Great Basin Naturalist
Volume 53 | Number 1
Article 8
4-2-1993
Cyanobacteria and cyanolichens: can they enhance
availability of essential minerals for higher plants?
Kimball T. Harper
Brigham Young University
Rosemary L. Pendleton
Shrub Sciences Laboratory, Intermountain Research Station, USDA Forest Service, Provo, Utah
Follow this and additional works at: http://scholarsarchive.byu.edu/gbn
Recommended Citation
Harper, Kimball T. and Pendleton, Rosemary L. (1993) "Cyanobacteria and cyanolichens: can they enhance availability of essential
minerals for higher plants?," Great Basin Naturalist: Vol. 53: No. 1, Article 8.
Available at: http://scholarsarchive.byu.edu/gbn/vol53/iss1/8
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Grcat Basin Naturalist·,)·'3tl), pp. ,')9-72
CYANOBACTERIA AND CYANOLICHENS, CAN THEY ENHANCE
AVAILABILITY OF ESSENTIAL MINERALS FOR IIIGHER PLANTS?
I
Kimball T. Ha'lJer and Hoselllary J,.
,
Pcndlchlll~
lJOtb field and ?;reenhouse sLudies, (':'alH)hact(~ria aJld cyaJlo]ichpns of cold-telllpf'rate rlf'SPltS oftP]}
f'nhance growth and essential elClIl('llt uptake In- associated herbs. ThaL er'f('ct is associated \vith hetter seedling estahlishment and larger s('cdlillgS, The following are IXlssible mechanisms for these cO'eds: (1) tIlt-' micwhiota COJlCf'ntratf'
essential f'lel1lents in available forms ill soil surface layers, (2) tht' lIJicrobial surface covers are lIsually clarb:'r colored than
thf' soil itself and produc(, wanll{'r soils (luring coo] s("aSOlls when soil waleI' is most availahle, (:1) the gelatinous sheaths of
several e:~l1lOhac:terial )?/'lwra common 011 alkaline deserts cUlltaill chelatiug compounds, <l1ll1 (4) conditions that favor
persistent microbial gnmths OJ] soil snrbcf's ,11 so bvor maintenance of larger rx)pulatiollS of ll!icroorgallisllls that fon]]
mycorrhizal and/or rhizosllPath ;Issociations with seed plants. There is c"idellce tllat associat('d animals llIay 1)(' llutritionall)
bClwfited by the enhanced mineral content of forage plants gnlwing in wf'll-dev(·loped (':'anohadcrial C!"llstS.
ABSTH:HT-In
Key Icords; aypto{!.rllnic crusts, lIIineral uptakc. plant !l1ItritiO/l, /lImit grOlrtfl, iIlycorrfli::lle, dcserts, ('y(//w!Hlcferil(
Collema, Microco1cllS.
Dense growths of cyanobacteJia, lichens,
xerophytic algae, mosses, and lIlicrofungi are a
common feature of soil surfaces in semimicl and
arid temperate regions workhvide (FJiedmann
'md Galun 1874, Haq)erand Marble 1988, West
1990). Such soil covers are cormnonlv nlUcll
darker than associated surfaces without such
growths (Fig. 1). Previous work on these Cl}Ttohiotic surface growths (or "clJ1Jtogalllic
crusts" as they arc often c<.Jled) has focused 011
their ahility to "flx" nitrogen in a hiologically
availahle f(mn (MacGregor and Johnson 1971,
Mayland ct a1. 1966, Shields 'md Durrell 18(4)
and to stahilize soil surfaces against water
(Bmth 1941, Fletcher 'md Martill 1948, Fritsch
1922) orwind erosion (MacKenzie ,mel Pearson
19(9). Other studies have shovvn that nitrogen
fixed hy cyanohacteJial components of the (1)1)tobiotic crusts is available to higher plants
(Fuller et a1. 1960, Mavlamj alld MacIntosh
1866, Stewart lfl(7).
The intent of this paper is to assemble existing data aIllI report new data bearing on the
innuence of cyanobactelial-lich assemhlages of
cryptohiota on mineral nutrition of associated
vascular plants.
~
~
PEHTINENT LITETIATUnE
A large literature documents the role of cyanobacteJia, cyanolichens, and free-liVing hacteria (nonsymhiotic) in desert soils (Halper and
Marble 1988, \Vest 1990). Since legulIles amI
other Va.scllhrrphmts that fonn symbiotic, nib."ogenfixing associations 'with baetelia are unCOllnnon
in cold-temperate deserts, their importance as
sources ofbiologically available nitrogen is minimal in such environments (\Vest 1981). Rychert
et ;,J. (1978) concluded that "blue-green algae"lichen C'rusts fix significant amounts of atmosphelic nitrogen in desert soils (they estimate
flxation of 10-100 kg N'ha-1yr- 1 in the Creat
Basin of North Amelica). Available infonnation
suggests that nOll symbiotiC', heterotrophiC nitrogen fixers are responSible for fixation of only Q
kg N'ha \T I in North AmeJican deserts (1\ychelt et a!. lm8, Stevn and Delwiehe lmO).
The input of availahl(: nitrogen in annual precipitation is apparently low, with estirnates running from 4--{i kgha I yr I (West Hl78) to 1-2
kg-lta I )'r- 1 (Sclllesinger 1991). SC'hlesinger
(1 8\)1) notes that available N in dry-fall exceeds
that in rainfall in some areas, but \Vest and
Skujins (1978) argue that since deserts produce
_~Dt'partLl1t'n( dBolany "",I Hani<" ~(';('ll"" B,igh"n, YOlll'g Ullin·"ily, Pn"'(J, L'lalJ ').f(~)2.
- Shn,h S<:i'" K<" 1,a],oralo,-,,- lll!<'nnountaill H"'''''''ch Stat~",. LJ SDA 1"<", "~I S.. 1"' k.·, 7:).) '\ o,ih .')0(1 F:a,t. 1'1''''-'', Utah 1)-1(;1.--;'
.58
(ill
1Volume ,S:)
GREAT BASI;\) :'\,\TUH.-\LlST
,
.
.,'.... .. ..
•
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... , >...
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Fig, J. Contrast lX'twecn natural soil color and the dark-colored cryptobiotic gro\\th on the soil surface. Such surface
groWl hs of cy,lllOhactl'ria, the- hhwk lichen Colll'l!ltl. amI :wrophytic IllOS,9'S are COlllllJOn 011 dt'SPli soils ill the iJltt'fHlOll11tain
\\"(",t of \"orth .\merica. Soil shU\nl is rleycloped frolll am,jellt lacustrine deposits. w('stern lHal!.
rnore dust thall thev receive, N in dust (the
prilll<U) SOUfCt-' ()f 1\ in (lry-hll1) prohahl:' rqxesents a net CXIX)rt fnnn deserts. Df'nitJificatioll
processes are active in deselts and 1ll<l:' c(!ual or
exceed rates
fixation (Skujins amI Kluhck
HJ7B).
It is estimated that \'ascular plallts tah- up
10-1 ,) kg N ha lyr- I in the cold deserts of t1le
Great Basin (\Vest and Skujins 19(7), \Ve can
infer from \\'ork h\. Homm,:\'. et al. (197K) that
al1lllLal uptake of N by vascular plants in the
wartn deserts of the northcm :Nloha\-e is slightly
greater than that reported by \Vest and Sklljins
(1977) for cold deserts, III either case, annual
uptake is greater tllan the com hi ned total of new
nitrogen added hy precipitation and heterotrophic bactetia. Since tbe ,lTllOll1lt of N fhecl hy
syrnhiotic organisms is apparently tIivi~J ill deserts of both the Greal Basin and the nO/them
:\Iohave, the inp"t of fixed I\ hy cyanobaetctialichen crusts is of significance in those desPlts
(Rychert
et al. 107B).
•
The influt'nce of CI:IJtohiotic crusts on available forms ofcsscnti,ll clclll('nls other than N in
or
su rbce soils of deserts lias been documented in
,1 \'<uiety of rcpOlts. Such studies often show that
available V exchangeable K, and Sl1rf~tcC soil
organic matter increase apace \\lth crypto1Jiotic
cover (Anderson et aL 198:2, KleineralHI Harper
1079 • 1977a, 1077h. McKl1i~ht 10BO). Thetrcnd
for clements otlwr than N is apparently re bted,
at h"'ast in pmt, to the tendency of the cryvtobiotic CJ11sts to trap soil fines (silt and day) and to
sequester essential elements in li\-ing cells
(Fletcher and \lartin ]Y4S, Kleiner and IIarper
1979).
Cr~vtohiotic crusts are usually darker than
associated soils in oeselts (Fig, 0. As a result,
soil slllfal'l's cO\'c..Ted lw such Cl11stS ahsorh radiant cneq.,.,l\. better than nearbv. uncl11stecl soils
,Hill afe wanner (Kleiner and Harper 1977b,
Harper alllI \larble 1988). Temperature differences may Iw at least SOC (llarper and f\ifarble
1YKH) and are prohahly greatest in cooler seaSOilS. In tilt: Great Basin, where the hulk of
biol(ll!;icallv
,
. l1sable moisture aCCllll1ulat8s from
winter storms. areas covered bv cvanobaetelialCollcma lichen Cntsts can he e\1Jt'eted to be
~
-
1993J
61
CY;\I\OBACTEHIA A;\"]) CYAI\OLICIIK'\S
signific<mtly wanner t1 tan i llterspersed 1I11crusted soils. Both soil miLTobes and associated
vascular plants (especially shallowly rooted spe-
cies amI seedlings) should experience accelerated spring growth on sites where soil
temperature is elevated hecause of well-developed IT)vtoLiotic growth. Enhanced growth of
seed plants rooted in clyptobiotic CJ1.1StS might
be expected because of more
f~lVorahlc
tcm-
peratures and more fertile soils. Physiologists
have long recognized tll<1t lTlallY physiological
processes have a Qw of 2-3; that is, as temperatures \vithin tllP rangp of easy tolerancp are
increased lOGe, metabolic rates for processes
sHch as enzymatic reactions, ion uptake, and iOll
transpOlt are don hlee! or trip lee! ( ;Iass 19H9).
Algologists amI microl)iologists have documented the natnre of organic secretions from
microorganisms and speculated on their
cco~
logical roles in the organisUl-envirOillnental
complex. Algae are known to secrele p(1)'sacchmides, amino acids, vitamins, growth factors,
steroids, saturated and unsaturated fi.lts, and
other beneficial or toxic compounds of unknown
structure (I ,efevre 19(4). The secretions often
form a gelatinous film around the cells. Among
cy:mobacte,ia, such sheaths are COllltllOll amI
include polys<lcch<uides, organic acids, anlino
aciels, and polypeptides (Llllge 1974). In
aquatic systems, cxtraccilltlar organiC' secretions
playa variety of roles including food for Ilf·terotrophic organisms, che1ating agents that increase availability of essential elcmcnts
(particularly iron and other trace elements),
growth stimulators, toxic compounds that discourage herbivOlY (and are sometimes autotoxic), and compounds that complex with and
inactivate toxic agents (such as copper) in water
(Lefevre 19fi4).
Lange (1974) demonstrated tlmt slteatltmaterials of cyanobacteria indude chelating agents
that permit the organisms to grmv \igorously in
water having a high pH in which several essential clements would othel\vise be available in
such 1m\' alllounts that active growtlt would be
impossible. lIe dem{)nstrated that somc sp(~cies
in each of the follOWing genera secreted enough
natural chelators to produce growth equivalent
to that of the same species in cultures that received artificiqI chclators: Anabaclla, Anacystis,
Lynghya, Aficrocystis, and Nostoc. He also
demonstrated that the natunJ chclators were
water soluble and that tlltrates of cultures in
which chelating species had grown suppOlted
good growtl I of llolldlelatillg species. The latter
species were unable to grow in the same water
if chclating species had not preViously grown in
it. Lange (1976) c()J]c1Ulled that the gelatinous
sheaths of cyanohactf'ria prmide a microenvironment around their cells, where cssentialnutlients can be concelltrated from an
environnlent in which those clements exist at
levels too low to sustain growth. III alkaline
df'Sf'ltS thf' hygroscopic nature of the copious
gelatinous sheaths produced by eyanobaeteria
(aJl(llllany associated algae, hade ria, and fungi)
sllggf'st anothf'r, Jlf'rhaps f'ssf'ntial, n)le for such
extracellular secretions, that of retaining
enough water around cells in dry l)f'liods to
prevpnt If'thal dpsiccation.
A large literature documents the important
role of mvcolThizal associations for mineral nutritional relationships of vasculm' plants (Allen
1991). Allen (1991) concl"ded that "major perturbations almost always reduce the inoculum
denSity" of 1l1ycOlThizal fungi. Bethlenfalvay ct
al. (198.5) determined that trampling of soils by
hoofed grazers (cattle) reduced 1I1ycOlThizal inoculum in crested wheatgrass pastures in Nevada. Koide and Moonev (1987) showed that
IXJcket gopher lmrrowing in othcJ"\visf' Ilndisturlwd se1lJentine herblcmds in coastal California also recItlced ll1\'corrhii',al i IIOCU lu 1Il. PelT\'
et
•
al. (19HB) rf'poltf'cl that sprollting shmbs Inay
maintain a myc(llThizal infection through the
stressful conditions induced bv \\~Idfirp. \Vllllstein and Pratt (l9H}) discussed the developlllf'llt of rhizoshe'lths of Ory::.opsis hYlllc/wides
(R. & S.) Riker (now classified as Stipa
hYllu'/Ioides H. & S.), a deselt grass. Ory::.:opsis
and several other grasses of arid, sandy soils
product' COl1SI)icuous rhiz,oslleatlls c(lnsisting ()f
dpnsf' tangles of root hairs and intermixed heterotrophiC bacteria capable of thing nitrogen
(\Vllllstein f't al. 1979). Unpuhlished data in the
files of the senior author suggest that rhizoshcaths apparentl.yeldHUlce mineralllptake of
Stlj){l hYlllcnoides for several elements.
The foregoing literature survey snggf'sts that
CI)11tohiotic Crtlsts may Significantly alter the
uptake of essential elements by associated desert seed plants. In this paperwp rpport preliminml' results on the effects of cryptobiotic covers
dominated bv
, cvanohacteria and Colle lila on
tissue chemistry of associated seed pl<llltS.
Collcmfl is a black-colored Hcllen in which the
photohiont is the cyanobacterium Nos{oc. Specifically, we will consider the eHects of the
~
•
.
62
GREY!' BASI); l\XITHILIST
'1'.\ 1l1.F ]. Tlw i ntl1JeIlCl' of c\-anob"ctcria I-CIJ/!eIIUl covcr
on various ch,lracteristics of the O~3-('m sllrLltt, 1<1\I-'( of
saud. For comparisoll, the same Ch,II',Il'tcristics for (,olllpa-
rabl(' la~-('rs of nt'arb~- saml b'pt fret' of smfi.lCf' growl h hy
wind action afE' prl'st'llted. 'I'll(' \'ahws for each smfact'
("ondition arc all an'rage of 1-/ S<llllplf'S (ullcdcd at three
dif!i·rent sites ill soutlw<lstt'fll Utah. Two composite samples
Wt'fl' tah'll Oil pach surface conditiun at \Viml \\'histlt'
Campground, San Juan Co lint)'. ,111(112 composite sam\Jles
WCf(' taken from hlo\\' santi aud IIp,,rh,, soiLs stahilizr·( ]A
cr:lltohiotie cover at two locations in Arches ~atiol1<l1 Park.
Grand e(lll1)tv, Utah
Characteristic
BI()\\, sand
Cvanobactcrial-CtJffmw salKI
(0/,)
$-)2,7
79. ]
lkaction (pIll
7,H
Sand
P('rcpnt
.
(oJ(,)
o..'')!
(J.g.3
~itro~f'n
O.OOS
0.021
Calciulll
1.449
:3,71;..),
Copper
0.20
0.21
Iron
S,I
7,S
Magnesiulll
:39.0
.57,0
Mallgancsc
4.6
1.5A
PhospllOrus
'):1 .-,
:....-
.51.S
PotassiUll1
fiq" . -I
i;7.0
h
III
n.:)
O,:}
On.;unit: lIlatkr
Sodillm
Zinc
----
-
---
cryptobiotic cover on soil fprtility, soil temperature in the cool se<L,>on, possible chelation
effects, and colonization of seed plant roots hy
mieroorgamsllls.
METHODS
Soil samples considered ill Tables 1 amI .'3
eonsisted of composite samples of the surface 5
em of the profllc taken at 10-12 randOlIl Iy chosen spots within each of the follmving surfacf,'
conditions: an-'as that supported a well-developed (i.e., >600/c) cover of c)-anohactelia and
the black lichen Col/emrl tenax, and areas onlv
a few meters away where prevailing winds o'r
foot traffic had prevented crust development.
All soil samples considered were collected in
southc<'l,>tcl1l Utah at sites identified in the legends of Tables 1 and 3_
Soil texture was determined using a hy'dnnneter procedure. Soil reaction \vas taken
with a glass electrode on a saturated soil-water
[Volume .5:3
paste. Organic matter \vas estinlated by digestion with 1.0 N potassiulll dichromate. Total soil
nitrogen W,-L') anal)-l'zed bi' the micro-Kjeldahl
procedure. P!JOSp!JOlUS \V<.l'> deterrnined with
the iron-TCA-lIlolvbdate method on a soil extract taken \vith 0.2:'\ acetic acid. Exchangeable
bases were freed [rom the soil with 1.0 N ammonium chloride. Ion concentrations in the extract \vere estimated by atomic absorption. All
soil analvses \vere made in the Soil and Plant
Analysis Laboratory, Department cif Agronomy
and HOlticnltmc, Bligham Young University,
and all anahtical methods were based on those
reeommcndcd by Black et al. 096:5).
Soils for pot trials in the glasshouse were
bulk-collected from the Sand Flats site, Grand
COl111ty, Utah, in January 199] and imillediately
spread in a thin layer on a laboratory floor to
air-dry. Samples from areas with and \vithout
ClyTJtohiotic cover consisted of the surface .5 cm
only. Once dried, soils from each surf~lce t)-Ve
were thoroughly mixed Ondlllling the biotic
cover for that sample set) to ensure a uniti:lnll
potting mixture. ~ 0 fertilizer ,-unenumentswere
added. Subsamples from each surface type were
taken for subsequent analysis of physical and
chemical characteristics. One liter of soil [rom
the sample taken from each surface type was
placed in a drained phL,>tie pot having a top
diameter of 1.5 CI11. Before pots were filled,
IHJles were covered \lith a coarse fiI>erdrainage
•
glass lnesh to preclude loss of soil. Soils from
each surface t}lw \Vcrc replicated 10 times in
indhidual pots. Pots were immediately placed
in a grid on a :vater-tight table in a glasshouse
and watered from the hottom with a 2 ..5-Cl1l
laver of water that was drained off as soon as soil
at the pot s1l1facp was thoroughly wetted by
capillarity. Pots were placed ill a 4 X .5 grid with
gJid intersections 30 em apart'. CI)"11tobiotic and
blow sand soil surface types were alternated in
tIle grid. Six presoaked seeds of Sorghum
!w[cpclIse (L.) Pel's. were plantpd in each pot on
11 February 1991. Pots werp irrigated with t<.lP
water as nepded to maintain nonstressful growing eonditions.
To evaluate thp effects of cvanobacterial
grmvth tllroUghout the rooting z;me, we initiated a second trial simultaneouslv with the foregoing pot trials. In that trial \V~ fmed narrow,
glass-walled planters with 0.9 liter of the same
cr)]Jtobiotic-covered soil. Each planter was 1..5
cm wide, 40 em long, and 30..5CTrl deep and was
divided into two compartments ofefIual size by
CYANOHACTEHlA A:\ID CYA~OUCHEI\S
63
a redwood strip 1.5 X 0.5 X 30.5 em inserted at soil ""ere grown from the same sped lot in the
the midpoint of the planter before adwng soil. saint=> soil and were propagated in the sallie
The glass walls of one oompn.rtment of each glasshuuse at the sam(~ time. These otherwise
planter were covered with aluminum foil to identical (..ouditiolls for growth were marked hy
exdm.le ligll!. Planter,.; were drained and aeratec-l a strong diflerenl.'e in root tempcmture. with
at their hottoms via a pettorated tygon tube (4 puts averaging --16°C and narrow planters
mm in diameter) open to outside air at hoth -2IOC. To determine the eflpe! of differeot
ends. These plallters wert> irrigated and planted rooting zone temperature-son mineral cOInposiwith presoaked SorghulII halepense sc-cd at a tion of Sorghum ahoveground growth, we anamte of6 seeds percomp<utmcnt on 16 Fehnlary lyzed and compareu the chemical eomposition
1991. This trial WiLli replicated 10 times. It was of top growth of pot-grown plants <U1U planternecessarv to water these phUlters on altenmte grown plants (see Hesults).
days with 2.S0-300 ml of water. For convenPlant tissue was ovell-tlrieu at 60°C for 12 hI'
ience, tap water was dnmm and stored in a and then ground in a steel rotary mill using a
plastic bucket io the glasshouse until needed for 40-mesh sieve. Samples were stored until anairri~ation of planters. This water averaged 8lyzed in capped plastic vials. lisS1Ie nitrogen was
12<><: warmer than wilter taken directly from tile determined llsing micru-Kjeldahl procedures.
tap. The cumuillation ofwanner irrigation water Duplicate l.O-g tissue samples from each exand less exposed soil surfal.'C from which water periUlent<.J replication were digested in it 1:5
(.'Ould evaporate resulted ill rout temperatures solution ofconcentrated sulfuric and nitric acid.
for plants gmwn in narrow planters that aver- Content of bioessential clements in the dig:esaged 3-8.5l>C wanner than those of Sorghum
t;lte \V;L'i detennillt~(l llsin~ atomic ahsorption
plants from the sal11~ se~d lot ~rown in the same procedures (Page ct a!' 1982).
soil hut wntert=>d frorn the bottom. Temlx.~ratllrc
The degree of root infection hy vesicular
differences were greatest immediately after irarhuscular mycolThizae and other root symrigation of the pots with eold tap water.
hionts such as nhi:ohium hacteria (associated
After three weeks cyanobactcri::u growth
with rOots of Lllpirllts) or Bacillus hacteria (ascovered tlJe glass walls of planters not covered
sociated with rhizosheaths of Slipa hyrrLeTlOides)
by aluminum t()il. The cyanohacteria obviously
was detennilleu by microscopic examination of
competed with Sorghum roots for essentiallllinroots of randOlnly selected plants gmwing in
erals. Plants growl I ill planters that received
well-developed cyanobacterial-Collenw crust or
light throltghOllt tile rooting zone were smaller,
and their leaves were discolored by reddish pig- on nearby cumparable sites where wind action
ments in eontmst to adjacent plants grown un- or animal tramc (sometimes <u-eas trampled by
der identical <.:onditiom except that light was pt:ople) had precluded growth o[ cryptobiota.
excluded from the rooting zone. A<:, a conse- \O\'ithin c<leh soil su rface type, plants were ranquence, glass walls of all planter <_'ompartments domly selected using the <juarter method (Cotwere t:overed with aluminum foil 3 weeks after tam 'lIld Curtis HJ50). Plaots 'vere mllected
planting. The foil remained ill place until phmt during early flowering (early May lfl92) in
top growth was harvested foranalysison 29 April \ViL'\hington and Grand cuunties, Utah. Bromlls
1991. Plants gmwn in planter compartments teclOrtWl L., CnJptantha plerocanJa (Ton)
previously illuminated in the rooting zone Greene, Cryptnntlw cmssiw?"l'nln (T. & G.)
quickly regained. nor1l1alleaf color and became Creene, Festllca octoflora \ValteT, LlIpi/HIS
indistinguishable in siw from adjacent plants 1-msiUfl.S Pursh, and Plrmtof!,o patagrmica Jacq.
bJTOwn in compartments with toil-covered root- were <...'Ullected in \Va."hington County.
ing zones. Chemical analyses of pr.mt tissue Coleof!,yne ramosissima Torr., .\. .fentzelia afhifrom these trials demonstrated that tissue awlis Doug. ex HfX)k., Stipa hymel1oides, aml
chemistry from plants that had their rooling StreptaJlt/lclla lot1gim!\triR (\Vats.) Ryclh. were
zone exposed to light for 3 weeks did not differ collected in Grand County
Using a shovel, we lifted the root ~"ystcms
significantly.lc)r any element considered from
that of plants that had not received light at any from the sandy soih in a block 'md then f",~d
them froUl associated sand by hand. Plant tops
time in the rooting zone.
Plants in narrow planters and those in pots were i1l11nediatelyexciserland roots were placed
of bottoUl-inigated, Lyanohacterial-enriched in 75% elhanol in labeled, screw-cap ~Iass
64
A
N
U
0.
6'h
6
PC1
6
••
•
[Volul11e
GREAT BASI'! NATURALIST
•
o
6
0
0
B
N
U
0.
.Fe
• N
m
Plant nomenclature f()llmvs \\7eI5h et a1.
(l9H7). Lichen nomenclature follows EGan
(1987). Statistical significance of differences 1"Whveell group means \Va.<; determined using an
unpaired t-test model (Snedecor and Cochran
19671. Significance of treatment effects in Tahle
5 was dctennined using analysis of variance
(ANOVA) with species treateel as blocks. Percentage data were arcsine transf(ml1ed prior to
analysis by tlie GLM procedure of tlie SAS
statistical package.
Centered, standardized principal components analysis (PCA) was used to analyze differences among samples colleeted from clllsted
soils and unclllsted soils (Pielou 1984). Various
soil chemical and physical parameters were
used in tllis analysis, which \vas comlucted using
the Statgraphics package .
.K
RESULTS
Zn
Ca
PC1
Fig:, 2. A: plot of the first two components of soil samples
from l'fyptnhiotically (Ttlstpd ,mel tlllcrusted surfac/:'s at
thwl:' diffel"t-'JJt locations {st'(, Tahle J\, Sampl<:>.s from Arch~s
:'\iational Park are indicat<:'d lw triangles
<lnd diarllnmk
•
s<lmplt's from \\'ind \Vhistll:' Calnpgr011nd are represented
0: drclPs. 13: plot of weighb for i ntlividllal parameters IIsed
to obtain the first hvo ('ompOllents showll in Fi~lm:' 2A (.S('C
•
•
te'd for c\planation).
sample jars. All root samples were taken from
the surface 1.5 em of soiL
In the laboratory, samples were cleared and
stained plior to microscopic evaluation of the
amount of colonization on roots. Clearing and
staining were accomplished using techniques
described by Koske and Gemma (1989). Using
tbe adapted grid line-intersect metbod of Ambler and Young (1977) as discussed in Giovannetti and Mosse (.1980), we reported degree of
mycorrhizal infection per specimen as the percentage of root length having developed arhuscules or vesicles. The percentage of root length
having nodules or rhizosheaths was estimated
ocularlv.
,
The effed of cl:)-ptobiotic grov.,th on surface
soil chemistI)' and texture is particularly impressive for such variables as organic matter, soil N,
exchangeable Mn, and "a",ulable" P (Table 1).
Exchangeable Ca W,lS also much higher on average in soils stabilized by cy<.Ulob,lderi<.u-lich
surface gro\\th. As in other studies (Fletcher
anel Martin [948, Kleiner and Harper 1972,
1977a, 1977h). our results show that soil silt and
clay are much greater in soils stabilized by cryptohiotic grcJ\\th. The response ofCa, Mn, and P
may be related to textural differences alone
(BI~ck [968), but the increase in soil organic
matter and N is probably directly relateel to the
presence of cl}Ttobiota.
Principal components analysis of the basic
data on which Table 1 is based showed marked
differences between cnlsted and uncnlsted
soils, even though three separate areas (hvo in
Arches .\\ltional Park and one at 'Vind 'Vhistle
Calnpground) were studied. The Hrst plincipal
component clearly separated the cnIsted soils of
the most intensively sampled Arches site from
the corresponding uncrllsted soils samples (Fig.
2A). Clllsted and unclllsted soils of the other
hvo sites wefe also separated by the first component. Clear differences among sites were evident in the separation that oc'Curred on the
second principal cOlnponent (Fig. 2A). The percentages of variance in the data accounted for
by PCl anel PC2 were 48% and 22%, respectivelv.
1993J
65
CVAM)BAerEHIA AND CVAN()UCIIENS
TAAU: 2. 'TiSSIIP f'lcmenla! wntcnl of plan Is of FrslIIC(I octoflonJ (il dilllillllli\'t> <lllllual) anel ,\kllt::.eUa lIlultiflora hI
short-li\'etll~n~lIniilllll-'rh) Kfl"""n On blo\\' sand ilnd lIearby sanu stabilizeu hy ('yanoh;ldcri;lI·C(Jllr~/l1ll crllsts. The F(~~1f1m
s!llnples Wcr(' taken at 'Vim) Whistlt> Campgrulllul in San Juall COllllt.\: Utah; tht.· MCII/:.difl sa.lllpl(~s \\'t're taken ill
C...ollrthous~ Wash DwX'S, Grand ClIllllty. Utah. All data ilrl" from Belnap and Harper (in Tl·\"iew). All tisSllf' t'oncentratinllS
are exp(e.'t~(,.·d as ammmt Ix'r unit dry weight of a}Xl\l'h'TOIll KI\-:wwth ami athK,lwd root tissut' bTl/sill-Ad fret-' ()f .~and. Smnple
size W'dS 5 (or each mean.
~
-~-.
Festuca ocloflora
Soil slIIfll(:e mnJiliull
Elerntont
N (%)
r
(%)
K (%)
C.(%I
Mg(%)
ell (ppm)
Fe (pplIl)
Mil (ppm)
Na (ppm)
Zn(pptn)
Bluw
Sigll.
lichcn co,\'cr
..
~al1d
dili<.'l'.
2.2.5
0.25
1.D.,)
0.14
1.64
0..'52
0.13
lOA
•
...
•
...
14\).4
•
NS
l.H8
0.65
(US
11.0
300.3
fiO.3
61.5
·13.0
·M..~,., »J:Ilir.l"l,,~~·ollfK-"'Oltat p
~
Soil surfac(' <:ouJifion
Cnl,lK II Jacte rial
_.
_
.
Ment.ulia multiflora
74.0
.SRS
:J.1.0
••
NS
NS
NS
._..
CVillloh,tderia!l
lichen lu\,cr
U!ow
Si~ll.
sand
difkr.
2.6]
0.20
3.04
2.50
0.:,3
8.6
fi39.8
98.2
77:2
22.0
2.18
0.24
2.fi7
-••
••
NS"
15.17
0.2.3
NS
9.0
465.4
82.4
NS
•
•
NS
63.4
•
20.0
~S
< .tL'>.
"Mu,,~ "'J:."m<':Int~ <liff"I\·"t It! I'
< Ill.
... """,,,~ ,;~"ifi(u"t~ cliffi,,,,,,t:tt,, < OOt
~I""l"~ U(~ <i~"ili<"'"tt.- clilr""'nL
Plotting the component weights (Fig. 2B)
yields an explanation for the separation of
Cll1Sted and uncrusted soils. The first component
most dearly represents the cliHeren(;cs between
llncl1Isted and crusted soils. Uncrusted soils
have higher values on this axis, which means
they have higher pH "nd S:lJId content (positivc
weights) and lower Ca, Mn, P. Mg. N, and K
(negativc weights). Iron and Zn tellded to he
higher in uncnlsted suils but were not a'i importallt in sep<l.rating points on the Hrst axis. The
seeond component most clearly represents sitespedfte differences. One Arches site (triant;les
in Fig. 2A) had higher N, K. "nd Fe (positively
weighted) and lower P, Mg. and sand (ne~atively
weighted) than the other two sites (Fig. 2B).
The prinCipal ("'omponents analysis shows that
despite some site-specific differences, crl1~ted
soils are generally higher in some essential minerals (N, K. P, Ca, M~, Mn) than are ullcmsted
soils. Site diHerences were "uso dearly delineated in the analyses.
Table 2 clearly shows that c.yptohiotic enlSts
do have asignifiwnt influence on tissue content
ofseveral bioessential elements in both Festuca
octoflora and Ment=elia 1I111ltiflvm (Nolt.) Gray.
Since Belnap and Halper (in re"ew) show that
soil textllral difTerenc'Cs are small «10% difference in pen..'Cntage sand) between blow sand
and adjacent sands stabilized by surface growth
of cryptobiota, the tissue content differences
seen in Table 2 would seem to be strongly influenced hy mi<.:roorganisms on the soil surface.
Tissue content of both seed plants was signific"ntly greater for N. Mg, and Fe when plants
were rooted in cyanobactelial-rich crusts. Although not "ul diflerences were statistically signifjC<Ult. 9 of 1.0 elements were present in
~rcater amounts in tissue of Festuca plants
grown on eryptohiotic,~lystabilized surbc'Cs; 8
of 10 elements were present in greater amounts
in tissue of A.fcllt=.elia plants grov.rn on the cryptobiotic surfaces. Finally, thc data sll~est possible competition between cryptobiota and seed
plants lor P and Mn. We also note that the
responses of Festuca and Alcnt::.elia were
unalike in respect to J' and Mn upt"ke.
Glasshouse trials demonstrate the soil "fertilization" effect of the eyanob"cterial-Collel1la
cover for growth of Sorghum (Jltbles .3. 4).
Differences observed between chemistry of
cymlObacteria-free ,Old cyal\obacterial-Collemnc'()Vered soih (Tahle 3) are smalL The cryptobiotic-covered soil b,] slightly more N, P, K, "nd
N". Thc soil Iree of cryptobiotic growth aver"!led somewh"t higher in ea and Fe than the
samples supportin~ cryptobiotic wowth.
66
[VOhlTll(> .53
GREAT BASIN NAI'UR\I,lST
T\uL1", :3. Cllara('h'ristics of C\'<lllohaC'tcrial-C()//clllasl<lbiuzed sllrfact' (0--5 un depth! s'lnds a n<l sands (rmll sallIe
(lepth zow:' onl)' <I few dill aW<I;.' tll,lt \\'l'n" not culonizcd hy
C'r)vtohiota. Thl-' lattf'f sauds had Ix'("n llllstahilized by hulllall tmmpling for at \('ast a (lecade, Samples ,Iff' [i'OIll Saud
Fbts, Cram! Count\', Utah. V"I11('s fur (',Itiom ,In' amounts
cxchange,lbk ill] ,0.\1 .:--JH~C1. These are the soils Oll \\'hicIJ
Sorglwl/llw{(,pcllsl' tisslle ('onsidt'I"f'd ill T,lhlc 4 \\'as grown.
~--~
-
Surbce couditi()ll
Soil dWfilCt!'listic
Fr('(' of
IIC<l\\
cryptobiotic
growth
('y.111 oJ Jacte'rial-
Te\ tnrc l '7r s ,Ill d 1
Hcaelion (pll)
7.4
(UJS
(:a
(Pillll)
1.00
0,038
2J)70
ell
(ppm)
(), -1-
F(~
ipplll'i
5
7k
:1.1
:J,-l-
:jl)
-1-7
SJ
H']
()rganic matter
'.
!\(t;(,J
\Ig (ppml
.\'In (pplll]
I' (ppm, av<tihble)
K ,-ppm)
"\<1 ipplll)
Zn ippm)
covcr
61
, ..J
('Ie.;'
CO!!ellI(f
O.1H]
] .S-l-,S
n.2
,
-Q
, 'J
crust-free soils on illfection of roots bv rhizosymbionts slim\-' that 6 of 10 species e\idenced
infection lw root svmbionts (Tahle .5). Of those
species wbose roots showed some inf<x.:tioll, 4 of
6 were annuals, and all infected alllll1<lls were
colonized bv, vesicular arhuscular nlvcorrhizae
,
(VA\Ii. The dL'gree of infection was ahva:"s
greater for plants grown in cyaJlobacterial~
Col!enul enlsted soil. Seedlings of the shrnl>
ColeoglJllc m IIwsissil1l{/ snppOited heavier VAl,,1
infectioll than associated annuals, and the rplative amount of root colonized bv the root symbiont was over three tinles' grpatcr ,,:hen
seedlings (,lllerged [rom cll.1sted soils. Roots of
the perennial grass Sti}Jfl hymelloides always
developed rltizosheaths on hoth t)]1es of surfuce, bllt tIle degree ()f sheath developmcnt \vas
greatest (m cnisted snrfaees (Tclble 5). The overall cfh,ct of cJ1Jsted soils on root illf(~ction bv
symbionts \vas positin: and statistically significant (hble ,5),
111
.S
.9
D1SCliSSIO'i
Sample Sut'
Civen the srnall physical and chemical differenc('s hetween soils (Table 3), the oftcn significant differences in Sorghum tissuc chemistry
when grown on those soils (Table 4) were llIlexpected. )Jitrogen and Zn were taken up in
significantly greater amounts on the eyanohacteriaJ-Collelllfl-enriched soiL prodlll'ing
(wer:3..5 tiIllCS more top grm\th than soils with
no cr;ptobiotie growth (Fig. 3). The elements
Ca, l~ Mn, and Na were present in signiHcantly
greater concentrations in tissue of plants grown
in the cryptobiotic-free soil. These data suggest
that (1 ) I\ or Zn (probably the f()fJner) is limiting
for plant growth in the test soil and (2) there is
\igorons competition between the cyanobacteria and Sorghum for Ca, E .MIl, and Na.
It also seems clear that nutlient uptake by
Sorglwm was strongly aH(x~tcd by tenll)t'ratllre
in the root zone (Table 4), Nitrogen, C,l, !\lg, Cu,
and Na \\-'Cre taken up in significantly larger
amounts from the evanobacterial-CollcHw
soil
,
at the higher temperature. Increased telnperatllre seemed to intensi~v competition between
the cyanohaetelia and Sorghum for P, Fe, and
Mn,
Preliminary data coneeming the influence of
eV<lnobacteIial-C'ol!eIlUl CIllStS and associated
The results presented prO\,ide strong support for the h!1)othesis that cr)ptobiotic soil
surface em'ers (at least those rich in cvanobactelia) have Significant effects on uptakc' ofbioessential elements by associated seed plants. rn
this study we have considered only species (or
devclopmental stages) with a major pOItion o[
their root svstem distributed in the snrbce 5 em
of soil. The cr:rtohiotic snrf~lces appear to consistently enhance uptake of some elements (e .g.,
N, K, Ca, :\-lg, anrl Zn), and to at least occasionally reduce uptake of other essential clerncnts
such as P, Fe, ~ln, and :\'a (Tahles 2, 41. Tllosc
effects are apparclltly pmtially explained hy enrichlnellt of soils (increased "availabilitv" of essential dements) bv cvanobacterial-C:ollelllfl
crnsts (Tahle 1,3), 11}: elc~'ati()n of soil teInpCfature during cool seasons when moisture is rnost
likely to he readily available {(n- plant growth,
and by greater likelihood of root colonization by
mycorrhizal
fungi
at
.
, and other root symbionts
.
sites that are stable enough to support welldeveloped cryptobiotic cnlsts, Onr preliminary
reslilts also suggest that cyanol)(lcterial-Collelllfl
crusts Illav result in an enhanced availabilitv of
certain elernents through accelerated df'cOl~po­
sition or production of chclating compounds
(i.e., ~-ln and P in Tahle I; eu, N, !\lg, and Zn in
Table 4). Taken together, the data in Tables :3
and 4 sllg,t;est that the enhanced uptake of ~ hy
.
19931
6i
(;"A;'V()RACTEHIA AND CY:\NOLlCHE:\IS
T,\1I1 ~.; -i. Tissue chemistr: of ahovt'v;rulllu] g;mwtlt uf Sorghllllllwkpf'11Wl grown in c)'~lllohadf'ri:lI-C"lIel1la free S~llld Hl"
sand hc'ad'" con'red (0\'('1" ~(J':{;) b\" (Y<llluhaderia ami COI/CIlIiI ill pots v.,eHcu from tht> hottom. AI.~() Sh(JI.\'1l is tiS51lt'
dlt'lllbiry ,;r Sor;f.lwlIl ~nl\\-ll i •• tll(' ~:1I11~ c)mlObaderial-CoIlPlIUl-slahili'lf'd .<i;lIlIl ht'ld in decp, narrow rectaugular planters.
A\'Crdgcs fuUO\\'('d by the same' !QI,\/{·n:a."f' letter do Hot differ signifkantl).' (p < .0.'5).
Soil and polliJ)~ comlitiolls
Tissue (;ontent of
eva noh:U:h-'riaJ- f fee
C\~lIloLJildcrialsoil
C\,lnoba(1erial soil
ill lXlls
soi I in poLs
in 1l;lrrOW plankr..
-COllt'cntration (% dry \\t.)
N
OJ;7 a
(l,7H b
!.41c
P
0.12 h
0.09
K
0.1·') a
..... ,
_,'::"CJ ,
2.4la
2.27 a
ea
0..'')7 a
0.44 h
0.64 a
0.J5 a
0.14 a
0.26 h
., .,
l'
COIl(:cnlralion (ppm c1J}'\\1.) -
ell
4.N a
5.5 a
8.s h
Fe
}ojfi.:l it
51.H a
2(.6 b
Mn
64.-1 a
53.0 h
47.1 c
"
Zn
11·f.:1 a
32.6 b
50.7 c
15.7 a
22.6 b
23.9 h
1.3 a
4.8 b
10
10
"'
-IG
-lG
-21
Sorll;lllllll ),;t-I(Vpot
(g-lop growth only)
No. of l"('plicr,tions
Av~.
rootilll; Wile
temp (C)
plants grown on crusted soils must include a
considerahle amount of N fixed simultaneously
by ~yanobaeteria in the culture or N rele'lsed hy
microorganisms deL'Omposing the tissue of cyanohacteria grown during the experiment.
Orihrinal differences in soil
were too small to
aC(.'Ol1nt for tlw large rliflerenCts ObSCIVCd in
plant uptake in the two cnltures.
Other studies have shown results similar to
mosi<;sima (Rosaceae) grown on weB-developed
cyanol>acterial-CnllellU1. crusts and on emnparahIe soils without sud} enlsts. Her data sl10w that
average plant sii'e
both species W<.l.'i signitlcalltl)' larger on enlsted soils, and tissue of both
species (xmtained Significantly more ,Ca, Mg,
and Cu per unit dry weight when F;mwn Oll
or
cryptobiohc surfa<.:t::s. Belnap also has unpublished leaf ehemistlY data for adult shruhs of
those rep<llted here. Marble (1990) demon- Coleugyne ral1wsi~sinUl and the long-livec..l,
strated that scalrin~ the surface 1.0 em ofc-yano- woouy-routed h(-:rh LepldiuUl I1wulanuUl var.
bacteriaJ·GolLemlJ cmst around rosettes of jOlles;; (Rydb.) C. L. Hitchc. As one might have
LepidiwrI numtanwn var. montallwn Nutl. two predicted, adult plants of these species showeJ
months prior to Howeling signifkantly reduced no enhancement of essential mineral uptake
ahovegr01md plant weight and tissue content of while growing on cyanobacterial-rich cnlsts.
K, Na, and ell at flowering time. Several other The vast majority of their feeocr roots lie well
elements (Ca, M~, Fe, Mn, and Zn) were also below thuse portions of the soil profile that are
lower ill tissue of plants around which the cryp- influcnceu by cryptohiotie Cl1Ists.
tobiotic CllJst had heen removed, hut those difAs seen in Table 4, Sorghum growth was
severely limited 011 soils free of ()'anobac(crial~
ferenccs were not statistically signifieant (p >
.(5). J. Belnap (unpublished) has ,malyzerl plant Colle/)~I inoculum (Fig. 3). Nitm?;en seemed
tissue for the annual Streptantludln lotlf!,i-rostris inadequate in sm:h soils to support healthy
(Bmssicaceae) and seedlin~s of CnIP.ngyne m- growth of Sorghum. In faL't:. growth \-V'd$ so minimal
68
[Volume .5:3
GREAT BASI" KATURALIST
.3
•
•
\
•
•
•
•
,
••
•
•
•
,"
,
.
,
••
,
,
. ',-,.,:~~~"
'~
•
•
:
"'j
,
•
•
.
'
"
..
""'-.'
."
" ,
. ,. ..
,
-
•
,
,
'
•
.,
.'
•
,
.
• •
· I.
•
•
•
•
r
.•
,
•
Fig. :3. Sorghum Iw!ef!cllse plants after 60 day.~ of growth OIl a soil mixturf' cOllsisting of thE" surface .5 em of a sand
colonized by a IW<lYY gnJ\\ih of cyanobactelia and Collelilo tenax (RJ and tlw ,~aJne depth horizon from a llearh~' site kept
free of sllch growth
hy
f(Xlt traffic (Ll, See T,lble:3 for characteristics of tlw two sous.
e
.
in those soils that: the species would probabl:'
never have flowered and set seed on that: substrate. \Vhen Sorghum was gro\vl1 on a soil
enriched hv
inclusion of the c.vanobacterial•
•
Collema inoculum, growth was much greater
even though only ~ and Zn occurred in significantly greater concentrations in the tissue (i.e.,
all other essential elements occurred in higher
concentration in phmts groyvn on clJvtobiotafree soil). These results suggest that even
though ey,mobacterial-rieh crusts sometimes
enhmlce uptake of several essential elements,
plant growth (at least Sorghum growth) W"lS
limited by N (and perhaps Zn) only on the soil
considered.
Evidence does exist that the cryptobiotic surface layers (especially those rich in cyanobacteria and/or cvanolichens) have a heneficial
"
influence on seedling establishment under field
conditions. Harper and Marble (1988) summarize the results of an experimental seechng of
five species onto plots dominated by cyanobactelia and the lichen Colle11lG. At time of seeding,
ronghly half of 83 plots were randomly chosen
for a treatment in which the surface 1.0 em of
cl;vtobiotic Cll1St '\vas scalped away. Each species WtL'; seeded on 10-92 r<mdomlychosen plots
through a template at .32 locations per 1.0-m1
plot. After the first gro\'\ing season four of the
five species had more seedlings on plots where
the cl)ptohiotic Cll1st was left intact; in total
there were slightly over three times as many
seedlings on the average cmsted plot as on the
average scalped plot. After three years a larger
percentage of the seedlings survived on crusted
than on scalped plots for a1l five species tested.
In Kevada. Eckert et a1. (1986) planted seeds
ofsix species on three types ofsurfaces: (1) those
covered by a sparse plant litter cover and heneath a shrub canopy. (2) polygonal patterned
Slllfaces covered by a \ig;orous grov.th of cr;ptogamic cover, and (3) polygonal pattenled surfacE'S with little cryptogamic cover and in
interspaces between shlllbs as was surface type
2. Five of the six species tested established 'LS
well on the type 2 surface as on other surface
types, or even better on t;pe 2 surfaces; the
other species established best on type.3 surfaces
1993]
69
CYANOBACTEHIA Ar\D C;YAN()!,IC:IIENS
T\BLE S. PCfCl'Iltap;e of" the root kn~tll COlolli/.e(l b.v rhizosyJllbiulltS Oil cyanobacterial crusted or comparahle soils
without a biotic CfUSt. Hoots of fln' randomly chosen plants wefe l'x<lmilled per sj)('cies ami soil surfacf' l~lIlditi()ll. The
effi.·ct or cyanobacterial crusts (treatment) on HlllOllllt of ('o]ollizati011 of routs !J\" rhizosyillhiollts is Siplific-dllt1y positiw'
(F-\~d1\(' for Al'\O\'A ==" 7.D4.p < .OJ, dJ. = ] 1. F-vahH' for specit's cf[Pc!SW,LS 0'.:26 (p < ,01, d./". = 5).1'!rmfago patagoninl
was omitted fro!ll the lattt'f <lnalvsis.
~-
Associate 1Ilicrolw
----
'\10 biotic nllsl
CV<llloha{'tt'rial ('nlst
----
th/!:o perC("llt of rnot length colonized
Hnmllls lectorlll11
,
VA
IlI\TOf.
1
Colf'0I!.Yllc ralllosissillW-
\ 'A
Jll\cot".
Fest1lca ()cfll[lora
VA
lllH·or.
,J
.5
Colorado Plateau
T
1
\Vashingtotl COllllt~
"
4
22
:34
'\10 s<lJ11plf-'
1:3
Lllpinlls jJusilflls
Rhi::,o!JiulIl
Plantago }Ja(agonica
VA
Stipa !lyme/wides
Ill\Tor.
Hhizusheaths 3
4fl (all weak)
100
(()(}[j,
,
slrolla)
"Hoob "r II", I(~]""i"g ']"'C'''' \I"'rt' 'l"di,'<1 Ionl nn llIH'orrloi"K' "n'" "h""T(',) C'''!/IJtrilltl", l'/cn~YII,,!,a. C'VI'/aIP/IUi cmwisqlfll". ,\l""f~dill "I!,;rwdi.<', and
Stl"I'f,/{wl/rril" IUIII!.U",\'1 ,'is, .-\11 of tlws.. "1"-"' 'i," "n' ")(1 III als.
,'\",,;,," lar "rl "",-"I" r' n1\1'In] ,i /,",
.
:: III h- ",(., III n~., "n.' "'~ 11'<'" I ,nl"lIt "'K']OC"' Wt'r...."", "i,,," 1 f,,,· (hi, 'pr'(·k-,.
'Hh iz, ,,<I\('al),.' an' (~"N' la"g] ("' "f r<~,1 I,,,ir,. l'.. II, "1',, 1>",-;1111.\' 1" ,",,,,,/xll-1 ikt· 1"oct,'ril Ill' ""1'"1,],, "f" fh"li",,- :",d "dl""r.." f '" ,,,) !<,,,in, i\\ ',,11,1<" 11 a",] Pr"ll I~J" I '.
" , ' ,
and did poorly on type 2 surf~{cps. Lesica and
Shelly (1 fJfJ2) reported that cryptogamic soil sur~
face cover appeared to increase sunival of established plants of Arahi.') feclt/ufa Rollins
(Brassicaceaf';) in Montana.
The forpgoing reports suggest that establishment and survival of seed plants native to
arid lands may often be enhanced by CI}lJtobiotic cover on soil surfaces. As Harper amI Marble (1988) show, several sciL'ntists have
successfully used inocula of cyanobacteJia to
increw·;e establishment ,1Od growth of aglicllltural crops in various parts of the world. Accordingly, ohservations of positive interactions
bet\veellcyanobad{>rial-lich C111stS and seedling
establishment and growth in natural arid land
environments are not surprising.
Although the influencp of cyanobactcrialrich soil Clllsts on essential llIinpral uptakp hy
associated sced plants appeared to be strongly
beneficial for N onh~ there is reason to helieve
that enhanced tissue content of N, Ca, Mg, N a,
and P may be beneflcial to 'L'isociateu herbivorous and granivorolls animals. Robbins (I9H3)
notes that increased dietary protein consistently
hastens growth and onset of reproductive maturity in herbivorous
animals. Cyanobacterial
crusts consistently incrcaseu protein content of
associateu shallow-moteu seed plants and seedlings of deeper-rooted plants in this study (TahIes 2, 4; Belnap personal communication).
.
Amnann (196.5), AUlllann and Enl1en (196.5),
Belovsky (1981), and Robbins (19&,) suggest
that sodium in plant tissues is often inadequate
to maintain healthy
herhivores. Robbins's
•
(19H:3) rt'\,iew of dietary sodium requirements
for animals suggested that diets \\-ith less than
0500 ppm sodiu m will eventually result in poor
growth or death of anim..Js. \Ve note that cyanobacterial crusts always enhanced phmt tissue
content of Na in this study (Tables 2, 4). In om
study, however, even plants grown on crusts did
not ('ontain the recormnended minimum content or Na. Thus, animals must resort to local
"mineral licks" to obtain aue(luate Na. Such licks
lllay he widely spaccd on sandy uplands such as
thosf-' sampled fiJI' this report. Small mammals
such as the granivorolls lwteromyid rodents
common Oll deserts considered here mav he
especially dependent on Na in plant tissue, ~ince
they• defend slllall territories that would rarely•
include a lick where supplementar)' minerals
coulll he acquired. III sl1cll cases, increased tissue content of Na in plants grmving on cyanobactelial-lich surface crusts lTlav
be of critical
•
importance to associated heteromyid rodents.
Hobbins (1 Y83) considered that "calcium deflciencies arc prohahly the major mincn.J prohlem encountered in captive wildlife." He noted
that Ca and P arc major eonstitnents of tIl('
vertehrate skeletal svstem. In lllatllre anilnals,
90% of ea and 809{.: of P occur in bone, which
70
[Volume 53
GREAT BASI'" N.'TlJRALlST
has a Ca:P ratio of about 2; 1. Since these elements are so intricately associated in bone, they
arc often discussed together. Birds use Ca not
onlyin bone bnt alsoin eggshells, which are 98%
CaCo.1 and less than 1% P. Osteoporosis is re-
lated to deficiencies in ea and/or P in the diet
or to major imbalances in their presence in the
food base. Osteoporosis has been reported for
free-ranging carnivores in Alaska, for reindeer
on lichen-dominated ranges, and for the desert
tortoise, a herbivore, from the wann deserts of
southwestern Utah (Jarchow 1987, Robbins
1983). Carnivores may be especially prone to
osteoporosis since flesh contains little CalcilllTI.
Osteoporosis in the desert tortoise is surprising;
Jarchow (1987) considered the disease to he·a
principal cause of death for the tortoise in Utah.
He found the onset ofosteoporosis to be premature and pathogenic in the animals examined.
No disease could be shO\vn to be associated \\-1th
osteoporosis; thus Jarchow (1987) concluded
that the condition was caused by
, dietarv
, deficiencies. Since the principal food plants taken
by the tortoise in southwestelll Utah (Hansen et
a!. 1976) do not appear to hc deficient in Ca
(Jarchow 1984), the limiting element is probably
P Jarchow's (1984) and our 0\<71 data (Tables 2,
4) both show less P in plant tissue than is considered necessary by Robbins (1983).
Since growth on cryptobiotic crusts has been
observed to increa.<;;e plant tissue content ofP in
Festuca octoflora (Table 2), Coleagyne ranwsi,sima seedlings, Lepidium montanum var.jonesii
(Belnap personal communication), and L. rrwntanum var. nwntantun (Marhle 1990), and to
have no effect on tissue P content in Streptanthella longirostns (Belnap personal communication), it seems possible that cryptobiotic crusts
could affect dietaIV
, intake of P by
, the desert
tortoise. Since our data show that P is also occasionally lower in plants growing on cyanobacterial crusts (e.g., Mentzelia in Table 2 and
Sorghum in Table 4), more research is needed
to detemline whether widespread coverage of
cryptobiotic crusts would increase or decrease
available P in the diet of the tortoise. Inasmuch
as this species is formally listed as eudangered
and does appear to be susceptible to
osteoporosis in nature, it is important that the
influence of cryptobiotic cnlsts on nutritive
quality of tOltoise food plants be better understood. Cvanobactericu-rich crusts are known to
occur i~ southwestern Utall in habitats frequented by the tortoise (Brotherson and
Masslich 1985), <md their importance in those
environments is also known to have been severely depleted by uses imposed by European
man (Anderson et al.1982, Callison et al.19&5).
Restored vigor of those cnlsts may improve dietary quality for desert tortoises.
Although Hobbins (1983) concluded that Mg
rarely poses a dietary problem for herbivores,
Gmnes et al. (1970) and Fairhoum and
Batchelder (1980) suggest that less than 0.25%
Mg in the forage base puts nnninant .animals at
risk for gnL<;s tetany, a nutritional disease resulting in vasodilation, hyperinitability, and muscle
damage, and possibly culminating in paralysis
and death. Magnesium is an essential element
for proper bone and tooth fonnation and is an
import<mt enZ)11le activator for all animals. Ahsorption of Mg by the digestive organs is apparently inhibited by high levels of Nand K in the
forage; thus, grdSs tetany is most often observed
when animals are feeding on lush spring grmvth
of grasses. We note that Hansen ct al. (1976)
found that annual grasses make up 68% of the
desert tOltoise's diet in southwestern Utah. Our
data show that cryptohiotic crusts consistently
enhanced Mg content of tissue of associated
plants (Tahles 2. 4). We snggest that the influence ofcryptobioticcrusts on Ylgin plants eaten
by
, the desert tortoise merits fUlther attention.
ACKNOWLEDGMENTS
This work wa..<; partially supported bv a sub•
•
contract from the Shrub Sciences Laboratory,
Intennountain Research Station, U.S. Forest
Service at Provo, Utah. The contract was funded
by the
ArmyCorps of Engineers , Construction Engineering Laboratory, Champaign, Illinois. \Ve thank J. Belnap for permitting us to
review unpublished data from her files. The
PCA analyses presented in Figure 2 were perfanned by Jeffrey Johansen, John Carroll University, University Heights, Ohio.
•
u.s.
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