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Introduction
Mites of the family Ascidae (Order: Mesostigmata) are commonly found on birds, with over 22 genera and 60 species having been identified (NASKRECKI; COLWELL, 1998). This group includes four genera of nasal mites:Lasioseius Berlese 1916, Proctolaelaps Berlese 1923, Rhinoseius Baker and Yunker 1964 andTropicoseius Bayer and Yunker 1964 (O'CONNOR et al., 1991; PROCTOR; OWENS, 2000; DUSBÄBEK et al., 2007).
Nasal mites are dispersed via a mechanism known as phoresis (Greekphore = to take) (PROCTOR; OWENS, 2000), whereby the temporal association between a mite phoronte and a bird appears to suggest a functional relationship (BAKER; YUNKER, 1964; HOFFMANN, 1996). According to MacChioni (2007), there are at least four types of phoreses classified by relation to the surface of the host, state of quiescence, recognition of signals to depart an individual host and, in some cases, synchronization with the life cycle of the host. In this relationship, plants act as a transitory habitat, while birds act as a means of transportation and dispersion but not as hosts for their reproduction (HUNTER, 1972; GUERRA et al., 2010).
Mites of the Ascidae family feed on pollen during the nymphal stage and on nectar during the adult stage (HUNTER, 1972). This food preference is considered to be relatively high, impinging on the food supply of nectarivorous birds and the duration of bird overflights and negatively impacting ornithophilous plant propagation (HEYNEMAN et al., 1991; LARA; ORNELAS, 2001;VELÁSQUEZ; ORNELAS, 2010). As a result, the co-specialization of the mite - hummingbird system is a negative interaction in terms of energy for birds (COLWELL, 1995).
The colonization of hummingbirds by nasal mite species has been reported in several Latin American countries (BAKER; YUNKER, 1964; DUSBÄBEK; ČERNÝ, 1970; HUNTER, 1972; FAIN et al., 1977; HYLAND, 1978; COLWELL; NAEEM, 1979; FAIN; HYLAND, 1980; MICHERDZINSKI; LUKOSCHUS, 1980; O'CONNOR et al., 1991; OHMER, 1991; NASKRECKI; COLWELL, 1998; DUSBÄBEK et al., 2007); however, few studies have considered the hummingbird species as a carrier. In this study, we describe the frequency of presentation of nasal mites on hummingbirds in the Andean region of Colombia and evaluate the degree of association between mite and hummingbird species.
Materials and Methods
This research was performed in a forest plantation located in Chinchiná, Caldas, Colombia, with an extension of 43 hectares along the Central Cordillera of the Colombian Andes (05° 03′ 32″ N and 75°44′ 07.6″ O) that is forested with native species (Cupania americana,Cedrela odorata, Aegiphila grandis andCordia alliodora) at an altitude of 825-1025 m.a.s.l and has an average temperature of 22.5 °C and an annual rainfall of 2245 mm.
Five samplings were carried out in April, May, July, August, and September of 2006, with June omitted due to logistical problems. The hummingbirds were captured using mist nets (12 × 2.5 × 0.036 m) located 100 meters from the edge of the plantation (capture effort 360 hours/month) that divided the study area into 40 plots. The birds were identified by a unique combination of color bands and classified according to the system developed by Remsen et al. (2013). Before the birds were released, the following capture variables were registered: date; plot; species; age (immature, adult and unknown), sex (male, female, unknown); reproductive variables, including brood patches (absent, loss of feathers, vascularized, wrinkled, moult, unknown) and protuberance (none, small, medium, large, unknown); and morphometric variables, including exposed culmen, total culmen, beak length, beak width and weight as described by the manual for monitoring birds proposed by Ralph et al. (1996).
Nasal mites were collected directly from the nostrils of birds with the aid of a fine brush (000) and were deposited into 70% ethanol in glass flasks. Mites were maintained in Entellan® following diaphanization via treatment with 10% KOH and drying at 30 °C for 24 hours (HENDERSON, 2001). Morphological characteristics related to gnathosoma, idiosoma and chaetotaxy were examined via optical microscopy at various magnifications (10X, 40X, 100X) and were used for identification according to the keys proposed by O'Connor et al. (1991) and Naskrecki and Colwell (1998). Each specimen was analyzed for 25 chaetotaxic characters. Morphometric changes in dorsal plate length (DPL), dorsal plate width (DPW) and setae z5 length (z5) were obtained and expressed as mean values (mm) and standard deviation (DS) (SILVA et al., 2009). The material deposited for reference in the laboratory of Veterinary Parasitology at the University of Caldas.
The data were processed in Excel, and the results were subsequently analyzed using the SPSS 19 package for contingency tables and the Pearson correlation test (p 0.05 and 0.001). For the morphometric variables, major components analysis was performed.
Results
Over the course of five months, 124 captures and 54 recaptures were performed for 178 hummingbirds spanning eight species (Amazilia saucerrottei, A. tzacatl, Chalybura buffonii, Chlorostilbon mellisugus, Florisuga mellivora, Glaucis hirsutus, Phaethornis guy and P. striigularis). Nasal mites were observed in 25.8% of the captured birds (46/178), as illustrated in Table 1.
Table 1. Number of hummingbirds captured each month during april - september 2006 in Colombia. The number of hummingbirds with nasal phoretic mites is in brackets.
| Species of hummingbird | April | May | July | August | September | Subtotal |
|---|---|---|---|---|---|---|
| Amazilia saucerrottei | 0 (0) | 9 (0) | 35 (14) | 0 (0) | 0 (0) | 44 (14) |
| Amazilia tzacatl | 1 (0) | 2 (0) | 1 (1) | 0 (0) | 0 (0) | 4 (1) |
| Chalybura buffonii | 18 (1) | 9 (0) | 17 (5) | 2 (0) | 7 (2) | 53 (8) |
| Chlorostilbon mellisugus | 1 (0) | 2 (0) | 10 (3) | 2 (0) | 0 (0) | 15 (3) |
| Florisuga mellivora | 1 (0) | 3 (0) | 3 (1) | 0 (0) | 0 (0) | 7 (1) |
| Glaucis hirsutus | 0 (0) | 1 (0) | 2 (2) | 0 (0) | 0 (0) | 3 (2) |
| Phaethornis guy | 3 (0) | 7 (0) | 7 (6) | 3 (2) | 2 (2) | 22 (10) |
| Phaethornis striigularis | 8 (0) | 2 (0) | 13 (2) | 3 (2) | 4 (3) | 30 (7) |
| Total | 32 (1) | 35 (0) | 88 (34) | 10 (4) | 13 (7) | 178 (46) |
The highest proportion of nasal mites (74%) was observed in July, coinciding with the frequent capture of A. saucerrottei(41.2%), P. guy (17.7%) and C. buffonii (14.7%) hummingbirds (Table 1). This relationship between mite and hummingbird species establishes a generalist dispersion pattern for Rhinoseius rafinskii and Tropicoseius uniformis mites, while specificity for host transporter was observed among Proctolaelaps rabulatus, R. luteyni, R. richardsoniand R. tiptoni (Table 2).
Table 2. Frequency of nasal phoretic mites and mite-hummingbird species relationship collected in an Andean forest from Colombia.
| Phoretic nasal mite | Mite species per hummingbird species | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Genera | Species | Femalee | Male | As | At | Cb | Cm | Fm | Gh | Pg | Ps |
| Proctolaelaps | rabulatus | 0 | 1 | 1 | |||||||
| Rhinoseius | caucaensis | 3 | 2 | 1 | 2 | 1 | 1 | ||||
| luteyni | 1 | 0 | 1 | ||||||||
| rafinskii | 25 | 2 | 8 | 4 | 3 | 2 | 8 | 2 | |||
| richardsoni | 0 | 1 | 1 | ||||||||
| tiptoni | 0 | 1 | 1 | ||||||||
| Tropicoseius | berryi | 9 | 5 | 5 | 1 | 2 | 2 | 4 | |||
| chazdonae | 3 | 0 | 1 | 1 | 1 | ||||||
| colwelli | 0 | 2 | 1 | 1 | |||||||
| erro | 6 | 0 | 1 | 1 | 1 | 1 | 2 | ||||
| uniformis | 18 | 2 | 5 | 2 | 3 | 1 | 1 | 4 | 4 | ||
| Total | 65 | 16 | 22 | 2 | 13 | 9 | 1 | 4 | 17 | 13 | |
Amazilia saucerrottei (As), Amazilia tzacatl (At), Chalybura buffonii (Cb),Chlorostilbon mellisugus (Cm),Florisuga mellivora (Fm), Glaucis hirsutus (Gh), Phaethornis guy (Pg),Phaethornis striigularis (Ps).
The eighty-one nasal mite specimens identified were classified as belonging to three genera: Tropicoseius (55.6%),Rhinoseius (43.2%) and Proctolaelaps(1.2%). R. rafinskii was the most abundant species (27/81), followed by T. uniformis (20/81) and T. berryi(14/81) (Table 2.). This study is the first report on the colonization of hummingbirds in Columbia by seven different species of nasal mites: P. rabulatus, R. luteyni, R. rafinskii, T. berryi, T. colwelli,T. erro and T. uniformis. Additionally, this report presents five cases of hyperphoresy by an unidentified mite that was transported by P. rabulatus, R. rafinskii andT. uniformis nasal mites.
Statistical analyses of the variables using the Pearson correlation test demonstrated associations between the presence of mites, plot (p= 0.05) and date of collection (p = 0.000) (Table 3). Mites were most frequently observed during the month of July (34/81). Although the condition of the feathers of the pectoral muscle "brood patches" (a variable of reproductive type) showed a positive association with the presence of mites (p = 0.016), birds lacking brood patches (absent) were more frequently transporters of mites (26/46) than individuals of the same sex and age.
Table 3. Capture, reproductive and morphometric variables related to the presence of nasal phoretic mites of hummingbirds in Colombia.
| Bird Variables | Number | Presence of nasal mites N (%) |
|---|---|---|
| Capture variables | ||
| Plot* | 178 | 46 (25.8) |
| Date** | ||
| April | 32 | 1 (3.1) |
| May | 35 | 0 (0.0) |
| July | 88 | 34 (38.6) |
| August | 10 | 4 (40.0) |
| September | 13 | 7 (53.9) |
| Capture | ||
| First capture | 124 | 35 (28.2) |
| Recapture | 54 | 11 (20.4) |
| Age | ||
| Immature | 8 | 3 (37.5) |
| Adult | 32 | 10 (31.3) |
| Unknown | 138 | 33 (23.9) |
| Sex | ||
| Female | 60 | 14 (23.3) |
| Male | 63 | 13 (20.6) |
| Unknown | 55 | 19 (34.6) |
| Reproductive variables | ||
| Brood patches * | ||
| Absent | 110 | 26 (23.6) |
| Loss of feathers | 15 | 9 (60.0) |
| Vascularized | 9 | 3 (33.3) |
| Wrinkled | 10 | 4 (40.0) |
| Moult | 1 | 0 (0.0) |
| Unknown | 33 | 4 (12.1) |
| Protuberance | ||
| None | 100 | 28 (28.0) |
| Small | 12 | 2 (16.7) |
| Medium | 20 | 8 (40.0) |
| Large | 13 | 4 (30.8) |
| Unknown | 33 | 4 (12.1) |
| Morphometric variables | ||
| Exposed culmen | 147 | 43 (29.3) |
| Total culmen | 137 | 42 (30.7) |
| Beak length | 147 | 43 (29.3) |
| Beak width | 147 | 43 (29.3) |
| Weight | 79 | 15 (19.0) |
Pearson correlation * p < 0.05; ** p < 0.001.
There was no statistical association between bird and mites species, although it was clear that both hummingbirds and nasal mites showed significant differences in their distributions between the plots studied (p = 0.026 and 0.050). In the case of birds, A. saucerottei, C. buffoni, P. guy and P. striigulariswere present in most plots, while A. tzacatl, C. mellisugus, F. mellivora and G. hirsutus were restricted to a subset of plots (Figure 1). Although the R. rafinskii,T. berryi and T. uniformis mite species were found in the majority of the plots, other mite species exhibited localized distribution (Figure 2). Sexual dimorphism among nasal mites was evident, and the females were more widely distributed across the plots than were males (Figure 2).
Figure 1. Spatial distribution of hummingbirds collected in a forest plantation in Colombia. Amazilia saucerrottei (As),Amazilia tzacatl (At), Chalybura buffonii (Cb), Chlorostilbon mellisugus(Cm), Florisuga mellivora (Fm), Glaucis hirsutus (Gh), Phaethornis guy (Pg),Phaethornis striigularis (Ps).
Figure 2. Nasal phoretic mite species collected in a forest plantation in Colombia. Proctolaelaps rabulatus (Pr),Rhinoseius caucaensis (Rc), Rhinoseius luteyni (Rl), Rhinoseius rafinskii (Rra),Rhinoseius richardsoni (Rri), Rhinoseius tiptoni (Rt), Tropicoseius berryi (Tb),Tropicoseius chazdonae (Tch), Tropicoseius colwelli (Tco), Tropicoseius erro (Te),Tropicoseius uniformis (Tu).
In total, 65 female and 16 male nasal mites were analyzed for at least nine and at most 25 chaetotaxic characteristics, resulting in their classification into three genera and eleven species. In addition, measurements were obtained for DPL, DPW and z5, the median values of which are presented in Table 4. These morphometric characteristics were not sufficient for differentiation between species, as indicated in Figure 3. The set of morphological characters related to gnatosoma, idiosoma and chaetotaxic characteristics were fundamental to the identification of nasal mites, but the morphometric variables (DPL, DPW and z5) did not facilitate differentiation.
Figure 3. 3-D dispersion graphic for analyses of major components (DPL, DPW and z5) of nasal phoretic mites recovered from hummingbirds in Colombia.
Table 4. Mean values and standard deviation of dorsal plate length (DPL), dorsal plate width (DPW) and setae z5 long (z5) for nasal mites recovered from hummingbirds in Colombia.
| Species of nasal mite | Male | Female | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| DPL | DPW | z5 | DPL | DPW | z5 | |||||||
| Mean (µm) | SD | Mean (µm) | SD | Mean (µm) | SD | Mean (µm) | SD | Mean (µm) | SD | Mean (µm) | SD | |
| Proctolaelaps rabulatus | 349.4 | 232.2 | ||||||||||
| Rhinoseius caucaensis | 372.6 | 9.55 | 202.8 | 0.00 | 71.2 | 11.10 | 434.5 | 18.46 | 294.6 | 37.98 | 59.3 | 7.85 |
| Rhinoseius luteyni | 415.0 | 192.6 | 67.7 | |||||||||
| Rhinoseius rafinskii | 434.6 | 322.9 | 80.4 | 437.7 | 45.51 | 275.8 | 55.10 | 72.1 | 17.54 | |||
| Rhinoseius richardsoni | 371.3 | 202.0 | 61.4 | |||||||||
| Rhinoseius tiptoni | 376.4 | 194.7 | 87.8 | |||||||||
| Tropicoseius berryi | 387.7 | 51.07 | 262.5 | 45.51 | 57.8 | 24.30 | 455.4 | 61.47 | 315.7 | 63.64 | 62.3 | 30.31 |
| Tropicoseius chazdonae | 425.8 | 63.33 | 268.8 | 28.57 | 49.9 | 38.61 | ||||||
| Tropicoseius colwelli | 437.0 | 18.24 | 269.0 | 29.27 | ||||||||
| Tropicoseius erro | 548.2 | 157.32 | 289.7 | 42.51 | 68.1 | 30.19 | ||||||
| Tropicoseius uniformis | 399.9 | 4.88 | 212.1 | 44.05 | 54.2 | 421.7 | 33.99 | 256.8 | 52.02 | 60.1 | 20.03 | |
Discussion
Few studies provide information about the mite - hummingbird relationship. In southern Colombia, studies by Fain and Hyland (1980) and Ohmer et al. (1991) registered a total of 16 species of phoretic mites present in the nostrils of twenty species of hummingbirds. Our results for the Andean region of this country show the presence of seven mite species (P. rabulatus,R. luteyni, R. rafinskii, T. berryi, T. colwelli, T. erro andT. uniformis). These new records are of great value, as they strengthen the understanding of these mites and their relationships with birds.
Observations made by O'Connor et al. (1991, 1997) of P. guy and by Colwell (1979) ofG. hirsutus indicate that a single bird may carry different nasal phoretic mite species. This observation was also made in the present work forR. rafinskii and T. uniformis, confirming that phoresis is a determining factor in the dispersion of mites.
Other studies developed by O'Connor et al. (1991) and Guerra et al. (2010) describe P. rabulatus species as exclusive flower mites of the Apocynaceae and Bromeliaceae families. Baker and Yunker (1964) previously documented T. braziliensis, T. peregrinator and T. erro mites in bromelia flowers from Brazil and Mexico and T. venezuelensis and T. heliconiae inHeliconia bracts (Venezuela and Panama) andHeliconia cuttings (Colombia). In Brazil, T. braziliensis mites were rediscovered and redescribed asRhinoseius braziliensis based on their presence in bromeliads (FLECHTMANN; JOHNSTON, 1978). The authors of these works suggest that birds such as hummingbirds do not act as carriers for mites. However, our identification of P. rabulatus as phoretic nasal mites of P. guy hummingbirds is of great value, as it contradicts the hypotheses formulated in previous studies; however, further observations to establish the true role of hummingbirds as P. rabulatus phorontes are needed.
Although no statistical associations were observed between variables related to morphometric aspects of the birds and the presence of mites, this study did find an association between phoresis and the reproductive variable "brood patches". The impact of phoretic mites on the reproductive development of their host birds remains unknown.
Colwell (1973, 1986) suggests that, under favorable weather conditions, nasal mite populations in a plantation are determined by two main factors: rapid reproduction within flowers and the ease of movement of female mites between inflorescences. In this study, the phenomenon of dispersion was evident during the month of July, when there was an increase in floral supply following an increase in precipitation. These are ideal conditions for an increase nasal mite, which is facilitated by dispersion via at least three of the eight species of hummingbirds (A. saucerrottei, P. guy and C. buffonii) (CASTAÑO et al., 2008).
Consistent with previous work, we identified several species of mites from a single hummingbird. Moreover, the species of birds (A. saucerrottei, P. guy and C. buffonii), their observed habitat specificity and their territorial foraging behavior are likely to have facilitated the spread of mites within the area studied. Female nasal mites were collected in the majority of the plots visited, as was demonstrated statistically.
