Carnivory in Byblis Revisited II: The Phenomenon
of Symbiosis on Insect Trapping Plants
Siegfried Hartmeyer
Keywords: carnivory: Byblis, Drosera, Roridula.
Introduction
When people think of carnivorous plants, they mostly think that those
little "killers" catch and digest anything they are able to overwhelm.
However, carnivorous plants benefit many arthropods, including ants, true
bugs, small crawfish, mosquito-larvae and spiders. Furthermore, numerous
bacteria and fungi profit from the presence of the captured prey. In some
cases the benefit is through sheer robbery, for example when ants steal
the prey from a sundew trap. Other times, the ants live on the plant and
defend it from herbivores. As they go about their lives, the ants drop
mineral rich feces on the leaves or inside the pitchers. This is a case
of classic symbiosis in which both sides benefit by the partnership. (The
plant also benefits from the more rapid processing of prey into nutrients.
This deters fungal development, which is a considerable danger especially
for plants that use glue traps but that do not produce enzymes.) This
kind of symbiosis is exploited by the non-carnivorous tobacco plant (Nicotiana
tabacum) which has gluey regions that protect the plant from herbivores.
These zones are cleaned by resident true bugs (Engitatus tenuis).
An analogous cleaning symbiosis is well known from cleaning stations in
coral reef habitats, where specialized shrimp and fish clean parasites
off much bigger species.
Other relationships occur which are borderline-symbiotic. For example,
a small red crawfish (Geosesarma malayanum) raids Nepenthes
ampullaria pitchers. It uses its claws to crush and consume the drowned
prey in a wasteful way. The crushing speeds digestion, which compensates
for the loss of part of the prey. This situation would be a true symbiosis
only if the crawfish were specialized to coexist with the carnivorous
plant population.
It is necessary to understand the details of symbiosis because a new
discussion about carnivory in plants is beginning. This is important for
plants (perhaps even including tobacco) which use glue traps. The results
of recent investigations about the plant-arthropod mutualism in Roridula
gorgonias and about the enzyme production on Byblis liniflora
are discussed below.
Is Roridula Carnivorous?

Figure 1: Symbiotic bug on Roridula gorgonias. Photo by Matthias
Schmidt. |

Figure 2: Symbiotic bug on Roridula gorgonias. Photo by Matthias
Schmidt. |
Roridula is a South African genus containing two shrubby species
which bear stalked glands that produce an effective India rubber-containing
glue. The carnivorous status of species in Roridula has been debated
ever since Charles Darwin first suggested they were carnivores (1875).
Work by Marloth (1910) and Lloyd (1935) countered Darwins conclusions
because the sticky shrublets do not have the sessile glands that produce
proteolytic enzymes and which absorb nutrients (as does Drosophyllum).
Roridula was repeatedly shown to be unable to produce own digesting
enzymes, so it was theorized that these plants (that have the strongest
glue of all the insect-trappers) only benefited from the captured prey
when nutrients from the decaying prey washed into the soil. Capsid bugs
(Miridae) which live on the plants were postulated as representing another
loss to the plant because, astonishingly, they freely move on the plant
and steal the immobilized insects. Furthermore, some species of spiders
use their webs to avoid the plants glue and feed upon the Capsid
bugs and arthropods stuck to the plant. But in spite of all this, Darwin's
theory remained popular and Roridula continues to be grown by carnivorous
plant enthusiasts.
During 1991 to 1996 I raised two plants of Roridula gorgonias
in my living room in Weil am Rhein, Germany. They were 1.2 m tall, and
had a good population of Pameridea bugs. The bugs remained on their
host plant and only on rare occasions the adults used their wings for
a reconnaissance of our house (no persons were attacked!). On sunny days,
when I moved the plants to my balcony, the bugs did not try to escape.
During the winter I fed the bugs with beetle larvae from pet shops, and
in the summer the plants caught enough flies and wasps for the bugs. When
arthropods were captured in abundance, the bug population grew so large
the plant was nearly suffocated by their feces (in nature the bug population
is moderated by spiders. By feeding the plant in moderation, there were
fewer feces and they gradually became paler and paler until they practically
disappeared (this happened even indoors). One year the plants were so
vigorous they produced sixty beautiful pink flowers! This is documented
in my first English-language video (1994), in which I suggested it was
an example of a true symbiosis. I soon became involved in the heated discussion
regarding the carnivorous status of Roridula. I maintained that
Roridula is a true carnivorous plant even though
it does not have enzymes that can dissolve its captured prey. I think
the nutrition is not absorbed via soil fertilization but much more effectively
through the predigested feces of its Pameridea partners. I think
the definition of true carnivorous plants (that is, trapping of prey,
digestion of prey by proteolytic enzymes, and absorbing the nutrients)
should include the passive digestion by true symbiosis, as long as the
nutrients are absorbed.
Supporting evidence appeared in 1996, when Ellis and Midgley published
detailed and highly interesting examinations. They used a method developed
by Dixon et al. (1980), who traced the 15N nitrogen
uptake in Drosera erythrorhiza. Yeast was combined with ammonium
sulfate tagged with 15N, and this mixture was fed to fruit
flies (Drosophila melanogaster) for five days. Ellis and Midgley
tested plants in the field and in the laboratory, both with and without
Pameridea bugs present. The fruit flies were placed on the plants,
and eaten by the Pameridea bugs. Several leaves of the plants were
later removed, cleaned of impurities, and their 15N isotope
content was analyzed. The plants with resident bugs showed a clearly higher
15N content, particularly in newly formed leaves. This confirms
the Roridula-Pameridea symbiosis. Roridula seems to absorb
the feces via stomata, as do many other non-carnivorous plants. Roridula
clearly benefits from its captured arthropods more efficiently than it
would by soil fertilization. However, it is truly carnivorous?
Are Byblis and Darlingtonia Carnivorous?
Near Perth Australia, China (1953) reported Capsid bugs on carnivorous
plants, specifically Setocornis bybliphilus on Byblis gigantea
and two Cyrtopeltis species on tuberous Drosera.
Unfortunately, during our visit there in 1991, my wife Irmgard and I saw
no Capsids on B. gigantea, and the tuberous Drosera were
dormant. In May 1995, while filming B. liniflora near Kununurra,
North Australia for our latest video (1995), we immediately found numerous
bugs living on them. The similarity of their behavior to that of Pameridea
bugs on Roridula was amazing. Although they were a little smaller,
they had the same dotted pattern on their back (typical for the family
Miridae), the same appetite for the plants prey, and the phenomenal
ability to use the glue drops as a cooling agent without becoming entrapped.
We filmed a smaller Miridae bug on Drosera ordensis and two more
species on Drosera indica variants near Darwin.
Like mosquito larvae living in Nepenthes pitchers, I thought the
bugs we were observing must have some kind of defense against proteolytic
enzymes produced by the host plants. However, I discovered that bugs living
on Byblis liniflora may not require such protection. In a series
of simple experiments using photographic film to test carnivorous plants
for enzymes, I examined several Drosera species, Byblis liniflora,
and Roridula dentata (Hartmeyer, 1997). Enzymes were detected by
their ability to digest the gelatin layer of the photographic film. While
all the sundews were shown to produce enzymes (as expected), none of the
trials detected enzyme production in Byblis liniflora! Those plants
capable of digesting the gelatin protein on photographic film can also
digest animal protein. Conversely, a plant unable to digest the gelatin
layer on film is also unable to digest animal protein. Recall that Byblis
liniflora has sessile glands for nutrient absorption which Roridula
lacks. However, these results suggest the Byblis-Setocornis
mutualism (and probably also the Byblis-Cyrtopeltis
mutualism) may be much more similar to the Roridula-Pameridea
mutualism than previously believed. Although Bruce (1905) reported on
digestive enzymes in Byblis gigantea, the fact that none were found
in Byblis liniflora recently sheds serious doubt on the carnivory
of the genus.
Incidentally, enzymes are not produced by Darlingtonia californica
or some Heliamphora species. Are they not carnivorous? Carnivorous
plant enthusiasts need not despair--there is hope for their Cobra Lilies
and expensive Pitcher Plants. Both genera have symbioses with arthropods.
Along these lines, numerous associations between carnivorous plants and
animals are featured in a recent documentary (Carow, 1996). Just enlarge
the definition of carnivory to include this situation!
Conclusion
The production of enzymes should not be a prerequisite for a plant to
be considered carnivorous--a symbiosis with another digesting agent should
be sufficient. In the past, symbioses were mistakenly considered strange
exceptions, but now it is apparently a widespread syndrome with carnivorous
plants. Indeed, with some plants it is an integrated part of the digestive
system! All the plants commonly considered carnivorous but which do not
produce enzymes have symbioses with arthropods. I hope these new examinations
of Byblis liniflora and Roridula gorgonias trigger interesting
discussions on the subject.
Plant
|
Arthropod
|
Occurrence
|
Byblis gigantea
|
Setocornis bybliphilus
|
Perth, Australia
|
Byblis liniflora
|
Setocornis/Cyrtopeltis species
|
Kununurra & Cairns, Australia
|
Darlingtonia californica
|
Metriocnemus edwardsi.
|
USA
|
Drosera erythrorhiza
|
Cyrtopeltis droserae, C. russelli
|
Perth, Australia
|
Drosera pallida
|
Cyrtopeltis droserae, C. russelli
|
Perth, Australia
|
Drosera stolonifera
|
Cyrtopeltis droserae, C. russelli
|
Perth, Australia
|
Drosera indica varieties
|
Setocornis/Cyrtopeltis species
|
Kununurra & Darwin, Australia
|
Drosera ordensis
|
A tiny Miridae species
|
North Australia
|
Heliamphora
|
Several mosquito larvae
|
Venezuela
|
Nepenthes bicalcarata
|
Camponatus schmitzi
Misumenops nepenthicola
Thomisus nepenthiphilus
Mosquito larvae
|
Borneo
|
Various Nepenthes
|
Several mosquito larvae
|
Asia, Australia, Madagascar, Seychelles
|
Roridula dentata
|
Pameridea marlothii
|
South Africa
|
Roridula gorgonias
|
Pameridea roridulae
|
South Africa
|
Sarracenia flava
|
Sarcophaga
|
USA
|
Sarracenia purpurea
|
Wyeomyia smithii
|
USA, Canada
|
Table 1: Examples of plant-animal mutualism in carnivorous plants and
allies
References:
Bruce, A.N. 1905, On the Activity of the Glands of Byblis gigantea,
Notes Royal Botanical Garden Edinburgh, 16, 9-4.
Carow, T. 1996, Todesfallen oder Lebensspender? Die neue Sicht der fleischfressenden
Pflanzen (documentary film, English translation: Deathtraps and Lifelines),
In Radke R. (ed.), ZDF (German TV) Naturzeit English version
presented at the First Conference of the ICPS, Atlanta, USA, 1997.
China, W.E. 1953, Two New Species of the Genus Cyrtopeltis (Hemiptera)
Associated with Sundews in Western Australia, The Western Australian Naturalist
4 (1), 1-8.
Darwin, C. 1875, The Insectivorous Plants, London.
Dixon, K.W., Pate, J., and Bailey, W.J. 1980, Nitrogen Nutrition of the
Tuberous Sundew Drosera erythrorhiza with Special Reference to
Catch of Arthropod Fauna by its Glandular Leaves, Aust. J. Bot. 28, 283-97.
Ellis, A.G., and Midgley, J.J. 1996, A New Plant-Animal Mutualism Involving
a Plant With Sticky Leaves and a Resident Hemipteran Insect, Oecologia,
106, 478-81.
Hartmeyer, S. 1996, Insectivorous Plants and Entomology, Bulletin of
the Australian Carnivorous Plant Society, 15, 12-15.
Hartmeyer, S. 1997, Carnivory of Byblis Revisited--A Simple Method
for Enzyme Testing on Carnivorous Plants, Carniv. Pl. Newslett., 26, 39-45.
Hartmeyer, S., and Hartmeyer, I. 1994, Beautiful & Hungry--Carnivorous
Plants, private production.
Hartmeyer, S., and Hartmeyer, I. 1995, Beautiful & Hungry Part 2--Carnivorous
Plants, private production.
Lloyd, F.E. 1934, Is Roridula Carnivorous? Can. J. Res. 10, 780--786.
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