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Fungi in the nests of ants
FUNGI
IN THE
NESTS OF ANTS.
PLATE II.
By Jessie S. Bayliss Elliott, D.Sc. Bi,m., B.Sc. Lond. The occurrence of fungi in the nests of ants has been repeatedly observed by Naturalists visiting tropical and subtropical countries, and during the last few years several investigators have given much attention to the subject. Moller· has published the results of extensive researches on the leaf-cutting ants of South America and demonstrated the truth of Belt's statement that "Ants are mushroom growers and eaters";t Tanner, Von Ihering and Wheeler have also written on the subject, and we are indebted to the researches of Petch:J: and others for our knowledge of the Termite fungi of Ceylon and elsewhere. But it is not generally known to Mycologists that the nests of two species of British ant-Lasius fuliginosus and Lasius umb1atus-also have fungi associated with them. It is associated with the black earthy, brittle substance known as carton, which these ants use in constructing their nests. CLADOSPORIUM MYRMECOPHILUM (Fres.) nov. comb. The fungus in the nest of Lasius fuliginosus, which occurs as a pure culture, was described in 1852 by Fresenius§ and named Septospo1ium my11JZecophilum. Saccardoll describes it as M aC10spo1ium my1mecophilum, but considers it may be identical with Cladotrichum mic10spo1um. Later, 1900, Lagerheim' investigated it and came to the conclusion that it was really a Cladot1ichum, and called it Cladot1ichum myrmecophilum. * Moller, Die Pilzgarten einiger Siidamerikanischer Ameisen. Schimper. Botanische Mittheilungen aus den Tropen. Heft VI., Jena 1893. t Belt, Naturalist in Nicaragua, page 79. ::: Petch, Annals of the Royal Botanic Gardens, Peradeniya, 1906 and 1913. Science Progress, October, 1907. § Fresenius, Beitriige zur Mykologie. Heft 2, page 49, t. VI. II Saccardo, Sylloge Fungorum. Vol. IV.: Hyphomycetes, page 538. 'I! Lagerheim, Ueber Lasi!,s tuliginosus und seine Pilz-zucht. Entomologisk Tidskrift, 1900, page 17.
139
This uncertainty as to genus arises from the fact that the conidia had never been found attached to the conidiophores. Through the kindness of Mr. H. Donisthorpe, a well-known authority on ants, I obtained a supply of carton taken freshly from a nest. After examining portions of it teased out in water (fig. I) I felt inclined to think that Fresenius had rightly assigned it to the genus Septosporium. Two kinds of dark-coloured hyphae were to be seen, creeping hyphae (fig. la) whose septa lay very close together, the cells often being inflated, thus giving ~he hyphae a nodulose appearance; and arising from the creeping hyphae numerous long erect hyphae (fig. Ib), generally simple, but sometimes branched (fig. Ie); it was conspicuous that many of these erect hyphae were truncate (fig. Ib). Conidia were not abundant, no doubt because consumed by the ants: they were dark coloured, oval, 10-14,... x 4-6,..., and mostly uniseptate, though unicellular ones were often seen (fig. IC & d); a few 3-celled and 4-celled forms were found, and also four examples of a triangular form of three-celled conidium (fig. 4). Like Fresenius and Lagerheim I could not find any of the conidia attached to the conidiophores except a few of the unicellular forms, which were apparently sessile on the nodulose creeping hyphae (fig. If). However, after making hanging-drop cultures of the fungus and allowing them to grow for a few weeks, uniseptate conidia attached to conidiophores appeared (fig. 2). It was now evident that the erect hyphae which Fresenius had considered sterile hyphae, and which certainly had every appearance of being so, were really conidiophores bearing terminal and lateral uniseptate conidia, the latter either sessile or on short branches. Some of the erect hyphae which had not been truncated became enormously long (fig. 3), and bore conidia laterally, sometimes sessile and sometimes on short branches. The conidia never appeared in chains nor were the conidiophores nodulose, hence the fungus is not a Cladotricltum but a Cladosporium and so should be called CLADOSPORIUM MYRMECOPHILUM nov. comb. All the different forms of conidium on germination usually produced a nodulose form of hypha (fig. 4). HORMISCIUM PITHYOPHILUM (WalIr.) Sacco var. MYRMECOPHILUM (var. nov.). About two years ago Mr. Donisthorpe· found that the ants of the species Lasius umbratus also constructed carton cells of * Donisthorpe. Myrmecophilolls notes for 1913. Entomologists' Record, Vol. XXVI., No.2, page 40.
140
a dark earthy brittle substance similar to that of which the nests of Lasius fuliginosus were formed, and after finding that the carton also contained fungus hyphae, very kindly sent me some to examine. These ants (L. umbratus) build small nests underground among the roots of trees, etc., where they construct only a few cells of this carton, making it by cementing together with saliva, fragments of wood fibre, sand, earth, etc. (fig. 5). It forms a very favourable substratum for the fungus which grows so luxuriantly that it becomes the predominant feature, and because of its dark olive green colour gives the carton the characteristic blackish appearance. The fungus is a species of H ormiscium very much resembling Hormiscium pithyophilum; it has a similar dark olive green colour, in masses appearing black, but it has a creeping habit, forming long branching chains of cuboid or oblong conidia which rarely become separate (fig. 6). The conidia are at first very pale olive, quite smooth and transparent, but later they become somewhat opaque and rather rough; their size is very variable, the cells of the conidial chains varying in diameter from 8p. to 14p., and in length from lOp. to 20p.. Each cell has one or more large oil drops present. In culturest the cells of the chain rarely become isolated, but on doing so, they become quite spherical (figs. 7 & 8), and on germination either produce similar long chains of conidia (fig. 9) or hyphae of wide dimensions from which conidial chains arise (fig. 10). It will be seen that this fungus differs from H ormiscium pithyophilum Sacco only in the slight roughness of the spores and in having long creeping branches, instead of short curved branches becoming thinner at the tips; this may be due to difference in habit since H. pithyophilum is found forming thick superficial patches on the leaves of pines, firs and yews. With reference to this, it may be noted some of the nests of L. umbra/us are found at the roots of decayed conifer trees or in the ground in the vicinity of conifer stumps, so the origin of the fungus in the carton may possibly have been infected pine needles. Considering the habitat and the somewhat different appearance of the fungus it seems appropriate to call it H ormiscium pithyophilum var. myrmecophilum. Just as the species of fungus associated with the carton of Lasius fuliginosus is always the same, so in the case of L. umbratus, the above described species of H ormiscium is always found to be present in the carton, no matter to what locality the nest from which it was taken belonged. t Hanging-drop cultures of fragments of carton moistened with water.
It has been suggested in the case of L. fuliginosus that the ants cultivate the fungus and. feed their larvae on it, but notwithstanding the abundance of the fungus in the Lasius umbratus carton, Mr. Donisthorpe considers it would not be sufficient food alone for the brood, though probably the ants do make use of it, as it is easily accessible, using it to supplement their other food, which consists largely of small insects and the excreta of aphides. In fact he considers it is probably the absence of this fungus which makes it exceedingly difficult to rear larvae of this species, while on the other hand, larvae of species of Lasius which do not make carton he has reared from the egg to the perfect state in a few months. Perhaps the more important function of the fungus in the carton is that of giving stability to the walls of the nest, for the ramifications of the fungus hyphae must help considerably in binding the particles of sand, fibre, etc., together. This carton fungus must not be confused with the wellknown" fungus gardens" found in the nests of the white ants of Ceylon, India, etc.; nor yet with those of the South American leaf-cutting ants. According to Petch* the nests of the white ants contain numerous chambers in which are found coarse sponge-like structures or "combs" composed of finely divided wood or other vegetable matter which has been digested by the ants and is in fact excrement. On these" combs" a fungus grows, hence the name " fungus garden." The "fungus gardens" of the leaf-cutting ants are similar comb-like structures and when investigated by Mollert were found to consist of the small fragments of leaves formed into minute balls and packed together into a spongy mass; in the course of time the spongy mass becomes interpenetrated by the mycelium of a fungus (Rozites gongylophora). In these cases the fungus seems simply grown for the purpose of food and does not occur in the walls of the nest, and so unlike the carton fungus has nothing to do with strengthening them. The leaf-cutting ants make an excellent provision for infecting the" fungus gardens" of new colonies with fungus from the old colony; according to Von Ihering,t a tiny ball of the old" garden" is carried away by the young queen in her infra buccal chamber when she goes out for her marriage flight, and is deposited in the hole made for the new brood, and until the * Peteh. Termite Fungi: a Resume. Annals R.B.G., Peradeniya, Vol. V.,
Part V., 1913. t Moller. I.e. page 22. : Von Ihering. I.R.M.S., page 299. New Colonies and Fungus Gardens. Zool. Anzeig., XXI. (1898), pp. 238.55.
first batch of workers is hatched out she attends to its welfare herself; probably a similar arrangement exists with the abovementioned two species of Lasius which make carton; and may thus account for the constant association of definite species of ant and fungus. Since the ft~ngus exists in the carton as a pure culture, all " foreign" fungi are doubtless " weeded" out, as in the fungus gardens of the white ants and leaf-cutting ants, for many varieties of fungus spores must be introduced into the nests by the passing of insects in and out. In conclusion I wish to express my thanks to Mr. H. Donisthorpe for drawing my attention to these fungi, and also to Prof. G. S. West, Mr. Carleton Rea, and Mr. Grove, for the loan of various books and pamphlets which I have used for reference.
H. pithyophilum (Wallr.) Sacco v. myrmecophilum var. nov. var. ramulis, non apice attenuatis, cellulis leniter asperulis. Hab. in nidis Lasii umbrati. EXPLANATION OF PLATE.
The carton from the nest of Lasius fuliginosus. FIG. 1. Small portion of carton teased out showing a, nodulose creeping hyphae. b, erect hyphae, truncate. c, uniseptate conidium. d, unicellular conidium. e, branched erect hypha, x 312. f, unicellular conidium, sessile on nodulose creeping hypha. FIG. 2. Carton after being moistened and kept in a hanging drop for a few weeks showing erect hyphae (conidiophores) with conidia attached, x 312. FIG. 3. Erect hyphae which have grown to a great length in a hanging drop bearing lateral conidia, sessile or shortly stalked, x 312. FIG. 4. Two-, three-, and four-celled conidia, some germinating and producing nodulose hyphae, x 312. Carton from the nest of Lasius umbratus. FIG. 5. Carton showing ramifying chains of conidia, grains of sand and wood fibre, x 85. FIG. 6. Chains of conidia, x 312. FIG. 7· Cells of a conidial chain rounding off, x 312. FIG. 8. Conidium, x 312. FIG.
9.
FIG. ro.
al(
~
Germinating conidia, x 3 12.
Conidial chains arising from a hyphae produced from a conidium, x 312.
Vol. V., Pi. II.
Trans. Brit. Myc. Coey.
J.
7·
S. Ila)
r-ol
li~~
Ellioll tit'1.
CIHdosporillJn mnJnecophilllnl (Frt'~.l
--10 I1(lfllli~ 'illlll
I ilh\ophihl')l (\\·allr.) SalT. \ar. 11\~ rlll··ophilllJn.
IN THE
NESTS OF ANTS.
PLATE II.
By Jessie S. Bayliss Elliott, D.Sc. Bi,m., B.Sc. Lond. The occurrence of fungi in the nests of ants has been repeatedly observed by Naturalists visiting tropical and subtropical countries, and during the last few years several investigators have given much attention to the subject. Moller· has published the results of extensive researches on the leaf-cutting ants of South America and demonstrated the truth of Belt's statement that "Ants are mushroom growers and eaters";t Tanner, Von Ihering and Wheeler have also written on the subject, and we are indebted to the researches of Petch:J: and others for our knowledge of the Termite fungi of Ceylon and elsewhere. But it is not generally known to Mycologists that the nests of two species of British ant-Lasius fuliginosus and Lasius umb1atus-also have fungi associated with them. It is associated with the black earthy, brittle substance known as carton, which these ants use in constructing their nests. CLADOSPORIUM MYRMECOPHILUM (Fres.) nov. comb. The fungus in the nest of Lasius fuliginosus, which occurs as a pure culture, was described in 1852 by Fresenius§ and named Septospo1ium my11JZecophilum. Saccardoll describes it as M aC10spo1ium my1mecophilum, but considers it may be identical with Cladotrichum mic10spo1um. Later, 1900, Lagerheim' investigated it and came to the conclusion that it was really a Cladot1ichum, and called it Cladot1ichum myrmecophilum. * Moller, Die Pilzgarten einiger Siidamerikanischer Ameisen. Schimper. Botanische Mittheilungen aus den Tropen. Heft VI., Jena 1893. t Belt, Naturalist in Nicaragua, page 79. ::: Petch, Annals of the Royal Botanic Gardens, Peradeniya, 1906 and 1913. Science Progress, October, 1907. § Fresenius, Beitriige zur Mykologie. Heft 2, page 49, t. VI. II Saccardo, Sylloge Fungorum. Vol. IV.: Hyphomycetes, page 538. 'I! Lagerheim, Ueber Lasi!,s tuliginosus und seine Pilz-zucht. Entomologisk Tidskrift, 1900, page 17.
139
This uncertainty as to genus arises from the fact that the conidia had never been found attached to the conidiophores. Through the kindness of Mr. H. Donisthorpe, a well-known authority on ants, I obtained a supply of carton taken freshly from a nest. After examining portions of it teased out in water (fig. I) I felt inclined to think that Fresenius had rightly assigned it to the genus Septosporium. Two kinds of dark-coloured hyphae were to be seen, creeping hyphae (fig. la) whose septa lay very close together, the cells often being inflated, thus giving ~he hyphae a nodulose appearance; and arising from the creeping hyphae numerous long erect hyphae (fig. Ib), generally simple, but sometimes branched (fig. Ie); it was conspicuous that many of these erect hyphae were truncate (fig. Ib). Conidia were not abundant, no doubt because consumed by the ants: they were dark coloured, oval, 10-14,... x 4-6,..., and mostly uniseptate, though unicellular ones were often seen (fig. IC & d); a few 3-celled and 4-celled forms were found, and also four examples of a triangular form of three-celled conidium (fig. 4). Like Fresenius and Lagerheim I could not find any of the conidia attached to the conidiophores except a few of the unicellular forms, which were apparently sessile on the nodulose creeping hyphae (fig. If). However, after making hanging-drop cultures of the fungus and allowing them to grow for a few weeks, uniseptate conidia attached to conidiophores appeared (fig. 2). It was now evident that the erect hyphae which Fresenius had considered sterile hyphae, and which certainly had every appearance of being so, were really conidiophores bearing terminal and lateral uniseptate conidia, the latter either sessile or on short branches. Some of the erect hyphae which had not been truncated became enormously long (fig. 3), and bore conidia laterally, sometimes sessile and sometimes on short branches. The conidia never appeared in chains nor were the conidiophores nodulose, hence the fungus is not a Cladotricltum but a Cladosporium and so should be called CLADOSPORIUM MYRMECOPHILUM nov. comb. All the different forms of conidium on germination usually produced a nodulose form of hypha (fig. 4). HORMISCIUM PITHYOPHILUM (WalIr.) Sacco var. MYRMECOPHILUM (var. nov.). About two years ago Mr. Donisthorpe· found that the ants of the species Lasius umbratus also constructed carton cells of * Donisthorpe. Myrmecophilolls notes for 1913. Entomologists' Record, Vol. XXVI., No.2, page 40.
140
a dark earthy brittle substance similar to that of which the nests of Lasius fuliginosus were formed, and after finding that the carton also contained fungus hyphae, very kindly sent me some to examine. These ants (L. umbratus) build small nests underground among the roots of trees, etc., where they construct only a few cells of this carton, making it by cementing together with saliva, fragments of wood fibre, sand, earth, etc. (fig. 5). It forms a very favourable substratum for the fungus which grows so luxuriantly that it becomes the predominant feature, and because of its dark olive green colour gives the carton the characteristic blackish appearance. The fungus is a species of H ormiscium very much resembling Hormiscium pithyophilum; it has a similar dark olive green colour, in masses appearing black, but it has a creeping habit, forming long branching chains of cuboid or oblong conidia which rarely become separate (fig. 6). The conidia are at first very pale olive, quite smooth and transparent, but later they become somewhat opaque and rather rough; their size is very variable, the cells of the conidial chains varying in diameter from 8p. to 14p., and in length from lOp. to 20p.. Each cell has one or more large oil drops present. In culturest the cells of the chain rarely become isolated, but on doing so, they become quite spherical (figs. 7 & 8), and on germination either produce similar long chains of conidia (fig. 9) or hyphae of wide dimensions from which conidial chains arise (fig. 10). It will be seen that this fungus differs from H ormiscium pithyophilum Sacco only in the slight roughness of the spores and in having long creeping branches, instead of short curved branches becoming thinner at the tips; this may be due to difference in habit since H. pithyophilum is found forming thick superficial patches on the leaves of pines, firs and yews. With reference to this, it may be noted some of the nests of L. umbra/us are found at the roots of decayed conifer trees or in the ground in the vicinity of conifer stumps, so the origin of the fungus in the carton may possibly have been infected pine needles. Considering the habitat and the somewhat different appearance of the fungus it seems appropriate to call it H ormiscium pithyophilum var. myrmecophilum. Just as the species of fungus associated with the carton of Lasius fuliginosus is always the same, so in the case of L. umbratus, the above described species of H ormiscium is always found to be present in the carton, no matter to what locality the nest from which it was taken belonged. t Hanging-drop cultures of fragments of carton moistened with water.
It has been suggested in the case of L. fuliginosus that the ants cultivate the fungus and. feed their larvae on it, but notwithstanding the abundance of the fungus in the Lasius umbratus carton, Mr. Donisthorpe considers it would not be sufficient food alone for the brood, though probably the ants do make use of it, as it is easily accessible, using it to supplement their other food, which consists largely of small insects and the excreta of aphides. In fact he considers it is probably the absence of this fungus which makes it exceedingly difficult to rear larvae of this species, while on the other hand, larvae of species of Lasius which do not make carton he has reared from the egg to the perfect state in a few months. Perhaps the more important function of the fungus in the carton is that of giving stability to the walls of the nest, for the ramifications of the fungus hyphae must help considerably in binding the particles of sand, fibre, etc., together. This carton fungus must not be confused with the wellknown" fungus gardens" found in the nests of the white ants of Ceylon, India, etc.; nor yet with those of the South American leaf-cutting ants. According to Petch* the nests of the white ants contain numerous chambers in which are found coarse sponge-like structures or "combs" composed of finely divided wood or other vegetable matter which has been digested by the ants and is in fact excrement. On these" combs" a fungus grows, hence the name " fungus garden." The "fungus gardens" of the leaf-cutting ants are similar comb-like structures and when investigated by Mollert were found to consist of the small fragments of leaves formed into minute balls and packed together into a spongy mass; in the course of time the spongy mass becomes interpenetrated by the mycelium of a fungus (Rozites gongylophora). In these cases the fungus seems simply grown for the purpose of food and does not occur in the walls of the nest, and so unlike the carton fungus has nothing to do with strengthening them. The leaf-cutting ants make an excellent provision for infecting the" fungus gardens" of new colonies with fungus from the old colony; according to Von Ihering,t a tiny ball of the old" garden" is carried away by the young queen in her infra buccal chamber when she goes out for her marriage flight, and is deposited in the hole made for the new brood, and until the * Peteh. Termite Fungi: a Resume. Annals R.B.G., Peradeniya, Vol. V.,
Part V., 1913. t Moller. I.e. page 22. : Von Ihering. I.R.M.S., page 299. New Colonies and Fungus Gardens. Zool. Anzeig., XXI. (1898), pp. 238.55.
first batch of workers is hatched out she attends to its welfare herself; probably a similar arrangement exists with the abovementioned two species of Lasius which make carton; and may thus account for the constant association of definite species of ant and fungus. Since the ft~ngus exists in the carton as a pure culture, all " foreign" fungi are doubtless " weeded" out, as in the fungus gardens of the white ants and leaf-cutting ants, for many varieties of fungus spores must be introduced into the nests by the passing of insects in and out. In conclusion I wish to express my thanks to Mr. H. Donisthorpe for drawing my attention to these fungi, and also to Prof. G. S. West, Mr. Carleton Rea, and Mr. Grove, for the loan of various books and pamphlets which I have used for reference.
H. pithyophilum (Wallr.) Sacco v. myrmecophilum var. nov. var. ramulis, non apice attenuatis, cellulis leniter asperulis. Hab. in nidis Lasii umbrati. EXPLANATION OF PLATE.
The carton from the nest of Lasius fuliginosus. FIG. 1. Small portion of carton teased out showing a, nodulose creeping hyphae. b, erect hyphae, truncate. c, uniseptate conidium. d, unicellular conidium. e, branched erect hypha, x 312. f, unicellular conidium, sessile on nodulose creeping hypha. FIG. 2. Carton after being moistened and kept in a hanging drop for a few weeks showing erect hyphae (conidiophores) with conidia attached, x 312. FIG. 3. Erect hyphae which have grown to a great length in a hanging drop bearing lateral conidia, sessile or shortly stalked, x 312. FIG. 4. Two-, three-, and four-celled conidia, some germinating and producing nodulose hyphae, x 312. Carton from the nest of Lasius umbratus. FIG. 5. Carton showing ramifying chains of conidia, grains of sand and wood fibre, x 85. FIG. 6. Chains of conidia, x 312. FIG. 7· Cells of a conidial chain rounding off, x 312. FIG. 8. Conidium, x 312. FIG.
9.
FIG. ro.
al(
~
Germinating conidia, x 3 12.
Conidial chains arising from a hyphae produced from a conidium, x 312.
Vol. V., Pi. II.
Trans. Brit. Myc. Coey.
J.
7·
S. Ila)
r-ol
li~~
Ellioll tit'1.
CIHdosporillJn mnJnecophilllnl (Frt'~.l
--10 I1(lfllli~ 'illlll
I ilh\ophihl')l (\\·allr.) SalT. \ar. 11\~ rlll··ophilllJn.