16.4.2  Parasitic plants and carnivorous plants

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Many families of vascular plants have representatives which exhibit either parasitism and carnivory and, given the wide taxonomic separation between such species, various forms of these remark-able adaptive features must have evolved independently, and on numerous occasions over their evolutionary history.

Two examples will be considered. The first concerns mistletoes (Amyema spp.), hemiparasitic flowering plants which acquire water, nutrients and certain organic compounds by tapping the xylem stream of branches of their tree hosts by means of specialised feeding organs (haustoria; Figure 16.13A). The second concerns carnivorous plants (Drosera spp.; Figure 16.13B) which trap insects with mucilage-producing glands on their leaves. The same glandular tissue that secretes mucilage then produces extracellular hydrolytic enzymes (proteases, peptidases and esterases) which digest the protein and other degradable materials of the insect carcasses. The resulting solutes (e.g. amino acids, sugars, phosphorus compounds) are then absorbed. Each case offers distinctive patterns of plant nutrition.


Figure 16.13 (A) Mistletoe (Amyema miquelii) attached to a eucalypt host. Note swollen haustorium which forms a graft-like union with the host branch. (B) A carnivorous plant (Drosera barbigera) showing glandular leaves capable of capturing and digesting insects. (C) Flowers and young fruits of the mistletoe Amyema linophyllum. Note staggered reproduction, whereby fruits ripen sequentially over a long period and thus offer an almost continuous supply of food for the principal dispersal agenst, the mistletoe bird. (D) Photomicrograph of part of the haustrial interface between a mistletoe (M) and its host (H). A lumen-lumen bridge between a xylem vessel of the host and the xylem elements of the mistletoe is marked with an asterisk. (E) A stem-tuberous carnivorous species Drosera erythrorhiza collected near the end of a good growing season. This plant grew from a parent tuber that is now replaced in situ by a replacement tuber (RT). Extra nutrient capital that is acquired each season is deposited in daughter tubers that form at the ends of rhizomes (R). (F) The hemipteran Cyrtopeltis sp. that walks with impunity across sticky leaves of carnivorous plants to feed on insect carcasses the plants have captured. The host plant is Drosera gigantea. (Photographs courtesy J.S. Pate)

(a)  Mistletoes and host plants


Figure 16.14 Representation of uptake, transport and partitioning of  the phloem-mobile and xylem-tapping nutrient potassium (K+) between a tree host and a xylem-tapping mistletoe. K taken up from soil (1) moves to the host shoot (2) and across the lumen-to-lumen xylem continuities (7) and parenchyma (8) of the haustorial interface and thence into the mistletoe (10). K in the host shoot is then pictured as being retained in host biomass (MH), lost through leaching by rain (5), in organ shedding (5) or cycled back to the root via phloem (4). Similar accumulation (MP) and cycling (items 11-14) are depicted for the mistletoe but with no backflow to the host. The mistletoe runs at an 'excess' of K due to a higher rate of transpiration and markedly active absorption of K by parenchyma of the hasutorial interface. Foliage shed by mistletoes is still fully loaded with K. (Based on Pate 1995)




Mistletoes are essentially rootless plants whose mature shoots attach directly to their woody hosts by means of graft-like junctions (Figure 16.13A). Flowering of Australian mistletoes occurs over a long period and their fruits ripen sequentially (Figure 16.13C). Fleshy fruits are eaten and seeds distributed almost entirely by the Australian mistletoe bird (Dicaeum hirundinaceum). Defecating birds wipe the extremely sticky seed masses, only recently ingested, onto adjacent branches of the host tree. Birds obtain only a small nutritional reward from these seeds. They eat large quantities of mistletoe seeds which take less than an hour to pass through. Seeds germinate immediately and, if branch contact is successful, a root-like haustorial structure digests its way into the host’s xylem stream. Once established, a complex ever-enlarging graft union then forms with the host. Secondary growth of the mistletoe haustorium is closely aligned laterally and becomes fully integrated with that of the host branch. Lumen-to-lumen con-tinuities are eventually established at the haustorial interface between tracheary (xylem) conducting elements of the parasite and exposed xylem vessels of the host (Figure 16.13D). It is through these connections that bulk mass flow of xylem vessel fluids takes place from host to parasite. However, most of the haustorial interface consists of parenchyma cells which are apparently involved in selective, metabolically controlled uptake of host nutrients (Figure 16.14).

Growth and survival of xylem-tapping mistletoes depend upon maintenance of a negative gradient in leaf water potential across the haustorial junction between host and parasite. This gradient is maintained day and night in favour of the mistletoe essentially by the mistletoe transpiring faster than its host. This feature, combined with the higher osmotic pressure of mistletoe compared to the host, results in a mistletoe being able to obtain water even when its host is severely water stressed (Case study 15.4).

Rates of photosynthesis of mistletoes are generally less than those of their hosts and this attribute, combined with high transpiration rates, results in the parasite usually exhibiting poorer water use efficiencies than its host (fewer millimoles of CO2 fixed per mole H2O transpired). One consequence of this high intake of xylem fluid is that mistletoes become progressively much more enriched than their hosts with respect to certain nutrients, especially K (Figure 16.14). Studies of mineral balance of a mistletoe throughout a season (Pate et al. 1991a) have shown that mistletoes abstract more than sufficient nutrients to meet requirements for growth and reproduction. Running at such an excess, mistletoes drop their leaves when still fully loaded with nutrients, whereas the host is likely to show the reverse of this and engage in most efficient pre-senescence retrieval of key limiting elements such as N, P and K. Mechanisms underlying these very different mineral economies of mistletoe and host have been defined (Figure 16.14).

As a further corollary to fast transpiration and direct intake of xylem fluid, mistletoes derive significant amounts of C in the form of organic acids, sugars, amino acids and other organic solutes absorbed from the xylem of their hosts. This heterotrophic intake of organic solutes may meet from 10% to 62% of a mistletoe’s daily requirement for C, and thereby compensate considerably for their relatively poor photosynthetic performance. Such inputs of C may be especially important where mistletoes are sited in poorly illuminated positions well inside their host tree canopies.

Leaves of Australian mistletoes are generally soft and fleshy in contrast to the tough sclerophyllous foliage of most host tree species. Being potentially attractive sources of food for a range of insects and grazing vertebrates, mistletoes have developed a range of anti-nutritional defence systems rendering them unpalatable or even poisonous to all but a few co-adapted predators. For example, mistletoes of the genera Amyema and Lysiana contain high concentrations of toxic amino compounds such as tyramine and djenkolic acid. In some cases the poisonous compound in question is obtained already synthesised from the host xylem and merely becomes concentrated in tissues of the mistletoe (Pate et al. 1991b). In other cases biosynthesis of the protective compound takes place within the parasite, using raw materials imported from the host.

(b)  Carnivorous plants

Sundews of the genus Drosera are found in every major land mass of the world, but almost three-quarters of the several hundred known species are found in Australia. They typically inhabit nutrient-poor acidic habitats where their ability to capture insects or other arthropod prey confers advantage by supplementing sparse sources of soil nutrients. N supplied by digestion of insect protein is the most important benefit to be derived from a carnivorous habit, especially where a habitat is markedly deficient in N. Insects are, of course, also concentrated sources of other important nutrient elements including P, S and micronutrients. Nevertheless, a carnivorous habit is not obligatory because many insectivorous species grow successfully and reproduce in artificial culture when fed exclusively with inorganic sources of nutrients.

Studies on species of Drosera growing in natural habitats such as the highly impoverished sand plain soils of Western Australia have shown that artificial feeding of leaves with small prey organisms such as spring tails (Collembola sp.) or fruit flies (Drosophila sp.) promotes a measurable improvement in plant growth and reproduction, giving rise to concomitant increases in tissue concentrations of N, P and other key nutrients in plant dry matter (Karlsson and Pate 1992). Growth in nature may therefore be limited by availability of prey.

While proving that benefit does result from this carnivorous habit, a question remains as to how dependent these plants are on insect prey in their natural habitats. A direct way to test this would be to record each item of prey caught by a carnivorous plant over a whole growing season, total up the amount of N in the seasonal catch and then compare this amount of N with the total increment in biomass N made by the plant over the season. A study of this kind, conducted by Dixon et al. (1980), used clonal populations of the southwestern Australian tuberous sundew Drosera erythrorhiza (Figure 16.13E) and included an 15N-labelling pot culture study to determine the efficiency with which insect N was consumed by leaves. Over three-quarters (76%) of N from the 15N applied as labelled fruit flies was absorbed. Using this information, and corresponding data on the total N of the catch and of the total N increment of the clones in natural habitat, about one-sixth (16%) of N gained by the clone must have come from native prey.

Such an investigation is not only time consuming but unfortunately provides only one value for dependence on insect N in a single population of only one species in a specific season and at one restricted locality. A much more powerful approach, also applied to southwestern Australian carnivorous plants, is to utilise differences in natural abundance ratios for the two stable isotopes of N (14N and 15N; Section 3.5.5). Data for insects caught by a carnivorous species are compared with natural abundance ratios for N in dry matter of that species and in cohabiting non-carnivorous species.

Natural abundance ratios for 15N:14N are usually expressed on a relative delta scale (δ15N as ‰) where a δ value of zero represents the ratio of isotopes found in atmospheric N. Positive δ values for a sample then denote enrichment in 15N relative to 14N, negative values the reverse. To explain this application, suppose that N within an insect caught by a carnivorous species showed a δ value of +5‰, while that of the N in dry matter of the carnivorous species was +4‰ and that for non-carnivorous reference species growing purely on soil N in the same habitat was +3‰. Your conclusion, based on simple arithmetic, would then be that the carnivorous species had gained half of its N from insects and the remaining half from available sources of N in the soil. Soil δ15N value of the latter was assumed to have been monitored effectively using the neighbouring non-carnivorous reference species. Values obtained in such a study (Schulze et al. 1991), encompassing a range of different growth and life forms of southwestern Australian sundews, indicated values for dependence on insect N of approximately 50% across all species studies, but lower values for rosette than for erect and climbing species.

In a special segment of the above study δ15N values were assessed for (1) normal plants of Drosera erythrorhiza carrying fully glandular leaves and visibly active in catching insects, and (2) certain mutant plants which completely lacked glands and would therefore have been totally dependent on soil N. These mutants provided perfect reference material to compare with normal prey-capturing representatives of the species. The resulting comparison of δ15N values for three matched adjacent clones of glandular and non-glandular plants indicated proportional dependence on insects of 12.2%, 14.3% and 32.3% (Schulze et al. 1991). These values are in reasonable agreement with the earlier value of 16% for the same species in the prey-inventory study.

Finally, a particularly interesting bug, the hemipteran Cyrtopeltis sp. (Figure 16.13F), lives on a number of species of carnivorous plants native to southwestern Western Australia. This bug has the unusual ability to traverse glandular leaves of a carnivorous plant without becoming caught in that plant’s ‘fly paper’ surfaces. The bugs forage among fresh carcasses on leaves at night, hiding during the daytime in lower non-glandular parts of the shoot. Does such scavenging comprise the major source of nutrition for Cyrtopeltis sp., or, like many other hemipterans, does it feed principally on plant sap? Again, using natural abundance δ15N values, J.S. Pate and co-workers in Western Australia solved the problem by comparing δ15N values for freshly collected carcasses, the insectivorous plant (Byblis sp.) on which the insects had been caught, and adults of Cyrtopeltis sp. that were inhabiting the Byblis. Cyrtopeltis sp. showed δ15N values in the range +4 to +6‰ (i.e. very close to that of the insect prey range 3–6‰) but several δ units more positive than that of the plant (+2 to +3‰). These δ15N values imply that Cyrtopeltis sp. is a carcass-scavenging non-vegetarian species, and only indirectly harmful to carnivorous plants by robbing them of nutritional substances from their insect catches, rather than drawing directly on plant sap.