Chapter III.
ALLELOPATHY
Q. In my 55 gal tank with garden soil and good lighting I’m getting good growth of some plants but not others. The five Anubias nana and four Echinodorus cordifolius seem really at home. However, the Hygrophila polysperma and the Hottonia inflata are not doing well. The Hygro’s leaves are curled and starting to shed, while the Hottonia has developed a brown layer on some leaves.
I wonder if the temperature has any bearing on the brown I’m getting on the Hottonia? One book says the temperature range for this plant is 64-73°F. (I keep the tank at 77°F.)
A. I wouldn’t be too concerned about plant species that aren’t doing well in your tank, provided that others are thriving. It’s true that a plant species may not do well, because conditions aren’t right for it. Thus, your Hottonia may like cooler water and your Hygrophila may need more CO2 than the other plants.
However, the other plants in your tank may be secreting chemicals (‘allelochemicals’) that inhibit the Hygrophila and Hottonia. Allelopathy between plants may explain many instances of a particular plant species not doing well in a particular home aquarium. For example, Amazon swordplants, Anubias nana, Limnophila, and some Cryptocoryne thrive together in my 50 gal. However, I have not been able to grow any Vallisneria in this tank. Yet Vallisneria thrives in other tanks. I accept allelopathy between plant species as natural and inevitable.
Theoretically, allelopathy is the production and release of chemicals (‘allelochemicals’) by organisms into their environment that act on other organisms. Although some animals do produce defensive chemicals, plants and other non-motile organisms are the masters of chemical defense. Plants produce a wide assortment of allelochemicals that inhibit other organisms. For unlike animals, plants are not protected by their size, speed, and strength. Basically, plants must use chemical defense to protect themselves from disease and consumption by herbivorous animals [1,2].
It seems that plants have made a major investment in chemical defense. For allelochemicals are not waste products, because plants produce them at considerable energy cost. Plants divert the essential amino acids phenylalanine and tyrosine from protein synthesis to the phenylpropanoid metabolic pathway (Fig III-1) to produce phenolic acids, tannins, flavonoids, stilbenes, and lignins. Many of these compounds are allelopathic. The chemical structures of three common phenolic allelochemicals are shown in Fig. III-2. Gallic acid and caffeic acid are phenolic acids, while quercetin is a flavonoid.
Figure III-1. Phenolic Allelochemicals Come from the Phenylpropanoid Metabolic Pathway.
Figure III-2. Chemical Structure of Three Phenolic Allelochemicals.
Because allelochemicals could inhibit the producing plant if they are not stored and handled properly, allelochemicals require more effort than just their production. But the total cost of allelochemicals may be worth the price. Consider that a 10% metabolic investment by the plant in allelochemicals may prevent a 90% loss to herbivore grazing.
Allelopathy in the aquatic environment would be expected to have many random secondary effects. Although the primary action is between the allelochemical producer and the target organism, most allelochemicals are water-soluble, and thus, could influence other organisms in the surrounding water. In a closed environment such as the aquarium where allelochemicals could accumulate, allelopathic effects would be further increased.
A. Allelopathy in Aquatic Plants
Aquatic plants contain a variety of allelochemicals whose primary function1 is to protect the plant from being eaten by fish and insects or being destroyed by disease. In general, aquatic plants are considered to be more resistant to disease and herbivory than terrestrial plants [6].
Q. I can’t seem to get infusoria to grow. I put a jar on the windowsill with fish mulm for nutrients, some snails, and Java moss. Even though the jar gets sunlight and the moss is growing well, I can’t seem to get the green water that I need for infusoria.
A. Green water algae will have a tough time competing with a healthy aquatic plant in a small volume of water. The water is probably loaded with all kinds of allelochemicals that are preventing algae and infusoria growth. You need to remove the Java moss if you want to grow infusoria.
I think hobbyists see allelopathy as some kind of isolated, strange event, such as a possible reason for not keeping Vallisneria and Sagittaria in the same tank. The truth, though, is that allelopathy is pervasive throughout the plant kingdom. It is only recently that we (as humans) are recognizing how plants use chemicals to compete and protect themselves. I would assume that all aquatic plants, including Java moss, actively produce and secrete allelochemicals into the water.
Allelopathic behavior has been reported in 97 species of aquatic plants [7]. Indeed, when investigators tested extracts from 17 different aquatic plant species, all 17 extracts inhibited either duckweed or lettuce seedlings (Table III-1). Included in the two studies were common aquarium plants like Cabomba, Hornwort, and Vallisneria. The most inhibitory plant by far was the yellow water lily Nuphar lutea; which caused death (not just inhibition) in both duckweed and lettuce seedlings.
Table III-1. Toxicity of Aquatic Plant Extracts.2
| AQUATIC PLANT | % INHIBITION OF: | |
| Lettuce | Duckweed | |
| Brasenia schreberi (water shield) | 70 % | 60 % |
| Cabomba carolina (cabomba) | 50 | 60 |
| Ceratophyllum demersum (hornwort) | 60 | 30 |
| Eleocharis acicularis (hair grass, spikerush) | 100 | 50 |
| Eleocharis obtusa (hair grass, spikerush) | 100 | 10 |
| Hydrilla verticillata (hydrilla) | 50 | 30 |
| Juncus repens (rush) | 70 | 40 |
| Limnobium spongia (frog’s bit) | 60 | 40 |
| Myriophyllum aquaticum (parrotfeather) | 40 | 70 |
| Myriophyllum spicatum (Eurasian watermilfoil) | 50 | 50 |
| Najas guadalupensis (water nymph) | 60 | 50 |
| Nuphar lutea (yellow water lily)- tops | Death | Death |
| Nuphar lutea (yellow water lily)- roots | Death | Death |
| Nymphaea odorata (white water lily)- tops | 60 | 80 |
| Nymphaea odorata (white water lily)- roots | 80 | 60 |
| Nymphoides cordata (floating hearts) | 60 | 40 |
| Potamogeton foliosus (a pondweed) | 50 | 40 |
| Sparganium americanum (bur-reed) | 50 | 30 |
| Vallisneria americana (Val, tapegrass) | 70 | 20 |
Allelochemicals isolated from aquatic plants (Table III-2) have been shown to inhibit a variety of organisms (Table III-3).
Table III-2. Allelochemicals found in Aquatic Plants.
(FULL NAMES of compounds are shown in Table III-3.)
| PLANT SPECIES | ALLELOCHEMICAL and REFERENCE |
| Acorus gramineus | caff, F, pC, S [11]; a-asarone and 3 other polyphenols [12] |
| Aponogeton krauseanus | Km, pOHB, Qu [11] |
| Bacopa monnieri | nicotine [11] |
| Ceratophyllum demersum | caff, cg, Cy, F, S [11]; sulfur [13] |
| Eichhornia crassipes | cg, pC, protocatechuic acid, V [14] |
| Eleocharis coloradoensis | dihydroactinidiolide, F, Lu, pC [15] |
| Eleocharis microcarpa | 33 oxygenated fatty acids [16] |
| Elodea callitrichoides | cg, Cy [11] |
| Elodea canadensis | caff, cg, Cy, Qu [11] |
| Elodea crispa | caff, cg [11] |
| Elodea densa | caff, cg, Cy, Qu [11] |
| Hottonia palustris | Qu [11] |
| Lemna minor | cg, isoorientin, S, vitexin [11] |
| Myriophyllum aquaticum | cyanogenic compounds [17] |
| Myriophyllum brasiliense | G, tellimagrandin II, Qu [18] |
| Myriophyllum proserpinacoides | E, Cy, cyanogenic compounds, Qu [11] |
| Myriophyllum spicatum | caff, cinn, E, F, G, pC, protocatachuic, S, Sy, tannic acid [19]; tellimagrandin II [20] |
| Myriophyllum verticillatum | 3 phenylpropanes, 2 oxygenated fatty acids [21] |
| Nuphar lutea | 6,6’ dihydroxythiobinupharidine [22] |
| Nymphaea capensis | caff, cy, E, F, Km, pC, Qu, S, tannins [11] |
| Pistia stratiotes | caff, cy [11]; a-asarone, 2 fatty acids, linolenic acid, a sterol [23] |
| Posidonia oceanica | caff, F, G, pC, pOHB, pC, protocatechuic, V [24]; F, pOHB, pC, S [25] |
| Potamogeton species | Ap, isoorientin, Lu [3] |
| Potamogeton crispus | Ap, Lu [3]; rutin [11] |
| Sagittaria variabilis | caff, Cy, F, Km, Qu, S [11] |
| Spartina alterniflora | F, pC [26] |
| Stratiotes aloides | caff, Cy, rutin [11] |
| Thalassia testudinum | caff, F, G, protocatechuic, pC, pOHB, V [24] |
| Typha latifolia | 3 sterols and 3 fatty acids inhibitory to algae [27] |
| Ultricularia vulgaris | Cy [11] |
| Vallisneria americana | F, G, pC, V [28] |
| Vallisneria spiralis | caff, pC [11] |
| Zostera nana | caff, pC, tannins [11] |
| Zostera marina | caff, F, G, pC, pOHB, protocatechuic, V [29,24]; Ap, Lu [30] |
Table III-3. Allelopathy of Compounds found in Aquatic Plants.3
| ALLELOPATHIC COMPOUND | ORGANISM (or organ) SHOWN TO BE INHIBITED BY |
| a-asarone | algae and cyanobacteria [23,31] |
| apigenin (Ap) | mitochondria [32]; aphids [33] |
| caffeic acid (caff) | many organisms [34]; enzyme [35]; cyanobacteria [21]; marine slime mould [29] |
| chlorogenic acid (cg) | many organisms [34]; aphids [33]; fungus [14] |
| t-cinnamic acid (cinn) | many organisms [34] |
| cyanidin (Cy) | many organisms [34] |
| cyanogenic compounds | many organisms [1] |
| dihydroactinidiolide | radish and watercress seedlings [15] |
| 6,6’ dihydroxythiobinupharidine | lettuce seedlings [22] |
| ellagic acid (E) | many organisms [34]; enzyme [35]; nitrifying bacteria [36] |
| ferulic acid (F) | cyanobacteria [36]; nitrifying bacteria [37]; enzyme [35]; lettuce seedlings [38]; watercress seedlings [15]; snail [26] |
| gallic acid (G) | nitrifying bacteria [36]; enzyme [35]; Hydrilla tubers [39]; cyanobacteria [21,18] |
| isoorientin | bacteria (Nitrosomonas) [40] |
| kaempferol (Km) | many organisms [41]; mitochondria [32] |
| linoleic acid | algae and cyanobacteria [23] |
| luteolin (Lu) | radish and watercress seedlings [15]; aphids [33] |
| nicotine | aphids [1]; duckweed, bacteria, lettuce seedlings [42] |
oxygenated fatty acids: P. stratiotes M. verticillatum E. microcarpa |
algae and cyanobacteria [23] algae [21] algae [16] |
| p-coumaric acid (pC) | many organisms; [34]; cyanobacteria [21,36]; nitrifying bacteria [37]; lettuce seedlings [38]; enzyme [35]; radish and watercress seedlings [15]; fungus [14] |
| p-hydroxybenzoic acid (pOHB) | many organisms [34]; Hydrilla tubers [39]; enzyme [35]; lettuce seedlings [38]; aphids [33]; herb seedlings [43]; nitrifying bacteria [37] |
phenylpropanes: M. verticillatum A. gramineus |
cyanobacteria [21] algae and cyanobacteria [12] |
| protocatechuic acid | fungus [14] |
| quercetin (Qu) | many organisms [34]; aphids [33]; cyanobacteria [18] |
| rutin | aphids [33] |
| sinapic acid (S) | cyanobacteria [21] |
sterols: P. stratiotes T. latifolia |
algae [23] algae [27] |
| sulfur | algae [13] |
| syringic acid (Sy) | lettuce seedlings [38]; herb seedlings [43]; nitrifying bacteria [37] |
| tellimagrandin II | cyanobacteria [18]; enzyme [20] |
| tannic acid | many organisms [1]; nitrifying bacteria [36] |
| vanillic acid (V) | cyanobacterium [36]; nitrifying bacteria [37]; Hydrilla tubers [39]; lettuce seedlings [38]; herb seedlings [43]; fungus [14] |
| vitexin | aphids [33] |
1.Phenolics as Allelochemicals in Aquatic Plants
It is natural that phenolics (rather than alkaloids, etc) play a prominent role in aquatic plant allelopathy.4 This is because phenolics are part of the plant’s phenylpropanoid metabolism for synthesizing lignins, which give structural support to terrestrial plants and trees allowing them to stand upright. During evolution when land plants moved into the water to become aquatic plants, they lost their need for lignins, because water buoyancy provided the needed structural support. Thus, the lignin content was gradually reduced.5 Most submerged aquatic plants now contain little if any of the unneeded lignins, but they still contain the phenolic precursors of lignins [45,46].
The fact that the phenolic precursors of lignins mildly inhibit a variety of organisms was fortuitous for aquatic plants. Because the phenylpropanoid pathway was already in place, aquatic plants didn’t have to create a completely new metabolic pathway to make allelochemicals. Over the course of evolution, spontaneous mutations almost surely occurred that increased the inhibitory properties of phenolics already being produced. Indeed, one investigator [31] showed how simple chemical alterations of common phenolic acids could dramatically affect their inhibition of algae.
The higher the aquatic plant’s phenolic content, the less chance it will be consumed [47,48]. Plants containing more than 6% phenolics are considered to be indigestible and of little food value to herbivores. (Agricultural forage crops, which are developed for palatability, contain less than 2-3% phenolics.) The phenolic content of aquatic plants averages about 6% ranging from a low of 0.8% for Elodea densa to a high of 15% for Cabomba caroliniana [45].
Phenolics may also affect allelopathy between aquatic plants. For example, plant species (Nymphaea odorata, Brasenia schreberi, and Cabomba caroliniana) that contain the highest levels of phenolics [45,46] were found to inhibit duckweed the most [8].
Phenolics inhibit diverse organisms, because they indiscriminately inactivate proteins [49]. The leather tanning industry is based on the ability of plant polyphenols like tannins to inactivate and polymerize proteins in curing animal skins [50]. In the live plant, these same tannins deter insect feeding by damaging proteins in the insect’s gut.
Phenolic acids may be found in very high concentrations in specialized ‘phenol cells’. In the waterhyacinth, phenol cells are mainly interspersed with ordinary cells in the subepidermal tissue of both leaf surfaces [51]. The phenolic acids in these cells are found in very high concentrations– about 1,000 ppm– and consist of chlorogenic, protocatechuic, vanillic, and p-coumaric acids [14]. Phenol cells are believed to play a role in waterhyacinth resistance to the fungus responsible for ‘leaf-spotting’ disease [52].
2.Allelochemical Release from the Plant
Do allelochemicals ever actually leave the aquatic plant? If they remain tightly bound within the plant, their impact on the aquarium environment– algae, bacteria, and other plants– would be limited.
Terrestrial plants frequently release allelochemicals into their surroundings [36]. For example, the roots of young papaya trees were found to secrete the allelochemical benzyl isothiocyanate at the rate of 2 µg/tree/day [53]. The soft chaparral shrub releases from its leaves a variety of water-soluble phenolic acids that are the same as those found in aquatic plants. Rainwater washes these compounds off the leaves and into the soil where they prevent the germination and growth of competitive herbs [43].
Aquatic plants probably release large amounts of allelochemicals, for they are leaky when they’re alive and even more so when they’re dead. The annual release of dissolved organic carbon (DOC) by submersed aquatic plants is believed to be about 4% of total carbon fixed when alive and 40% when dead [54]. [Bacteria convert much of this DOC to humic substances (see page 61).] Furthermore, aquatic plants continuously turn over their leaves, replacing older, decaying leaves with new leaves. For example, the water lily Nymphaea odorata growing in the Southern USA reportedly had 7 full leaf turnovers per year. Along with this abundant biomass turnover is the enhanced potential for allelochemical release into the water [55].
Indeed, allelochemicals have been found in the culture media of aquatic plants. When duckweed is grown in sterile culture media, “cinnamic acids are quickly detected in the medium and, after several days, flavonoids are found” [11]. Myriophyllum brasiliense reportedly released a small amount of its allelopathic polyphenols into the culture media [18]. Within 10 days, Myriophyllum spicatum released 2-4 mg of phenolic acids per gram of dry plant matter [20]. Several allelochemicals were found in pond water containing Eleocharis microcarpa [16].
Although much of the DOC released by aquatic plants is quickly metabolized by bacteria, some DOC always resists decomposition. For example, bacteria metabolized much of the DOC released by Scripus subterminalis within 3 days, but 40 days later about 5 to 10% still remained [56]. This long-lasting DOC would include phenolic compounds (both humic substances and freshly synthesized allelochemicals), because they are innately resistant to bacterial degradation. Decomposition of different plant residues after one year were found to be 99% for sugars,
90% for hemicellulose, 75% for cellulose, 50% for lignins, 25% for waxes, and only 10% for phenolic compounds [57].
3.The Subtle Nature of Aquatic Plant Allelopathy
Most plant allelochemicals are only mildly inhibitory, so scientists sometimes have problems proving allelopathy:
“The probability is very high that the allelopathy of plants results from the combined effect of many, mildly potent chemicals. This lack of specificity and potency can be aesthetically dissatisfying and difficult for scientists to prove. Thus, scientists continue to search for more definite evidence of specific and highly potent phytotoxins, although in reality the inhibitory quality of plants may lie in the combined actions of a large number of individually inadequate toxic compounds.” [43]
Indeed, an allelochemical may inhibit more when combined with other allelochemicals than when tested alone (i.e., the ‘synergistic effect’) [59]. For example, two not-too-potent phenolics (gallic acid and caffeic acid) inhibited blue-green algae 6 times more strongly when they were mixed together than when they were tested alone [21]. This is an important finding, because the low potency of many phenolic allelochemicals suggests that they might have little or no effect outside the laboratory. However, if there are a lot of allelochemicals (as there are) and they are acting synergistically, then allelopathy is possible.
Allelopathy in aquatic plants is not dramatic. It is subtle. However, all aquatic plants continuously produce a large number and variety of defensive compounds that mildly inhibit all organisms. It is likely that these allelochemicals might have subtle and unrecognized effects on the plants, bacteria, algae, and invertebrates in aquatic ecosystems.
4.Aquatic Plants versus Algae
Aquatic botanists have observed that lake areas with heavy plant growth often have reduced algal growth [20]. Granted that some of this apparent inhibition may be due to plant competition with algae for light and nutrients. However, plant-produced allelochemicals could cause a portion of the inhibition. Other inhibition may be due to humic substances [61]. Humic substances, which are phenolic compounds, are derived from the decomposition (rather than the synthesis) of plant phenolics (see page 61).
One investigator [62] tracked algal growth as a function of phenolics (mainly humic substances) in 6 Spanish ponds over a two year period. Because of seasonal floods, phenolics in the ponds varied in concentration from 4 to 26 mg/l. When concentrations were at or above 10 mg/l and nutrient levels were low, algal growth was lessened. In an investigation using phenolic extracts from Myriophyllum spicatum [19], a 10 mg/l concentration of phenolics moderately inhibited algae and cyanobacteria.
Although phenolic allelochemicals and non-specific humic acids may help control algal growth, other compound types are probably involved in aquatic plant allelopathy. Chara globularis (‘skunk-weed’) produces two sulfur-containing compounds, a dithiolane and a trithiane, which were found to strongly inhibit algal photosynthesis [13]. In another study, 33 of the 43 different oxygenated fatty acids found in the pondwater containing the spikerush Eleocharis microcarpa inhibited blue-green algae in vitro [16].
Table III-4 shows the inhibition of various algae by allelochemicals of the emergent plant Typha latifolia. The activity of plant allelochemicals was compared to the algaecide copper sulfate. Two species of blue-green algae (Anabaena flosaquae and Synecococcus leopoliensis) were quite sensitive to both the crude plant extract and the sterol.
Table III-4. Typha latifolia Inhibition of Algae Compared to Copper Sulfate [27].
‘Plant Extract’ is an ethyl ether extract. Sterol ‘C’ is stigmast-4-ene-3, 6-dione.
The bioassay was done on petri dishs containing nutrient agar inoculated with exponentially growing algae. Acetone solutions containing known quantities of chemicals were dried on filter disks, which were then added to the petri dishs. The plates were incubated in the light until alga growth became visible. Growth inhibition was manifested as clear zones around the filter disks.
| Algal Species (0.5 mg) | Plant Extract (0.7 µmol) | Sterol 'C' (0.5 µmol) | Copper Sulfate (0.5 µmol) |
| Anabaena flosaquae | ++ | ++ | ++ |
| Aulosira terrestre | - | - | ++ |
| Chlamydomonas sphagnophila | - | - | - |
| Chlorella emersonii | + | + | +++ |
| Chlorella vulgaris | + | + | - |
| Closterium acerosum | + | - | - |
| Coccomyxa elongata | + | - | - |
| Euglena gracilis | - | - | - |
| Muriella aurantiaca | + | + | - |
| Navicula pelliculosa | + | - | + |
| Nostoc commune | - | - | + |
| Phormidium autumnale | ++ | - | + |
| Porphyridium aerugineum | + | - | - |
| Porphyrosiphon notarisii | ++ | - | + |
| Scytonema hofmanni | ++ | - | + |
| Selenastrum capricornutum | + | - | - |
| Stichococcus bacillaris | + | - | - |
| Synecococcus leopoliensis | ++ | +++ | ++ |
Symbols: - is no inhibition of algal growth; + is a 7-14 mm diameter of inhibition; ++ is 15-23 mm diameter of inhibition; and +++ is a 23 mm diameter of inhibition.
Although most allelochemicals of aquatic plants only mildly inhibit algae, some are more potent inhibitors. While studying nutrient uptake from polluted waters, investigators [18] suspected that Myriophyllum brasiliense was secreting inhibitory substances against the nearby blue-green algae. Using careful extraction methods, they were able to isolate from the plant two very potent polyphenols, Tellimagrandin II and 1-desgalloyleugeniin.
Myriophyllum spicatum‘s success in dominating North American lakes may be due to its phenolics. The plant’s phenolic compounds were shown to completely inhibit blue-green algae at a concentration of 10 mg/l; green algae was inhibited by 20 mg/l [19]. Tellimagrandin II, which was first discovered in the terrestrial perennial Tellima grandiflora and subsequently in other members of the order Rosales [63], was found in high concentrations in M. spicatum [20]. The investigator calculated that if M. spicatum released only 1% of its Tellimagrandin II, the release would be enough to severely affect both ephiphytic (attached to plant) and planktonic (suspended) algae [64].
Eurasian Water Milfoil
(Myriophyllum spicatum).
M. spicatum appears to produce allelochemicals against a variety of different organisms (duckweed, blue-green algae, mosquito larva, and the aquatic plant Najas marina). It releases a fairly potent allelochemical (Tellimagrandin II) that may protect it from algae.
Plant drawing from IFAS [65].
Recently, a group of investigators has systematically screened several aquatic plants for allelochemicals against algae. Seven different phenolic acids were isolated from Acorus gramineus, including some that inhibited several species of algae and cyanobacteria with a toxicity comparable to copper sulfate [12]. The investigators also found assorted allelochemicals– sterols, polyprenols, fatty acids, and a-asarone– in Pistia stratiotes [23]. The most inhibitory compound was the phenolic acid a-asarone, which inhibited 14 of the 19 algal species tested [31].
Although the above studies show that plants contain small quantities of potent algal inhibitors like a-asarone and Tellimagrandin II, many aquatic plants may not produce these compounds in quantities sufficient to control algal growth in nature (or in our aquariums). The bulk of aquatic plant allelopathy probably lies with the sheer quantity (~6% of plant dry weight) of total miscellaneous phenolic acids.
5.Aquatic Plants versus Bacteria and Invertebrates
Because allelochemicals are often non-specific inhibitors, aquatic plants may inhibit bacteria. For example, investigators tested extracts of Brasenia schreberi against nine species of bacteria, both gram-negative and gram-positive; all nine species were inhibited by various fractions of the plant extract [66]. Extracts of the water lily Nymphaea tuberosa showed high antimicrobial activity against several species of bacteria [67]. The allelochemicals responsible for the inhibition were identified as tannic acid, gallic acid, and ethyl gallate, all common phenolics found in many aquatic plants. Moreover, several studies show that allelochemicals produced by aquatic plants inhibit cyanobacteria (‘blue-green algae’). (This infers that other bacteria might be inhibited as well.)
Q. Vallisneria gigantea has proved a great challenge for me, although it is supposed to be a relatively easy plant to grow. After an initial flush of growth, with luxuriant scrolling of leaves over the surface of the tank, the plants seem to always decline.
Another problem I have experienced is with mystery snails. While the snails have been observed occasionally munching on the newest growth of H. polysperma, little lasting damage occurs. V. gigantea seems to be a favorite food. The snails will make it their exclusive food until they virtually consume all of it. The same snails placed in a tank with V. spiralis revert to an exclusive algae diet. Why consume V. gigantea and not V. spiralis? No other plants in the 75 gal tank are attacked like this. Have other aquatic gardeners had this experience? Are there other plants with which mystery snails cannot be trusted?
A. Your question about Vallisneria gigantea and mystery snails is most interesting.
There is one large snail Pomacea canaliculata that apparently devours plants. However, most snails consume only dead or dying plants. Indeed, most snails benefit plants by cleaning the leaves. All healthy aquatic plants contain protective chemicals (allelochemicals) that repel snails and other herbivores, but once the plant tissue begins to disintegrate, these repellent chemicals leach out. Only then do the snails feed on the plant. Since you have described a problem with V. gigantea dying, possibly the snails are merely consuming a dying plant and leaving the healthy V. spiralis alone.
Aquatic plants apparently release chemicals into the water that repel invertebrates. Thus, daphnia moved away from Elodea, Myriophyllum, and Nitella in experimental tanks more than they did in control tanks with plastic plants [68]. Another investigator [69] showed that extracts of Myriophyllum spicatum inhibited midges and mosquito larva. Allelopathy may explain what biologists have observed in nature– reduced populations of mosquitoes, midges, and daphnia in stagnant lake areas of heavy plant growth.
Snails avoid eating healthy leaves of aquatic plants, but will consume dead or diseased ones [70,71]. For example, when periwinkle snails were offered a choice between freshly collected leaves of the saltwater Spartina alterniflora, they preferred dead (but intact) leaves over healthy leaves about three to one. The lower ferulic acid content in the dead leaves was believed to account for the difference in preference [26]. (Ferulic acid, an allelopathic phenolic acid, would leak out as the leaves died and make them less inhibitory.)
6.Chemical Warfare between Aquatic Plants
Aquatic plants often grow better alone than when paired with another species [67]. Besides protecting themselves from being eaten, aquatic plants also synthesize allelochemicals that make them more competitive in their immediate environment. That is, they can poison neighboring plants and take over the territory.
a.) Allelopathy in the Substrate
Allelochemical release into the substrate has been proven conclusively for the dwarf spikerush (Eleocharis coloradoensis). This tiny plant, which in nature could eliminate heavy stands of large pondweeds, was suspected of secreting allelochemicals into the substrate.
In a series of experiments, investigators [72] first showed that the pondweeds Potamogeton nodosus and especially P. pectinatus did not multiply well when their tubers were planted in soil containing the dwarf spikerush. However, because the plants were growing together in the same aquaria, the reduced growth of the pondweeds could have been due to competition for nutrients or possible modifications of water quality by the spikerush.
Dwarf Spikerush Eleocharis coloradoensis (a hairgrass).
This small (2”-3”), turfforming plant found in the western USA competes well with much larger plants by releasing poisons into the substrate. Although allelopathy has been suspected and probably occurrs in other Eleocharis, it has been proven definitively for E. coloradoensis.
Drawing from Hotchkiss [76].
So the same investigators proceeded on to a more definitive experiment where the plants were grown in separate aquaria. Dwarf spikerush were grown for 3 months in one set of containers, while the pondweeds were grown in separate, lower-level containers. A plastic hose at the bottom connected the containers. Water, driven by gravity, slowly percolated down through the soil where the spikerush was growing and passed up through the soil of the pondweed cultures. The control for this experiment was the same setup without the spikerush. The leachate from the spikerush soil reduced growth in the pondweeds to less than half; chlorosis was also apparent in the treated plants. The investigators were also careful to show that the nutrient content of the spikerush leachate was similar to the bare soil leachate, indicating that nutrient deficiencies were not responsible for the poor growth of the pondweeds.
However, even these experiments did not conclusively prove that the spikerush was allelopathic. Bacteria and other microbes in the root area can enhance or degrade allelochemicals secreted by plant roots. Soil humus and clay can absorb allelochemicals and lessen their inhibition [73,74]. All these factors could affect allelopathic activity in sediments and soils. Only if the spikerush remained inhibitory in the absence of bacteria and soil particles, could the inhibition be attributed directly to spikerush allelochemicals. When later investigators [75] cultured Eleocharis coloradoensis in sand and nutrient media under sterile conditions, the root exudates were still inhibitory (i.e., against P. pectinatus and Hydrilla vercillata). These final experiments provided definitive evidence that the spikerush releases inhibitory allelochemicals into the substrate.
Although the dwarf spikerush contains several known inhibitory compounds, its allelopathy is believed to be due mainly to dihydroactinidiolide [15].
Allelopathy also occurs in the overlying water and can be quite specific. For example, investigators [77] planted twenty Najas alone or paired with 20 plants of another species in large (200 liter) containers containing a sandy loam soil. The three other species that Najas was paired with were Potamogeton lucens, Scirpus litoralis, or Myriophyllum spicatum. During the 2 month growth period, Najas was given enough room so that plants were not restricted by either space or nutrients. The results showed that Najas grew just as well with P. lucens and S. litoralis as it did alone. However, Najas growth was reduced in half when it was grown with M. spicatum.
In a separate experiment, water from pure M. spicatum cultures was added each week to containers with Najas. Growth of Najas over the summer in M. spicatum water was less than 1/3 of its growth in ordinary tap water. Again, investigators were careful to show that nutrient depletion was not the cause of the Najas’ poor growth. M. spicatum was also shown to be inhibited by Najas. The results could explain why Najas marina and Myriophyllum spicatum do not usually grow together in native water bodies (of Israel).
Apparently, Hydrilla and Ceratophyllum sometimes do not grow well together in nature. Investigators [78] sought to find a reason why just a few shoots of Hydrilla entering Indian ponds and reservoirs could quickly and totally eliminate stands of Ceratophyllum. So Ceratophyllum demersum and C. muricatum were grown either alone or with Hydrilla verticillata in cement tanks containing garden soil. Plants were separated by wire netting so that the plants were not in direct competition; they just shared the same water. The results were dramatic. Initially both Hydrilla and the Ceratophyllum species grew well together, but after 30 days, the Ceratophyllum turned pale and gradually decayed. After 70 days, the Ceratophyllum had died, while Hydrilla had grown well in all available space. Control plants (Ceratophyllum demersum and C. muricatum grown without exposure to Hydrilla) were healthy and grew well.
7.Defensive Chemicals Induced by Infection
Although all plants contain a large variety of phenolic acids, some phenolic acids may also be induced by infection [79]. For example, the slime mould Labyrinthula zosterae devastated North Atlantic seagrass beds of Zostera marina in the 1930s. When investigators [80] purposely infected this plant species with the slime mould, the plant’s phenolic acid production was stimulated, especially near the infection site (Fig. III-3). At 2 cm from the slime mold lesion, the phenolic acid concentration was about 0.2 mg/kg dry wt, but 8 cm away the phenolic acid concentration decreased to about 0.1 mg/kg. Caffeic acid, in particular, was shown to increase about 5-fold in infected leaves, thereby reaching inhibitory concentrations [29].
Figure III-3. Phenolic Acid Concentrations near the Infection Site of Zostera marina Leaves.
Phenolic acid concentration is based on dry weight.
Fig. 3 from Vergeer [80] redrawn and used with permission from Elsevier Science.
Marine Eelgrass (Zostera marina).
Z. marina, the most widely distributed sea grass in America, forms large underwater meadows. When Z. marina was deliberately infected with a pathogenic slime mold, plants released protective phenolic acids around the infection site.
Plant drawing from Hellquist [81].
Plants threatened by algae may increase their defensive phenolic acids. A large parasitic algae (Caulerpa taxifolia), accidentally introduced into the Mediterranean Sea in 1984, has invaded large seagrass meadows of Posidonia oceanica along the French coast. Algae attach to the plant’s rhizome and subsequently damage or kill the plant. Investigators [82] showed that the leaf area occupied by phenol cells was 43% in threatened plants, almost twice that of plants from sediment areas that had not been invaded. In a separate study, the phenolic acids (especially ferulic acid) in threatened plants (641 µg/g dry wt) was almost twice that of plants from non-invaded areas (391 µg/g dry wt) [25].
8.Auto-inhibition
Allelopathic auto-inhibition, in which a plant inhibits its own species, has been reported in a variety of native plants and agricultural plants [1]. For example, the allelochemical amygdalin (a cyanogenic glycoside) was found in the bark of peach tree roots. Bacteria in the soil break down the non-inhibitory amygdalin into a cyanide that strongly inhibits young peach trees [83].
Q. My plants have everything. Lighting is strong, the substrate is an ideal mixture of soil, sand, and vermiculite. I use CO2 injection, micronutrient fertilizers, and add pieces of pond fertilizer plugs to the substrate each month. I get excellent plant growth and no algae. However, after about a year there’s a decline in plant vigor and the increasing presence of algae. Is it because the substrate becomes increasingly anaerobic?
A. Possibly, but an anaerobic substrate is probably a secondary effect. The primary problem is that the plants have stopped growing for some reason. The substrate degradation you’re seeing could be due to allelopathy.
Many plant species release allelochemicals that either inhibit other plants or themselves (‘auto-inhibition’). The aquarium substrate with its solid bottom is particularly conducive to the gradual buildup of allelochemicals. Moreover, in your tank with the CO2 injection and rapid plant growth, allelochemicals may build up faster in the substrate than they can be decomposed by bacteria or bind to soil particles. The accumulation of auto-inhibitory allelochemicals may be one reason why your substrate gave out.
Auto-inhibition has also been reported for several species of algae [84] and emergent aquatic plants [67]. For example, soil extracts from the reed Phragmites karka strongly inhibited seed germination in this species.
But why would plants release compounds that inhibit their own species? One investigator [73] explains that auto-inhibition may help plants regulate their own population density. Frequently, auto-inhibition involves toxicity to seeds and seedlings but not adult plants. While auto-inhibition limits the number of plants, especially under stressful conditions, it does not destroy the species. Therefore, auto-inhibition may be an adaptive strategy than enhances species survival.
B. Allelopathy in Algae
Algae produce their own allelochemicals, some probably designed to compete with other algae, others to deter algae-eating protozoa and other herbivores. The intended target organism is often difficult to determine, because secondary effects abound in aquatic ecosystems. One investigator [85] expressed frustration in studying algal allelopathy: “Allelochemistry is so pervasive in aquatic systems that in our laboratory, even when we specifically try to avoid it, we find it wherever we look. Our greatest problem is sorting it out.”
Another investigator [86] routinely used the filamentous algae Pithophora to keep his aquariums free of other algae, especially ‘green-water’ algae. Eventually, he set up 4 experimental aquariums containing guppies with and without the Pithophora algae. Even though the aquariums had continuous lighting, aquariums containing Pithophora remained clear for all 4 weeks, whereas the water in the aquariums without Pithophora became green in 7 days. The growth of the green– water algae seemed to have nothing to do with nitrate and phosphate levels in the water (Table III-5).
Table III-5. Effect of Pithophora Algae on ‘Green Water’ Algae [86].
| Tank | Treatment | Water Color | Phosphates (mg/l P*) | Nitrates (mg/l N*) | ||
| Initial | Final | Initial | Final | |||
| 1 | None | Green | 2.0 | 1.1 | 5.5 | 1.9 |
| 2 | None | Green | 0.05 | 0 | 1.6 | 7.5 |
| 3 | Pithophora algae | Clear | 0.9 | 1.4 | 2.4 | 14.0 |
| 4 | Pithophora algae | Clear | 0.04 | 0.07 | 0.8 | 1.4 |
* For converting values in the table to mg/l phosphates and mg/l nitrates, see ‘Abbreviations and Conversions on pages 186–187.
Algae are leaky vessels; they release about every substance they make, including allelochemicals [87]. One investigator [85] surveyed over 200 different pairings of algal species from a Connecticut lake for possible allelopathy. (‘Pairings’ consisted of exposing one algal species to heat-treated filtrates from another algal species.) Over two-thirds of the 200 pairings were allelopathic, in that the filtrate either inhibited or stimulated the tested species. Moreover, the investigator found that the lab results matched the sequence of algal blooms in the lake itself. That is, alga species dominating the lake during one season secreted substances into the water that inhibited their predecessors and stimulated their successors.
Algae may be able to inhibit competitors not just by releasing allelochemicals into the water but by transferring the allelochemicals directly into their targets. Thus, one investigator [64] grew a blue-green algae that produced the lipophilic allelochemical Fischerellin A in the presence of tiny beads that had a lipophilic surface. This lipophilic (fat-soluble) surface would experimentally mimic the cell surface of competing blue-green algae. Interestingly, no Fischerellin A was detected in the water; rather the allelochemical was found attached to the beads suggesting that the algae probably transfers the allelochemical directly to target organisms.
Do algae produce allelochemicals that affect plants? Apparently they do. Allelopathic terpenoids of the macroalgae Caulerpa taxifolia have been cited as one reason this algae has been able to decimate underwater meadows of the aquatic plant Posidonia oceanica [82]. And the waterhyacinth became chlorotic, grew poorly, and eventually died when introduced into cement tanks containing a mixture of various common algae [88].
When investigators [89] exposed Zannichellia peltata to filtered water from blue-green algae, the plant’s growth was significantly inhibited (about 25%). However, culture water from the plants did not affect the algae. The investigators concluded that allelochemicals released by blue-green algae may play a role in algal take-overs in some polluted waters.
When duckweed was grown with individual algal species isolated from wastewater, 7 of the 9 species induced chlorosis in the duckweed [91]. Under certain conditions, three algal species could actually kill the duckweed. Interestingly, when duckweed was tested against combinations of algal species, the results were unpredictable. For example, two algal species that strongly inhibited duckweed when tested individually against duckweed, actually stimulated the duckweed when both were grown together with duckweed.
In contrast to the subtle nature of aquatic plant allelopathy, algal allelopathy can be quite dramatic [92,93]. About 1% of algal species release extremely toxic allelochemicals, some of the most lethal biological toxins known. Oceanic ‘red tides’ of certain dinoflagellate algae can cover hundreds of square miles and wreak havoc on marine life. Not only do they kill fish, but they can also cause ‘shell-fish poisoning’ in man– respiratory paralysis and death within 12 hours [94].
The toxins secreted by certain dinoflagellates and blue-green algae include potent neurotoxins and hepatoxins [95]. Blue-green algae in livestock drinking water are responsible for some cattle death each year. After the algae are ingested, they die in the animal’s digestive tract and release their toxins [96].
Zannichellia peltata. Z. peltata, a brackish water plant from southern Europe, was found to be susceptible to the allelochemicals of blue-green algae.
Drawing from van Vierssen [90] and used with permission of Elsevier Science.
C. Allelopathy in the Aquarium
Often strange things happen in planted aquariums for which there appears to be no rational explanation. I wrote this chapter, because I realized that nutrients, water chemistry, and light could not be the only factors controlling the aquarium ecology.
For example, tanks with heavy plant growth often seem to have very little algae. All of my tanks have adequate light, often with many hours of direct sunlight. Nitrate and phosphate levels greatly exceed algal requirements. The fact that algae does not do well despite intense light and high nutrient levels, suggests that allelochemicals released by the plants might help control algal growth.
Plant allelochemicals are relatively harmless and would not be expected to injure fish in the aquarium. However, the allelochemicals of some algal species can be highly toxic. Thus, I once watched what happened to some fish (Lamprologus leleupi) when I innocently scraped off a heavy algal film from the aquarium glass. Within hours, the fish were literally jumping out of the tank and could only be saved by putting them into completely new water. (Other fish species in the tank were wholly unaffected.) I suspect that the alga was a toxic species, and that upon its death, it released an allelochemical that was neurotoxic to the L. leleupi, but not the other fish. (That algal toxins affect certain fish species more than others has been described [93].)
Q. Do you see any advantage in setting up a ‘High-tech’ aquarium?
A. Yes, and it is because allelopathy is reduced in these tanks. Generally, high-tech systems advocate frequent water changes. Also, many tanks have substrate heating cables, which induce water circulation into and out of the substrate. In essence, the substrate is continuously ‘washed’ so that the allelochemicals are brought into the overlying water where they can either be metabolized or diluted out.
Thus, allelochemicals are prevented from accumulating in both the water and substrate in high-tech systems. Auto-inhibition is lessened and strongly allelopathic plants are prevented from dominating other species. Generally, a much wider variety of plant species can thrive within the same tank. Thus, hobbyists with ‘High-tech’ aquaria can indulge in aquascaping and carefully controlled planting schemes.
Several years after this one incident, I received a large, late-night shipment of fancy, show-quality guppies. Not having time to set up a separate tank and knowing the guppies were from healthy stock, I divided up the guppies and added some to three well-established tanks. The show guppies in two of the tanks behaved strangely, dive-bombing into objects and swimming erratically. I thought it was their fright from the late-night handling, but the next day these guppies were dead. Meanwhile, common ‘feeder’ guppies and their babies in these same two tanks were completely unaffected. I might have attributed the cause to some defect in the show guppies, except that the third set of show guppies in my 50 gal Rainbowfish tank appeared wholly normal. After much thought, I attributed the difference to algal allelopathy. This is because the two problem tanks contained small amounts of green mat algae whereas the Rainbowfish tank had a light dusting of ‘fuzz’ algae on the glass, but none of the green mat algae. I believe that one or more species of the green mat algae (see page 164) was secreting a neurotoxin to which the show guppies, but not the common guppies, were exquisitely sensitive.
Also, allelopathy between plants may explain less dramatic, but more common phenomena I have observed in my aquariums. Some plant species in my tanks dwindle away with time for no apparent reason. Because all my tanks contain high nutrient levels and adequate light, I believe that some species are poisoned by the allelochemicals released by other species.
I’ve made a few changes in my aquariums since I became aware of allelopathy. I like to keep prized plant species in their own pots, so that the plant’s roots are protected from substrate allelochemicals from neighboring plants. I keep plants that I particularly like in their own tanks. For example, I have set aside separate tanks for Cryptocoryne, Vallisneria, and Swordplants. I’m not too dismayed when a newly introduced plant species doesn’t do well in an established tank. Above all, I don’t expect to keep a wide variety of plants in a single tank.
Although allelopathy in the aquarium includes negative interactions between organisms, I generally accept allelopathy as being a natural part of their competition. Moreover, allelochemicals probably keep algae under control and help protect fish from bacterial disease. Aquariums, because of their small water volume and contained substrate, lend themselves to allelopathic interactions between organisms. A variety of allelochemicals released by plants, bacteria, and algae accumulate and produce many unexpected (and unintended) effects. I believe that allelopathy is rampant in the home aquarium.
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1Allelochemicals may have other functions. For example, the two flavonoids apigenin and luteolin are allelopathic (see table on page 38), but they may also provide protection from harmful UV radiation for the aerial growth of some aquatic plants [3]. And caffeic and chlorogenic acids apparently act as chelators for root uptake of iron by some terrestrial plants [4,5].
2Data from Elakovich and Wooten [8,9].
Percent inhibition of lettuce seedlings represents the root length for lettuce seedlings grown in petri plates containing plant extracts as compared to controls (those grown in petri plates without plant extracts). Duckweed inhibition represents the number of new fronds in nutrient media with plant extracts as opposed to the controls (duckweed without plant extracts).
Except for the water lilies, investigators prepared extracts from whole plants. Two hundred grams of fresh plant matter from each species was chopped and thoroughly mixed with 200 ml of distilled water and refrigerated for 1-3 days. The extracts were filter-sterilized and then diluted (1:5) with the growth media of the lettuce and duckweed plants.
The duckweed bioassay was run under sterile conditions with bacteria-free duckweed.
3Abbreviations follow well-known allelopathic phenols. Caff, cinn, E, F, G, pC, pOHB, protocatechuic, S, Sy, and V are simple phenolic acids and phenylpropanes, while Ap, Cy, Km, Lu and Qu are flavonoids. Linoleic is a C18 fatty acid. The newly isolated and identified phenylpropanes, oxygenated fatty acids, sterols, and tannins are described in the references.
4Alkaloids like nicotine, digitoxin, strychnine, morphine, and curare are well-known allelochemicals of terrestrial plants [1]. Water lilies have been found to contain a variety of alkaloids [17]. However, alkaloids in other aquatic plants are apparently scarce; fifteen species of submerged plants were found to contain less than 0.06% alkaloids [44].
5McClure [11] provides phylogenetic evidence for the gradual reduction of lignin that occured along with aquatic plant evolution. Vanillin and syringaldehyde are specific phenol precursors of lignin. The more primitive species of the Lemnaceae (e.g., Spirodela intermedia, S. polyrhiza, and S. oligorhiza) contain these phenols, whereas the more evolved species of Lemnaceae (e.g., Lemna minor, L. gibba, and L. trisulca) do not.