Science of the Total Environment 639 (2018) 921–928

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Science of the Total Environment

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Transference of bioactive compounds from support plants to the termites

Constrictotermes cyphergaster (Isoptera)
Iamara Silva Policarpo a, Alexandre Vasconcellos a, Thiago Pereira Chaves b, Joanda Paolla Raimundo c,
Ana Cláudia D. Medeiros d, Henrique D.M. Coutinho e,⁎, Rômulo Romeu Nóbrega Alves f
a
Departamento de Sistemática e Ecologia, CCEN, Universidade Federal da Paraíba, Laboratório de Termitologia, 58051-900 João Pessoa, PB, Brazil
b
Universidade Federal do Piauí, Campus Professora Cinobelina Elvas, Bom Jesus, PI 64900-000, Brazil
c
Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual da Paraíba, Campina Grande, Paraíba 58.429-500, Brazil
d
Laboratório de Desenvolvimento e Ensaios de Medicamentos, Centro de Ciências Biológicas e da Saúde, Universidade Estadual da Paraíba, Campina Grande, Paraíba 58.429-500, Brazil
e
Laboratório de Microbiologia e Biologia Molecular, Universidade Regional do Cariri, Crato, CE 63105-000, Brazil
f
Departamento de Biologia, Universidade Estadual da Paraíba, Laboratório de Termitologia, 58051-900 João Pessoa, PB, Brazil

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• The use of animals for the treatment of

different human diseases is common in
traditional medicine.
• Termites are among the species most
commonly used in folk medicine.
• Potential microbiological activities of
termites may be associated with their
relationships with plants.
• The antimicrobial potential of ethanol
extracts of the bark of supporting plants
is higher than the antimicrobial poten-
tial of the termite C. cyphergaster ex-
tracts;
• The combination of the extracts of
C. cyphergaster and its nests with antibi-
otics produces a strong synergistic
activity.

a r t i c l e i n f o a b s t r a c t

Article history: This study aims to investigate the microbiological potential of the termite species Constrictotermes cyphergaster
Received 3 February 2018 (Silvestri, 1901) and its support plants. We collected five C. cyphergaster nests from three different support plant spe-
Received in revised form 14 May 2018 cies. Microbiological assays were performed on these extracts using the serial microdilution method in triplicate to
Accepted 14 May 2018
measure the minimum inhibitory concentration (MIC) of each microorganism for the analysed extract. The ethanol ex-
Available online xxxx
tracts of the termite C. cyphergaster showed no significant activity against strains of Staphylococcus aureus and
Keywords:
Escherichia coli, with an MIC N1000 μg mL-1. Only the extracts of the nests and termites with the nest had the same
Traditional medicine MICs. These results were in contrast to the extracts of Spondias tuberosa (Umbuzeiro), Poincianella pyramidalis
Termites (Catingueira), and Amburana cearensis (Cumaru), which demonstrated significant activity against S. aureus with
Medicinal plants MICs b1000 μg mL-1. The modulating activity of the extracts tested in the present study demonstrated potentiation
Bioprospecting of most antibiotics across the bacterial strains tested when combined with the extracts for both S. aureus and E. coli.
Semiarid These results indicate that the extracts tested in the present study may be composed of animal and vegetable origins
with the potential to modify the activity of antibiotics and thus may aid in antimicrobial therapy.
© 2018 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Universidade Regional do Cariri, Urca, Rua Cel. Antonio Luis 1161, Pimenta, 63105-000, Brazil.
E-mail address: hdmcoutinho@gmail.com (H.D.M. Coutinho).

https://doi.org/10.1016/j.scitotenv.2018.05.173
0048-9697/© 2018 Elsevier B.V. All rights reserved.
922 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928
1. Introduction
Biodiversity is an invaluable source of information and bioactive
chemicals that support human health (Chivian, 2002). Plants and ani-
mals have been documented in several geographical regions (WHO,
2002; Ferreira et al., 2012; Alves and Rosa, 2013; Van Vliet et al., 2017;
Hajdari et al., 2018) as sources of remedies in traditional medicine
worldwide. Although plants and their derivatives constitute most of
the products used in traditional medicine, whole animals or their
parts and animal sub-products are also important constituents of
materia medica in different human societies (Marques, 1995; Alves
and Rosa, 2013).
Among the invertebrates, insects have played an important role as
sources of therapeutic products in traditional medicine (Costa Neto,
2005; Costa Neto et al., 2006; Dossey, 2010). Insects and the products
derived from them have been used by human cultures for medicinal
purposes in different geographical regions (Figueirêdo et al., 2015;
Kritsky, 1987; Morris, 2004; Costa Neto, 2005; Dossey, 2010). For an
array of reasons, insects and their biological defence systems offer a im-
portant source of chemicals with great potential for use as novel medic-
inal compounds (Dossey, 2010; Dettner, 2011; Alves and Albuquerque,
2013).
Termites (Isoptera) are an insect group that is commonly used in tra-
ditional folk medicine (Wilsanand, 2005; Coutinho et al., 2009;
Figueirêdo et al., 2015). In Brazil, several termite species are commonly
used for the treatment of human diseases, including bronchitis, influ-
enza, whooping cough, asthma, sinusitis, hoarseness and tonsillitis
(Alves et al., 2013). Studies with animal extracts have demonstrated
the efficiency of some species against bacterial strains (Coutinho et al.,
2009, 2010; Chaves et al., 2014). Termites feed on living and dead
plant material. Some termite species use trees as support for nest con-
struction, and some of these support trees are used in folk medicine
(Wilsanand, 2005; Albuquerque et al., 2007). This scenario provides
an good research opportunity in the field of bioprospection because
the potential microbiological activity of animals may be associated
with their relationships with plants. Possible correlations between me-
dicinal flora and fauna need to be evaluated in pharmacological studies
(World Resources Institute, 2000), and the use of animals and plants in
folk medicine may help identify and further characterize useful species.
Therefore, termites provide an excellent opportunity to evaluate the
medicinal properties of biological resources and the importance of the
interactions between the animals and plants used in traditional medi-
cine. Additionally, the possible pharmacological activity of termites
will contribute to a greater appreciation for these animals, which are
usually known for their negative aspects associated with economic
losses.
Bacterial infections are currently the focus of public health, mainly
due to the significant growth of bacterial resistance. Infections caused
by Staphylococcus aureus are the most common, showing a greater diffi-
culty in treatment due to its resistance to various antibiotics (Tortora et
al., 2008). The species Pseudomonas aeruginosa is the leading cause of
nosocomial infections, attacking the skin, urinary tract, ear, and eye
(Murray et al., 2004). Escherichia coli are the most common species of
the genus Escherichia, associated with severe urinary tract infections,
meningitis and gastroenteritis (Murray et al., 2004; Tortora et al., 2008).
In the present study, we investigated Constrictotermes cyphergaster,
which is one of the most important termite species that build conspicu-
ous nests (with visible structures) in ecosystems with sparse vegetation
in South America (Melo and Bandeira, 2004). This species is considered
dominant among other termite species in the caatinga (Neotropical dry
forest). Additionally, C. cyphergaster actively participates in the decom-
position of plant organic matter and nutrient cycling (Vasconcellos et
al., 2007). Bezerra-Gusmão et al. (2013) observed that the supporting
plants used by this termite species were shrubs that occurred at a high
density, including Poincianella pyramidalis (Tul). LP Queiroz
(Catingueira), which affected the distribution of termite mounds in
arid environments. We investigated the plant species P. pyramidalis
(Catingueira) of the Fabaceae family, Spondias tuberosa Arruda
(Umbuzeiro) of the Anacardiaceae family, and Amburana cearensis
(Allemo) AC Smith (Cumaru) of the Fabaceae family, which are used
by C. cyphergaster as support. These plants are widely used in folk
medicine for treating diseases (Silveira and Pessoa, 2005; Lins-neto
et al., 2010; Almeida et al., 2010; Medeiros et al., 2012). Therefore,
this study aimed to assess whether (i) the antimicrobial potential
of termites depended on the supporting plants, (ii) the supporting
plants had higher or lower antimicrobial potential than the
termites and (iii) variation was present in the antimicrobial
potential of the extracts of the supporting plants, nests and termites.
In this context, this study investigated the microbiological potential
of the termite species Constrictotermes cyphergaster and its
supporting plants.
2. Materials and methods
2.1. Study site and sampling
The termite material was collected in the Private Reserve of Natural
Heritage (Reserva Particular do Patrimônio Natural - RPPN) Fazenda
Almas (7°28′S and 36°53′W), in São José dos Cordeiros, state of Paraíba,
Brazil (Barbosa et al., 2007) (Fig. 1). During the study period, 15 samples
were collected from nests that used Poincianella pyramidalis (Tul). LP
Queiroz (Catingueira) (5 samples) and Amburana cearensis (Allemao)
AC Smith (Cumaru) (5 samples), both of the Fabaceae family, and
Spondias tuberosa Arruda (Umbuzeiro) (5 samples) of the
Anacardiaceae family as supporting plants. The samples were collected
from different specimens of each plant species. The specimens were
randomly selected in the collection area, and the collected specimens
were distanced at least 50 m from one another. We collected termites,
the inner wall of the nest, and the stem bark from these specimens.
The samples were collected using a hatchet. The nests and termites
were transferred to sterilized glass containers, and samples of the
stem bark of the supporting plants were stored in Kraft paper bags.
The termite species was identified by Prof. Alexandre Vasconcellos
from the Systematics and Ecology Department (Federal University of
Paraíba - UFPB). Two samples were deposited in the Isoptera Collection
of the Exact Sciences of Nature Center UFPB under the numbers 2047
and 2048. The botanical identification was carried out in the “Prof.
Lauro Pires Xavier Herbarium” (JPB), Systematics and Ecology Depart-
ment, Federal University of Paraíba, where vouchers specimens were
deposited with following reference numbers: JPB 30.589 for Amburana
cearensis, JPB 34.322 for Spondias tuberosa and JPB 41.167 for
Poincianella pyramidalis.
2.2. Preparation of extracts
The collected animals were manually separated from the nest and
divided into three samples as follows: i) termites only, ii) nests only,
and iii) termites and nests at a 1:1 ratio. The collected stem bark was
broken down into small fragments, dried in a forced air oven at 40 °C
until the complete stabilization of moisture, ground in a knife mill,
and sieved through a 10-mesh sieve to obtain bark powder, which
was used to prepare the extracts.
Twenty grams was extracted from each sample by cold soaking
using ethanol as the solvent for 5 days at room temperature. Subse-
quently, after filtration, the extracts were concentrated on a rotary
evaporator at 40 °C until complete evaporation of the solvent was
achieved. The 60 obtained samples included 15 samples of termites
alone, 15 samples of nests alone, 15 samples of termites and nests,
and 15 samples of stem bark, being isolated from each support plant
in which they were collected.
 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928 923

Fig. 1. Location of the municipality of São José dos Cordeiros, Paraíba, and the RPPN Fazenda Almas.
(Source: Santos, 2012)

2.3. Strains
Standard strains of Staphylococcus aureus and Escherichia coli were
used; their resistance profiles are shown in Table 1. The strains were
maintained in Mueller-Hinton agar slants and were cultured before
the assay at 37 °C for 24 h on culture plates containing the same culture
medium. All strains were obtained from the Laboratory of Microbiology
of Universidade Estadual da Paraíba – UEPB.
2.4. Active pharmaceutical ingredient (API)
All tested APIs were obtained from Sigma Chemical Corp. (St. Louis,
MO, USA) and dissolved in sterile water prior to use.
2.5. Determination of the minimum inhibitory concentrations (MICs) and
modulatory activity
The MIC of the antimicrobials was determined in the presence and ab-
sence of sub-inhibitory concentrations (125 μg mL-1). The culture plates
were incubated as described above, and the assays were conducted in
triplicate.
2.6. Chemical assays
2.6.1. Determination of total polyphenols, total flavonoids and condensed
tannins
The total polyphenol content of plant extracts was measured using
spectrophotometry in the visible region by the method of Folin–
Ciocalteu described by Chandra and Mejia (2004) with minor modifica-
tions. The total flavonoids were determined by the method described by
Meda et al. (2005). The content of condensed tannins was verified
through the method described by Makkar and Becker (1993).
2.7. Statistical analysis

The minimum inhibitory concentrations (MICs) were determined by The results are expressed as the geometric means obtained using
microdilution in 96-well plates (CLSI, 2012) using Mueller-Hinton two-way ANOVA, followed by Bonferroni's post hoc test. The data
broth. The modulatory activity of the extracts on bacterial resistance were analysed using GraphPad Prism version 5.0, with p N 0.001
to antimicrobials was evaluated as detailed by Coutinho et al. (2010a). (Matias et al., 2013)

Table 1 3. Results and discussion

Bacterial resistance profiles.

Bacteria Source Resistance profile

The ethanol extract of Constrictotermes cyphergaster demonstrated
no clinically significant activity against the S. aureus and E. coli strains,
Staphylococcus aureus ATCC –
with MICs N1000 μg mL-1. Similarly, the ethanol extracts of the nests
(ATCC 25923)
Escherichia coli (ATCC ATCC – alone and termites combined with nests showed MICs N1000 μg mL-1.
25922) These results indicate the lack of variation of the antimicrobial potential
Staphylococcus aureus 345 Catheter OXA, PEN, AZI, SFM, CFO, NOR, AMP, GENT of the extracts of C. cyphergaster, the nests, and their combinations. Con-
tip
versely, this variation was evident in the comparison of the MICs of the
Escherichia coli 534 Catheter AMP, CRO, NOR, CAZ, ATM, TET, COM,
tip GEN, CFL, CLI, SFM extracts of the supporting plants because some specimens had MICs
≤1000 μg mL-1 against S. aureus (Tables 2, 3, and 4).
OXA = oxacillin; PEN = penicillin; AZI = azithromycin; SFM = sulfamethoxazole + tri-
methoprim; CFO = cefoxitin; NOR = norfloxacin; AMP = ampicillin; GENT = gentami-
The bark extracts of S. tuberosa and P. pyramidalis (Catingueira)
cin; CRO = ceftriaxone; CAZ = ceftazidime; ATM = aztreonam; TET = tetracycline; showed moderate activity against standard and resistant strains of S. au-
CPM = cefepime; CFL = cephalothin CLI = clindamycin. reus, with MIC values of 500 μg mL-1 (Tables 2 and 3). The bark extract
924 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928

of A. cearensis did not show significant antimicrobial activity, with MICs Table 3
of 1000 μg mL-1 for most specimens; however, variation was observed Minimum inhibitory concentrations (MICs) of the ethanol extracts of Constrictotermes
cyphergaster, the nests, and the bark of Poincianella pyramidalis (μg/mL); Cc: Extract of C.
in the antimicrobial potential of the specimens of this species (Table 4). cyphergaster; Nc: Extract of the C. cyphergaster nest; Cc+Nc: Extract of termites together
None of the tested concentrations of the plant extracts inhibited the with the nest; Pp: Extract of the P. pyramidalis bark.
growth of the standard and resistant E. coli strains.
Extracts Microorganisms
The bark extract of P. pyramidalis presented a MIC of 500 μg mL-1
against the standard and resistant S. aureus strains, indicating moderate SA (ATCC 25923) SA 345 EC (ATCC 25922) EC 534
antimicrobial activity; this activity was higher than the activity of the Cc 1 N1000 – N1000 –
bark extracts of the other investigated supporting plants (Table 3). Nc 1 N1000 – N1000 –
However, variation in the MIC of the bark extract of S. tuberosa was ob- Cc + Nc 1 N1000 N1000 N1000 N1000
Pp 1 500 500 N1000 N1000
served against the S. aureus strains; for instance, specimen 4 (St 4) had a Cc 2 N1000 – N1000 –
MIC of 1000 μg mL-1, whereas the other specimens presented MIC Nc 2 N1000 – N1000 –
values of 500 μg mL-1 (Table 2). We also observed variation in the Cc + Nc 2 N1000 – N1000 –
MIC of the bark extracts of A. cearensis, with specimen 2 (Ac 2) not Pp 2 500 – N1000 –
Cc 3 N1000 – N1000 –
showing strong antimicrobial activity (MIC N1000 μg mL-1), whereas
Nc3 N1000 – N1000 –
the other specimens presented MIC values of 1000 μg mL-1 (Table 4). Cc + Nc 3 N1000 – N1000 –
In a complementary manner, we also evaluated whether the extracts Pp 3 500 – N1000 –
combined with antibiotics exerted antibacterial activity against the Cc 4 N1000 – N1000 –
multidrug resistant strains of E. coli and S. aureus. For this purpose, we Nc4 N1000 – N1000 –
Cc + Nc 4 N1000 – N1000 –
selected the ethanol extracts of C. cyphergaster together with the nest Pp 4 500 – N1000 –
and bark extracts of S. tuberosa, A. pyramidalis, and P. cearensis from Cc 5 N1000 – N1000 –
the first collected specimens of the samples used in the antimicrobial Nc 5 N1000 – N1000 –
activity analysis because no significant differences in the MICs of the ex- Cc + Nc 5 N1000 – N1000 –
Pp 5 500 – N1000 –
tracts were found for C. cyphergaster, the nests, their combinations, and
the supporting plants of the other specimens against the bacterial
strains. The results of the assays to evaluate the modulatory activity of
the antibiotics indicated that the combination of the extracts with a cyphergaster and its nests, the S. tuberosa and P. pyramidalis extracts
MIC of 125 μg mL-1 significantly reduced the MICs of most of the tested showed no synergistic effect with ceftriaxone. Similarly, the extract of
antibiotics, with the exception of clindamycin against S. aureus (Fig. 2) C. cyphergaster combined with the extract of the nests of a specimen
and ciprofloxacin and ceftazidime against E. coli (Fig. 3). of S. tuberosa (CcSt) did not show a synergistic effect when combined
The results indicated the synergistic effect of the extracts of C. with levofloxacin. In contrast, a reduction in the MIC was observed
cyphergaster and its nests and the antibiotics against S. aureus, particu- when levofloxacin was combined with the other extracts (Fig. 2).
larly the combination with chloramphenicol, which resulted in a The results of the assays with E. coli 534 indicated synergism of all
marked reduction of the MIC from 500 to 250 μg mL-1. A reduction in extracts with levofloxacin, including reduction of the MIC from 62.5 to
the MIC was also observed for ceftriaxone (250–62.5 μg mL-1) when 7.8 μg mL-1 with the combination of the extract of C. cyphergaster
combined with the extract of C. cyphergaster and the nest of a specimen with its nests made with the supporting plants. Similarly, the Pp and
of S. tuberosa (CcSt) and P. pyramidalis (CcPp) (Fig. 2). Moreover, the Ac extracts decreased the MIC of levofloxacin from 62.5 to 15.62
synergistic effect of the S. tuberosa, P. pyramidalis, and A. cearensis ex- μg mL-1. The MIC of cefazolin against E. coli 534 was 49.60 μg mL-1.
tracts with chloramphenicol and levofloxacin allowed the reduction of However, the combination of cefazolin with CcSt, St, and Ac reduced
the MIC from 500 to 250 μg mL-1. In contrast to the extracts of C. the MIC to 31.25 μg mL-1. Moreover, the CcPp and Pp extracts did not

Table 2
Minimum inhibitory concentrations (MICs) of the ethanol extracts of Constrictotermes
cyphergaster, the termite nests, and the bark of Spondias tuberosa (μg/mL); Cc: Extract of
C. cyphergaster; Nc: Extract of the C. cyphergaster nest; Cc+Nc: Extract of termites together
with the nest; St: Extract of the S. tuberosa bark.
Table 4
Minimum inhibitory concentrations (MICs) of the ethanol extracts of Constrictotermes
cyphergaster, the nests, and the bark of Amburana cearensis (μg mL−1); Cc: Extract of C.
cyphergaster; Nc: Extract of the C. cyphergaster nest; Cc + Nc: Extract of termites together
with the nest; Ac: Extract of the A. cearensis bark.

Extratos Microorganismos Extracts Microorganisms

SA (ATCC 25923) SA 345 EC (ATCC 25922) EC 534 SA (ATCC 25923) SA 345 EC (ATCC 25922) EC 534

Cc 1 N1000 – N1000 – Cc 1 N1000 – N1000 –

Nc1 N1000 – N1000 – Nc 1 N1000 – N1000 –
Cc + Nc1 N1000 N1000 N1000 N1000 Cc + Nc 1 N1000 N1000 N1000 N1000
St 1 500 1000 N1000 N1000 Ac 1 1000 1000 N1000 N1000
Cc 2 N1000 – N1000 – Cc 2 N1000 – N1000 –
Nc 2 N1000 – N1000 – Nc2 N1000 – N1000 –
Cc + Nc 2 N1000 – N1000 – Cc + Nc 2 N1000 – N1000 –
St 2 500 – N1000 – Ac 2 N1000 – N1000 –
Cc 3 N1000 – N1000 – Cc 3 N1000 – N1000 –
Nc 3 N1000 – N1000 – Nc 3 N1000 – N1000 –
Cc + Nc 3 N1000 – N1000 – Cc + Nc 3 N1000 – N1000 –
St 3 500 – N1000 – Ac 3 1000 – N1000 –
Cc 4 N1000 – N1000 – Cc 4 N1000 – N1000 –
Nc 4 N1000 – N1000 – Nc4 N1000 – N1000 –
Cc + Nc 4 N1000 – N1000 – Cc + Nc 4 N1000 – N1000 –
St 4 1000 – N1000 – Ac 4 1000 – N1000 –
Cc 5 N1000 – N1000 – Cc 5 N1000 – N1000 –
Nc 5 N1000 – N1000 – Nc 5 N1000 – N1000
Cc + Nc 5 N1000 – N1000 – Cc + Nc 5 N1000 – N1000
St 5 500 – N1000 – Ac 5 1000 – N1000 –
 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928 925

Fig. 2. Modulatory activity of the ethanol extracts of Constrictotermes cyphergaster and supporting plants on the resistance of S. aureus to antibiotics. ***: Significant value with p b 0.001; ns:
Non-significant value with p N 0.05. LEV: levofloxacin; CLO: chloramphenicol; CLI: clindamycin; CFO: Ceftriaxone; CcSt: Extract of C. cyphergaster and the nest of a specimen of S. tuberosa;
CcPp: Extract of C. cyphergaster and the nest of a specimen of P. pyramidalis; CcAc: Extract of C. cyphergaster and the nest of a specimen of A. cearensis; St: Extract of the S. tuberosa bark; Pp:
Extract of the P. pyramidalis bark; Ac: Extract of the A. cearensis bark.

exhibit significant activity when combined with cefazolin (Fig. 3). Our
results indicated no synergism between the extracts and ciprofloxacin
and ceftazidime.
Through chemical tests, it was possible to appoint the presence and
concentration of substances in the extracts that confirmed significant
modulating activity. The concentration of these compounds is shown
in Table 5 and was expressed in milligrams equivalent to the standards
used.
Regarding the antimicrobial activity, a MIC greater than 1000 μg mL-
1 was found for the ethanol extracts of C. cyphergaster and its nests
against the E. coli and S. aureus,strains whereas the S. tuberosa, P.
pyramidalis, and A. cearensis extracts did not exhibit clinically significant
activity against the E. coli strains. This MIC was considered high because
Rios and Recio (2005) reported in a study of medicinal plants that the
MICs of extracts with antimicrobial activity should be less than 1000
μg mL-1.
Similarly, other authors reported that plant extracts with MICs less
than 100 μg mL-1 had high inhibitory activity, extracts with MICs rang-
ing from 100–500 μg mL-1 had moderate activity, extracts with MICs
ranging from 500–1000 μg mL-1 had weak activity, and extracts with
MICs larger than 1000 μg mL-1 lacked antimicrobial activity (Fabry et
al., 1998; Holetz et al., 2002; Dall Angol et al., 2003; Tanaka et al.,
2005). Considering these ranges, the ethanol extracts of S. tuberosa
and P. pyramidalis revealed moderate activity (500 μg mL-1) and the ex-
tract of A. cearensis revealed weak activity (1000 μg mL-1) against the
tested S. aureus strains. The correlation between the MICs of the ethanol
extracts of C. cyphergaster and its nests indicated that these extracts
were inactive against the S. aureus and E. coli strains and that all of the
plant extracts were inactive against the E. coli strains.
The absence of inhibitory activity of these ethanol extracts against
the Gram-negative bacterium (E. coli) may be correlated with structural
differences in the outer membrane between this bacterial species and
the Gram-positive S. aureus because this membrane acts as a barrier to
the entry of the active substances present in the extracts (Urzua et al.,
1998). The increased bacterial resistance may also be due to the pres-
ence of the potentially active compounds at very low concentrations
or the lack of metabolites active against this bacterial species in the ex-
tracts (Koneman et al., 2001). Trabulsi and Alterthum (2005) reported
that the higher rate of inhibition of Gram-positive bacteria occurred be-
cause 90% of the cell walls of these bacteria were made of peptidogly-
cans. In contrast, the cell walls of Gram-negative bacteria were more
complex, which increased the resistance of these bacterial species
against antimicrobials.
The moderate activity of the supporting plants against the S. aureus
strains indicated that the antimicrobial potential of the bark ethanol ex-
tracts of S. tuberosa, P. pyramidalis, and A. cearensis was higher than the

Fig. 3. Modulatory activity of the ethanol extracts, Constrictotermes cyphergaster, and supporting plants on the resistance of E. coli to antibiotics. ***: Significant value with p b 0.001; ns:
non-significant value with p N 0.05. LEV: levofloxacin; CIP: ciprofloxacin; CFZ: cefazolin; CFT: Ceftazidime; CcSt: Extract of C. cyphergaster and the nest of a specimen of S. tuberosa; CcPp:
Extract of C. cyphergaster and the nest of a specimen of P. pyramidalis; CcAc: Extract of C. cyphergaster and the nest of a specimen of A. cearensis; St: Extract of the S. tuberosa bark; Pp: Extract
of the P. pyramidalis bark; Ac: Extract of the A. cearensis bark.
926 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928
Table 5
Concentration of secondary metabolites (mg g-1) determined for the extract of C.
cyphergaster and the nest of a specimen of S. tuberosa (CcSt); Extract of C. cyphergaster
and the nest of a specimen of P. pyramidalis (CcPp); Extract of C. cyphergaster and the nest
of a specimen of A. cearensis (CcAc); Extract of the S. tuberosa bark (St); Extract of the P.
pyramidalis bark (Pp) and the extract of the A. cearensis bark (Ac).
Extract Total polyphenols Flavonoids Tannins
Pp 36.94 ± 0.451 19.09 ± 0.782 59.08 ± 0.693
CcPp 74.51 ± 0.151 23,09 ± 0.372 171.22 ± 0.773
St 17.47 ± 0.201 8.51 ± 0.312 47.17 ± 0.723
CcSt 70.20 ± 0.231 21.98 ± 0.382 170.69 ± 0.833
Ac 81.05 ± 0.241 25.36 ± 0.272 190.69 ± 0.813
CcAc 79.02 ± 0.191 24.58 ± 0.202 186.96 ± 0.803
1
Gallic acid equivalent (GAE).
2
3
Quercetin equivalent (QE).
Catechin equivalent (CE).
activity of C. cyphergaster and its nests. The antimicrobial activity of the
analysed supporting plants was clearly demonstrated. The activity of
the S. tuberosa extract against S. aureus reinforced the findings of
Rocha et al. (2013), who used the same microdilution method and
found a similar activity of the S. tuberosa extract against S. aureus. Sim-
ilarly, other studies have confirmed the antimicrobial activity of S.
tuberosa. Costa et al. (2013) used a different methodology (disc agar dif-
fusion) and found that the S. tuberosa extract was effective against S. au-
reus and Enterococcus faecalis. Carvalho (2012) found that that
Streptococcus and Candida were sensitive to this plant extract. Similarly,
the high antimicrobial activity of P. pyramidalis demonstrated in our
study supported the results of Lima et al. (2006), who found that etha-
nol extracts of the bark and leaves of this plant species were active
against S. aureus. Moreover, the aqueous extract of P. pyramidalis
showed strong activity against oral microorganisms, indicating its po-
tential for the treatment of oral diseases (Alviano et al., 2008). A phyto-
chemical research of P. pyramidalis extracts revealed the presence of
several compounds with recognized antimicrobial activity, including
ursolic acid, quercetin, catechin, sitosterol, flavonoids, and gallic acid
(Saraiva et al., 2012). Therefore, the biological activity presented in
our study and the above-mentioned studies might be a result of the ac-
tivity of these constituents.
Our results indicated that the combination of the tested extracts
with antibiotics potentiated the activity of most antibiotics against the
E. coli and S. aureus strains. The use of natural products in combination
with antibiotics has been well investigated, and the products of medic-
inal fauna have shown the potential to enhance the action of antibiotics
against multidrug-resistant bacteria (Coutinho et al., 2009, 2010, 2014;
Ferreira et al., 2011; Santos et al., 2012; Oliveira et al., 2014).
Although the antimicrobial activity of the extracts of C. cyphergaster
and its nests was not significant, the modulatory activity of these ex-
tracts was considered significant because the combination of the ex-
tracts with most tested antibiotics reduced the MIC against resistant
strains of S. aureus and E. coli and potentiated the activity of levofloxacin
and cefazolin against strains of EC 534 and the activity of levofloxacin,
chloramphenicol, and ceftriaxone against strains of SA 345 (Figs. 2 and
3). Similarly, Coutinho et al. (2009) observed a reduction in the MICs
of gentamicin and neomycin, indicating modulatory activity of the
Nasutitermes corniger extract. The study by Chaves et al. (2014) also re-
ported a synergism of the N. corniger extract and antibiotics against E.
coli and S. aureus strains, indicating that compounds from N. corniger
and possibly other termite species could change the modulatory activity
of antibiotics against multidrug-resistant bacteria.
The chemical exam performed in this work indicated the presence of
flavonoids, polyphenols and tannins in the extracts tested in the modu-
latory activity (Table 5). It is possible that these metabolites affect the
lipid bilayer of the bacteria, disrupting the cell membrane and enhanc-
ing the influx of antibiotics and their effect (Chaves et al., 2014). The
content of the total number of tannins was high compared to total flavo-
noids and polyphenols, this compound can act on the metabolism in
microorganisms through inhibition of enzymes, the electron transport
system, oxidative phosphorylation and inactivation of microbial
adhesins and proteins of the cell envelope (Scalbert, 1991; Cowan,
1999).
The synergism between the extract of C. cyphergaster and its nests
and the antibiotics may be due to the secondary metabolites existent
in the extracts that are synthesized by plants because C. cyphergaster
is xylophagous, and the secondary metabolites of the supporting plants
used as food source are found in the digestive system of the animal and
in the faeces used to build the nests (Medeiros, 2004; Lima and Costa-
Leonardo, 2007). Therefore, the possible antimicrobial potential of C.
cyphergaster is associated with the plant used as support. Dixon et al.
(2001) reported that the synergistic activity of natural products and an-
tibiotics might be due to secondary metabolites, such as flavonoids and
tannins, which are produced by plants in response to microbial
infections.
No significant differences in the modulatory activity of the antimi-
crobials from C. cyphergaster and its nests and the plant antimicrobials
were observed, and this activity was not increased when the extracts
were combined with the tested antibiotics. Previous studies have con-
firmed the activity of supporting plants. For instance, the study of
Figueredo et al. (2013) found a reduction in the MIC and consequently
the potentiation of the activity of gentamicin and amikacin combined
with an A. cearensis extract against E. coli strains. Similarly, Alencar et
al. (2015) found modulatory activity of antibiotics from the extracts of
species of the genus Spondias, suggesting that these species were
sources of natural products with the potential to modulate the activity
of antibiotics against multidrug-resistant bacterial strains.
In a broader perspective, the antimicrobial activity of products iso-
lated from termites has been evidenced, including the peptides
spinigerin and termicin isolated from Pseudocanthotermes spiniger,
which show antibacterial and antifungal activity. These peptides are
found in the salivary glands and granules of red blood cells of this ter-
mite species, respectively (Lamberty et al., 2001). Similarly, studies on
the molecular biology of species of genus Nasutitermes demonstrated
their potential to produce antimicrobial peptides (Bulmer and Crozier,
2004, 2006).
Termites and other social insects build nests that contain an associ-
ated microbiota, which includes microorganisms that live in symbiosis
with these insects and provide protection against bacterial and fungal
infections (Chaves et al., 2014). This microbiota includes actinomycetes,
some of which have been isolated and had their antimicrobial activity
demonstrated. Visser et al. (2012) isolated Actinobacteria from the
nests of Microtermes sp., Macrotermes natalensis and Odontotermes spp.
and demonstrated their antimicrobial activity. Moreover, Bonfim
(2012) confirmed the activity of Actinobacteria and Bacillus isolated
from the nests of Nasutitermes against Gram-positive bacteria.
The ethanol extracts of C. cyphergaster and its nests and the bark ex-
tracts of the analysed supporting plants strongly modulated the activity
of most of the tested antibiotics. The synergistic activity of these extracts
indicates the high potential for the use of natural products in combina-
tion with synthetic drugs in the Brazilian pharmaceutical market.
Among the products of plant and animal origin, extracts are considered
complex mixtures, and this complexity limits microbial adaptability.
Therefore, microorganisms have a low likelihood of acquiring resistance
against these products (Coutinho et al., 2009b). Furthermore, when
combined with antibiotics, extracts can act directly against bacterial
species by either modulating or increasing the activity of specific antibi-
otics, thereby reversing the natural resistance of bacteria to specific an-
tibiotics (Souza et al., 2014).
4. Conclusion
Our results indicate that the antimicrobial potential of ethanol ex-
tracts of the bark of supporting plants is higher than the antimicrobial
potential of the C. cyphergaster extracts. Moreover, we found variation
 I.S. Policarpo et al. / Science of the Total Environment 639 (2018) 921–928
in the antimicrobial potential of the extracts of C. cyphergaster and its
nests. Conversely, the combination of the extracts of C. cyphergaster
and its nests with antibiotics produces a strong synergistic activity be-
cause C. cyphergaster is a xylophagous species. These results indicate
that the antimicrobial potential of this termite species depends on the
plants used as support.
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