Interactions between Domestic Mites and Fungi

Review 216- Interactions between Domestic Mites and Fungi Laurent Van Asselt Institut royal des Sciences Naturelles de Belgique, Bruxelles, Belgique...
Author: Mildred Morris
1 downloads 0 Views 514KB Size
Review 216-

Interactions between Domestic Mites and Fungi Laurent Van Asselt Institut

royal des Sciences Naturelles de Belgique, Bruxelles, Belgique

Key Words Mites ; Dermatophagoides farinae ; Dermatophagoides pteronyssinus ; Acarus siro ; Tyrophagus putrescentiae ; Fungi

Abstract In the indoor environment, mites and fungi are two of the most important causes of asthma and rhinitis in people. Although these two subjects are often studied separately, to do so ignores the important ecological relationship between them. For example, fungi may be a source of nutrients, providing the sterols and vitamins required by one of the most important house-dust mites, Dermatophagoides pteronyssinus. In addition, two other mite species also found in the indoor environment, Acarus siro and Tyrophagus putrescentiae, are attracted by fungi and feed on some species of them. In return, these two mite species are capable of inoculating the micro-organisms into clean food commodities. This review is an attempt to highlight the complex interaction between mites and fungi and to give an overview of our knowledge of this microscopic world. It also hopes to give a clearer understanding of the mechanisms by which fungicides can control, or not, the development of domestic mite populations.



Mites are Chelicerata, belonging to the class of Arachnida and to the subclass of Acari. Among the thousands of species identified today some live in houses and are therefore brought together under the term ’domestic mites’. These domestic mites are themselves divided into housedust mites and stored food mites, according to their usual habitat. A number of them are responsible for respiratory and cutaneous allergies (allergic rhinitis, asthma, dermatitis) in sensitive individuals [1-9]. The most widespread species of house-dust mites in Europe and in the USA are Dermatophagoides pteronyssinus, Dermatophagoides farinae, and Euroglyphus maynei (Acari: Pyroglyphidae) [10, 11 ], while the stored-food mites found in houses are mostly represented by Acarus

siro, Tyrophagus putrescentiae (Acari: Acaridae), and Gly-

cyphagus domesticus (Acari: Glycyphagidae) [ 12]. All these mites display particular relationships with xerophilic fungi. In this deliberately interpretative review I will try to outline the advances in knowledge that have been made concerning these ecological relationships in the domestic environment. Because so many mites are known and a lot of the species may be considered as domestic mites, to narrow the field particular attention is paid to D. pteronyssinus and D. farinae for house-dust mites and A. siro and T putrescentiae for stored-food


Laurent Van Asselt Institut royal des Sciences Naturelles de Belgique Département d’Entomologie, 29 rue Vautier B-1000 Bruxelles (Belgium) E-Mail [email protected]

Relationships between House-Dust Mites and Fungi It seems probable that the primary habitat of D. farinae and D. pteronyssinus was originally bird or rodent nests [12, 13]. However, the development of housing to be a closed environment with high humidity and good heat insulation has resulted in the invasion and proliferation of these mites in human dwellings particularly in mattresses, carpets, soft furniture and furnishings and accumulations of house dust. These species are now so well adapted to human dwellings that they have become their most common habitat today [ 12]. The indoor environment has also seen the proliferation of fungi. In maritime climate regions they often belong to the Cladosporium, Eurotium, Aspergillus and Penicillium groups [14-18]. Such fungi have been considered as an important source of allergens, permanently present in house dust [19]. Nevertheless, Hay et al. [20] demonstrated unequivocally that the fungus Aspergillus penicilloides associated with D. pteronyssinus does not contribute to mite allergenicity. The allergens from these two species are quite different. Up to now, very few experimental studies have been conducted on the relationships between house-dust mites and fungi. Van de Lustgraaf [21 ] observed that the fungi A. penicilloides and E. repens play an important role in the food chains of D. pteronyssinus. Presence of these fungi stimulated the development of D. pteronyssinus populations. Van Bronswijk and Sinha [22] proposed that the fungus A. amstelodami predigests human dander (predigestion of the lipid content of the skin scales to assimilate fatty acids) and could also be involved in the production or release of sterols. de Saint Georges-Gridelet [23] suggested that A. penicilloides contributes to the B and D vitamin requirement of D. pteronyssinus. However, with regard to the contribution of fungi to the modification of dietary components for mites, Douglas and Hart [24] concluded that no experimental studies provided unambiguous evidence for this. They did though demonstrate an increased development rate of D. pteronyssinus when the diet of yeast and wheat germ was supplemented with A. penicilloides, suggesting that this fungus is of nutritional value to the mites. Complementary studies by de Saint Georges-Gridelet [25] showed that by eliminating fungi from the diet of D. pteronyssinus, development of nymphs was

severely delayed.

It is known that mites feed on fungi since spores of A. penicilloides have been observed in all parts of the alimentary canal of D. pteronyssinus [21, 24]. Some of them are found undamaged in faecal pellets. The presence of non-

digested spores does not imply that no spores are digested that the fungi have no alimentary value. Fungal mycelium, not easily observable in the gut of the mite, could be an important source of nutrients. Otherwise, for housedust mites, fungal absorption seems to be a passive phenomenon. When studying the feeding behaviour of D. pteronyssinus Hart and Douglas [26] also observed undigested spores of dominant fungal species in their guts. But more interesting was the fact that different mite strains have preferences for specific and different fungal species. The authors suggest an unintentional selection, occurring during the laboratory work, of mite strains with particular feeding behaviour and/or digestive physiology. Although all these observations were made with laboratory cultures of mites, similarities have been demonstrated with xerophilic fungi found in the natural dust system [27]. Fungi not only have positive interactions with mites but also detrimental effects in some cases. Indeed, van de Lustgraaf [21 ] showed that the fungus A. penicilloides can decrease the growth of the house-dust mite population when present in prolific amounts. This is not only the case for D. pteronyssinus in culture but also for stored-food mites [28]. This observation could be explained by the occurrence of toxic substances in the fungal diet [21, 28, 29] and/or by the fact that dense fungal colonisation of the substratum mechanically inhibits the movement of mites [21, 30]. Note that the latter explanation for a negative impact of fungus is related to the physical structure of the or

culture medium. A fine and compact substrate induces


high proliferation of fungus and consequently, an adverse effect on D. pteronyssinus [30]. In this context, the use of fungicides to eliminate fungi and indirectly mites in mattresses has been investigated by various authors. For example, the antimicrobial agent Nipagin has been studied for its effect on the mite D. pteronyssinus. Nipagin kills fungi, depriving the mites of their food source and thereby preventing the development of a new generation of mites. In the same manner, van Bronswijk et al. [31 ] have reported successful reduction in mite populations following elimination of fungi using fungicides. On the other hand, limited success using fungicides has also been reported [32, 33] and the value of the treatment with a fungicide as a long-term control for the eradication of fungi and indirectly of mites has yet to be established. These data allowed Hay et al. [34] to formulate a hypothesis concerning the failure observed by the use of a fungicide to eliminate mites. Fungicide does not allow the complete eradication of the fungi in a house. It can only reduce the quantity of fungi to a reasonable threshold. However, even small quantities of fungi are 217

sufficient to permit the redevelopment of the mite. In consequence, de Saint Georges-Gridelet [35] considered it important that a fungicide should only be used if it could exert maximum activity in the suppression of endemic fungi. These various considerations ignore the fact that killed fungi still remain a good source of nutriments [24]; there is the risk of fungal resistance developing and there is a continual ingress of spores from the outside. For D. pteronyssinus, it is important not only to control the excess of fungi in the medium but also to avoid their deficiency. Indeed, there is a fragile equilibrium between excess (mechanical and toxicological restraint) and absence (nutritious deficiency) of fungi depending essentially on the number of mites and on the initial quantity of fungi. Some substances produced by mites have a fungistatic effect since, after removal of the substances, fungal

again [36, 37]. Mainly produced by two voluminous oil glands, the opisthonotal glands, such substances have been found in D. pteronyssinus and D. farinae [38]. There are other chemical controls. Citral is used by various astigmatid mites (e.g. T putrescentiae) as an alarm pheromone. But this substance has also been discovered, without any pheromonal effects, in some mite exudates (e.g. from D. pteronyssinus and D. farinae) and has been assigned as a mould inhibitor [36-39]. Citral is a mixture of two geometric isomers: neral (35%; cis-) and geranial (63%; trans-). It inhibits the growth ofAspergillus spp. and other fungi infesting house dust or stored food. In 1975, Kuwahara et al. [40] found an alarm pheromone in the body fluid of T putrescentiae and identified this substance as neryl formate. Neryl formate also has a fungistatic effect but to a lesser extent than citral [36]. growth


Relationships between Stored-Food Mites and Fungi Stored-food mites are found in high numbers in the rural environment, principally in cereal stocks. In the natural environment they are mostly found in the nests of mammals (especially rodents) or in tree hollows and bird nests [14, 41]. The presence of stored food, and organic matter associated with dust, in our houses have allowed their development in the indoor environment. A. siro and T. putrescentiae, two of the mites most frequently present in stored food conserved under bad conditions, show a close association with micro-organisms [42]. These mites have a nearly world-wide distribution. Their association with fungi could be explained by the


requirements of moderate temperature and high humidity [43, 44]. The mites feed and reproduce on a great number of seed-borne fungi [45-47]. But in spite of a fungivorous enzyme system [48], A. siro is always less productive on a fungal diet than on a diet composed of wheat germ and brewer’s yeast [49]. From this point of view, it appears that T. putrescentiae is a more efficient fungivore than A. siro [47, 48, 50]. The extent of stored food damage should be dependent on the nutritional value of the fungus for the mite and its substrate. Indeed, although mites feed and breed well on stored products, it has been demonstrated that A. siro cannot feed easily on unbroken grains [42]. In fact it is the growing fungus which allows mites access to the germ where they can feed and reproduce. The association between fungus and stored-food mites seems to be reciprocal. Some fungi attract mites using volatile semio-chemicals [49-51 ], offering them a source of food (by themselves or by contaminating foodstuffs) enabling mite reproduction and proliferation. From this point of view, Griffiths et al. [52] have measured the percentage of living common


spores found in the faeces and shown that the most attractive fungi for A. siro are the species that the mites digest

the best. In contrast, living fungal spores, ingested by the mite or carried on the numerous setae of the mite body, are spread allowing the colonisation by the fungus of all the substratum [52]. This reciprocity is not always so evident as in the examples above. Indeed, it has been observed that the number of colonies of some Aspergillus glaucus and Penicillium spp. decrease when A. siro is present [53]. Mites can thus avoid an excessive development of fungi by secreting fungitoxic substances [36, 37, 54] or by feeding on the fungi. As for the house-dust mites, fungistatic substances like citral and neryl formate have been discovered in T putrescentiae, while A. siro secreted 2-hydroxy-6-methyl benzaldehyde, a substance suspected to have an antifungal effect. However, some chemicals without any known effect are found in their exudate [55]. When fungi are pathogenic, their growth is more abundant in the presence of A. siro than in its absence [53], which could be explained by the fact that the brief existence of the mites is not enough to avoid a significant chemical or trophical control of the fungus. Furthermore, since a pathogenic species like Wallemia sebi [28] is attractive for A. siro [Van Asselt, unpublished data], the mites assist mechanical propagation of spores. In this case, we can conclude that there is only a one-way relationship between the mites and this fungus.


Fungal Attractivity It has been demonstrated that fungi attract stored food mites [51, 56, 57]. At first, the nature of the attractant was thought to be related only to the increase in relative humidity around the fungi, or due to the production of carbon dioxide (which is attractive for some tick species).

However, experiments using dry fungi or solvent extracts of fungi [52] have highlighted the existence of an attractive effect on mites revealing the presence of semio-chemicals in living fungi. Indeed, studying Trichothecium roseum (Fungi imperfecti), Vanhaelen et al. [58, 59], isolated cis- and trans-octa-1,5-dien-3-ol which was shown to be a strong attractant of T putrescentiae. For house-dust mites, in spite of the demonstrated importance of fungi, no direct attraction by fungi has been demonstrated [52]. The absence of any reaction to fungi by the mite may be explained by its low requirement for a fungal diet and by the abundance of spores present in the natural medium of the mite. An abundance which may lead the mite to find adventitiously the necessary nutritious complement. This hypothesis does not exclude the existence of volatile products resulting from the degradation of the medium by the fungi. Up to now, no tests have been performed in relation to this group of volatile prod-


It is evident that the relationships between mites and fungi are complex and not well characterised. The role of fungi in the existence of stored-food mites differs from that for house-dust mites. In house-dust mites, eating fungi in small quantities is essential for their life cycle, while for stored-food mites the attractive effect of fungi acts as an indicator of available food. Therefore, to avoid predation of food by stored-food mites it would seem to be essential to avoid the development of fungi in the indoor environment with the aim of avoiding any attraction of the mites. This could be done by using a fungicide but more efficiently by a reduction of the humidity which allows fungal propagation. Concerning house-dust mites, since only small quantities of fungi are needed by them, preventing the development of fungi would seem to have less effect and so be of little interest as a device to control mite populations. However, as with the stored-food mites, control of the indoor humidity (which should be maintained below 70%) should have an effect against both mites and fungal 1. propagation.




References R, Spieksma FThM, Varekamp H, Leupen MJ, Lyklema AW: The house-dust mite (Dermatophagoides pteronyssinus) and the allergens it produces: Identity with the house-dust allergen. J Allergy 1967;39:325. 2 Spieksma FTHM, Voorhorst R: Comparison of


skin reactions to extracts of house dust, mites and human skin scales. Acta Allergol 1969;24: 124. 3 Green WF, Woolcock AJ: Tyrophagus putrescentiae: An allergenically important mite. Clin


1 Voorhorst

Allergy 1978;8:135-144. OD, Brostoff J, Wraith DG, Brighton

4 Cuthbert

WD: ’Barn allergy’: Asthma and rhinitis due to storage mites. Clin Allergy 1979;9:229-236. 5 Arlian LG, Geis DP, Vysenski-Moher DL, Bernstein IL, Gallagher JS: Antigenic and allergenic properties of the storage mite Tyrophagus putrescentiae. J Allergy Clin Immunol 1984;74: 166-171. 6 Van Hage-Hamsten M, Johansson SGO, Höglund S, Tüll P, Wirén A, Zetterstrom O: Storage mite allergy is common in the farming population. Clin Allergy 1985; 15:555-564.


Angrisano A, DI Berardino L, Fregoso A, Zatta G, Bagliani G, Compostella R: Dermatophagoides and storage mites: Statistical analysis of RAST results. Ann Allergy 1990;64:358-361. Revsbech P, Duenolm M: Storage mite allergy among bakers. Allergy 1990;45:204-208. Van Hage-Hamsten M, Johansson SGO: Stor-

age mites. Exp Appl Acarol 1992;16:117-128. 10 Fain A: Nouvelle description de Dermatophagoides pteronyssinus (Trouessart, 1897): Importance de cet acarien en pathologie humaine 11

(Psoroptidae). Acarologia 1966;9:870-888. Spieksma FThM, Spieksma-Boezeman MIA: The mite fauna of house dust with particular reference to the house-dust mite Dermatophagoides pteronyssinus (Trouessart, 1897) (Psoroptidae: Sarcoptiformes). Acarologia 1967;9:

226-241. 12 Fain A, Guérin B, Hart BJ: Mites and Allergic Disease. Allerbio-Varennes en Argonne, Guérin, 1990. 13 O’Connor BM: Evolutionary origins of astigmatid mites inhabiting stored products; in Rodriguez JG (ed): Recent Advances in Acarology. New York, Academic Press, 1979, vol. 1, pp 273-278.

14 Ishii A, Takaoka M, Ichnioe M, Kabasawa Y, Ouchi T: Mite fauna and fungal flora in house dust from homes of asthmatic children. Allergy

1979;34:379-387. 15

Beguin H: Mould biodiversity in homes. II. Analysis of mattress dust. Aerobiologia 1995;


Nolard N: Mould biodiversity in homes. I. Air and surface analysis of 130 dwell-



Beguin H,

ings. Aerobiologia 1994;10:157-166. Beguin H, Nolard N: Prevalence of fungi in carpeted floor environment: Analysis of dust samples from living-rooms, bedrooms, offices and school classrooms. Aerobiologia 1996;12:113120.


van Bronswijk JEMH, Linskens HF: House-dust community (fungi, mite) in different climatic regions. Oecologia 1981 ;48 : 183-185. 19 Gravesen S: Fungi as a cause of allergic disease.


Rijkaert G,

Allergy 1979;34:135-154. Hay DB, Hart BJ, Douglas AE: Evidence refuting the contribution of the fungus Aspergillus penicilloides to the allergenicity of the house dust mite Dermatophagoides pteronyssinus. Int Arch Allergy Immunol 1992;97:86-88.


Lustgraaf B: Ecological relationships xerophilic fungi and house-dust mites (Acari: Pyroglyphidae). Oecologia (Berl) 1978;

21 Van de between

33:351-359. 22

Bronswijk JEMH van, Sinha RN: Role of fungi in the survival of Dermatophagoides (Acarina: Pyroglyphidae) in house dust environment. En-

viron Entomol 1973;2:142-145. 23 Saint Georges-Gridelet D de: Vitamin requirements of the European house dust mite, Der-

matophagoides pteronyssinus (Acari: Pyroglyphidae), in a relation to its fungal association. J 24

Med Entomol 1987;24:408-411. Douglas AE, Hart BJ: The significance of the fungus Aspergillus penicilloides to the house dust mite Dermatophagoides pteronyssinus .

Symbiosis 1989;7:105-116. Georges-Gridelet D de: Bioécologie et stratégie de contrôle de l’acarien des poussières domestiques Dermatophagoides pteronyssinus (Trouessart, 1897); thèse Université Catholi-

25 Saint

que de Louvain, Faculté des Sciences, 1981. 26 Hart BJ, Douglas AE: The relationship between house dust mites and fungi; in The Acari: Reproduction, Development and Life History Strategies. London, Chapman & Hall, 1990, pp 319-324. 27 Hay DB, Hart BJ, Pearce RB, Kozakiewiez Z, Douglas AE: How relevant are house dust mitefungal interactions in laboratory culture to the natural dust system? Exp Appl Acarol 1992;16: 37-47. 28 Solomon ME, Hill ST, Cunnington AM, Ayerst G: Storage fungi antagonistic to the flour mite (Acarus siro). J Appl Ecool 1964; 1: 119-125. 29 Rodriguez JG, Potts MF, Patterson CG: Myco-

Effects on stored prodmites; in Griffiths DA, Bowman CE (eds): Acarology VI. Chichester, Horwood, 1987, pp

toxin-producing fungi: uct

343-350. 30 Saint Georges-Gridelet D de: Physical and nutritional requirements of house-dust mite Dermatophagoides pteronyssinus and its fungal association. Acarologia 1987;28:345-353. 31 Bronswijk JEMH van, Reumer JWF, Pickard R: Fungicide induced reduction of pyrogliphid mites and their allergens in mattress dust. Exp Appl Acarol 1987;3:271-278. 32 Reiser J, Ingram D, Mitchell EB, Warner JO: An anti-mite mattress spray (Natamycin) in the treatment of childhood asthma; in Mite Allergy, a World-Wide Problem. Bad Kreuznach, Sept 1988, pp 84-85. 33 Colloff MJ, Lever RS, McSharry C: A controlled trial of house dust mite eradication using Natamycin in homes of patients with atopic dermatitis: Effect on clinical status and mites populations. Br J Dermatol 1989;121: 199-208.


Hay DB, Hart BJ, Douglas AE: Effects of the fungus Aspergillus penicilloides on the house dust mite Dermatophagoides pteronyssinus: An experimental re-evaluation. Med Vet Entomol 1993;7:271-274. 35 Saint Georges-Gridelet D de: Strategies de contrôles des acariens des poussières de maison. Belg Pest Control Mag 1995;4:3-7.

47 Sinha RN, Mills JT: Feeding and reproduction of the grain mite and the mushroom mite on some species of Penicillium. J Econ Entomol

36 Matsumoto K, Wada Y, Okamoto M: The alarm pheromone of grain mites and its antifungal effect; in Rodriguez JG (ed): Recent Advances in Acarology. New York, Academic Press, 1979, vol 1, pp 243-249. 37 Okamoto M, Matsumoto K, Wada Y, Nakano H: Studies on antifungal effect of mite alarm pheromone citral. 1. Evaluation of antifungal effect of citral. Jpn J Sanit Zool 1978;29:255260. 38 Kuwahara Y, Leal WS, Suzuki T: Comparison of volatile components between Dermatophagoides farinae and D. pteronyssinus (Astigmata, Pyroglyphidae). Jpn J Sanit Zool 1990;41:2328. 39 Cole LK, Blum MS: Antifungal properties of the insect alarm pheromones, citral, 2-heptanone, and 4-methyl-3-heptanone. Mycologia

1001. 49 Parkinson CL, Barron CA, Barker SM, Thomas AC, Armitage DM: Longevity and fecundity of Acarus siro on four field and eight storage fun-


1975;67:701-708. 40 Kuwahara Y, Ishil S, Fukami H: Neryl formate : Alarm pheromone of the cheese mite,

Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). Experientia 1975;31:1115-1116. 41 Zdarkova Y: Stored product acarology; in Dusbabek F, Bukva V (eds): Modern Acarology. Prague, Academia, The Hague, SPB Academic Publishing, 1991, vol 1, pp 211-218. 42 Hughes AM: The Mites of Stored Food. Ministry of Agriculture, Fisheries, and Food. Tech Bull 9. London, HMSO, 1961. 43 Solomon ME: Tyroglyphid mite in stored products : Nature and amount of damage to wheat. Ann Appl Biol 1946;33:280-289. 44 Sinha RN, Wallace HAH: Association of granary mites and seed borne fungi in stored grain in outdoor and indoor habitats. Ann Entomol Soc Am 1996;59:1170-1181. 45 Sinha RN: Ecological relationships of stored food products mites and seed born fungi. Proc 1st Congr Acarology. Acarology 1964 ;6 :373389. 46 Sinha RN: Feeding and reproduction of some stored product mites on seed born fungi. J Econ Entomol 1966;59:1227-1232.

1968 ;61 :1548-1552. Comparative enzymology of eco-

48 Bowman CE:

nomically important astigmatid mites; in Griffiths DA, Bowman CE (eds): Acarology VI. Chichester, Horwood, 1984, vol 2, pp 993-

gi. Exp Appl Acarol 1991;11:1-8. 50 Sinha RN, Whitney RD: Feeding and reproduction of the grain and the mushroom mite on wood-inhabiting Hymenomycetes. J Econ Entomol 1969;62:837-840. 51 Thomas MC, Dicke RJ: Response of the grain mite Acarus siro (Acarina: Acaridae), to fungi associated with stored-food commodities. Ann Entomol Soc Am 1971;64:63-68. 52 Griffiths DA, Hodson AC, Christensen CM: Grain storage fungi associated with mites. J

Econ Entomol 1959;52:514-518. 53

Armitage DM, Georges CL: The effect of three species of mites upon fungal growth on wheat. Exp Appl Acarol 1986;2:111-124.

54 Kuwahara Y, Leal WS, Suzuki T, Maeda M, Masutani T: Pheromone study on astigmatid mite XXIV: Antifungal activity of Caloglyphus polyphyllae sex pheromone and other mite exudates. Naturwissenschaften 1989;76:578-579. 55 Curtis RF, Hobson-Frohock A, Fenwick GR, Berreen JM: Volatile compounds from the mite carus siro L. in food. J Stored Prod Res 1981; A 17:197-203. 56 Thomas MC, Dicke RJ: Attraction of the grain mite Acarus siro (Acarina: Acaridae), to solvent extracts of fungi associated with stored-food commodities. Ann Entomol Soc Am 1972;65: 1069-1073. 57 Geeraerts J: Etude par le test en croix de l’attraction exercée par divers champignons sur

Tyrophagus putrescentiae (Schrank, 1781).Mykosen 1975; 18:385-392. 58 Vanhaelen M, Vanhaelen-Fastré R, Geeraerts J, Wirthlin T: Cis- and trans-octa-1,5-dien3ol, new attractants to the cheese mite Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae) identified in Trichothecium roseum (Fungi Imperfecti). Microbios 1979;23:199-212. 59 Vanhaelen M, Vanhaelen-Fastré R, Geeraerts J: Occurrence in mushrooms (Homobasidiomycetes) of cis- and trans-octa-1,5-dien-3-ol, attractants to the cheese mite Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). Ex-

perientia 1980;36:406-407.

Suggest Documents