The cattle tick, Rhipicephalus australis (Canestrini 1887) (Acari: Ixodidae), was introduced in New Caledonia in 1942 and the annual economic losses caused by this parasite are staggering. Locally, R. australis was synonymized with the tick formerly called Rhipicephalus microplus, until R. australis was reinstated as a separate cattle tick species in 2012 [18]. Therefore, in this study this tick is called R. australis (syn. R. microplus). This cattle farming parasite R. australis is the main tick and one of the most important in the world from an economic point of view. This tick causes large losses to ranchers [10, 51], and as being a disease vector, it reduces reproductive efficiency, meat and milk production and can produce ‘pinholes’ which reduce the hide value [7, 68]. The principal control method involves the use of synthetic acaricides by dip, spray, injection or pour-on treatments [45, 50]. The continuous use of these chemical compounds has led to the selection and development of strains of R. australis (syn. R. microplus) resistant to organophosphates, pyrethroids and formamidine, a phenomenon that is a major concern for worldwide cattle breeders [17, 33, 45]. Moreover, such chemical control causes meat and milk contamination that can also have undesirable effects on other organisms and the environment [17, 20, 31, 46].
The need of new scientific investigations for alternative ways to control this tick is related to the evolution of resistance of R. australis (syn. R. microplus) to synthetic acaricides. As a matter of fact, various studies have been developed in order to find plant extracts with acaricidal properties [4, 7, 8, 12, 17, 25, 29, 32, 36, 37, 42, 46, 68] in order to discover natural compounds at least as effective as classic treatments but also environmentally friendly and susceptible to be produced on a large, commercial scale [34].
Several studies have already been done to assess the potential acaricide activity of natural substances on R. australis (syn. R. microplus). In a first study, Borges et al. (2011) inventoried 55 plants belonging to 26 families tested against this parasite [7]. In a second review in 2016, Benelli et al. describe the results of 62 extracts on R. australis (syn. R. microplus) excluding essential oils [4]. In 2020 Quadros et al. listed 27 plants-derived substances with potential for tick control and prevention on R. australis (syn. R. microplus), including monoterpenes (e. g. α-pinene, citronellal, eucalyptol, geraniol, limonene…), spilanthol (a fatty acid amine), β-caryophyllene (a sesquiterpene), azadirachtin (a tetranotriterpenoid), allicin (an organosulfur), eugenol (a phenylpropanoid), copaifera oleoresin and digitoxin (a steroidal glycoside) [46].
In New Caledonia, several works have been devoted to the acaricidal activity of natural substances on R. australis (syn. R. microplus) larvae but mainly concerned essential oils. Lebouvier et al. [36, 37], showed that essential oils from endemic trees of New Caledonia could provide natural acaricides for the control of the cattle tick R. australis (syn. R. microplus). Nevertheless, the development of an alternative tick control strategy must be associated with a high safety profile as well as availability and remanence. Therefore, the potential toxicity of essential oils, their low extraction yield and their volatile nature reduce their valorization and application potential despite the many biological activities they may present [36, 39]. Therefore, it seems that organic solvent extracts from plants have many positive aspects for valorization in the control of cattle ticks and the Piperaceae family is a very interesting example.
Piperaceae family is represented by 5 to 13 genera and 2000 to 4000 species (depending on the taxonomical authority) and is known to have acaricidal compounds such as monoterpenes, sesquiterpenes, alkaloids and phenylpropanoids [5, 13, 14, 27, 40, 41, 44, 47, 52, 55, 69]. The genus Piper is very large, and several species of Piper have been used as spice and in traditional medicine and bear an immense commercial, economical and medicinal importance. Some Piper species have simple chemical profiles, while others, such as Piper nigrum contain very diverse suites of secondary bioactive metabolites [52]. Piper nigrum L., commonly known as black pepper, is a climber originally native to India. The acrid and pungent taste of P. nigrum fruits attracted attention of chemists as early as 1819 when Oestred isolated piperine. Since that time, search for active constituents from different Piper species is being continued and this has been intensified in recent years, particularly because of interesting biological activities of various chemicals from several Piper species [14, 23, 38, 52, 55, 59–63, 69]. Indeed, some Piper species are listed as remedies for stomach pain, asthma, bronchitis, fever, abdominal pain, haemorrhoidal afflictions, rheumatism, as anti-inflammatory and stimulant agents, but also as insect repellents, insecticidal, acaricidal, antifungal and antibiotic [19, 26, 32, 38, 49, 55, 59, 60, 61, 70]. The chemistry of Piper species has been widely investigated, and phytochemical investigations from all parts of the world have led to the isolation of several physiologically active compounds, including alkaloids, amides, propenylphenols, lignans, neolignans, terpenes, steroids, pyrones, piperolides, chalcones, flavones, and flavanones [9, 14, 26, 35, 38, 47, 53, 57, 58–63, 64, 65, 66, 69].
Several Piperaceae have also been studied against cattle ticks [8, 12, 23, 32] and their major characteristic and active constituents could be attributed to a considerable variety of amide alkaloids [3, 54, 55, 69] and to a possible synergistic action [6, 13, 42, 43, 53, 55]. Therefore, an investigation on either major or minor compounds seems to be of particular interest.
As part of our research program towards plant-based harmless bioactive compounds for agronomic purposes in New Caledonia, 200 extracts obtained from 70 plant species (from endemic, introduced or invasive species) were tested on R. australis (syn. R. microplus). The most active extracts were obtained with Piper nigrum, especially with the EtOH extracts of dried fruits as well as the EtOAc and the MeOH extracts of stems which all exhibited 100% activity on the cattle tick, as determined by the FAO modified method (LPT) [67]. The acaricidal effect of P. nigrum extracts were compared to other chemicals and natural products described in the literature. The dried mature fruits ethanolic extract showed the best extraction yield (7%) and was selected for bio-guided fractionation. The result was the isolation and structure elucidation of 5 major compounds from the bioactive fractions, including one compound described for the first time in P. nigrum, previously found in the aerial part of Piper sarmentosum [66] and 4 compounds known for P. nigrum.