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Cocytius antaeus visits the "super ghost" cluster at Corkscrew Swamp Sanctuary, where a gecko awaits on the bald cypress trunk amongst the root mass of D. lindenii. Photo by Mac Stone.
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The structural variation of orchids enables myriad fascinating symbiotic relationships with organisms across kingdoms. Orchids are frequently known for having elaborate arms races with their pollinators that result in intricate morphologies in both parties, and flowers with long corollas hypothesized to be pollinated only by individual species of l...
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... were captured (22:16:39 hr), and on the last date in September, one image was recorded (02:31:09 hr). On August 23 rd , an individual of C. antaeus was recorded over the course of two minutes, with images captured at 23:15:15 hr (3), 23:15:46 hr (3), and 11:17:15 hr (3). On this occasion, a gecko was present on the trunk amongst the root mass (Fig. 3), which the moth approached and made contact using its proboscis. All individuals were males, and images of the visitation spanning 120 seconds appear to be of the same individual. Pollinia was not affixed to the moth on any of these three visitations, however, pollen from Ipomoea alba was visibly covering the head of the final two ...
Citations
... Pollination systems of tall forest trees are poorly studied, due to the difficulties in observing pollinator activity at the canopy level. Methods used to study pollination at crown height include using baited traps over tree branches (Roubik, 1993), elevated pan traps (Urban-Mead et al., 2021), camera trapping (Houlihan et al., 2019), canopy cranes (Inari et al., 2012), and rope climbing techniques (Rosa et al., 2013). Only the latter two enable direct observations of floral visitors and, thus, more reliable information of pollination. ...
Forest canopies provide important resources for insect communities via flowers.
Yet, pollination systems of tall forest trees are poorly studied, resulting from the
difficulties in observing pollinator activity at the canopy level and great temporal
variation in flower production. In temperate forest canopies of the southern hemisphere, small, whitish and generalist flowers seem to dominate. Here, we observed insect flower visitors, at the canopy level, to four southern Afrotemperate
forest tree species bearing small, white to green flowers in a large, indigenous forest. Additionally, we quantified flower traits and collected pollen from representative insect visitors.
We conclude that within generalist pollination systems, distinct and non-random mutualisms can develop between different species of plants and a diverse suite of
pollinators, and that floral traits could partially predict such interactions.
... Whereas camera traps could be used to monitor pollinator behavior in Orchidaceae, there are a few shortcomings in insect-pollinated taxa: 1) some camera models have a Macro function, but they are comparatively expensive, and 2) the identification of the pollinator species may be difficult without a good image resolution, and, depending on the insect group, impossible without a few insect vouchers (for example, species identification in some cases requires the examination of the genitalia in some insect groups, as in some groups of Diptera). Thus, camera traps alone don't seem advisable for orchids pollinated by insects, unless pollinators have already been identified and cameras are used complementarily (ex: to film and quantify orchid visits, behavior, permanency at flowers, etc.) (Houlihan et al. 2019). On the other hand, camera traps may be extremely useful for studying Orchidaceae pollinated by birds (Johnson & Van Der Niet 2019). ...
Orchids are globally threatened by habitat loss and poaching. In this context, we present suggestions to maximize the gathered scientific information without compromising the continuity of orchid populations: 1. To keep population coordinates in secrecy and avoid unnecessary or careless postings on social media; 2. To acquire and carry valid, working/collecting permits; 3. To make a complete photographic record of the orchid features before pressing the specimens; 4. Plant and insect (pollinators) vouchers are to be kept to the strictly necessary and must be deposited in accredited Herbaria and Entomological collections, respectively; 5. Orchid fruits for propagation purposes should be collected only when they are ripe enough, well-developed, and devoid of insects/illnesses. Recommendations to address all these methodological suggestions are presented. In particular, we advocate that it is completely unnecessary to kill (press) entire orchid specimens and provide instructions to properly voucher epiphytic and terrestrial orchids without pressing whole plants. The advantages of working in association with Living Orchid Collections held in Botanical Gardens or other Institutions are discussed. Only pollinarium-carrying insects are to be considered orchid pollinators and should be sampled in moderate numbers, for their identification by taxonomists. Appropriate techniques to record natural orchid pollination are also discussed.
... Hawkmoths are well known for foraging on nectar from flowers, often while hovering (Arditti et al., 2012;Houlihan et al., 2019;Johnson et al., 2017;Lees and Zilli, 2019;Miller, 1997;Raguso and Willis, 2003;Wasserthal, 1997). Hovering is one of the most metabolically expensive forms of locomotion (Haverkamp et al., 2016;Kammer and Heinrich, 1978). ...
Hovering hawkmoths expend significant energy while feeding, which should select for greater feeding efficiency. Although increased feeding efficiency has been implicitly assumed, it has never been assessed. We hypothesized that hawkmoths have proboscises specialized for gathering nectar passively. Using contact angle and capillary pressure to evaluate capillary action of the proboscis, we conducted a comparative analysis of wetting and absorption properties for 13 species of hawkmoths. We showed that all 13 species have a hydrophilic proboscis. In contradistinction, the proboscises of all other tested lepidopteran species have a wetting dichotomy with only the distal ∼10% hydrophilic. Longer proboscises are more wettable, suggesting that species of hawkmoths with long proboscises are more efficient at acquiring nectar by the proboscis surface than are species with shorter proboscises. All hawkmoth species also show strong capillary pressures which, together with the feeding behaviors we observed, ensure that nectar will be delivered to the food canal efficiently. The patterns we found suggest that different subfamilies of hawkmoths use different feeding strategies. Our comparative approach reveals that hawkmoths are unique among Lepidoptera and highlights the importance of considering the physical characteristics of the proboscis to understand the evolution and diversification of hawkmoths.
... In addition, little is known about their phorophyte associations. The ghost orchid is probably the only epiphytic orchid for which its pollinators 39,40 , fragrance composition 41 and host tree affinities 42 have been studied. Leafless D. lindenii is native to lowland forests in Florida and Cuba 42 . ...
... For a long time the giant sphinx (Cocytius antaeus, Sphingidae) was considered to be the sole pollinator of Dendrophylax lindenii as its proboscis is of comparable length to the corolla of D. lindenii 45 . Using remotely controlled cameras Houlihan et al. 39 revealed that it is also pollinated by the fig sphinx moth (Pachylia ficus, Sphingidae) and pawpaw sphinx moth (Dolba hyloeus, Sphingidae) in Florida 39,40 . The size and bark characteristics of the host (phorophyte) are important factor affecting the distribution of epiphytes. ...
... For a long time the giant sphinx (Cocytius antaeus, Sphingidae) was considered to be the sole pollinator of Dendrophylax lindenii as its proboscis is of comparable length to the corolla of D. lindenii 45 . Using remotely controlled cameras Houlihan et al. 39 revealed that it is also pollinated by the fig sphinx moth (Pachylia ficus, Sphingidae) and pawpaw sphinx moth (Dolba hyloeus, Sphingidae) in Florida 39,40 . The size and bark characteristics of the host (phorophyte) are important factor affecting the distribution of epiphytes. ...
The identification of future refugia for endangered species from the effects of global warming is crucial for improving their conservation. Because climate-driven shifts in ranges and local extinctions can result in a spatial mismatch with their symbiotic organisms, however, it is important to incorporate in niche modelling the ecological partners of the species studied. The aim of this study was to evaluate the effect of climate change on the distribution of suitable niches for the ghost orchid ( Dendrophylax lindenii ) and its phorophytes and pollinators. Thus, its five species of host trees and three pollen vectors were included in the analysis. Climatic preferences of all the species studied were evaluated. The modelling was based on three different climate change projections and four Shared Socio-economic Pathway trajectories. All the species analysed are characterized by narrow temperature tolerances, which with global warming are likely to result in local extinctions and range shifts. D. lindenii is likely to be subjected to a significant loss of suitable niches, but within a reduced geographical range, both host trees and pollen vectors will be available in the future. Future conservation of this orchid should focus on areas that are likely be suitable for it and its ecological partners.
... While work has been done on the biology of the ghost orchid -exodermis structure and its relationship to mycorrhizal fungi (Chomicki et al. 2014), desiccation tolerance (Coopman & Kane 2019), greenhouse acclimatization methods (Coopman & Kane 2018), and germination and seedling development (Hoang et al. 2017) -until recently little was known about its ecology (but see Mújica et al. 2018, Ray et al. 2012. Recent ecological studies have primarily focused on the orchid's population biology and pollinator ecology (Danaher et al. 2020, Houlihan et al. 2019, Mújica et al. 2021, Sadler et al. 2011, Zettler et al. 2019). This work examined a population of ghost orchids in Fakahatchee Strand Preserve State Park (FSPSP) in Collier County in southwest Florida to determine if ghost orchids in FSPSP exhibit host preference, vertical stratification, substrate diameter stratification, and a distribution pattern similar to that of their host plants. ...
This study examined a population of ghost orchids (Dendrophylax lindenii) in Fakahatchee Strand Preserve State Park in Collier County, Florida, to determine if they exhibit host species preference, vertical stratification, substrate diameter stratification, or a distribution pattern similar to their host plants. Twenty-five ghost orchids were found on three host plant species: 20 (80%) were on pop ash (Fraxinus caroliniana), four (16%) on arthritis vine (Hippocratea volubilis), and one (4%) on pond apple (Annona glabra). Our analysis indicated a statistically significant occurrence of ghost orchids on pop ash relative to other woody plant species in the study area. Although most orchids were found below 3 m from the forest floor, this was not statistically significant when compared to orchids above 3 m. A weak trend (p=0.06) for increasing occurrence was observed in the next to largest (14.1 cm to 17.2 cm diameter at breast height) size class among the five size classes of pop ash in this study. The spatial analyses indicated that both the stems of pop ash and ghost orchids demonstrate non-random clumping on the landscape. In addition, the presence of an individual orchid increases the probability of multiple ghost orchids on a stem. These results further emphasize the importance of pop ash as a host species in Florida’s ghost orchid populations and add to the list of hosts (arthritis vine) in the literature. Continuing to study the vertical position of ghost orchids will be important as climate change has the potential to alter humidity patterns and the occurrence of both low temperature events and hurricanes. Improved understanding of host plant preference, microhabitat requirements, spatial distribution, and continued long-term monitoring of population dynamics are critical for the conservation of the ghost orchid.
... This approach is likely to be highly effective in bird-pollinated orchids, particularly as most bird species can be identified from images alone. In addition, recent work has shown that these cameras can also be used to capture footage of some insect species (Micheneau et al., 2010;Danaher et al., 2019;Houlihan et al., 2019;Balducci, van der Niet & Johnson, 2020;Johnson et al., 2020;Lombardi et al., 2021), ideally using a camera with a short focal range. An exciting development is the use of Raspberry Pi computing systems as a cheap way of capturing footage of pollinators (Droissart et al., 2021). ...
Orchidaceae show remarkable diversity in pollination strategies, but how these strategies vary globally is not entirely clear. To identify regions and taxa that are data-rich and lend themselves to rigorous analyses or are data-poor and need attention, we introduce a global database of orchid reproductive biology. Our database contains > 2900 species representing all orchid subfamilies and 23 of 24 tribes. We tabulated information on habit, breeding systems, means of pollinator attraction and the identity of pollinators. Patterns of reproductive biology by habit, geography and taxonomy are presented graphically and analysed statistically. On the basis of our database, most orchid species sampled are pollinator dependent (76%) and self-compatible (88%). Pollinator attraction based on rewards occurs in 54% of the species, whereas 46% use some means of deceit. Orchids generally have highly specific pollinator interactions (median number of pollinator species = 1). Nonetheless, on average, specificity is lower for species offering rewards, occurring in multiple continental regions or Northern America (as defined by the Taxonomic Database Working Group Level 1 regions). Although our database reveals impressive knowledge gains, extensive gaps in basic observations of orchid reproductive biology exist, particularly in tropical regions and diverse lineages of fly-pollinated species. The database is expected to facilitate targeted studies, further elucidating the ecological and evolutionary drivers of orchid diversity. ADDITIONAL KEYWORDS: biogeography-breeding systems-floral deception-Orchidaceae-pollinator diversity-pollinator rewards-reproductive biology-sexual deceit.
... This approach is likely to be highly effective in bird-pollinated orchids, particularly as most bird species can be identified from images alone. In addition, recent work has shown that these cameras can also be used to capture footage of some insect species (Micheneau et al., 2010;Danaher et al., 2019;Houlihan et al., 2019;Balducci, van der Niet & Johnson, 2020;Johnson et al., 2020;Lombardi et al., 2021), ideally using a camera with a short focal range. An exciting development is the use of Raspberry Pi computing systems as a cheap way of capturing footage of pollinators (Droissart et al., 2021). ...
Orchidaceae show remarkable diversity in pollination strategies, but how these strategies vary globally is not entirely clear. To identify regions and taxa that are data-rich and lend themselves to rigorous analyses or are data-poor and need attention, we introduce a global database of orchid reproductive biology. Our database contains > 2900 species representing all orchid subfamilies and 23 of 24 tribes. We tabulated information on habit, breeding systems, means of pollinator attraction and the identity of pollinators. Patterns of reproductive biology by habit, geography and taxonomy are presented graphically and analysed statistically. On the basis of our database, most orchid species sampled are pollinator dependent (76%) and self-compatible (88%). Pollinator attraction based on rewards occurs in 54% of the species, whereas 46% use some means of deceit. Orchids generally have highly specific pollinator interactions (median number of pollinator species = 1). Nonetheless, on average, specificity is lower for species offering rewards, occurring in multiple continental regions or Northern America (as defined by the Taxonomic Database Working Group Level 1 regions). Although our database reveals impressive knowledge gains, extensive gaps in basic observations of orchid reproductive biology exist, particularly in tropical regions and diverse lineages of fly-pollinated species. The database is expected to facilitate targeted studies, further elucidating the ecological and evolutionary drivers of orchid diversity.
... Epiphytes inherently depend on other species as host plants and are often specialized to particular sites due to host characteristics, for example, bark rugosity, trunk diameter, or mycorrhizal associations Callaway et al., 2002;McCormick & Jacquemyn, 2014;S ayago et al., 2013;Yang et al., 2017;Zarate-García et al., 2020). Populations of epiphytes, orchids in particular, are considered as dynamic due to both their climate-sensitive physical positions that are prone to disturbance and specialized species interactions (Houlihan et al., 2019;Huston, 1994;Ravent os et al., 2015;Zuleta et al., 2016). This sensitivity makes epiphytic orchids indicative of tropical ecosystem health (Benzing, 1998;Zotz & Bader, 2009). ...
In a time of global change, having an understanding of the nature of biotic and abiotic factors that drive a species' range may be the sharpest tool in the toolbox of conservation and management of threatened species. However, such information are lacking for most tropical and epiphytic species due to the complexity of life history, the roles of stochastic events, and the diversity of habitat across the span of a distribution. In this study, we conducted repeated census across the core and peripheral range of Trichocentrum undulatum, a threatened orchid that is found throughout the island of Cuba (species core range) and southern Florida (the northern peripheral range). We used demographic matrix modeling and stochastic simulations to investigate the impacts of herbivory, hurricanes, and logging (in Cuba) on projected population growth rates (λ and λs) among sites. Our study indicates that the Florida population is under high extinction risk and most populations in the core range show less interannual variability, but, with the exception of one population, are also in decline. The peripheral population experienced higher herbivory damage than did the core populations, by a native inflorescence‐crippling fly, Melanagromyza miamensis, and an invasive, mortality‐triggered scale, Diaspis boisduvalii. The latter was found in the Florida population only. Hurricanes increased levels of mortality and had a negative effect on λ. However, λ increased following hurricane events due to increased recruitment and decreased herbivory. Life table response experiments suggest that higher adult survival was the largest contributor to the higher λ observed in the growing Cuba populations, as compared with the population in Florida. Logging simulations in Cuba indicate that populations can maintain stability only if selective logging of host trees occurs at low frequency. Reintroduction of the species in its northern peripheral habitat is needed to ameliorate the threats from sea‐level rise and invasive herbivorous insects to secure the current species' northern, continental range margin. Our study exhibits how vital rates and ecological interactions vary across a species distribution and respond under differing stochastic events.
... Therefore, it is no surprise that this group of Lepidoptera has received ongoing attention in insect science and has been mentioned in the earliest stages of evolutionary biology (Darwin, 1862;Müller, 1873). Today, Sphingidae are famous models for morphological co-adaptations of insects and flowers (e.g., Arditti et al., 2012;Miller, 1997;Nilsson, 1988Nilsson, , 1998Wasserthal, 1998), pollination biology (e.g., V. Grant & Grant, 1983;Houlihan et al., 2019;Johnson & Raguso, 2016;Nilsson et al., 1985), mutualistic insect-plant networks (Johnson et al., 2017;Sazatornil et al., 2016), sensory physiology of flower-visiting behavior (e.g., review Stöckl & Kelber, 2019), and biophysics of fluid-feeding (Kornev et al., 2017). Many Sphingidae are critical for the pollination of specialized sphingophilous flowers, where some plant species with particularly deep flowers depend on pollination by sphingid moths with a matching proboscis (e.g., V. Grant & Grant, 1983;Houlihan et al., 2019;Johnson et al., 2017;Nilsson, 1988;Wasserthal, 1997). ...
... Today, Sphingidae are famous models for morphological co-adaptations of insects and flowers (e.g., Arditti et al., 2012;Miller, 1997;Nilsson, 1988Nilsson, , 1998Wasserthal, 1998), pollination biology (e.g., V. Grant & Grant, 1983;Houlihan et al., 2019;Johnson & Raguso, 2016;Nilsson et al., 1985), mutualistic insect-plant networks (Johnson et al., 2017;Sazatornil et al., 2016), sensory physiology of flower-visiting behavior (e.g., review Stöckl & Kelber, 2019), and biophysics of fluid-feeding (Kornev et al., 2017). Many Sphingidae are critical for the pollination of specialized sphingophilous flowers, where some plant species with particularly deep flowers depend on pollination by sphingid moths with a matching proboscis (e.g., V. Grant & Grant, 1983;Houlihan et al., 2019;Johnson et al., 2017;Nilsson, 1988;Wasserthal, 1997). ...
... This feeding organ enables access to large quantities of nectar in big flowers, which in turn are needed to compensate the energyconsuming flight behavior. However, it was shown that longproboscid hawk moths are generalistic flower visitors (Haber & Frankie, 1989;Johnson et al., 2017;Miller, 1997) and the evolution of particularly long proboscises expands access to matching long nectar spurs in flowers of which some are specialized to use these insects as pollinators (Houlihan et al., 2019;Wasserthal, 1997). ...
The morphology of the proboscis and associated feeding organs was studied in several nectar‐feeding hawk moths, as well as a specialized honey‐feeder and two supposedly non‐feeding species. The proboscis lengths ranged from a few millimeters to more than 200 mm. Despite the variation in proboscis length and feeding strategy, the principle external and internal composition of the galeae, the stipes pump and the suction pump were similar across all species. The morphology of the smooth and slender proboscis is highly conserved among all lineages of nectar‐feeding Sphingidae. Remarkably, they share a typical arrangement of the sensilla at the tip. The number and length of sensilla styloconica are independent from proboscis length. A unique proboscis morphology was found in the honey‐feeding species Acherontia atropos. Here, the distinctly pointed apex displays a large subterminal opening of the food canal, and thus characterizes a novel type of piercing proboscis in Lepidoptera. In the probably non‐feeding species, the rudimentary galeae are not interlocked and the apex lacks sensilla styloconica; galeal muscles however, are present. All studied species demonstrate an identical anatomy of the stipes‐ and suction pump, regardless of proboscis length and diet. Even supposedly non‐feeding Sphingidae possess all organs of the feeding apparatus, suggesting that their proboscis rudiments might still be functional. The morphometric analyses indicate significant positive correlations between galea lumen volume and stipes muscle volume as well as the volume of the food canal and the muscular volume of the suction pump. Size correlations of these functionally connected organs reflect morphological fine‐tuning in the evolution of proboscis length and function. This article is protected by copyright. All rights reserved.
... This rare species exists as a leafless epiphyte in forests of South Florida and Western Cuba and yields a striking floral display consisting of fragrant white flowers with long (11-17 cm) nectar spurs. Recent studies have confirmed that D. lindenii is pollinated by hawk moths (Danaher et al., 2019;Houlihan et al., 2019) consistent with many other members of its subtribe (Angraecinae). Accordingly, we hypothesized that the sugars present in the nectar of D. lindenii would be the same as those reported for other hawk moth-pollinated orchids, but we also wanted to determine if other chemical compounds may be present other than just carbohydrates. ...
Numerous studies have confirmed the importance of nectar for effective pollination and reproductive success in orchids, but the chemical composition of floral nectar has received surprisingly little attention. We report the chemical compounds present in the nectar of the well known ghost orchid, Dendrophylax lindenii (Lindl.) Benth. ex Rolfe, using gas chromatography and mass spectrometry (GC/MS) analysis. This rare species exists as a leafless epiphyte in forests of South Florida and Western Cuba and yields a striking floral display consisting of fragrant white flowers with long (11-17 cm) nectar spurs. Nectar samples were obtained from naturally-occurring populations within the Florida Panther National Wildlife Refuge during July, 2021 and analyzed in the laboratory one wk later. Present results revealed the
presence of three sugars (glucose, fructose, and sucrose), three acids (lactic, malic, and threonic), as well as 4-hydroxyl benzyl alcohol. In addition, all three sugars were detected on the upper surface of flower’s labellum where moisture is known to collect due to its concave shape. This study supports the contention that sugars are an ubiquitous component of orchid floral nectar, but the presence of the other
compounds (acids) deserve further investigation. Further knowledge about the compounds in D. lindenii nectar will provide more insight into how and why hawk moths visit and pollinate the flowers of this rare orchid in nature.
