Arthropods: Prospect of Household Food Security

*Jonathan Ibrahim and Dalyop Daniel Gyang*

## **Abstract**

Food security is a "situation that exists when all people, at all times, have physical, social, and economic access to sufficient, safe, and nutritious food that meets their dietary needs and food preference for an active and healthy life". With a growing world population and increasingly demanding consumers, the production of sufficient protein from livestock, poultry, and fish represents a serious challenge for the future and prompts the need for other sources of nutrition to be explored. Approximately more than 1,900 arthropod species are edible. This requires the development of cost-effective, automated mass-rearing facilities that provide a reliable, stable, and safe product for consumption. This chapter discusses arthropods as food, arthropods as animal feed, nutritional composition, the secondary metabolites of edible insects and potential medicinal substances, development and utilization of edible insect's resources, insect farming, impact of insect quality on consumers' preference and acceptability (insect processing and product quality, processing and marketing, and consumer acceptance), food safety and legislation, as well as the way forward.

**Keywords:** arthropod, prospect, household, security, impact

### **1. Introduction**

The largest phylum in the animal kingdom, which includes well-known insects, spiders, ticks, and crustaceans, as well as numerous smaller, lesser-known species and a plethora of bizarre forms only known as fossils. Arthropods account for approximately 95% of all animal species. The number of recognized species is expected to be in excess of one million, with insects accounting for the majority. Nobody is sure how many arthropod species there are. Authorities believe it might be in the tens of millions [1]. The body of an adult arthropod is normally made up of a succession of ring-like segments with a pair of numerous jointed limbs on each segment that move on each other via muscles. However, other parasites, such as pentastomids and rhizocephalans, show no signs of segmentation as adults. Arthropods' integument produces a stratified cuticle containing chitin. This exoskeleton must be shed regularly to allow for growth, a process known as molting or ecdysis. Young stages change significantly from adults, and some parasitic organisms have extremely distinct body forms than their closest relatives. Arthropods are distinguished from all other creatures by their traits [1].

Food insecurity is worsening as a result of rising population and constraints on food importation, among other things. As a result, there is a high prevalence of hunger and malnutrition, with children and women being particularly susceptible. Apart from the increased risk of hunger brought on by the deteriorating food situation, the widespread prevalence of Protein Energy Malnutrition (PEM) has resulted in high rates of illness and death, particularly among babies and children in developing nations. While every effort is being made to increase food production through conventional agriculture, including current interest in the possibilities of exploring the vast number of less familiar plant resources that exist around the world [2], almost no attention has been paid to the consumption of Arthropods, a traditionally recognized and available source of protein and fats. Furthermore, protein meals are scarce, making them out of reach for lowincome households, which sadly make up the majority of the population in most emerging nations [3]. The scarcity of common animal nutrition sources and the high expense of the few available plant sources should spur urgent study into the nutritious potentials of arthropods.

### **2. Arthropods as food**

Most species of arthropods are obtained from nature in tropical nations. More than 2000 bug species are found in an inventory of edible insect species eaten across the world using solely scientific names rather than common ones. In terms of most species consumed, certain countries stand out. This, on the other hand, is primarily due to the amount of research completed. Ramos-Elorduy, for example, published a large number of publications in Mexico on entomophagy (the eating of insects), and Belgian scientists discovered more than 60 edible caterpillars in the Democratic Republic of Congo, a former Belgian colony [4]. This also implies that many edible bug species are yet unknown, necessitating more research [4]. Insects are more commonly consumed in tropical regions because they are bigger and generally congregate in clumps, making gathering easier. In addition, because there is no winter season, bug species can be found throughout the year. Most insect species are seasonal because they are dependent on the availability of their host plant; others, such as most aquatic insects, can be found all year. Beetles (31%), caterpillars (18%), wasps, bees, and ants (15%), crickets, grasshoppers, and locusts (13%), true bugs (11%), and termites, dragonflies, flies, and others (12%) are among the insects consumed [4, 5].

Spiders and scorpions are examples of arthropods that are eaten. Some species are semi-domesticated, meaning that some precautions are taken to make harvesting more predictable [6]. Palm trees, for example, may be chopped down to encourage palm weevils of the genus Rhynchophorus (*Coleoptera: Curculionidae*) to lay their eggs on the trunk. The larvae are gathered when a particular amount of time has passed. In many areas of the world, these larvae are considered a delicacy. In the tropics, nothing is known about how frequently and how much insects are consumed [7]. This is due to the fact that insects are not counted as food or feed in national agricultural statistics. In underdeveloped nations, the vast majority of insects are collected from natural populations in nature, farmlands, or woods. Edible insects provide a low-cost and effective way for vulnerable groups to enhance their livelihoods and the quality of their traditional foods. In western nations, the use of insects as food has recently acquired popularity. Several businesses have begun to breed insects for human consumption. In the United States, for example, crickets are frequently used

in processed foods like as protein bars. They are already available in supermarkets in several countries.

## **3. Arthropods as animal feed**

Arthropods have been studied as a feed constituents for aquatic and domestic animals. Insect meal has been shown to have appropriate palatability for chickens, pigs, fish species, and ruminants. Insects can replace 25–100% of soymeal or fishmeal depending on the animal type [8]. The Black soldier fly *Hermetia illucens (Diptera: Stratiomyidae*) and the Domestic house fly *Musca domestica* are the most promising species for large-scale production *(Diptera: Muscidae)*. Mealworms, termites, grasshoppers, crickets, and caterpillars are among the other species that are evaluated (such as the silkworm). The use of the Black soldier fly as a feed for chickens, pigs, channel catfish, African catfish, blue tilapia, turbot, and rainbow trout has been examined [8]. Agricultural by-products such as coffee pulp, palm kernel meal, and manure, as well as organic waste materials such as fish offal, market waste, municipal organic waste, dewatered fecal sludge, organic leachates, and Distiller's Dried Grains with Solubles (DDGS) can all be recycled using fly larvae [9].

The use of insects in aquaculture has recently attracted a lot of attention. This is due to the decreasing availability of fishmeal as a primary source of dietary protein in compounded feed for a number of important farmed species [10]. Fishmeal is manufactured from pelagic fish caught in international seas. International fisheries are overfished, and existing techniques are unsustainable [11]. Fish and shellfish farming has been the fastest growing food producing sector in the previous several decades (it is still expanding at 6% per year) and has become a major business in many nations, increasing demand for fishmeal [11]. In 2012, farmed food fish accounted for 42% of all fish produced worldwide, including both capture and aquaculture (it was just 13% in 1990) [11]. As a result, fishmeal and fish oil output has decreased from 30 million tons (live weight) in 1994 to 16 million tons in 2012 [12]. This scarcity has driven a hunt for other protein sources, including the utilization of insects [11]. Insect meal is a promising alternative to soymeal in aquaculture, as vegetable-based diets have a number of drawbacks. These include amino acid imbalances, anti-nutritional elements, low palatability, and a large amount of fiber and non-starch polysaccharides [13].

Insects have been allowed in aquaculture feed since 2013, according to a European Union (EU) regulation. In Norway, research has shown that insect meal is an excellent protein source for farmed salmon [14]. The Norwegian Research Council has invested over one million euros to research the possibilities of employing insects as a safe and nutritious fish feed element [14].

## **4. Nutritional composition**

The nutritional profile of edible insects is difficult to generalize. Despite the wide variety, data from 236 edible insect species demonstrate that they offer adequate energy and protein, fulfill human amino acid needs, are high in monounsaturated and polyunsaturated fatty acids, and are rich in various minerals and vitamins [15, 16]. In comparison to normal beef, the high iron and zinc concentration is particularly interesting. As a result, entomophagy has been recommended to address these mineral deficiencies in

underdeveloped nations, particularly in light of the fact that the global population at risk for these deficiencies is more than 17% for zinc and 25% for iron [17].

Mealworms and crickets, for example, contain a protein level of 19 to 22%, making them suitable for human consumption [18]. In terms of protein content, this is equivalent to typical meat products [17]. The scientists found that the necessary amino acid levels in the insect species they studied were equivalent to soybean proteins, but lower than casein. Gels might be produced and soluble fractions obtained using a simple water extraction process for potential culinary applications [19].

## **4.1 Edible insect protein**

Insects can be a more effective source of protein, and edible insects have a bright future [20]. Protein concentration varies depending on the insect condition, according to studies. Adults have the largest protein concentration, followed by pupas, and finally larvae [20]. According to protein estimates of insects of various ages, the adult has 71.07% protein content, the pupa has 58.59% protein content, and the larva has 50.83% protein content [5]. The protein composition of insects from various tropics differs as well. Orthoptera is ranked higher than Homoptera, as well as Odonata, Diptera, Hymenoptera, Hemiptera, Lepidoptera, and Coleoptera [21].

Amino acid is the fundamental functional unit of biological macromolecular protein, as well as a significant component of the food that insects consume. The amino acid concentration of edible insects ranges from 10 to 70%, with 10 to 30% being necessary amino acids. The majority of insect amino acid ratios are adequate and have approached or even exceeded the WHO/FAO recommended ratios [5]. The presence of a considerable number of free amino acids linked to insect freshness was also discovered [22]. The content of free amino acid of edible insects in the blood is about 3000–23,400 mg/kg, which is more than any other higher animal in the cosmos [22].

## **4.2 Carbohydrate of edible insects**

Edible insects' carbohydrates (sugars) are highly rich in glucose, triose, glycogen, erythritol, ketose sugar, fructose, and ketoheptose. The sugar content of sea algae (the constituent blood sugar of insects) is also high [23]. Edible insects carbohydrates are simple to digest and absorb with total sugar content ranging from 1–10% or even lower which is highly good for human health [24]. The total sugar content of *Cyclopelta parva* is 1.45%, while *Tessaratoma papillosa* has a sugar concentration of 0.15% [20].

The major component of edible insect skin and bones is chitin. N-Acetyl-Dglucosamine copolymer is its chemical name, and it has adsorption properties for a certain toxin. It is also a low-calorie food with a high nutritional content that is beneficial to one's health. Chitin aids in the prevention of high blood pressure by promoting intestinal peristalsis, weight reduction owing to fat, antiaging, enhancing immunological function, and so on. The edible insect body content of chitin is generally between 15 and 18%. Chitin content varies according to insect nature, such as the chitin content of dry silkworm pupa (3.73%) and Skim pupa's content is 5.55% [25].

#### **4.3 Mineral elements and vitamin of edible insects**

Edible insects are high in mineral elements such as calcium, phosphorus, iron, and zinc, among others, which are frequently required by the human body as

*Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

supplements. Feed insects have been reported to be able to meet the Fe, Cu, Zn, and Mg mineral requirements of animals [26]. Mineral elements such as Mn, Fe, Cu, and Zn are found in abundance in locusts [26]. Zn, Se, Mn, and Mg [27] are abundant in many ants. Edible insects are high in Se, Co, Ni, and Cd trace elements, in addition to the constant element (73). The Se content of the Chinese rice locust and yellow powder bug is 4.62 and 4.75 mg/kg, respectively [28]. Se can help with detoxification, carcinogenic activity inhibition, carcinogen destruction, and cancer cell growth and division prevention [28]. Other elements found in *Formica (Coptoformica) mesasiatica Dlussky* [28] include Ni (1.22 mg/g), Co (1.36 mg/g), and Cr (1.52 mg/g).

Vitamins B1 (thiamine), B2 (riboflavin), B3 (niacin), B6 (pyridoxine), C, D, E, K, and carotene are all found in the bodies of insects [28]. *Macrotermes annandalei* contains 25.0 I.U./g of vitamin A, 85.4 I.U./g of vitamin D, and 11.7 I.U./g of vitamin E. Vitamins are necessary for sustaining the human body's regular physiological function [28].

#### **4.4 Lipid contents of edible insects**

Oil and fats are abundant in insects [20]. Pupae and larvae have a greater fat content than adult insects [20]. The fat content of the insect decreases once it has feathered. The fat content of edible insects is usually between 10 and 50% [20]. Unsaturated fatty acid and palmitic acid are higher in edible insects [20]. Among them, linolenic acid content is higher. They can be employed as medicinal raw materials in the form of textiles and stencils [20]. The fat content of wasps was discovered in a recent study. Fat content in larvae is 29.01%, in pupae it is 27.25%, and in adults it is 17.22% [20]. Lepidoptera have more unsaturated fatty acids and palmitic acid, while *Coleoptera* have more oil acids [20]. Infrared spectroscopy of insect wax revealed that it is mostly made up of long-chain hydrocarbons, fatty alcohols, fatty acids, and some molecules with aromatic rings mixed in [29].

### **5. The nutritional evaluation of insect oil/fat**

Insect oils (fat) are nutritional compounds with a wide range of physiological and biological effects. It is highly valued in research, development, and application, regardless of quantity or quality [30]. The fat content of an insect's body varies during its life cycle. It is intimately linked to the insect species' development [30]. Many studies have shown that the fat content of insects varies between species. In the same species, the oils (fat) of the pupa and larva were greater than those of the adults. The oil content of the insects was also greater throughout the winter [30].

The dry body fat level of insects was typically 10%, while many other insects have fat content of 30%, or even up to 77.16% [30]. Insects are high in fat and have a balanced fatty acid profile. The ratio of saturated to unsaturated fatty acids in edible insects is usually less than 0.4 [30]. Its partial fatty acid content ratio is similar to that of fish, therefore it may be utilized as a natural health care product. Insects' saturated fatty acids (SFA) are largely made up of palmitic acid (C16:0), not stearic acid (C18:0), which is abundant in vertebrates [30]. In addition, insect oil contains carbon fatty acids with an odd number of carbons, such as pentadecanoic and heptadecanoic acids, which are very unusual in nature but exceedingly frequent in insects [27]. The concentration of heptadecanoic acid in termite adults, housefly larvae, and housefly adults was all greater than 2% [27]. Because odd-number carbon fatty acids have a

unique raw active action, they were discovered to have higher anticancer activity [27]. As a result, many researchers are interested in the enrichment and separation of odd number carbon fatty acids in insects, resulting in a hotspot in insect oil research. Insect oil is a natural active product solvent that contains lecithin and fat soluble D raw ingredient (such as vitamin A, D, E). These active natural compounds have a significant physiological and biological function with a high value [30].

## **6. The secondary metabolites of edible insects and potential medicinal substances**

A great number of researches in recent years have demonstrated that insect secondary metabolites are valuable sources for discovering novel leading chemicals [31]. Compounds generated from fatty acid, polyketide, terpenoid, nucleoside, and amino acid routes are among the structurally varied arthropod natural products having insect constituents. However, majority of these chemicals' production has not been well investigated [31].

The historic use of plants as remedies, referred to as "ethnobotany," has long been acknowledged and investigated [29]. Insects have long been used as remedies in a variety of civilizations, particularly in traditional Chinese medicine. It might be beneficial in the creation of effective medications. Another ongoing project is finding novel antibacterial structures from natural insect products. More recent investigations [31] are being conducted to investigate the therapeutic effects of isolated chemical components from insects and other arthropods.

## **7. Development and utilization of edible insect's resources**

Based on the diverse insects eaten resources classification, edible insects may be split into food insects, drug/medicinal insects, and drug dual-use insects, among others [22]. Edible insects are intended for everyday food intake, and they have significant nutritional value for humans to create and use. In 2013, the United Nations' Food and Agriculture Organization (FAO) published "Edible Insects: Future Prospects for Food and Feed Security" [22]. It explains the several advantages of consuming insects for humans all around the world. It was proposed in the Fifth Latin American Congress of Dietitians and Nutritionists in 1980 to replace the human food scarcity, which sees them as part of the food source. Insects as human food in many countries has become increasingly visible now [22]. Red ants, grasshoppers, and some predaceous diving beetles (Dytiscidae) have enough insect protein to compete with lean beef, according to scientists. Adult insect protein content is abundant, far exceeding that of pork, cattle, poultry, fish, and eggs. Insects will be the third group in the future, following cell raw material and microbial protein sources, according to experts [32]. People in disadvantaged areas require important nutrients, and the services of insects and spiders are equally beneficial. In industrialized countries such as the United States, insects and spiders are higher protein foods that are considered healthful. With high fat, protein, vitamin, fiber, and mineral content, insects are a very nutritious and beneficial dietary source [22].

At the home level or in bigger industrial scale enterprises, gathering and growing insects can provide employment and economic revenue. It has the potential to employ millions of people all around the world (Reference needed). Furthermore, data

#### *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

suggests that most breeding insects emit less detrimental greenhouse emissions to the environment than animals (Reference needed). This discovery will aid in the reduction of food production costs and greenhouse gas emissions. In China, the processing technology of the functional food and health food industries of edible insects has accelerated at an unprecedented rate in recent years, in tandem with the advancement of contemporary science and technology. For instance, a concentrated insect protein oral beverage including honey, royal jelly, pollen, and propolis, as well as the customary shellac ash. (Reference is required) Some insect oils are primarily employed as fat soluble functional components [32].

#### **7.1 Insect farming**

The majority of bug species in tropical regions are obtained from nature. Insects, on the other hand, must be cultivated like mini-livestock if they are to become a valuable resource. Furthermore, edible insect resources in nature are already under pressure from over-exploitation, habitat deterioration, and pesticide usage [33, 34]. The collecting and selling of the Mopane caterpillar *Imbrasia belina* (*Lepidoptera: Saturniidae*), for example, jeopardizes the long-term usage of forestry resources. As a result, a harvesting period restriction has been proposed [35].

Thailand is one of the countries where insect farming plays a vital role, with 20,000 farms producing roughly 7500 tons per year with operations spreading into Laos [36]. Several multinational programs are currently functioning in Africa to encourage insect breeding for human consumption, with a focus on crickets [37]. Farming commercially significant insect species like the Mopane caterpillar has been attempted [38]. However, virus transmission within a confined population is still an issue, and it is not yet economically feasible [38]. Bug rearing firms in the Western world manufacture a variety of insect species for pet food [39]. Some firms in the Netherlands have set up dedicated manufacturing lines for human consumption of mealworms, crickets, and locusts [39]. When insects are used as feed, however, feedstock firms demand big, consistent, and consistent supply, which can only be produced in industrial automated raising facilities [39]. Increased insect production for food and feed on a big scale will provide numerous new hurdles, including disease issues. The *Acheta domesticus densovirus* (AdDNV) is one example, which has decimated commercial house cricket (*Orthoptera: Gryllidae*) rearing throughout Europe and portions of North America [40].

Nigerians gather edible insects from the wild, which is hampered by seasonality, quality time wasted during collecting, and little quantity obtained (Reference needed). As a result of its scarcity, the supply of edible insects will be disrupted, resulting in high cost. In Nigeria, insect farming will help with food provision, particularly in rural areas that are closer to the wild additional revenue for essential expenses such as food, agricultural equipment, and education; and it will help with food shortages due to seasonal drought in output (Reference needed). Insect farming for food also provides chances for landless people and women involved in the collecting, farming/cultivation, processing, and sale of insects to improve their nutrition, get employment, and earn money [41, 42]. Edible insects may be found in all of Nigeria's ecological zones, with each geopolitical zone having a unique edible bug that can be grown for profit. According to Alamu *et al.* [43], of the 22 most eaten insects in Nigeria, 77.3% were Lepidoptera (27.3%), Coleoptera (27.3%), Orthoptera (22.7%), and Isoptera, Hemiptera, and Hymenoptera (22.7%). This demonstrates that edible insect consumption in Nigeria is diverse. Only a small number of insects are farmed

in Nigeria, and those that are farmed are not in commercial quantities. *Rhynchophorus spp*., or palm weevils, are excellent low-cost providers of vital nutrients. They are extremely tasty and are commonly prepared roasted, and they have a low carbon footprint when farmed commercially. Palm weevils are a traditional meal for most rural societies (especially in the south), but they are not farmed for consumption; instead, they are harvested in the wild. Muafor *et al.* [44] described traditional grub harvesting and grub semi-farming as indigenous ways of palm weevil cultivation. These agricultural techniques account for 30 to 75% of household income. Ebenebe & Okpoko [45] reported that, palm weevils were reared on eight distinct culturing substrates (coconut fiber, coconut fiber with palm wine, mahogany sawdust, mahogany sawdust with palm wine, palm frond petiole, palm bunch midrib, sugarcane tops (SCT), and spoilt water melon (SWM)). In terms of materials and labor, palm weevil farming is a cost-effective business. Within three to four months, the larvae attain adulthood and may be collected for eating; they are high in protein.

*Cirina forda* is a Nigerian delicacy eaten mostly by people from the south. It has a high protein, fat, and necessary mineral content. Because there is now no commercial farm providing this wonderful protein source, cultivating it for food will be profitable. A large number of the insects are collected in the wild before being processed and sold in major marketplaces in Nigeria's southwest. *Cirina forda* larvae may be grown on the leaves of a growing *Vittelaria paradoxa* tree, according to Ande and Fasoranti [46]. All instars matured and were gathered within one month. Despite the huge potential contained in the larvae, they have not been economically produced in decades. Starting this business has the potential to be very profitable. According to Ebenebe and Okpoko [45], cricket (*Gymnogryllus lucens*) is the most popular insect eaten in Nigeria, but it can only be caught in the wild.

## **8. Impact of insect quality on consumers' preference and acceptability**

Nutrient content (protein being a key component), insect quality (especially taste, flavor, look, palatability), and external variables (availability, easy pricing, suitable social milieu) are all essential considerations in accepting insects as food [47]. Forestdwelling people have easy access to natural regions, not only in underdeveloped nations but also in rural areas such as Japan [34]. Consumer reactions to wild insects and their food products, as well as their preferences, acceptability, and consumption of insect-based meals, are currently unknown. Anecdotal evidence suggests that in Africa and India, certain wild edible insect species are preferred and accepted above cultivated ones such as silkworms or crickets [34].

Alemu *et al.* [43] observed no significant difference in whole or powdered termite eating in Kenya. Before purchasing termites, such as *Macrotermes falciger*, buyers evaluated the insect stock for freshness, presence of legs, cleanliness, species type, and oil content at the local market. Fried adults were selected by the majority of purchasers (77.6%) [43]. Long-bodied termite soldiers were in high demand and favored over late variants [48]. In Tanzania, Kenya, and Uganda, the grasshopper (*R. differens*) is a traditional delicacy, a source of nutrition, and a delightful multifunctional insect [47]. Consumers preferred salted, boiled, and smoked grasshoppers or deep fried grasshoppers in cotton seed oil above any other single processing technique (smoking, deep frying, sun-drying, toasting, boiling) [47]. *R. differens* adults that had been cooked with salt, onion, and tomato and then dried were favored above those that had merely been deep-dried with salt and onion in another

#### *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

study. The acceptability ratings for these goods were 7.2 and 5.2, respectively (on a scale of 0–9, with 9 being the highest approval) [48].

People in Uganda favored boiled and dried grasshoppers with salt, onion, and tomatoes to those that were just boiled and dried without tomatoes in the case of *R. nitidula* [48]. With the exception of grasshoppers, whose legs are often removed, entire insects are valued in India; larvae, pupae, and adult termites are sometimes combined and sold together by local sellers [49]. Overall, while there was a higher acceptance for insects without much attention to the species, fear of trying an unknown product, lack of taste experience, and a belief of low social acceptance were identified as major barriers to popularizing edible insects [50]. Despite the fact that taste alone failed to distinguish insects from cheese or bread in more than half of the probands tested there was a very low acceptability [51]. Acceptability is also influenced by accurate labeling. Siozios, [52] discovered many discrepancies in identification in packets containing mopane caterpillars, winged termites, and grasshoppers while testing the correctness of insect goods on the UK market. This may make customers less willing to accept and consume insects or insect products.

Information on entomophagy, past experience and familiarity with edible insects, look, flavor, and overall likability of a species are all important considerations when choosing edible species. As a result, views regarding insects as food and food supplemented with edible insects can be influenced by information and knowledge [53]. In fact, a survey conducted two years following the introduction of edible insects in Belgium demonstrated a rising favorable reaction in terms of acceptability, according to Van Thielen *et al.* [54]. A comparable poll of Danish customers found that 23% of them would eat insects [55].

#### **8.1 Insect processing and product quality**

Traditionally, insects are consumed raw or processed (dried, crushed, pulverized, grounded, pickled, cooked, boiled, fried, roasted/grilled, toasted, smoked or extruded [54]. Besides these techniques, Kewuyemi *et al.* [56] suggested fermentation to enrich the inherent composition of insect-based products and to induce anti-microbial, nutritional and therapeutic properties. Similarly, defatted *T. molitor* larvae and oil could be used as food ingredients. Defatted mealworm powder is high in protein, minerals, and bioactive substances, and has a savory flavor due to the abundance of amino acids. The oil is high in tocopherol and has a long shelf life [57]. Insects are frequently fasted before processing, and big specimens are degutted or defatted since the gut may contain undigested plant material, excreta, bacteria, and other contaminants; also, degutted insects have greater crude fiber protein levels [56]. Tribal communities have consistently embraced this approach since it is efficient and practical, especially for huge lepidopteran larvae. Insects that have been processed can be freeze-dried, sun-dried, or canned. Consumer preferences, insect species availability and compatibility, social custom, religious rites, tribal ethics, and family tradition may all influence processing procedures [58]. Anuduang *et al.* [59] investigated the antioxidant characteristics of silkworm powder at four different drying temperatures (80, 100, 120, and 140°C) and found that the lowest drying temperature maintained the most phenolic compounds and antioxidants.

When choosing a food item based on "post-ingestive fitness," the processing method can aid in the removal of anti-nutrients and other harmful components while also extending the shelf life. As a result, processing is necessary to retain nutritional content, increase shelf life, and obtain functional and fortified foods [57]. Products are supplemented with insect chitosan (a polysaccharide derivative of chitin) in food processing facilities, which is more soluble and so favored over raw chitin [60]. Traditional wisdom based on centuries of experience is regularly used by local communities to improve insect-based cuisine [61]. Methods can, of course, evolve and be replaced by others, since each has benefits and disadvantages that are tailored to area circumstances. In North-East India, for example, roasting, grilling, and frying are commonly used because insects taste better than boiling and baking [62].

Vitamins are generally heat sensitive, and heat processing reduces the quantity of these essential chemicals fully or partially. To avoid insect damage, storage conditions are critical. However, whereas the level of tocopherol in *T. molitor* and *Zophobas morio* did not change in various settings [63], the antioxidant capabilities of silkworm powder did. Nyangena *et al.* [64] investigated the effects of traditional processing techniques on the proximate composition and microbiological quality of *Acheta domesticus, Ruspolia differens, Hermetia illucens*, and *Spodoptera litoralis*, including boiling, toasting, solar-drying, oven drying, boiling + oven drying, boiling + solardrying, toasting + oven-drying, toasting + solar-drying, toasting + oven-drying. Traditional processing enhanced microbiological safety but reduced nutritional value, according to the researchers [63].

#### **8.2 Processing and marketing**

The Mopane caterpillar trade is significant business in southern Africa. Styles estimated in 1994 that an annual population of 9500 million mopane caterpillars in South Africa's 20,000 km2 of mopane veld was worth more than US\$ 80 million, with around 40% going to producers who are mostly impoverished rural women [59]. To alleviate child malnutrition, supplemental diets based on edible termites were designed and assessed in Kenya. It can be processed into economical and safe meals with acceptable nutrient density, according to the findings [65]. To stimulate entomophagy in Kenya, termites and lake flies were baked, boiled, and cooked to extend shelf life and then processed into common consumer items like crackers, muffins, sausages, and meat loaf. These are ways for making naturally gathered items available for extended periods of time. Techniques including drying, acidifying, and lactic fermentation can be used to preserve edible insects and insect products without the need of a refrigerator [30]. However, insects should be farmed to better manage and ensure the supply of such insect goods. Then freeze-drying (dehydration of the frozen insect via sublimation) is commonly used [30].

#### **8.3 Consumer acceptance**

In tropical areas, insects are a major source of protein, yet Europeans are wary of eating them. Bequaert ascribed western people's reluctance to eating insects to 'prejudice' and cultural, conditioning over a century ago: "What we eat and what we do not eat is, after all, a question of tradition and fashion (rather than) anything else" [66]. DeFoliart also saw the western mindset and prejudice against eating insects as a significant impediment to the introduction of this sustainable food source. Yen [67] predicted that 'westernization' of insect-eating communities would lead to a shift away from entomophagy, while western countries, as main consumers of cattle protein, would miss out on a chance to lessen their environmental impact. Others have emphasized the necessity for techniques to overcome the psychological and

#### *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

cultural hurdles to entomophagy, citing the value of insects as human food as a difficult test case [68]. In Belgium and the Netherlands, research found that motives for sustainable food consumption promoted the acceptance of insects as a protein source [67, 69]. Customers in Thailand, where insects are a part of the local culinary culture, saw insects differently from Dutch consumers in terms of flavor and familiarity. Mealworms, for example, were greatly disliked by Thai participants owing to their link with larvae found in decaying debris [67]. The Dutch individuals, who were more familiar with mealworms as food, did not have this link. The following solutions have been offered to alleviate the aversion to eating insects [67].


### **9. Food safety and legislation**

A number of writers have addressed food safety concerns, with urgent legal implications. Contaminants such as heavy metals, mycotoxins, pesticide residues, and infections are all potential risks. The existing research on insect eating in tropical regions shows that insects gathered for human consumption do not pose any substantial health risks [70], but there is little information on insects cultivated for food or feed. Nobody regarded insects to be food or feed at the time the legislation was enacted, therefore when the word "animal" is used in the statute, insects are frequently included. The EU Regulation 1099/2009, for example, states that animals must be murdered in approved slaughterhouses in the presence of an Animal Welfare Officer; this plainly does not apply to insects [24].

In the case of insects as food, the EU has yet to rule whether an insect product is regarded a novel food because it was not consumed "in a considerable degree" in the EU prior to May 15, 1997. If this is the case, the manufacturer must supply a Novel Food Dossier, among other documents, demonstrating that the product is safe for consumers. The EU adopted a rule in 2013 permitting the use of non-ruminant proteins in aquaculture feed for fish; a removal of the restriction on insect proteins in feed for food-producing pigs and poultry is being studied [23].

Food containing insects, such as the Yellow mealworm *Tenebrio molitor* (*Coleoptera: Tenebrionidae*), may cause allergy reactions in those sensitive to home dust mites and crustaceans [25]. Recent evidence reveals that insects and crustaceans (such as shrimps), which have long been thought to be taxonomically distinct branches of the arthropod family tree, are really taxonomically linked [28]. When an insect product is found to be allergic, adequate labeling is essential.

### **10. The way forward**

The recent surge in interest in insects as food and feed was sparked in part by the release of an FAO report in 2013, which has been downloaded more than 7 million times. Wageningen University and the FAO jointly organized the first conference on this topic, "Insects to Feed the World," in the Netherlands in 2014. This meeting drew 450 people from 45 different nations. In the agriculture, food, feed, and health sectors, research institutes, universities, private firms, international organizations, civil society, and government agencies were all represented [71].

Edible insects harvested from natural resources support livelihoods since they may be consumed and/or sold. Research on sustainable harvesting, semi-domestication, and farming is required to avoid overexploitation. Some insect pests, such as edible grasshoppers in Mexico, can be harvested as a management tool [72].

Insect farming veterinary science is still in its infancy. Insect diseases that may emerge during large-scale rearing are poorly understood in terms of biological and genetic characterization, phylogeny, host range, transmission, persistence, epidemic potential, and animal safety, including human safety [73]. Disease transmission has been a problem in the conventional livestock industry on a global scale. Microbial contamination prevention, detection, identification, and mitigation are critical for a successful and safe insect production. Insects can be used to convert organic waste streams like manure into high-protein goods, which is an intriguing prospect. However, further empirical investigations and monitoring are needed to determine the quality of the utilized garbage and the insects created. If insect-based food or feed is contaminated with dangerous bacteria, mycotoxins, or heavy metals, the potential risk to human health must be addressed immediately [73].

In the western world, legislative barriers are currently impeding the advancement of the emerging sector of insects as food and feed. The unfamiliarity with insects as food in the European Union, according to De-Magistris *et al.* [74], may impact EU decision-making since consumers are "conditioned" by cultural patterns and neophobia when it comes to edible insects. As a result, there may be less receptivity to new ideas. On the one hand, the EU investigates and promotes innovative and sustainable food ingredients such as insects, but on the other, it stifles innovation by imposing a regulatory framework that protects consumers from hazards associated with novel food items.

Because it is labor demanding and feed prices are considerable, concerns have been raised about the viability of mass-producing insects. To create vast numbers of highquality and safe insect products in a cost-effective and reliable manner, automation of manufacturing operations would be required. Another option to save feedstock costs is to employ low-value organic by-products and waste streams [75].

A lot of firms are working on this project throughout the world. One firm can process 20 tons of fly larvae every day, yielding seven tons of insect meal and three tons of insect oil. Because vast amounts of feed are necessary for pets, fish, and cattle, and *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

because the components for fishmeal and soymeal continue to rise in price, the use of insect meal as an alternative protein source is becoming a more attractive choice. More attention is needed to optimize desired insect features by selecting specific strains or utilizing genetic enhancement procedures [75].

Cultural and individual expectations regarding the species to be used as food and how they should be prepared should be considered when developing insect-based food products. It is inadequate to emphasize the health and environmental benefits to encourage usage. Gastronomy study is also required to determine whether insects are acceptable as a sustainable food source (deliciousness). Multiple disciplinary approaches (multi-disciplinarily, inter-disciplinarily, and trans-disciplinarily) are required to advance the new agricultural sector of insects as food and feed, as complex problems must be solved that transcend traditional boundaries and require the collaboration of non-academic stakeholders [75].

## **11. Conclusions**

The biggest phylum in the animal kingdom, containing well-known insects, spiders, ticks, and crustaceans, as well as several smaller, lesser-known species and a plethora of bizarre forms only known as fossils. Arthropods make up over 95% of all animal species [1]. There are about one million recognized species, the majority of which are insects [1]. Nobody knows how many arthropod species there are. Some officials believe it may be as high as ten million [1]. The body of an adult arthropod is normally made up of a succession of ring-like segments with a pair of numerous jointed limbs on each segment that move on each other via muscles. It is becoming obvious that arthropod resources may be mass manufactured for use in food production for sustainable development. In terms of nutritional value, food components, and chemical makeup, it is a valuable resource. Meanwhile, the use of edible arthropods has posed a problem in terms of food security, environmental conservation, and the destruction of traditional culinary culture [1].

## **Acknowledgements**

We wish to acknowledge the publishers, for the opportunity to add to the pool of knowledge, some drops of reviewed ideas. We hereby register our profound gratitude to the editors involved in publishing this work for the required quality and desired acceptability.

*Arthropods – New Advances and Perspectives*

## **Author details**

Jonathan Ibrahim1 \* and Dalyop Daniel Gyang2

1 Department of General Study, Gombe State College of Health Sciences and Technology, Kaltungo, Nigeria

2 Department of Pharmacy Technicians, Gombe State College of Health Sciences and Technology, Kaltungo, Nigeria

\*Address all correspondence to: jibrahim@chstkaltungo.edu.ng

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

## **References**

[1] Frederick RS, Jerome CR, Patsy AM. Arthropoda. USA: Access Science from McGraw-Hill Education; 2014

[2] Ojiako OA, Igwe CU. The nutritive, anti-nutritive and hepatotoxic properties of *Trichosanthes anguina* (Snake Tomato) fruits from Nigeria. Pakistan Journal of Nutrition. 2008;**7**:85-89

[3] Ojiako OA, Igwe CU, Agha NC, Ogbuji CA, Onwuliri VA. Protein and Amino acid compositions of *Sphenostylis stenocarpa, Sesamum indicum,Monodora myristica* and *Afzelia africana* seeds from Nigeria. Pakistan Journal of Nutrition. 2010;**9**:368-372

[4] Van Itterbeeck J, van Huis A. Environmental manipulation for edible insect procurement: a historical perspective. Journal of Ethnobiology and Ethnomedicine. 2012;**8**(3):1-19

[5] Jongema Y. List of Edible Insect Species of the World. Wageningen: Wageningen University; 2014

[6] Arnold VH. Edible insects contributing to food security? Journal of Agriculture and Food Security. 2015. DOI: 10.1186/s40066- 015-0041-5. ISBN 978-925-107595-1

[7] Van Huis A, Van Itterbeeck KH, Mertens E, Halloran A, Muir G, et al. Edible Insects: Future Prospects for Food and Feed Security. Rome: Food and Agriculture Organization of the United Nations; 2013

[8] Makkar HPS, Tran G, Heuzé V, Ankers P. State-of-the-art on use of insects as animal feed. Animal Feed Science and Technology. 2014;**197**:1-33

[9] Kenis M, Koné N, Chrysostome CAAM, Devic E, Koko GKD,

Clottey VA, et al. Insects used for animal feed in West Africa. Entomologia. 2014;**2**(218):107-114

[10] Arnold VH, Joost VI, Harmke K, Esther M, Afton H, Giulia M, et al. Edible insects Future prospects for food and feed security. FOA Forestry Paper 171. 2013

[11] Olsen RL, Hasan MR. A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends in Food Science and Technology. 2012;**27**(2):120-128

[12] FAO. Amino Acid Content of Food and Biological Data on Proteins. Rome: Food and Agricultural Organization/ United National Joint Committee; 2014

[13] Sánchez-Muros MJ, Barroso FG, Manzano-Agugliaro F. Insect meal as renewable source of food for animal feeding: a review. Journal of Cleaner Production. 2014;**65**:16-27

[14] Lock ER, Arsiwalla T, Waagbø R. Insect larvae meal as an alternative source of nutrients in the diet of Atlantic salmon (*Salmo salar*) postsmolt. Aquatic Nutrition. 2015. DOI: 10.1111/anu.12343

[15] Rumpold BA, Schlüter OK. Nutritional composition and safety aspects of edible insects. Molecular Nutrient Food Research. 2013;**57**(5):802-823

[16] Rumpold BA, Schlüter OK. Potential and challenges of insects as an innovative source for food and feed production. Innovative Food Science Emergency Technology. 2013;**17**:1-11

[17] McLean E, Cogswell M, Egli I, Wojdyla D, De Benoist B. Worldwide prevalence of anaemia, WHO vitamin and mineral nutrition information

system. Public Health Nutrition. 2009;**12**(4):444-454

[18] Gibson RS. Dietary-induced zinc deficiency in low income countries: challenges and solutions the avanelle kirksey lecture at Purdue university. Nutrition Today. 2015;**50**(1):49-55

[19] Yi L, Lakemond CMM, Sagis LMC, Eisner-Schadler V, Van Huis A, Van Boekel MAJS. Extraction and characterization of protein fractions from five insect species. Food Chemistry. 2013;**141**(4):3341-3348

[20] Deng Y, Chen XM, Wang SY, et al. Common edible insects and nutritional value from food: How regulations and information can hamper radical innovations in the European Union. British Food Journal. 2010;**117**(6):1777-1792

[21] Rong BX, Gan SY. Ants and preparation of trace element analysis. Chinese Traditional Invertebrates Zoo Biology. 1998;**17**:123-134

[22] Van Huis A. Potential of insects as food and feed in assuring food security. Annual Review of Entomology. 2013;**58**(1):563-583

[23] DeFoliart G. Insect as human food; Gene DeFoliart discusses some nutritional and economic aspects. Journal of Crop Protection. 1992;**11**:395-399

[24] Verbeke W. Profiling consumers who are ready to adopt insects as a meat substitute in a Western society. Food Quality and Preference. 2015;**39**:147-155

[25] Charlton AJ, Dickinson M, Wakefield ME, Fitches E, Kenis M, Han R, et al. Exploring the chemical safety of fly larvae as a source of protein for animal feed. Journal of Insects Food and Feed. 2015;**1**(1):7-16

[26] Oliveira JS, de Carvalho JP, de Sousa RF, et al. The nutritional value of four species of insets consumed in Angola. Ecology of Food and Nutrition. 1976;**5**:91-97

[27] Rong BX, Gan SY. Ants and preparation of trace element analysis. Chinese Traditional and Herbal Drugs. 1987;**18**:47-49

[28] Zhou ZH, Yang W, Xu DP, et al. Analysis of Resource Value of Edible Insect. China: Science and Technology Press; 2002. pp. 71-146

[29] Wen LZ. Nutrition of edible insects in Mexico. Entomological Knowledge. 1998;**35**(1):58-61

[30] Liu XG, Ju XR, Wang HF, et al. Insect oil and its nourishment appraisement. Journal of the Chinese Cereals and Oils Association. 2003;**6**:11-13

[31] Matthew G, Schroeder FC. Insect natural products; comprehensive natural products II. Technology of Food Industry. 2014;**17**:390-394

[32] Klunder HC, Wolkers-Rooijackers J, Korpela JM, Nout MJR. Microbiological aspects of processing and storage of edible insects. Food Control. 2012;**26**:628-631

[33] Payne CLR. Wild harvesting declines as pesticides and imports rise: The collection and consumption of insects in contemporary rural Japan. Journal of Insects Food and Feed. 2015;**1**(1):57-65

[34] Payne CLR, Evans JD. Nested houses: Domestication dynamics of humanwasp relations in contemporary rural Japan. Journal of Ethnobiology and Ethnomedicine. 2017;**13**:13

[35] Akpalu W, Muchapondwa E, Zikhali P. Can the restrictive harvest *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

period policy conserve mopane worms in southern Africa? A bioeconomic modeling approach. Environmental Development Economy. 2009;**14**(5):587-600

[36] Hanboonsong Y, Jamjanya TT, Durst PB. Six-legged Livestock: Edible Insect Farming, Collection and Marketing in Thailand. Bangkok: Regional Office for Asia and the Pacific of the Food and Agriculture Organization of the United Nations; 2014

[37] Hanboonsong Y, Durst PB. Edible Insects in Lao PDR: Building on Tradition to Enhance Food Security. Bangkok: Regional Office for Asia and the Pacific of the Food and Agriculture Organization of the United Nations; 2014

[38] Ghazoul J. Mopani Woodlands and the Mopane Worm: Enhancing Rural Livelihoods and Resource Sustainability. London: DFID; 2006

[39] Alltech. Global Feed Survey. 2015. Available from: http://www.alltech.com/ sites/

[40] Szelei J, Woodring J, Goettel MS, Duke G, Jousset FX, Liu KY, et al. Susceptibility of North-American and European crickets to *Acheta domesticus* densovirus (AdDNV) and associated epizootics. Journal of Invertebrate Pathology. 2011;**106**(3):394-399

[41] Gahukar RT. Edible insects farming: Efficiency and impact on family livelihood, food security, and environment compared with livestock and crops. 2016. pp. 85-111. DOI: 10.1016/ B978-0-12-802856-8.00004-1

[42] Gahukar RT. Edible insects collected from forests for family livelihood and wellness of rural communities: A review. Global Food Security. 2020;**2020**:25

[43] Alamu OT, Amao AO, Nwokedi CI, Oke OA, Lawa IO. Diversity and nutritional status of edible insects in Nigeria: A review. International Journal of Biodiversity and Conservation. 2013;**5**(4):215-222

[44] Muafor FJ, Gnetegha AA, Philippe LG, Patrice L. Exploitation, Trade and Farming of Palm Weevil Grubs in Cameroon. Bogor, Indonesia: CIFOR; 2015

[45] Ebenebe CI, Okpoko VO. Preliminary studies on alternative substrate for multiplication of African palm weevil under captive management. Journal of Insects as Food and Feed. 2016;**2**(3):171-177

[46] Ande AT, Fasoranti JO. Some aspects of the biology, foraging and defensive behaviour of the emperor moth caterpillar, Cirina forda (Westwood). International Journal of Tropical Insect Science. 1998;**18**(03):177-181

[47] Van Huis A. Edible insects: Marketing the impossible? Journal of Insects Food Feed. 2017;**3**:67-68

[48] Netshifhethe SR, Kunjeku EC, Duncan FD. Human uses and indigenous knowledge of edible termites in Chombe district, Limpopo Province, South Africa. South African Journal Sciences. 2018;**2018**:11

[49] Mmari MW, Kinyuru JN, Laswai OK, Okoth JK. Traditions, beliefs and Indigenous technologies in connection with the edible longhorn grasshopper, Ruspolia differens (Serville) in Tanzania. Journal of Ethnobiology and Ethnomedicine. 2017;**13**:60

[50] Fombong FT, Van der Borght M, Broeck JV. Influence of freeze-drying and oven-drying post blanching on the nutrient composition of the edible insect, Ruspolia differens. Insects. 2017;**8**:102

[51] Schäufele I, Albores EB, Hamm U. The role of species for the acceptance

of edible insects: Evidence from a consumer survey. British Food Journal. 2019;**121**:2190-2204

[52] Siozios S, Massa A, Parr C, Verspar RL, Hurst GD. DNA barcoding reveals incoorect labelling of insects sold as food in the UK. Peer Journal. 2020;**8**:e8496. DOI: 10.7717/peerj.8496

[53] Meyer-Rochow VB, Hakko H. Can edible grasshoppers and silkworm pupae be tasted by humans when prevented to see and smell these insects? *Journal of Asian Paific*. Entomology. 2018;**21**:616-619

[54] Van Thielen L, Vermuyten S, Storms B, Rumpold B, van Campenhout L. Consumer acceptance of foods containing edible insects in Belgium two years after their introduction to the market. Journal Insects Food and Feed. 2019;**5**:35-44

[55] Barsics F, Megido RC, Brostaux Y, Barsics C, Blecker C, Haubruge E, et al. Could new information influence attitude to food supplemented with edible insects? British Food Journal. 2017;**119**:2027-2039

[56] Kewuyemi Y, Kesa H, Chinna CE, Adebo OA. Fermented edible insects for promoting food security in African. Insects. 2020;**11**:283

[57] Melghar-Lalanne G, Hernandez-Alvarez AJ, Salinas-Castro A. Edible insects processing: Traditional and innovative technologies. Comprehensive Review on Food Sciences and Food Safety. 2019;**2019**:18

[58] Son YJ, Choi SY, Hwang IK, Nho CW, Kim SH. Could defatted mealworm (Tenebrio molitor) and mealworm oil be used as food ingredients*?* Food. 2020;**9**:40

[59] Anuduang A, Loo YY, Jomduang S, Lim SJ, Mustapha WAW. Effect of thermal processing on physico-chemical and antioxidant propertie in mulberry silkworm (*Bombyx mori* L.) powder. Foods. 2020;**9**:871

[60] Williams JP, Williams JR, Kirabo A, Chester D, Peterson M. Nutrient content and health benefits of insects. In: Dossey AT, Morales-Ramos JA, Rojas MG, editors. Insects as Sustainable Food Ingredients: Production, Processing and Food Applications. New York, NY, USA: Elsevier Inc; 2016. pp. 61-84

[61] Chakravorty J, Ghosh S, Meyer-Rochow VB. Practices of entomophagy and entomotherapy by members of the Nyishi and Galo tribes, two ethnic groups of the state of Arunachal Pradesh (North East India). Journal of Ethnobiology and Ethnomedicine. 2011;**7**:5

[62] Meyer-Rochow VB, Chakravorty J. Notes on entomophagy and entomotherapy generally and information on the situation in India in particular. Applied Entomology and Zoology. 2013;**48**:105-112

[63] Gahukar RT. Edible insects collected from forests for family livelihood and wellness of rural communities: *A review*. Global Food Security. 2020;**25**:100348

[64] Nyangena DN, Christopher M, Samuel I, John K, Hippolyte A, Sunday E, et al. Effects of traditional processing techniques on the nutritional and microbiological quality of four edible insect species used for food and feed in East Africa. Journal of Foods. 2020;**9**(5):574

[65] Sabolová M, Adámková A, Kouˇrimská L, Chrpová D, Pánek J. Minor lipophilic compounds in edible insects. Potravinarsmt. 2016;**10**:400-406 *Arthropods: Prospect of Household Food Security DOI: http://dx.doi.org/10.5772/intechopen.106752*

[66] Bequaert J. Insects as food: How they have augmented the food supply of mankind in early and recent years. Natural Historical Journal. 2015;**21**:191-200

[67] Yen AL. Edible insects: traditional knowledge or western phobia? (Special Issue: Trends on the edible insects in Korea and abroad.). Entomological Research. 2009;**39**(5):289-298

[68] Kinyuru JN, Konyole SO, Owuor BO, Kenji GM, Onyango CA, Estambale BB, et al. Nutrient composition of four selected winged termites in western Kenya. Journal of Food Composition and Analysis. 2013;**30**(2):120-124

[69] Looy H, Dunkel FV, Wood JR. How then shall we eat? Insect-eating attitudes and sustainable foodways. Agricultural Human Values. 2014;**31**:131-141

[70] Tan HSG, Fischer ARH, Tinchan P, Stieger M, Steenbekkers LPA, Van Trijp HCM. Insects as food: exploring cultural exposure and individual experience as determinants of acceptance. Food Quality and Preference. 2015;**42**:78-89

[71] Verhoeckx KCM, Van Broekhoven S, Den Hartog-Jager CF, Gaspari M, DeJong GAH, Wichers HJ, et al. House dust mite (Der p 10) and crustacean allergic patients may react to food containing Yellow mealworm proteins. Food and Chemical Toxicology. 2014;**65**:364-373

[72] Pennisi E. All in the (bigger) family revised arthropod tree marries crustacean and insect fields. Science Total Environment. 2015;**347**(6219):220-221

[73] Van Huis A, Vantomme P. Conference report: insects to feed the world. Food Chain. 2014;**4**(2):184-192

[74] De-Magistris T, Pascucci S, Mitsopoulos D. Paying to see a bug on my food: How regulations and information can hamper radical innovations in the European Union. Britain Food Journal 2015;**117**(6):1777-1792

[75] Cerritos R, Cano-Santana Z. Harvesting grasshoppers *Sphenarium purpurascens* in Mexico for human consumption: a comparison with insecticidal control for managing pest outbreaks. Journal of Journal of Crop Protectionection. 2008;**27**(3-5):473-480

## **Chapter 10**

## Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview

*Simone Magela Moreira, Ariane Flávia do Nascimento and Bruna Macena Pereira de Souza*

### **Abstract**

Spotted fever is caused by *Rickettsia rickettsii* and is transmitted through tick's saliva. Humans, ticks, and capybaras (*Hydrochoerus hydrochaeris*) are often coexisting in environments that favor the spread of Brazilian spotted fever (BSF). Although capybaras do not transmit *R. rickettsii*, they can amplify these bacteria among tick vector populations, playing a significant role in the one health approach and epidemiology of the disease. Urban populations of capybaras have increased, especially in Southeast Brazil, as well as the number of cases and lethality of BSF have increased in the country since the 1980s. This expansion is mainly determined by the availability of food and the absence of predators. Thus, urban areas, including parks and university campuses, provide an abundance of food and protection against predators, ensuring the multiplication of the species and increasing the risk of transmission to humans due to the proximity of man with animals in the urban environment. Therefore, this chapter aims to address aspects of spotted fever, considering the many dimensions of the species involved, contributing to public strategies and policies.

**Keywords:** urban disease, arthropod vectors, family Caviidae, rickettsiosis

### **1. Introduction**

Brazilian Spotted Fever (BSF) also known as New World Spotted Fever or São Paulo Exanthematic Typhus [1] is becoming increasingly widespread among regions of Brazil. Since 2001, Brazil has reported the urbanization of BMF, particularly in the states of São Paulo and Minas Gerais where the disease is already considered endemic in many areas [2].

BSF is an infectious, multisystemic, and febrile disease caused by the species *Rickettsia rickettsii* and *R. parkeri*, which are the first responsible for the most serious manifestations, whose lethality can reach 80%, in situations of late diagnosis or lack of access to health services, common in developing countries. Although the expansion of occurrence spaces can have many causes, a commonly associated ecological element is the presence of capybaras, currently found in water bodies and lawns in urban areas [3]. They participate in the transmission cycle, being considered important

amplifiers of vector ticks [4], affecting the endemicity and zoonotic aspects [5] of the occurrences. In fact, these rodents are spreading far beyond rural areas, forming clusters in leisure spaces, parks, and lakes present in highly urbanized cities, making infestation by ticks common in people who visit these places [6, 7].

Vector-borne diseases are relevant to human, animal, and environmental health, as pathogens, vectors, and hosts interact through pathologies and can change their epidemiology over time [8]. When considering the changes promoted by the exploitation of natural resources that result in the fragmentation of habitats and changes in ecosystems, it is possible to assume that there is a greater interaction between humans and arthropod-borne pathogens.

In this context, the global strategic framework for health, created to mitigate the risk and minimize the impact of emerging infectious diseases at the animalhuman-ecosystem interface and socio-economy, highlights the need for action in One Health Perspective that fits perfectly with the approaches relating to the BSF. Based on the principles of "one world," "one health," the referred framework resulted from an action between specialized agencies, such as the World Health Organization (WHO), the United Nations (UN) Food and Agriculture Organization (FAO), and the International Organization for Animal Health (OIE), which jointly recognized the link between human welfare, animals, and the environment [9]. Diseases involving humans and animals (domestic and wild) should be addressed as a priority in an interdisciplinary manner to combat threats and promote the health of life on Earth [10]. The approach must be holistic for disease prevention and for the integrity of the ecosystem that sustains all forms of life.

Due to the complexity of the parasitic cycle involving different hosts (wild animals, arthropod vectors, and humans), the conditions and variables that affect interactions are not completely understood, particularly when related to vector diseases. Therefore, the present narrative intends to provide some clues for a better understanding of some of the main characteristics associated with the occurrence of BSF.

### **2. Vector-borne diseases in the urban environment**

In 1950, only 30% of the world's population lived in urban areas. World's population is increasingly urban with more than half living in urban areas. This number continues to increase, and by 2050, two-thirds are expected to be living in newly urbanized areas [11]. However, the size and density of human populations are creating challenges for many dimensions of human health, including the (re)emergence of zoonotic diseases, particularly those transmitted by vectors [12].

Changes in landscape structure stimulate the loss, rotation, or homogenization of biodiversity, increasing the contact between humans and animals, which can influence the dynamics of transmissions in communities of reservoir hosts and vectors, contributing to modulations in epidemiological processes and the expansion of pathogens that reach the humans [13, 14]. The beginning of the 2020s was marked by a serious pandemic that initially presented itself with zoonotic characteristics, whose cause corroborates the new thinking that as humans spread, pathogens also spread, representing an even greater problem in countries with a large number of poor people and in emerging economies. This is because, in such locations, in addition to much nature being transformed into agricultural or urban areas, health systems are usually underfunded and have difficulties in dealing with possible outbreaks [15].

#### *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

Cities, as densely populated areas, have always been habitats for domestic animals. For some time, however, they are increasingly housing "wild" animals as they present themselves as safe and well-supplied places where these animals have chosen to survive and raise their descendants. This is because, in their decisions, when choosing a residence, food and security are more attractive than other aspects of the landscape [16]. As a result, a park close to busy streets, with noisy children, has been more attractive to these animals than the curious quietness of rural landscapes, "drenched in chemicals" [17].

Of course, given the complexities of ecosystems and rapid global changes, the effects of land use on the ecological factors that sustain zoonotic occurrences cannot be hastily judged [18]. Although there is evidence that the diversity of local species affects the transmission of pathogens [19], this result is not generic, with the greatest risks for diseases caused by pathogens transmitted by arthropod vectors being proven [20, 21], as in the BSF cycle.

The reason why such pathogens spread after environmental changes is not that we suddenly come into contact with wild animals, such as jaguars and wolves. This hypothesis does not answer the modern questions that involve the maintenance, for decades, of these zoonotic cycles in the most anthropized environments. On the contrary, researchers reveal that most common wild animals, particularly those known to carry pathogens threatening to humans, are more prolific in these areas [15]. However, the biases that cooperate for the intense multiplication of these vectors after the urbanization process are not yet fully clarified. Surprisingly, animals that generally carry many viruses or bacteria seem to better tolerate the destruction of nature, when compared with those that carry fewer pathogens [22]. One reason for this could be that these animals are usually quite small and short-lived or have adaptive immune strategies that do not let them get sick from the pathogens they host.

The tendency for hosts and non-hosts to respond differently to human-induced changes in their habitats has been observed in some specific disease systems, but may contribute to the documented links between anthropogenic ecosystems and emerging zoonoses [21, 23] and for BSF, transmitted in an urban cycle that involves ticks, capybaras, and humans. Hosts with an accelerated life cycle contribute to an increase in their abundance, virtually due to life history trade-offs—between reproductive rate and investment— [24], associated with the ability to be resilient in the face of anthropic pressures [25]. In addition, characteristics such as host status, human tolerance [26], as well as the challenge load and co-evolution of shared pathogens [13] contribute to the clarification of such interactions.

### **3. Species involved in the transmission of spotted fever in Brazil**

BSF is caused by Gram-negative bacteria of the genus Rickettsia (Rickettsiales: Rickettsiaceae), transmitted by vectors that use different vertebrate hosts, altering the endemicity and zoonotic aspects of their occurrence. Due to their strictly intracellular survival, these bacteria are classically transmitted to humans by arthropods, which include ticks, mites, fleas, and lice. However, many non-pathogenic human species have been described, of which the true roles in the ecological relationships with the vectors and with the pathogenic rickettsiae have not yet been fully clarified [27].

Since 2001, Brazil has reported an expansion of transmission areas, which is seriously integrated with the increase in the number of reported cases and in their lethality. The bioagent *R. rickettsii* is the main species causing BSF, being restricted to the Americas with confirmations, in addition to Brazil, Canada, United States, Mexico, Costa Rica, Panama, Colombia, and Argentina. However, in the country, other rickettsiosis from the spotted fever group has already been isolated, such as *Rickettsia parkeri* cepa Mata Atlântica and *R. parkeri stricto sensu*, whose notifications are associated with less severe and, as a rule, non-lethal clinical conditions [28, 29]. Added to this diversity of infectious agents, there is a variety of potential vectors that make the enzootic and epidemic cycle of BMF in Brazil quite complex, as a result of possible eco-epidemiological variations.

Ticks can act as vectors and reservoirs in the transmission dynamics of pathogens from the spotted fever group. Several species of Rickettsia can coexist in the same environment, so that different species of ticks that parasitize different mammals can also become infected. The main ticks implicated in the transmission of *R. rickettsii* in the United States are *Dermacentor andersoni* and *D. variablilis*; in some areas in Mexico and in the state of Arizona in the United States, *Rhipicephalus sanguineus* has been indicted as the vector; in South America, the tick species *Amblyomma cajennense* is the most commonly incriminated vector.

However, in the context of the BSF, the following interactions are currently described: [i] *R. rickettsii* transmitted by the tick *Amblyomma sculptum* and *Amblyomma aureolatum* in the Southeast and parts of the South region; [ii] *R. parkeri* Atlantic Forest strain vectored by *Amblyomma ovale* in Atlantic Forest fragments in the South, Southeast, and Northeast of the country; and [iii] *Amblyomma tigrinum* infected with R. *parkeri* is in the Pampa biome in the South region, distinguishing these Brazilian areas from others in Latin America [28, 30, 31].

Below, images of the two main tick species associated with the transmission of the bacterium *R. rickettsii*, which causes Brazilian spotted fever (**Figure 1**).

Bacterial infection in arthropods occurs during hematophagy performed on a rickettsemic, vertebrate host; being favored by transovarian and/or transstadial transmission, which balances part of the damage caused by infection in vector ticks [33]. In turn, the transfer of the pathogen to another vertebrate occurs when the infected ectoparasite takes a new blood meal, after the changes in phases. Thus, the occurrence of Rickettsia in a given space is based on the coexistence of ixodid species

**Figure 1.** *Adult male ticks of the species (A) A. sculptum and (B) A. aureolatum. Source: [32].*

#### *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

susceptible to infection and on vertebrates capable of sustaining this tick's population. Both can vary over time and space, influencing the epidemic cycle by overlapping human activities with the proximity of other vertebrate hosts and the seasonality of the tick [30, 34].

In this aspect, some key factors in the epidemiology of BSF, particularly the occurrence of *R. rickettsii* in southeastern Brazil, are already partially clarified and point to the need for amplifying hosts to maintain transmission. Larvae, nymphs, and adults of *A. sculptum* are partially refractory to rickettsia and less than half of infected females are able to promote transovarian transfer (transmission to offspring) effectively. In addition, higher mortality and lower reproductive performance are observed when the tick is infected, compared with those free from the pathogen [35]. Given this finding, mathematical models indicated that *A. sculptum* cannot sustain *R. rickettsii* for successive generations without the genesis of new cohorts of infected ticks, via horizontal transmission, made possible by vertebrate amplifying hosts, during rickettsemia.

Horses are primary hosts of the *Amblyoma sculptum* tick. They act in the maintenance of these arthropods and in the movement of rickettsiae between environments. Even though they are not susceptible to infection, horses serve as sentinels in epidemiological studies, showing the distribution of the disease and predicting human cases [36]. However, in the contexts of the occurrences, the capybara (*Hydrochoerus hydrochaeris*) appears as the largest amplifying host of *R. rickettsii* for *A. sculptum* in BSF endemic areas in southeastern Brazil [7, 37–39]. In the state of São Paulo, some areas became endemic for BSF after the detection of an increase in the number of individuals in free-ranging capybara clusters [40].

Thus, the sanitary monitoring of capybara populations is essential for the control and conservation of public health. For the record, it is worth mentioning that the tick *Amblyomma dubitatum* has also been frequently discovered infesting capybaras in southeastern Brazil, despite not playing an essential role in the epidemiology of BSF [41–43].

## **4. Aspects of the epidemiological scenario**

The first report of spotted fever in Brazil occurred in São Paulo, in 1929 [1], and *R. rickettsii* transmitted by the tick A. cajennense was indicated as the causal agent. In the report, the similarities with Rocky Mountain spotted fever were already highlighted. In the following two decades, new occurrences were described in the state of Minas Gerais [44] and in São Paulo, where the species *Rickettsia typhi* was isolated for the first time [45]. After this period, BSF remained for several years as a silent disease, subordinated to existing flaws in medical care, diagnosis, and information processes.

Between the 1980s and 2000s, case reports are seen in scientific journals, indicating infections that occurred in southeastern Brazilian states, after four cases in Rio de Janeiro [46] and in the state of Espírito Santo, which came to be considered as an endemic region for BSF [47]. The states of Minas Gerais and São Paulo showed a serious reemergence, in whose epidemic outbreaks occurred in 1984, 1992, 1995, and the lethality reached about 50% of diagnosed patients [48–50]. Despite this, it was only in 2001 that the BSF notification became mandatory and, in 2014, it was determined that, in addition to being mandatory, it must be immediate, taking place within a maximum period of 24 hours, in order to improve surveillance, diagnosis, and treatment [51].

Due to the continuous increase in cases and the expansion of the areas of occurrence, BSF was considered an emerging disease in Brazil, without, however, a significant advance in information and knowledge about the disease, among the scientific, medical classes, and the general population [31]. Even today, there is not enough data to determine the impact of BSF on the Brazilian population, since prospective longitudinal studies documenting the natural course of the disease have not been performed.

In the brief history described above, two important aspects stand out in the epidemiological context. Failures in the diagnosis were confirmed through laboratory documents in the various fatal cases that occurred in Minas Gerais until the early 2000s [52]. Equally important, in 1996, Lemos et al. [53] isolated bacteria from the group of *Rickettsia* sp. of spotted fever in the tick *Amblyomma cooperi*, vectors collected from capybaras in São Paulo. It is clear that the impact of the BSF on public health will not be properly evaluated until appropriate methods of diagnosis and epidemiological surveillance are effectively implemented. Recent data bring some clarity about the incidence rates and some aspects (i) of humans affected by the disease; (ii) ticks (maintained by capybaras); and (iii) transmission environments, and need to be analyzed [54, 55]. The transversality between these aspects will be briefly described below.

In the Brazilian occurrences of BSF, white men, aged between 20 and 64 years, coming from rural areas are more commonly infected and report having had contact with ticks during their leisure activities, unlike women who have a domestic and peridomestic environment, as the likely site of infection [56]. Most cases affecting males corroborate the data described in international reports from the Centers for Disease Control and Prevention [57] and the European Center for Disease Prevention and Control [58]. The fact that most cases are represented by white ethnicity may be influenced by the difficulty in observing the rash when in black individuals, and further compromise the diagnosis of BSF in this ethnic group [59].

Studies in endemic areas of BSF have shown that the disease is correlated with environments where there are large populations of the tick *A. sculptum*, which, in turn, are supported by the presence of capybaras, fundamental hosts for this species, in anthropic environments. On the contrary, landscapes similar to these, where there are low parasite loads or where the tick *A. dubitatum* is predominant, did not become endemic areas, even with the presence of capybaras [7]. Recently, research conducted by Geraldi et al. [35] revealed that there are other aspects that contribute to the dynamics of transmission by demonstrating that there are variations in the susceptibility of the tick to infection by *R. rickettsii*, which may explain the different frequencies of BSF in areas where the vector A. sculptum and capybaras cohabit. However, the complete elucidation of the mechanisms that govern this susceptibility and their effects on the risk of the disease in urban environments still need further studies [7].

Historically, BSF notifications predominate in southeastern Brazil, with the percentage of fatal cases ranging from 30–50% [60]. Particularly in the state of São Paulo, there are extensive areas where transmission has been proven, with 978 laboratory confirmed cases between 2001 and 2018 [7]. The disease, however, continues to advance through new territories, reaching the south, northeast, and central-west regions of Brazil [56], varying estimates on the prevalence and incidence (**Figure 2**).

Some factors seem to influence the lethality percentages. Undeniably, the strain that prevails in Brazil is much more virulent when compared with the *R. rickettsii* that occurs in North America, responsible for Rocky Mountain spotted fever [61]. However, *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

#### **Figure 2.**

*Geographical distribution of confirmed cases of spotted fever by federative unit (FU) and average incidence rate in affected municipalities and between 2007. Source: [56].*

aspects such as the lack of specificity in its clinical signs and the absence of exanthema (classic marker) in many patients lead to suspicion and make early diagnosis difficult. Diseases such as dengue, viral exanthematous diseases, and leptospirosis present clinical signs similar to those of BSF, requiring specificities in the differential diagnosis and increasing the possibility of the use of inappropriate drugs that prevent therapeutic cure [62]. Furthermore, it should not be forgotten that infections caused by R. parkeri, a strain present in several regions of the Atlantic Forest, present mild clinical signs, with inoculation bedsores and lymphadenopathy, introducing other elements that make adequate medical management difficult [63]. Furthermore, the geographically restricted availability of parenteral doxycycline, the drug of choice for the treatment of severe cases, highlights the neglected status of BSF in Brazil [64, 65]. A review of the treatment protocol for BSF took place in 2013 and doxycycline is now recommended regardless of patient age, being provided by the Ministry of Health for strategic locations in endemic areas. However, in silent areas or with recent introduction of the agent, the difficulty in accessing the drug remains [66].

In Brazil, rapid environmental changes, the absence of stable policies for environmental preservation, and the low socioeconomic condition of the population are associated with the high importance of BSF—expressed by the high lethality in outbreaks that predominate in family nuclei—establishing this Rickettsiosis as a relevant public health problem. Therefore, continued studies and solutions to support surveillance strategies will help in future assessments of epidemiological aspects.

## **5. The growing urbanization of capybaras and Brazilian spotted fever**

Mammals represent the most successful evolutionary class among vertebrates. Facilitated by a brain that promotes learning and being capable to maintain a constant body temperature, they developed, throughout evolution, a variety of life strategies that allowed them to colonize the most diverse habitats, establishing themselves on all continents [67].

*H. hydrochaeris* is among the largest rodents found in the Neotropics. When Iberian settlers arrived in South America at the end of the fifteenth century, they came across a diverse fauna and the species was originally named, after analogies with other European animals known to them. However, the name capybara originates from the indigenous word (Tupi): kapii'gwara, which means grass eater (ka'pii = "grass" + g wara = "eater") [68]. It had its first detailed description in the mid-seveteenth century, based on observations in the state of Pernambuco, when northeastern Brazil was occupied by the Dutch. Later, in the search to define their origin and their preferred habitats, mistakes were made, but according to [69], the São Francisco River, one of the main Brazilian rivers, should be listed as the typical locality for the species, as mentioned by [70].

In Brazil, capybaras can be found in all 26 states and the Federal District (**Figure 3**) mainly in agricultural habitats, with a predominance of pastures and sugarcane fields where they can reach high densities. They are considered competitors that cause damage to a variety of crops, including sugarcane, corn, rice, bananas, soybeans, and compete for food with cattle, affecting agricultural production [70, 71]. In addition to these places, they frequent bodies of water (rivers, dams, and reservoirs) within urban limits, in public parks, and residential areas [69], currently causing conflicts, particularly in the Southeast, where they invade properties, eat ornamental plants in gardens, and are involved in traffic accidents on the streets and roads [3].

Recent increases in BSF cases [72] and the probable association with high capybara densities have accentuated considerations about the epidemiological role of this rodent in the urbanization of the disease. The expansion of occupation areas occurs as agricultural deforestation occurs, mainly due to the availability of food and the decline of their natural predators, such as jaguars [48, 49]. Thus, they can form numerous populations in certain environments, coming to be considered urban pests. This is because, in anthropogenic wetlands, where it finds an abundant source of food, *H. hydrochaeris* can develop with a carrying capacity greater than that observed in untouched environments. These facts raise important points about the roles played and the risk of transmission in important zoonosis, such as BSF [50].

It is also worth emphasizing relevant aspects regarding the presence of animals in urban daily life: the presence of wild animals in human groups can be interpreted as a possibility of greater exposure to nature and a source of benefits for the mental health of individuals [73], and increasing the value of recreational ecosystem services provided by green areas [74]. The relationship with nature offers benefits, even if there is no handling or prolonged intimacy in contact with animals. Simple eye contact, regardless of duration, can have a broad and robust impact on people's affective and cognitive conditions [73, 75].

According to the biophilia hypothesis [76], as a result of evolution, humans have always sought to connect with other life forms. This hypothesis translated some of the multiple dimensions of humans' innate relationship with nature, including emotional connections with landscapes and animals. In the last decade, *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

#### **Figure 3.**

*Distribution of capybaras (Hydrochoerus hydrochaeris) in Brazil. Black dots show records of the species' presence. Source: [69].*

the benefits of this contact have been increasingly studied [77]. Improvements in neuropsychological development and mental health have been reported when experiences occur in early childhood [78, 79], but benefits such as reductions in social and emotional difficulties and even deterioration cognitive impairment can extend into old age [80].

Urbanization, as it threatens to weaken the link between humans and nature [81], converging with Wilson's proposals relating to biophilia, may favor (or even promote) the acceptance of capybaras in the enclosures of a City. However, it is worth mentioning that as capybaras constitute groups that occupy leisure spaces, parks, and lakes, which, when located in areas with occurrence of BSF, increase the risk of tick infestations among people who visit these places [7, 82].

Although capybaras cannot transmit *R. rickettsii*, they play an important role in public health, as they amplify the agent among tick populations [4]. Thus, despite the presence

of capybaras increasing biodiversity in cities and reinforcing the biophilia hypothesis, they pose a risk in the transmission of pathogens, requiring interdisciplinary participation and integrated actions to improve disease control. Researchers have already proven that BSF-endemic areas have much higher tick loads both in capybaras and in the environment, when compared with areas where the disease is not frequent [7]. And, to make the scenario even more complex, mathematical models have shown that the introduction of a single capybara infected with *R. rickettsii* parasitized by at least one infected tick is enough to establish an infection by *R. rickettsii* in the entire population of *A. sculptum* hosted by up to 50 capybaras [37]. In maintaining the infection, it is noteworthy that a capybara, during the primary infection, can remain in bacteremia for about 14 days, infecting other ticks that feed on its blood during this period [35].

The tick *A. sculptum* infected by *R. rickettsii* remains infected even after ecdysis (changes of stages), being able to transmit the bacteria in the following stages [35]. Thus, even with its preferred hosts in endemic areas, *A. sculptum* can accidentally parasitize humans in all its active stages [51], completing the zoonotic cycle.

Transmission to humans depends on the duration of contact between the tick and the person, requiring at least 4–6 hours for transmission to occur [5]. However, as very small tick stages can transmit rickettsiae, it is very common for people to remain infested long enough with the ticks without realizing it. Symptoms appear between 2 and 14 days after infection [83] and are mostly nonspecific. Early treatment is essential and mortality is associated with the difficulty in establishing the diagnosis, the delay in starting the specific therapy, and the little knowledge of the medical profession about the disease [84].

Tetracyclines and chloramphenicol are the only drugs with proven efficacy to treat BSF. In adults, treatment requires high dosage and needs to be continued for a few days after the fever subsides. Thus, in Brazil, despite the high prevalence and the fact that many areas are considered endemic for BSF, the lack of knowledge about the disease often leads to a delay in diagnosis, complicating the prognosis [85]. Therefore, it is important to take advantage of every opportunity to disseminate and expand knowledge about this disease.

Finally, it is worth noting that capybaras and ticks are only parts of the BSF cycle, requiring a deeper understanding of the different aspects of ecological relationships and monitoring of environmental conditions to reduce infections in humans [86]. We consider that cities are moldable and serve as a habitat for people and animals, and it is essential to analyze the extent to which urban ecology has been concerned with offering opportunities for new and different forms of interaction in human-animal relationships. According to the French anthropologist Philippe Descola [87], it is becoming increasingly clear that the established concepts—since the Renaissance about city and countryside; culture and nature or humans and animals are not sustainable and need to be revisited in contemporary times.

## **6. Final considerations**

In terms of future perspectives, given the persistence of the urbanization pattern, it seems clear that the BSF will not disappear easily from Brazil. In view of the above, there is a need for constant and rigorous epidemiological surveillance in urban areas where capybara is present. However, in the management of the conflicts mentioned above, disinformation must be fought [60] and short-term solutions are not inefficient. Public policies must adapt to manage the issue of BSF, in its urban occurrences,

#### *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

taking into account the many dimensions of the relationships between humans, other animal species, and the environment.

In order to reduce the risk of transmission and minimize the impact of BSF, surveillance and response systems should be instituted at national and regional levels, supporting public and animal health services with strategies to protect the health of ecosystems.

In addition, the greater lethality of BSF is also evidenced by its neglected status in Brazil, such as the lack of information in the health and surveillance sectors and the unavailability, in many regions of the country, of first-choice medication for the treatment of severe clinical cases of the disease.

We understand that the issue of the BSF and all aspects that involve its control must be rethought, correcting interventions not directed to health, with the development of feasible and accessible analysis methodologies within an integrative, multidisciplinary, and multisectoral vision with all that, directly or indirectly, have to do with this problem, in an articulation of planning, governance, and public health, in the search for health cities.

Finally, we emphasize the need to change the current emphasis on the short-term response to the disease and to encourage the construction of more sustainable systems capable of responding effectively to future events that involve the various nuances of the BSF that arise from the environment-animal-human interface.

## **Author details**

Simone Magela Moreira, Ariane Flávia do Nascimento\* and Bruna Macena Pereira de Souza Federal Institute of Minas Gerais, Bambuí, Minas Gerais, Brazil

\*Address all correspondence to: ariane.nascimento@ifmg.edu.br

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **References**

[1] Piza JT, Meyer JR, Gomes LS. Typho Exanthematico de São Paulo. São Paulo: Sociedade Impressora Paulista; 1932

[2] Souza MO. Multiscale analysis for a vector-borne epidemic model. Journal of Mathematical Biology. 2014;**68**(5):1269-1293. DOI: 10.1007/ s00285-013-0666-6

[3] Bovo AA, KMPMB F, Verdade LM, Moreira JR. Capybaras (Hydrochoerus hydrochaeris) in Anthropogenic Environments: Challenges and Conflict2016. pp. 118-189. DOI: 10.1515/ 9783110480849-013

[4] Labruna MB. Brazilian spotted fever: The role of capybaras. In: Moreira JR, Ferraz KMPMB, Herrera EA, et al., edição. Capybara: Biology, Use and Conservation of an Exceptional Neotropical Species. 2013. pp. 371-383. DOI: 10.1590/1089-6891v18e-44671

[5] Darby AC, Cho NH, Fuxelius HH, Westberg J, Andersson SGE. Intracellular pathogens go extreme: Genome evolution in the Rickettsiales. Trends in Genetics. 2007;**27**(10):511-520. DOI: 10.1016/j. tig.2007.08.002

[6] Medeiros AP, Souza AP, de Moura AB, Lavina MS, Bellato V, Sartor AA, et al. Spotted fever group Rickettsia infecting ticks (Acari: Ixodidae) in the state of Santa Catarina, Brazil. Memórias do Instituto Oswaldo Cruz. 2011;**106**(8):926-930. DOI: 10.1590/ S0074-02762011000800005

[7] Luz HR, Costa FB, Benatti HR, Ramos VN, Serpa MCA, Martins TF, et al. Epidemiology of capybara-associated Brazilian spotted fever. PLoS Neglected Tropical Diseases. 2019;**13**(9):e0007734. DOI: 10.1371/journal.pntd.0007734

[8] Harrus S, Baneth G. Drivers for the emergence and re-emergence of vectorborne protozoal and bacterial diseases. International Journal for Parasitology. 2005;**35**(11-12):1309-1318. DOI: 10.1016/j.ijpara.2005.06.005

[9] World Organisation for Animal Health (OIE) Contributing to One World, One Health. A Strategic Framework for Reducing Risks of Infectious Diseases at the Animal-Human-Ecosystems Interface. Paris, France: World Organization for Animal Health (OIE); 2008 https://www.fao. org/3/aj137e/aj137e00.pdf

[10] Wildlife Conservation Society. One World, One Health: Building Interdisciplinary Bridges to Health in a Globalized World Conference. 29th September 2004, The Rockefeller University, New York, NY. 2004. http:// www.oneworldonehealth.org/sept2004/ owoh\_sept04.html

[11] United Nations, Department of Economic and Social Affairs, Population Division. World Urbanization Prospects: The 2014 Revision, Highlights (ST/ESA/ SER.A/352)

[12] Myers SS et al. Human health impacts of ecosystem alteration. Proceedings of the National Academy of Sciences of the United States of America. 2013;**110**:18753-18760

[13] Plowright RK et al. Pathways to zoonotic spillover. Nature Reviews Microbiology. 2017;**15**:502-510. DOI: 10.1038/nrmicro.2017.45

[14] Shah HA, Huxley P, Elmes J, Murray KA. Agricultural land-uses consistently exacerbate infectious disease risks in Southeast Asia. Nature *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

Communications. 2019;**10**:4299. DOI: 10.1038/s41467-019-12333-z

[15] Gibb R, Redding DW, Chin KQ, et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature. 2020;**584**:398-402

[16] Morizot B. Philosophie der Wildnis oder die Kunst vom Weg abzukommen. Reclam Philipp Jun. Ditzingen2020. p. 191

[17] Volker A, Claus-Peter H. Das Verstummen der Natur. Das unheimliche Verschwinden der Insekten, Vögel und Pflanzen – und wie wir es noch aufhalten können. Bonn. 2019. p. 336.

[18] Gottdenker NL, Streicker DG, Faust CL, Carroll CR. Anthropogenic land use change and infectious diseases: A review of the evidence. EcoHealth. 2014;**11**:619-632

[19] Civitello DJ et al. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America. 2015;**112**:8667-8671

[20] LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences of the United States of America. 2003;**100**:567-571

[21] Kilpatrick AM. Globalization, land use, and the invasion of West Nile virus. Science. 2011;**334**:323-327

[22] Kamiya T, O'Dwyer K, Nakagawa S, Poulin R. What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological reviews of the Cambridge Philosophical Society. 2014;**89**:123-134

[23] Pulliam JRC et al. Agricultural intensification, priming for persistence and the emergence of Nipah virus: A lethal bat-borne zoonosis. Journal of The Royal Society Interface. 2012;**9**:89-101

[24] Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC. Constitutive immune defences correlate with lifehistory variables in tropical birds. Journal of Animal Ecology. 2008;**77**:356-363

[25] Purvis A, Gittleman JL, Cowlishaw G, Mace GM. Predicting extinction risk in declining species. Proceedings of the Biological Society. 2000;**267**:1947-1952

[26] Joseph MB, Mihaljevic JR, Orlofske SA, Paull SH. Does life history mediate changing disease risk when communities disassemble? Ecology Letters. 2013;**16**:1405-1412

[27] Burgdorfer W. Considerações ecológicas e epidemiológicas da febre maculosa das Montanhas Rochosas e do tifo do matagal. Em: DH Walker edição. Biologia de doenças rickettsiais. Vol. 1. 1988. pp. 33-50

[28] Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, et al. Update on tick-borne rickettsioses around the world: A geographic approach. Clinical Microbiology Reviews. 2013:657-702. DOI: 10.1128/ CMR.00032-13

[29] Weck B, Dall'Agnol B, Souza U, Webster A, Stenzel B, Klafke G, et al. Spotted fever group Rickettsia in the Pampa biome, Brazil, 2015-2016. Emerging Infectious Diseases. 2016;**22**:2014-2016. DOI: 10.3201/ eid2211.160859

[30] Szabó MPJ, Pinter A, Labruna MB. Ecology, biology and distribution of spotted-fever tick vectors in Brazil.

Frontiers in Cellular and Infection Microbiology. 2013;**3**:1-9. DOI: 10.3389/ fcimb.2013.00027

[31] Oliveira SV, Guimarães JN, Reckziegel GC, da BMC N, de KM A-V, Fonseca LX, et al. An update on the epidemiological situation of spotted fever in Brazil. Journal of Venomous Animals and Toxins including Tropical Diseases. 2016;**7**:65-72. DOI: 10.1186/ s40409-016-0077-4

[32] Moraes-Filho J. Brazilian spotted fever. Journal of Continuing Education in Animal Science of CRMV-SP. 2017;**15**(1):38-45

[33] Eremeeva ME, Dasch GA. Challenges posed by tick-borne rickettsiae: Eco-epidemiology and public health implications. Frontiers in Public Health. 2015;**3**:55. DOI: 10.3389/ fpubh.2015.00055

[34] Szabó MPJ, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna M. In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic Rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology. 2013;**140**:719-728. DOI: 10.1017/ S0031182012002065

[35] Gerardi M, Ramírez-Hernández A, Binder LC, Krawczak FS, Gregori F, Labruna MB. Comparative susceptibility of different populations of Amblyomma sculptum to Rickettsia rickettsii. Frontiers in Physiology. 2019;**10**:653. DOI: 10.3389/fphys.2019.00653

[36] Sangioni LA, Horta MC, Vianna MCB, Gennari SM, Soares RM, Galvão MAM, et al. Ricketsial infection in animals and brazilian spotted fever endemicity. Emerging Infectious Diseases. 2005;**11**:265-269

[37] Polo G, Mera Acosta C, Labruna MB, Ferreira F. Transmission dynamics and control of *Rickettsia rickettsii* in populations of *Hydrochoerus hydrochaeris* and *Amblyomma sculptum*. PLoS Neglected Tropical Diseases. 2017;**11**:e0005613

[38] Polo G, Mera Acosta C, Labruna MB, Ferreira F, Brockmann D. Hosts mobility and spatial spread of Rickettsia rickettsii. PLoS Computational Biology 2018a;14:e1006636. pmid: 30586381

[39] Costa FB, Gerardi M, Binder LC, Benatti HR, Serpa MCA, Lopes B, et al. Rickettsia rickettsii (Rickettsiales: Rickettsiaceae) infecting Amblyomma sculptum (Acari: Ixodidae) ticks and capybaras in a Brazilian spotted feverendemic area of Brazil. Journal of Medical Entomology. 2019;**57**(1):308- 311. DOI: 10.1093/jme/tjz141

[40] Sousa KCM, Calchi AC, Herrera HM, Dumler JS, Barros-Battesti DM, Machado RZ, et al. Anaplasmataceae agents among wild mammals and ectoparasites in Brazil. Epidemiology and Infection. 2017;**145**(16):3424-3437

[41] Guedes E, Leite RC, Pacheco RC, Silveira I, Labruna MB. Rickettsia species infecting Amblyomma ticks from an area endemic for Brazilian spotted fever in Brazil. Revista Brasileira de Parasitologia Veterinária. 2011;**20**:308-311

[42] Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB. Nymphs of the genus *Amblyomma* (Acari: Ixodidae) of Brazil: Descriptions, redescriptions, and identification key. Ticks and Tick-Borne Diseases. 2010;**1**:75-99

[43] Martins TF, Barbieri AR, Costa FB, Terassini FA, Camargo LM, Peterka CR, et al. Geographical distribution of

#### *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

Amblyomma cajennense (sensu lato) ticks (Parasitiformes: Ixodidae) in Brazil, with description of the nymph of A. cajennense (sensu stricto). Parasites & Vectors. 2016;**9**:1-14

[44] Dias E, Martins AV. Spotted fever in Brazil. A summary. The American Journal of Tropical Medicine and Hygiene. 1939;**19**:103-108

[45] Travassos J, Rodrigues PM, Carrijo LN. Tifo murino em São Paulo. Identificação de Rickettsia mooseri isolada de um caso humano. Memórias do Instituto Butantan. 1949;**21**:77-106

[46] Gonçalves AJR, Lopes PFA, Melo JCP, et al. Rickettsioses: A propósito de quatro casos diagnosticados no Rio de Janeiro de febre maculosa brasileira. Folha Médica. 1981;**82**:127-134

[47] Sexton DJ, Muniz M, Corey GR, et al. Brazilian spotted fever in Espirito Santo, Brazil: Description of a focus of infection in a new endemic region. The American Journal of Tropical Medicine and Hygiene. 1993;**49**:222-226. DOI: 10.4269/ ajtmh.1993.49.222

[48] Queirogas EF et al. Dimensões públicas do espaço contemporâneo [tese]. Universidade de São Paulo; 2012

[49] Verdade LM, Gheler-Costa C, Penteado M, et al. The impacts of sugarcane expansion on wildlife in the state of São Paulo, Brazil. Journal of Sustainable Bioenergy Systems. 2012;**2**:138-144. DOI: 10.4236/ jsbs.2012.24020

[50] Passos Nunes FB et al. The dynamics of ticks and capybaras in a residential park area in southeastern Brazil: Implications for the risk of Rickettsia rickettsii infection. Vector-Borne and Zoonotic Diseases. 2019;**19**(10):711-716. DOI: 10.1089/vbz.2019.2479

[51] Souza CE, Moraes-Filho J, Ogrzewalska M, Uchoa FC, Horta MC, Souza SS. Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Veterinary Parasitology, Leiden. 2009. DOI: 10.1016/j.vetpar.2008.12.010

[52] Galvão MAM. Febre maculosa em Minas Gerais: Um estudo sobre a distribuição da doença no Estado e seu comportamento em área foco periurbano. [tesis doctoral]. Belo Horizonte: Faculdade de Medicina – UFMG; 1996.

[53] Lemos ERS et al. Primary isolation of spotted fever in the group rickettsiae from Amblyomma cooperi collected from Hydrochaeris hydrochaeris in Brazil. Memórias do Instituto Oswaldo Cruz. 1996;**91**:273-275

[54] HHB M, Colombo S, Silva MV. Spotted fever: Isolation of Rickettsia from a skin biopsy sample. Revista do Instituto de Medicina Tropical de São Paulo. 1992;**34**:37-41. DOI: 10.1590/ S0036-46651992000100007

[55] de Oliveira SV, Guimarães JN, Reckziegel GC, et al. An update on the epidemiological situation of spotted fever in Brazil. Journal of Venomous Animals and Toxins including Tropical Diseases. 2016;**22**:22. DOI: 10.1186/ s40409-016-0077-4

[56] Oliveira SV et al. Um caso fatal de febre maculosa brasileira em área não endêmica no Brasil: A importância de ter profissionais de saúde que entendam a doença e suas áreas de transmissão. Revista da Sociedade Brasileira de Medicina Tropical. 2016;**49**(05):653-655. DOI: 10.1590/0037-8682-0088-2016

[57] Centers for Disease Control and Prevention (CDC). Rocky Mountain Spotted Fever (RMSF). 2022. Available from: https://www.cdc.gov/rmsf/stats/ index.html

[58] European Center for Disease Prevention and Control (ECDC). Epidemiological situation of rickettsioses in EU/EFTA countries. Technical Report, 2013

[59] Favacho ARM, Rozental T, Calic SB, Scofield MAM, Lemos ERS. Fatal Brazilian spotless fever caused by Rickettsia rickettsii in a darkskinned patient. Revista da Sociedade Brasileira de Medicina Tropical. 2011;**44**(3):395-396. DOI: 10.1590/ S0037-86822011000300028

[60] Walker DH, Raoult D. Rickettsia rickettsii and other spotted fever group rickettsiae (Rocky Mountain spotted fever and other spotted fever). In: Mandell, Douglas, Bennett, editors. Principles and Practices of Infectious Diseases. 6ª edição ed. Filadélfia, PA: Churchill Livingstone; 2005. pp. 2287-2295

[61] Labruna MB, Santos FC, Ogrzewalska M, Nascimento EM, Colombo S, Marcili A, et al. Genetic identification of rickettsial isolates from fatal cases of Brazilian spotted fever and comparison with Rickettsia rickettsii isolates from the American continents. Journal of Clinical Microbiology. 2014;**52**:3788-3791. DOI: 10.1128/ JCM.01914-14

[62] Angerami RN, Câmara M, Pacola MR, Rezende RCM, Duarte RMR, Nascimento EMM, et al. Features of Brazilian spotted fever in two different endemic areas in Brazil. Ticks Tick Borne Diseases. 2012;**3**(5-6):346-348. DOI: 10.1016/j.ttbdis.2012.10.010

[63] Silva N, Eremeeva ME, Rozental T, Ribeiro GS, Paddock CD, Ramos EAG,

et al. Eschar-associated spotted fever rickettsiosis, Bahia, Brazil. Emerging Infectious Diseases. 2011;**17**(2):275-278. DOI: 10.3201/eid1702.100859

[64] Chapman AS, Bakken JS, Folk SM, Paddock CD, Bloch KC, Krusell A, et al. Diagnosis and management of tickborne rickettsial diseases: Rocky Mountain spotted fever, ehrlichioses, and anaplasmosis—United States: A practical guide for physicians and other healthcare and public health professionals. MMWR - Recommendations and Reports. 2006;**55**:1-27

[65] Oliveira SV, Willemann MCA, Gazeta GS, Angerami RN, Gurgel-Gonçalves R. Predictive factors for fatal tick-borne spotted fever in Brazil. Zoonoses Public Health. 2017;**64**:44-50. DOI: 10.1111/zph.12345

[66] Brasil. Ministério da Saúde. Portaria N° 16, de 15 de maio de. Torna pública a decisão de incorporar a doxicilina injetável e o cloranfenicol suspensão para terapêutica da febre maculosa brasileira e outras riquetsioses no Sistema Único de Saúde – SUS. 2014. [Available in]: http:// conitec.gov.br/images/incorporados/ doxiciclina-e-clorafenicol-final.pdf

[67] Rocha JL, Brito JC, Nielsen R, Godinho R. Convergent evolution of increased urine-concentrating ability in desert mammals. Trends in Ecology and Evolution. 2021;**36**(7):637-650. DOI: 10.1111/mam.12244

[68] Houaiss A, Villar MS, Franco FMM. Dicionário Houaiss da Língua Portuguesa. Rio de Janeiro: Ed. Objetiva; 2004

[69] Moreira JR, Wiederhecker H, Ferraz KMPMB, Aldana-Domínguez J, Verdade LM, Macdonald DW. Capybara demographic traits. In: Moreira JR, Ferraz KMPMB, Herrera EA, *Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview DOI: http://dx.doi.org/10.5772/intechopen.106639*

Macdonald DW, editors. Capybara: Biology, Use and Conservation of an Exceptional Neotropical Species. New York: Springer; 2012. pp. 147-167

[70] Ferraz KMPMB, Ferraz SFB, Moreira JR, Couto HT, Verdade LM. Capybara (Hydrochoerus hydrochaeris) distribution in agroecosystems: A cross-scale habitat analysis. Journal of Biogeography. 2007;**34**:223-230

[71] Verdade LM, Ferraz KMPMB. Capybaras (Hydrochoerus hydrochaeris) in an anthropogenic habitat in Southeastern Brazil. Brazilian Journal of Biology. 2006;**66**(1b):371-378. DOI: 10.1590/S1519-69842006000200019

[72] Labruna MB. Brazilian spotted fever: The role of capybaras. In: Moreira JR, KMPMB F, Herrera EA, Macdonald DW, editors. Capybara: Biology, Use and Conservation of an Exceptional Neotropical Species. 1ª ed. 2012. pp. 371-383. DOI: 10.1007/978-1-4614-4000-0\_23

[73] Bratman GN, Hamilton JP, Hahn KS, Daily GC, Gross JJ. Nature experience reduces rumination and subgenual prefrontal cortex activation. Proceedings of the National Academy of Sciences of the United States of America. 2015;**112**:8567- 8572. DOI: 10.1073/pnas.1510459112

[74] Díaz S, et al. Linking functional diversity and social actor strategies in a framework for interdisciplinary analysis of nature's benefits to society. Proceedings of the National Academy of Sciences of the United States of America. 2011;**108**:895-902. DOI: 10.1073/ pnas.1017993108

[75] Taylor AF, Frances EK, William CS. Views of nature and self-discipline: Evidence from inner city children. Journal of Environmental Psychology. 2002;**22**(1-2):49-63

[76] Wilson EO. Biophilia and the conservation ethic. In: Kellert SR, Wilson EO, editors. The Biophilia Hypothesis. Washington DC: Island Press; 1993. pp. 31-41

[77] Zhang R, Zhang CQ, Rhodes RE. The pathways linking objectively-measured greenspace exposure and mental health: A systematic review of observational studies. Environmental Research. 2021;**198**:111-233. DOI: 10.1016/j. envres.2021.111233

[78] Liao J, Zhang B, Xia W, Cao Z, Zhang Y, Liang S, et al. Residential exposure to green space and early childhood neurodevelopment. Environment International. 2019;**128**:70- 76. DOI: 10.1016/j.envint.2019.03.070

[79] Andrusaityte S, Grazuleviciene R, Dedele A, Balseviciene B. The effect of residential greenness and city park visiting habits on preschool children's mental and general health in Lithuania: A cross-sectional study. International Journal of Hygiene and Environmental Health. 2020;**223**(1):142-150. DOI: 10.1016/j.ijheh.2019.09.009

[80] Cherrie MPC, Shortt NK, Mitchell RJ, Taylor AM, Redmond P, Thompson CW, et al. Pearce Green space and cognitive ageing: A retrospective life course analysis in the Lothian Birth Cohort 1936. Social Science & Medicine. 2018;**196**:56-65

[81] Terry H et al. Nature and health. Annual Review of Public Health. 2014;**35**:207-228

[82] Medeiros B. Crianças vão ao Zoo do DF e voltam para casa infestadas de carrapatos. Metrópoles, 2018. Available from: https://www.metropoles.com/ distrito-federal/criancas-vao-ao-zoo-dodf-e-voltam-para-casa-infestadas-decarrapatos

[83] Angerami RN, Silva MV, Santos FCP, et al. Febre Maculosa Brasileira: Aspectos clínicos, epidemiológicos, diagnósticos e terapêuticos. In: Meira AM, Monti JA, Ferraz KMPMB, et al. editors. Febre Maculosa: Dinâmica da Doença, Hospedeiros e Vetores. 2013. pp. 32-51. ISBN: 97885-86481-28-4.

[84] Spolidorio MG, Labruna MB, Mantovani E, Brandão PE, Richtzenhain LJ, Yoshinari NH. Novel spotted fever group rickettsiosis, Brazil. Emerging Infectious Diseases. 2010;**16**(3):521-523

[85] Fiol FSD, Junqueira FM, Rocha MCP, Toledo MI, Barberato Filho S. A febre maculosa no Brasil. Revista Panamericana de Salud Pública. 2010;**27**:461-466

[86] Ribeiro KT, Rocha GFS, Saraiva DG, Silva AP, Vilela DAR, Lima PCS, et al. Das capivaras e carrapatos a uma proposta de comunicação e manejo no Parque Nacional da Serra do Cipó para redução de riscos à saúde. Oecol Aust. 2010;**14**(3):668-685

[87] Philippe D. Jenseits von Natur und Kultur. Berlin; 2013. p. 638. DOI: 10.15463/rec.1189729441

Section 4
