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The Handbook of Mites of Economic Plants: Identification, Bio-Ecology and Control

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Mites pose a serious problem to plants worldwide, attacking crops and spreading disease. When mites damage crops of economic importance the impacts can be felt globally. Mites are among the most diverse and successful of invertebrates, with over 45,000 described species, with many more thousands to be discovered. They are responsible for a significant portion of the losses of crops for food, fibre, industry and other purposes, and require expensive and often controversial pest control measures. Understanding these mites is vital for entomologists, pest researchers, agronomists and food producers. Knowledge of mite pests helps to inform control strategies and optimize the production of economic plants and the agrarian economy. This encyclopedia provides a thorough coverage of the mites and the problems they cause to crops, yet it is easily searchable, organised by mite species and subdivided into helpful headings. It takes a worldwide view of the issue of mites injurious to economic plants, describing mites prevalent in different regions and discussing control methods appropriate in different environments.æThis book provides an encyclopaedic reference to the major mites, described by family in terms of their internal and external morphology, bio-ecology and family systematics. Methods of mite collection and laboratory study is described, as well as species diagnostic characteristics, worldwide distribution, host plants, identification by the type of damage they cause and control strategies, including chemical and biological intervention and integrated pest management measures. Mites of the following families are included: (Eriophyoidea, Tarsonemidae, Tuckerellidae, Tenuipalpidae, Tetranychidae, Acaridae, Penthaleidae). Mites of Economic Plants is an important resource for students of entomology and crop production, and as a thorough reference guide for researchers and field workers involved with mites, crop damage and food production.

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23 Chapters

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1: Introduction to the Acari


1  Introduction to the Acari

Systematic Position and Ecological Role

The Acari, or mites, are small animals; the adults range from

300 to 500  μm in body length, except for some eriophyoids which are approximately 100 μm long and certain ticks whose females measure about 30,000  μm long. They belong to the phylum Arthropoda, a monophyletic taxon of terrestrial and marine invertebrates (Weygoldt, 1998) which are characterized by jointed legs and a chitinous exoskeleton. Two groups of

Arthropoda, the Pantopoda and the Chelicerata, lack antennae and mandibles, and molecular analyses have shown that the

Chelicerata is a sister taxon of a clade including the Crustacea and the Insecta (Telford and Thomas, 1998). From a systematic point of view, the Chelicerata is a subphylum that includes the class Arachnida, a primarily terrestrial group that includes the subclass Acari along with several orders (Amblypygi,

Araneae, Opiliones, Palpigradi, Pseudoscorpionida, Ricinulei,

Schizomida, Scorpiones, Solifugae and Uropygi) (Weygoldt and Paulus, 1979a,b). Members of the subclass Acari lack opisthosomatic spinnerets and conspicuous primary segmentations (or tergites arranged segmentally). The Acari includes the superorders Acariformes and Parasitiformes, and is morphologically differentiated from other relatively simple arachnids (Krantz, 2009a). Adults of the Acari usually have four pairs of legs, with the exception of eriophyoids, which have two pairs. Their biological cycle progresses through the stages of egg, larva and nymph. The larva is six legged and the nymph eight legged. Another characteristic that sets the Acari apart from the other Arachnida is that the phase which hatches from the egg has fewer legs than subsequent phases, while the eggs of spiders, scorpions, pseudoscorpions and opilionids all hatch into eight-legged organisms.


2: External Morphology


2  External Morphology


Body Division

In the Acarina, the developing integument appears first as

­undifferentiated tissue, covered by a thin layer of ‘cuticulin’ and separated from the underlying ‘epidermis layer’ by a ‘Schmidt layer’. As development proceeds, the anatomical organization of the integument undergoes further transformation and shows from the outside inwards an ‘epicuticular layer’ (the epicuticle), a ‘procuticular layer’ (the procuticle), which consists of an outer

‘exocuticular layer’ and an inner ‘endocuticular layer’, an underlying Schmidt layer, an epidermal layer and, finally, a basal lamina set below the epidermis. This anatomical organization underlies the external ‘cerotegument’; this consists of an outer

‘cement layer’ and an underlying ‘wax layer’ that are set on the outer epicuticle and the underlying inner epicuticle (Fig. 2.1).

Together, the epicuticular complex – the cerotegument and the outer and inner epicuticle – provides multilayered protection. The cerotegument is a secreted layer that is formed by the epidermis, from which ‘pore canals’ travel towards the inner epicuticle, which includes an underlying cuticulin layer and a covering cuticulin layer. Overall, the cerotegument may have various consistencies, but its cement layer is dense and frequently sculptured. Together, the wax and cement layers of the cerotegument are involved in the regulation of water loss and/or water intake (Alberti et al., 1981; Norton et al., 1997).


3: Internal Morphology


3  Internal Morphology

Like other Arthropoda, the internal morphology of mites primarily involves the idiosoma, which includes the ‘haemocoel’, a cavity that extends also to the legs and surrounds the internal organs that constitute the different systems of the body

(circulatory, nervous, reproductive, glandular, digestive and excretory).

degree of sexual dimorphism may depend on neurosecretory development (Krantz, 2009a). The cholinergic system (acetylcholine, choline acetylase, cholinesterase) and synaptic action are basic to nerve function.

Supraoesophageal ganglion

Circulatory System

The haemocoel is filled with ‘haemolymph’, a free-flowing liquid whose circulation is facilitated by body movement and the dorsoventral contraction of the idiosomal muscles. The haemolymph contains various substances, such as amino acids (Boctor,

1972), lipids (Woodring and Galbraith, 1976), sugars (Aboul-Nasr and Bassal, 1971), etc. and several cellular elements, the ‘haemocytes’, which are adapted to different functions, such as clotting, macrophagy and tissue dissolution, the development of which may involve germinal cells (Evans, 1992; Alberti and


4: Biology


4  Biology

‘Biological instars’ and ‘reproduction’ are two basic factors of mite life. They affect the ecology of mite populations, and knowledge of their characteristics is of strategic importance in the control of injurious species.

typical morphology, size and colour. It is oval, long, flattened, or some other shape, with the external surface smooth, striate, reticulate, etc., and variously coloured, such as white, red or orange.

During the process of deposition, it usually has strong elasticity.

Biological Instars

The prelarva

The life cycle of Acari develops through the egg and six (sometimes more) biological instars that follow: the prelarva, larva, protonymph, deutonymph, tritonymph and adult. There are usually two or three nymphal instars between the larval instar and the adult. In no more than a few cases is there only a single nymphal instar, as in the ticks. Protonymphal, deutonymphal and tritonymphal instars are found in the Prostigmata, Astigmatina and some other acarine groups. The adult represents the final stage after a series of three or four moultings, although in some groups there may be post-imaginal moulting during the adult stages.


5: Ecology


5    Ecology

Study of the ecology of mites is a crucial step in the process of acquiring knowledge of mites (and other organisms), and includes traditional natural history, taxonomy, modern evolutionary and behavioural ecology, and theoretical models. Such studies can also provide insight into the evolution of plant mites. Here, the focus is on those aspects that help a better understanding of the dynamics of populations and on outbreaks of pest mites in the field. Readers interested in further insights can consult the contributions of Sabelis (1985a,c, 1996) or the more recent work of Saito¯ (2010), and other publications.

Feeding Habits and Habitats

The feeding habits of mites involve various aspects of their morph­ ology and lifestyle. Their morphological features (mouthparts, postoral digestive systems, etc.) usually reflect the ecological approach that these animals exhibit with respect to various food resources and habitats. From this viewpoint, morphology, habitats and behavioural patterns are interdependent and may markedly influence systematic features.


6: Collecting and Detecting, Preserving, Preparing and Rearing


6  Collecting and Detecting, Preserving,

Preparing and Rearing

The study and examination of mites, both live and dead, is carried out for identification purposes and/or to gain further knowledge of their bio-ecology. To accomplish these tasks, protocols for collecting, preserving, preparing and rearing the different mite categories and groups of mites have been developed over time. According to their bio-ecology, the study and collection of mites living on plants of economic importance involves the host plant, the soil, supports of a different nature around the plant, and sometimes the three habitats together.

Different analytical tools, such as light microscopy (using the dissecting microscope, phase contrast microscope or Nomarski interference microscope), electron microscopy (using the scanning electron microscope and the transmission electron microscope) and physico-chemical and biochemical methods

(electrophoretic analysis, molecular methods, etc.) can be employed. The aspects of mite collection treated in this chapter do not include sampling techniques and methods for estimating populations, which are covered in Chapter 9, on mite control.


7: Mites and Plant Damage


7   Mites and Plant Damage

Pest mites sensu stricto belong to the Tetranychoidea and

Eriophyoidea, both of which have mouthparts that are able to pierce plant tissues and suck out their contents. Other mite groups (Acaridae, Erythraeidae, Penthaleidae, etc.) have dif­ ferent mouthparts that are not strictly adapted to phytophagy, but are nevertheless also able to cause severe damage. The feeding mechanism, together with the plant response, determine the damage typology. Plant damage by mite pests has been

­extensively investigated in the Tetranychoidea and Eriophyoidea, but less so in the Tarsonemidae and other minor phytophagous groups. Sometimes, the symptoms can be easily taken for boron deficiency, or they may be confused with virus symptoms or even with herbicide action, such as on the new leaves of papaya infested by the broad mite, Polyphagotarsonemus latus (Banks).

The main part of this chapter is devoted to an account of the damage to plants that is caused by the main phytophagous groups of mites (Tetranychoidea, Eriophyoidea) and others


8: Mites as Biocontrol Agents of Weeds


8  Mites as Biocontrol Agents of Weeds

Weeds compete in agriculture in various ways. They may d

­ irectly affect the management of cultivated plants and reduce the yield, or act in other ways, such as by limiting the utilization of land for grazing. Weeds can be indigenous, exotic or cryptogenic

(neither demonstrably native nor introduced) (Carlton, 1996).

Herbicides comprise about 50% of all the agrochemicals sold worldwide (Woodburn, 1995), which compares with 30% for insecticides. The biological control of weeds could represent a desirable solution to this problem, and the use of arthropods to accomplish this was proposed in the 1830s (Goeden, 1988).

The strategy is to employ natural enemies to reduce the density of weeds to an acceptable level (Van Driesche et al., 2008). This type of control is usually applied against invasive weeds and requires the importation of natural enemies from their areas of origin. These natural enemies are herbivores (mites, insects, etc.) and must not damage other (accompanying) plant species.


9: Control


9    Control

Outbreaks of mite populations can have a serious impact on crops of economic plants, including yield losses, the high costs of mite control and/or undesirable ecotoxicological effects. In order to control such outbreaks, there is a need to understand the bio-ecology of mite pests and the factors regulating the development of their populations. Population monitoring, the assessment of damage and knowledge of the appropriate means and strategies for control are fundamental to making rational decisions. It is not possible to base decisions on knowledge acquired elsewhere, or to standardize control measures and strategies worldwide. Each mite species must be examined according to its environment, as this can variously influence the behaviour of its populations.

As with other injurious pests, the control of mites harmful to economic plants is achieved by physical, chemical, biological and other means – cultural, integrated pest management (IPM), etc. – according to the control strategy that is adopted. In this chapter, the general features of the strategies and means that are usually employed are discussed: physical control, chemical control, biological control (including the use of natural enemies) and IPM. Host plant resistance is discussed as a biological strategy mainly related to IPM. The use of genetically modified organisms (GMOs) is not considered as, in the opinion of the author, they lack any ecological foundation and are therefore considered to be environmentally harmful to serious agriculture.


10: Brief History of the Main Published Works on the Mites of Economic Plants


10  Brief History of the Main Published Works on the Mites of Economic Plants

The mites of economic plants are mainly included in the superfamily Eriophyoidea and the families Tetranychidae and

Tenuipalpidae. Other families, e.g. the Tarsonemidae and the

Penthaleidae, have relatively few injurious species. Summarizing the history of these mite groups according to their economic importance is very difficult because of the very large number of references. This brief history covers only the main works on economic acarology, and the references that are included on systematic and taxonomic aspects highlight the importance of basic knowledge in the intervention that is applied. The discussion is arranged by geographic area. The Mediterranean region is taken to include the North African countries, the Middle

East, Turkey and Cyprus; the northern Mediterranean countries are included in the section on Europe.


The European history of acarology follows for long stretches of time the world history of the discipline, in conjunction with North


11: Classification of and Key for the Identification of Major Taxa


11  Classification of and Key for the Identification of Major Taxa

The major taxa included here are the higher categories of the subclass Acari – the superorders Parasitiformes and Acari­ formes, and the key to families that is presented identifies the lower categories of the superorder Acariformes and its two orders Trombidiformes and Sarcoptiformes.

Higher Categories of the Subclass Acari

At present, there is no a definitive version of the higher classi­ fication of the Acari, because of a lack of knowledge of the fossil record and the existence of many unclear relationships between groups. The latest studies consider the Acari to be a subclass of the class Arachnida (Krantz, 1978; Johnston, 1982; Lindquist,

1984; Evans, 1992; Walter and Proctor, 1999; Zhang, 2003).

Zhang (2003) divides the subclass into three superorders

(Opilioacariformes, Parasitiformes and Acariformes) and seven orders; within these three superorders, the Opilioacariformes include the order Opilioacaridida, the Parasitiformes include the orders Holothyrida, Mesostigmata and Ixodida, and the


12: The Family Histiostomatidae Berlese


12  The Family Histiostomatidae Berlese

Morphological Characteristics, Systematics and Bio-ecology

The body of mites of the family Histiostomatidae is large and not dorsoventrally flattened. The gnathosoma is strongly modi­ fied and adapted to feed on minute particles in suspension. The chelicerae are laterally compressed, not chelate, with the digi­ tus fixus comb like and equipped with many fine teeth. The digitus mobilis is short, fused to the base of the digitus fixus, and with few short distal teeth. The palpi have a freely movable and flattened distal segment, with long tarsal solenidion and eupathididal setae (Figs 12.1C and 12.4B). The prodorsum has four pairs of setae (ve, vi, sce, sci) and the hysterosoma ten pairs of dorsal setae (c1, c2, c3, d1, d2, e1, e2, f2, h1, h2); one pair of setae

(h3) is commonly set ventrally. The opisthonotal glands are commonly located between setae e1 and e2. The bursa copulatrix is set between the setae h1 (Fig. 12.1A). The genital valves of the female are fused to the body medially, and form a transverse oviporus; the genital papillae of both sexes are often seen as large rings on the ventral surface and are not closely associated; the posterior pair is set on the ventral opisthosoma (Figs 12.1B and 12.2A) (Hughes, 1976; O’Connor, 2009).


13: The Family Acaridae Latreille


13  The Family Acaridae Latreille

Morphological Characteristics, Systematics and Bio-ecology

The body of the members of the Acaridae is soft, of medium length, and pale whitish to brownish coloured. Some species are weakly pigmented. The integument is smooth, rough or finely furrowed; sometimes completely sclerotized or ornamented with cuticular tubercles. A sejugal furrow separates the idiosoma into the propodosoma and hysterosoma

(Fig. 13.1A).

The dorsal surface of the gnathosoma is not extended and forms a small lobe between the cheliceral bases. The chelicerae are chelate and dorsally free, laterally compressed and with a large basal region stretching forward and forming the digitus fixus articulated with the digitus mobilis; at the base of this articulation there is a small cheliceral seta (cha) (Fig. 13.1C).

Both chelicerae move in a vertical plane and are often toothed distally. The chelicerae are located above the labrum or true epistome, and partially involved in the mouth structure. The labrum is grooved and extends posteriorly and its side walls are related to the ventral area of the gnathosoma; on it are inserted the pharynx dilator muscles. The ventral gnathosoma, called the hypostome or infracapitulum, originates mainly from the fusion of the palpcoxae; it has two whip-like subcapitular ventral setae (m) and extends anteriorly into two inner lobes or malae. The palpi have two freely articulating segments (articles); each coxa bears dorsally a palpal supracoxal seta (elcp) (Fig. 13.1D).


14: The Family Erythraeidae Robineau-Desvoidy


14    The Family Erythraeidae Robineau-Desvoidy

Morphological Characteristics, Systematics and Bio-ecology

The Erythraeidae have a large and reddish body. The chelicerae are retractable into the idiosoma, and the palp bears a

‘thumb-claw’ process. The prodorsum has a median longitudinal ‘crista metopica’ and two pairs of sensilli, with two sensilli set at each distal part (Fig. 14.1). The ‘idionotal setae’ are commonly setiform (Walter et al., 2009). The biological cycle of these mites develops throughout three active stages (larva, deutonymph and adult), with the protonymph and tritonymph quiescent. The larva is heteromorphic to the deutonymph and adult, and in only a few species are the post-larval biological stages correlated with their larval stage. Their identification therefore needs the use of separate keys (Welbourn and Young,

1987). The family numbers eight subfamilies (Erythraeinae,

Callidosomatinae, Abrolophinae, Balaustiinae, Phanolophinae,

Myrmicotrombidiinae, Leptinae, Augustsonellinae) (Walter et al.,


15: The Family Penthaleidae Oudemans


15   The Family Penthaleidae Oudemans

Morphological Characteristics, Systematics and Bio-ecology

The Penthaleidae have a soft body, black to dark green in colour, with the legs long and red coloured. The chelicerae are chelate, separate at the base and each possessing a cheliceral seta (cha); the fixed digit is regressed, commonly slender and sometimes finger like at the tip; the movable digit is sickle like to prong like and smooth, and sometimes strongly stylet like (Fig. 15.2A). The palpi are four segmented and lack a tibial claw (Fig. 15.2B). The stigmata are set at the base of the chelicerae and do not have external peritremes. The ventral gnathosoma has four pairs of setae, the distal pair are the

­adoral setae (or1–2) and the proximal pair, the longer, subcapitular setae (sbc1–2). The prodorsum has an anteromedian projection, the ‘naso’, a pair of internal vertical setae (v1) and a pair of trichobothrial internal scapular setae (sc1) (Figs 15.1,

15.3). The idiosoma (particularly on the ventral surface) and the legs are hypertrichous. Four pairs of lyrifissures (ia, im, ip, ih) may be present, with the fourth pair located on the ventral surface. The anal opening is terminal, dorsoterminal or dorsal, surrounded by three pairs of pseudanal setae (ps1–3)


16: The Family Eriophyidae Nalepa



Morphological Characteristics, Systematics and Bio-ecology

The Eriophyidae are very small, worm-like or fusiform mites, approximately 200 μm long. The eriophyid body consists of the gnathosoma, the prodorsum and an extended and annular opisthosoma (Fig. 16.1). The prodorsal shield lacks anterior setae (vi or ve) and the scapular setae (sc) may be present or absent (Fig. 16.2). The gnathosoma is usually prognathous and directed anteriorly; it has two stumpy palpi, the infracapitulum and the chelicerae. The palpi are parallel to the infracapitulum, and each consists of a base and three segments. The mouth is surrounded by a series of stylets derived from the digits of the chelicerae, the oral stylet or the labrum, and the infracapitulum or rostrum, which has a ‘U’-shaped cross section. The walls of the infracapitulum form a membranous sheath in front and externally have edges that overlap dorsally, concealing from seven to nine stylets (Fig. 16.3). The stylets include one pair of cheliceral shafts divided towards the apex into a dorsal digitus fixus and a ventral digitus mobilis that are separated from the labrum, and one pair of auxiliary stylets, also known as the inner infracapitular stylets. The basal segments of the chelicerae are close to one other and to the motivator, which provides a basal support for the chelicerae (Nuzzaci and Alberti, 1996).


17: The Family Phytoptidae Murray


17   The Family Phytoptidae Murray

Morphological Characteristics,

Systematics and Bio-ecology

The general morphological characteristics of the Phytoptidae are the same as those of other eriophyoid mites (see Chapter 16,

Eriophyidae), and details of their external morphology and setal notation given here are fundamentally based on

Lindquist (1996) and Amrine et al. (2003). The family is dis­ tinctive in having on the prodorsal shield from one to five setae, with anterior setae present (paired or unpaired vi and/ or paired ve). The gnathosoma can be variously sized and is often large, and the chelicerae are straight or slightly and evenly curved; the palp is commonly short and truncate and enclosing the oral stylet. The legs have the usual setae and frequently the solenidion j on tibia I. All empodia are undiv­ ided. The opisthosoma bears the usual setae, and the setae h1 are sometimes long. The female genital coverflap lacks ridges; the anterior female apodeme always extends forward for a moderate distance, and the spermathecal tubes are commonly long, sometimes extending diagonally forward and then re­ curving caudally (see Fig. 17.1).


18: The Family Diptilomiopidae Keifer


18  The Family Diptilomiopidae Keifer

Morphological Characteristics,

Systematics and Bio-ecology

The morphological characteristics of the family Dipti­ lomiopidae are similar to those of the Eriophyidae. The pro­ dorsal shield has two or no setae, the scapular setae (sc) are present or absent, and the unpaired setae vi and ve are largely absent. The gnathosoma is sharply bent towards the base, with cheliceral stylets folded in the same way and long oral stylets. The opisthosoma frequently lacks the setae c1; the re­ maining setae are present, or sometimes any one of the setae c2 or d or setae h1 are absent. The chaetotaxy of the coxal plate is complete, plate I is sometimes without the setae 1b and rarely with the setae 1a. The leg chetotaxy is complete but may be missing the basiventral femoral setae I and II, the antaxial genual seta of genu II, the paraxial tibial seta of tibia

I and both the paraxial and fastigial tarsal setae (ft ¢) or the paraxial and unguinal tarsal setae (u¢) of legs I and II; the tibia I lacks a solenidion; the tarsal empodium may be thick and is commonly divided. The genital coverflap sometimes has one or two rows of ridges and spots or semilunar granules.


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