Annu Rev Cuterebrinae

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Insect/Mammal Associations: Effects of Cuterebrid Bot Fly Parasites on Their Hosts Frank Slansky Department of Entomology and Nematology, University of Florida, Gainesville, Florida 32611; email: fslansky@ufl.edu

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Key Words

First published online as a Review in Advance on September 14, 2006

coevolution, emasculation, feeding compensation, Oestridae, resource budget

The Annual Review of Entomology is online at ento.annualreviews.org This article’s doi: 10.1146/annurev.ento.51.110104.151017 c 2007 by Annual Reviews. Copyright  All rights reserved 0066-4170/07/0107-0017$20.00

Abstract The effect of parasites on their hosts has implications for basic and applied ecology (e.g., species’ population dynamics and distributions, biological control, and threats to at-risk species) and coevolution. Cuterebrid bot flies comprise one of the most-studied groups of insect parasites of mammals. Interest in their impact dates from at least 1857, when Cuterebra emasculator was so named because of the erroneous belief that its larvae castrate their hosts. This review addresses the effects of cuterebrid larvae on host biochemistry, physiology, behavior, and ecology. Despite high prevalence (peak values commonly range from 30% to 70%), at average intensities (one to three larvae per host) these parasites generally have little effect on the fitness or population dynamics of their typical hosts. This outcome likely reflects parasite/host coevolution favoring parasites that minimize harmful effects on hosts required for their survival and hosts that best tolerate perennial parasites they cannot avoid. In contrast, aggravated effects occur at higher intensities and with atypical hosts. Additional field studies involving experimental manipulation of infestation and spanning more than a few seasons are required to confirm these conclusions.

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INTRODUCTION Bot: larva of a bot fly or warble fly

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Typical host: an organism belonging to a species naturally or usually parasitized by a host-specific parasite Atypical host: an organism accidentally parasitized by a host-specific parasite; not a member of the natural or typical host species

Cuterebrid bot flies are one of the most highly studied groups of insect parasites of wild mammals. They are included in the Cuterebridae (20, 78) or the Cuterebrinae subfamily of the Oestridae (69, 103). Catts (20) reviewed the biology of flies in the cuterebrid genera Cuterebra and Dermatobia, and he discussed what little information was available on some of the other genera, such as Alouattamyia, Rogenhofera, and Pseudogametes, each of which likely should be included in Cuterebra (69) (for more recent overviews, see References 21, 26, and 88). Here I expand on what Catts (20) termed host pathology—the actually or presumably deleterious effects these parasites may have on their hosts, a subject that has been generating interest at least since 1857, when Cuterebra emasculator was so named by Fitch (36) because of the erroneous belief that its larvae castrate their hosts. Parasite/host interactions continue to draw considerable attention because of their diverse implications for basic and applied ecological phenomena (e.g., species’ population dynamics and distributions, biological control, and threats to atrisk species) and coevolution (12, 22, 30, 51, 74, 94). Here I first discuss relevant aspects of the biology of these flies and then review literature addressing the effects of cuterebrid larvae on their hosts. My coverage is primarily for Cuterebra, with less emphasis on Dermatobia and other cuterebrid genera. I occasionally provide information on other parasites to suggest likely possibilities for the biology and host impacts of cuterebrids when comparable data for the cuterebrids are scarce or lacking. Most relevant in this regard are larvae of Hypoderma species, cattle pests that, similar to Cuterebra, migrate within the host to subcutaneous sites of establishment (20, 102).

CUTEREBRID BIOLOGY AND HOST INFESTATION The 30-plus Cuterebra species undoubtedly evolved as host-specific, obligate parasites (20, 18

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78, 103). As far as is known, each species usually parasitizes only one or a few species of either New World rodents (e.g., mice, rats, chipmunks, tree squirrels, and voles) or lagomorphs (rabbits and hares), which comprise their typical hosts. Unlike other myiasiscausing flies that place eggs or larvae directly on hosts (21), female Cuterebra oviposit on habitat substrates (e.g., foliage, twigs, and exposed roots), often near mammal burrows and nests (6, 20). When encountered by a potential host, Cuterebra eggs rapidly hatch in response to the animal’s body heat and the infectivestage larvae attempt to transfer to it (20). This off-host oviposition behavior provides opportunities for infestation of atypical hosts, which have included non-native rodents (e.g., house mice and imported rats) and lagomorphs (domestic rabbits) as well as Carnivora (e.g., cats, dogs, raccoons, and skunks), Artiodactyla (e.g., pigs, goats, and deer), and Primates (humans), among others (7, 35, 45, 47, 78, 79, 95; F. Slansky, unpublished data). Dermatobia hominis, a Neotropical species that infests hosts by ovipositing on blood-feeding dipterans, is the most generalized of the cuterebrids, routinely infesting a wide variety of mammals (as well as birds), but especially cattle and humans (21, 26, 77). In contrast, another Neotropical species, Alouattamyia baeri, is the only cuterebrid exclusively parasitizing primates (howler monkeys) (26, 63). The distinction between typical and atypical hosts is crucial to the subject of this review, because atypical hosts and the larvae infesting them frequently incur pathologies and behavioral changes not usually seen when Cuterebra larvae infest typical hosts. Indeed, the general lack of exaggerated effects when Cuterebra larvae infest typical hosts likely reflects the extent to which these intimately associated species have coevolved toward relatively benign interactions. Infestation of atypical hosts is usually considered an incidental occurrence (20, 21), but whether some Cuterebra species are evolving to include certain of these species in an expanded typical host spectrum remains to be investigated.

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First instars of Cuterebra enter a host’s body through an orifice, the eyes, or a wound, and then they typically move to the nasopharyngeal, tracheal, or esophageal regions where they reside for a few days (4, 42, 49, 91). They subsequently migrate for a week or so through the thoracic and abdominal cavities or under the fascia of muscles (42, 49), likely facilitated by the secretion of collagenase and other enzymes, as with Hypoderma larvae (68, 102). In contrast, D. hominis larvae invade through the host’s skin and seldom move far from this point (21, 26, 77). When a cuterebrid larva (also called a bot) settles at a subcutaneous site, an external swelling occurs as a warble forms (25), and the larva creates a warble pore. Typically, there is only one larva per warble; rarely do two or more larvae share a warble or reside in separate warbles but use the same warble pore (4, 9, 25, 46, 99). Warble location is often characteristic of a particular Cuterebra species/hostspecies association. Sites range from the head to the inguinal area and include most locations in between; generally, only the ears, limbs, and tail are not invaded (2, 9, 25, 86, 88). Sillman & Smith (86, p. 166) hypothesized that “significant physiological and biochemical differences in the environment beneath the skin of various regions of the [host’s] body may be factors in the striking regional preference” of migrating Cuterebra larvae. Cogley (25) suggested the inguinal area may provide more room for warble development and better protection for larvae than other sites on a mouse’s body. Cuterebra larvae infesting atypical hosts may form warbles at uncharacteristic sites (3, 4, 18, 75). Once settled, a cuterebrid larva molts to the second instar (Figure 1) and typically completes development at this location—only rarely does an early second-instar Cuterebra abandon its initial site and move to a new location where it makes another warble pore (2, 88). Rare reports of apparent third instar relocation (13) seem highly unlikely. Whether migrating larvae consume a so-called collagenous soup, as in Hypoderma, is unknown; lar-

vae within a warble ingest interstitial fluid (for its chemical composition, see Reference 37) that exudes into the warble, and possibly cellular and tissue debris (27, 50, 71, 102). After their Peromyscus mice hosts were injected with I125 -labeled albumin, Cuterebra larvae became radioactive externally within 1 min, and internally within 1 h (50; see also Reference 66). Whether cuterebrid larvae derive nutrition from bacteria present in the warble (70) is unknown. [This is not the case for Hypoderma larvae (102).] Cuterebrid larvae presumably are not hematophagous but probably ingest blood that leaks into the warble. The unexpected presence of many erythrocytes in the gut of Cuterebra buccata larvae developing in domestic rabbits (100) may have resulted from incomplete larval encapsulation, as often seen with atypical hosts, which possibly facilitated access to host blood. Larvae reach maturity in approximately 4 to 10 weeks, depending on the species of cuterebrid and host (20, 88). Developmental time may be altered in atypical hosts (2, 3,

Warble: encapsulated pocket produced by a vertebrate host in response to the presence of a bot in its subdermal tissue Warble pore: an opening in the host’s skin created by a bot, through which it respires and voids liquid excrement

Figure 1 Second-instar cuterebrids (head to left). (a) Cuterebra sp. from a domestic cat (location unknown; dorsal view; 13.6 mm long). (b) Dermatobia hominis from a cow in Costa Rica (ventral view; 12.7 mm long). www.annualreviews.org • Host Effects of Cuterebrid Infestation

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Figure 2 Third-instar cuterebrids (ventral views; head to left). (a) Cuterebra sp. (probably C. buccata) from an eastern cottontail (Sylvilagus floridanus) in Florida (34.0 mm long). (b) D. hominis from a cow in Costa Rica (13.2 mm long).

18). Fully grown third instars (Figure 2) leave their host by backing out through the warble pore and then pupate underground (20). With typical hosts and average intensities, an evacuated warble closes in a few days, and the lesion usually heals in a week or two (2–4, 9, 25, 46, 50, 70, 73, 85, 88), as with certain oestrids (25, 102).

EFFECTS OF CUTEREBRID LARVAE ON THEIR HOSTS Introduction

Intensity: number of parasite individuals per host individual

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Adults of many fly species affect their hosts variously through biting, blood removal, vectoring pathogens and/or parasites, and startling (39, 64). Because cuterebrid flies do not feed or oviposit on their hosts, and pupation occurs in the soil, their host effects result from the presence and activities of the larvae. Unlike other myiasis-causing flies such as calliphorids, whose larvae can feed and grow on both living and dead animals (21), cuterebrid Slansky

larvae require live hosts to develop fully (14, 88, 103). Thus, natural selection should favor cuterebrid larvae that do not kill their hosts and that minimize deleterious effects so as not to degrade the animal on which they depend for sustenance to the point where their own growth is hindered and/or survival threatened (15, 20, 43, 97) (for general discussions of parasite/host coevolution, see References 34, 60, and 104). For example, consumption of interstitial fluid rather than dermal and muscle tissues (common larval foods for the more hostdamaging species of flies; see Reference 21) may be an adaptation limiting host impact. Nonetheless, cuterebrid larvae may affect a host in a variety of ways, among them damaging its tissues, diverting energy and nutrients from its resource budgets, altering its physiology and behavior, and directly or indirectly causing its death. In some situations hosts may obtain certain benefits from being parasitized (96). For example, Cuterebra-infested mice may live longer, although this longevity comes at the expense of decreased reproduction (17) (see Reproduction and Mortality, below). The magnitude of the effects parasites exert on their hosts, as with potentially toxic chemicals, generally depends on the relative dose. As a basic approximation, a relative dose for cuterebrid larvae is their total mass (number of parasites multiplied by their individual masses) relative to the mass of the host. The primary focus here is on larval energy and nutrient demands (including water) relative to the resource budgets of the host (with body mass as a crude surrogate for resource budgets). In addition, the effects of tissue damage and toxins secreted, for example, by the parasites are also influenced by their relative dose. Depending on the species, the fresh mass of fully grown cuterebrid larvae ranges from <1 g to almost 4 g, with those of lagomorphinfesting species the heaviest (3, 9, 31, 46, 70, 71, 89). At an intensity of one larva per adult host, the greatest relative impact based on body mass probably occurs with the smallest host

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species (mice and voles). For example, the fresh mass of a mature cuterebrid larva may approach 5% of the mass of its mouse host (66). However, actual measurements of resource budgets are necessary to definitively evaluate the proportion of host resources diverted by parasites. Use of comparative body masses for this purpose is limited for several reasons. First, it is a static approach that does not account for changes in physiology and behavior of hosts that may affect their resource budgets. Second, it assumes similar mass-specific ingestion, overall efficiency of food utilization, and tissue composition (e.g., protein, lipid, and water) for different species of cuterebrid larvae, which may be an invalid assumption. For example, nearly mature larvae of Cuterebra approximata contained 30%– 40% dry mass composed of 35% lipid (89), whereas those of A. baeri consisted of approximately 20% dry mass with 20% lipid and 50% protein (63). The primacy of the relative dose of these parasites to their host impacts is likely one of the key factors interfering with cuterebrids evolving to attain the presumably ideal situation of minimizing their harmful effects. The more-or-less haphazard nature of exposure results in parasitization of hosts of different ages, sizes, breeding conditions, and nutritional and immunological status with a variable number of larvae. This variability creates noise in these parasite/host associations and leads to unpredictable infestation situations that can magnify the deleterious effects of these parasites. For example, a healthy adult male eastern gray squirrel with access to abundant food and water may be affected little by three or four Cuterebra larvae, but deleterious consequences may result if an adult male with limited resources, a pregnant or lactating adult female, or an immature squirrel (Figure 3a) experienced the same intensity of infestation (88; see also Reference 66). Typically, most naturally infested animals harbor one to three larvae, but the number occasionally ranges from four to eight and rarely is even higher (4–6, 11, 12, 15, 31, 38, 52,

62, 63, 85, 88, 97, 99) (Figures 3b and 4). Neotoma wood rats tolerated up to seven larvae of Cuterebra tenebrosa, but at higher intensities host mortality exceeded 50%, survivors were emaciated, their warbles became purulent, and healing was prolonged (4). (See Reference 5 for a larval-dosage experiment with Sylvilagus rabbits and Reference 97 for an example of how host age can influence larval impact.) This complexity in cuterebrid parasite/host associations—involving variation in the external environment, the host’s internal conditions, the intensity of infestation, and other factors (31, 41, 62, 63, 65, 66, 94)— must be considered when evaluating the effect of these parasites on their hosts. If not

Figure 3 Eastern gray squirrels (Sciurus carolinensis) in Florida infested with Cuterebra emasculator larvae (previously published in Reference 88). (a) Nest-bound infant with an early-stage warble on its side; the warble pore is visible slightly above and behind the squirrel’s elbow. (b) Heavily infested adult exhibiting extensive fur loss. www.annualreviews.org • Host Effects of Cuterebrid Infestation

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Figure 4

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Ten second instars and six third instars of C. emasculator removed from the squirrel shown in Figure 3b. The simultaneous presence of both instars of various ages suggests multiple infestations.

indicated otherwise, mention of a situation for cuterebrid-infested individuals (e.g., decreased hemoglobin and increased food intake) below is made in reference to hosts with an average intensity of infestation compared with uninfested individuals.

Irritation Irritation during the initial stages of parasitization manifests as sneezing, wheezing, and pawing and scratching of the face and head, especially with atypical hosts (2–4, 18, 49, 50). Altered activity patterns (9, 92) and decreased food intake (50) within the first week or so postinoculation also may reflect irritation caused by invading larvae. Typical hosts generally seem oblivious to Cuterebra warbles on their bodies, although some irritation is evident in eastern gray squirrels, which frequently scratch warbles (88). As a full-grown larva begins expanding the warble pore by repeatedly moving partially in and out through this opening (70), increased irritation may occur (2). Some atypical hosts attempt to remove larvae from warbles (2, 4, 18), likely because of the irritation they cause.

Tissue Damage Dyspnea: difficulty breathing

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Migration of first-instar Cuterebra through the host has not been studied histologically (see Reference 102 for such a study of Slansky

Hypoderma larvae in cattle). Overt pathological symptoms in typical hosts during this period seem rare, probably because of the small size (a few millimeters long) of the parasite at this stage (18). However, some irritation may occur, and host immunological responses are triggered. Creation of the warble pore probably has little deleterious impact because the small wound causes limited blood loss (88), but fur may be lost around warbles on some animals (3, 46, 63, 88) (Figure 3b), possibly increasing their thermoregulatory demands. The presence of a cuterebrid larva in a host’s subdermal tissues initiates localized inflammatory and proliferative responses that lead to the formation of a capsule with either two (25) or three layers (9) [also see the supplemental website for photos of warbles in various stages of development (follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org) and Reference 99 for a photo of a dissected warble]. The layer adjacent to the larva is largely avascular collagenous material with some necrosis. [However, this layer in Hypoderma warbles on cattle is richly supplied with capillaries (102).] Surrounding this layer is a thicker, morediffuse layer of less-densely packed collagenous fibers that blends into the normal connective tissue (9, 25, 70). Host responses to cuterebrid larvae involve invasion of the area by neutrophils, lymphocytes, macrophages, eosinophils, and mast cells, and proliferation of fibroblasts and endothelial cells (9, 70, 73). Larvae of various oestrids provoke similar responses (24, 102). Warbles on atypical hosts are often poorly developed (4, 5, 18), possibly increasing pathological effects. Atypical hosts may display symptoms of Cuterebra infestation usually not observed with typical hosts, such as temporary paralysis during larval migration (5, 16). In addition, with some atypical hosts (especially domestic cats and dogs), larvae can invade the eyes, respiratory tract, or cerebrospinal tissues, causing various pathologies including dyspnea, paralysis, seizures, and blindness,

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often with a fatal outcome for the host (32, 45, 47, 54). Human cases involving Cuterebra and Dermatobia have variously included subcutaneous, nasopharyngeal and ocular infestations (7, 21, 28, 44, 77).

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Blood Composition and Nonreproductive Organ Mass Decreases in erythrocyte count, hemoglobin concentration, and hematocrit percentage of Cuterebra-infested Peromyscus mice (31, 83) were magnified by the intensity of infestation (50). Such changes were not observed in infested Tamias chipmunks (10), although their spleens, and those of certain other hosts (23, 70, 97), were enlarged (61). In some of these studies, and in some cases depending on host age and sex, infested individuals had smaller thymus glands and/or enlarged adrenal glands. Alterations occurred in plasma proteins of cuterebrid-infested Peromyscus mice (50, 71) and Alouatta howler monkeys (63). In addition, the white-blood-cell count may increase substantially. Infested mice did not bleed as readily (31) likely because of elevated fibrinogen levels (71). A general nutritional deficit from consumption of tissue fluids by the larvae and decreased food intake by the host (at least during the early stage of infestation) probably contributed to at least some of the alterations in blood composition and organ sizes described here. Payne et al. (71) proposed that selective consumption of albumin by the larvae might occur. The albumin/globulin ratio was negatively correlated with both the age (mass) of the larvae and their number per mouse (71) or monkey (63). Blood values generally returned to preinfestation levels within a week or two after the larvae left their hosts (31, 50, 71).

Immune Responses Few studies have quantified immunological responses of typical hosts to Cuterebra larvae, although substantial increases in white blood

cells that may be positively correlated with the intensity of infestation have been documented (9, 31, 38, 50). Atypical hosts (laboratory mice and rats and domestic rabbits) produced antibodies when infested by these parasites (75, 100), as did domestic rabbits inoculated with D. hominis larvae (58). In addition, A. baeri larvae stimulated immunoglobin production in howler monkeys (8). Antigens triggering these responses probably reside in larval alimentary secretions (58, 100), as documented for certain oestrids (68). Some researchers (8, 75, 85, 100) have suggested the involvement of immunoresponses in host resistance to cuterebrid invasion, as demonstrated with Hypoderma larvae (40, 68). With Cuterebra, some host individuals were completely refractory (91), and not all larvae inoculated into susceptible hosts established warbles (2–4). However, these studies did not attempt to link larval mortality with host immunological status. Repeated infestations of typical (4, 5, 100) and atypical (75) hosts may provide no or partial resistance to subsequent infestations, and the extent of acquired resistance can depend on mode of entry of the larvae (nose, eyes, or anus) (43). Lower prevalence in older (versus younger) field-caught hosts in some studies (15, 53, 63; but see References 48, 53, 82, 97) may reflect resistance acquired from previous cuterebrid infestations, but the extent of larval exposure of the host age classes must first be determined to evaluate this hypothesis. Co-occurrence of second- and third-instar Cuterebra (4, 88, 99) (Figure 4) suggests that secondary larval establishment is not precluded by an ongoing infestation. Whether host immune responses can hinder development of, and/or kill, second- and/or thirdinstar Cuterebra is unknown. Mortality for these instars ranges from little or none to as high as approximately 50% (2, 4, 5, 50). [The latter value occurred at a high inoculation dose; with fewer larvae per host, mortality dropped to 13% (3).] Larval countermeasures to host immune responses have not been investigated in Cuterebra, but they have been www.annualreviews.org • Host Effects of Cuterebrid Infestation

Prevalence: percentage of individuals in a sample population of a host species infested by parasites of a particular species

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well characterized in Hypoderma and include destruction of bovine immunoglobin and part of the complement cascade by larval salivary enzymes (68) (see also Reference 58 for discussion of host immunomodulation by D. hominis larvae). Catts (19) suggested that the ability of some Cuterebra species to infest atypical Old World rodents or lagomorphs to a greater extent than New World rodents that are not their hosts may result from a lack of evolutionary experience of the former with these parasites, and thus the absence of selection to develop resistance to infestation, in contrast to what may have occurred with the latter. Unfortunately, this intriguing hypothesis cannot be evaluated until the mechanism(s) of host resistance is (are) known. Both host and larval factors probably prevent occupied warbles on typical hosts from becoming highly purulent.

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may alter a host’s activity patterns. For example, after the first week or so postinfestation, and continuing for almost two weeks after the larvae exited, Peromyscus mice experimentally inoculated with a single Cuterebra larva generally reduced strenuous activity (running in an exercise wheel) and increased less-strenuous maintenance behavior (92). However, upon exposure to the odor of predatory weasels, running activity of infested mice increased to a greater extent than that of uninfested individuals, equaling preinfestation levels. In other studies, Cuterebra-infested and uninfested individuals did not differ in distances roamed or home ranges (17, 48). Seemingly larger home ranges of parasitized hosts may be an artifact of differential recapture success for uninfested and infested individuals (48). The activity of Tamias chipmunks whose postexit warbles became purulent was “severely reduced” (10).

Mobility and Activity Awkwardness in movement has been reported particularly for small hosts such as mice and voles, and especially when larvae inhabit the lower abdomen (31, 82, 83, 92, and references therein). Large warbles may also interfere with an animal’s ability to enter its burrow (31). However, some reports indicate no detectable effects of Cuterebra infestation on the mobility of small rodents (48, 92) (although activity patterns may be affected). For example, Sillman (85, p. 91) stated, “[i]n the laboratory, [Cuterebra-] infested mice [Peromyscus] were as agile in eluding capture [by humans] as uninfested mice.” However, he noted that as the larvae began to exit, “the mice were obliged to keep one or the other hind limb raised as they ran.” Larvae of Cuterebra jellisoni often settle around the eyes of Lepus jackrabbits; at a sufficiently high intensity, a host’s activity can be affected because its vision is reduced, even to the point of temporary blindness (2). A parasite’s drain on its host’s resource budgets and the likely need to increase foraging in an attempt to compensate for these deficits 24

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Feeding, Food Utilization, and Growth Infested hosts may attempt to meet the resource (energy and nutrients) drain imposed by their parasites through consuming more food, increasing assimilation and/or conversion efficiencies, metabolizing stored reserves (e.g., lipid), and/or reallocating resources, such as by limiting dispersal or reproduction (17, 72, 81). If the parasites create a drain on the host’s water budget, the host’s responses could include increased drinking, water retention, and production of metabolic water (81). A few studies have investigated such responses by Cuterebra-infested Peromyscus mice. After declining during larval migration, food intake increased for the remainder of the infestation (50; see also Reference 92), which allowed the mice to reestablish and maintain body weight, although their persistent anemia suggests continuation of a net nutritional drain. Increased consumption continued for a week or so after larval exit as the mice regained preinfestation blood values. In contrast, no difference was found in food consumption

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or assimilation efficiency between Cuterebrainfested and uninfested Peromyscus mice (66). Estimates for Peromyscus mice (weighing approximately 20 g fresh mass) indicated that a single Cuterebra larva (∼1 g maximum fresh mass) consumes approximately 3% of a mouse’s nutrient budget and stimulates a 3%–6% increase in its metabolic rate (66, 89). These percentages may change in an additive manner as the number of larvae per host increases (66), but this hypothesis may not be valid because larvae from multiple infestations can weigh less than when only one larva develops in a host (89). Field-captured, Cuterebra-infested animals sometimes weigh less than their uninfested counterparts (13, 31, 38, 67; but see References 9, 11, 66, 83, 85, and 94). Although these results may reflect effects of the parasites, they are not definitive because weight differences among individuals caused by factors other than Cuterebra larvae (e.g., genetic differences, nutritional influences, and other parasites) could alter these animals’ exposure and/or susceptibility to these parasites (15). Thus, reduced body weight could be a cause or consequence of infestation. Other studies have documented definite effects of Cuterebra larvae on host growth. For example, in a mark/recapture field study, growth rate of infested Microtus voles generally was reduced, although infested members of the lowest weight class grew faster than their uninfested counterparts (15; see also Reference 66). Adverse effects on host mass are expected, especially at high intensities of infestation, probably at least in part because of limitations in host compensatory abilities. Emaciation in heavily infested hosts has been reported (3, 13, 38; L.R. Kenyon, personal communication).

(a) the scrotum of these hosts only becomes prominent upon descent of the testes during their breeding seasons (and thus mistaking a Cuterebra warble for a scrotum whose contents had been consumed by the larva within), and (b) the larvae ingest body fluid rather than intact tissue (84). Many studies have confirmed that Cuterebra larvae do not consume a host’s testes (9, 25, 61, 70, 90, 97), but when present in the inguinal area (Figure 5), they may hinder descent of the testes or displace them into the abdomen (31, 62, 98, 99). Apparent scrotal atrophy was observed rarely in postinfestation Sylvilagus rabbits (13). Few cases of parasitic

Figure 5

Reproduction Interest in the effect of Cuterebra larvae on host reproduction dates to at least 1857, when the misconception of emasculation by C. emasculator larvae originated (36). This error likely resulted from a lack of knowledge that

Two third-instar Cuterebra sp. (probably C. emasculator) emerging from warbles in the lower abdomen of a recently killed eastern chipmunk (Tamias striatus) in Massachusetts (one larva is partially concealed between the chipmunk’s hind legs). Observation of such infestations led Fitch (36) to erroneously conclude that larvae of C. emasculator castrate their hosts. (a) Each larva is just beginning to emerge through its warble pore, accompanied by visible fluid loss. (b) In less than 10 min after the photo in (a) was taken, one larva has completely exited the host. www.annualreviews.org • Host Effects of Cuterebrid Infestation

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castration include vertebrates, and none involve insects emasculating mammals (56). Some field studies described reduced, and sometimes little or no, reproduction in Cuterebra-infested individuals (although the number of observations is rather limited) (15, 17, 23, 83, 85). Such effects may occur especially if a larva-imposed nutritional drain interfered with a host’s ability to produce or fertilize eggs, sustain fetuses, and/or nourish offspring. Changes suggestive of a nutritional drain include decreases (which can be age-dependent) in the weight of ovaries, testes, and other reproductive structures of parasitized individuals (90, 97, 99), although whether these effects altered fertility or fecundity has not been evaluated. In contrast, no reductions were found for infested Peromyscus mice in the number of embryos, corpora lutea, or placental scars (97), and the testes and uteri of adult Tamias chipmunks were larger (as was their overall body size) in Cuterebrainfested individuals (61). There is limited evidence of fetal resorption in Cuterebra-infested mice (83, 91) and of the inability of infested female rodents to rear their young (85, 88). In a long-term field study, the only significant decrease in measured reproductive parameters of Peromyscus mice (assessed only for females) was in number of litters per female, which translated into an insignificant decline in overall offspring produced by infested mice during the bot fly season; surprisingly, “infested females actually exhibited disproportionately high rates of breeding activity” (17, p. 759). Warbles located inguinally could interfere with copulation, especially during the later stages of larval development (25, 99). Warbles near a female host’s teats (59, 85, 88) may hamper its infants’ ability to nurse. Also, suckling on warbles could reduce milk intake and might result in ingestion of bacteria and/or toxins (88). However, whether warble location actually affects reproduction has not been assessed. Some studies indicate that cuterebrid larvae have little or no effect on host reproduction (11, 17, 65, 94, 99). Such results might be expected in cases in which infestation oc-

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curred outside the host species’ main reproductive period (9, 53, 62).

Mortality As discussed above, the requirement for living hosts should select for cuterebrid larvae that exert fewer deleterious effects, especially avoidance of killing their hosts (at least during their residency within an animal). Supporting this hypothesis are laboratory (4, 5, 31) and field studies (11, 17, 48, 50, 53, 61, 65) demonstrating or suggesting that these larvae generally cause little or no mortality of typical hosts with average intensities of infestation, and in fact they may increase host longevity (17, 53). In contrast, other field studies concluded that infestation by cuterebrid larvae actually or likely increased host mortality (15, 62, 63, 82, 94). Evaluation of host mortality in field studies typically is based on recapture success, but other factors (e.g., alterations in activity patterns and/or emigration of infested individuals) can also affect probability of recapture. Indeed, increased survival of Cuterebra-infested hosts (99) could be an artifact resulting from their accrual among the longer-term residents at a site, in contrast to the situation with transients (48; see also References 17 and 53). Another problem in interpreting results of most of these studies is that they relied on naturally infested animals. For example, if a physiologically weakened individual became infested with bots, and if this condition (but not the infestation itself) caused it to be killed by a predator, then one might erroneously conclude that parasitization was responsible for its capture by the predator. An appropriate experimental design for evaluating parasite effects includes the manipulation of infestation such as by inoculating larvae into or preventing their invasion of hosts randomly assigned to one or more treatment groups and appropriate control groups (65, 94). Issues of experimental design aside, a variety of factors likely magnify the deleterious effects exerted by cuterebrid larvae, even

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to the point where they contribute to host mortality. There are many potential causes of cuterebrid-induced host death. Physiological stress resulting from such conditions as anorexia, dehydration, and altered blood composition may be a direct cause of mortality. In addition, the effects of infestation on host physiology and behavior (e.g., nutritional drain, tissue damage, and altered foraging) could influence a host’s susceptibility to pathogens, other parasites, and predators. Unfortunately, most studies relevant to this subject did not attempt to identify the cause(s) of death. In fact, making such determinations, especially in field situations, can be difficult, if not seemingly impossible. Thus, the coverage below is often more suggestive than definitive. Physiological stress. Occasional deaths of hosts in field situations may have been caused directly by Cuterebra larvae, especially at high intensities of infestation (38). At average intensities, mortality of typical hosts housed under suitable laboratory conditions tends to be low, but it increases with higher numbers of larvae per host (4, 5). In such situations, host death is often coincident with the exiting of larvae, for both typical (10) and atypical (F. Slansky, unpublished data) hosts. Occasional observations of increased water consumption by heavily infested animals (10, 88) suggest that dehydration may be a component of physiological stress imposed by Cuterebra larvae. More than one Cuterebra larva per Peromyscus mouse likely could create a net water loss unless the host increased water intake, increased production of metabolic water, and/or decreased other avenues of water loss (66). Effects of infestation may be magnified if a host’s access to resources was limited (17, 63, 66), but no studies involving cuterebrids have investigated such possibilities. Increased mortality of parasitized Peromyscus mice when trapped live during cold nights (compared with uninfested mice of similar weight) likely reflects Cuterebra-induced physiological stress (67). In contrast, survival did not differ signif-

icantly between Cuterebra-infested and uninfested Microtus voles subjected to cold temperatures (23). Decreased winter survival (postinfestation) could be another consequence of cuterebrid parasitization (13, 105). Pathogens. There is no definitive documentation that cuterebrid infestation can alter a host’s susceptibility to pathogens. However, suggestive of this are increased purulence and delayed healing of postexit warbles in hosts with a high intensity of infestation (4, 10, 50; L.R. Kenyon, personal communication). With atypical hosts (Figure 6)—as well as with Sciurus tree squirrels and Tamias chipmunks, typical hosts of C. emasculator (9, 10, 70)—infection and prolonged healing of postexit warbles can occur (2, 3, 18). Pneumonia in Cuterebra-infested cottontail rabbits (13) may also reflect a weakened immune system. The general lack of serious infection with an average intensity of infestation likely reflects actions of both the host and the larvae. Antibacterial properties of myiasis-causing blow flies (Calliphora spp.) and screwworms (Cochliomyia hominivorax) result in part from symbiotic gut bacteria (e.g., Proteus mirabilis) that produce bactericidal compounds (33). Whether a similar situation exists in cuterebrid larvae has not been investigated, but

Figure 6 Third-instar Cuterebra sp. coated with presumed purulent matter from its atypical host, a house mouse (Mus musculus) in Washington (ventral view; head to left; 14.5 mm long). www.annualreviews.org • Host Effects of Cuterebrid Infestation

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P. mirabilis and another Proteus species are associated with D. hominis larvae (80). The hemolymph of larvae of Cuterebra (and certain oestrids)—but not their cuticle, gut, tracheae, or fat body—is bacteriostatic against some species (57), although this property may be irrelevant to preventing bacterial contamination within a warble.

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Other parasites. The presence of cuterebrid larvae may facilitate infestation by other parasites, such as larvae of the grey flesh fly, Wohlfahrtia vigil, in adult Microtus voles, which typically has a fatal outcome for the host (14; see also Reference 29). Cuterebrid warbles may stimulate infestation by other species of flies in howler monkeys (8, 63), cottontail rabbits (76), and atypical hosts (55). Whether an ongoing infestation affects the establishment of subsequent cuterebrid larvae is unknown. Predators. Several authors have suggested that hampered mobility likely reduces an infested animal’s ability to escape a predator (82, 93, 99). Other effects such as irritation, listlessness (13), and increased feeding and drinking could increase a host’s exposure to, and/or reduce its vigilance in detecting, predators. Cuterebra tissue in owl pellets and fox scat, for example, indicates that infested animals are consumed by predators (93). However, alterations in activity patterns of infested individuals may reduce, rather than increase, their exposure to predators (92, 93). Unfortunately, few studies have attempted to test these hypotheses. In a laboratory study, Peromyscus mice with one Cuterebra larva were no more susceptible to predatory weasels, and in some situations they may be less vulnerable, than uninfested individuals (93). However, mice with two or more larvae were more susceptible to capture. Of course, as for laboratory studies in general, the applicability of these results to field situations is uncertain. The only field study attempting to test experimentally the increased predation hypothesis monitored Microtus voles naturally infested with one larva 28

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each or prevented from becoming infested through use of a pesticide (94). This procedure presumably did not affect the treated individuals other than to prevent parasitism by Cuterebra larvae and probably also to remove other ecto- and endoparasites. In addition, voles were equipped with transmitters, allowing the researchers to locate carcasses and determine whether predators were the proximate cause of death. During two field seasons, predators were the main source of mortality, killing 14% (first season) and 33% (second season) of the voles. The probability of predation did not differ significantly between the pesticide-treated and control groups in either year, although weekly survival was higher in the treated voles during the year with higher predation. One limitation of this study is that statistical comparisons were only able to be made between the treated and control groups, but Cuterebra prevalence was less than 20% in each year, so many individuals in the control (parasitized) group were not infested; in addition, a few of the treated individuals became infested. Thus, it remains uncertain if the lack of significant Cuterebra-induced predation resulted from the low parasite prevalence during the study or if it is an accurate indication that these parasites have little influence on the risk of predation of their hosts. Nonetheless, the authors (94, p. 1291) concluded that “[t]he interaction between parasites and predators obviously has a variable effect on the population dynamics of voles, and is probably not capable of regulating their population dynamics or causing regular population fluctuations.”

Population-Level Effects Key questions about parasite/host associations include whether the effects of parasites on individual hosts influence their population dynamics and/or distributions (12, 22, 30, 53, 74, 94, 104). In 1857, Fitch (36) suggested that periodic population declines of eastern gray squirrels likely were caused not by food limitation and/or emigration (as proposed by other

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naturalists at the time), but by C. emasculator larvae. Although the main premise underlying Fitch’s hypothesis (parasitic castration) is invalid, the possibility remains that cuterebrid bot flies may have population-level impacts on their hosts. Population dynamics. Field studies encompassing a few infestation seasons (as is the case for most such studies of cuterebrids) generally provide little evidence of strong deleterious impacts on host populations. However, these studies typically are insufficient for rigorously evaluating such effects, not only because of their short durations, but also because of small sample sizes, too few host parameters measured (including year-to-year carryover effects), lack of adequate statistical analyses, use of nonmanipulative experimental designs, and/or the lack of attention to other factors that may interact with effects of these parasites (i.e., host density, food abundance, other natural enemies, and abiotic environment). In one of the few relevant long-term studies (10 years, with some 30,000 Peromyscus mice trapped), peak population density of the mice was not significantly lower either during years of high Cuterebra prevalence or in the year immediately following these, but their population growth rate was significantly reduced during years of “intense bot fly infestation” because of a decrease in reproduction by infested females (17). These results are reasonably robust because the researchers evaluated statistically the independent effect of mouse density on these parameters. Two other long-term studies of cuterebrid infestation— 9 years, spiny rats (Proechimys) in Panama (1); 20 years, two Peromyscus mice species and Tamias chipmunks in Pennsylvania (53)— focused on fluctuations in prevalence rather than host impacts (although the latter also assessed residence durations). Adler et al. (1, p. 697) speculated that, because of low prevalence values, “population level consequences [on the host species] of bot infestation are likely trivial,” and Jaffe et al. (53) doubted that infestation decreased longevity of the three

species studied. Although their study lasted only two years, Steen et al. (94) concluded that Cuterebra-induced predation probably did not regulate vole population dynamics. Geographic distribution and habitat preference. Most cuterebrid species have relatively limited geographic ranges (78), and habitat preferences have been documented (1, 12, 101; but see Reference 17). Thus, if there are fitness costs to infested hosts, cuterebriddriven natural selection could influence the geographic distributions and/or habitat preferences of these species, but these possibilities have scarcely been investigated. Bergstrom (12) hypothesized that cuterebrid infestation may influence the outcome of competition between, and thus the distribution of, two Tamias chipmunk species along an elevational gradient. Whether tree squirrels in southern Florida, where C. emasculator is scarce or absent (F. Slansky, unpublished data), show improved performance compared with those in other parts of this state where this bot fly is prevalent has not been determined.

CONCLUSIONS AND UNANSWERED QUESTIONS Many observations and considerable research over the past 150 years have generated a wealth of information about cuterebrid-parasite/mammal-host associations. Nonetheless, many questions remain unanswered, among them issues of larval migration and subdermal site selection; host and parasite immunology; larval feeding, food utilization, and development; causes and consequences of altered blood composition and nonreproductive organ sizes; costs to a host of warble development and maintenance; larval influences on host movement, relationships with pathogens, other parasites and predators, and mating and other aspects of reproduction; resource drain on, and compensatory abilities of, infested hosts; and the effects of infestation on host fitness, population dynamics, competition, geographic www.annualreviews.org • Host Effects of Cuterebrid Infestation

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distribution, and habitat preference. In addition, the extent to which the effects of cuterebrid infestation (or the lack thereof) reflect coevolution of these associations is a key question arising from this review. Despite the many questions highlighted here, a variety of actually or likely deleterious effects on typical host individuals have been described. In addition, high proportions of infested individuals have frequently been documented; maximum prevalence values commonly ranged from 30% to 70% (4, 5, 12, 15, 23, 38, 52, 53, 61–63, 82, 83, 99; but see References 1, 17, 67, 94, and 97). These high values, along with the demonstrated or presumed effects of infestation on individual hosts, support the view that cuterebrids cause significant ecological impacts. Indeed, because many of these studies focused on the smallest hosts (especially Peromyscus mice and Microtus voles), one would expect that if cuterebrid larvae cause such effects, these should be readily detectable in field situations, in contrast to hosts with larger body masses and thus greater resource budgets. Nonetheless, results of the studies reviewed here lead to the overall conclusion that at average intensities larvae of these flies in general seem to have little or no deleterious effect on typical host fitness or population dynamics. This conclusion remains tentative, however, because studies providing definitive answers to the questions of whether, and if so, under what circumstances, cuterebrid bot flies exert ecological impacts do not exist. As discussed above, most of the relevant field

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studies have limitations that prevent reaching robust conclusions. The need for experimental manipulation of infestation and measurement of abiotic and biotic environmental factors over several years, along with rigorous statistical analyses, suggests a seemingly impossible expectation for any such research project. Aggravated effects of cuterebrid infestation are evident with typical hosts at high intensities and with atypical hosts. These strongly deleterious impacts highlight the seemingly benign nature of the association between cuterebrids and their typical hosts at average intensities. Given the context of parasite/host coevolution likely applicable for these associations, these outcomes are perhaps not surprising. As described above, associations between species of cuterebrids and their typical hosts likely have been evolving toward situations in which the parasites, being relatively host specific and dependent on live hosts, typically exert minimal deleterious effects, and the hosts, which do not possess mechanisms for avoiding parasitization, have evolved coping mechanisms that further limit the deleterious effects of these parasites. Of these associations, perhaps those exhibiting the most-significant deleterious effects are historically the most recent and least coevolved. These considerations should make cuterebrid/mammal associations highly deserving of research investigating parasite/host coevolution. Indeed, aspects of these associations may help refine the concept of parasitism.

SUMMARY POINTS 1. Cuterebrid larvae are subcutaneous parasites primarily of native rodents and lagomorphs (typical hosts) in the Americas. 2. Effects of cuterebrid bot fly larvae on their hosts have been studied for approximately 150 years. 3. Average intensities of infestation typically range from one to three larvae per host individual (although the number occasionally ranges from four to eight and rarely is even higher) and maximum prevalence values commonly range from 30% to 70%.

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4. Documented and suggested effects of cuterebrid larvae on host biochemistry, physiology, and behavior have the potential to affect the ecology and evolution of these animals. 5. In general, cuterebrids exert little or no population-level effects on their typical hosts at average intensities, although long-term studies employing experimental manipulation of infestation and measuring relevant abiotic and biotic environmental factors, along with rigorous statistical analyses, are necessary to confirm this conclusion.

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6. Significant fitness costs to typical hosts at above-average intensities of infestation demonstrate the importance of relative dose of these parasites in determining their host impacts. 7. Aggravated effects when atypical hosts (i.e., exotic rodents and lagomorphs and nonrodent/nonlagomorph mammals) are invaded highlight the seemingly benign associations between cuterebrids and their typical hosts at average intensities. 8. The associations between cuterebrids and their typical hosts likely reflect coevolution, leading to parasites with behaviors that limit their deleterious effects and hosts possessing mitigation and compensation mechanisms that further limit deleterious effects of parasitization.

ACKNOWLEDGMENTS I am grateful to Lou Rea Kenyon for discussions about cuterebrids and assistance in the preparation of this document. I thank Janella Abordo, Paula Kelly, and Maria Riestra for tracking down much of the literature relevant to this review at the library, and D. Habeck and M. Lohman for supplying some of the larvae used in the photos. Photo credits: C. Welch (Figures 1, 2, and 6), F. Slansky and L.R. Kenyon (Figures 3 and 4), and A. Gola (Figure 5).

LITERATURE CITED 1. Adler GH, Davis SL, Carvajal A. 2003. Bots (Diptera: Oestridae) infesting a Neotropical forest rodent, Proechimys semispinosis (Rodentia: Echimyidae) in Panama. J. Parasitol. 89:693–97 2. Baird CR. 1971. Development of Cuterebra jellisoni (Diptera: Cuterebridae) in six species of rabbits and rodents. J. Med. Entomol. 8:615–22 3. Baird CR. 1972. Development of Cuterebra ruficrus (Diptera: Cuterebridae) in six species of rabbits and rodents with a morphological comparison of C. ruficrus and C. jellisoni third instars. J. Med. Entomol. 9:81–85 4. Baird CR. 1979. Incidence of infection and host specificity of Cuterebra tenebrosa in bushytailed wood rats (Neotoma cinerea) from central Washington. J. Parasitol. 65:639–44 5. Baird CR. 1983. Biology of Cuterebra lepusculi Townsend (Diptera: Cuterebridae) in cottontail rabbits in Idaho. J. Wildl. Dis. 19:214–18 6. Baird CR. 1997. Bionomics of Cuterebra austeni (Diptera: Cuterebridae) and its association with Neotoma albigula (Rodentia: Cricetidae) in the southwestern United States. J. Med. Entomol. 34:690–95 7. Baird JK, Baird CR, Sabrosky CW. 1989. North American cuterebrid myiasis. J. Am. Acad. Dermatol. 21:763–72 www.annualreviews.org • Host Effects of Cuterebrid Infestation

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8. Baron RW, Colwell DD, Milton K. 1996. Antibody immunoglobulin G (IgG) response to Alouattamyia baeri (Diptera: Cuterebridae) parasitism of howler monkeys, Alouatta palliata, in Panama. J. Med. Entomol. 33:946–51 9. Bennett GF. 1955. Studies on Cuterebra emasculator Fitch 1856 (Diptera: Cuterebridae) and a discussion of the status of the genus Cephenemyia Ltr. 1818. Can. J. Zool. 33:75–98 10. Bennett GF. 1973. Some effects of Cuterebra emasculator Fitch (Diptera: Cuterebridae) on the blood and activity of its host, the eastern chipmunk. J. Wildl. Dis. 9:85–93 11. Bergallo HG, Martins-Hatano F, Juca N, Gettinger D. 2000. The effect of botfly parasitism of Metacuterebra apicalis (Diptera) on reproduction, survival and general health of Oryzomys russatus (Rodentia), in southeastern Brazil. Mammalia 64:439–46 12. Bergstrom BJ. 1992. Parapatry and encounter competition between chipmunk (Tamias) species and the hypothesized role of parasitism. Am. Midl. Nat. 128:168–79 13. Boisvenue RJ. 1955. Studies on the life history and ecology of Cuterebra spp. occurring in Michigan cottontails with systematic studies on cuterebrine larvae from other mammals. PhD diss. Michigan State Univ., East Lansing. 218 pp. 14. Boonstra R. 1977. Effect of the parasite Wohlfahrtia vigil on Microtus townsendii populations. Can. J. Zool. 55:1057–60 15. Boonstra RC, Krebs J, Beacham TD. 1980. Impact of botfly parasitism on Microtus townsendii populations. Can. J. Zool. 58:1683–92 16. Bradley TA. 2001. What every veterinarian needs to know about rabbits. Exotic DVM 3. 1:42–46 17. Burns CE, Goodwin BJ, Ostfeld RS. 2005. A prescription for longer life? Bot fly parasitism of the white-footed mouse. Ecology 86:753–61 18. Capelle KJ. 1970. Studies on the life history and development of Cuterebra polita (Diptera: Cuterebridae) in four species of rodents. J. Med. Entomol. 7:320–27 19. Catts EP. 1965. Host-parasite interrelationships in rodent bot infections. Trans. N. Am. Wildl. Nat. Res. Conf. 30:185–96 20. Catts EP. 1982. Biology of New World bot flies: Cuterebridae. Annu. Rev. Entomol. 27:313–38 21. Catts EP, Mullen GR. 2002. Myiasis (Muscoidea, Oestroidea). See Ref. 64, pp. 317–48 22. Clay K. 2003. Parasites lost. Nature 241:585–86 23. Clough GC. 1965. Physiological effect of botfly parasitism on meadow voles. Ecology 46:344–46 24. Cogley TP. 1987. Effects of Cephenemyia spp. (Diptera: Oestridae) on the nasopharynx of black-tailed deer (Odocoileus hemionus columbianus). J. Wildl. Dis. 23:596–605 25. Cogley TP. 1991. Warble development by the rodent bot Cuterebra fontinella (Diptera: Cuterebridae) in the deer mouse. Vet. Parasitol. 38:276–88 26. Colwell DD. 2001. Bot flies and warble flies (order Diptera: family Oestridae). In Parasitic Diseases of Wild Mammals, ed. WM Samuel, MJ Pybus, AA Kocan, pp. 46–71. Ames: Iowa State Univ. Press 27. Colwell DD, Milton K. 1998. Development of Alouattamyia baeri (Diptera: Oestridae) from howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. J. Med. Entomol. 35:674–80 28. Cornet M, Florent M, Lefebvre A, Wertheimer C, Perez-Eid C, et al. 2003. Tracheopulmonary myiasis caused by a mature third-instar Cuterebra larva: case report and review. J. Clin. Microbiol. 41:5810–12 29. Craine ITM, Boonstra R. 1986. Myiasis by Wohlfahrtia vigil in nestling Microtus pennsylvanicus. J. Wildl. Dis. 22:587–89 Slansky

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30. Crockett CM. 1998. Conservation biology of the genus Alouatta. Int. J. Primatol. 19:549– 78 31. Dunaway PB, Payne JA, Lewis LL, Story JD. 1967. Incidence and effects of Cuterebra in Peromyscus. J. Mammal. 48:38–51 32. Dvorak LD, Bay JD, Crouch DT, Corwin RM. 2000. Successful treatment of intratracheal cuterebrosis in two cats. J. Am. Anim. Hosp. Assoc. 36:304–8 33. Erdman GR. 1987. Antibacterial action of myiasis-causing flies. Parasitol. Today 3:214–16 34. Ewald PW. 1994. Evolution of Infectious Disease. New York: Oxford Univ. Press 35. Fischer K. 1983. Cuterebra larvae in domestic cats. Vet. Med./ Small Anim. Clin. 78:1231– 33 36. Fitch A. 1857. Emasculating bot-fly, Cuterebra emasculator, new species (Diptera. Oestridae). In Third Report on the Noxious and Other Insects of the State of New York, ed. A Fitch, pp. 478–85. Albany: N.Y. State Agric. Soc., Suppl. 37. Fogh-Andersen N, Altura BM, Altura BT, Siggaard-Andersen O. 1995. Composition of interstitial fluid. Clin. Chem. 41:1522–25 38. Geis AD. 1957. Incidence and effect of warbles on southern Michigan cottontails. J. Wildl. Manage. 21:94–95 39. Gibbs HC. 1985. Effects of parasites on animal and meat production. In Parasites, Pests, and Predators, ed. SM Gaafar, pp. 7–27. Amsterdam: Elsevier 40. Gingrich RE. 1973. Effects of diet and immunosuppression of Mus musculus on infestation, survival and growth of Hypoderma lineatum (Diptera: Oestridae). J. Med. Entomol. 10:482– 87 41. Gingrich RE. 1979. Effects of some factors on the susceptibility of Peromyscus leucopus to infestation by larvae of Cuterebra fontinella (Diptera: Cuterebridae). J. Parasitol. 65:288–92 42. Gingrich RE. 1981. Migratory kinetics of Cuterebra fontinella (Diptera: Cuterebridae) in the white-footed mouse, Peromyscus leucopus. J. Parasitol. 67:398–402 43. Gingrich RE, Barrett CC. 1976. Natural and acquired resistance in rodent hosts to myiasis by Cuterebra fontinella (Diptera: Cuterebridae). J. Med. Entomol. 13:61–65 44. Glasgow BJ, Maggiano JM. 1995. Cuterebra ophthalmomyiasis. Am. J. Ophthalmol. 119:512–14 45. Glass EN, Cornetta AM, deLahunta A, Center SA, Kent M. 1998. Clinical and clinicopathologic features in 11 cats with Cuterebra larvae myiasis of the central nervous system. J. Vet. Intern. Med. 12:365–68 46. Haas GE, Dicke RJ. 1958. On Cuterebra horripilum Clark (Diptera: Cuterebridae) parasitizing cottontail rabbits in Wisconsin. Parasitology 44:527–40 47. Harris BP, Miller PE, Bloss JR, Pellitteri PJ. 2000. Ophthalmomyiasis interna anterior associated with Cuterebra spp in a cat. J. Am. Vet. Med. Assoc. 216:352–55 48. Hunter DM, Sadleir RMFS, Webster JM. 1972. Studies on the ecology of cuterebrid parasitism in deermice. Can. J. Zool. 50:25–29 49. Hunter DM, Webster JM. 1973. Determination of the migratory route of botfly larvae, Cuterebra grisea (Diptera: Cuterebridae) in deermice. Int. J. Parasitol. 3:311–16 50. Hunter DM, Webster JM. 1974. Effects of cuterebrid larval parasitism on deer-mouse metabolism. Can. J. Zool. 52:209–17 51. Jacobson HA, Guynn DC, Hackett EJ. 1979. Impact of the botfly on squirrel hunting in Mississippi. Wildl. Soc. Bull. 7:46–48 52. Jacobson HA, McGinnes BS, Catts EP. 1978. Bot fly myiasis of the cottontail rabbit, Sylvilagus floridanus mallurus in Virginia with some biology of the parasite, Cuterebra buccata. J. Wildl. Dis. 14:56–66 www.annualreviews.org • Host Effects of Cuterebrid Infestation

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60. Classic discussion of parasite/host coevolution.

66. Novel experimental evaluation of the effect of Cuterebra larvae on mouse resource budgets.

68. Thorough review of immunological issues involved in myiasis.

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53. Jaffe G, Zegers DA, Steele MA, Merritt JF. 2005. Long-term patterns of bot fly parasitism in Peromyscus maniculatus, P. leucopus, and Tamias striatus. J. Mammal. 86:39–45 54. Juliff WF. 1982. Parasitic encephalitis in a dog. Southwest. Nat. 35:38–39 55. Knipling EF, Bruce WG. 1937. Three unusual host records for cuterebrine larvae (Diptera: Oestridae). Entomol. News 48:156–58 56. Kuris AM. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. Q. Rev. Biol. 49:129–48 57. Landi S. 1960. Bacteriostatic effect of hemolymph of larvae of various botflies. Can. J. Microbiol. 6:115–19 58. Lello E, Boulard C. 1990. Rabbit antibody responses to experimental infestation with Dermatobia hominis. Med. Vet. Entomol. 4:303–9 59. Leonard AB. 1933. Notes on larvae of Cuterebra sp. (Diptera: Oestridae) infesting the Oklahoma cottontail rabbit. Trans. Kans. Acad. Sci. 36:270–74 60. May RM, Anderson RM. 1983. Parasite-host coevolution. In Coevolution, ed. DJ Futumya, M Slatkin, pp. 186–206. Sunderland, MA: Sinauer 61. McKinney TD, Christian JJ. 1970. Incidence and effects of botfly parasitism in the eastern chipmunk. J. Wildl. Dis. 6:140–43 62. Miller DH, Getz LL. 1969. Botfly infections in a population of Peromyscus leucopus. J. Mammal. 50:277–83 63. Milton K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on free-ranging howler monkey (Alouatta palliata) population in Panama. J. Zool. 239:39–63 64. Mullen G, Durden L, eds. 2002. Medical and Veterinary Entomology. San Diego, CA: Academic. 597 pp. 65. Munger JC, Karasov WH. 1991. Sublethal parasites in white-footed mice: impact on survival and reproduction. Can. J. Zool. 69:398–404 66. Munger JC, Karasov WH. 1994. Costs of bot fly infection in white-footed mice: energy and mass flow. Can. J. Zool. 72:166–73 67. Nichols LB. 1994. The effect of bot fly (Cuterebra) infestation on cold-night trap mortality in cactus mice (Peromyscus eremicus). Southwest. Nat. 39:383–86 68. Otranto D. 2001. The immunology of myiasis: parasite survival and host defense strategies. Trends Parasitol. 17:176–82 69. Pape T. 2001. Phylogeny of Oestridae (Insecta: Diptera). Syst. Entomol. 26:133–71 70. Payne JA, Cosgrove GE. 1966. Tissue changes following Cuterebra infestation in rodents. Am. Midl. Nat. 75:205–13 71. Payne JA, Dunaway PB, Martin D, Story JD. 1965. Effects of Cuterebra angustifrons on plasma proteins of Peromyscus leucopus. J. Parasitol. 51:1004–8 72. Pelton MR. 1968. A contribution to the biology and management of the cottontail rabbit (Sylvilagus floridanus mallarus) in Georgia. PhD diss. Univ. Georgia, Athens 73. Pereira MCT, Leite VHR, Leite ACR. 2001. Experimental skin lesions from larvae of the bot fly Dermatobia hominis. Med. Vet. Entomol. 15:22–27 74. Price PW. 1997. Insect Ecology. New York: Wiley. 874 pp. 3rd ed. 75. Pruett JH, Barrett CC. 1983. Development by the laboratory rodent host of humoral antibody activity to Cuterebra fontinella (Diptera: Cuterebridae) larval antigens. J. Med. Entomol. 20:113–19 76. Roberts RA. 1933. Additional notes on myiasis in rabbits (Dipt.: Calliphoridae, Sarcophagidae). Entomol. News 44:157–59 77. Roncalli RA. 1984. The biology and the control of Dermatobia hominis, the tropical warblefly of Latin America. Prev. Vet. Med. 2:569–78 Slansky

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78. Sabrosky CW. 1986. North American Species of Cuterebra, the Rabbit and Rodent Bot Flies (Diptera: Cuterebridae). College Park, MD: Entomol. Soc. Am. 240 pp. 79. Safdar N, Young DK, Andes D. 2003. Autochthonous furuncular myiasis in the United States: case report and literature review. Clin. Infect. Dis. 36:73–80 80. Sancho E, Caballero M, Ruiz-Martinez I. 1996. The associated microflora to the larvae of the human bot fly Dermatobia hominis L. Jr. (Cuterebridae) and its furuncular lesions in cattle. Mem. Inst. Oswaldo Cruz 91:293–98 81. Schmidt-Nielsen K. 1990. Animal Physiology: Adaptation and Environment. Cambridge, UK: Cambridge Univ. Press. 602 pp. 4th ed. 82. Scott TG, Snead E. 1942. Warbles in Peromyscus leucopus noveboracensis. J. Mammal. 23:94– 95 83. Sealander JA. 1961. Hematological values in deer mice in relation to botfly infection. J. Mammal. 42:57–60 84. Seton ET. 1920. Does the Cuterebra ever emasculate its host? J. Mammal. 1:94–95 85. Sillman EI. 1955. Studies on the biology of a cuterebrid (Cuterebridae, Diptera) infesting Peromyscus leucopus noveboracensis, Fischer, the white-footed mouse in southern Ontario. Rpt. Entomol. Soc. Ontario 86:89–96 86. Sillman EI, Smith M. 1959. Experimental infestation of Peromyscus leucopus with larvae of Cuterebra angustifrons. Science 130:165–66 87. Slansky F, Kenyon LR. 2002. Bot fly (Diptera: Cuterebridae) infestation of nest-bound eastern gray squirrels. Fla. Entomol. 85:369–71 88. Slansky F, Kenyon LR. 2003. Cuterebra bot fly infestation of rodents and lagomorphs. J. Wildl. Rehab. 26:7–16 89. Smith DH. 1975. An ecological analysis of a host-parasite association: Cuterebra approximata (Diptera: Cuterebridae) in Peromyscus maniculatus (Rodentia: Cricetidae). PhD diss. Univ. Montana, Missoula. 177 pp. 90. Smith DH. 1977. Effects of experimental bot fly parasitism on gonad weights of Peromyscus maniculatus. J. Mammal. 58:679–81 91. Smith DH. 1977. The natural history and development of Cuterebra approximata (Diptera: Cuterebridae) in its natural host, Peromyscus maniculatus (Rodentia: Cricetidae), in western Montana. J. Med. Entomol. 14:137–45 92. Smith DH. 1978. Effects of bot fly (Cuterebra) parasitism on activity patterns of Peromyscus maniculatus in the laboratory. J. Wildl. Dis. 14:28–39 93. Smith DH. 1978. Vulnerability of bot fly (Cuterebra) infected Peromyscus maniculatus to shorttail weasel predation in the laboratory. J. Wildl. Dis. 14:40–51 94. Steen H, Taitt M, Krebs CJ. 2002. Risk of parasite-induced predation: an experimental field study on Townsend’s voles (Microtus townsendii). Can. J. Zool. 80:1286–92 95. Suedmeyer WK, Catts EP, Greiner E. 2000. Cuterebra myiasis in a group of red kangaroos (Megaleia rufa), a Bennett’s wallaby (Macropus rufogriseus fruticus), and a Gunther’s dik dik (Maloqua guentheri smithi). J. Zoo Wildl. Med. 31:124–28 96. Thomas F, Poulin R, Guegan JF, Michalakis Y, Renaud F. 2000. Are there pros as well as cons to being parasitized? Parasitol. Today 16:533–36 97. Timm RM, Cook EF. 1979. The effect of bot fly larvae on reproduction in white-footed mice, Peromyscus leucopus. Am. Midl. Nat. 101:211–17 98. Timm RM, Lee RE Jr. 1981. Do bot flies, Cuterebra (Diptera: Cuterebridae), emasculate their hosts? J. Med. Entomol. 18:333–36 99. Wecker SC. 1962. The effects of bot fly parasitism on a local population of the whitefooted mouse. Ecology 43:561–65 www.annualreviews.org • Host Effects of Cuterebrid Infestation

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RELATED RESOURCES Borgsteede C. 2005. The Art of Being a Parasite. Transl. D Simberloff. Chicago: Univ. of Chicago Press. 291 pp. (From French) Borgsteede FHM. 1996. The effects of parasites on wildlife. Vet. Q. 18:S138–40 Proctor HC. 2003. Feather mites (Acari: Astigmata): ecology, behavior, and evolution. Annu. Rev. Entomol. 48:185–209 Schmidt GD, Roberts LS. 2000. Foundations of Parasitology. Boston: McGraw Hill. 670 pp. 6th ed. Scholl PJ. 1993. Biology and control of cattle grubs. Annu. Rev. Entomol. 39:53–70 Scott ME. 1988. The impact of infection and disease on animal populations: implications for conservation biology. Conserv. Biol. 2:40–56 Steelmann D. 1976. Effects of external and internal arthropod parasites on domestic livestock production. Annu. Rev. Entomol. 21:155–78

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Contents

Annual Review of Entomology Volume 52, 2007

Frontispiece Charles D. Michener p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p xiv

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The Professional Development of an Entomologist Charles D. Michener p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Insect/Mammal Associations: Effects of Cuterebrid Bot Fly Parasites on Their Hosts Frank Slansky p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 17 Phenology of Forest Caterpillars and Their Host Trees: The Importance of Synchrony Margriet van Asch and Marcel E. Visser p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 37 Arthropod Pest Management in Organic Crops Geoff Zehnder, Geoff M. Gurr, Stefan Kühne, Mark R. Wade, Steve D. Wratten, and Eric Wyss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 57 The Sublethal Effects of Pesticides on Beneficial Arthropods Nicolas Desneux, Axel Decourtye, and Jean-Marie Delpuech p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p81 Impact of Extreme Temperatures on Parasitoids in a Climate Change Perspective Thierry Hance, Joan van Baaren, Philippe Vernon, and Guy Boivin p p p p p p p p p p p p p p p p p p p p 107 Changing Paradigms in Insect Social Evolution: Insights from Halictine and Allodapine Bees Michael P. Schwarz, Miriam H. Richards, and Bryan N. Danforth p p p p p p p p p p p p p p p p p p p p p 127 Evolutionary Biology of Centipedes (Myriapoda: Chilopoda) Gregory D. Edgecombe and Gonzalo Giribet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 151 Gene Regulation by Chromatin Structure: Paradigms Established in Drosophila melanogaster Sandra R. Schulze and Lori L. Wallrath p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 171 Keys and the Crisis in Taxonomy: Extinction or Reinvention? David Evans Walter and Shaun Winterton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 193 Yellow Fever: A Disease that Has Yet to be Conquered Alan D.T. Barrett and Stephen Higgs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209 vii

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Molecular Mechanisms of Metabolic Resistance to Synthetic and Natural Xenobiotics Xianchun Li, Mary A. Schuler, and May R. Berenbaum p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231 Group Decision Making in Nest-Site Selection Among Social Insects P. Kirk Visscher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 255 The Role of Allatostatins in Juvenile Hormone Synthesis in Insects and Crustaceans Barbara Stay and Stephen S. Tobe p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 277 Nectar and Pollen Feeding by Insect Herbivores and Implications for Multitrophic Interactions Felix L. Wäckers, Jörg Romeis, and Paul van Rijn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 301

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Biology and Evolution of Adelgidae Nathan P. Havill and Robert G. Foottit p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 325 Biology of the Bed Bugs (Cimicidae) Klaus Reinhardt and Michael T. Siva-Jothy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351 The Use of Push-Pull Strategies in Integrated Pest Management Samantha M. Cook, Zeyaur R. Khan, and John A. Pickett p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375 Current Status of the Myriapod Class Diplopoda (Millipedes): Taxonomic Diversity and Phylogeny Petra Sierwald and Jason E. Bond p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 401 Biodiversity Informatics Norman F. Johnson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421 Cockroach Allergen Biology and Mitigation in the Indoor Environment J. Chad Gore and Coby Schal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 439 Insect Conservation: A Synthetic Management Approach Michael J. Samways p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465 Interactions Between Mosquito Larvae and Species that Share the Same Trophic Level Leon Blaustein and Jonathan M. Chase p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 489 Indexes Cumulative Index of Contributing Authors, Volumes 43–52 p p p p p p p p p p p p p p p p p p p p p p p p p p p 509 Cumulative Index of Chapter Titles, Volumes 43–52 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 514 Errata An online log of corrections to Annual Review of Entomology chapters (if any, 1997 to the present) may be found at http://ento.annualreviews.org/errata.shtml viii

Contents