Phoretic dispersal on bumblebees by bromeliad flower mites (Mesostigmata, Melicharidae) T. J. Guerra, G. Q. Romero, J. C. Costa, A. C. Lofego & W. W. Benson
Insectes Sociaux International Journal for the Study of Social Arthropods ISSN 0020-1812 Volume 59 Number 1 Insect. Soc. (2012) 59:11-16 DOI 10.1007/s00040-010-0091-4
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Author's personal copy Insect. Soc. (2012) 59:11–16 DOI 10.1007/s00040-010-0091-4
Insectes Sociaux
RESEARCH ARTICLE
Phoretic dispersal on bumblebees by bromeliad flower mites (Mesostigmata, Melicharidae) T. J. Guerra • G. Q. Romero • J. C. Costa A. C. Lofego • W. W. Benson
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Received: 28 August 2009 / Revised: 28 December 2009 / Accepted: 17 March 2010 / Published online: 2 April 2010 Ó International Union for the Study of Social Insects (IUSSI) 2010
Abstract Nectarivorous flower mites (Mesostigmata: Melicharidae) live mostly on hummingbird-pollinated plants in the New World. We observed Proctolaelaps sp. living on Neoregelia johannis (Bromeliaceae) in a coastal rain forest site in south-eastern Brazil. Flower anthesis of this bromeliad lasted a single day. We recorded mites moving into, feeding from, presumably mating and reproducing, and exiting bromeliad flowers within just a single day. We observed three ant species predating flower mites on bromeliads. The main visitor was the bumblebee Bombus morio, which always landed on the inflorescence to access nectar inside the bromeliad flowers. We found Proctolaelaps sp. mites on 47% of 38 bumblebees inspected, with each Bombus hosting 2 mites on average; only adults and mostly female mites (93%) usually found on the bumblebees’ gula region of the head. This is the first study to document nectarivorous flower mites living on a melittophilous host plant using bumblebees for phoretic dispersal. Keywords Bumblebees Flower mites Bromeliaceae Atlantic Forest Phoresy
T. J. Guerra (&) J. C. Costa W. W. Benson Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), C.P. 6109, Campinas, SP 13083-970, Brazil e-mail:
[email protected] G. Q. Romero A. C. Lofego Departamento de Zoologia e Botaˆnica, IBILCE, Universidade Estadual Paulista (UNESP), Sa˜o Jose´ do Rio Preto, SP CEP 15054-000, Brazil
Introduction The hummingbird flower mites (Acari: Mesostigmata: Melicharidae), formerly included in the Ascidae (Krantz and Walter, 2009), comprise a well-known ecological group which lives, mates and feeds mostly on ornithophilous host plants, being found from USA to Argentina and Chile (Colwell and Naeem, 1994). They are mainly nectarivorous and also feed on pollen, but flowers constitute an ephemeral habitat and due to their limited dispersal ability, a key step in their life cycle is phoresy on pollinators to colonize new hosts (Colwell, 1985). Hummingbird flower mites comprise more than 50 species distributed in four genera: Proctolaelaps Berlese, Rhinoseius Baker & Yunker, Tropicoseius Baker & Yunker, and Lasioseius Berlese, and almost all nectarivorous species in these genera were recovered from nostrils of hummingbirds (Baker and Yunker, 1964; O’Connor et al., 1991; Dusbabek et al., 2007). However, many species in the genera Proctolaelaps and Lasioseius are not nectarivorous or inhabitants of flowers, even though some species also use insects for phoretic dispersal (Krantz and Walter, 2009). Some Neotropical flower mites live in plants pollinated by butterflies (Boggs and Gilbert, 1987) and bats (Tschapka and Cunningham, 2004), using these animals for phoretic dispersal. Similar association occurs in the Ameroseiidae, where members of Afrocypholaelaps and Neocypholaelaps live in flowers and are phoretic on honey bees in Australia and Asia (Seeman and Walter, 1995; Ramanan and Ghai, 1984). Nearly 100 plant taxa in 17 dicot and 8 monocot families host these flower mites in Neotropical region (Colwell, 1979; Naskrecki and Colwell, 1998), including at least seven genera of hummingbirdpollinated bromeliads: Aechmea, Gravisia, Guzmania, Pitcarnia, Puya, Tillandsia and Canistrum (Colwell 1979;
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Garcia-Franco et al., 2001; Lara and Ornelas, 2002; Siqueira-Filho and Machado, 2001). Although some Atlantic Forest bromeliads are pollinated by bumblebees (Araujo et al., 2004; Canela and Sazima, 2005), we found no report of flower mites on these species. Nevertheless, to our knowledge there is no case of a nectarivorous mite living on a melittophilous host plant in the neotropical region, nor any reported phoresy of flower mites on bumblebees. While studying the flower biology of Neoregelia johannis (Bromeliaceae) at a lowland Atlantic Forest site in southeastern Brazil, we observed bumblebees as the main flower visitors to this bromeliad. Indeed, we also found the flower mite Proctolealaps sp. (Melicharidae, Ascoidea) utilizing bromeliad flowers and inflorescences as habitat, which led us to hypothesize phoretic dispersal on bumblebees by flower mites. Here we report our observations on the natural history of this flower mite, including the daily pattern of host plant use, interactions with natural enemies and phoresy on bumblebees.
Materials and methods Study site We carried out this study between January and February in 2006 and 2007 at ‘‘Praia da Fazenda’’ located in the Parque Estadual da Serra do Mar (PESM), Nu´cleo Picinguaba, Sa˜o Paulo State, southeastern Brazil (23°220 S, 44°500 W, at sea level). The climate is wet tropical with an annual rainfall up to 2,600 mm and average temperature about 21°C with no well defined wet and dry seasons (data source: Instituto Agronoˆmico de Campinas, Campinas, Brazil). The study site is characterized by ‘‘restinga’’ lowland forest, a vegetation type related to plain areas near the sea with poor sandy soils, with trees reaching approximately 15 m, a dense understory and many epiphytes, especially bromeliads. Host plant Neoregelia johannis (Carrie`re) L.B. Smith. (Bromeliaceae) is a large bromeliad with leaves reaching up to one meter forming phytotelmata. In the study area this species occurred on trunks from near the ground to 10 m in the canopy, but was also abundant on the ground and close to the shoreline. Flowers of N. johannis are distributed on a large green strobiliform inflorescence which is mostly immersed within the phytotelmata. We observed this species blooming in January and February, during the period we stayed in the study site, but we did not determine plant phenology. This bromeliad has an inconspicuous greenish
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inflorescence from which may open each day up to seven flowers, usually in vertical position (Fig. 1a–c). Three white petals form an actinomorphic tubular corollas, measuring 20.6 ± 1.8 mm (range = 16.4–23.5, N = 18) from the internal base of corolla tube to flower mouth. Mouth diameter at anther height is 4.4 ± 0.5 mm (range 3.5–5.2, N = 14). Six stamens are included on petals, two per petal and the anthers are juxtaposed in the centre and dehisced outward. Flowers have one style in the centre and the stigma is located just below the stamens. Mite behaviour and phoresy on flower visitors In February 2006 and 2007 we randomly cut off one open flower of 19 and 53 reproductive plants, respectively, to search for mites inside them. Twenty fresh flowers infected with mites were longitudinally sliced for observation under a stereomicroscope to determine the position and behaviour of mites inside the flowers. We also marked 15 individual plants in 2007, recording mite movements over the day at 2-h intervals during entire anthesis. We recorded mite activities, including their interactions with other organisms found on plants (e.g., ants), and their location on eight focal plants over 14 h on 4 days, starting at 3:00 am before flower opening, during flower anthesis until approximately 17:00 pm after complete flower closing. In 2006, nine flowers with mites during anthesis were cut after they closed completely, placed in glass vials and then evaluated for the presence of mites. Another 20 flowers, one per plant, were collected around 12:00 h to count number of mites inside. We determined the frequency of flower visitors by performing direct observations in 2006 and 2007. We observed only inflorescences from terrestrial and epiphytic individuals growing only on heights less than 2 m, all located inside the Restinga Forest, on its edges along a sand road and close to the beach. We observed 1–4 neighbouring bromeliads simultaneously at distances of 5– 10 m for a period of 20 min, then moved to a another point 50–100 m distant. On each day we moved among 7–9 distinct observation points, always from 5:30 am to 12:30 pm. We considered as a sample each period of observation, calculating visitation frequency by dividing total number of visits by number of plants observed in each 20-min period. In January–February 2006 we made observations during 5 days in 42 periods (14 h) and in 60 periods (20 h) on 6 days in January–February 2007. We considered as a visit any approach in which a potential pollinator probed flowers touching the stigma and stamens to access nectar inside flowers. We captured bumblebees foraging on N. johannis during one day in February 2006 and on another day in February 2007. Captured bumblebees were frozen and then examined
Author's personal copy Flower mite phoresy on bumblebees
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Fig. 1 a The flower mite Proctolaelaps sp. (Melicharidae) on closing flowers of Neoregelia johannis (Bromeliaceae); b the ant Gnamptogenys sp. (Formicidae) preying on mites on fully opened flower; c Bombus morio (Apidae) landed on inflorescence feeding on nectar.
In detail pollen grains adhered to bumblebee’s tongue; d the flower mite Proctolaelaps sp. phoretic on bumblebee at Praia da Fazenda, South-eastern Brazil. (photos: a C.B. Araujo; b, c T.J. Guerra; d W.W. Benson)
under stereoscopic microscope to determine the presence and location of mites. We made slides with mites collected from bumblebees to determine the identity, sex and stage for comparison with those collected from flowers. To determine sex ratio of mites found on 20 flowers, we made slides with 20 adult mites selected without conscious bias. Flower mites were deposited in the Acari Collection of Departamento de Zoologia e Botaˆnica (DZSJRP-Acari, No 8.147–8.168), Universidade Estadual Paulista (UNESP), Campus de Sa˜o Jose´ do Rio Preto, Sa˜o Paulo, Brazil (http://splink.cria. org.br).
All flowers inspected had mites, and the number of mites per flower varied from 3 to 158 (mean ± SD, 41.1 ± 43.3, n = 20). Proctolaelaps sp. was observed mainly on not immersed parts of the inflorescences, mostly on bracts and sepals while flowers were still inside in the inflorescence from late afternoon until dawn. They were observed on fallen leaves and rosettes formed by host leaves, also utilizing these microhabitats as shelter during the afternoon and night. To reach partially immersed inflorescences, mites located on leaves were able to walk on the water surface. Daily 1–7 flowers emerge randomly at different parts of the inflorescence and mite behaviour was tightly adjusted to a 1-day flower anthesis pattern. Flowers emerge completely closed from inside the inflorescences around 4:00 am, well before sunrise which occurred approximately at 5:30 am. At this time, groups of mites start to climb closed flowers. When flowers begin to open after 5:00 am with a slow outward bending of its petal tips, and as soon as the flower opens mites start to enter. During anthesis most individuals of Proctolaelaps sp. stayed inside the flowers. In all slit opened flowers most mites were found at the
Results The mite Proctolaelaps sp. was the only species of mite inside flowers of N. johannis; larvae, deutonymphs, protonymphs, adult males and females occupied flowers. Among adult mites found on N. johannis flowers 90% were females (n = 20). These mites infested all 19 reproductive plants surveyed in 2006 and on 52 out of 53 plants in 2007.
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internal base of the corolla tube in contact with the nectar. Flowers were fully open at approximately 9:00 am, but then the petal tips reverse direction, moving inward and closing slowly till nearly 16:00 in the afternoon, when petals close completely. Just before this, there is a mass departure of mites from crowded flowers (Fig. 1a). Late in the afternoon closed flowers start to withdraw into the inflorescence. After moving out of the flowers, mites sheltered on inflorescences and bromeliad leaves again until next day flowers start to open. We found no mites inside closed flowers (n = 9). During mite observations we recorded three unidentified ant species (Formicidae) preying on Proctolaelaps sp.: Odontomachus sp. (n = 2), Gnamptogenys sp. (n = 7; Fig. 1b) and Solenopsis sp. (n = 4). When inside the flowers, mites seem to be protected from predation by the two largest ants, Odontomachus and Gnamptogenys, which cannot trespass anthers. However, the smaller Solenopsis can get inside flowers to capture mites. Three ant species were found inside slit-opened flowers with mites: Conomyrma sp. (n = 1), Azteca sp. (n = 1) and Solenopsis sp. (n = 5), but the former two are probably nectar thieves. The crab Armases rubripes (Grapsidae) was observed feeding on the inflorescences, taking pieces of petals (n = 4). These flowers were confirmed to have mites, but crabs stopped feeding when observers approached, and unfortunately it was not possible to verify if crabs ate flower mites with their meal. During observations in 2006 we recorded 136 visits by potential pollinators, but the bumblebee Bombus (Fervidobombus) morio (Swederus, 1787) (Apidae) were responsible for almost 99% of visits. We recorded a single visit by the hummingbird Ramphodon naevius Dummont (Throchilidae), also recorded visiting two plants outside focal observations. In 2007 we recorded 335 visits and bumblebees were also responsible for nearly 99% of visits. In 2007 we recorded three visits made by the hummingbird Thalurania glaucopis Gmelin (Throchilidae), but occasionally we also recorded the hummingbirds R. naevius and Amazilia sp. (Throchilidae). The bee Trigona fulviventris Gue´rin, 1835 (Apidae) were also observed in both years, but usually visiting few plants in groups of 3–6 individuals to steal pollen without feeding on nectar and touching the stigma. All bumblebees captured were female workers of B. morio. They started to visit plants very early in the morning just after sunrise, always accessing nectar inside the flowers. In 2006 bumblebees visited plants 4.6 times/h, more or less constantly through the flower anthesis. In 2007 bumblebees seemed to be much more abundant visiting plants 9.7 times/h, regularly through the morning until flowers were closed. Bumblebees generally probed all flowers in the inflorescence, sometimes the same flower more than once. Unlike hummingbirds that visit plants quickly while
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hovering, bumblebees always land on inflorescences, walking among flowers, inserting their long tongues between stamens with pollen grains, which usually sticks to the tongue and often touches the stigma (Fig. 1c). Bumblebees remain stationary for few seconds while feeding on nectar and this behaviour was favourable for mites to climb onto the bumblebee’s tongue and head. We found Proctolaelaps sp. mites on 47% of 38 bumblebees inspected, with each hosting 1.9 ± 0.32 (mean ± SD, n = 18) mites. We found only adults of Proctolaelaps sp. on bumblebees, with adult females comprising 93% of individuals collected. However, the fraction of females phoretic on bumblebees did not differ from expected by observed number of females on N. johannis flowers (Fisher exact test, one tailed, p = 0.54). In addition, we also found another three mite species on bumblebees’ bodies: 29 Pneumolaelaps sp. (Laelapidae) representing 72% adult females and 28% deutonymphs; 46 deutonymphs of an unidentified Astigmata; and 3 individuals of an unidentified Scutacaridae. Whereas 72% of Proctolaelaps sp. individuals were found on gula region in the head of bumblebees (Fig. 1d), 10% were found on the abdomen and 18% on the legs. In contrast, 87.5% of the Pneumolaelaps sp. were found on the abdomen and 12.5% in the legs. Similarly, most of the Astigmata found were on the abdomen (46.9%), and the remainders were found on the head (18.7%), wings (25%) and legs (9.4%). The Scutacaridae species was found exclusively on the thorax of bumblebees.
Discussion This Proctolealaps sp. has a life history typical of other flower-inhabiting mites. Individuals move into, feed from, presumably mate and reproduce, and exit flowers; all timed precisely within just a single day. The daily movements of Proctolaelaps sp. on N. johannis prevent individuals from being trapped inside flowers, which completely close entering back into inflorescences immersed in the water of the tank bromeliad. Similar behaviour occurs for nectarivorous flower mites found on hosts with 1-day flowers (Dobkin, 1984; Colwell 1985). We found all life stages, except eggs, inside flowers as expected for mites living on short lived flowers. The density of mites per flower was variable, reaching up to 160 individuals in a single flower. Variance and mean number of Proctolaelaps sp. on flowers are similar to other flower mite species found on ornithophilous hosts (Colwell and Naeem, 1994). Predation by ants is one factor that might regulate Proctolealaps sp. populations in N. johannis. At least three ant species were observed preying on these mites at Praia da Fazenda. Despite the commonness and diversity of ants and flower
Author's personal copy Flower mite phoresy on bumblebees
mites in tropical communities this seems to be the first report on this kind of interaction. The only report on flower mite predation found relates to an unidentified hemipteran bug which is supposed to be specialized predator of Rhinoseius spp. in Costa Rica (Colwell, 1973). This is the first study to report a flower mite species living on a melittophilous host plant and phoretic on bumblebees in the Neotropics. Many parasitic mite species are associated with bees (Krantz and Walter, 2009), but their role as phoretic agents of nectarivorous mites is poorly known (e.g., Seeman and Walter, 1995). Proctolaelaps is diverse in species and habits, is widespread worldwide, and includes many species associated with nests of bumblebees, birds and mammals, with beetles, but also found in decaying organic materials (Krantz and Walter, 2009). Indeed, some species are free-living predators that feed on small arthropods including other mites, nematodes, fungi, or pollen (Nawar, 1992). In New World at least 16 described species are supposedly nectarivorous and related to flowers of ornithophilous plants using hummingbirds for phoretic dispersal (Dusbabek et al., 2007). Nonetheless, phoresy on insects by nectarivorous species were reported only by Boggs and Gilbert (1987), who observed Proctolaelaps lobata living on flowers of Lantana (Verbenaceae) species, migrating seasonally between Mexico and Texas through phoresy on 15 butterfly species. Treat and Niederman (1967) found three species of Proctolaelaps on noctuid moths, but the use of flowers as habitat and nectarivorous diet of these mites are still unclear. Another exception to association with hummingbird plants is one unidentified flower mite found in a chiropterophilous palm in Costa Rica being phoretic on bat pollinators, but also phoretic on the herbivorous beetle Lagochile collaris (Scarabaeidae) that feed on flowers (Tschapka and Cunningham, 2004). We found more adult females than males phoretic on bumblebees. In fact, mated adult mated females are typically the phoretic life stage of mites in the Ascoidea group (Krantz and Walter, 2009). However, number of female mites phoretic on bumblebees corresponded to number expected by their relative abundance on flowers, indicating that males and females disperse through phoresy as readily as females. The position on bumblebees differed among nectarivorous and parasitic mites. Whereas nest mites were found mostly on bumblebee’s thorax and abdomen, the flower mite Proctolaelaps sp. was found mainly bees’ gula close to the tongue, which is presumably the easiest way to depart or arrive on flowers during nectar foraging by bumblebee. The other three mite species phoretic on B. morio are mites commonly associated with bumblebees’ nests (Eickwort, 1994; Royce and Krantz, 1989) and usually disembark within nests, although some nest-inhabiting mites will use flowers to transfer among foraging bumblebees
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(Schwarz and Huck, 1997) and honeybees (Ramanan and Ghai, 1984). Bombus morio was the most frequent flower visitor of N. johannis in Praia da Fazenda, thus acting as the main vector of Proctolaelaps sp. within the bromeliad population. This bumblebee is also a frequent flower visitor to Bromelia antiacantha (Canela and Sazima, 2005). This bromeliad species has features that attracts birds and bees, with nectar utilized by six hummingbird species and B. morio in Praia da Fazenda. In addition, B. morio was observed as the main pollinator of Aechmea gamosepala (Bromeliaceae), also feeding on nectar of ornithophilous bromeliads in Rio Verde estuary, an Atlantic Forest site also in Sa˜o Paulo state (Araujo et al., 2004). Our data seems to corroborate B. morio as an important flower visitor of bromeliads in Atlantic Forest in south-eastern Brazil. Indeed, we also found Proctolaelaps sp. inside flowers of B. antiacantha at the end of its blooming period in January 2007, and also inside flowers of Nidularium sp. (Bromeliaceae) at the end of N. johannis blooming in February 2007 at Praia da Fazenda. Our observations suggest that Proctolaelaps sp. is associated to bromeliad species at the study site. Indeed, most bromeliads in Atlantic Forest bloom for relatively short periods, with species flowering more or less sequentially through the year (Araujo et al., 2004). Therefore, phoresy on B. morio could play an important role on Proctolaelaps sp. population dynamics, promoting host plant colonization and switching throughout the year. Acknowledgments We thank G. Martinelli, C. Matos and F.S. Castro, for identification of bromeliad, bees and ants, respectively. We also thank one anonymous reviewer and R.K. Colwell for comments and suggestions on the manuscript. This work was conducted during Ecology Field Course totally supported by Programa de Po´s-Graduac¸a˜o em Ecologia at Universidade Estadual de Campinas, coordinated by W.W. Benson and A.V.L. Freitas. T.J. Guerra was supported by doctoral scholarship from CAPES. G.Q. Romero was supported by research grants from Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo (FAPESP, grants 04/13658-5 and 05/51421-0).
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