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Ectoparasitos asociados con murcielagos en el noreste de Tolima, Colombia.



Because they cover a wide trophic spectrum and often exhibit high habitat specificity, bats (Chiroptera) represent a good model for analyzing the consequences of habitat fragmentation and environmental changes (Perez-Torres and Ahumada, 2004; Jones et al., 2009). Bats also represent a key group for understanding the evolution and ecology of parasitism, because their ectoparasites are often specialized, with many taxa closely associated with particular species of ectoparasites (Dick and Patterson, 2006).

There have been relatively few studies of bat ectoparasites in Colombia. Early studies of obligate ectoparasitic Diptera in Colombia and Panama highlighted the presence of the families Streblidae (16 species) and Nycteriibidae (2 species) (Bequaert, 1940). Machado-Allison and Antequera (1969) reported the distribution and hosts of spinturnicid mites, including the presence of the genus Spinturnix. Subsequently, Marinkelle and Grose (1981) published a list of ectoparasites in Colombian bats of the orders Diptera, Hemiptera and Siphonaptera, as well as 5 families of mites, reporting a total of 88 species. Recently, Dick et al. (in press) developed a catalogue of Streblidae of Colombia, reporting 73 species recorded in Colombia. Despite these efforts, information on Colombian bat ectoparasites is still scarce (Tarquino-Carbonell, 2014). We studied associations between ectoparasites and their chiropteran hosts in a fragment of tropical dry forest in the northern department of Tolima, presenting data on prevalence and intensity of infestation, and determining interdependence between ectoparasites and hosts.


Study area

The study was carried out in Chorrillo, a site of approximately 50 ha of fragmented forest, in the Ambalema municipality in northeastern Tolima, Colombia (4[degrees] 26' N, 74[degrees] 4 8' W) approximately 273 m above sea level. The average annual temperature is 25.7 [degrees]C, and relative humidity is 80%. Rainfall averages 3116 mm annually (Hijmans et al., 2005). The vegetation cover and climatic conditions correspond to tropical dry forests (Holdridge, 1967).

Field Methods

The material was collected between August and November 2012, 3 nights per month, every night from 18:00 to 00:00 h. Five mist nets of 12 x 3 m were used at the understory and checked every 30 min. Bats were extracted from the mist net using a red flashlight and separated into individual bags to prevent contamination between hosts. The handling and collection of the organisms were made following the guidelines of the American Society of Mammalogists (Gannon et al., 2007; Sikes et al., 2011). Morphometric data were taken using a digital caliper with 0.1 mm precision. Ectoparasites were collected with fine forceps and placed in Eppendorf tubes containing 70% ethanol, each one labeled with the capture number from each bat.

Laboratory methods

Bats were prepared as standard museum specimens and identified using keys and descriptions from Gardner (2008). Mites were mounted in Hoyer's and Lactophenol medium (Faraji and Bakker, 2008), and examined using a Nikon Labophot microscope YF21-E with phase contrast and Nikon DS-Fi1 camera, and a Leica MS-5 stereomicroscope. Insects were examined in ethanol. We identified Macronyssidae mites using Radovsky (1967), Spinturnicidae with Herrin and Tipton (1975). We used Kohls et al. (1965) to identify the species of Ornithodoros. Diptera were identified with the keys of Wenzel (1976) and pictorial keys from Graciolli and Carvalho (2001). The specimens collected as samples are preserved in the Zoological Collection of the University of Tolima (CZUT).

Data analysis

To evaluate the association of ectoparasites among different hosts, we used the following indices (Bush, 1997):

Prevalence: the number of hosts infected with 1 or more individuals of a particular parasite species (or taxonomic group) divided by the number of hosts examined for that parasite species.

Mean intensity: the average intensity of a particular species of parasite among the infected members of a particular host species

To determine if there are associations between the parasite and the bat taxa, a contingency table was realized to each of the families of parasites found and a Fisher's test was applied like in another studies (Almeida et al., 2011). Variables such as number of parasitic hosts and presence of two or more parasite families at the same time are taken into account in this contingency table, testing for significant differences between each parasite family with respect to the other families


We recorded 140 bats belonging to 21 species and 5 families. Phyllostomidae was the most abundant family with the highest number of species registered (Table 1). The most frequently captured bat species were Carollia perspicillata (35%), Artibeus planirostris (14%) and Desmodus rotundus (11%). Species in the subfamily Phyllostominae, as well as in the families Emballonuridae and Vespertilionidae, were less common in general.

Associations between ectoparasites and bats

Eight bat species (29.28%) were parasitized by streblid flies, 6 species (14.28%) by spinturnicids, 5 species (9.28%) by the macronyssids and 5 species (7.85%) by argasid ticks (Table 2). A total of 69 hosts representing 14 bat species were found to be parasitized. Some species of ectoparasites collected were found in coexistence on the same host; in particular ~64% of these associations were found on D. rotundus. The most common association between ectoparasites families was between Streblidae and Spinturnicidae.

Streblidae. Eleven bat fly species were recorded for this family. The most abundant bat fly is Trichobius parasiticus, present in D. rotundus, and Trichobius joblingi, found on C. perspicillata. The bat flies reported in this study (Table 3) represent 18% of all species registered in Colombia (Guerrero, 1997).

The most abundant bat fly was T. joblingi, found on both species of Carollia. Four species of Trichobius were found on five species of bats.

Spinturnicidae. Six spinturnicid species were found in association with six host species (Table 4). The most abundant species was Periglischrus iheringi, followed by Periglischrus ojasti. We found adult males, females and, in smaller numbers, male protonymphs of P. iheringi on two host species (Table 4).

Macronyssidae. Four macronyssid species were present on 12 individuals of five bat species (Table 5). The most frequently encountered species was Raddfordiella desmodi, only found in D. rotundus, followed by Macronyssoides conciliatus in A. planirostris.

Argasidae. This family was represented by only two species (Table 6); however, they were found in large numbers and on five different host species, including diverse subfamilies with different trophic guilds (i. e. fisher bat and vampire bat).

We also found Trombiculidae larvae on a Saccopteryx bilineata male, although they could not be identified to species due to deterioration of the proboscis.

The frequency data of Streblidae was significantly associated (Fisher's p = 0.003) with the frequency values of each of the other three families of parasites found in this study. No other significant associations were found between families.


Phyllostomidae was the family with greatest species richness and abundance (Table 1). This is consistent with results of studies of bat richness in other Colombian tropical dry forests (Ballesteros et al., 2007; Sanchez et al., 2007; Mantilla-Meluk, 2009). These results might be attributed to the variety of trophic guilds that this family presents and their wide geographic distribution in the country (Ballesteros et al., 2007; Sanchez et al., 2007; Mantilla-Meluk, 2009). In terms of species richness and local areas of importance for bat conservation, Chorrillo has almost a third of the bat species reported for the Department of Tolima (Galindo-Espinosa et al., 2010; Gutierrez et al., 2010; Solari et al., 2013).

Species of Carollia are characterized by their adaptation to changes in habitat conditions, a pattern applicable to various Neotropical areas (Kalko, 1998; Simmons and Voss, 1998; Soriano, 2000; Willig et al., 2007). Artibeus planirostris can move easily between open and fragmented areas, eating a wide variety of fruits, allowing seed dispersion within forests (Cadena et al. 1988). The evidence indicates that D. rotundus is especially abundant in areas with a high density of domestic animals (Sanchez et al., 2010). This factor could explain their high abundance in the study site during the sampling period.

The low number of species from the families Emballonuridae and Vespertilionidae could be related to limitations of sampling methods and the flight behavior of the species, because these families are characterized by high flight between and above the forest canopy (Bergallo et al., 2003; Simmons and Voss, 1998). Moreover, relative to phyllostomids, their echolocation allows them to better detect and avoid mist nets (Ortegon-Martinez and Perez-Torres, 2007). Specifically, members of Phyllostominae usually hunt their prey at higher open spaces or forest edges (Montenegro and Romero- Ruiz, 1999), thus explaining their low catch.

Associations between ectoparasites and bats

Streblid flies are typical and widespread in the Neotropics (Carrrejo and Gonzalez-Obando, 1992). This family lives mainly on bats of the family Phyllostomidae, which are also widely distributed and abundant throughout the Neotropics (Guerrero, 1996). On the other hand, the most species-rich genus was Trichobius. Species in this genus are generally quite mobile with greater ability to fly relative to other bat flies. For example, T. joblingi, a winged fly that lives in roost sites often shared by two or more host species, actively moves outside the body of the host (Guerrero, 1996; Dick and Patterson, 2006). In fact, this genus is usually quite abundant in studies of this type (Guerrero, 1996; Dick and Patterson, 2006; Almeida et al., 2011).

Aspidoptera phyllostomatis has been reported on Artibeus jamaicensis (Guerrero, 1997), but there is no record of its occurrence on Artibeus planirostris. However, changes in Artibeus taxonomy for northern South America (Larsen et al., 2007, 2010) and recent reviews show that A. jamaicensis is restricted to the Colombian Caribbean region (Solari et al., 2013). For the Magdalena valley of Department of Tolima, these bats must be recognized as A. planirostris (Solari et al., 2013). Therefore, in this study we note that the species of Artibeus recorded in northern Tolima is A. planirostris, which was parasitized by Aspidoptera phyllostomatis.

The incidence of Streblidae was very high for some bat species such as C. perspicillata and D. rotundus (Table 3), although the prevalence in this study is lower than that previously reported in Colombia (Marinkelle and Grose, 1981) for the same species. Low host specificity has been proposed for these bat flies, as many species of bats that share the same roost sites are exposed to similar parasites (Theodor, 1957). On the other hand, Streblidae are very common among phyllostomid species, which could explain this finding compared to groups of mites already reported in other studies (Guerrero, 1996). Bat flies are often dependent on the presence of the other groups; i.e., bat flies will be associated with particular species depending on which bat species are present in particular roosts.

The high interdependence found for streblids in the contingency table reflects by abundance of Streblidae on C. perspicillata and D. rotundus, revealing their strongest association in relation to other groups of ectoparasites. Thus, bat flies on C. perspicillata were significantly more likely to be the only parasites on their host to be found in association with other parasites. The significant results for the other 3 families of ectoparasites and their equal proportions suggest that the remaining families were associated uniformly for this study. Taxa exhibiting the lowest ectoparasite prevalence and mean intensity were those species that shelter in open areas. Also, caves allow greater horizontal transfer of ectoparasites relative to open habitats (Guerrero, 1993; Guerrero, 1996; Dick and Paterson, 2006)

It has been proposed that the presence or absence of one parasitic fly species may facilitate the presence or absence of another fly species, by representing the persistence of two species of parasites in a host over time (Dick and Gettinger, 2005). In some cases, these associations americanus has been described parasitizing Brazilian Myotis spp. (Silva et al., 2013). Ours is the first report of this association for the region of Tolima. occur even when the parasites are in different genera (Dick and Gettinger, 2005). The degree of specificity in bat flies as obligate ectoparasites has been debated and some studies suggest a high specificity (Dick and Gettinger, 2005), although higher host densities could provide a substrate rich for bat flies and might be affecting associations of these flies (Guerrero, 1993; Dick y Paterson, 2006). However, certain factors that influence the specificity such as physical isolation, climate, competition, predation and physiological and morphological adaptation are recognized (Marshall, 1976, 1982).

The dynamics of mites as obligate ectoparasites of bats, unlike other groups such as Streblidae, have not been studied in recent decades and little is known about the regional distribution of species in the case of Colombia (Bequaert, 1940; Machado-Allison and Antequera, 1969; Marinkelle and Grose, 1981). These studies only include new species descriptions, reflecting the paucity of recent studies on taxonomy of ectoparasites and parasite-host relationship.

The Spinturnicidae family, found only on the wings and tail membranes of the host, exhibit a life cycle morphologically adapted and modified relative to other Mesostigmata (Rudnick, 1960). In general, this family can be easily found in any given bats group of the New World due to their morphological, ecological and behavioral conditions (Dowling, 2006). Periglischrus iheringi is commonly found in species of Artibeus and Uroderma, and other species as S. lilium (Herrin and Tipton, 1975). This species has been reported in Colombia in several leaf-nosed bat species including some species of Glossophaga (Marinkelle and Grose, 1981) without references to A. planirostris, which might indicate contamination or misidentification of the host. However, the association between these two species has already been extensively described from previous works in Brazil (Almeida et al., 2008; Silva et al., 2013).

Periglischrus ojasti has been reported in Colombia parasitizing S. lilium and S. ludovici, while P. acutisternus has primarily been reported in association with species of Phyllostomus, as we found in this study (Marinkelle and Grose, 1981). In the Neotropics, Spinturnix americanus has been described parasitizing Brazilian Myotis spp. (Silva et al., 2013). Ours is the irst report of this association for the region of Tolima.

The proportion of Macronyssidae was low relative to other groups, such as streblids. Their range of movement is much lower than other groups, gives them greater specificity in relation to other groups of ectoparasites (Radovsky, 1967). We found no males of this family on any hosts, likely because Macronyssidae males do not consume blood (Radosky, 1967). The low number of macronyssid mites collected in this study makes it difficult to compare their prevalence with other studies, which reported higher numbers of mites. For example, Radffordiella desmodi species has been found in association with Desmodus in Costa Rica (Rojas et al., 2008). Steatonyssus occidentalis has been found in some genus of Vespertilionidae (Radovsky, 1967). Macronyssoides conciliatus can be found in Molossus genus (Radovsky, 1967), and the recently described P. bakeri (Morales-Malacara and Guerrero, 2007) can be found in some Phyllostomidae. The low number of specimens collected in this study may indicate contamination, so it is necessary to obtain more samples to gain an accurate understanding of their prevalence.

Argasid ticks can be found in well-established colonies of bats, where high transfer of ectoparasites occurs (Guerrero, 1996). Ornithodoros hasei has been found in association with species of the genus Artibeus, Phyllostomus, Noctilio, Rhogeeesa and Molossus for Colombia (Marinkelle and Grose, 1981). Ornithodoros (Pavloskyella) natalinus has only been reported previously on bats of the genus Natalus (Capinera, 2008). We present the first report of Ornithodoros (Pavloskyella) natalinus on individuals of D. rotundus for this region.

Results from our study suggest this locality can provide important information about bat-ectoparasites relationships in dry forests, an ecosystem that has previously been only rarely studied. In particular, we found that bat species most frequently parasitized (C. perspicillata, D. rotundus and A. planirostris) are those which inhabit transformed spaces and secondary vegetation, exhibiting habitat flexibility. This habitat preference, in addition to ectoparasite ecology, roosting site, bat biology and host behavior, influence the association and competition between different ectoparasites families and the parasite load of the hosts. Our data relating to prevalence of major groups and species of ectoparasites present in bat populations of northern Tolima could help inform and provide direction for further research on these topics.

Recibido 24 abril 2015. Aceptado 17 junio 2015. Editor asociado: M Lareschi


To Viviana Garcia, Azucena Ramirez, Fabian Santos, Kevin Gonzalez, Daniel Duran, Enryque Torres, Steven Lievano, Luisa Beltran, Daniela Ortiz, and Angela Navarro for their field supportment. To the Instituto de Zoologia y Ecologia Tropical from the Universidad Central de Venezuela and the people who made it possible to stay in this country to review the material. To Luz Stella Sierra, Jenny Sierra, Jennifer Sierra, Paola Mojica for their help in Caracas. To the people from Chorrillo for receiving us very generously in the location. We are very grateful to Carl Dick and an anonymous reviewer for their suggestions. Special thanks to Erin Kane for their comments. The lead author is especially grateful to Fredy Quintero for his support in this work. This research was funded by the Comite Central de Investigaciones and Grupo de Investigacion en Zoologia of University of Tolima.


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Andrea del Pilar Tarquino-Carbonell (1), Karina A. Gutierrez-Diaz (1), Emma Y. Galindo-Espinosa (1), Gladys Reinoso-Florez (1), Sergio Solari (2), and Ricardo Guerrero (3)

(1) Grupo de Investigacion en Zoologia, Universidad del Tolima, Barrio Santa Helena, 730006 Ibague, Tolima, Colombia [Correspondencia: Andrea del Pilar Tarquino-Carbonell <>]

(2) Grupo Mastozoologia, Instituto de Biologia, Universidad de Antioquia, 050010 Medellin, Antioquia, Colombia.

(3) Instituto de Zoologia y Ecologia Tropical, Universidad Central de Venezuela, 1050 Caracas, Venezuela.
Table 1
Bat species reported in this study.

Family                            Species                N     %

Emballonuridae     Rhynchonycteris naso                  1    0.7
                   (Wied-Neuwied, 1820)
                   Saccopteryx bilineata                 1    0.7
                   (Temminck, 1838)

Noctilionidae      Noctilio albiventris                  1    0.7
                   (Desmarest, 1818)

Phyllostomidae     Trachops cirrhosus (Spix, 1823)       6    4.3
                   Tonatia saurophila (Koopman and       1    0.7
                   Williams, 1951)
                   Phyllostomus hastatus                 1    0.7
                   (Pallas, 1767)
                   Lophostoma silvicola                  1    0.7
                   (d'Orbigny, 1836)
                   Lonchophylla robusta                  1    0.7
                   (Miller, 1912)
                   Glossophaga soricina                  3    2.1
                   (Pallas, 1976)
                   Carollia perspicillata                49   35
                   (Linnaeus, 1758)
                   Carollia brevicauda (Schinz, 1821)    4    2.9
                   Sturnira lilium (E. Geoffroy, 1810)   7     5
                   Dermanura anderseni (Miller, 1902)    1    0.7
                   Artibeus planirostris (Spix, 1823)    20   14
                   Artibeus lituratus (Olfers, 1818)     7     5
                   Uroderma bilobatum (Peters, 1866)     1    0.7
                   Desmodus rotundus                     16   11
                   (E. Geoffroy, 1810)

Vestertilionidae   Eptesicus brasiliensis                1    0.7
                   (D'Orbigny and Gervais, 1847)
                   Myotis albescens                      1    0.7
                   (E. Geoffroy, 1806)
                   Myotis riparius (Handley, 1960)       2    1.4

Molossidae         Molossus rufus (Geoffroy, 1805)       15   11

Table 2

Parasitic associations found in this study.

Hosts               N    A   B    C    D    A+D   A+B+C

A. planirostris    20    2   2    7    2     0      0
A. lituratus        7    0   0    5    4     0      0
C. brevicauda       4    0   0    0    5     0      0
C. perspicillata   49    0   0    0    25    0      0
D. rotundus        16    3   7    5    9     1      1
E. brasliensis      1    0   1    0    0     0      0
G. soricina         1    0   0    0    1     0      0
L. silvicolum       1    0   1    0    0     0      0
M. rufus           15    3   1    0    0     0      0
M. albescens        1    0   0    1    0     0      0
N. albivetris       1    1   0    0    0     0      0
P. hastatus         1    0   0    1    1     0      0
S. lilium           7    0   0    2    2     0      0
Total              124   9   12   21   49    1      1

Hosts              A+B+D   B+C   B+D   B+C+D   C+D

A. planirostris      0      1     0      0      1
A. lituratus         0      0     0      0      1
C. brevicauda        0      0     0      0      0
C. perspicillata     0      0     0      0      0
D. rotundus          1      1     3      2      0
E. brasliensis       0      0     0      0      0
G. soricina          0      0     0      0      0
L. silvicolum        0      0     0      0      0
M. rufus             0      0     0      0      0
M. albescens         0      0     0      0      0
N. albivetris        0      0     0      0      0
P. hastatus          0      0     0      0      1
S. lilium            0      0     0      0      0
Total                1      2     3      2      3

n = total number of hosts. A. Argasidae - A. B. Macronyssidae - C.
Spinturnicidae - D. Streblidae - A + D. Argasidae + Streblidae
(if found at the same time).

Table 3
Bat fly associations found in this study.

                                                       Sex ratio

Hosts           N    nP   Parasites                     [male]/

Artibeus        20   2    Megistopoda aranea             0.50

Artibeus        7    2    Aspidoptera phyllostomatis     1.00
lituratus            2    Megistopoda aranea             3.00

Carollia        4    1    Mastoptera minuta              0.00
brevicauda           1    Strebla guajiro                0.00
                     2    Trichobius joblingi            0.60

Carollia        49   3    Speiseria ambigua              0.33
perspicillata        1    Strebla guajiro                0.00
                     22   Trichobius joblingi            0.77

Desmodus        16   9    Trichobius parasiticus         1.21

Glossophaga     3    1    Trichobius uniformis           0.00

Phyllostomus    1    1    Trichobius longipes            0.50
hastatus             1    Mastoptera guimaraesi          1.69

Sturnira        7    3    Megistopoda proxima            2.00


Hosts           N    nP   N     %     P(%)  MI

Artibeus        20   2    3    100    10    1.5

Artibeus        7    2    2    33.3   29    1
lituratus            2    4    66.7   29    2

Carollia        4    1    1    10     25    1
brevicauda           1    1    10     25    1
                     2    8    80     50    4

Carollia        49   3    4    6.9    6     1.3
perspicillata        1    1    1.7    2
                     22   53   91.4   45    2.4

Desmodus        16   9    53   100    56    5.8

Glossophaga     3    1    1    100    33    1

Phyllostomus    1    1    3    7.9    100   3
hastatus             1    35   92.1   100   35

Sturnira        7    3    3    100    43    1

nP = number of parasitized hosts, N = number of collected
parasites, P (%) = Prevalence, MI = mean intensity

Table 4
Spinturnicid mite associations found in the study.

Hosts          N    nP           Parasites               P

                                                      N     %

Artibeus       20   3    Periglischrus iheringi       2    100

Artibeus       7    2    Periglischrus iheringi       0     0

Desmodus       16   5    Periglischrus herrerai       0     0

Myotis         1    1    Spinturnix americanus        0     0

Phyllostomus   1    1    Periglischrus acutisternus   10   100
hastatus       1    1    Periglischrus torrealbai     0     0

Sturnira       7    2    Periglischrus ojasti         0     0

Hosts          N    P[male]    [male]    [female]

                    N    %    N     %    N    %

Artibeus       20   0    0    14   100   3   100

Artibeus       7    2   100   9    100   4   100

Desmodus       16   0    0    9     0    0    0

Myotis         1    0    0    4     0    0    0

Phyllostomus   1    0    0    0     0    0    0
hastatus       1    0    0    9    100   2   100

Sturnira       7    0    0    8    100   7   100

Hosts          N    Total   P(%)   MI

Artibe us       20    19      20    6.33

Artibeus       7     15      30    7.5

Desmodus       16     9      30    1.8

Myotis         1      4     100     4

Phyllostomus   1     10     100     10
hastatus       1     11     100     11

Sturnira       7     15      30    7.5

nP = number of parasitized hosts, P = protonymph,
P[male] = protonymph female, P (%) = Prevalence, MI = mean intensity

Table 5
Macronyssid mite associations found in the study

Hosts                   N    nP

Artibeus planirostris   20   2
Desmodus rotundus       16   8
Eptesicus brasilensis   1    1
Lophostoma silvicolum   1    1
Molossus rufus          15   1

Parasites                      p       [female]   Total     P     MI
                             N    %    N    %               (%)

Macronyssoides conciliatus   0    0    4   100       4      10    2
Radffordiella desmodi       34   100   6   100       40     50    5.71
Steatonyssus occidentalis    8   100   1   100       9     100    9
Parichoronyssus bakeri       0    0    2   100       2     100    2
Macronyssoides cociliatus    0    0    3   100       3     6.7    3

nP = number of parasitized hosts, P = protonymph, P (%) = Prevalence,
MI = mean intensity

Table 6
Argasid tick associations found in the study

Hosts                   N    nP

Artibeus planirostris   20   2
Desmodus rotundus       16   1
                        16   2
Molossus rufus          15   3
Myotis albescens        1    1
Noctilio albiven        1    1

Parasites                 L   Total   P(%)   MI
                     N    %

Ornithodoros hasel   8    0   8    10    4
Ornithodoros hasel   5    0   5    10    5
O. pavloskiella      14   0   14   10    7
Ornithodoros hasel   5    0   5    20    1.7
Ornithodoros hasel   1    0   1    100   1
Ornithodoros hasel   11   0   11   100   11

nP = number of parasitized hosts, larvae L = P (%) = Prevalence,
MI = mean intensity
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Title Annotation:texto en ingles
Author:del Pilar Tarquino-Carbonell, Andrea; Gutierrez-Diaz, Karina A.; Galindo-Espinosa, Emma Y.; Reinoso-
Publication:Mastozoologia Neotropical
Date:Dec 1, 2015
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