Trap architecture in carnivorous Utricularia (Lentibulariaceae)
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Transcript of Trap architecture in carnivorous Utricularia (Lentibulariaceae)
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0367-2530/$ - se
doi:10.1016/j.flo
�CorrespondE-mail addr
1Present add
Lehrstuhl fur B
Universitat Wu
Germany.
Flora 201 (2006) 597–605
www.elsevier.de/flora
Trap architecture in carnivorous Utricularia (Lentibulariaceae)
Kerstin Reifenratha,1, Inge Theisena, Jan Schnitzlera, Stefan Porembskib,Wilhelm Barthlotta,�
aNees-Institut fur Biodiversitat der Pflanzen, Universitat Bonn, Meckenheimer Allee 170, D-53115 Bonn, GermanybInstitut fur Biowissenschaften, Allgemeine und Spezielle Botanik, Universitat Rostock, Wismarsche Str. 8, D-18051 Rostock,
Germany
Received 17 October 2005; accepted 22 December 2005
Abstract
Within carnivorous plants, the bladderworts (Utricularia) possess the most complicated traps whose mechanisms arenot yet completely understood. For the first time, a representative survey of different traps from both subgenera(Utricularia and Polypompholyx) is presented.
Based on scanning- and transmission electron microscopy, traps of 14 species of Utricularia (out of 215 species)representing 11 sections (out of 35 sections) and including all life forms (aquatic, epiphytic, and terrestrial) wereinvestigated. Additionally, it was tested whether life forms correlate with trapping mechanisms. Most morphologicaland anatomical features of the traps vary considerably between the different life forms, e.g. position of trap and trapentrance as well as form and position of trap appendages. Morphological data support the basal position of subgenusPolypompholyx within the genus. Some characteristics of the traps of terrestrial Utricularia multifida (subgenusPolypompholyx) differ remarkably from traps of the other species, e.g. trap-door anatomy and trap walls. This mightbe an indication for a primordial (non-suction) trapping mechanism in the former species, similar to that of the eel-traps of the closely related genus Genlisea.r 2006 Elsevier GmbH. All rights reserved.
Keywords: Carnivorous plants; Utricularia; Trap; Functional morphology; Functional anatomy
Introduction
Among angiosperms, the carnivorous syndromeevolved several times with different morphologicaladaptations allowing plants to trap and digest prey(Albert et al., 1992; Barthlott et al., 2004; Barthlott
e front matter r 2006 Elsevier GmbH. All rights reserved.
ra.2005.12.004
ing author.
ess: [email protected] (W. Barthlott).
ress: Julius-von-Sachs-Institut fur Biowissenschaften,
otanik II – Okophysiologie und Vegetationsokologie,
rzburg, Julius-von-Sachs-Platz 3, D-97082 Wurzburg,
et al., in press; Juniper et al., 1989). The Lentibular-iaceae comprise the three genera Pinguicula, Genlisea
and Utricularia, which exhibit different types of trappingmechanisms. Pinguicula (Cieslak et al., 2006) possessessticky leaves that function as flypaper traps, whileGenlisea (Barthlott et al., 1998) exhibits funnel-shapedtraps. Here, we focus on the highly specialised andunique suction traps of the genus Utricularia. Earlyobservations of the anatomy, morphology and themovement of Utricularia traps include studies by Cohn(1875), Czaja (1922a, b), Darwin (1875), Gobel (1889,1891), Lutzelburg (1910), Merl (1922), and Schmid(1912). Lloyd (1929, 1932, 1933, 1942) attempted to
ARTICLE IN PRESSK. Reifenrath et al. / Flora 201 (2006) 597–605598
explain the ‘‘entrance mechanism’’ and trap movements,while Fineran and Lee (1975, 1980) and Sydenham andFindlay (1973) studied the physiology of the traps.
More recent observations were made by Brugger andRutishauser (1989), Rutishauser and Sattler (1989) andRutishauser and Isler (2001), dealing with the ontogenyand homology of plant structures. In his comprehensivemonograph, Taylor (1989) offers an overview of thedistribution, taxonomy, and general morphology ofUtricularia. Taylor’s work includes 214 species, subdi-vided into 35 sections based on several characteristics ofthe trap morphology. Three life forms of Utricularia canbe recognized (Taylor, 1989): (a) aquatic, free-floatingspecies (37 species, 2 sections) lacking any roots or root-like organs, (b) terrestrial species (162 species, 30 sections)with flowers, stems, leaves or leaf-like phylloclades, androot-like rhizoids and stolons anchored in the soil, and (c)facultative epiphytic species (15 species, 4 sections) beingsimilar to terrestrial forms, but commonly anchored ontree branches or moss-covered trunks.
The aim of our study is to compare the characteristictrap features of the different life forms with regard to theecological adaptions for different habitats. We analyzethe morphology and anatomy of the traps from arepresentative spectrum of Utricularia species in order toreveal patterns of their variability between different lifeforms and taxonomic groups, and discuss their potentialsignificance for the trapping mechanism.
Material and methods
Fourteen Utricularia species from 11 sections includ-ing all three life forms were selected from greenhousecultivations of the Botanical Gardens Bonn (specieslist, accession nos., and investigated characteristics inTable 1). For morphological and anatomical studieslight microscopy (LM), transmission electron micro-scopy (TEM: Zeiss EM 10 and a Siemens Elmiskop101), and scanning electron microscopy (SEM: LEO440i; LEO Electron Microscopy Ltd., Cambridge UK)were used. For TEM, three types of fixation are used: (a)glutar-aldehyde (2% in 0.05M buffer Pipes, pH 7)followed by the transfer in osmiumtetroxide anddehydration in acetone, (b) freeze-substitution in liquidpropane (�18 1C) or diethylether (�11 1C) at �8 1C witha solution of osmiumtetroxide in acetone, and (c) fast-fixation in methanol (Neinhuis and Edelmann, 1996).
Results
Trap and entrance position
Traps are produced from various tissues, includingphylloclades, shoots, stolons, and rhizoids (Table 1).Stolons and phylloclades were found to be subterranean
or at least in contact to soil surface and covered bymoisture when producing traps. Five combinations oftrap positions were found in different sections: (a) shoot-branches, (b) stolons, (c) rhizoids and stolons, (d)phylloclades, rhizoids, and stolons, (e) phylloclades andstolons, and (f) rhizoids in accordance with Taylor (1989).
The entrance position is determined in relation to theposition of the trap stalk. Confirming Taylor’s data, wedistinguish three different positions: basal, lateral, andterminal, each found within several sections (Table 1).
Two- and four-armed glands
Two-armed glands occur on the interior side of thethreshold, while four-armed glands are situated on theinner trap wall (Fig. 1a and b). The function of the formeris the transport of water out of the trap after the suctionprocess, while the latter are involved in the secretion ofdigestive enzymes and absorption of the prey’s nutrients(Fineran and Lee, 1975). Both kinds of glands were foundin all traps investigated. Taylor (1989) offers somedetailed descriptions of the different gland types.
Appendages
The entrance of most traps is surrounded byappendages, which usually are connected with the trapin dorsal position of the door, often covering theexterior region of the entrance. We differentiate betweenfive different types of appendages, plus the case ofreduced appendages (Table 1).
Dorsal appendages (Fig. 2a and d):
(a)
One pair of non-branched, wide appendages islocated in dorsal position of the entrance andoriented in a rolled manner on both sides of theentrance against the trap wall (Utricularia alpina,Utricularia calycifida, Utricularia longifolia, Utricu-laria prehensilis, Utricularia quelchii, and Utricularia
reniformis). The appendages sometimes cover parts ofthe entrance and form lateral tunnel-shaped entranceson both sides (Utricularia multifida) (Fig. 2d).
(b)
One pair of finely branched, antennae-shapedappendages is fixed in dorsal position of the trapentrance. The entrance can be observed from frontalview (Utricularia australis).(c)
One pair of hairy, antennae-shaped appendages isfixed in dorsal position of the entrance. Theappendages are non-branched and allow the frontalview on the door (Utricularia subulata) (Fig. 2a).Dorsal and lateral appendages (Fig. 2b):
One single spike-shaped appendage emerges in dorsalposition of the entrance, bending downwards to the
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Table
1.
Characteristictrapfeaturesofdifferent
Utr
icu
lari
aspecies
Section(T
aylor,
1989)
Accessionno.
Trappositions
Appendages
position(type)
Entrance
position
Bristles(e.g.
triggerhairs)
Trapdiameter
(mm)
Threshold
shape
Epiphytic
Utr
icu
lari
aspecies
Iper
ua
ren
ifo
rmis
05716
Stolons
1Basal
(+)
1.6
(0.7–1.5)
Wedge-shaped
Orc
hid
ioid
esa
lpin
a17166/12367
Stolons
1Basal
(+)
0.9
(0.5–1.0)
Chin-shaped
qu
elch
ii08567
Stolons
1Basal
(+)
0.9
(0.6–1.0)
Wedge-shaped
Terrestrial
Utr
icu
lari
aspecies
Ca
lpid
isca
livi
da
12919
Stolons,
phylloclades,
rhizoids
5Terminal
+1.0
(1.0–2.0)
Wedge-shaped
san
der
son
ii05713/12916
Stolons,
phylloclades,
rhizoids
5Terminal
+1.0
(1.0–1.5)
Wedge-shaped
Oli
go
cist
ap
reh
ensi
lis
11834
Stolons,
phylloclades,
rhizoids
1Basal
+1.0
(0.6–1.5)
Wedge-shaped
Ple
ioch
asi
ad
ich
oto
ma
16419
Stolons
4Lateral
�2.0
(1.0–2.0)
Chin-shaped
Po
lyp
om
ph
oly
xm
ult
ifid
a17178
Rhizoids
1Basal
�1.2
(2.0–2.5)
Chin-shaped
Psy
llo
sper
ma
caly
cifi
da
14514
Stolons,rhizoids
1Basal
+0.6
(1–1.5)
Chin-shaped
lon
gif
oli
a16928
Stolons,rhizoids
1Basal
+0.6
(1.0–1.5)
Chin-shaped
Set
isca
pel
lasu
bu
lata
12917
Stolons,
phylloclades
3Lateral
+0.4
(0.2–0.7)
Chin-shaped
Sto
mo
isia
jun
cea
15056
Stolons,
phylloclades,
rhizoids
6Lateral
�0.5
(0.3–0.6)
Wedge-shaped
Aquatic
Utr
icu
lari
aspecies
Utr
icu
lari
aa
ust
rali
s09028
Shoot-branches
2Lateral
(+)
1.4
(0.5–2.5)
Chin-shaped
Ves
icu
lin
ap
urp
ure
a17022
Shoot-branches
6Terminal
�1.2
(1.0–2.0)
Reduced
Appandages:type1:in
pairs,dorsal,wide,unbranched;type2:in
pairs,dorsal,finelybranched,antennae-shaped;type3:in
pairs,dorsal,hairy,antennae-shaped;type4:onedorsalandtw
olateral
wing-shaped;type5:manydorsal,lateralandventral;type6:rudim
entary.Bristles:+
existent;�
notexistent;(+
)proved
triggerhairfunction.Diameter
oftraps:ownmeasurementscomparedwith
literature
(Taylor,1989).
K. Reifenrath et al. / Flora 201 (2006) 597–605 599
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Fig. 2. (a) Entire trap of U. subulata (scale bar 100mm), (b) U. dichotoma (scale bar 200 mm), (c) U. sandersonii (scale bar 100mm), (d)
U. multifida (scale bar 100mm), (e) U. juncea (scale bar 300 mm), and (f) U. purpurea (scale bar 200 mm).
Fig. 1. Transversal-lateral cross-section of the trap of U. subulata (scale bar 100mm) (a) and U. longifolia (scale bar 200mm) (b).
K. Reifenrath et al. / Flora 201 (2006) 597–605600
door. On both lateral sides of the entrance, two wing-shaped, deeply lobed appendages run in parallel down-wards to the stalk of the trap (Utricularia dichotoma).
Dorsal, lateral, and ventral appendages (Fig. 2c):
The trap entrance is surrounded by rows of appen-dages, which are arranged to a roof-like ‘‘upper lip’’,consisting of five rows and a ‘‘lower lip’’, counting fourrows. These hair-like appendages with ball-shaped,gland-like tips stick vertically out the trap (Utricularia
livida and Utricularia sandersonii)
Rudimentary appendages (Fig. 2e and f):
Some traps only show a very small tissue elevation inthe position of the appendages, surrounding the doorand offering an exposed position of the entrance. Wedefine these structures as rudimentary appendages(Utricularia juncea and Utricularia purpurea).
Trap doors and bristles
Anatomically, the door consists of two layers of cells,the cells of the inner layer being larger in diameter than
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the outer layer (Figs. 3a, 4a, c, and d) (in contrast to thecellular composition of the trap walls). The central areaof the door, when bearing bristles, consists of a verythin, small-celled tissue (Figs. 3f, 4a, and d). InU. multifida, the upper part of the door is very stiffand consists of a number of cells not forming cell layers(Fig. 4e).
SEM studies of trap doors show that ten speciesusually bear four or five with a maximum of sevenstiff bristles in the central region outside of the door(Figs. 1a, 3e, and f), while four species lack bristlesentirely (Table 1). Most authors consider these struc-tures to be so-called triggerhairs (Juniper et al., 1989),implying that a touch of the bristles fires the trap(Cohn, 1875; Darwin, 1875; Gobel, 1891; Lloyd, 1936;Merl, 1922). This was confirmed in our study for fourspecies by artificially stimulating the bristles of livingtraps with a hair, observed with a dissecting microscope.The remaining six species with bristles were either toosmall for this treatment, or could not be stimulated(Table 1).
We were able to confirm Lloyd’s (1936) observationthat bristles on the outside of the door of theinvestigated traps of U. purpurea are not stiff, but
Fig. 3. (a) SEM pictures (transversal-lateral cross-section) of the tr
(scale bar 200mm), (c) U. purpurea (scale bar 100 mm), (d) U. sanders
U. subulata (scale bar 100mm). b, bristles; d, door; g, gland hairs; p
instead are very flexible hair-like structures with ball-shaped tips (Fig. 3c). They occur in arrangements of upto 14 and lack the characteristics of triggerhairs.
Threshold
In most species, closed trap doors rest on a massivethreshold (Figs. 3a, b, d–f, 4b, and c), which isrudimentary in one species investigated: U. purpurea
(Fig. 4d) (Table 1). In transversal-lateral cross-sectionsof the traps, two types of thresholds can be distinguishedbased on shape and cellular composition: (1) the chin-shaped threshold (Cohn, 1875) points into the lumenof the trap and is about twice as wide as the trap wall(Figs. 3a, b, f, 4b, and c). The central part consists of anarrangement of large lumen cells of relatively homo-genous size. From this threshold, a different type couldbe distinguished which is here referred to as (2) wedge-shaped threshold (Figs. 3d, e, and 4a). In lateral-transversal sections, this threshold is about four times aswide as the trap wall. It is composed of three rows ofdifferent-sized cells, which are largest at the trap wallnear the outer part of the threshold and smaller towardsthe inner part.
ap entrance of U. alpina (scale bar 100 mm), (b) U. dichotoma
onii (scale bar 100mm), (e) U. quelchii (scale bar 30mm), and (f)
, pavement epithelium; t, triggerhairs; th, threshold.
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Fig. 4. (a) LM pictures (semi-thin-sliced) of the trap entrance of U. quelchii (scale bar 150mm), (b) U. multifida (scale bar 80 mm), (c)
U. dichotoma (scale bar 150 mm), (d) U. purpurea (scale bar 30 mm), (e) U. multifida (scale bar 100 mm), and (f) U. quelchii (scale bar
1,2mm). b, bristles; d, door; g, gland hairs; p, pavement epithelium; t, triggerhairs; th, threshold.
Fig. 5. TEM picture of the lower part of the trap door of U.
reniformis leaning on the velum and the pavement epithelium
(scale bar 20mm). d, door; p, pavement epithelium; th,
threshold.
K. Reifenrath et al. / Flora 201 (2006) 597–605602
Common to both types is a layer of small cells bearingtwo-armed glands directed towards the lumen of the trap(Fig. 4b). The stalk of some traps seems to represent anouter extension of a chin-shaped threshold (U. alpina,U. dichotoma). The outer layer of both threshold types
bears a double row of small gland cells at the side wherethe door rests, the pavement epithelium (Figs. 3e, 4a–c,and 5), which is known to secrete mucilage and producesthe velum (Figs. 3a, e, and 5), a membranous layer,projecting balloon-like into the space of the trap entrance(Lloyd, 1942; Withycombe, 1924). In the closed trap, thefree end of the door is positioned on top of this pavementepithelium; both, the pavement epithelium and the velumsupport the sealing of the door. In U. purpurea, there isonly a single large lumen cell instead of a threshold,covered with a small-celled epidermis (rudimentarythreshold) (Figs. 3c and 4d).
Trap size
Several sections contain species showing dimorphictraps, varying in size (e.g. sections Pleiochasia, Utricu-
laria) (Table 1).
Trap wall
The wall of all traps studied consists of two cell-layers, with the exception of U. multifida, where three orfour cell-layers were found. The cells of the inner layer
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were smaller in diameter than the cells of the outer layer,although variability within species was pronounced.Differences of the mean diameter of the cells of the innerand outer layers vary between 32% and 52%. Thediameter of rear walls was on average 55% (732 SD)larger than sidewalls in all investigated species butU. multifida. The latter show larger diameters of the rearwalls (180%) in contrast to the sidewalls of the sametraps.
Discussion
Morphology of traps in relation to function
Most morphological and anatomical features of trapsstudied hitherto have been found to vary between species.Many structures, such as threshold, bristles and appen-dages can be reduced or even absent (Rutishauser andSattler, 1989; Taylor, 1989). This might be an indicationthat either such traps perform a different trappingmechanism or that the structures are not essential forcarnivory. Traps from all species investigated containeddifferent invertebrates, either entire or in pieces (Fig. 1b).This however may not be an unequivocal indication ofcarnivory, since animals may also live as commensals intraps (Richards, 2001).
Our results as well as the data of Taylor (1989) showthat the average trap size of aquatic species (0.2–6mm) isgenerally larger than that of the epiphytes (0.4–2.5mm)with the exception of Utricularia humboldtii withdimorphic traps (big traps between 0.5–1.2 cm, smalltraps 1.0–1.5mm). Within the terrestrial Utricularia, thesection Pleiochasia shows large traps up to 6mm indiameter (e.g. U. inaequalis), while other terrestrial trapsare much smaller (0.2–2.5mm). Regardless of theecological groups, we assume that a varying trap sizewithin and between species helps to assure a broader preyspectrum in a given habitat. The results of wallmeasurements show, that in general the rear walls consistof a number of disordered cells, and are 60% thicker thanthe sidewalls, which are always restricted to two cell-layers, except for U. multifida. Assuming that theseproperties support the trap movements when catchingprey, the rear wall may stabilize the whole trap, while theflexible sidewalls support the water sucking process.
The traps of U. multifida show a number ofconspicuous characteristics. The sidewalls consist ofthree or four cell layers instead of two in the otherterrestrial species, together with a multi-celled doormaking the whole trap very robust. Additionally, theentrance is more or less covered by the dichotomouslydivided appendages fixed in dorsal position of the door,forming two lateral tubular channels densely coveredwith hairs (Fig. 2d). Based on these results wehypothesize that these traps might not function with a
low pressure-suction movement. We suggest regardingthese traps as channel traps with a permanent opendoor, resembling the traps of related genus Genlisea
(Barthlott et al., 1998).
Trap architecture and life forms
Epiphytic species: In contrast to the terrestrialbladderworts, the traps of the epiphytic species arerather uniform. The habitat of epiphytic Utricularia aremoss-covered branches and trunks of trees, similar tothose of epiphytic species of the Bromeliaceae (Taylor,1989). In both cases, the availability of water representsthe limiting factor for colonization. Confirming Taylor’sobservations, we identified ground-, moss- or water-covered stolons as trap-producing tissues of this group.Branched appendages, fixed on the dorsal part of theentrance, and bending downwards to both sidewalls ofthe trap, are more or less covering the front of the door.Together with the basal position of the entrance withregard to the trap stalk, we assume that the appendagesform a water-storage just in front of the door, eitherpreventing the trap from desiccation or insuring theability of trapping under various environmental condi-tions. All epiphytic Utricularia species investigated beartrigger hairs on the outer surface of the trap door andprey was found inside all bladders.
Terrestrial species: Because of the heterogeneousexpression of most characters within the investigatedspecies, it is hard to assign any common feature to thegroup of terrestrial Utricularia. The position of the trapon the plant varies between stolons, phylloclades andrhizoids, while the position of the entrance in relation tothe stalk varies between basal, lateral, and terminal.Most investigated traps show appendages surroundingthe entrance and most bear triggerhairs or at leastbristles on the outer part of the door, though anyobvious connections between the mentioned features arelacking. The appendage-less and bristle-less sectionStomoisia occurs in the same habitats as other terrestrialspecies bearing appendages or bristles or both.
Concerning the extraordinary appendages of U. livida
and U. sandersonii, which we assume to have someglandular characteristics because of the gland-like tips,further detailed investigations are required.
Aquatic species: We distinguish two groups, incongruence with Taylor’s (1989) classification into twosections, with the larger section Utricularia representingthe predominantly investigated bladderworts. The trapsof species belonging to this section are very homo-geneous: They occur laterally on finely branched shoots,the entrance is in lateral position to the stalk of the trap,and in dorsal position of the entrance stiffly, branchedappendages stick out of the trap. These appendages arecalled ‘‘antennae’’ and are considered as ‘‘Leitsysteme’’
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to guide the prey to the entrance of the trap (Darwin,1875; Lutzelburg, 1910). The outer part of the trap doorbears stiff bristles, which are known as triggerhairs. Thesmaller section Vesiculina bears smaller traps thanUtricularia, terminally on finely branched shoots; theentrance is in terminal position in relation to the stalk ofthe trap. These traps are lacking any appendages.Instead of stiff triggerhairs, a bunch of glandulartrichomes were found on the outer surface of the trapdoor (‘‘Schleimhaare’’, Lutzelburg, 1910). Thus, theauthors do not support Lloyd’s (1933) hypothesis thatthese trichomes are analogous to common triggerhairs(despite his failure to fire these traps by giving a stimulusto the trichomes). Further observations are required toattain more information about their function. Incontrast to the chin-shaped threshold of the traps ofthe section Utricularia, we found a rudimentary thresh-old in U. purpurea (section Vesiculina).
The subdivision of the genus according to Taylor(1989) is largely based on trap characteristics. Mullerand Borsch (2005) presented a phylogeny based onextensive molecular data for all sections, confirming thebasal position of Polypompholyx and Pleiochasia as wellas the derived position of the aquatic species. Asdescribed above, we suggest a close relation betweenthe genus Genlisea and the species U. multifida (sectionPolypompholyx), based on the hypothesis that the trapsof the latter do not function with a suction mechanism,but with tunnel-shaped entrances leading to a door-lessdigesting chamber. Consequently, we comfirm a phylo-genetically basal position of section Polypompholyx asstated in Muller et al. (2004). The greatest similarities toPolypompholyx are found in some species of the likewiseterrestrial, species-rich section Pleiochasia, that also lackbristles on a quite massive door and have traps ofsimilar size.
Acknowledgements
We thank H.J. Ensikat (Nees-Institute) for hisassistance at the scanning- and transmission electronmicroscopy. For information, datasets and discussions –especially with regard to the phylogeny of Lentibular-iaceae – we thank Dr. T. Borsch and K. Muller (bothNees-Institute). This study was supported by theDeutsche Forschungsgemeinschaft (Ba 605/9-3).
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