Organic parasite control for poultry and rabbits in British Columbia, Canada

Plants used for treating endo- and ectoparasites of rabbits and poultry in British Columbia included Arctium lappa (burdock), Artemisia sp. (wormwood), Chenopodium album (lambsquarters) and C. ambrosioides (epazote), Cirsium arvense (Canada thistle), Juniperus spp. (juniper), Mentha piperita (peppermint), Nicotiana sp. (tobacco), Papaver somniferum (opium poppy), Rubus spp. (blackberry and raspberry relatives), Symphytum officinale (comfrey), Taraxacum officinale (common dandelion), Thuja plicata (western redcedar) and Urtica dioica (stinging nettle).


Introduction
Consumers, butchers and restaurant-owners are increasingly demanding that meat animals be reared in environmentally-sensitive ways that also take animal welfare concerns into consideration (e.g. access to pasture); these organic farming management practices also improve meat quality [1][2][3][4][5]. The meat from poultry and rabbits is more efficient to produce in terms of land use, feed and water use than beef and pork and thus produces a lower environmental impact [6][7][8][9][10]. Some consumers are also concerned about chemical residues (like flubendazole) in meat [11,12]. The access to pasture demanded by animal welfare agents increases the need for parasite control in food animals [11,13]. Organic agriculture allows a restricted number of substances to be used for pest control.
Some conventional livestock farmers add subclinical levels of antibiotics to the animal feed of millions of food animals as growth promoters [14]. Some of these antibiotics are not absorbed and are excreted in manure which is then applied as a fertilizer to food crops. As much as 387 g of chlortetracycline and 202 g of tylosin per hectare is estimated to be added to the soil with the application of pig manure. Greenhouse studies conducted on corn (Zea mays L.), green onion (Allium cepa L.), and cabbage (Brassica oleracea L. Capitata group) showed that all three crops absorbed chlortetracycline from pig manure but tylosin was not absorbed [14]. Botanical and mineral products used for animal health are less likely to become soil contaminants than chlortetracycline since they are natural products.

Ethnoveterinary research
Ethnoveterinary medicinal research is often undertaken as part of a community-based approach that serves to improve animal health and provide basic veterinary services in underserved areas [17]. This paper reports on research that documented and validated (in a nonexperimental way) ethnoveterinary medicines used for parasite control by small-scale, organic livestock rabbit and poultry farmers in British Columbia (B.C.), Canada.

Organic rabbit and poultry production
Most rabbits are raised on farms for home consumption or for the pet industry. In 2001 over 17,000 rabbits on 264 farms were reported; this figure represented a 14% decline in the number of rabbits and a 71% decline in the number of farms with rabbits [18]. There were no certified organic rabbit producers in British Columbia and only two in Canada [19,20].
In the case of poultry, organic egg production represented less than 2 percent of all egg production in B.C. and less than half of 1 percent across Canada [21]. Small-scale farmers produce 100,000 chickens annually. Flocks containing less than 99 layers, or 199 broilers, are not covered by the provincial quota and are not regulated by the provincial Egg or Chicken Marketing Boards.
There are three categories of specialty chicken regulated by the Provincial Marketing Boards. These categories contain 3.6% of the total permit allocation for all chicken production in B.C. (1,085,005 kg live weight) [22]. There were 19 farmers in the specially-fed/housed chicken category, holding half of the allocated permits; 16 of the 19 farmers were located in the Lower Mainland area of B.C. This specially-fed/housed category includes vegetable-fed chickens, chickens raised with no or limited antibiotic use, and chickens classified as organic, certified organic, natural, range fed, SPCA certified, Cornish and roasters [22]. There were also 19 small-scale farmers in the farm gate category, and 20 Lower Mainland farmers in a third category who raised Asian specialty chickens (e.g. Silkies, Taiwanese). The annual economic value of the specialty chicken industry was estimated at $18.0 million dollars, or 7.7% of the entire economic value of all chicken production in B.C. ($232.7 million in 2002); 54.9% of the value of broiler hatching egg production of $32.8 million and 20% of the economic value of egg production of $90 million [22].

Data collection
Ethnoveterinary data for British Columbia was collected for a wide range of animals who were under the care of farmers, veterinarians and animal care specialists over a six-month period in 2003. All of the available literature about livestock farmers and the secondary literature on ethnomedicinal plants, folk medicine and related fields in British Columbia was reviewed [23,24]. The research area included south Vancouver Island, the Lower Mainland, and the Thompson/Okanagan region of the Interior. A purposive sample of livestock farmers was used to find 60 key informants. Participants were identified from membership lists of organic farmers, horse and dog breeders and trainers, horse stables, sheep, cattle and goat breeders, naturopaths, farm women's networks, meat processors, holistic veterinarians and other specialists in alternative medicine for animals. Ten farmers (nine poultry and one rabbit farmer), and three herbalists provided the data presented here on plants used for poultry and rabbit parasite control. The participating poultry farmers were either organic (commercial operations) or farm-gate producers, including one also raising Asian specialty chickens.
Two visits were made to each farm or respondent, with interviews conducted on the first visit to identify the ethnoveterinary remedies known to and/or used by the individual. The data form was revised on campus and then posted to the relevant address and followed up with a phone interview or a second visit to re-confirm the accuracy of the data (Figure 1). During the second visit, the data recorded and summarized from the initial interview was checked and elaborated on, in order to establish that dosages were accurately noted, for input on content, and to clarify any points. The respondentapproved data forms were compiled into a draft manual.
Where possible, voucher specimens of plants established as remedies were collected by two student ethnobotanists and two herbalists, identified, processed and labelled, then deposited in the University of Victoria herbarium.
The plant-based remedies were evaluated for safety and efficacy with a non-experimental method, prior to including them in the final version of the manual. Published sources such as journal articles, books, and databases on pharmacology and ethnomedicine available on the Internet were searched to identify the plants' known chemical compounds and clinically tested physiological effects. This data was incorporated with data on the reported folk uses of the plants, and their preparation and administration in North America and Europe. For each species or genus the ethnomedicinal uses in other countries was noted, followed by a summary of chemical constituents, as well as any known active compounds. This type of ethnopharmacological review and evaluation is based on previous work [25]. The non-experimental validation of the plants is provided in the discussion section of this paper.

Validation workshop
The International Institute of Rural Reconstruction (IIRR) developed the workshop method used in this research [26]. The workshop process results in the selection of ethnoveterinary practices and remedies that can be effectively recommended for use by the general public and farmers to alleviate minor diseases and problems in domesticated animals.
Ten participants with experience in traditional human and ethnoveterinary medicine took part in a participatory five-day-long workshop hosted by the first author and a German ethnoveterinary consultant (Dr. Evelyn Mathias) in October 2003. Two editorial assistants/facilitators also participated. The facilitators asked participants very specific questions about the medicinal plants used [26]. Each animal/livestock species was covered in a morning or afternoon session. At the poultry session there were three farmer participants and one herbalist, who were already acquainted with the participatory workshop method from the previously-held ruminant workshop. They reviewed collectively the previously prepared draft manual on poultry and rabbits that was in turn based on the earlier oneon-one interviews. Guided by the discussions, the poultry and rabbit data was further clarified, edited and included in the user-friendly manual with the information on other livestock species [27] (Figure 2). There was no separate discussion for rabbits.

Results
Nineteen plants from 12 plant families were documented as used for poultry parasite control, and 11 plants from eight families were used for parasite control in rabbits ( Table 1). Most of these plant species are introduced weeds or kitchen herbs. Some details of how preparations were made are outlined below.

Leg mites (Cnemidocoptes mutans)
One cup [250 mL] of cooking oil (e.g. canola or dregs of olive oil) was mixed with a few tbsp [~50 mL] of sulphur powder and diatomaceous earth. After stirring well this mixture was rubbed on the birds' legs, or their legs were dipped in the mixture. This procedure was used to suffocate mites.

Internal parasites in poultry
Poultry were given access to growing epazote (Chenopodium ambrosioides L.) so that they could nibble it. Alternatively handfuls of epazote were thrown to the chickens while they were stilled penned if ample quantities were available. Lambsquarters (Chenopodium album L.) was used as an alternative to epazote and both plants are also considered very nutritious food for poultry. Mugwort (Artemisia vulgaris L.) was grown in the fields or pathways of the farm so that birds could self-medicate. Birds were also allowed to self-medicate with the following herbs: burdock (Arctium lappa L.), comfrey (Symphytum officinale L.), dandelions (Taraxacum officinale Weber), peppermint (Mentha piperita L.), wild Canada thistle (Cirsium arvense (L.) Scop), stinging nettle (Urtica dioica L.), and salmonberry shoots and leaves (Rubus spectabilis Pursh).

Caecal/cecal worms (Heterakis gallinarum) and blackhead disease (Histomonas meleagridis)
A handful of crumbled dry leaves of wild tobacco (Nicotiana rustica L.) (grown on the farm) was added to 1 bucket of feed. Alternatively a strong decoction was made by filling a canning kettle with the leaves of the wild tobacco and then pouring water into the kettle until full. The kettle was simmered for a few days until the mixture was reduced to one-fourth of the original amount. One cup (250 mL) of the resulting decoction was diluted with 1 gallon of water [ca. 5 L] and given as the drinking water to the flock. Five gallons of water (with 5 cups [about 1 L] of the decoction diluted in it) was said to last for five days (depending on the number of birds in the flock).

Discussion and Conclusion
The non-experimental validation of the plants is presented in Table 2, in alphabetical order of the plants' scientific names. Table 2 also contains the references numbered 28 -68.
Sulphur is not toxic to mammals and is allowed in pest control in organic agriculture (see http://www.scotland.gov.uk/Publications/2005/05/13153740/37541). Chenopodium ambrosioides is one of the plants that are allowed for pest control [70]. Similarly, farm-grown tobacco is allowed for pest control on organic livestock farms even though the nicotine affects acetylcholine receptors in the nervous system [71,72]. A recent study showed that tobacco bio-oil blocked the growth of the bacteria Streptomyces scabies and Clavibacter michiganensis and the fungus Pythium ultimum (all crop pests). The tobacco bio-oil also killed Colorado potato beetles [73]. Some of the plants used to treat poultry and rabbits are also used to treat pets and pigs in British Columbia. Juniper species oil and Thuja plicata Donn ex D. Don have been previously reported as flea treatments for pets. Juniper berries were used to treat stomach problems in pets [25,74]. Mugwort (Artemisia vulgaris L.) used to treat endoparasites in poultry and pigs; was reported for fly control of pets [74]. Echinacea leaves were used for disease prevention in chicks while Echinacea roots were used to treat microbial infections in pigs [25]. Peppermint (Mentha piperita L.) whole plant was used against endoparasites in poultry while the oil was used for stomach problems in pets. Slippery

Medicinal plant Validation information Reference
Acer macrophyllum Big-leaf maple leaves were used as bedding for poultry & rabbits, but not specifically to control parasites in the litter. The fallen, dried leaves were raked up in the autumn, and were then stored for use over the year. The leaf litter has more Ca, K, Mg, molybdenum (Mo), and zinc (Zn) than other trees. The litter decomposes quickly and has a high pH. The leaves contain tannins. [28,29] Ascophyllum nodosum Norwegian sea kelp (Ascophyllum nodosum) was used as a starter ration for chicks that prevented disease. This species, given as a supplement (2% DM) for two weeks prior to slaughter to feedlot steers and heifers (Bos indicus x Bos taurus) decreased the prevalence of enterohemorrhagic Escherichia coli and it may prevent increases in Salmonella species. Supplementation of Ascophyllum nodosum to a diet of fescue hay enhanced immune function in lambs and protected against prolonged heat-induced oxidative stress. The vitamin content of Ascophyllum nodosum is highest in September and February at 500 mg/kg dry matter. The plant has summer antimicrobial activity but none in spring or winter. Maximal calorific values occur in July in the period of maximum growth.
[ [33][34][35] Artemisia vulgaris Mugwort whole plant was used to treat endoparasites in poultry. 300 mg/kg doses of methanol extracts of the aerial parts of A. vulgaris and A. absinthium were found to reduce the larval form of Trichinella spiralis in rats. Artemisia scoparia flowers and Artemisia pallens essential oil have shown anthelmintic activity. This use is traditional and was part of a compound remedy used to rid the human body of Taenia with Senna, Spigelia marilandica or Artemisia santonica together with pumpkin seeds and slippery elm bark.
[ [36][37][38] Chenopodium album and Chenopodium ambrosioides Lamb's quarters and epazote whole plants were used for endoparasites in poultry. Chenopodium album possesses anthelmintic activity in vitro and in vivo against mature Haemonchus contortus and its eggs and was slightly less effective than Levamisole. The traditional infusion of Chenopodium ambrosioides used as a vermifuge is safer than using the herb's essential oil. [39,40] Cirsium arvense Wild Canada thistle whole plant was used for endoparasites in poultry. This plant contains lignin, callose and silicon. Taraxasterol has moderate anti-inflammatory activity. Tricin-5-0-glucoside, Quercetin-3-O-rhamnoglucoside, Quercetin-3-O-digalactoside, cirsimaritin, pectolinaringen are also found. Some of these compounds have antimicrobial activity [41][42][43][44][45] Echinacea purpurea An Echinacea product (containing Echinacea purpurea (L.) Moench 20,000 mg/40 grams) was added to chicks' feed, or, alternatively, Echinacea leaves were chopped and fed to chicks. Echinacea enhances immune function in rats by increasing antigen-specific immunoglobulin production. Streptococcus pyogenes, Hemophilus influenzae and Legionella pneumophila were inactivated by Echinacea. Echinacea aerial and root ethanol extract also reversed the pro-inflammatory responses of Staphylococcus aureus (methicillin-resistant and sensitive strains) and Mycobacterium smegmatis but had a lesser bactericidal effect. [46,47] Fucus vesiculosus Kelp meal was added to the chicks' feed bins every two weeks: 2 cups (about 500 ml) for 300 young birds. Soluble fractions of the marine alga Fucus vesiculosus (42.3% yield) are composed of neutral sugars (18.9-48 g/100 g), uronic acids (8.8-52.8 g/100 g), sulfate (2.4-11.5 g/100 g), small amounts of protein (< 1-6.1 g/100 g), and nondialyzable polyphenols (0.1-2.7 g/100 g). The main neutral sugars were fucose, glucose, galactose, and xylose. Sulfated polysaccharides may be natural antioxidants. [48] Galium aparine Cleavers fresh or dried leaves and stems were used for diarrhoea in poultry. This plant has traditionally been used for stomach conditions in North America. The insect antifeedant anthraquinone aldehyde nordamnacanthal (1,3-dihydroxy-anthraquinone-2-al) is found in Galium aparine. [35,49,50] Juniperus sp. (Dermanyssus gallinae) red bird mites in poultry were prevented with cedar shavings in the bedding. The antimycobacterial activity of Juniperus communis roots and aerial parts was attributed to a sesquiterpene (longifolene) and two diterpenes (totarol and trans-communic acid). Transcommunic acid was not a stable compound in this experiment. Juniper leaf essential oil had some effectiveness against Dermanyssus gallinae at 0.14 mg oil/cm(3).
[ 51,52] Mentha piperita Peppermint whole plant was used against endoparasites in poultry. Peppermint oil has larvicidal activity against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus mosquitoes. Methanolic, dichloromethane and hexanic extracts of Mentha × piperita had activity against Giardia lamblia but an infusion did not.
[ [53][54][55] Nicotiana rustica A handful of the chopped stems, seed pods and leaves of wild tobacco (Nicotiana rustica L.) (grown on the farm) was added to the bedding in nest boxes to reduce external parasites. Wild tobacco (handful of crumbled dry leaves or decoction) was used for endoparasites in poultry; the chopped dried stems were used for red bird mites. Anthelmintic activity was found in Nicotiana tabacum. Nicotine was used as an insecticide in the past. [56] Lans and Turner Journal of Ethnobiology and Ethnomedicine 2011, 7:21 http://www.ethnobiomed.com/content/7/1/21 elm (Ulmus fulva Muhl.) was fed to chicks for disease prevention and used for stomach problems in pets [25,74]. Table 2 shows that the anti-parasitic and dietary uses of Arctium lappa L., Artemisia sp., Ascophyllum nodosum (L.) Le Jolis, Chenopodium ambrosioides L., Cirsium arvense (L.) Scop., Fucus vesiculosus L., Galium aparine L., Mentha piperita, Nicotiana sp., Papaver somniferum L., Rubus spp., Symphytum officinale L., Taraxacum officinale Weber, Thuja plicata Donn ex D. Don, Ulmus fulva L. and Urtica dioica L. are supported by ancient and current scientific studies and reports. For example the essential oils from various plants have shown toxicity to different insect pests. Artemisia judaica L., inhibits the normal feeding activity of the cotton leafworm (Spodoptera littoralis), Juniperus occidentalis Hook, has activity against adult mosquitoes (A. aegypti), Xenopsylla cheopis (rat flea) and Ixodes scapularis (tick). Chenopodium ambrosioides L., has activity against Planococcus citri (citrus mealybug) and western flower thrips (Frankliniella occidentalis) [71].

Papaver somniferum
Farmers in our study used leaves and plants of opium poppy (Papaver somniferum) to treat diarrhoea in their poultry. This implies using the side effects of pain treatment with opioids: hard dry stools and increased gastroesophageal reflux. Activation of mu-opioid receptors by opoids in the gastrointestinal tract is responsible for inhibition of gut motility. [57] Rubus spectabilis Salmonberry whole plant is eaten by poultry and said to control endoparasites. This is possibly based on traditional knowledge since Rubus trivialis was given for scours in sheep and Rubus strigosus infusion was recommended for diarrhoea. Rubus species berries contain bioactive flavonoids, including anthocyanins and proanthocyanidins that promote health. [35,58,59] Symphytum officinale Comfrey fed fresh or dried leaves were used for diarrhoea and endoparasites in poultry. The plant is mucilaginous and high in protein. Self-medicating birds apparently did not ingest enough pyrrolizidine alkaloids to be harmed and the content of these alkaloids varies from plant to plant. [60,61] Taraxacum officinale Common dandelion (Taraxacum officinale) was used by the participants in our study to treat endoparasites in poultry, and as food for both poultry and rabbits. Taraxacum officinale pretreatment (aqueous decoction of dried herb -10 mg/kg) can reduce the severity of cholecystokinin (CCK)-octapeptide-induced pancreatitis in rats. This plant use is traditional. Many studies conducted on dandelion extracts or its constituents (polyphenolics and sesquiterpenes) from the leaves or roots have shown anti-inflammatory and other activities.
[ [62][63][64] Thuja plicata Western red-cedar shavings were used to protect poultry against red bird mites. Thuja occidentalis was tested and found to have some effectiveness against the poultry red mite Dermanyssus gallinae. [65] Thuja plicata Methanol extracts of western red cedar (commonly used for animal bedding) were tested for antimicrobial activity against anaerobic bacteria and yeast. The test microbes included Fusobacterium necrophorum, Clostridium perfringens, Actinomyces bovis and Candida albicans which are found in foot diseases and other infections in animals; the results were not significant. Betathujaplicin is a tropolone-related compound purified from the wood of Thuja plicata. All Staphylococcus aureus isolates were inhibited by beta-thujaplicin with MICs of 1.56-3.13 mg/L. However, a paradoxical zone phenomenon occurred, with each isolate producing regrowth at higher beta-thujaplicin concentrations. [66,67] Ulmus fulva Slippery elm bark powder is put in the feed for the first two weeks for disease prevention chicks. This use is traditional. [35,68] Urtica dioica Urtica dioica was used for endoparasites in poultry in our study. A leaf infusion of Urtica dioica L.
(2.5 g dry plant leaves infused in 1 L boiled water) protected rats that were given the chemical carcinogen trichloroacetic acid. [69] Lans and Turner Journal of Ethnobiology and Ethnomedicine 2011, 7:21 http://www.ethnobiomed.com/content/7/1/21 Botanical compound studies on livestock pests have also been conducted (see Table 2). Thuja occidentalis L. arborvitae and Juniper spp. (Juniperus) leaf essential oils were found to be effective against the poultry red mite Dermanyssus gallinae [53,65]; therefore adding these plants to poultry bedding could be recommended. Mentha longifolia auct. non (L.) Huds. (synonym Mentha spicta L.) ethanol and water extracts had 67.1 and 63.1% efficacy respectively against naturally acquired pinworms (Syphacia obvelata) in mice suggesting the usefulness of certain mint species for endoparasite control [78]. Chenopodium ambrosioides L., has a long history of use against endoparasites. Mice infected with Schistosoma mansoni cercariae were given Chenopodium ambrosioides L., methanol extracts at high concentrations (750 and 1000 ppm) and the extracts diminished the cercarial infectivity of the mice [79]. The hexane extract of C. ambrosioides L., showed anthelmintic activity in vitro and a reduction of the inflammatory reaction produced by the infection of Toxocara canis larvae in vivo in mice and showed no toxicity [80].
The use of opium poppy (Papaver somniferum L.) for diarrhoea in poultry was based on its opiate activity; opoids would alleviate diarrhoea by hardening the stools [57].
Kelp was fed to chicks and this practice may improve the food safety of organic poultry. The use of kelp is supported by one study which found that Norwegian sea kelp (Ascophyllum nodosum (L.) Le Jolis) given as a supplement (2% DM) for two weeks prior to slaughter to feedlot animals (Bos indicus x Bos taurus) decreased the prevalence of enterohemorrhagic Escherichia coli and it may prove effective in controlling the spread of Salmonella species [30].