Download Evolutionary action of tropical animals on the reproduction of plants

Biol. J . Linn. SOC.,1, pp. 85-96
April 1969
Evolutionary action of tropical animals on the
reproduction of plants
L. VAN DER PIJL
Sportlaan 236, The Hague, Netherlands
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The value of structural characters should be assessed by their role in local reproductive
processes. Just as in genetics the abstract species has been replaced by the population, the
functional contacts between animals and plants should not be considered on the species level
but in relation to the whole local ecosystem. Incidental cross-links therein are described as
leading to ‘concurrent evolution’ as a corollary. Inside the rain forest homeostasis is provided in
the vegetative sphere by pest-pressure, all-year germination and accidental replacement, but it is
especially strong in the reproductive sphere, by mutual collaboration in time, this via a feedback
by means of internal, permanent animal life. These circumstances explain the lack of vicariance
and the polymorphy, maintaining nevertheless normal interspecific selection. A comparison
with seeds, seedlings, flowers, etc., from temperate vegetation is illustrative. There, abiotic factors, edaphic and climatic, are dominant and the whole is more open to external influences.
Their anemochory (wind dispersal) and autochory (self dispersal) prove to be not fundamental
for plant-life.
In the tropics archaic dispersal methods (by fish and reptiles) of archaic, juicy, large
seeds (sarcotesta) persist in a conservative, homeostatic environment alongside modem
methods. Both lead to typically tropical traits and may serve to explain phylogenetic trends.
These are discussed for Leguminosae. The aril is a compromise suited for dryer regions, but
maintaining archaic attractivity of the seed-not yet the pericarp-fruit.
‘Bat-fruits’ provide a typical modem touch.
Archaic pollination-methods (for example by beetles and simple flies) are bound to the
ecosystemas a whole, which provides subsistence. Deceptive cross-links (short-circuits) are here
more important than food for such unadapted visitors. The flowers probe instincts chemically.
Some flowers provide a brood-place, as in Ficus, which breeds its own wasps in an ancient relationship, allowingFicus to escape from the forest. Monophily (deceptive or not) is not necessarily
late.
The bond with other hymenopterans (wasps) arose also as an incidental cross-connection.
Later this developed into a fixed relationship with flower-insects. Orchids as active ‘ecological
parasites’ demonstrate the exploitation of pre-existing animal life.
The more modem impact of birds and bats is described in a synecological context, which
makes some parts of syndromes understandable. Case-histories are given to illustrate the interaction between dispersal and pollination, between functions and structures in seed (fruit)
and flowers. We see their clashes and the solution, always found, leading to permanently
necessary changes. Dispersal may be anticipated in apparently functionless (or supposedly
phylogenetical) floral characters.
Points from a pollination-syndrome may form preadaptations for a dispersal-syndrome
and vice versa. The calycesof oriental Ttifoliumspecies illustrate monospermy, and their capitula
the possible origin of these characters and the inferior ovary in the Compositae.
CONTENTS
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Tropical ecosystems
Reproductive processes in interaction .
Dispersal .
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Pollination
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Some case-histories demonstrating interaction after environmental changes
References
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TROPICAL ECOSYSTEMS
Knowledge of the syndromes of seed dispersal and types of pollination is essential
for the evaluation of the functional significance of structural characters. I attempt here
to contribute to the understanding of the ecological morphology of plant reproductive
organs. In this field, morphology represents fixed, or as it were fossilized ecology.
Complete ecology is synecology, In evolutionary thinking the abstract species has
been replaced by the population. It also seems necessary therefore to revise the study
of contacts between a plant and an animal species into contacts inside whole ecosystems, with concurrent speciation as a later corollary.
A study of the special influence of animal life in the tropics starts in a sense with a
wrong concept. Life in the humid tropics has just not undergone the impoverishment
in forms shown elsewhere by plants and animals and caused by glaciation and aridity.
Tropical ecosystems, show, especially where moisture conditions are favourable,
the normal and basic spectrum of life, not an array of curious specialities. I n addition
to recent refinements this broad sample of life shows archaic states which have elsewhere disappeared. Its study is also of general importance as during Cretaceous times,
when angiosperms (angiovulates) radiated, tropical conditions were more widespread.
The rain forest with its strong homeostasis, that is maintenance of constancy of
the internal environment, allows an abundant animal life which in its turn enables the
plants to exploit it.
Such contacts do not necessarily represent direct, active, influence by animal
species or even co-evolution of individual species. Flowers and fruits may establish
links (short-circuits) with already evolved animal life and these may then develop
into narrow specialized connections. Life is a maze of cross-connections and feedback systems. Ehrlich and Raven studied the co-evolution of butterflies and plants
with regard to larval feeding; the food connections of the adults, however, cross such
links. A plant may be autonomous in its basic vegetative physiology but may be at
the same time dependent and active in the sphere of reproduction, probing the living
environment and influenced by it. This probing by flowers is often chemical and
chemo-mutations may thus be basic in considering speciation. Orchids do this, though
they remain uniform in their mode of dispersal, while grasses and Compositae remain
uniform in their pollination but specialize in exploring different means of dispersal.
I must here neglect the influence of tropical animals on the vegetative parts of the
plant, although this influence may be direct and active. For example, an absence of
ruminants in Australia has exterted a strong local influence; and pest-pressures must
have exerted a general one. The polymorphy in the rain forest and its derivatives
can be regarded as a protection against pest-pressure. Dense stands of any species
are thinned out by pests, the vacant places becoming occupied by other species. This
provides homeostasis vegetatively.
This polymorphy has been assigned to the absence, or weakness, of the struggle for
life between related species (cf. Fedorov, 1966), but the real background may be
found in the common bond with pollinators and dispersers subsisting on related
species which follow separate rhythms in time, often spread over the years (cf. Snow,
1962). This means mutual avoidance in time reproductively, but also coherence and
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collaboration. The constant presence of the necessary animals in a self-supporting
system is thus provided. In contrast with temperate vegetation many factors decide
what species shall grow and where, so ensuring a permanent equilibrium. Permanent
and rhythmic germination can also mask competition. So can the different requirements in different phases of one plant and of different layers in the vegetation.
In temperate vegetation we find less homeostasis and simpler competition; also
a stronger influence of external abiotic factors, such as the wind, on reproductive
processes; a limitation in number and size, as well as to certain periods, of zoochorous
(animal-dispersed) fruits ; absence of specialized fruit-eaters ; only temporary change
to a fruit diet by animals; and absence of flower-feeding vertebrates.
In secondary tropical forests, a parallel type of pioneer vegetation, we already see
a move towards these characters. Here there is quicker dispersal, stronger dormancy,
germination in light, independence of the biosystem as a whole, and a stronger
influence of those pollinators which are independent of the whole ecosystem. This is
in contrast with the rain forest proper, where fruits are mostly fleshy and seeds
mostly large and non-dormant, germinating immediately and in shade, awaiting
as seedlings an opportunity for further growth. Large seeds may, of course, have
other ecological backgrounds.
The anemochorous (wind-dispersed) component in the rain forest comprises mostly
top-storey trees, tall lianes, and epiphytes. Some trees of the genus Vmoniu are recent
intruders adapted and adopted by their capacity to germinate in shade. In tropical
forests under marginal edaphic conditions physiological competition leads to that
dominance by one or a few species which is considered normal in Europe.
REPRODUCTIVE PROCESSES IN INTERACTION
Factors influencing pollination and dispersal must be analysed separately, but there
is much interaction, often neglected.
Characters of the flower may exert a residual, often functionless influence on the
fruit, and conversely, characters affecting dispersal may be anticipated in the flower,
though they are there without function or morphological significance. There is no need
to describe the strange calyces seen in the flowers of some Labiatae, which will
later become functional in the fruiting stage. Vascular bundles in the outer integument
of the ovule may be no more than precursors of their later function in a fleshy sarcotesta.
Though it may seem descriptively redundant and though there is interaction, a
functional distinction should be made between monovuly in the flower and monospermy in the fruit. Monovuly is mostly functional in wind-pollination of the flower
and is connected with a poor chance of multiple pollen deposition on the stigma,
Monospermy is functional in the fruit, either for zoochory or (with indehiscence)
connected with dispersal by water or wind, or merely to ensure enlargement of
the seed. Characters, both evolutionarilyanticipatory or residual, can become important
as preadaptations to be utilized in a sphere of life to which they were not originally
connected. The use of the wrong term obscures insight into the function of angiovuly,
the sexually important enclosure of the ovules, usually designated angiospermy. It is
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also possible to envisage a clash between the two functions, leading to difficulties
in survival in a changing environment. I have previously postulated such a clash
between the sexual fixation of megaspore plus prothallus inside the sporangium and
dispersal in the pteridosperms. In a later phase of evolution a clash may also have
occurred between original angiovuly in the flowering phase and consequent angiospermy, disturbing the original mechanism of seed-dispersal by animals as already
evolved and still seen in tropical gymnosperms. Traces of this clash and the ways in
which it has been resolved are still present in lower families in the tropics, The solution
was sometimes by means of secondary structural devices, sometimes secondary
gymnospermy, sometimes direct monospermy, or sometimes passive or irregular
dehiscence of the enclosing capsule.
DISPERSAL
Dispersal rarely attains the precision and specificity of pollination, although sometimes there are not only specific agents, but the requirements of a special substrate are
also built in. Diplochory (dispersal by more than one means) and co-ordinated dispersal
tend to establish at once new ecosystems. Thus I have demonstrated that many
Malesian shore plants are dispersed both by sea and by bats. The apparently difficult
question: ‘Which were there first on islands, fruit-bats without fruit or bat-fruits
without bats’, can now be answered by accepting the second alternative.
Dispersal has an effect on genetic exchange and on speciation.
I deal first with seed dispersal, although this really comes after flower pollination.
Historically, however, seeds were present before real flowers. Pteridosperms and
gymnosperms had nude megasporangia and their ripe seeds were swallowed by
animals. Nowadays Cycadaceae, Ginkgo, Podocarpus and Cephalotaxus still have large
juicy seeds with a sarcotesta, and there are also some gymnospermous relics in ‘angiosperms’.
The original agents of dispersal must have been vegetarian fish and reptiles. Many
primitive angiovulate plants in the tropics show traces of this link, particularly in
undisturbed regions such as Borneo and Amazonia. It should be remembered that
much of the latter area is subject to regular inundation. The fruits of some Dwio
species in Borneo have been called ‘impossible’, because they are coloured, they fall
at maturity, and they have poor dehiscence, although provided with a swollen, edible
arilloid. Some of these fruits are borne at the base of the trunk. They seem to show
a syndrome of characters stemming from the age of reptiles, although the latter are
now largely, but not entirely, supplanted. A number of such seeds are used as fish
bait, including those of Inga where the primitive pods fall without dehiscing and
where the dispersed nude embryo points to a watery environment at its initiation.
I have asked, without result, many South American institutes to look into the fate of
seeds inside the fish.
Perhaps it is not an accident that such basicarpy and basiflagellicary are found only
in less advanced groups of plants with primitive fruits. The term geocarpy is too
indefinite in this connotation.
In more recent times a divergence has occurred from the reptile-dispersal syndrome
towards adaptation for that by birds, with an emphasis on colour, and for mammal
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dispersal with an emphasis on smell. In some genera, Ficus, Stelechocarpus, Dun’o
and Ingu, the three conditions persist: probably also in Juglans, Rosaceae, Degeneria,
and palms like Zuluccu, the latter two examples also having seeds with a
sarcotesta.
Certainly the old theory of Sernander, maintained in textbooks, that anemochory
(wind-dispersal) is the basic method, is fundamentally wrong. Originally seeds had
a large, autonomous prothallus inside; later on, a small, triggered, secondary endosperm, thus also avoiding the wastefulness of a prothallus near an unfertilized ovum
(as occurs in many gymnosperms). The large nude seeds maintained their sarcotesta
outside. We can only guess how large, dry, coniferous seeds with a reduced sarcotesta
were originally dispersed. In some species of Aruucuriu and Pinus they are still hidden
in a cache by animals and partly germinate into thickets. Small wind-dispersed seeds,
here too, represent a derived condition.
The next stage, now under angiospermous conditions, we find in the tropics, with
dehiscent fruits and exposed seeds which retain the sarcotesta. In many Ranales,
Liliiflores, Euphorbiaceae, Leguminoseae etc, this is an adaptation to ornithochory
(bird-dispersal). I n other plants the sarcotesta can remain covered by the pericarp,
thus being more suitable to mammals. Both of these archaic fruit-types are lacking in
Europe.
The next stage in morphological and ecological progression is the ‘arillate’ seed
well known from Corner’s Durian Theory, which, however, neglected the phase of
reptile dispersal, gymnosperms and the sarcotesta. Ecologically, aril-like structures or
arillodes-localized outgrowths of the testa-are a compromise between the juicy,
non-dormant sarcotesta and the requirements of dormancy and hardening. This
type is fitted to regions outside the humid forest.
Corner (1949) has already indicated the limitation of arillodes to primitive families.
Their presence in tropical members of the Papaveraceae, coupled with ornithochory,
supports the chemotaxonomic classification of this family in the neighbourhood of
the Ranales.
The red tropical ‘coral-seeds’ (Abrus) form a small but conspicuous group,
deceiving fruit-eating birds. They illustrate the principle of ecological parasitism so
common in ecosystems and occur in groups with a sarcotesta acting as a model.
Autochory is here an exception and it is illogical to start with it in textbooks. From the
comparative spectra of dispersal in different regions, it can be concluded that it is a
method particularly useful for pioneers in arid regions, often combined with derived
epizoochory. Autochory occurs in tall tropical leguminous trees with large seeds which
are without special mechanisms of dispersal, although it mostly occurs in weeds.
At the end of evolutionary lines in primitive families, and in all advanced families,
the attractive part of the fruit has changed to the pericarp, now at last playing
an ecological role, the old primitive attractiveness of the seed being suppressed.
Initially, only the inner part of the pericarp was involved, as a pulpy endocarp. Many
leguminous follicles, for instance in Cumiu, are attractive in this way, especially to
ruminants. Purely pericarpal, leathery pods are dispersed likewise.
Tropical Loranthaceae reach, as parasites, the floral refinement in dispersal already
mentioned. They achieve specificity in dispersal by close links with flower-peckers
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(Dicaeidae), which also visit their flowers. The seeds are deposited on their specific
substrate, viz. tree branches, or (in the case of hyperparasitism) on the branches of
other Loranthaceae.
Birds may show specific preferences and influence distribution specifically, also
according to size and biotope. Tropical representatives of animal groups may differ
from the temperate ones in their choice of food. Fruit-eating pigeons and rodents
are examples of this. Carnivorous mammals and birds (vultures) may be attracted by
tropical oil-fruits. Such incidental cross-connections (short-circuits) may again develop
into concurrent evolution of new lines.
Tropical fruit-bats are recent but important agents of dispersal over a limited
range, and I have described the syndrome of their fruits in a monograph (van der
Pijl, 1968). Large fruits and seeds are typical features, as well as lack of colour, a
smell resembling that of fatty acids, and an ‘outside’ position of the fruits, i.e. clear
of the foliage, the fruits thus being accessible to the visiting bats. The typically
tropical arrangements of caulicarpy and flagellicarpy are also explained by relationships with bats. Sometimes even certain seeds, of Swurtziu species for example, are
flagellispermous. The open-leaved pagoda-like shape of the crown of some other
trees shows adaptations in this direction, and certainly so when it is confined to the
female tree only as in Chlorophoru. That caulicarpy is an ecological adaptation is also
evident from its various anatomical origins. There is also much interaction with cauliflory. Typical smells may arise out of precursor-substances, already present in certain
taxa.
Ants are also newcomers. Their influence on tropical flowers is a destructive one
and flower-scents often act as repellants against them. The part they play in dispersal
in the tropics is strangely small when compared with Europe. It can be an important
one in such specialized ant-plants as some ant-epiphytes. This new connection with
ants has caused evolution of elaiosomes even from fern sporangia-organs which
have remained unchanged in general structure through geological time. Change of
position and new structures of the flower caused in anticipation by myrmecochory
are more frequent in the spring-flora of northern regions. Many elaiosomes found in
Europe are, however, reduced remnants of tropical sarcotestas and arilloids. Recent
biosystematic work by Berg and Bresinsky indicated taxonomic development on the
basis of recent change to ant-dispersal in woods.
A detailed discussion of tropical island floras and their speciation cannot be given here.
Carlquist (1966) recently produced interesting evidence linking dispersal, isolation
and adaptation to a new more stable habitat with open niches. The weak capacity for
dispersal found there nowadays is described as secondary ‘precinctiveness’.
Incipient speciation within a species is frequently seen when the diaspores are
spread to, or become adapted to, two different habitats. The dispersal by more than
one method, already mentioned, is a means whereby divergence occurs. The speciation
of desert-plants has been influenced through adaptation to geocarpy, atelechory
(limitation of dispersal) and to synaptospermy (non-disjunction of diaspores). The
distinction between appliances for dispersal and germination is often not a clear one,
but I cannot discuss this in detail here.
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POLLINATION
It has been doubted whether specialization of the flower is in fact necessary, the
assumption being made that generalized flowers are those which are most efficiently
pollinated. This assumption neglects qualitative aspects.
Diversification within a family has been described by van der Pijl & Dodson (1966)
in the Orchidaceae, and in the subtropical Polemoniaceae by Grant. Grant even found
instances of reversion to beetle-pollinators (cantharophily) accompanied by aggregation of the flowers and reduction in their size. Grant furthermore emphasized the
synecological necessity of diversification; the distribution of groups of species over the
different pollination classes was equal in different, comparable regions, but a difference
in proportions occurred in different climates. Sometimes a local bee population proved
insufficient for the population of a plant species, and this must have caused competition
for pollinators and encouraged specialization and speciation. For orchids pollinatorspecificity has been proved as a major factor accounting for distribution and speciation.
In tropical pollination, too, we find archaic features jogether with the refinements
connected with specialized tropical animals. Originally this concerned the transport
of fern-spores, perhaps partly eaten by beetles. These are likely to have been the
only group of insects present and suitable before the evolution of real flowers and
they could switch to pollen, as they do in higher gymnosperms. The original angiovulate flower seems also to have already abolished the transport of its spores by wind.
Archaic features are preserved among the tropical cycads which often have beetles
living semi-parasitically on them. They also occur in primitive flowers of the order
Ranales (Annonaceae, Magnolia, Eupomatia, Calycanthus), and in Arales and Cyclanthaceae. Such tropical flowers may produce strong fruity or aminous smells at night.
The beetles concerned are not flower-visitors but are often attracted specifically by
odours deceptively imitating those of their normal substrates. In the family Araceae
beetles and flies are attracted by a smell of dung or decaying meat. It would be interesting to ascertain the normal substrate of the pollinating beetles caught in the flowers
of Victoria waterlilies. Deception seems as usual a method of attraction as the provision
of food, and this is employed again in a very refined way among the orchids. The
flies and bees so deceived show no parallel evolution with the flowers they visit,
which often belong to advanced families of plants. Pollination here involves the whole
ecosystem, which has to provide the real food. The plant may provide a breeding
place for the visiting insect (as in Ficus), an archaic occurrence in the tropics. Thrips
may also have played a role in this respect.
The situation is somewhat misrepresented in textbooks, Davis & Heywood (1963)
for example, by an assumption that the first flowers were subject to promiscuous visits
and that monotropy (limitation of an insect species to one flower) and monophily (of
a flower to one species of visitor) only came later. These two principles are, however,
ancient and basic. Chemical specificity reacts with an ancient sensitivity to specific
chemicals, and speciation so caused is not recent.
Pollination by beetles (cantharophily) is ensured by devices falling into two classes :
(1)small flowersin dense spikes or flat umbels (Arales, Fagales, primitive Compositae) ;
and (2) larger flowers with special devices, often protogynous. Dr Gottsberger is now
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studying this aspect of Monimiaceae in Brazil. Grant, considering the question of
inferior ovaries, has indicated the dangers of visits by beetles, counteracted by
inferiority.
More recently some beetles have become specially adapted for feeding on flowers
and these are found now even in Europe both on open flowers and inflorescences
bearing nectar or pollen, thus falling into a different class from the point of view of
pollination. These could induce the secondary development of flowers specialized
for beetles. This is seen in the proteaceous plant from South Africa, Leucadendron
discolor, where the inflorescence is condensed into a structure forming a perfect
parallel with Magnolia; Dr Melville might consider this in his concept of the flower
of Magnolia as a product of condensation.
The most primitive Hymenoptera were not as yet adapted for visiting flowers
and, if they took nectar at all as adults, they took it from vegetative organs, extrafloral
nectaries for example (present in ferns), and these served for their subsistence. In the
tropics this sort of feeding and secretion occur frequently. Only later a shift in emphasis
towards the flower arose. T h e anxiety to find the first flowers without flower-insects
is not material and the usual solution ‘concurrent evolution’ is redundant in this
phase. Parasitic wasps require insects as larval food, which binds their flowers to the
whole ecosystem. Wasps, like those which pollinate figs, were already specific to
individual flower and insect species. Davis was wrong in assuming that this archaic
relationship is a recent development.
Solitary bees developed as regular flower-visitors. It cannot be denied that, originally, the visits may have been promiscuous, but the present forms show oligotropy,
an instinctive specific bond. I must, however, give a warning that the term used by
entomologists, oligolecty, or specific pollen choice, does not necessarily imply specific
pollination; it may mean no more than theft of pollen and this has misled some biosystematists.
Solitary bees, by subsisting even as larvae entirely on flower-food, have become
reliable pollinators, and acquired greater independence from food found incidentally
in the ecosystem. They have been able to evolve plentifully in arid and temperate
regions. Some remain dependent as far as nesting materials are concerned, dung,
oils and resins. This explains the fact that tropical euglossid bees are attracted to
orchid flowers offering such substances. Orchids as ‘ecological parasites’ on the whole
ecosystem, by means of deceptive mimicry, often attract both primitive and advanced
insects which have evolved on other flowers offering genuine food. Some orchids
even deceive stinging parasitic wasps with a pseudo-insect stung like a prey. Orchids
are not the passive, influenced partners in their relationship with their dupes.
Ficus was able to live outside the rain forest by breeding its own specific pollinators
(also parasites).
Social bees attained better independence of the total ecosystem, became bound to
flowers only but to none in particular (secondary polytropy), but this bond attained
the necessary specificity by their ‘constancy’ (temporal monotropy). This provided
plants with a new basis for speciation. Some fine reviews on speciation (Baker, 1960;
Baker & Hurd, 1968) suffer from the neglect of differentiation between diverse flowerinsect bonds. I see no need to assume that the specialization in groups of higher
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taxonomic rank is of a fundamentally different type. Times, conditions, vegetations
and pollinators change, also the relative importance of telechory and atelechory, of
selfing and crossing. After fixation on one successful level of one organ, a new differentiation may become necessary, if only by changes in another sphere of life, as
sketched here repeatedly.
Baker (1960) and Fedorov (1966) consider that trees in stable forests differ from
the more versatile pioneers in temperate ones in that they maintain polymorphy by
means of inbreeding-connected with the diffuse dispersion of species members.
This statement needs substantiation since most information about inbreeding there
refers to montane cloud-forests, unfavourable to insect visits. A comparative review
of anti-selfing devices, such as dicliny, would be useful. The cases of orchids and
Ficus with their hundreds of diclinous species and strong pollinator-specificity are
warnings. The opinion of Fischer that competitive selection there works more
between individual plants and members of other species, neglects the competition in
the seedling stage inside clearings.
Typical traits of specialized tropical flowers are shown by those pollinated by birds
and bats for example. Both kinds of visitors exert a marked influence both by their
presence and by their ability to fill niches in the scheme of pollination. This occurs
although they show no monotropy and no constancy. Any influence on speciation
must be related to other factors in the life and structure both of the flowers and their
visitors, such as lengths of bills and tubes. I know only a few genera (Musa, Parkia)
where a number of sympatric species seem to be pollinated by bats. Their periodicity
may differ. Both bat-flowers and bird-flowers have evolved independently in many
existing taxa.
Bird-flowers
The syndrome of bird-flowers is well-known. They are most typical in tropical
montane regions where cold-blooded vertebrates are at a disadvantage. This is clearly
shown in the families Cactaceae and Orchidaceae. Although specialized flower-birds
take their protein from captured insects, very rarely from pollen (compare the first
Hymenoptera), they require as adults a constant supply of nectar. In the tropics many
groups of birds have developed a line into this niche, some being still in a transitional
phase. In Europe traces of such early links are scarce, and a constant supply for nectar
specialists is out of the question. Gradual, temporal immigration into Europe (as
occurs in North America) is hindered by sea and desert.
The botanical interest lies in the feed-back from birds on later flowers.
The typical colour of bird-flowers is red, with ‘parrot colours’ next in importance.
These may act directly on the senses of the birds, or may, according to Grant &
Grant (1968), act synecologically in lowland tropical and in temperate zones. In the
latter, red may be the only possible common signal left for bird-flowers in a vegetation
full of other colours. The presence of perches is a diagnostic character for birdflowers in the Old World. Specializationtowards bird-pollination through the presence
of red or hard tubular flowers, or profusion of nectar, can originate from characters
in the syndrome for other methods, The flowers of Tropaeolum majw, unlike those of
related but more advanced species, are adapted to visits by birds through their colour
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and broad spur, but nevertheless still retain the smell and fringe indicative of mothpollination.
The reduction of the lower lip in many tropical Labiatae does not point to a
common origin or to blind repetition, but to convergent ornithophily. Many other
similarities remain puzzling to taxonomists who do not consider tropical ecology (cf.
Good, 1956).
Bat-flowers
Flowers adapted to visits by bats have become so adapted recently in geological
time. The adaptation could have occurred via various syndromes, provided that the
typical smell of fermentation is present (or could have arisen from precursors) and
that the position of the flower is suitable. The first transition may have been stimulated by fruit-bats, which also like nectar but are less specialized and adapted than
true flower-bats (Macroglossidae). Fruit-bats have persisted in their visits to batflowers providing solid food. Flower-bats rely on flowers even for their protein supply
in the form of pollen. A description of the bat syndrome would be a repetition of the
one described for bat-fruits, though an abundance of nectar and pollen should be
added, and also a tendency to open at night. In some cases there exists an interaction
between the flower and the fruit, especially between the cauliflorous and caulicarpous
and the flagelliflorous and flagellicarpous positions. In Musa and Sonneratia both
flowers and fruits profit from bats.
A number of flowers are intermediate in their development between bat- and birdflowers.
As bat-flowers are rare, to maintain the food system there must be synecological
links in time of flowering between the plant species of one region. Fruit-bats can
bridge such gaps. In the Southern United States immigration of flower-bats can
bridge the time-gaps for Agave and Curnegiea (already naturally cauliflorous). The
projecting inflorescence of Agaoe is no longer miraculous.
Specialjlower-classes
There are a few special flower-classes in the tropics which are of minor importance,
though producing typical traits. One example is provided by the Xylocopa-flowers
with ant-guards and protected flower-bases, and (in Leguminosae) resupinate flowers.
Unspecialized flowers are often 100% punctured by Xylocopa (carpenter-bees).
Recently van der Pijl & Dodson (1966) have pointed out a resemblance between
certain orchids (Oncidium species) and Malpighiaceae inhabiting the same region.
Both are visited by females of Centris species (Hymenoptera) which collect oils from
both. The narrow claws shown by the petals of Malpighiaceae are no longer just
oddities when we see that an attractive oil (sometimes nectar) is secreted on the
calyx-tips alternating with the petals.
SOME CASE-HISTORIES DEMONSTRATING INTERACTION AFTER
ENVIRONMENTAL CHANGES
Having discussed pollination and dispersal and the way in which their needs have
been mutually opposed historically, it is necessary to consider in more detail some
ACTIONOF ANIMALS
ON PLANTS
95
instances of interaction in the past in order to reach a synthesis. Let me first take the
case of Quercus and Castanea, which are essentially tropical forest genera though they
are already somewhat tolerant of low temperatures. They have, accordingly, indehiscent
fruits with large seeds and only weak dormancy. Their poor dispersal mechanism,
which is, however, sufficient for even distribution, seems to be by means of rodents
which are dyszoochorous. These genera clearly show monospermy, whereas traces of
polyovuly persist in the flowering stage, and monovuly is not functional in the flowers,
as these are entomophilous. They are pollinated by beetles and flies, are scented, and
arranged in dense erect spikes in most subgenera (new genera) of the old genus Quercus.
These genera by reason of their preadaptations have managed to escape from the
tropics and invade more windy, temperate zones. Some sections of Quercus s.I., and
the whole genus Castanea, have remained in some degree entomophilous with erect
flower spikes. T h e flowers already show some characters of the later anemophilous
syndrome : unisexuality, small size of flower, long styles and secondary monovuly.
'The erect male spikes of tropical Quercus species were replaced in the north by pendant
catkin-like inflorescences, in this way becoming adapted to complete anemophily in
a new region.
Dispersal could be carried out locally by squirrels living entirely on nuts capable
of being stored in the winter. Distant dispersal for pioneering purposes could take
place by the fortunate presence of nut-collecting birds, which previously lived on
large pine seeds and which have been seen to transport acorns over a distance of some
kilometres. A synecological prerequisite is the presence of coniferous forest as a
primary biotope and source of food.
Similar reorganization can be imagined to have taken place in other genera. I n
Juglans it has been from a reptilian-dispersed drupe which is still dropped on to the
ground. Other genera have become particularly adapted to wind dispersal.
In taxa (including genera such as Quercus) possessing pendant catkins the question
is again raised: convergence or common origin ?
Let us now consider the Compositae, in bygone times a terminal family. T h e
flowers, small and aggregated into heads, seem fixed by the original adaptation to
beetles. The main diversification happened typically by, or in, dispersal methods.
These exclude old endozoochory and suit pioneering in open vegetations and the
making of new biological contacts. The inferior ovary may be a floral adaptation
although its apparent monovuly is not, because the flower is entomophilous.
We must here also consider dispersal. Zohary and Burtt have already postulated
that in this family two distinct but interacting evolutionary trends may be distinguished,
based on pollination and dispersal respectively. This may have been valid in the
prehistory of the family. The transformation of the free calyx segments into bristles
or pappus for dispersal is already obvious in the flowering stage.
We must turn aside for a moment to consider some Leguminosae, leading up to
the genus Trifolium. I n the Leguminosae there is a main general trend in the development of the fruit, accompanied by many sidelines, as follows:
(1) a follicle containing seeds with a sarcotesta, for reptiles and birds;
(2) a follicle containing arillate seeds, for birds;
96
L.VAN DER PIJL
(3) a dehiscent legume containing many dry seeds;
(4) an indehiscent dry, one-seeded pod adapted for either endozoochory (to be
swallowed by ruminants together with the foliage under conditions of increasing
aridity) or serving for atelechory and synaptospermy under desert conditions.
A further fifth stage may follow. The fourth stage in both its aspects occurs in Trifolium though clearly not by the autonomous reduction to singleness so often postulated by supporters of orthogenesis. The flowers in Trifolium are aggregated for floral
reasons.
In many species of Trtfoliun. growing in steppes, secondary accessory organs of
dispersal have arisen, sometimes with the persistent calyx acting as the unit of dispersal. The calyx may then enclose the reduced pod and may even be constricted
above it, making the fruit inferior. In some species the free calyx-teeth have been
modified into epizoochorous spines and in others into a feathery pappus for anemochory. The whole picture thus form an almost perfect parallel with the evolution
of the achene in Compositae, though with one exception. When we see that Trifolium
already shows aggregation of the flowers and the presence of involucral bracts round
the heads, we should not excludethe possibility of a future family of ‘Papiliocompositae’
paralleling the Compositae themselves.
Now for the exception. Early anticipation of the inferior position of the carpel
through fusion of the calyx with the ovary was up till now impossible as the function
of the flower itself would be hindered because of the inaccessibility of the nectar.
In other families, including the Compositae to which we now return, this interaction
was possible because of an upward shift in the position of the nectary. Floral protection against beetles may have assisted in encouraging the inferior ovary.
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P. D., 1968. Intrafloral ecology. A . Rev. Ent. 13: 385-414.
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V. H., 1963. Principles of angiosperm taxonomy. Edinburgh: Oliver & Boyd.
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AN. A., 1966. The structure of the tropical rainforest and speciation in the humid tropics.
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*PIJL,L. VAN DER & DODSON,
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