Perfect shelter: plant architecture and its influence on pests and natural enemies

Leaf domatia are small natural structures that have different shapes, such as invaginations, cavities, pockets (with or without hairs), tufts of hairs, etc. existing on the lower surface of the leaves (abaxial surface), from the base of the limb to approximately 2/3 of its length. Domatia are located at the junctions of the veins, that is, in the smaller angle between the central vein and the secondary veins of certain species of dicotyledons (rarely in monocots) (Figure 1).

Domatia exist in plants of several species and more than 30 families of woody angiosperms around the world (spermatophyte plants whose seeds are protected by a structure called fruit), with abundant occurrence in tropical and subtropical forests. These leaf structures can vary in quantity, development and shape according to environmental conditions.

In 1864, “small articulated octopod animals and their eggs”, that is, mites, had already been observed inside small cavities existing in the angles of union between the median and secondary veins of coffee trees, Arabic coffee L., (today called domatia). The term domatia or acarodomacy was used for the first time in 1887, therefore, 127 years ago, by a Swedish researcher, after observations that these structures served as shelter and home for mites (from the Greek domatium = small house).

Although some researchers, most of them botanists, consider that leaf domatia are useful only as morphological characteristics and of only taxonomic interest, as there are no known physiological functions for them, others suggest that these structures harbor mites that promote benefits for plants.

Some evidence demonstrates the existence of mutualism between plants that have leaf domatia and mites, such as, for example, (1) the occurrence of mites within the domatia, (2) the presence of domatia increases the chance of mites being found on plants and ( 3) mite activity increases the chances of finding plants with domatia. The observation of the appearance of predatory mites in and around domatia on numerous plants allows us to consider the possibility of facultative mutualism between mites and domatia.

Domatia may therefore represent the most abundant, ancient and widely distributed form of mutualism between plants and arthropods.

Research has shown that there are interactions between some morphological characteristics of plants, such as trichomes (appendages of the epidermis present in various plant organs, constituting their clothing), hairiness, domatia, etc. and natural enemies of pests, which can somehow influence the capacity of these organisms in reducing pest arthropod populations.

There is, therefore, a broad facultative mutualism between domatia and beneficial mites (predators and fungivores), in which leaf domatia serve as shelter and breeding grounds, which, in turn, reduce the number of phytophagous arthropods and pathogens found on plants.

Mites can be observed in the domatia of plants of different species, which suggests that the mites find their food there. However, this may not be the rule, as many studies reject the hypothesis that there is mutualism between mites and domatia, because they do not always contain mites. There are domatia with a complete absence of mite development inside them and there is also insufficient information about mite and domatia associations.

The presence of mites has been reported Tydeus sp. (Tydeidae), Agistemus sp. (Stigmaeidae), Typhlodromus haramotoi (Prasad, 1968) (Phytoseiidae), among others, in coffee leaf domatia, C. arabica, and Bdella sp. (Bdellidae) and Amblyseius herbicolus (Chant, 1959) (Phytoseiidae) in Coffea liberica bull

Probably, the Tydeidae and Iolinidae mites are the most found in domatia and for this reason, mites from these families are commonly called domatia mites, mites that may also be serving as food for predatory mites, even as an alternative food. Tideids are found in coffee trees at any time of the year, however, apparently without causing any harm.

Domatia can also harbor microbiophagous mites, that is, those that feed on “microbes” and thus favor plants by consuming phytopathogenic fungi or epiphytes, resulting in a reduction in the severity of plant diseases such as, for example, downy mildew, plasmopara spp., Phytophthora infestans (Peronosporaceae) etc.

Some phytophagous mites can cause serious problems for the health of plants, but they have numerous natural enemies, especially belonging to the Phytoseiidae family of predatory mites. A potential benefit that plants gain is that predatory mites can act as their “bodyguards" against pest mites. In addition to mites, leaf domatia can also occasionally harbor small insects such as thrips and stink bug nymphs, possibly also predators, and mealybugs.

Predatory mites and also those that feed on decomposing material (detritivores), fungi (fungivores) or other microbes, represent 90% of the arthropods found within leaf domatia. All are considered beneficial for the plant, none are considered harmful, the first because they are natural enemies of mites and small insects, and the fungivores because they help to reduce pathogens and mobilize nutrients sequestered by fungi, algae, yeast bacteria, lichens, etc. .

The domatia of coffee trees serve as shelter and oviposition site for the predatory mite Iphiseiodes zuluagai Denmark & ​​Muma, 1972 (Phytoseiidae) (Figure 2), one of the mites that have been studied in maintaining coffee tree pest mites in balance. This is an indication of the importance of domatia as a place and source of their survival, suggesting a mutualistic plant-predator interaction and certainly for other species of predatory mites also found on coffee plants.

Research results show that Arabica coffee trees (C. arabica) have many developed domatia and approximately 70% more domatia than Robusta and Conillon (Coffea canephora Pierre & Froehner), where domatia are scarce and poorly defined. It is believed that this is why Arabica coffee trees have around eight times more predatory mites of the species I. zuluagai and up to approximately 0,7 times fewer pest mites [Brevipalpus phoenicis (Geijskes, 1939) (Tenuipalpidae) - (Figure 3) and Oligonychus ilicis (McGregor, 1917) (Tetranychidae)] than C. canephora and this can also be explained due to the positive effect of domatia on predator survival.

Domatia still contribute to the reduction, in C. arabica, of the cannibalism that exists between the adult predatory mite of I. zuluagai on the young of its own species, a factor equally favorable to the increase in the predator's population.

Everything indicates that the most obvious benefit of a leaf domatia to the predatory mite is to offer protection and shelter, especially as a place to lay its eggs and change phase (molt) during its development cycle. Several studies have demonstrated the use of domatia by Phytoseiidae preferentially for oviposition and molting. Under field conditions, more than 75% of all eggs laid by phytoseiids have been found within domatia. Laboratory tests have shown that leaf domatia protect eggs from the effects of low humidity, and in the presence of domatia, a predatory mite lays twice as many eggs as in its absence.

Only since the 90s has the response of mites to plant architecture been considered, but it is clear that structures that may exist on the leaf surface alter the abundance of mites, influence predator-prey interactions and are important for understanding the relationship between seedling mites and plants.

Mites found in coffee leaf domatia in Brazil

Species	Families	References
-	Iolinidae	Spongoski et al., 2005
Agistemus brasiliensis Matioli, Ueckermann & Oliveira	Stigmaeidae	Mineiro et al., 2006
Amblyseius aerialis (Muma)	Phytoseiidae	Mineiro et al., 2006
Bdella sp.	Bdellidae	Mineiro et al., 2006
Brevipalpus phoenicis (Geijskes)	Tenuipalpidae	Mineiro et al., 2006
Daidalotarsonemus sp.	Tarsonemidae	Mineiro, 2006
Euseius citrifolius Denmark & ​​Muma	Phytoseiidae	Spongoski et al., 2005 Mineiro et al., 2006
Euseius concordis (Chant)	Phytoseiidae	Mineiro et al., 2006
Homeopronematus sp.	Iolinidae	Mineiro et al., 2006
Iphiseiodes zuluagai Denmark & ​​Muma	Phytoseiidae	Matos et al., 2006
Lorrya beautiful Cooreman	Tydeidae	Spongoski et al., 2005 Mineiro et al., 2006
Lorrya sp.	Tydeidae	Spongoski et al., 2005 Mineiro et al., 2006
Oligonychus ilicis (McGregor)	Tetranychidae	Mineiro, 2006
Parapronematus acaciae	Iolinidae	Spongoski et al., 2005
Saproglyphus sp.	Winterschmidtiidae	Mineiro al., 2006
Spinibdella sp.	Bdellidae	Mineiro et al., 2006
Tarsonemus confusus E	Tarsonemidae	Spongoski et al., 2005
Tarsonemus sp.	Tarsonemidae	Mineiro et al., 2006
Triophtydeus sp.	Meyexellidae	Mineiro et al., 2006
Typhlodromus camelliae (Chant & Yoshida-Shaul)	Phytoseiidae	Mineiro, 2006
Tyrophagus sp.	Acaridae	Mineiro, 2006
Zetzellia malvinae Matioli, Ueckermann & Oliveira	Stigmaeidae	Mineiro et al., 2006
Zetzellia sp.	Stigmaeidae	Spongoski et al., 2005

Species

Families

References

-

Iolinidae

Spongoski et al., 2005

Agistemus brasiliensis Matioli, Ueckermann & Oliveira

Stigmaeidae

Mineiro et al., 2006

Amblyseius aerialis (Muma)

Phytoseiidae

Mineiro et al., 2006

Bdella sp.

Bdellidae

Mineiro et al., 2006

Brevipalpus phoenicis (Geijskes)

Tenuipalpidae

Mineiro et al., 2006

Daidalotarsonemus sp.

Tarsonemidae

Mineiro, 2006

Euseius citrifolius Denmark & ​​Muma

Phytoseiidae

Spongoski et al., 2005

Mineiro et al., 2006

Euseius concordis (Chant)

Phytoseiidae

Mineiro et al., 2006

Homeopronematus sp.

Iolinidae

Mineiro et al., 2006

Iphiseiodes zuluagai Denmark & ​​Muma

Phytoseiidae

Matos et al., 2006

Lorrya beautiful Cooreman

Tydeidae

Spongoski et al., 2005

Mineiro et al., 2006

Lorrya sp.

Tydeidae

Spongoski et al., 2005

Mineiro et al., 2006

Oligonychus ilicis (McGregor)

Tetranychidae

Mineiro, 2006

Parapronematus acaciae

Iolinidae

Spongoski et al., 2005

Saproglyphus sp.

Winterschmidtiidae

Mineiro al., 2006

Spinibdella sp.

Bdellidae

Mineiro et al., 2006

Tarsonemus confusus E

Tarsonemidae

Spongoski et al., 2005

Tarsonemus sp.

Tarsonemidae

Mineiro et al., 2006

Triophtydeus sp.

Meyexellidae

Mineiro et al., 2006

Typhlodromus camelliae (Chant & Yoshida-Shaul)

Phytoseiidae

Mineiro, 2006

Tyrophagus sp.

Acaridae

Mineiro, 2006

Zetzellia malvinae Matioli, Ueckermann & Oliveira

Stigmaeidae

Mineiro et al., 2006

Zetzellia sp.

Stigmaeidae

Spongoski et al., 2005

Captions of figures cited in the text

Figure 1 - Lower leaf surface (abaxial surface) of coffee tree, Coffea arabica, showing domatia in the smaller angles between the central vein and the secondary veins. Photo: Paulo Rebelles Reis

Figure 2 - Adult female Iphiseiodes zuluagai (Phytoseiidae) after depositing an egg inside the leaf domatia of a coffee tree, Coffea arabica, (left), and mite larva of the same species inside the domatia (right). Photo: Paulo Rebelles Reis

Figure 3 - Adult female Brevipalpus phoenicis (Tenuipalpidae) inside the domatia (left) and leaving the leaf domatia of coffee plants, Coffea arabica, (right). Photo: Paulo Rebelles Reis