Introduction

The cosmopolitan mite Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) is one of the most abundant and frequent species found in stored foods (wheat, soy, cheese etc.), and it is a species with economic and medical-veterinary importance (Duek et al. 2001; Mullen and O’Connor 2009). These mites can also colonize human-created habitats, such as households, dust in urban environments, medical and laboratory facilities, farms, and food factories (Franz et al. 1997; Solarz et al. 2007). High infestations by this mite cause degradation of food and feed products, speeding up their deterioration in storage facilities (Kucerova and Horak 2004).

Unsatisfactory sanitary conditions (e.g., if the food is inadequately stored) may provide conditions for growth of fungi (Osborne and Stein 2007), which can be concurrently infested with mites (Stejskal and Hubert 2008). Studies concerning mite-fungus interaction have shown: (1) fungal consumption by fungivorous mite species, such as T. putrescentiae, which can develop and reproduce exclusively on fungal diets (Nesvorná et al. 2012; Smrž et al. 2016); (2) selective transfer of fungal species by mites, with fungi attractive to mites being dispersed more (Hubert et al. 2003); and (3) grain contamination by fungi which are pathogenic to mites (Armitage and George 1986). The migration of T. putrescentiae populations in a wide range of ecosystems is known to contribute to the dispersal of viable spores of several fungal species, which can be transported on the vector’s body surface or deposited with their feces, rapidly spreading the spores throughout the substrate on which they live (Nesvorná et al. 2012; Franzolin et al. 1999; Hubert et al. 2004). Fungi may benefit from the dispersal of spores attached to the body surface or of undigested spores in the excreta (Hubert et al. 2003; Griffiths et al. 1959). In addition, mite grazers are attracted by fungal volatiles (Vanhaelen et al. 1980). These interactions promote the dissemination of fungi throughout the stored grains, influencing both pests.

Molds and yeasts are widely disseminated by air, dust, fomites, plants and animal microbiota. Although there are few reports of human pathogenic fungi in stored food, these fungi are found in the environment (Mohapatra et al. 2017). Therefore, cross-contamination of stored food and feed by human pathogenic fungi, which are transported by mites from their primary environmental habitats, is feasible. Food contamination with human pathogenic yeasts has already been reported, and virulence factors of foodborne yeasts demonstrate a potential risk to human health (Rajkowska and Kunicka-Styczyńska 2018). Furthermore, the presence of mycotoxigenic fungi in stored grains is well known (Mediavilla et al. 1996), as well as the presence of fungal species whose spores may be important as allergen-producing agents for humans, which could be carried by mites (Hubert et al. 2004; Walsh and Dixon 1996). In addition, T. putrescentiae has received attention as one of the leading causes of allergic asthma, allergic diseases, and rhinitis in humans (Arlian et al. 1984; Nuñez et al. 2016). Anaphylaxis after eating T. putrescentiae-contaminated food has already been described (Matsumoto et al. 1996). Therefore, studies on interactions between mites and human pathogenic fungi are urgently required.

Our main objective was to expand the current knowledge concerning the interaction between mites (in particular T. putrescentiae) and fungi, elucidating whether (I) T. putrescentiae can disperse and sustain population growth on human pathogenic fungi as well as on fungi isolated from stored food; (II) T. putrescentiae fitness is influenced by fungal species or cell morphology (filamentous x yeast-like fungi); and (III) T. putrescentiae preferentially disperses fungal species that provide it with the best performance.

Materials and methods

Stock colonies of Tyrophagus putrescentiae

Individuals of T. putrescentiae were obtained from cornmeal provided by an animal-feed producer in Teutônia, Rio Grande do Sul State, Brazil. The stock colony was initiated approximately 8 months before the beginning of the study. The colonies were maintained in a plastic Petri dish (15 × 2.5 cm) placed on a layer of foam matting continuously moistened with distilled water inside the dish. The edges of the dish were covered with a layer of cotton wool to prevent mites from escaping. Each colony unit was filled up with dry yeast (Saccharomyces cerevisiae), which was used as food source for the mites, and environmental conditions were not controlled. Unsexed adults were used in the assays.

Fungal cultures

Two groups of fungi were used in the experiments: eight environmentally important species, isolated from samples of cornmeal and rice flour using the method set forth by Normative Instruction (IN) no. 62 of August 26, 2003 (Brazilian Ministry of Agriculture, Livestock and Food Supply—MAPA: Ministério da Agricultura, Pecuária e Abastecimento); and 16 isolates, each with a medically relevant fungal species or genus maintained in the Culture Collection of the Federal University of Rio Grande do Sul (UFRGS), Brazil. One week before the experiments, each fungus was spread in Petri dishes containing Sabouraud agar with chloramphenicol (0.24 g/L) and cultures were incubated in a climate chamber at 25 ± 1 °C. The list of fungal species is described in Table 1.

Table 1 Eight environmentally important fungal species isolated from food samples and their GenBank accession numbers and 16 medically important fungal species from the Culture Collection of Federal University of Rio Grande do Sul (UFRGS) used in the experiments
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Identification of fungal species

The identification of the clinical isolates was maintained as they were received. Identification of stored food fungi at the genus level was performed through macro- and micromorphological observations of the isolates. The genomic DNA of the isolates was extracted using Power Soil DNA Isolation Kit® (MoBio, USA), following the manufacturer’s guidelines. Polymerase Chain Reaction (PCR) conditions and primers for identifications of environmentally important fungi are in Table 2. The PCR was comprised of primers described in Table 2; 1 × buffer PCR (Invitrogen); 2 mM magnesium chloride for β-tubulin gene (Ben-A), elongation factor 1α gene (EF-1α); and 3 mM for Internal Transcribed Spacer (ITS) and part of calmodulin gene region (Calm); 0.12 mM dNTP mix for ITS and 0.4 mM for the other regions; 0.04 U Taq DNA polymerase for ITS and 0.03 U Taq platinum DNA polymerase (Invitrogen) for the other regions; and 5 µL of DNA. The PCR products were purified using ExoSAP-IT (Affymetrix, USA) according to the manufacturer’s instructions. Sequencing was performed in an ABIPRISM 3100 Genetic Analyzer (Applied Biosystems). In all environmental isolates, ITS rDNA region sequencing was compared with the type strains deposited in GenBank using the Basic Local Alignment Search Tool (BLAST) algorithm. To confirm Penicillium and Aspergillus species, calmodulin was also compared to the type strains (Samson et al. 2004, 2014). Phylogenetic trees were performed using sequencing of ITS, Ben-A, and EF-1α to identify Fusarium species (Watanabe et al. 2011), whereas ITS and EF-1α were required for the identification of Trichoderma species (Druzhinina et al. 2008).

Table 2 Identification methods of environmentally important fungal species by sequencing
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Evaluation of Tyrophagus putrescentiae growth on fungal species

The isolates of 24 fungal species (eight environmental and 16 medically important species) were inoculated separately in the center of the Petri dishes (9 × 1.5 cm) containing Sabouraud agar with chloramphenicol, and incubated at 25 ± 1 °C for 1 week, in triplicates. The study was divided in two phases. The first phase started 1 week after fungal inoculation, when 50 mites were added to each previously inoculated Petri dish. The dishes were covered with Parafilm M® (Bemis NA, Neenah, Wisconsin, USA) to prevent mites from escaping. The Petri dishes were incubated at 25 °C for 28 days and observed at weekly intervals using a stereoscopic microscope Leica EZ4 HD with a digital camera (Leica). After the 28th day, mites (live immature stages and adults) and eggs were counted in each Petri dish. Afterwards, the second phase of the study was initiated.

Tyrophagus putrescentiae spread of fungal species to new Petri dishes

After the end of the first phase, 50 mites or less (according to the maximum obtained) from each replicate of fungal species were collected using a sterile brush. Mites were collected outside visible fungal colonies and transferred into Petri dishes containing Sabouraud agar with chloramphenicol (0.24 g/L). The Petri dishes were covered with Parafilm, incubated at 25 °C for 28 days, and observed at weekly intervals by taking photos. On the 28th day, mites (immature stages and adults) and eggs were counted in each Petri dish.

Control studies

Two types of control studies were performed: (1) one replicate containing each fungal species and no mites, and (2) a triplicate containing only mites (no fungus) to check whether T. putrescentiae was contaminated by a different microorganism than the one with which it was fed (dry yeast—S. cerevisiae). Both controls were performed in Petri dishes containing Sabouraud agar with chloramphenicol (0.24 g/L). Control plates (1) were monitored for 21 days to evaluate fungal growth in the absence of mites. The aim of control (1) was to observe normal fungal growth without interference from mites to evaluate if mites in the experiments were consuming the fungi. Control (2) was monitored for 7 days to evaluate mite contamination. Photos were taken to show that no contamination by other microorganisms occurred, and to show fungal growth without mites.

All experiments were conducted in a climate chamber (EletroLab EL 202) at 25 ± 1 °C and 80 ± 5% r.h. in the dark. All materials used during the study were sterilized using autoclave or UV ray.

Data analysis

Population growth response to diet was studied using Kruskal–Wallis test. Differences among fungal species were compared using Student–Newman–Keuls post hoc tests. Both tests were performed using the BioEstat 5.0 statistical program (α = 0.05) (Ayres et al. 2007).

Results

Identification of environmentally important fungi

Isolates obtained 99 or 100% of identity and ≥ 97% of cover with type strains of each fungal species. Identification and ITS region GenBank accession numbers of the isolates are show in Table 1.

Development of Tyrophagus putrescentiae population on fungi

Mite population increased when feeding on most fungal species, whereas it decreased or showed a non-significant increase in the presence of Rhizophus azygosporus, Sporothrix sp., Aspergillus terreus, Aspergillus fumigatus, Aspergillus niger, Aspergillus oryzae, and Aspergillus flavus (Table 3). The highest population increases were on Trichophyton mentagrophytes, Alternaria sp., Microsporum gypseum, and Aspergillus chevalieri (Kruskal–Wallis test: H ratio = 68.44, df = 23, p < 0.05) (Table 3). With Fusarium guttiforme and the medically important fungi Microsporum canis, M. gypseum, T. mentagrophytes, and Sporothrix sp., mites were observed to feed on whole mycelium on day 28, ‘clearing’ the plates (Fig. 1). Total mortality of individuals was observed only on A. flavus, as mite population did not survive until the end of the 28-day period.

Table 3 Mean (± SD) population growth (no. mites per replicate) of Tyrophagus putrescentiae on environmentally and medically important fungal species
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Fig. 1
figure 1

Fungal species utilized in the first phase of experiment. Initially (after 1 week of fungal inoculation, 50 Tyrophagus putrescentiae were added), and after 7, 14, 21 and 28 days with mites

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From the 24 fungal species tested, only eight formed colonies in the new Petri dishes after transfer by T. putrescentiae (second phase). Therefore, mite population increase was calculated only for these eight species (Table 4). Aspergillus clavatus, Candida tropicalis, Candida albicans, F. guttiforme, Hyphopichia burtonii, Penicillium citrinum, R. azygosporus, and T. mentagrophytes were the fungal species that were dispersed, showing positive mite growth and used as food by mites. Tyrophagus putrescentiae populations showed better performances on F. guttiforme, P. citrinum, and T. mentagrophytes when compared with the others (Kruskal–Wallis test: H-ratio = 18.59, df = 7, p < 0.05) (Table 4; Fig. 2). Although it had negative growth rates in the first phase when feeding on A. fumigatus and A. niger, T. putrescentiae dispersed these fungi to new plates, but could not keep their colonies. Tyrophagus putrescentiae showed negative population growth on R. azygosporus in the second phase, reinforcing the poor growth obtained in the first phase on this fungal species. The controls confirmed that the mite stock was not contaminated by fungi other than S. cerevisiae, with which it was fed during storage, and experimental conditions were suitable for fungal development (data not shown).

Table 4 Mean (± SD) population growth (no. mites per replicate) of Tyrophagus putrescentiae on dispersed fungal species
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Fig. 2
figure 2

Fungal species utilized in the second phase of experiment, showing the effects of Tyrophagus putrescentiae grazing on fungal species after 7, 14, 21 and 28 days

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Discussion

This is the first study on the specific population growth of T. putrescentiae on several fungi, particularly some medically important species. Tyrophagus putrescentiae population increased when feeding on several fungi species, dispersed and kept feeding on the environmental fungi F. guttiforme, H. burtonii, P. citrinum, and R. azygosporus (isolated from food samples) and the medically important fungi A. clavatus, C. tropicalis, C. albicans, and T. mentagrophytes. The consumption of these fungal species resulted in a mite population explosion. The growth on other tested fungal species was not as significant, but mite populations increased on most fungi. Fungi are known to stimulate mite population growth, especially the fungivorous ones (Nesvorná et al. 2012; Hubert et al. 2004).

Although mite growth on the medically important fungi maintained in Culture Collections is known, and T. putrescentiae has already been demonstrated to feed on the spores and hyphae of all the dermatophytes, other moulds, and yeasts (Duek et al. 2001), it was quite surprising to observe the sharp population growth of mites on several human pathogenic fungi.

The yeast-like H. burtonii is known as ‘chalky mould’, and can spoil foods through powdery and filamentous colonies due to the fragmentation of hyphae into short lengths (Deschuyffeleer et al. 2011). This is the first study that reports the interaction between mites and H. burtonii. The latter is known to produce powerful amylases (Takeuchi et al. 2006), and could provide support to mite digestion on stored products such as cereals and grains. It is a clearly beneficial interaction for the mite while it supports fungal dispersion, and this kind of interaction may occur with other fungal species, as well. The experiments in the present study were carried out in Sabouraud agar, which has glucose as its main carbon source. It would be interesting to evaluate the interaction between mites and yeast in a medium containing starch as carbon source to see whether stored-product mites could actually benefit from amylase production by the yeast. Yeasts and arthropods are known to play an important role on each other’s development. For instance, yeast spores can survive digestion by Drosophila melanogaster (Diptera), which suggests that these flies can serve as effective vectors of yeasts under natural conditions (Reuter et al. 2007). On the other hand, larvae of these insects show preference for yeast species that lead to faster development and increased adult body weight (Anagnostou et al. 2010).

Duek et al. (2001) reported an association between T. putrescentiae and species belonging to the yeast genus Candida. Our study demonstrated that T. putrescentiae was able to grow and disperse on some human opportunistic yeast pathogens (C. albicans and C. tropicalis) while others were not dispersed although mites were able to develop on them (C. parapsilosis and Trichosporum sp., Tables 3 and 4). As the four species form pseudohyphae and/or true hyphae, cell morphology does not seem to explain the lack of dispersal of C. parapsilosis and Trichosporum sp. in the present study.

The high development and dispersal ability of T. putrescentiae on T. mentagrophytes, which is an etiological agent of dermatophytosis, is unsettling. Trichophyton mentagrophytes is considered a zoonotic species, and can be transmitted from animals to humans through direct contact. Therefore, the relationship between animal-mite-human in household environments may maximize clinical cases of dermatomycosis caused by this fungus. The association of T. mentagrophytes and mites belonging to the genus Cheyletiella (Acari: Cheyletidae) was shown to cause intensely itchy papules with necrotic areas on the skin areas in contact with animals (Dobrosavljevic et al. 2007). Thus, T. putrescentiae bites could transmit dermatophytes to human hosts, and this study highlights the great potential of T. putrescentiae to act as a host to human pathogenic fungi.

Although T. putrescentiae was able to develop on E. floccosum, M. canis, M. gypseum, and T. rubrum in the first phase, these fungi were not dispersed. The contrast between the dispersal of T. mentagrophytes and the lack of dispersal of the other dermatophytes in the present study reinforces that fungal cell morphology does not play a role in dispersal by mites.

The positive growth of T. putrescentiae feeding on A. clavatus in the two study phases represents a potential risk as both pests develop on cereals that can be used in animal feed (Varga et al. 2003). Aspergillus clavatus produces a neuromycotoxin that affects ruminants after ingestion of contaminated feedstuff (Botha et al. 2018) and, as T. putrescentiae is the most abundant and predominant mite species found in cereal-based food products, the association with A. clavatus is disturbing. The interaction between mite and fungus could occur in stored products (Kheradmand et al. 2007), processing and packaging areas of feed factories (Rybanska et al. 2016).

Even pathogenic or mycotoxigenic fungal species that resulted in negative growth or no growth of mite populations could be disseminated to the second phase. This is the case of two Aspergillus species (A. fumigatus and A. niger) tested in this study. Sinha (1966) showed that A. niger was rejected by astigmatid mites, which corroborates our results, since T. putrescentiae is also classified as belonging to the Astigmatina cohort. A possible explanation is that T. putrescentiae cannot feed on these species or their nutritional value is very low to sustain mite population. The dissemination of fungi which are not used as food by mites points to a fortuitous dispersal of fungal spores attached to mites’ bodies, regardless of any interaction between mites and fungi.

The fact that T. putrescentiae grew well on A. chevalieri but could not disperse it is interesting, as the latter is a species reported to cause opportunistic cutaneous aspergillosis (Naidu and Singh 1994) (Tables 3 and 4). Although no study on Aspergillus has been found, Hubert et al. (2014) investigated the effect of different T. putrescentiae densities on Fusarium poae transmission on non-sterile barley grains, and observed that high densities of fungus were overgrazed, while lower mite population density supported the transfer of F. poae. The present study did not address the effect of mite density, but it could be a likely explanation for T. putrescentiae behavior towards A. chevalieri. Alternatively, studies on A. chevalieri survival through mite digestive tract could help to elucidate this issue.

Tyrophagus putrescentiae could not survive in the presence of A. flavus in the experimental conditions of the present study. Franzolin et al. (1999) observed the growth of T. putrescentiae in the presence of A. flavus and using maize grains as food source, and observed an effective dispersal of viable fungal spores from the inoculated compartment to the uncontaminated one. The same authors reported an increase in aflatoxin concentrations whenever the mite was present. Notwithstanding, according to Rodrigues et al. (1984), aflatoxins can generally prevent or reduce mite oviposition but do not affect T. putrescentiae. Instead, A. flavus and A. clavatus, which could also produce mycotoxin, caused an astonishing increase in mite population. Therefore, the mycotoxin production of these fungal isolates could be evaluated to check the correlation between mycotoxin and mite survival. The opposite growth behavior of T. putrescentiae population on the various Aspergillus species evaluated does not seem to be related to fungus phylogeny, as both A. clavatus and A. fumigatus belong to Aspergillus section Fumigati, and mites hardly grew in presence of the latter.

Although this study demonstrated that it is difficult for T. putrescentiae populations to develop on Sporothrix, this fungus has been recently reported as partner in a new fungus-mite mutualism mediated by birds (Theron-De Bruin et al. 2018). The mite species Glycyphagus sp. and Proctolaelaps vandenbergi were abundant in inflorescences of Protea trees and on cape sugarbirds, carried Sporothrix fungal spores regularly, and were capable of using the fungus as food source. These findings emphasize that fungus-mite associations may be specific, and therefore, generalizations should be postulated with caution.

We demonstrated that T. putrescentiae was able to use F. guttiforme as food source, confirming the suitability of Fusarium species to support mite growth (Nesvorná et al. 2012; Hubert et al. 2012). Hubert et al. (2012) demonstrated changes in bacterial community associated with T. putrescentiae after shifting to Fusarium diets, suggesting a preference for Bacillaceae species known as chitinase producers, which might participate in fungal mycelium hydrolysis. F. guttiforme is a well-known plant pathogen which causes pineapple fusariosis in Brazil (Ploetz 2006) and can contaminate stored grains with mycotoxins (Bottalico and Perrone 2002); however, it is still hard to determine whether such mite-fungus interaction would lead to the suppression of F. guttiforme growth in fruits. Based on our findings, we suggest that infestations of T. putrescentiae could disseminate the fungus on different types of food, reaching a high economic damage level.

Penicillium citrinum and Penicillium aethiopicum produce mycotoxins responsible for intoxication in humans and animals (Frisvad et al. 2004; Rosa 1986). Although T. putrescentiae was able to grow on both fungi in the first experiment phase, only P. citrinum was dispersed and allowed for mite development in the second phase. Differential influence of Penicillium species has already been demonstrated for mites GIycyphagus domesticus and Histiostoma sp.; some species are suitable for mite multiplication, while others were toxic for mites (Racovitza 1969). Tyrophagus putrescentiae could support the dissemination of P. citrinum, as well as other mycotoxigenic fungi, in storehouses, mainly when kept under unsatisfactory sanitary conditions.

In this study, the fungus R. azygosporus, which has been reported associated with zygomycosis (Ribes et al. 2000), was isolated from the food sample. The weak population growth rate of T. putrescentiae in the first phase and its negative growth in the second phase could be explained by the high density of filaments of R. azygosporus, possibly preventing mite motility when grazing on fungal mycelium. In spite of that, T. putrescentiae was capable of successfully dispersing R. azygosporus. Therefore, T. putrescentiae demonstrated potential for R. azygosporus transmission and could infect immunosuppressed hosts either in household environments or in hospitals under unsatisfactory sanitary conditions.

Two factors are determining for a successful interaction: the mite’s ability to use the fungus and the digestibility of a particular fungal species (Maraun et al. 2003; Pankiewicz-Nowicka et al. 1984). The reason why T. putrescentiae did not develop its populations on several fungi might be associated with fungal digestibility. To understand fungal digestibility, it is important to know that ancestors of storage mites were mycophagous (O’Connor 1982), and they have been found to host bacterial communities in the gut, parenchymal tissues, and reproductive tract (Kopecky et al. 2014). Also, T. putrescentiae is known to acquire bacteria and fungi (Trichoderma spp.) with chitinolytic activity to digest chitin from fungal cell walls (Smrž et al. 1991; Smrž and Čatská 2010), and its feeding habits change due to the bacterial community associated with the gut and parenchymal tissues (Smrž 2003). Mites produce bacteriolytic enzymes that hydrolyze the cell walls of gram-positive bacteria, showing that microorganisms can either enable or hamper both mite fitness and population growth (Erban and Hubert 2008; Erban et al. 2016). Several fungal species differ in the chemical structures of their cell walls, with a diversity of chitins and many types of chitinolytic enzymes that are specific to such substrates (Gow et al. 2017). Smrž et al. (2016), using histological methods and fluorescence microscopy, proved that there is a nearly symbiotic relationship between chitinolytic bacteria and digested fungi (spores and mycelium) associated to T. putrescentiae. It is possible that the many cases where mites did not feed on fungi could be related both to the associated chitinolytic bacteria efficiency and/or to the resistance of fungal spores to hydrolysis. Therefore, one possible inference is that these factors could affect the digestibility of fungi by mites.

Another possible explanation for the inability of T. putrescentiae to grow on some fungal species could be the size of fungal spores, which could impair fungal passage through the buccal apparatus of mites. However, as the average range of fungal spores is 2–15 µm and the pharynx of mites can be distended from 2 to 3 µm up to 20 µm to accommodate solid structures (Colloff 2009), we do not believe that spore size was a limiting factor for the use of fungi as food by mites. Even when fungi presented cellular structures larger than the upper limit for distension of the mouth apparatuses of mites, as is the case of P. citrinum, which has giant cells (500–1000 μm) (Katoh et al. 1978), T. putrescentiae was capable of multiplying on it, probably through fungal mycelia ingestion. Smrž et al. (2016) stated that chitinolytic enzymes seemed to be unnecessary in the digestion of spore contents, and spore walls were mechanically broken by T. putrescentiae chelicerae so that their contents could be digested. The buccal apparatus of mites can break fungal cell walls (spores and/or hyphae) allowing them to feed on different fungal diets (Smrž et al. 2016; Silva et al. 2018).

Fungal pigmentation could interfere on mite palatability, as mites were observed to be grazing more on white hyphae than pigmented ones. For instance, the consumption of white mycelium of F. guttiforme, T. mentagrophytes, M. canis, and M. gypseum was observed (Fig. 2). Fungal pigments are known as environmental stress protectors, and the ingestion of fungal conidia by amoeba was higher when conidia were devoid of the fungal spore pigment (Hillmann et al. 2015). In fact, the melanized surface of some fungal conidia has been found to protect against the model amoeba Dictyostelium discoideum (Novohradská et al. 2017).

Although mites increased their populations at the expense of most fungi tested, dispersal was selective and might vary according to mite species (Hubert et al. 2003). For example, mites had high population growth on Alternaria sp., M. canis, M. gypseum, and A. chevalieri in the first phase, but were not able to disperse these fungal species.

We conclude that T. putrescentiae dispersed and sustained its population growth on human pathogenic fungi as well as on fungi isolated from stored food, and could act as a dissemination vector for medically important fungi. According to our results, we can partly consider that T. putrescentiae preferentially disperses the fungal species that provide it with best fitness. Cell morphology (filamentous × yeast-like fungi) did not influence T. putrescentiae fitness, but there was a differential effect associated to fungal species. Although we were not able to explain this differential effect, we suggest it might be related to fungal cell composition, to the potential resistance to cell wall hydrolysis by chitinases, and to the presence of pigments.