ARTICLE IN PRESS

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: barthlott@uni-bonn.de (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

ARTICLE IN PRESS

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

ARTICLE IN PRESS

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

ARTICLE IN PRESSK. Reifenrath et al. / Flora 201 (2006) 597–605 601

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.

ARTICLE IN PRESS

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

ARTICLE IN PRESSK. Reifenrath et al. / Flora 201 (2006) 597–605 603

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’’

ARTICLE IN PRESSK. Reifenrath et al. / Flora 201 (2006) 597–605604

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).

References

Albert, V.A., Williams, S.E., Chase, M.W., 1992. Carnivorous

plants: phylogeny and structural evolution. Science 257,

1491–1495.

Barthlott, W., Porembski, S., Fischer, E., Gemmel, B., 1998.

First protozoa-trapping plant found. Nature 392, 447.

Barthlott, W., Porembski, S., Seine, R., Theisen, I., 2004.

Karnivoren: Biologie und Kultur Fleischfressender Pflan-

zen. Ulmer, Stuttgart.

Barthlott, W., Porembski, S., Seine, R., Theisen, I., in press.

Carnivorous plants. Biology and cultivation. Timber Press,

Portland.

Brugger, J., Rutishauser, R., 1989. Bau und Entwicklung

landbewohnender Utricularia-Arten. Bot. Helv. 99, 91–146.

Cieslak, T., Polepalli, J.S., White, A., Muller, K., Borsch, T.,

Barthlott, W., Steiger, J., Marchant, A., Legendre, L., 2005.

Phylogenetic analysis of Pinguicula (Lentibulariaceae):

chloroplast DNA sequences and morphology support

several geographically distinct radiations. Am. J. Bot. 92,

1723–1736.

Cohn, F., 1875. Ueber die Function der Blasen von Aldrovanda

und Utricularia. Cohn’s Beitrage Biol. Pfl. 1, 71–92.

Czaja, A.T., 1922a. Die Fangvorrichtung der Utriculariablase.

Z. Bot. 14, 705–729.

Czaja, A.T., 1922b. Ein allseitig geschlossenes, selektivperme-

ables System. Ber. Deutsch. Bot. Ges. 40, 381–385.

Darwin, C., 1875. Insectivorous Plants. John Murray,

London.

Fineran, B.A., Lee, M.S.L., 1975. Organization of quadrifid

and bifid hairs in the trap Utricularia monanthos. Proto-

plasma 84, 43–70.

Fineran, B.A., Lee, M.S.L., 1980. Organization of mature

external glands on the trap and other organs of the

bladderwort Utricularia monanthos. Protoplasma 103,

17–34.

Gobel, K., 1889. Der Aufbau von Utricularia. Flora 72,

291–297.

Gobel, K., 1891. Pflanzenbiologische Schilderungen. N.G.

Elwert‘sche Verlagsbuchhandlung, Marburg.

Juniper, B.E., Robins, R.J., Joel, D.M., 1989. The Carnivor-

ous Plants. Academic Press, London, San Diego.

Lloyd, F.E., 1929. The mechanism of the water tight door of

the Utricularia trap. Plant Physiol. 4, 87–102.

Lloyd, F.E., 1932. The door of Utricularia, an irritable

mechanism. Can. J. Bot. 10, 780–786.

Lloyd, F.E., 1933. The carnivorous plants – a review with

contributions. Trans. Roy. Soc. Can., 3. Ser. 27, 38–51.

Lloyd, F.E., 1936. Struktur und Funktion des Eintrittsmecha-

nismus bei Utricularia. Beih. Bot. Centralbl. 54, 292–320.

Lloyd, F.E., 1942. The Carnivorous Plants. Chronica Botanica

Company, Donald Publishing, Waltham, Massachusets,

New York.

Lutzelburg, P.v., 1910. Beitrage zur Kenntnis der Utricularien.

Flora 100, 145–212.

Merl, E.M., 1922. Biologische Studien uber die Utricularia-

blase. Flora 108, 59–74.

Muller, K., Borsch, T., 2005. Phylogenetics of Utricularia

(Lentibulariaceae) and molecular evolution of the trnK

intron in a lineage with high substitutional rates. Plant Syst.

Evol. 250, 39–67.

Muller, K., Borsch, T., Legendre, L., Porembski, S., Theisen,

I., Barthlott, W., 2004. Evolution of carnivory in

Lentibulariaceae and the Lamiales. Plant Biol. 6, 477–490.

Neinhuis, C., Edelmann, H.G., 1996. Methanol as a rapid

fixative for the investigation of plant surfaces by SEM.

J. Microsc. 184, 14–16.

ARTICLE IN PRESSK. Reifenrath et al. / Flora 201 (2006) 597–605 605

Richards, J.H., 2001. Bladder function in Utricularia purpurea

(Lentibulariaceae): is carnivory important? Am. J. Bot. 88,

170–176.

Rutishauser, R., Isler, B., 2001. Developmental genetics and

morphological evolution of flowering plants, especially

bladderworts (Utricularia): fuzzy arberian morphological

complements classical morphology. Ann. Bot. 88,

1173–1202.

Rutishauser, R., Sattler, R., 1989. Complementarity and

heuristic value of contrasting models in structural botany.

III. Case study on shoot-like ‘‘leaves’’ and leaf-like

‘‘shoots’’ in Utricularia macrorhiza and Utricularia purpurea

(Lentibulariaceae). Bot. Jahrb. Syst. 111, 121–137.

Schmid, G., 1912. Beitrage zur Okologie der insektivoren

Pflanzen. Flora 104, 335–383.

Sydenham, P.H., Findlay, G.P., 1973. The rapid movements of

the bladder of Utricularia sp. Aust. J. Biol. Sci. 26, 1115–1126.

Taylor, P., 1989. The genus Utricularia: a taxonomic mono-

graph. Royal Botanic Gardens, Kew; Her Majesty’s

Stationery Office, London.

Withycombe, C.L., 1924. On the function of the bladders in

Utricularia vulgaris L. Bot. J. Linn. Soc. 46, 401–413.