScience tion is still lacking,however. Foundation research grantsGB 8790and PIB 3364. The effectiveness of the shoot of the atmospheric The assistanceof JANICE DERR is gratefullyapbromeliad as an organforsalt absorption overlonger preciated.
. .

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BOTANICALGAZETTE
APPENDIX

PATTERNS OFFORM ANDFUNCTION WHICH COULD ADAPT VASCULAR PLANTS TOMINERAL-DEFICIENT HABITATS

1. Slowratesof growthand smallstatureat maturity. in living tissuewithoutsacrificing necessary vigorand 2. Regularasexualreproduction of monocarpic or small reproductive capacity. polycarpic shoots coupledwith the efTicient recovery 6. The capacityto substituteone elementfor anotherin of nutrientsused to sustainthe vegetativeportionsof certain metabolicroles. previousgenerations of shoots. 7. The ability to exploit mineralsourcesnormallyun3. Patternsof sexual reproduction which requireminiavailable to higherplants. mumexpenditures of nonrecoverable mineral nutrients 8. Highaffinities forminerals in very dilutesolutions and (thoseusedfor seedand fruitproduction). the ability to absorbrapidlyand sequesterthese es4. Resistanceto mineralloss by leaching. sentialelements whenthey becomeavailable. 5. The abilityto toleratelow levelsof essentialnutrients
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