In vitro acaricidal effect of tannin-rich plants against the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae)

Veterinary Parasitology 175 (2011) 113–118

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In vitro acaricidal effect of tannin-rich plants against the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) A. Fernández-Salas a,b , M.A. Alonso-Díaz a,∗ , R. Acosta-Rodríguez a , J.F.J. Torres-Acosta b , C.A. Sandoval-Castro b , R.I. Rodríguez-Vivas b a

Centro de Ense˜ nanza, Investigación y Extensión en Ganadería Tropical, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Km 5.5 Carretera Federal Tlapacoyan-Martínez de la Torre, C.P. 93600, Martínez de la Torre, Veracruz, Mexico Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km 15.5 Carretera Mérida-Xmatkuil, Mérida, Yucatán, Mexico

b

a r t i c l e

i n f o

Article history: Received 1 June 2010 Received in revised form 3 September 2010 Accepted 15 September 2010 Keywords: Rhipicephalus microplus Tannins Tropical plants Plant extracts In vitro

a b s t r a c t The objectives of this study were to evaluate the in vitro acaricidal effects of lyophilized extracts of four tannin rich plants (Acacia pennatula, Piscidia piscipula, Leucaena leucocephala and Lysiloma latisiliquum) against diverse stages of Rhipicephalus (Boophilus) microplus, and to asses whether tannins were involved in the acaricidal effect using polyethylene glycol (PEG) to block tannins. Larval immersion (LIT) and adult immersion (AIT) tests were used to evaluate the acaricidal effect of each of the lyophilized extracts against larval and adult stages of R. microplus respectively. Larvae and adult ticks were exposed to increasing concentrations of each plant extract (0, 1200, 2400, 4800, 9600 and 19,200 ␮g ml−1 ) for 10 min. Larval mortality was recorded at 48 h post-incubation. Adult mortality was recorded daily over 14 days, at which point their reproductive efficiency was evaluated. PEG was added to the extracts to verify whether tannins were involved in the acaricidal effect. The effect on egg laying inhibition and larval mortality was analyzed using the GLM procedure in SAS. A Kruskal–Wallis test was used to assess the effect of PEG on LIT results. Calculation of the lethal concentration 50 (LC50) was performed using a probit analysis. All extracts reduced the viability of R. microplus larval stages (P < 0.001), and viability was restored with the addition of PEG suggesting an important role of tannins in the acaricidal effect (P < 0.001). The LC50 values of L. latisiliquum and P. piscipula plant extracts were 6.402 and 2.466 ␮g ml−1 . None of the tannin-rich plant extracts affected adult mortality (P > 0.05). Lysiloma latisiliquum extract inhibited egg hatching of R. microplus (P < 0.01). Tannin-rich plant extracts from A. pennatula, P. piscipula, L. leucocephala and L. latisiliquum showed potential acaricidal activity. Further in vivo studies are needed to confirm this finding. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Rhipicephalus (Boophilus) microplus is the major threat to the cattle industry in tropical and subtropical areas

∗ Corresponding author. Tel.: +52 232 3243941; fax: +52 232 3243943. E-mail addresses: [email protected], [email protected] (M.A. Alonso-Díaz). 0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2010.09.016

(Dominguez-García et al., 2010). Control of R. microplus has primarily involved the frequent use of commercial chemical acaricides. However, as a consequence of their extensive use on R. microplus, the species has developed resistance to all major classes of acaricides in several countries including Mexico (Rodríguez-Vivas et al., 2006a,b; Perez-Cogollo et al., 2010). The increasing number of farms with ticks resistant to chemical acaricides in Mexico highlights the necessity of exploring alternative tick control methods.

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Natural bioactive compounds are a promising alternative for tick control (Ribeiro et al., 2007; Fernandes and Freitas, 2007). They might offer additional advantages such as low toxicity to mammals and more environmentally friendly (Batish et al., 2008; Rosado-Aguilar et al., 2010). Tropical plants and shrubs are important sources of bioactive compounds (Makkar, 2003; Alonso-Díaz et al., 2010), including tannins. These are common in tropical legumes and are an important plant defense mechanism against fungi, bacteria, and herbivorous insects (Eck et al., 2001; Heil et al., 2002). Tannin consumption had shown to be beneficial for human (Okuda, 2005) and animal health through their bactericidal (Akiyama et al., 2001; Banso and Adeyemo, 2007), antioxidant (Amarowicz et al., 2000; Smirnova et al., 2009), nematocidal (Hoste et al., 2006; Alonso-Díaz et al., 2008a,b) and insecticidal (Ayres et al., 1997; Barbehenn et al., 2009) properties. It is unknown whether these polyphenolic compounds will have acaricidal effect against different development stages of R. microplus. Hence, the objectives of this study were to evaluate the in vitro acaricidal effect of four tanninrich plant extracts (Acacia pennatula, Piscidia piscipula, Leucaena leucocephala and Lysiloma latisiliquum) against diverse developmental stages of Rhipicephalus (Boophilus) microplus, and to confirm the role of tannins in the acaricidal effect using polyethylene glycol (PEG) as a tannin blocker. 2. Materials and methods 2.1. Biological material: plant material and extraction Plant leaves were collected from the deciduous tropical forest of Yucatan, Mexico (20◦ 48 N, 89◦ 42 W) near the Faculty of Veterinary Medicine of the Universidad Autónoma de Yucatán (FMVZ-UADY). The average annual temperature varies from 26 to 27.8 ◦ C, and the annual rainfall ranges from 940 to 1100 mm (INEGI, 2002). Prior to the beginning of the trial, plants were collected and identified at the FMVZ-UADY herbarium. The extracts used in this trial were obtained from fresh leaves of the tannin-rich tropical fodder trees A. pennatula, P. piscipula, L. leucocephala and L. latisiliquum. These plant species were chosen because of their high con˜ et al., tent of condensed tannins (CT) (Monforte-Briseno 2005; Bobadilla-Hernández et al., 2007; Alonso-Díaz et al., 2008c). Extracts were obtained by chopping fresh leaves of each plant species (500 g), and placing the material in a mixer containing 1 l of acetone:water (70:30) with 1 g of ascorbic acid to avoid oxidation. The mixture was then sonicated for 20 min in a water bath (Branson 5510® ), and filter paper used to remove the solid material from the extract. The acetone was evaporated from the extract at 58 ◦ C using a Roto-Vapor (Buchii R-114® ). The aqueous solution was washed four times with 500 ml of methylene chloride to remove chlorophyll and lipids. A separation funnel was used for discarding the methylene chloride fraction. The remaining fractions were frozen and lyophilized at −20 ◦ C during 72 h. Then, each lyophilized extracts was kept refrigerated at 4 ◦ C in air-tight containers until they were used for biochemical and biological assays.

2.2. Polyphenolic compound composition of the plant extracts Quantification of extracted polyphenolic compounds was carried out by Alonso-Díaz et al. (2008a), and included total phenols (TP) (using Folin–Ciocalteu), total tannins (TT) (using Folin–Ciocalteu + PEG), condensed tannins (CT) (using the Vanillin method) and biological activity (BA) (units measured as relative precipitation per gram of extract using resorcinol as a standard). The highest levels of CT and BA were found in A. pennatula extracts (95.98 g/100 and 11.54 units respectively). L. latisiliquum and L. leucocephala extracts contained 46.91 g/100 and 7.00 units, and 45.71 g/100 and 5.80 units, respectively. The lowest values were found in the P. piscipula extract (26.07 g/100 and 5.00 units). 2.3. Ticks Four hundred engorged female ticks of R. microplus were collected from at least 30 cattle in a dual-purpose farm with recent evidence of resistance to amidines (López A.R. unpublished data, 2010). Engorged ticks were placed in Petri dishes, with the cover perforated to allow ventilation. The ticks were then transported to the Parasitology Laboratory at CEIEGT-FMVZ-UNAM. Upon arrival, engorged ticks were washed and some of them immediately used in the Adult Immersion Test. Other ticks were incubated under laboratory conditions at 27 ± 1.5 ◦ C and 70–80% relative humidity (RH) (Cen-Aguilar et al., 1998) to allow for egg laying and egg hatching. 2.4. Bioassays 2.4.1. Larval Immersion Test (LIT) The LIT was used to evaluate the effect of plant extracts against the R. microplus larval stage (Shaw, 1966). One hundred to 300 larvae were exposed to increasing concentrations of each plant using five extract dilutions (1200, 2400, 4800, 9600, and 19,200 ␮g ml−1 ) and one control (distilled water) for 10 min. After this time, larvae were transferred to filter-paper packages (Whatman No. 1), identified and sealed with “Bulldog” clips. Packages were incubated for 48 h at 27 ± 1.5 ◦ C and 70–80% RH, and dead larvae were recorded to obtain mortality. Only larvae that had the ability to walk were considered alive. Larvae without movement, ataxia, or movement only of appendages were considered dead. Three replicates were performed per treatment for each plant extract. 2.4.2. Adult Immersion Test (AIT) The acaricidal effect on engorged female ticks was evaluated using the AIT (Drummond et al., 1967). For each plant extract, 96 ticks weighing approximately 0.2–0.3 g each were used. Four groups of 8 ticks were created, for three extract dilutions (4800, 9600, and 19,200 ␮g ml−1 ) and one control (distilled water), with three repetitions each. Treated groups were immersed for 10 min in one of the extract dilutions, while the control group was immersed for 10 min in distilled water. After treatment, engorged ticks were adhered to masking tape strips in Petri dishes

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Piscidia piscipula

100

100

90

90

80

80

Mortality (%)

Mortality (%)

Acacia pennatula

70 60 50 40 30

70 60 50 40 30

20

20

10

10 0

0 19200

9600

4800

2400

1200

0

19200

9600

Doses (µg.ml-1)

90

90

80

80

70

70

60 50 40 30

1200

0

40 30 20 10

2400

0

50

10 4800

1200

60

20

9600

2400

Lysiloma latisiliquum 100

Mortality (%)

Mortality (%)

Leucaena leucocephala

19200

4800

Doses (µg.ml-1)

100

0

115

1200

0

0

19200

Doses (µg.ml-1)

9600

4800

2400

Doses (µg.ml-1)

Fig. 1. Effect of four tannin rich plant extracts on the larval mortality of Rhipicephalus microplus.

and incubated at 27 ± 1.5 ◦ C and 70–80% relative humidity (Cen-Aguilar et al., 1998) for a period of 14 days. Ticks were examined with a stereoscope and mortality counts were recorded daily. Dead ticks were identified by the presence of cuticular darkness, lack of malpighian tube movement and haemorrhagic skin lesions. The mortality was calculated using the corrected mortality formula (Abott, 1925) recommended by FAO (2004). After 15 days, the number of female ticks laying eggs was recorded and the eggs of each group were weighed using an analytical scale, after which approximately 100 eggs were placed in glass vials under the same conditions. After 21 days, the vials were observed and the hatching rates for the different treatments were estimated and compared to the controls. Egg laying inhibition (Drummond et al., 1967) and egg hatching inhibition (Rodríguez and Cob, 2005) were determined for all groups. To evaluate the effect of tannins on ticks, another series of LITs were performed using 19,200 ␮g of each plant extract/ml of distilled water with polyethylene glycol (PEG, a tannin inhibitor; Makkar, 2003) (at a dose of 38,400 ␮g ml−1 ), and without PEG (Barrau et al., 2005). Controls with distilled water were also included in the bioassay, and three replicates were performed for each treatment. 2.5. Statistical analysis The effect of larval mortality and egg laying inhibition was analyzed using the GLM procedure in SAS. Treatment effects on adult mortality and egg hatching inhibition were analyzed using a Kruskal–Wallis test (SAS, 1991).

Kruskal–Wallis test was also used to assess the effect of PEG on LIT results and Dunn test was used to verify differences amongst treatments. Calculation of the lethal concentration 50 (LC50) was performed using a probit analysis (LeOra, 2003). A value of P < 0.05 was considered significant. 3. Results 3.1. Larval mortality The four tannin-rich plants evaluated in this study showed acaricidal effects against larvae of R. microplus (P < 0.001) (Fig. 1). The mortality values for A. pennatula, P. piscipula, L. leucocephala and L. latisiliquum were 54.8%, 88.14%, 66.79% and 56.0%, respectively. The inclusion of PEG in the four tannin-rich plant extracts decreased values of tick mortality and these were similar to control values (P < 0.05), confirming the acaricidal effect of tannins on R. microplus larvae (Fig. 3). 3.2. Adult mortality and inhibition of egg laying and egg hatching The four plant extracts showed no acaricidal effect on adult stages of R. microplus (P > 0.05). The plant extracts did not show any significant effect on egg laying inhibition (Table 1). However, adult ticks treated with L. latisiliquum extract showed egg hatching inhibitions of 43.05%, 43.51%, and 69.34% at 4800, 9600, and 19,200 ␮g ml−1 respectively (P < 0.05) (Table 1).

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Fig. 2. Dose–effect relationship against the larval stage of Lysiloma latisiliquum and Piscidia piscipula.

Table 1 Effect of four plant extracts on egg laying inhibition (%ELI) and egg hatching inhibition (%EHI) of Rhipicephalus microplus. A. pennatula

P. piscipula

%ELI

%EHI

a

Control 4800 ␮g ml−1 9600 ␮g ml−1 19,200 ␮g ml−1

%ELI

a

0 11.3a 9.3a 8.4a

a

0 38.00a 39.00a 35.00a

0 11.0a 19.8a 15.7a

L. leucocephala %EHI a

0 27.49a 31.47a 39.21a

%ELI a

0 1.8a 3.4a 7.3a

L. latisiliquum %EHI a

0 32.14a 19.72a 29.00a

%ELI a

0 23.2a 20.0a 36.4a

%EHI 0a 43.05b 43.51b 69.34b

Different literal between rows indicate difference statistically significant (P < 0.05).

3.3. Lethal concentration 50 (LC50)

4. Discussion

Lysiloma latisiliquum and P. piscipula had the strongest dose–effect relationship against larvae of R. microplus (P < 0.001) (Fig. 2). The LC50 values of these plant extracts were 6.402 and 2.466 ␮g ml−1 respectively. The calculation of LC50 was not possible for A. pennatula and L. leucocephala extracts.

The objectives of this study were to determine whether tropical tannin-rich plant extracts affected the biology of different stages of R. microplus and whether tannins were involved in the acaricidal effect. The four tannin-rich plant extracts had acaricidal effects against larvae of R. microplus. Indeed, L. latisiliquum and P. piscipula, the extracts with moderate levels of tannins and biological activity, showed dose-dependent acaricidal effects. The LC50 values of these plants extracts were 6.402 and 2.466 ␮g ml−1 respectively, showing that mortality is linked with the dose applied (Fig. 2). To our knowledge there are no published studies on the acaricidal effect of tannin-rich plants against R. microplus, but the results might be comparable with those obtained using medicinal plants. Zahir et al. (2009) reported the effect of extracts prepared from leaves of Psidium guajava and Solannum trilobatum. They showed 62–76% and 65–74% mortality, respectively (at 2 mg ml−1 ), against larvae of R. microplus. Ribeiro et al. (2007) reported 100, 96.7, 84.7 and 52.7% mortality of R. microplus larvae using crude methanolic extracts of Hypericum polyanthemun at concentrations of 50, 25, 12.5 and 6.25 mg ml−1 , respectively, while Silva et al. (2009) reported 70.42% mortality for R. microplus larvae exposed to 200 mg ml−1 of hexane extract from Piper aduncum. In contrast, some extracts from medicinal plants have higher toxicity for R. microplus larvae (>95%). Oleoresin extracted from Copaifera

Plant extracts with and without tannins C= control

30

Mortality (%)

25

T= treatment

T + PEG= Treatment/PEG L. latisiliquum

A. pennatula

20

P. piscipula

L. leucocephala b

b

b

b

15 10 5 0

a C

T T

+

a

a

G PE

C

T T

+

a

a

G PE

C

T T

+

a

a

G PE

C

a T T

+

G PE

Fig. 3. Effect of four tannin rich plant extracts on the larval mortality of Rhipicephalus microplus, tannin rich extract and the tannin blocker (PEG) and control group. Different literal between bars, indicate difference statistically significant (P < 0.05).

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reticulate produced 99% larval mortality in R. microplus at concentrations of 3.49 mg ml−1 (Fernandes and Freitas, 2007). Moreover, Rosado-Aguilar et al. (2010) reported 99% larval mortality using methanolic extracts of leaves and stems of Petiveria allicea at 122 mg ml−1 and 165 mg ml−1 , respectively. Although, in vitro studies on medicinal plants often use different concentrations of extracts (varying from ␮g ml−1 to mg ml−1 ), our results show toxic effects against R. microplus larvae with low doses of extracts; hence, the tannin-rich plant extracts used are a promising alternative for the control of ticks. Several studies exist where the acaricidal properties of plant extracts against R. microplus have been attributed to terpenoids (Pereira and Famadas, 2006; Fernandes and Freitas, 2007; Ribeiro et al., 2007, 2010; Magadum et al., 2009). To our knowledge, this is the first study where tannin participation in acaricidal effects from tannin-rich plant extracts was confirmed by using a specific blocker. Tannin specific inhibitors (i.e. PEG) have been used to evaluate tannin biological activity in tropical browse forages (Makkar et al., 1995). It is known that PEG is also able to bind and inactivate tannins and flavonol glycosides. In our study, the restoration of mortality percentages to values similar to controls after PEG addition indicates that tannins from the plant extracts were involved in the acaricidal effect against R. microplus. The biological activity of tannins have been related to medicinal properties of plant extracts against gastrointestinal nematodes in small ruminants (Hoste et al., 2006; Alonso-Díaz et al., 2008a,b), but it was unknown whether those compounds had any acaricidal properties. Therefore, our study might help to stimulate future investigations using tannin-rich plants as a new option for the control of ticks, especially R. microplus. The population-limiting property of any plant extract is an important step in assessing the efficacy of extracts on R. microplus (Magadum et al., 2009). In our study, an L. latisiliquum extract at 19,200 ␮g ml−1 reduced the egg laying capacity of ticks by 36.4% (P = 0.05) and inhibited egg hatching by 69.34% (P < 0.01). These results are consistent with previous reports using R. microplus as a model. Silva et al. (2009) reported 35.02–46.78% of inhibition of oviposition for engorged females exposed to 100 mg ml−1 of different leaf extracts from Piper aduncum. Crude extracts from Petiveria alliacea leaves evaluated against engorged females showed an egg laying inhibition of 40.1% and egg hatching inhibition of 21.3% at 200 mg ml−1 concentrations (Rosado-Aguilar et al., 2010). The efficacy of any alternative methods for the control of R. microplus will be improved if it can adversely affect several steps in the biology of the targeted parasite. In the present study, the L. latisiliquum extract showed an inhibitory effect on egg hatching, and the higher efficacy of the extracts against larval stages demonstrates the potential use of these plants as sources of biopesticides and as economic and sustainable alternatives to commercial forms. Increasing extract doses may improve results. Tannin-rich plant extracts from A. pennatula, P. piscipula, L. leucocephala and L. latisiliquum showed potential as acaricides due to their significant effect on larval mortality. The L. latisiliquum extract also showed an inhibitory effect on egg hatching. These compounds can be considered

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as possible candidates for the alternative control of ticks, thus reducing dependence on commercial acaricides, but it is necessary to further evaluate their acaricidal activity under in vivo conditions. Conflict of interest statement The authors of this manuscript have no financial or personal relationships with other people or organizations that could inappropriately influence or bias the content of the paper. References Abott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265–267. Akiyama, H., Fujii, K., Yamasaki, O., Oono, T., Iwatsuki, K., 2001. Antibacterial action of several tannins against Staphylococcus aureus. J. Antimicrob. Chemother. 48, 487–491. Alonso-Díaz, M.A., Torres-Acosta, J.F.J., Sandoval-Castro, C.A., AguilarCaballero, A.J., Hoste, H., 2008a. In vitro larval migration and kinetics of exsheathment of Haemonchus contortus larvae exposed to four tropical tanniniferous plant extracts. Vet. Parasitol. 153, 313–319. Alonso-Díaz, M.A., Torres-Acosta, J.F.J., Sandoval-Castro, C.A., CapetilloLeal, C.M., Brunet, S., Hoste, H., 2008b. Effects of four tropical tanniniferous plant extracts on the inhibition of larval migration and the exsheathment process of Trichostrongylus colubriformis infective stage. Vet. Parasitol. 153, 187–192. Alonso-Díaz, M.A., Torres-Acosta, J.F.J., Sandoval-Castro, C.A., Hoste, H., Aguilar-Caballero, A.J., Capetillo-Leal, C.M., 2008c. Is goats’ preference for forage trees affected by their tannin or fibre content when offered in cafeteria experiments? Anim. Feed Sci. Technol. 141, 36–48. Alonso-Díaz, M.A., Torres-Acosta, J.F.J., Sandoval-Castro, C.A., Hoste, H., 2010. Tannins in tropical tree fodders fed to small ruminants: a friendly foe? Small Rumin. Res. 89, 164–173. Amarowicz, R., Naczk, M., Shahini, F., 2000. Antioxidant activity of crude tannins of canola and rapeseed hulls. J. Am. Oil Chem. Soc. 77, 957–961. Ayres, M.P., Clausen, T.P., MacLean, S.F., Redman, A.M., Reichardt, P.B., 1997. Diversity of structure and anti-herbivore activity in condensed tannins. Ecology 78, 1696–1712. Banso, A., Adeyemo, S.O., 2007. Evaluation of antibacterial properties of tannins isolated from Dichrostachys cinerea. Afr. J. Biotechnol. 15, 1785–1787. Barbehenn, R.V., Jaros, A., Lee, G., Mozola, C., Weir, Q., Salminen, J.P., 2009. Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. Vet. Parasitol. 55, 297–304. Barrau, E., Fabre, N., Fouraste, I., Hoste, H., 2005. Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glycosides. Parasitology 131, 531–538. Batish, D.R., Singh, H.P., Kohli, R.K., Kaur, S., 2008. Eucalyptus essential oil as a natural pesticide. Forest Ecol. Manage. 256, 2166–2174. Bobadilla-Hernández, A.R., Ramírez-Avilés, L., Sandoval-Castro, C.A., 2007. Effect of supplementing tree foliage to grazing dual-purpose cows on milk composition and yield. J. Anim. Vet. Adv. 6, 1042–1046. Cen-Aguilar, J.F., Rodríguez-Vivas, R.I., Domínguez-Alpizar, J.L., Wagner, G.G., 1998. Studies on the effect on infection by Babesia sp on oviposition of Boophilus microplus engorged females naturally infected in the Mexican tropics. Vet. Parasitol. 78, 253–257. Dominguez-García, D., Rosario-Cruz, R., García, C., Oaxaca, J., De la Fuente, J., 2010. Boophilus microplus: aspectos biológicos y moleculares de la resistencia a los acaricidas y su impacto en la salud animal. Trop. Subtrop. Agroecosyst. 12, 181–192. Drummond, R.O., Graham, O.H., Ernest, S.E., 1967. Evaluation of insecticides for the control of B. annulatus (Say) and B. microplus (Canestrini) (Acari: Ixodidae) on cattle. In: II International Congress on Acarology, pp. 493–498. Eck, G., Fiala, B., Linsenmair, K.E., bin Hashim, R., Proksch, P., 2001. Trade-off between chemical and biotic anti-herbivore defense in the South East Asian plant genus Macaranga. J. Chem. Ecol. 10, 1979– 1996. Food and Agriculture Organization of the United Nations (FAO), 2004. Resistance Management and Integrated Parasites Control in Ruminants/Guidelines, Module 1-Ticks: Acaricide Resistance, Diagnosis,

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