Evolution of Aquatic Angiosperm Reproductive Systems

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Western Connecticut State University
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Faculty Papers Biology & Environmental Sciences
12-1996
Evolution of Aquatic Angiosperm Reproductive
Systems
Tom Philbrick PhD
Western Connecticut State University, [email protected]
Donald E. Les PhD
University of Connecticut
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Philbrick, Tom PhD and Les, Donald E. PhD, "Evolution of Aquatic Angiosperm Reproductive Systems" (1996).Faculty Papers. 5.
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Evolution of Aquatic Angiosperm
Reproductive Systems
What is the balance between sexual and asexual reproduction
in aquatic angiosperms?
C. Thomas Philbrick and Donald H. Les
A
s angiosperms diversified and greater chemical and thermal stabil-
flourished in terrestrial habi- Aquatic plants are an ity than air, and it buffers against (or
tats, some species ultimately even precludes) many types of cata-
colonized freshwater or marine en- extremely heterogeneous strophic disturbance that plague ter-
vironments and became aquatic. restrial habitats, such as rapid tem-
Aquatic plants are species that per- assemblage of species perature changes, fires, floods, and
petuate their life cycle in still or strong winds. At higher latitudes,
flowing water, or on inundated or that survive in similar seasonal stability of aquatic habitats
noninundared hydric soils. Aquatic is faithfully maintained by the den-
angiosperms inhabit oceans, lakes, habitats but as a result of sity of water, which is greatest (de-
rivers, and wetlands. pending on salinity) at approximately
fundamentally different
4°C (Wetzel 1975). Thus, even in
The transition to an aquatic life
the coldest temperatures, lake and
has been achieved by only 2% of the evolutionary pathways
river bottoms typically remain ice
approximately 350,000 angiosperm
free.
species (Cook 1990). Nonetheless,
the evolutionary invasion of aquatic with specific growth forms: emersed Coastline and freshwater shore
environments by terrestrial an- from the water, free-floating, float- aquatic habitats have been viewed
giosperms is estimated to represent ing-leaved, or submersed. These cat- as inherently unstable (Laushman
50-100 independent events (Cook egories represent different degrees 1993) due to erosional processes,
1990). Although aquatic plants are of adaptation to aquatic life and are tidal fluctuations, and wave dynam-
typically discussed as a unified bio- widely convergent among aquatic ics. However, habitat stability should
logical group, the ways that species angiosperms. be evaluated not only in terms of
have evolved to life in the aquatic As in terrestrial plants, reproduc- characteristic short-term variation,
milieu are as diverse as the different tion in water plants consists of both but also over the course of longer,
evolutionary lineages that became sexual and asexual mechanisms. evolutionarily significant time
aquatic (Hutchinson 1975, Scul- Sexual reproduction (the chief source frames. In this sense, stability re-
thorpe 1967). Reproductive and of hereditary variation via genetic flects the consistent expression of
other life-history traits of aquatic recombination) in plants is consid- predictable habitat characteristics
angiosperms are closely associated ered to be advantageous in changing over long time periods. In essence,
or heterogeneous environments, and aquatic habitats may be quite vari-
asexual reproduction (which per- able, yet vary in a similar, predict-
petuates genetic uniformity) is con- able fashion through time. The an-
C. Thomas Philbrick is an associate
sidered to be more successful in stable giosperm family Podostemaceae
professor in the Department of Biologi-
cal and Environmental Sciences, West- or uniform habitats (Grant 1981, (riverweeds) illustrates this concept
ern Connecticut State University, Williams 1975). Consequently, the well. Riverweeds grow tenaciously
Danhury, CT 06810. Donald H. Les is evolution of aquatic plant reproduc- attached to rocks in tropical river
an associate professor in the Depart- tive systems should reflect the rela- rapids and waterfalls. Although the
ment of Ecology and Evolutionary Biol- tive stability of their habitats. rushing current makes this habitat
ogy, University of Connecticut, Storrs, unstable ecologically, the seasonally
A vast assortment of freshwater
CT 06169-3042. The authors share re- high and low water levels make it a
and marine environments exists.
search interests in the systematics and predictable habitat in which river-
evolution of aquatic flowering plants. Nevertheless, aquatic habitats tend weeds flourish (Philbrick and Novelo
© 1996 American Institute of Biologi- to be stable (Hartog 1970, Sculthorpe 1995).
cal Sciences. 1967, Tiffney 1981). Water exhibits
December 1996 813
No aquatic habitat is absolutely milfoil {Myriophyllum spicatum,
stable. Factors such as continental Haloragaceae) have spread over vast
drift have lead to drastic ecological areas by asexual means. Field stud-
changes in coastal marine environ- ies (Les 1990) indicate that plots
ments. Cultural eutrophication and planted with small fragments of
pollution can rapidly alter the trophic water milfoil can reach carrying ca-
status of aquatic habitats. The spo- pacity in only 16 months (Figure 1).
radic outbreak of pathogens, such as Such results express the futility of
the agent responsible for the devas- control efforts if aquatic weed intro-
tating wasting disease of the seagrass 10 13 14 16 1B 20 23 34 ZE 37 ductions are not recognized, and
Zostera marina (Zosteraceae; Muchl- plants eradicated, immediately after
Figure 1. Asexual reproduction in
stein et al. 1991), is yet another initial colonization.
aquatic plants occurs rapidly. Biomass
aspect of instability in aquatic envi- (grams of dry weight) measured in 2 m Most aquatic plants are not
ronments. X 2 m field plots planted initially with troublesome but possess mechanisms
In evolutionary time frames, 100 small fragments of Eurasian water for asexual reproduction similar to
aquatic habitats represent a mosaic milfoil (Myriophyllum spicatum). those of their weedy counterparts.
Within 16 months, vegetative growth
of both stable and unstable condi- Many common names such as wa-
had reached maximum biomass levels
tions to which complex adaptation terweed, pondweed, and riverweed
(carrying capacity). Biomass had more
has been necessary. Recalling the are unwarranted but bave probably
than doubled during the first four-month
paradigm for the evolution of asexual growing season (from Les et al. 1988). originated because of tbe tendency
and sexual reproductive systems, it for water plants to grow in luxuriant
is evident that both systems should beds formed by vigorous vegetative
retain important functions in the etatively produced progeny) are not growtb. Some native aquatic plants
majority of water plant species. In always identical genetically to the are actually more productive than
this article, we discuss possible evo- parent (see below). In any case, they introduced weedy species but have a
lutionary factors to account for the represent a legitimate example of less effective vegetative growtb ar-
balance between sexual and asexual reproduction in which discrete, new chitecture. For example, experiments
reproduction that is maintained in individuals are produced and dis- in wbicb vegetative fragments from
aquatic angiosperms. persed. botb a native pondweed and intro-
duced milfoil species were planted
Asexual reproduction is impor-
simultaneously sbow greater bio-
tant in the establishment, growth,
Asexual reproduction mass productivity in the native spe-
and maintenance of aquatic plant
cies (Table 1; Les et al. 1988). Addi-
Asexual reproduction includes both populations. For example, in weedy tional experiments have furtber
seed production without fertiliza- aquatic plants, most emergent spe- indicated no evidence of competi-
tion (agamospermy) and vegetative cies disperse by sexual propagules, tion between these species under
reproduction. Because the extent of whereas floating and submersed spe- normal environmental conditions
agamospermy among aquatic plants cies disperse vegetatively (Cook (Les et al. 1988). Elevated nutrients
is poorly understood (Les 1988a), 1993, Spencer and Bowes 1993). resulted in tbe accelerated growtb of
we limit our discussion to vegetative Nevertheless, the principal means of both species (Les 1990), but milfoil
reproduction, which is often assumed population increase for all three biomass was mostly allocated to pro-
to be the dominant mode of repro- growth forms is by vegetative repro- duce long, vertical sboots, wbereas
duction in water plants (Hutchinson duction (Spencer and Bowes 1993). much pondweed biomass was allo-
1975, Sculthorpe 1967). Abraham- Certainly, the ease and rapidity by cated to borizontal rhizomes (Table
son (1980) considered that geneti- which aquatic weeds spread through- 1). Rapid vertical growtb under en-
cally identical offspring render the out nonindigenous regions attests to banced nutrient regimes enables mil-
process of vegetative reproduction the efficiency of vegetative repro- foil to quickly grow to tbe water
more similar to growth (increase in duction. surface, where it shades native plants,
size of an individual) than to repro- Nuisance aquatic weeds such as indirectly causing their decline.
duction (increase in the number of
vj2it&Th.ya.cmth. {Eichhornia crassipes,
individuals). However, ramets {veg-
Pontederiaceae) and Eurasian water The ability to reproduce vegeta-
Table 1. One season of vegetative growth compared between a native pondweed {Potamogeton amplifoUus) and the
nonindigenous Eurasian water milfoil {Myriophyllum spicatum) planted experimentally in a Wisconsin lake (from Les et al.
1988). Data are expressed as means; NA = not applicable {Myriophyllum does not produce rbizomes). The original shoot
cuttings of Potamogeton lacked rhizome tissue.
Shoot biomass (g) Shoot length (cm) Rhizome length (cm) Leaf number
Species Initial Final Initial Final Initial Final Initial Final
Potamogeton amplifoUus 0.25 1.18 3.2 50.0 0.0 47.5 4 52
Myriophyllum spicatum 0.20 0.88 15.0 190.0 NA NA 39 490
814 BioScience Vol. 46 No. 11
tively is ubiquitous among aquatic
species, regardless of their taxonomic
affiliation (Grace 1993, Hutchinson
1975, Les and Philbrick 1993,
Sculthorpe 1967). However, aquatic
plants are more common propor-
tionally in monocots than dicots (Les
and Schneider 1995). Tiffney and
Niklas (1985) postulated that the
greater proportion of aquatic mono-
cots is associated with the high inci-
dence of rhizomatous growth (i.e.,
by horizontal underground stems) in
monocots. In contrast, far fewer di-
cots are rhizomatous (Grace 1993).
This correlation suggests that clonal
growth is conducive to the evolution
of aquatic species.
Although annuals (in which re-
production is exclusively sexual) and
perennials are relatively evenly dis-
tributed among terrestrial plant
groups, most aquatic plants are pe-
rennial. Perennial water plants pos-
sess many contrivances for vegeta-
tive reproduction (Figure 2), including
corms, rhizomes, stolons, tubers, and
turions (Grace 1993, Hutchinson
1975, Sculthorpe 1967, Vierssen
1993). Even the few predominantly
annual aquatic plant genera such as
Najas (Najadaceae) may reproduce
vegetatively during the growing sea-
son by extensive lateral growth, frag-
mentation, or the occasional pro-
duction of turions (Agamietal. 1986,
Sculthorpe 1967).
Asexual reproduction is also com-
mon among terrestrial plants, and
the transport of tubers, corms, and
small bulbs confers high potential
vagility (ability to disperse) to pe-
rennial angiosperms (Stebbins 1950).
Water plants excel in this capacity
with a variety of vegetative struc-
tures that are highly specialized to
function efficiently as propagules,
some even capable of long-distance
dispersal. Vegetative propagules are Figure 2. Aquatic plants employ many types of vegetative structures for reproduc-
tion, (a) Modified horizontal stems (rhizomes) grow quickly to anchor aquatic
important agents of gene flow in
plants in unconsolidated, shifting substrates. This specimen of pondweed
aquatic plants (Barrett et al. 1993,
{Potamogeton amplifolius) resulted from the planting of a small four-leaved
Les 1991). The highly vagile
fragment that initially lacked a rhizome. The growth illustrated here occurred
propaguies of aquatic plants are ex-
during a single summer season, (b) Highly specialized vegetative leaves help to
ceptions to the generalization (Wil- insulate this spherical turion of biadderwort (Utricularia vulgaris). Turion leaves
liams 1975) that asexual offspring differ morphologically from normal foliage leaves such as those subtending the
develop close to the parent, as op- structure. Turions resist unfavorable environmental conditions and are efficient
posed to sexual offspring, which are propagules for aquatic plants, (c) Severed or injured vegetative tissue is capable
more widely dispersed. of generating "gemmiparous" plantlets in several aquatic species, such as lake
cress {Neobeckia aquatica). Detached leaves (shown here) or nearly any part of a
The most notable vegetative lake cress plant (as small as 0.5 mm) can produce a gemmiparous plant. However,
propagule in aquatic plants is the populations of this species have declined significantly because it is sexually sterile
turion (Figure 2b), a specialized and the vegetative fragments function poorly in long-distance dispersal. Bars = 1
cm.
structure with few functional coun-
December 1996 815
terparts in the terrestrial flora. Amphibolis suggests a compromise mens into natural habitats can lead
Turions are dormant vegetative buds between sexual and asexual repro- to serious weed problems. The origi-
enclosed by specialized leaves that duction. Although viviparous seed- nal presence of the notorious water
differ substantially in structure from lings possess the genetic advantages hyacinth (£. crassipes) in the United
normal foliage leaves. The often well- of a sexual derivation, the prerooted States may have resulted from the
insulated turions are sometimes re- leafy stems can establish in much the careless disposal of souvenir plants
ferred to as "winter buds," although same fashion as vegetative fragments. (Sculthorpe 1967). The morphology
in such species as Potamogeton Vegetative propagules of aquatic of many aquatic plants contributes
crispus (Potamogetonaceae) they plants are dispersed by a variety of to their human-induced dispersal.
enable plants to overcome the stress- abiotic vectors (water, wind) and For example, once introduced into a
ful summer rather than winter sea- biotic agents (amphibians, birds, lake, the long stems of plants like
son (Vierssen 1993). The winter buds mammals, reptiles; Hutchinson Elodea (Hydrocharitaceae) and
of terrestrial woody plants also fit 1975, Landolt 1986, Sculthorpe Myriophyllum easily become en-
this basic definition because their 1967). The minute size of plants in tangled on boat motors and trailers
bud scales are modified leaves. How- the duckweed family (Lemnaceae) and are eventually transported to
ever, buds of trees and shrubs re- facilitates the dispersal of whole in- different sites.
main viable only when attached to dividuals. In this family of the world's The taxonomically widespread
the parent plant and are incapable of smallest angiosperms, individuals evolution of vagile vegetative
dispersal and establishment. De- can be dispersed over several kilo- propagules in aquatic plants is due
tached turions of water plants are meters as a result of cyclones, and to several factors. Particularly in
free-living propagules. In the extreme the smallest duckweeds {Wolffia) temperate regions, where most natu-
case of "asexual annuals" (Hutchin- have even been found in hailstones ral lakes occur, aquatic habitats are
son 1975), turion production is ac- (Landolt 1986). It is impressive that not only short lived, but also subject
companied by the decay of the re- some species among these diminu- to recurrent, catastrophic destruc-
mainder of the plant during periods tive plants are also capable of pro- tion due to glaciation. These events
of stress. ducing yet smaller, vegetative turions have undoubtedly selected for vagil-
(Landolt 1986). Ultimate versatility ity in aquatic plants. Vagility of
Other vegetative structures of dis-
in vegetative dispersal structures is aquatic plants is not, however, ex-
persal in aquatic plants include "win-
exemplified by the lake cress clusively a feature of vegetative
ter buds," which are enclosed by
[Neobeckia aquatica)., in which even propagules. Many species, such as
leaves not significantly modified
minute root, stem, or leaf fragments marine angiosperms, rely on sexu-
from foliage leaves, and shoot frag-
(less than 0.5 mm) are capable of ally derived seeds for their remote
ments. Fragments play an important
regenerating entire new individuals dispersal, and even the most clonal
role in the vegetative reproduction
vegetatively. of aquatic angiosperms usually re-
of aquatic plants, with each indi-
tain the ability to reproduce sexu-
vidual node often capable of regen- Vegetative propagules have been
ally. Indeed, only a few aquatic spe-
eration (Grier 1920). Many of the instrumental in the dispersal of wa-
cies, such as bladderwort (Utricularia
important aquatic weeds are dis- ter plants by people. The adventi-
australis, Lentibulariaceae) and lake
persed in this fashion. tious rooting stems of watercress
cress {Neobeckia)., are not known to
Yet another kind of vegetative {Nasturtium officinale, Brassicaceae) produce viable seed (Les 1994, Tay-
propagule, gemmiparous (pseudo- were widely introduced throughout lor 1989). The rarity of lake cress
viviparous) plantlets (Figure 2c), are temperate regions, where they are underscores the importance of sexual
produced from leaves of some aquatic used in salads (Sculthorpe 1967). reproduction to facilitate long-dis-
plants, including species of Card- Various countries import nonin- tance dispersal. This species has de-
amine and Neobeckia (Brassicaceae; digenous aquatic species and propa- clined precariously throughout its
Sculthorpe 1967), Hygrophila gate them vegetatively for sale as historical range, despite a tremen-
(Acanthaceae; Miihlberg 1980) and ornamental aquarium and water dous capacity for vegetative regen-
the so-called viviparous species of garden plants. All species in the in- eration and local dispersal (Les
Nymphaea (Nymphaeaceae; Masters ventory of a recent North American 1994).
1974). True vivipary (seedling water garden catalogue (William
growth while the fruit remains at- Tricker, Inc., in Independence, Ohio) Ir is difficult to identify specific
tached to the parent plant) occurs in were shipped either as whole plants evolutionary factors that account for
the marine species Amphibolis or fragments. Most hardy water lil- the widespread occurrence of asexual
antarctica (Cymodoceaceae). The ies are infertile hybrids and are reproduction in water plants. Veg-
small seedlings of Amphibolis propagated vegetatively (Swindells etative reproduction correlates
(which are produced by sexual re- 1983). Although hybrid water lilies highly with both polyploidy and
production) eventually detach from do not ordinarily become problems, hybridization in angiosperms. The
the parent plant and are dispersed. shipments occasionally contain stems importance of vegetative reproduc-
Anchorage and establishment are as- of nefarious weedy species such as tion in stabilizing hybrid and poly-
sisted by a comblike structure that Hydrilla verticillata (Hydrocharita- ploid reproduction (in which a
develops from the apex of the fruit ceae) draped around their rootstocks. diminished capacity for sexual re-
and remains firmly attached to the The intentional or accidental release production is experienced) is well
seedling (Aston 1973). Vivipary in of cultivated, nonidigenous speci- understood (Grant 1981, Les and
816 BioScience Vol. 46 No. 11
Pbilbrick 1993, Stebbins 1950). they often root in tbe water before venture or under conditions in wbich
However, as Stebbins (1950) ob- reacbing suitable establishment sites the production of aerial flowers is
served, it is unlikely that vegetative (Barrett etal. 1993, Silander 1985). difficult.
reproduction arose because of fac- Furthermore, tbe proportion of Sexual reproduction may fail in
tors sucb as bybridization and poly- aquatic babitats suitable for growth aquatic plants for several additional
ploidy. Instead, it probably func- of vegetative propagules is mucb reasons (Barrett et al. 1993). Many
tions to maintain tbese conditions. greater tban that for seed germina- aquatic species are distributed widely
Other factors bave undoubtedly con- tion (Sculthorpe 1967). (Scultborpe 1967), and individual
tributed to the prominence of veg- In many aquatic plants, particu- plants may be incapable of adjusting
etative reproduction in aquatic larly marine angiosperms, strongly their flowering responses to tbe
plants, and several bypotbeses ad- rhizomatous growtb forms (Figure myriad pbotoperiods, temperatures,
dress this issue from contrasting per- 2a) belp to resist tbe damaging forces and other environmental conditions
spectives. of waves and tidal currents (Hartog tbat occur tbroughout a broad geo-
1970). An elaborate network of ad- graphic range. Members of tbe veg-
Survival in aquatic habitats. Vegeta- ventitious roots or rhizomes is re- etatively prolific duckweed family
tive reproduction functions effi- quired to withstand tbe loose and (Lemnaceae), for example, are wide-
ciently in aquatic environments, and shifting substrates tbat characterize spread geograpbically, and flower-
water plants provide many examples many aquatic babitats (Scultborpe ing in these plants is influenced by
of features associated witb habitat- 1967). Rbizomatous growtb is also many environmental factors (Landolt
related survival. Reduction of me- advantageous to aquatic species by 1986). Almost all duckweed species
chanical tissue in vegetative organs facilitating survival in babitats sub- retain tbe ability to flower, yet most
of submersed aquatic plants is com- ject to periodic drougbt (Hutcbinson are collected in flower less than 6%
mon and renders tbem fragile and 1975). Grace (1993) and Silander of tbe time and natural populations
susceptible to fragmentation by tbe (1985) summarized additional ad- are much more likely to reproduce
action of waves, wind, currents, and vantages of clonal reproduction, in- asexually than sexually (Landolt
interactions witb biotic elements cluding rapid numerical increase, 1986).
(Sculthorpe 1967). Altbougb stem unlimited production of favorable
Reduced flowering of aquatic
breakage and ensuing damage to gene combinations, bigh vagility
plants in deep-water babitats is com-
water-conducting tissue (xylem) where spatial variation in favorable
mon (Hutcbinson 1975). An obvi-
would bave disastrous consequences sites exists, efficient resource acqui-
ous limitation on aerial flowering is
for a terrestrial plant, barmful ef- sition wbere resource limitation ex-
tbat eitber stems or flower stalks
fects of fragmentation are mitigated ists, and effective storage structures
must project from tbe surface. Tbe
by tbe absence or reduction of xylem wbere large neigbbors or a vernal
deeper tbe plant, tbe more resources
in most submersed aquatic plants. environment predominates. Tbe po-
are necessary to produce a reproduc-
Terrestrial plants rely on internal tential benefits of rbizomatous, or
tive structure tbat reaches tbe water
mecbanical tissue to maintain an otberwise clonal, growtb account at
surface. Flongated reproductive
erect posture and to reduce break- least partially for the higb frequency
structures are more Hkely to become
age, wbereas water lends external of vegetative reproduction observed
physically damaged. This may ex-
support to delicate aquatic plant in botb aquatic monocots and di-
plain why species sucb as Butomus
sboots and belps to retain tbe viabil- cots.
umbellatus (Butomaceae) and Gra-
ity of detacbed or fragmented tis-
tiola aurea (Scropbulariaceae) flower
sues.
freely in tbeir emergent forms but
Failure of sexual reproduction. De-
seldomly in tbeir submersed forms
Fragmentation can also be ob- spite the intricate pollination mecba-
(Hutcbinson 1975, Scultborpe 1967).
served in terrestrial species, such as nisms of some water plants (Cook
Various deptb-related pbysical fac-
the litter of tree branches tbat typi- 1988, Scbultborpe 1967), most
tors, sucb as increased hydrostatic
cally follows a windstorm or beavy aquatic plants retain tbe floral sys-
pressure, reduce tbe incidence of
rain. However, a major difference is tems of tbeir terrestrial ancestors,
flowering in some aquatic species
tbat whereas aquatic plant fragments wbicb were not originally adapted
(Hutcbinson 1975).
immediately find tbemselves in a to function in water. Some species
babitat suitable for establishment have acquired floral modifications Although seed production is pro-
(or are dispersed to otber suitable that allow pollination to function portional to vegetative biomass in
sites), fragments of terrestrial plants efficiently in wet habitats, a phe- annual aquatic species (Vierssen
usually require planting in tbe soil to nomenon known as bydropbily. 1993), it is likely that adaptation to
survive (Hutchinson 1975). Thepto- However, for species wbose sexual vegetative reproduction in perenni-
tective aquatic environment allows organs are poorly adapted to aquatic als has involved various energetic
the production of relatively fragile babitats, clonal reproduction is an tradeoffs between vegetative and
structures tbat excel in clonal repro- efficient alternative. Because asexual sexual reproduction due to resource
duction (Grace 1993). At tbe same reproduction is a means of overcom- limitations (Cook 1985, Grant 1981,
time, tbese structures are potentially ing reliance on pollinators (Abra- Sculthorpe 1967). Sucb tradeoffs may
more successful at colonization and hamson 1980), it may facilitate ad- result in a reduced level of flower-
subsequent population growtb tban aptation to deep-water habitats ing. For example, in Potamogeton
sexually derived propagules because wbere terrestrial pollinators do not pectinatus, tuber size and seed pro-
December 1996 817
duction are inversely related (Yeo clonal aquatic weeds limits their rived offspring (Les and Philbrick
1965). Several turion-forming spe- adaptive ability in nonindigenous 1993, Silander 1985). Levels of ge-
cies of Utricularia produce few flow- ranges (Barrett et al. 1993). netic variability in asexual popula-
ers (Rossbach 1939). Some species of tions may even surpass those in
Utricularia are "vegetative apomicts," Genetic uniformity. Asexual repro- sexual populations (Silander 1985).
in which viable seed production has duction has been described as "any Recent studies of the vegetatively
not been documented (Taylor 1989). means of propagation that does not prolific lake cress (N. aquatica) have
Sexual reproduction in other species involve genetic recombination" revealed surprisingly high levels of
is displaced by vegetative reproduc- (Abrahan:ison 1980). Therefore, interpopulational genetic variation
tion. Vegetative turions develop in widespread asexual reproduction in in this sexually sterile triploid.^ Ad-
place of flowers in Baldellia ranun- aquatic plants may have evolved as a ditional studies of genetic variation
culoides, Caldesia parnassifolia, and means of maintaining genetic uni- in clonal aquatic plant species are
in species of Echinodorus (Alisma- formity within populations (Les necessary to determine the degree of
taceae; Hutchinson 1975, Sculthorpe 1988a). In contrast to genetically genetic uniformity both within and
1967). diverse, sexually derived offspring, among their populations. Although
asexual reproduction can replicate the efficiency of vegetative repro-
Sexual reproduction in clonal
optimally fit genotypes and main- duction should typically result in
aquatic plants conceivably could also
tain coadapted multigenic polymor- populations that are fairly homoge-
decline due to the accumulation of
phisms (Les 1988a, Silander 1985). neous genetically, factors such as
somatic mutations that influence
In stable environments, the ability the immigration of genetically dis-
sexual function. Nevertheless, the
to clone superior genotypes by veg- tinct vegetative propagules can re-
actual causes of limited sexual re-
etative reproduction is arguably ad- sult in more complex variational
production need to be studied more
vantageous. patterns (Les 1991).
rigorously to determine how eco-
logical, genetic, and other factors Many aquatic plants, particularly Empirical documentation of natu-
interact (Barrett et al. 1993). those with widespread distributions, ral genetic variation in aquatic plant
Although sexual reproduction possess broad ecological tolerances populations exists for relatively few
may often fail in aquatic habitats, (Stuckey 1971). Wide ecological species. However, the available in-
many aquatic plants appear to be amplitude seems necessary because formation suggests that aquatic plant
capable of persisting entirely by veg- any changes in the water potentially populations are not altogether uni-
etative means. In the predominantly influence all plants in contact with form genetically. Isozyme studies
unisexually flowered family Hydro- it. Consequently, aquatic habitats indicate that submersed species are
charitaceae, several dioecious (male are less likely to provide "microsites" characterized by limited levels of
and female flowers on separate in which narrowly adapted geno- genetic variation, yet patterns of
plants) species have become weedy types may persist. Adaptation to genetic variation in emergent aquatic
even though only one sex had been dynamic water conditions is evident species are, as in terrestrial species,
introduced (Cook 1993, Hutchinson in widespread aquatic species such associated with breeding systems and
1975, Sculthorpe 1967). Specific as Lemna aequinoctialis and life histories (Barrett et al. 1993).
cases include Elodea canadensis (en- Lemna turionifera (Lemnaceae), Some aquatic plant species such as
tirely female in Europe), Egeria which can tolerate an extreme range Howellia aquatica (Campanulaceae;
densa (strictly male outside its na- of pH from 3.2 to more than 9.0 Lesica et al. 1988) and A. antarctica
tive range), Lagarosiphon major (en- (Landolt 1986). The adaptation of (Waycott et al. 1996) appear to be
tirely female beyond its native range), aquatic plants to pH extremes is not entirely uniform genetically, but
and H. verticillata (female in its surprising, given that diurnal pH other submersed aquatic species pos-
introduced ranges in southeastern variation within aquatic habitats sess substantial levels of genetic
United States and California). How- alone can exceed two pH units; pH variation (Barrett et al. 1993).
ever, these examples offer evidence change can be stimulated by photo-
Evidently, the level of genetic vari-
of only short-term survival. Once a synthesis of submerged plants
ability in aquatic plant populations
prolific pest in Europe, E, canadensis (Wetzel 1975). Once a species has
is influenced by many interacting
has ultimately shown significant broadly adapted to environmental
factors. Each aquatic plant species
decline (Cook 1993). The cause is extremes, vegetative reproduction
represents a unique, complex system
unclear, although ecological factors, assures that all future offspring will
of interacting life-history traits re-
including nutrient deficiencies, have possess the appropriate genotype for
lating to particular reproductive,
been suggested. Whatever the rea- surviving whatever conditions may
dispersal, establishment, and survival
son for its decline, the case of E. be encountered during dispersal to
requirements (Waycott and Les
canadensis indicates that exclusive new habitats (Les 1988a).
1996). Two monoecious, water-pol-
vegetative reproduction in water
linated species, Zoster a marina
plants may be insufficient to facili- However, the hypothesis of ge-
(Zosteraceae; a monocot) and
tate long-term adaptation to varying netic uniformity is problematic. Al-
Ceratophyllum demersum (Cerato-
environmental conditions, particu- though cionally derived offspring are
phyllaceae; a dicot), provide a good
larly under dynamic selective re- usually assumed to be identical ge-
gimes. There is evidence that limited netically to their parents, somatic
sexual reproduction in adventive mutations can evidently generate sig- 'D. H. Les and J. D. Gabel, 1996, work in
nificant variability in asexually de- progress.
818 BioScience Vol. 46 No. 11
Z. marina commonly reproduces
sexually and why different popula-
tions of this plant (which are founded
by sexual propagules) show greater
genetic cohesiveness than those of
C. demersum. Certainly, higher lev-
els of sexuality are expected in
aquatic species that rely on seeds for
dispersal. The pattern of genetic
variation between and within popu-
lations will contrast widely across
the wide range of tradeoffs between
sexual and asexual reproduction that
exists among aquatic plants.
Because vegetative reproduction
is prevalent in most aquatic species,
their life histories must be adapted
to at least some degree of genetic
uniformity. Still, it is difficult to
determine whether vegetative repro-
duction has evolved principally to
assure genetic uniformity or for some
entirely different reason, with ge-
netic uniformity as an inevitable
consequence. Even if genetic unifor-
mity were essential for aquatic plant
survival, it could be achieved via
either sexual or asexual means. A
shift to inbreeding by self-pollina-
tion could conceivably result in the
production of offspring that are as
uniform genetically as those pro-
duced by vegetative reproduction.
In any event, prolonged genetic uni-
formity seems unlikely for water
plants, given that the genetically
homogenizing effects of asexual re-
production can be offset by even
Figure 3. Suhmersed aquatic plants often possess highly modified vegetative sporadic sexual events that occur at
organs but retain flowers v/ith features similar to their terrestrial ancestors. some level in most aquatic plant
Detrimental contact of flowers with water is prevented hy a variety of contriv- species.
ances, (a) This typical specimen of Lobelia dortmanna from Connecticut shows
the exceptionally long floral stalks that extend from a completely suhmersed
rosette of basal leaves. These flowers do not differ in any fundamental way from Sexual reproduction
those of terrestrial Lobelia species, (b) Flowers of bladderwort {Utricularia
radiata) resemble those of the closely related terrestrial snapdragons Sexual reproduction by means of
(Scrophulariaceae). A series of inflated "spongy floats" helps to prevent the flowering, pollination, and seed pro-
contact of hiadderwort flowers with the water, which may disrupt their function. duction is a primary reproductive
The floats are modified portions of the highly dissected submerged stems, which
mode for terrestrial ancestors of
contain bladders that trap small organisms for nutrition. Bar = 1 cm.
aquatic plants. Although a shift from
sexual to asexual (vegetative) repro-
contrast. The incidence of sexual ferentiation and higher sexuality in duction is often associated with the
reproduction is much higher in Z. Z. marina may reflect dispersal evolution of aquatic plants, a com-
marina (Laushman 1993) than in C. mechanism constraints. Although plete absence of flowering and seed
demersum (Les 1991). Overall, the both species are perennial, C. set characterizes only a few aquatic
levels of genetic polymorphism are demersum seldom produces seeds species (see above). The majority of
similar for both species, yet much and disperses largely by vegetative aquatic angiosperms retain the abil-
more variation exists between popu- propagules (Les 1991). In contrast, ity to flower and set seed and do so,
lations in the latter than the former. Z. marina spreads locally by rhi- albeit sometimes rarely (Sculthorpe
Multiclonal populations are also far zomatous growth (Laushman 1993) 1967). Sexual reproduction is obvi-
less common in Ceratophyllum but has no principal means of long- ously important to many aquatic
(Laushman 1993, Les 1991). Re- distance dispersal other than by seeds groups, although its exact role re-
duced among-population genetic dif- (fruits). This finding may explain why mains to be elucidated. Yet it is
December 1996 819
inappropriate to dismiss tbe impor- Pollen wetted by rain or water from wbicb are self-fertile, pollen tubes
tance of sexual reproduction in wa- anotber source becomes inviable due avoid contact witb water by grow-
ter plants. Tbe elaborate contriv- to premature germination or rup- ing internally tbrougb vegetative tis-
ances that preserve floral function in ture (Corbet 1990). Fvolutionarily, sues as tbey pass from male (stami-
aquatic babitats are unlikely to bave tbe pollination systems of aquatic nate) to female (pistillate) flowers of
evolved in water plants witbout se- angiosperms bave remained func- the plant (Pbilbrick and Anderson
lection to retain sexual reproduc- tional in several ways. Some floral 1992).
tion. Moreover, water-mediated organs bave adapted to avoid con-
cross-pollination (hydrophily) is tact with water. Other flowers bave Modifications to terrestrial pollina-
unique to aquatic plants and repre- acquired modifications tbat allow tion systems. Tbe widespread main-
sents perhaps the most divergent shift their terrestrial systems to function tenance of aerial flowers in aquatic
in angiosperm pollination systems. more efficiently in wet habitats. A angiosperms bas led to tbe premise
Because the evolution of pollination few species bave ultimately acquired that tbe aquatic environment exerts
systems bas been central in tbe suc- adaptations for water pollination little selective pressure on floral sys-
cess of angiosperms, tbe novel origin (hydropbily) in whicb pollen remains tems (Hutcbinson 1975, Scuitborpe
of bydropbily in water plants fur- viable and is transported in direct 1967). A closer examination of botb
tber implicates tbe importance of contact witb water. biotic (mainly insect) and abiotic
sexual reproduction in tbeir evolu- (wind, water) pollination systems
tion. reveals features tbat may be specific
Avoidance of water. Floral organs
adaptations to the aquatic environ-
The adaptation of angiosperm of aquatic plants avoid contact witb
ment.
sexual reproductive systems to water both directly and indirectly.
aquatic conditions must represent a In some aquatic species, dry repro- Flowers are disproportionately
difficult evolutionary transition. In ductive organs are maintained by biased toward wbite color in aquatic
many cases, angiosperms bave ac- modified flowers tbat close and en- plants (Scultborpe 1967). We calcu-
quired complex vegetative adapta- trap an air bubble when pulled be- late tbat wbite flowers occur in ap-
tions to aquatic babitats but bave low the water surface. However, proximately 43% of all aquatic gen-
retained tbe aerial floral systems of many aquatic plants overcome tbe era (40%ofdicots,48% of monocots;
terrestrial plants. Floral systems of detrimental effects of water by pre- based on data in Cook 1990). The
aquatic plants are generally conser- venting tbe contact of aerial flowers higb proportion of wbite flowers in
vative and reflect their terrestrial witb the surface. This is often facili- water plants may enhance fitness by
heritage. Scultborpe (1967, p. 245) tated by modified leaves, brancbes, making flowers more conspicuous
wrote: "It is in tbeir [sexual] repro- and floral axes (Sculthorpe 1967). to pollinators. In tbe visible spec-
ductive phase tbat vascular hydro- Groups of floating leaves reinforce trum, dark flowers lack the contrast
pbytes betray tbeir terrestrial ances- aerial flowering axes in Cabomba rendered by white petals against the
try witb tbe greatest clarity." In and Brasenia (Cabombaceae), dark background of water or float-
bladderwort {Utricularia species), Nymphoides (Menyantbaceae), ing vegetation. Because wbite petals
tbe submersed vegetative organs are Potamogeton and Callitriche (Calli- are typically ultraviolet (UV) ab-
so bighly modified (Figure 3b) tbat trichaceae), some species of Poly- sorptive and water is UV reflective,
typical morpbological models of leaf gonum (Polygonaceae), and Ranun- white petals may also enhance con-
and shoot structure are difficult to culus. Tbe floral axis of Utricularia trast in tbe UV spectrum.
apply (Taylor 1989). In contrast, radiata (Figure 3b) is supported by
However, an alternative explana-
bladderwort flowers are aerial and radiating "spongy floats" (Taylor
tion for tbe frequency of white flow-
possess both a structure and range of 1989) composed of loosely packed,
ers in aquatic plants is that floral
pollinators similar to tbat of terres- air-filled tissue. In Hottonia inflata
pigments in botb tbe visible and UV
trial plants. Other aquatic plants in (Primulaceae), the flower stalk itself
spectra are under no selection in
whicb bigbly modified vegetative (peduncle) is inflated (Scultborpe
water plants. Angiosperms typically
structures occur in conjunction witb 1967). Swollen upper stems of some
possess yellow flavonoid compounds
aerial terrestrial flowers include Myriopbyllum species provide a simi-
that also serve as biochemical pre-
Megalodonta (Asteraceae), Limno- lar function (Crow and Hellquist
cursors to common floral pigments
phila (Scrophulariaceae), and Ra- 1983).
known as anthocyanins. Flavonoids
nunculus (Ranunculaceae).
are frequently lost in submersed tis-
Flowers of aquatic plants often
sues of aquatic plants (Les and
Tbe maintenance of pollination extend from the water surface on
Sheridan 1990). The white petals
presents a particularly critical prob- long stalks (Figure 3a). In Lobelia
may simply reflect a background bue
lem in wet environments. In most dortmanna (Lobeliaceae), aerial
tbat results from the loss or lack of
terrestrial and aquatic angiosperms, flowers project from tbe submersed
otber floral pigments. In eitber case,
transfer of pollen to stigma is dis- rosettes on stalks up to 2 m long.
white flower color would be bighly
rupted by contact witb water. Be- Nymphaea and Ranunculus pro-
convergent among water plants but
cause bydration is one of tbe first duce flowers tbat float at tbe end of
unadaptive. Fcological and pbylo-
stages of pollen germination on the long, resilient stalks that conform to
genetic studies of aquatic genera sucb
stigma (Ricbards 1986), contact witb surface motions and prevent tbe im-
as Ranunculus and Utricularia, in
water sets in motion a series of bio- mersion of flowers by waves.
whicb flower color varies among
chemical events at tbe wrong time. In some species of Callitriche,
820 BioScience Vol. 46 No. 11
species, could provide more mean- (release and capture of wet, water-
ingful insight into the significance of borne pollen), this abiotic pollina-
flower color in the aquatic environ- tion system entails structural and
ment. White can also be nonpigment biochemical modifications of aerial
related, as in the reflection of Iighr pollination systems and the com-
from the intercellular spaces of pet- plete abandonment of aerial flow-
als (Faegri and Van der PijI 1979). ers. The perception that hydrophily
The conservative nature of floral is a general characteristic of aquatic
form in aquatic species predicts that plants is grossly misguided. Fewer
water plants would share a similar than 130 aquatic plant species (less
suite of pollinators with terrestrial than 5% of aquatic species overall)
plants, yet there is little empirical in nine plant families (seven mono-
data to support this claim. Some cot, two dicot) are hydrophilous (Cox
aquatic organisms, such as fish, have 1993, Les 1988a, Philbrick 1991).
no apparent role in aquatic plant
The types of hydrophily have de-
pollination, but recent studies indi-
fied precise classification (Cox
cate that the pollinator pool of wa-
1993). Moreover, the literature re-
ter plants may include aquatic in-
lated to hydrophilous pollination is
sects. Aquatic insects are diverse
complicated by varying or vague use
biologically, and many have life his-
of terms (Philbrick and Anderson
tories tied directly to aquatic plants.
1 992; see Cox 1993, Les 1988a, and
The association between aquatic in-
Philbrick 1988,1991, for additional
sects and plants (flowers) is not typi- Figure 4. Ceratophyllum is a water-
discussions and references). Two
cally related to floral rewards as it is pollinated dicot with minute unisexual
general classes of hydrophily occur
in terrestrial plants. Most pollina- flowers. Pollen released underwater
in angiosperms—surface, two-di-
tors of terrestrial plants visit the from dehiscing anthers (a) must pass
mensional and subsurface, three-di-
through the water to a small opening in
flowers for collection of pollen and/
mensional—although distinctions
the side of the pistillate flower (b) to
or nectar. By contrast, aquatic in-
complete pollination. Ceratophyllum is between the types are not always
sects use flowers for mating, shelter,
an example of a species that carries out clear. Subsurface, or underwater,
protection from predators, and pos-
every aspect of its life cycle (except, pollination represents the most ex-
sible lairs for capturing prey. Aquatic
perhaps, dispersal) in complete sub- treme modification of pollination
insects make up varying proportions mergence. Bar = 1 cm. systems to rhe aquatic environment.
of the pollinator pool for several
In this type of pollination, the flow-
aquatic plant species. Two of the
ers are submersed in the water, pol-
four primary pollinators of Nuphar terrestrial anemophilous (wind-pol-
len is released underwater, and both
(Nymphaeaceae) species are aquatic linated) plants. Limnohium (Hydro-
pollen and stigma are functionally
beetles (Coleoptera) and flies charitaceae) and Brasenia are the
wet during pollination.
(Diptera; Schneider and Moore only known aquatic genera that have
1977). In Nymphoides, four of the seemingly shifted to an anemophil- Hydrophilous species occupy
six pollinators are aquatic insects ous pollination system subsequent freshwater, brackish (estuarine), and
(Diptera; Van Der Welde and Van to entering the aquatic environment marine environments. Most genera
Der Heijden 1981). In Cabomha (Cook 1988). that contain hydrophilous species
caroliniana, four of the five pollina- There is little evidence to suggest are small taxonomically (less than
tors are aquatic flies or bees (Hy- that anemophily in aquatic plants ten species). The largest hydrophil-
menoptera; Schneider and Jeter differs in any fundamental way from ous genus is Najas, with approxi-
1982). Aquatic insects such as these anemophily in terrestrial plants mately 40 species (Cook 1990). Phy-
may play an important part in the (Cook 1988). However, the trend logenetic analyses of the angiosperm
pollination of water plants and thus for anemophilous terrestrial species subclass Alismatidae (in which all
exert a unique suite of selective pres- of Callitriche to have pollen with a hydrophilous monocots occur) re-
sures on their floral evolution. significantly thicker outer wall (ex- veals that hydrophily has evolved at
ine) than related amphibious species least seven times.^ Including Calli-
It was presumably because of se- (Philbrick and Osborn 1994) may triche and Ceratophyllum (Figure 4),
lection in habitats disruptive to bi- represent the outcome of aquatic the only hydrophilous dicot genera,
otic systems that abiotic pollination selective pressures. Little additional hydrophily has evolved as many as
systems evolved in angiosperms information is available on aspects nine times in angiosperms. Although
(Whitehead 1969). If the aquatic of anemophily in aquatic an- the evolution of hydrophily is com-
environment is inherently disruptive giosperms. plex, this system represents a strik-
ing convergence of aquatic plant
to biotic pollination, abiotic polli-
pollination systems.
nation should predominate in aquatic Hydrophily. Hydrophily (water pol-
plants. Cook (1988), however, lination) represents a remarkable Hydrophilous pollination exhib-
showed that the incidence of wind
evolutionary departure from the
pollination in aquatic genera is only
pollination systems of terrestrial
^D. H. Les, M. A. Cleland, and M. Waycntt,
31%, reflecting their ancestry from
plants. In its most extreme form 1996, manuscript accepted for piiblication.
December 1996 821