Microbes As Pathogens

Microbes can be formidable foes. Most animals battle infection throughout their lives, and devote substantial resources to responding defensively to microbial invaders (e.g., Irving et al., 2001). Cockroaches, like other animals that utilize rotting organic matter ( Janzen, 1977), must fend off pathogenesis and avoid or detoxify the chemical offenses of microbes. Most Blattaria lead particularly vulnerable lifestyles. They are relatively long-lived insects that favor humid, microbe-saturated environments; many live in close association with conspecifics, particularly during the early, vulnerable part of life. They also have a predilection for feeding on rotting material, con-specifics, feces, and dead bodies. Pathogens and parasites such as protozoa and helminths (e.g., Fig. 5.10) are no doubt a strong and unrelenting selective pressure, but cockroach defensive strategies must be delicately balanced so that their vast array of mutualists are not placed in the line of fire. An example of these conflicting pressures lies in cockroach social behavior. On the one hand, beneficial microbes promote social behavior. Transmission of hindgut microbes requires behavioral adaptations so that each generation acquires microflora from the previous one, and consequently selects for association of neonates with older conspecifics. On the other hand, pathogenic microbes exploit cockroach social behavior, in that their transmission occurs via inter-individual

Fig. 5.10 Hairworm parasite (Paleochordodes protus) of an adult blattellid cockroach (in or near the genus Supella) in Dominican amber (15-45 mya). From Poinar (1999); photo courtesy of George Poinar Jr.

transfer. Oocysts of parasitic Gregarina, for example, are transmitted via feces (Lopes and Alves, 2005), and the biological control of urban pest cockroaches with pathogens is predicated largely on their spread via inter-individual contact in aggregations (e.g., Mohan et al. 1999; Kaakeh et al.,1996). Roth and Willis (1957) document inter-individual transfer of a variety of gregarines, coccids, amoebae, and nematodes via cannibalism, coprophagy, or proximity.

Cockroaches have a variety of behavioral and physiological mechanisms for preventing and managing disease. At least two cockroach species recognize foci of potential infection and take behavioral measures to evade them. Healthy nymphs of B. germanica are known to avoid dead nymphs infected with the fungus Metarhizium anisopliae (Kaakeh et al., 1996). The wood-feeding cockroach Cryp-tocercus sequesters corpses and controls fungal growth in nurseries (Chapter 9). The former behavior may function to shield remaining members of the family from infection. Vigilant hygienic behavior or fungistatic properties of their excreta or secretions may also play a role throughout the gallery system. Fungal overgrowth of tunnels is never observed unless the galleries are abandoned (CAN, pers. obs.).

The glandular system of cockroaches is complex and sophisticated, with seven types of exocrine glands found in the head alone (Brossut, 1973). The mandibular glands of two species (Blaberus craniifer and Eublaberus distanti) secrete an aggregation pheromone; otherwise the function of cephalic glands is unknown (Brossut, 1970,1979). The secretion of some of these may have antimicrobial properties, and could be spread over the surface of the body to form an antibiotic "shell" during autogrooming, particularly if the cockroach periodically runs a leg over its head or through its mouthparts during the grooming behavioral sequence. Autogrooming therefore may function not only to remove potential cuticular pathogens physically, but also to disseminate chemicals that curtail their growth or spore germination. Dermal glands are typically spread over the entire abdominal integument of both males and females (200-400/mm2) (Sreng, 1984), and five types of defensive-type exocrine glands have been described (Roth and Alsop, 1978) (Fig. 5.11). Most of the latter produce chemical defenses effective against an array of vertebrate and invertebrate predators (Fig. 1.11A),but the influence of these chemicals on non-visible organisms is unexplored. They may well function as "immediate effronteries" to predators as well as "long term antagonists" to bacteria and fungi (Roth and Eisner, 1961; Duffy, 1976), and act subtly, by altering growth rates, spore germination, virulence, or chemotaxis (Duffy, 1976). Most cockroach exocrine glands produce multi-component secretions (Roth and Alsop, 1978). The man-

Fig. 5.10 Hairworm parasite (Paleochordodes protus) of an adult blattellid cockroach (in or near the genus Supella) in Dominican amber (15-45 mya). From Poinar (1999); photo courtesy of George Poinar Jr.

Fig. 5.11 Diagrammatic sagittal section of a cockroach abdomen, showing gland types I-IV and location of the secretory field for gland type V. One of the two type I glands has been omitted and its position indicated by an arrow. Only half of the medially opening Type III gland is shown. From Roth and Al-sop (1978),after Alsop (1970),with permission from David W. Alsop.

Fig. 5.11 Diagrammatic sagittal section of a cockroach abdomen, showing gland types I-IV and location of the secretory field for gland type V. One of the two type I glands has been omitted and its position indicated by an arrow. Only half of the medially opening Type III gland is shown. From Roth and Al-sop (1978),after Alsop (1970),with permission from David W. Alsop.

dibular glands of Eub. distanti, for example, is a blend of 14 products (Brossut, 1979).Brossut and Sreng (1985) list 93 chemicals from cockroach glands, some of which are known to be fungistatic in other systems, for example, phenols (Dillon and Charnley, 1986, 1995), naphthol, p-cresol, quinones (Brossut, 1983), and hexanoic acid (Rosengaus et al., 2004). Phenols have been identified from both the sternal secretions and the feces of P. americana, and neither feces nor the filter paper lining the floor of rearing chambers exhibit significant fungal growth (Takahashi and Kitamura, 1972). Other cockroaches also produce a strong phenolic odor when handled (Roth and Alsop, 1978). It is of interest, then, that phenols in the fecal pellets and gut fluids of locusts originate from gut bacteria, and are selectively bacteriocidal (Dillon and Charnley, 1986, 1995). Given the extraordinarily complex nutritional dynamics between cockroaches and microbes in the gut and on feces, these kinds of probiotic interactions are probably mandatory. It is a safe assumption that cockroaches engage in biochemical warfare with microbes, but they have to do so judiciously.

Blattaria have both behavioral and immunological mechanisms for countering pathogens that successfully breach the cuticular or gut barrier. Wounds heal quickly (Bell, 1990), and cockroaches are known to use behavioral fever to support an immune system challenged by disease. When Gromphadorhina portentosa was injected with bacteria or bacterial endotoxin and placed in a thermal gradient, the cockroaches preferred temperatures significantly higher than control cockroaches (Bronstein and Conner, 1984). The immune system of cockroaches differs from that of shorter-lived, holometabolous insects, and mimics all characteristics of vertebrate immunity, including both humoral and cell-mediated responses (Duwel-Eby et al., 1991). Blaberus giganteus synthesizes novel proteins when challenged with fungi (Bidochka et al., 1997), and when American cockroaches are injected with dead Pseudomonas aeruginosa, they respond in two phases. Initially there is a short-term, non specific phase, which is superseded by a relatively long-term, specific response (Faulhaber and Karp, 1992). When challenged with E. coli, P. americana makes broad-spectrum antibacterial peptides.Activity is highest 72-96 hr after treatment, and newly emerged males respond best (Zhang et al., 1990). Cellular immune responses are mediated by hemocytes, primarily granulocytes and plas-matocytes (Chiang et al., 1988; Han and Gupta, 1988) whose numbers increase in response to invasion and counter it using phagocytosis and encapsulation (Verrett et al., 1987; Kulshrestha and Pathak, 1997).

Sexual contact carries with it the risk of sexually transmitted diseases (e.g., Thrall et al., 1997), but no cockroaches were listed in an extensive literature survey on the topic (Lockhart et al., 1996). Wolbachia, a group of cyto-plasmically inherited bacteria that are widespread among insects (including termites—Bandi et al., 1997) have not yet been detected in cockroaches, but few species have been studied to date (Werren, 1995; Jeyaprakash and Hoy, 2000). Further surveys of Blattaria may yet detect Wolbachia, but because they are transmitted through the cytoplasm of eggs, these rickettsiae may have trouble competing with transovariolly transmitted bacteroids (Nathan Lo, pers. comm. to CAN).

The cost of battling pathogens likely has life history consequences for cockroaches, since it does in many animals that inhabit more salubrious environments (Zuk and Stoehr, 2002). Immune systems can be costly in that they use energy and resources that otherwise may be invested into growth, reproduction, or maintenance, thus making them subject to trade-offs against other fitness components (Moret and Schmidt-Hempel, 2000; Moller et al., 2001; Zuk and Stoehr, 2002). It may be possible, for example, that the prolonged periods of development typical of many cockroaches may be at least partially correlated with an increased investment in immune function. The life of a cockroach has to be a fine-tuned balancing act between exploiting, cultivating, and transmitting microbes, while at the same time suppressing, killing, or avoiding the siege of harmful members of the microbial consortia that surround them. Until recently, these relationships have been difficult to study because the microbes of interest are poorly defined, many have labile or nondescript external morphology, and most cannot be cultured in vitro. The availability of new methodology that allows insight into the origins, nature, and functioning of microbes (Moran, 2002) in, on, and around cockroaches portends a bright future for studies on the subject. Until then, it should be considered that the ability of cockroaches to live in just about any organic environment may have its basis in their successful management of the varied, sophisticated, cooperative, and adversarial relationships with "inconspicuous associates" (Moran, 2002).

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