Anthophilous beetles ubiquitously inhabit night-blooming cacti but exhibit distinct responses to the spatial distribution of flowers

DOMINGOS-MELO, ARTHUR; MAIA, ARTUR C.D.; MILET-PINHEIRO, PAULO

doi:10.1590/0001-3765202420231361

Abstract

Night-blooming cacti, primarily pollinated by bats and hawkmoths, also attract beetles seeking food and safe shelter for mating and brooding their offspring. The influence of flower density on beetle visitation rates remains unclear, with responses varying by species and environmental factors. In the Caatinga Seasonally Dry Tropical Forest, we studied the flower occupancy distribution of two beetle species, Cyclocephala paraguayensis and Nitops aff. pilosocerei, in Pilosocereus pachycladus cacti. Our findings indicate that both beetle species act as commensals with minimal impact on effective pollination. They forage for nectar and pollen without causing damage to pistils or ovaries. N. aff. pilosocerei was more abundant than C. paraguayensis, and their distributions significantly differed, with N. aff. pilosocerei displaying a more uniform spread. Instances of both species occupying the same flower were more frequent than exclusive occupation. Nitops aff. pilosocerei abundance exhibited spatial autocorrelation. Flower height and beetle species influenced the total number of beetles within flowers. Future studies should explore the impact of cactus flower distribution on beetle abundance with other species, conduct selective pollination experiments to determine their role as pollinators, and investigate how flower-beetle interaction systems are affected by flower and individual distribution in processes like florivory and pollination.

Key words
beetle pollination; Caatinga dry forest; Cyclocephalini; density‐dependence; Nitidulidae; Pilosocereus

INTRODUCTION

One of the main factors driving the foraging patterns of floral visitors is how resources are distributed across the environment (Pyke 2016). According to the optimal foraging theory, for most anthophilous (i.e., flower-loving) animals, it is reasonable to expect that increases in the local density of flowers in a population and/or the number of flowers per plant positively affect floral visitor attractiveness as it reduces the time for finding flowers (Grindeland et al. 2005; Klinkhamer et al. 2001; Leiss & Klinkhamer 2005; Silva et al. 2022). However, the opposite situation may also occur, specially when lower floral abundance decreases competition for animal attraction, improving visitation rates per flower (Steven et al. 2003; Barley et al. 2022). Due to intrinsic characteristics, this situation may not be easily elucidated among some animal groups, as is the case of beetles (Coleoptera). Different from most other anthophilous animals, beetles do not visit flowers quickly and sequentially, but rather tend to use them as shelter and mating places as long as resources are available. Therefore, a proper assessment of the behavior of these beetles requires longer observation periods and use of invasive techniques, such as flower dissection (Paulino-Neto 2014, Bernhardt 2000). In spite of this, a few studies have been successful in this task, and have shown that responses to flower density may depend on the beetle species and environmental characteristics (García-Robledo 2010; García-Robledo et al. 2005)

Beetle fossil record dates back to the Early Permian (Zhang et al. 2018), even though their remarkable diversity appears to have been driven by the Angiosperm Terrestrial Revolution in the mid-Cretaceous (Benton et al. 2022). Today, Coleoptera constitute the most species-diverse insect order, representing ca. 25% of all known life on Earth (Grove & Stork 2000; Hunt et al. 2007). The exploitation of flowers plays a prominent role among the various ecological niches occupied by beetles, and anthophilous species are reported in no less than 30 of the extant families, especially within the giant suborder Polyphaga (Bernhardt 2000; Gottsberger 2016; Kirmse & Chaboo 2020; Li et al. 2021; Mawdsley 2003; Moore & Jameson 2013; Paulino-Neto 2014; Sayers et al. 2019; Wardhaugh 2015; Willmer 2011; Haran et al. 2023). In fact, beetles are among the earliest pollinators, a key ecosystemic role that likely evolved from pollinivory (Peris et al. 2020). Although they can act as opportunistic flower visitors and secondary pollinators, beetles are actually often involved in highly specialized pollination systems, indispensable to the reproductive success of ca. 900 spp. of angiosperms in the Neotropics alone (Brieva-Oviedo & Núñez-Avellaneda 2020; Carreño-Barrera et al. 2021; Dieringer & Jee 1994; Gottsberger 1986; Maia et al. 2023; Prance & Anderson 1976; Schatz 1990). Flower-beetle interactions, nonetheless, may also be antagonistic, as in florivory (Schlindwein & Martins 2000; Cardel & Koptur 2010; Kirmse & Chaboo 2018), or seed-feeding (da Silva & Rossi 2019; Sousa-Lopes et al. 2020), or even be configured as complex multitrophic relationships combining both mutualistic and antagonistic roles (Nunes et al. 2018).

Irrespective of the outcome of these interactions, flowers are an important resource for beetles. They not only provide food but also a safe shelter where beetles can find partners for mating and brooding their offsprings (Bernhardt 2000, Paulino-Neto 2014, Haran et al. 2023). Thus, understanding the factors underlying flower-beetle interactions is crucial. In this regard, mass-flowering trees with generalist pollination traits (i.e., light colors, open and small flowers) have been shown to play an important role in assembling and nurturing the megadiverse community of canopy beetles in Amazonian rainforests (Kirmse & Chaboo 2020). However, this leaves out countless scenarios of more specialized flower-beetle pollination systems (Li et al. 2021). In this context, night-blooming plant taxa could be of vital importance for beetles in arid ecosystems since they usually bear large flowers with high amounts of rewards that can be accessed without the severe environmental conditions of the day, such as high temperatures and low humidity (Borges et al. 2016; Macgregor & Scott-Brown 2020). For example, chiropterophilous (bat-pollinated) and sphingophilous (hawkmoth-pollinated) cacti flowers (Cactaceae) are exploited by beetles.

The exploitation of cacti flowers by beetles has been widely reported and includes different families, among which Buprestidae (e.g., Acmaeodera and Tetragonoschema), Chrysomelidae (e.g., Babiohaltica, Camptotes, Diabrotica, Iphimeis, and Nodonta), Melyridae (e.g., Hypebaeus, Tanaops, and Trichochrous), Nitidulidae (e.g., Carpophilus and Nitops), Melolonthidae (e.g., Cyclocephala and Euphoria), Staphylinidae, and Tenebrionidae stand out (Agüero et al. 2018; Aguilar-García et al. 2022; Blair & Williamson 2008; Briseño-Sánchez et al. 2020; Bustamante et al. 2010; Casas et al. 1999; Ferreira et al. 2018; Grant et al. 1979; Janeba 2009; Johnson 1992; Martínez-Peralta & Mandujano 2011; McFarland et al. 1989; Raguso et al. 2003; Rego et al. 2012; Schulumpberger & Badano 2005; Silva & Sazima 1995). Selective pollination experiments have demonstrated that many groups of animals are effective pollinators of cacti (e.g., Ortega-Baes et al. 2011; Rocha et al. 2019). However, this approach has never been employed for beetles. In this sense, although small pollen loads may be carried in the bodies of anthophilous beetles, their behavior of remaining for long periods in flowers and the fact that they rarely come into contact with stigmas strongly suggest that they do not act as effective cacti pollinators (Rocha et al. 2019; Silva & Sazima 1995).

Night-blooming cacti are often pollinated by bats or hawkmoths, which are more common in tropical and extra-tropical regions respectively (Freilij et al. 2023, Gorostiague et al. 2023). However, they are also frequently visited by beetles, as their nocturnal anthesis overlaps with the activity period of these insects. Chiropterophilous cacti, like many other bat-pollinated species, represent an abundant source of readily-accessible floral resources due to their commonly open floral morphology (Domingos-Melo et al. 2020a). They may be consumed by many other animal taxa besides effective pollinators alone. These flowers produce copious amounts of nectar that supply the high energetic demands of nectar-feeding bats (Bobrowiec & Oliveira 2012; Domingos-Melo et al. 2020b; Göttlinger et al. 2019). At the same time, they also produce large amounts of pollen as an adaptation to bats’ high pollen transport capacity through their fur (Muchhala & Thomson 2010). It is also arguably an important protein source for the bats themselves (Gribel & Gibbs 2002).

In the present study, we investigated the cactus Pilosocereus pachycladus Ritter, a bat and hawkmoth-pollinated species whose flowers are intensively exploited by different beetle taxa. We used it as a model to describe how the distribution of flowers in the population can reveal occupation patterns by anthophilous beetles. Our main objectives were to i) identify the anthophilous beetle species associated with P. pachycladus, ii) describe how different beetle species share flowers and individuals of P. pachycladus within the population, iii) verify whether there is spatial autocorrelation in occupation by anthophilous beetles across individuals in the population, and iv) determine whether the number and height of flowers affect occupation patterns by anthophilous beetles.

MATERIALS AND METHODS

Model species and studied population

The genus Pilosocereus Byles and Rowley comprises columnar cacti with a wide variety of growth habits and whose natural distribution extends throughout the intertropical region of the American continent (Taylor & Zappi 2020). It is one of the most abundant and diverse South American cacti genera, with more than 30 spp. reported from Brazil alone (Taylor & Zappi 2020). Among these, our model species, Pilosocereus pachycladus, stands out as one of the most widely distributed cacti in northeastern Brazil, where it occurs as an endemic to the Caatinga seasonally dry tropical forest (Lavor et al. 2020). It is a primarily chiropterophilous species and an important resource for many specialized nectarivorous bats, although hawkmoths and bees can also contribute to its pollination (Cordero-Schmidt et al. 2017, Rocha et al. 2019, Queiroz et al. 2021, Cordero-Schmidt et al. 2021). Different beetle species have also been reported in flowers of P. pachycladus, including the cyclocephaline scarabs Cyclocephala celata Dechambre, 1980 and C. paraguayensis Arrow, 1903 (Melolonthidae), as well as the sap beetle Nitops aff. pilosocerei Kirejtshuk and Kurochkin, 2007 (Nitidulidae), which is ubiquitously recovered in Pilosocereus spp. flowers in the Caatinga (Menezes & Sampaio 2021; Rocha et al. 2019). A comprehensive description of the interaction between nocturnal cactus flowers and different beetle taxa in general is exemplified with P. pachycladus in Fig. 1a-i.

Figure 1
Overview of floral visiting behavior of Carpophilini (Nitidulidae) and Cyclocephalini (Melolonthidae) beetles in Cactaceae, illustrated by interactions of Cyclocephala paraguayensis and Nitops aff. pilosocerei with the columnar cactus Pilosocereus pachycladus in the Caatinga Seasonally Dry Tropical Forest, Brazil. To access the flowers, the beetles can use two different strategies: (a-b) they can perforate the floral bud during bud development or pre-anthesis, or (c) enter directly through the flower opening during anthesis. Cases of bud perforation have been reported for some species of Carpophilini (although it is not a ubiquitous behavior in the group, and was not confirmed in the population studied here), while Cyclocephalini beetles search only for already opened flowers a few hours after anthesis begins during the early night. (d) Once in the cacti flowers, beetles can consume different resources, including nectar, pollen, or even floral tissues. However, unlike the interactions with several other plant families, beetles cannot reach the ovules in the inferior ovary of these epigynous flowers; beetles also use flowers as non-nutritive floral rewards for sheltering and mating. (e) When flowers close the following morning, the beetles remain inside. In the next few days, as wilting occurs, the beetles begin to leave the flowers: (f) while Cyclocephalini do it in about two days, (g-h) Carpophilini beetles can remain in the flower for longer periods, even after the end of anthesis, since floral tissue residues persist on developing fruits. (i) They also use floral tissue residues as oviposition substrate for the development of their larvae. The illustration was elaborated from our own observations and descriptions present in the literature (Rego et al. 2012; Yoshimoto et al. 2018; Miranda-Jácome et al. 2021; Menezes & Sampaio 2021; Raguso et al. 2003; Silva & Sazima 1995). The color image is available in the online version. Image credits: Natanael Nascimento.

We studied the interactions between P. pachycladus and anthophilous beetles along a trail at the Alcobaça Archaeological Site at Catimbau National Park, state of Pernambuco, Brazil (8°31’53”S 37°11’44”W; 780 m.a.s.l.). It is an area of the Caatinga seasonally dry tropical forest embedded on deep, impoverished quartzite sandy soils, with a hot and semi-arid climate under annual average temperatures of 23 °C and precipitation ranging from 480 to 1,100 mm (Rito et al. 2017). There, we studied a cluster of P. pachycladus subsp. viridis N.P.Taylor and Albuquerque-Lima, a subspecies whose range expands from the state of eastern Pernambuco to the north through the states of Paraíba and Rio Grande do Norte (Taylor & Albuquerque-Lima 2020).

Sampling of beetles

We collected all beetles occupying all the flowers from 30 individuals of P. pachycladus taken at random along the trail, configuring a ~ 300 m transect and respecting a minimum distance of ~ 10 m between plants.

The collection procedure involved: i) recording GPS coordinates for each of the 30 individuals; ii) counting the number of open flowers per individual; and iii) collecting each flower and recording their height along the shoot axis from the ground. We only collected freshly closed flowers, understood as having been occupied by beetles the night before (Fig 1e). They were gathered between 08:00 and 10:30h, during which the perianth closes and entraps the beetles inside the floral chamber. Immediately following collection, each flower was individually bagged within a sealed thick paper bagand taken to the field station for processing. The integrity of the floral tissue was also inspected to verify any evidence of perforation in the bud stage. A set of the collected flowers were sectioned longitudinally to observe the behavior of the beetles inside. At the field station, the flowers were individually rinsed and immersed in 70% alcohol to promote the fixation of the occupying beetles, which were then counted, measured (body length and width; n=10 per species) and identified to species level (Menezes & Sampaio 2021; Moore et al. 2018).

Statistical analysis

Considering that we recorded only two beetle species (see Results section below), our first interest was to verify whether there was a difference in the frequency in which they occurred together or singly in P. pachycladus flowers. Thus, we categorized both flowers and individuals into those occupied by one, another, or both beetle species, and compared their frequencies using a χ2 test for homogeneity. After this, we used mixed-effect nested models with Poisson distribution to access the total variance of each beetle species abundance by partitioning it into its hierarchical component – ie. among individuals (n = 30) and within individuals (n = one to eight flowers).

To verify how the spatial distribution of P. pachycladus individuals affected beetle occupation in flowers, we used the geographic coordinates of the 30 focal plants to conduct spatial correlation tests for the number of beetles using the Moran index (I). This index is a measure of spatial autocorrelation, indicating how related are the values of a variable based on the locations where they were measured; in a simplified interpretation, I equal to 1, 0, or -1 indicate, respectively, correlation, random distribution, or dissimilarity between the magnitude and the spatial distribution in space. The observed value of I should be different than the expected to be considered significant (Gittleman & Kot 1990). In this way, we evaluated spatial autocorrelation for each of the two beetle species considering the average number of individuals per flower in each plant. The tests were conducted with the ape package (Paradis & Schliep 2019) in R environment (R Core Team 2021).

Additionally, we verified how the occurrence of beetles in the flowers was determined by its distribution in the P. pachycladus individuals. For this purpose, we considered the number of flowers and their height along the vertical shoot axis. Previously, we detected that the height of flowers was correlated with the number of flowers on the individuals where they occur (cor = 0.65; df = 58; p < 0.0001), a pattern that makes sense since larger individuals can emit more flowers. In this way, to avoid multicollinearity, we performed the analysis considering only the height of individual flowers. We opted to fit a GLMM with negative binomial distribution and linear parameterization, since our count data had an over-dispersed distribution, due clumped occurrence of beetles. In this analysis, we included beetle species and floral height, as well as their interaction, as explanatory variables; the flowers and cacti individuals as a random variable; and the number of beetles of each species per flower as a dependent variable. The GLMM was conducted with the GlmmTMB package (Brooks et al. 2017), and the fit of the model was checked with the DHARMa package (Harting 2020), both in R environment (R Core Team 2021).

RESULTS

We collected 77 closed flowers from 30 Pilosocereus pachycladus individuals. All flowers had beetles totaling 1,219 specimens of two species only: Cyclocephala paraguayensis (n=135) and Nitops aff. pilosocerei (n=1,084). These species differ in size, with the former (the largest) measuring 6.2 ± 0.9 mm by 11.3 ± 2.2 mm wide, while the latter is 2.7 ± 0.2 mm long by 1.2 ± 0.1 mm wide. Despite often being found together, we observed no intra or interspecific antagonistic interactions within flowers. Additionally, there was no evidence of perforation in flower buds, indicating that beetles only accessed flowers after anthesis. Both species were observed inside floral chambers, where they consumed leftover nectar, foraged for pollen, and fed on floral tissues. Interestingly, they did not damage the pistils, ovaries or touch the stigma lobes positioned at the flower’s entrance. The amount of pollen they consumed was negligible compared to the overall yield per flower. Also, we did not observe individuals from either species touching the stigma lobes positioned at the flower’s entrance.

While the occurrence of C. paraguayensis in P. pachycladus was restricted to 1 – 19 individuals per flower, the total number of N. aff. pilosocerei could add up to 61 individuals in a single flower. Considering all flowers in each focal plant, the total number of C. paraguayensis and N. aff. pilosocerei could reach up to 42 and 102 individuals per plant, respectively. The frequency distribution of C. paraguayensis and N. aff. pilosocerei differed significantly at both the flowers’ (D = 0.72; p < 0.0001; Fig. 2a) and individuals’ level (D=0.83; p<0.0001), with C. paraguayensis and N. aff. pilosorei showing a markedly biased and a more uniform distribution, respectively (Fig. 2b).

Figure 2
Patterns of occurrence of the beetles Cyclocephala paraguayensis (Cyclocephalini, Melolonthidae) and Nitops aff. pilosocerei (Carpophilini, Nitidulidae) on flowers and individuals of Pilosocereus pachycladus (Cactaceae) in the Caatinga Seasonally Dry Tropical Forest, Brazil. Density plots show the distribution of the number of beetles in (a) individual flowers and (b) whole cactus plants. Barplots indicate the frequency of (c) flowers and (d) individuals occupied by each beetle species, with dotted lines representing the expected frequencies. (e) Variance components on the amount of each beetle species expressed as percentages within and among plant individuals. (f) Spatial autocorrelation in the distribution of beetles across individuals in the population, with hollow dots indicating the expected I values (Moran Index) and the vertical lines representing their respective standard deviations, while filled dots indicate the observed values. (g) A scatterplot shows the effect of floral height along the shoot axis on the number of beetles in each flower, with continuous lines indicating regression trendlines for the fitted models and colored areas indicating the 95% confidence intervals. The color image is available in the online version.

Concerning the sharing of flowers between the two beetle species, while around half of the flowers (n = 39; 50.65%) contained only N. aff. pilosocerei, 38.96% (n = 30) contained both beetle species, and 10.39% (n = 8) contained only C. paraguayensis, resulting in different frequencies (χ2 = 19.82; df = 2; p < 0.0001 – see Figure 2c). Interestingly, this difference is reversed when we consider the total number of beetles present in each P. pachycladus individual. While the flowers of most focal plants (n = 20; 66.7%) were occupied by beetles of both species, 30% (n = 9) of the plants had only N. aff. pilosocerei, and a single plant (3.3%) was occupied exclusively by C. paraguayensis (χ2 = 18.20, df = 2, p < 0.001 – see Figure 2d). Both in C. paraguayensis and N. aff. pilosocerei, the number of beetles per flower varied more within than between individuals, although this difference was less pronounced in the latter (see Figure 2e).

We detected different scenarios of spatial autocorrelation in the distribution of anthophilous beetles among individuals of P. pachycladus in the studied population (see Fig. 2f). For C. paraguayensis, there was no spatial autocorrelation in the total number of beetles per plant (Moran Index = -0.014; p = 0.57), while for N. aff. pilosocerei, there was a subtle effect (Moran Index = 0.092; p = 0.015).

The number of recently closed flowers per P. pachycladus individual ranged from one to eight, with most focal plants exhibiting only two flowers at a time. The flower height ranged from 1.2 to 6 m, with most occurring between 2 and 4 m. The height of the flowers (estimate = 0.30; se = 0.14; z = 2.23; p = 0.026) and beetle species (estimate = 3.56; se = 0.54; z = 6.59; p < 0.00001) influenced the total number of beetles inside the flowers. The interaction of these two variables also had a significant effect (estimate = -0.60; se = 0.16; z = -3.66; p = 0.0002). While C. paraguayensis appears to be only slightly positively affected, N. aff. pilosocerei occupation decreases as flower height increases (Figure 2g).

DISCUSSION

Both anthophilous beetle species found in our study, C. paraguayensis and N. aff. pilosocerei, were previously documented in association with the flowers of the columnar cactus P. pachycladus in the Caatinga SDTF (Menezes & Sampaio 2021; Rocha et al. 2019). We demonstrate that, although individuals of these morphologically distinct beetle species share the exclusive niche constituted by the night-blooming flowers of P. pachycladus, how they occupy these flowers differs substantially. While the occurrence of both species in P. pachycladus individuals is subject to spatial autocorrelation across the investigated population, for C. paraguayensis this trend refers to the total number of beetles per plant, while for N. aff. pilosocerei it refers to the average number of beetles per flower in each plant. Additionally, while the occurrence of C. paraguayensis is only slightly affected by the number of flowers and their height in a plant, the number of N. aff. pilosocerei was significantly higher in plants with fewer flowers, as well as in lower flowers. We interpret these results by considering the functional aspects of both beetle species, as well as presenting possible consequences.

Although C. paraguayensis and N. aff. pilosocerei belong to phylogenetically distant clades of the Polyphaga superorder (Zhang et al. 2018, McKenna et al. 2019, Cai et al. 2018, 2022), most taxa within both the Cyclocephalini (Melolonthidae) and Carpophilini (Nitidulidae) are associated with flowers across different angiosperm families. The Cyclocephalini have mainly been reported as pollinators of early divergent angiosperm lineages (e.g., Annonaceae, Araceae, Nymphaeaceae, and Magnoliaceae), but some species of Cyclocephala are also associated with eudicot flowers, involving 11 families and 20 plant genera (Moore & Jameson 2013). These include several published or anecdotal records of interaction with cactus genera such as Cereus, Echinopsis, Opuntia, Pilosocereus, and Xiquexique (Ferreira et al. 2018; Moore & Jameson 2013; Rocha et al. 2019; Silva & Sazima 1995). In turn, most of the Carpophilini are acknowledged as specialized fruit, nectar, and/or pollen-feeders and can be found in association with widely divergent gymnosperm and angiosperm taxa across tropical and non-tropical habitats worldwide (Cline et al. 2014; Crowson 1988; Herrera & Otero 2021; Jürgens et al. 2000; Procheş & Johnson 2009). Some species can be highly generalist in terms of resource-providing plant species and can visit flowers in up to 25% of plant species in given environments (Bellec et al. 2022; Herrera & Otero 2021). Several authors have shown that species within this tribe often establish close relationships with night-blooming columnar cacti, including Pilosocereus and Stenocereus (Menezes & Sampaio 2021; Miranda-Jácome et al. 2021; Yoshimoto et al. 2018).

Regarding the possible reasons for the attraction of the reported beetles to the flowers of P. pachycladus, it is important to consider that the floral traits of night-blooming columnar cacti seem to make them particularly attractive to these beetles. Plants pollinated by Cyclocephalini have flowers/inflorescences with a large size, nocturnal anthesis, light colors, and thick floral tissues (Moore & Jameson 2013; Paulino-Neto 2014). On the other hand, there is no clear pattern in the morphological floral traits of Carpophilini-pollinated plants, since they interact with a wide variety of small flowers (Cline et al. 2014; Herrera & Otero 2021). Both beetle groups also show a particular preference for thermogenic, intensely fragrant flowers (Jürgens et al. 2000; Maia et al. 2012, 2014, 2023; Favaris et al. 2023; Bian et al. 2021). Therefore, in addition to the morphological features found in nocturnal flowers of Cactaceae, there are also certain scent compounds that are attractive to beetles, e.g., (E)-nerolidol and methyl benzoate - (Kaiser & Tollsten 1995, Schlumpberger & Raguso 2008, Gonzalez-Terrazas et al. 2016, Albuquerque-Lima et al. 2023a). Regarding thermogenesis, although it cannot be stated that this process occurs in cacti flowers, it is reasonable to hypothesize that the presence of thick aquiferous parenchyma in the hypanthium (Gonzalez et al. 2021, Stefano et al. 2001) provides at least some thermal insulation that allows the flowers to deal with the intense thermal oscillations of drylands, which can be very hot during the day and cold during the night.

The abundance patterns of both beetle species found in the flowers of P. pachycladus seems to be in accordance with what is reported in the respective groups to which they belong. For C. paraguayensis, the lack of precise quantification in other studies with Cactaceae flowers limits direct comparisons. Even so, when considering their occurrence in other systems, we find numbers quite similar to ours. Taking as an example the Cyclocephalini pollination in Araceae, while some species rarely show more than one or two beetles inside an inflorescence, others reach a maximum of a few dozen (Maia & Schlindwein 2006, Gottsberger et al. 2013, Maia et al. 2013), which matches our sampling. However, in some aroid species, such as in Philodendron selloum, one inflorescence may be occupied by up to 200 individual of the beetle Erioscelis emarginata (Gottsberger & Silberbauer-Gottsberger 1991).

Regarding the number of N. aff. pilosocerei individuals present in the flowers of the population studied here, our findings are within the range reported for other interactions involving Carpophilini and Cactaceae, although the frequency distribution was more uniform. In these systems, the basic condition is the presence of a few beetle individuals along almost all flowers of the population, although it is not uncommon for the same flower to show aggregations of dozens or even hundreds of beetles (Figueroa-Castro et al. 2014; Menezes & Sampaio 2021; Miranda-Jácome et al. 2021). As such aggregations are not a ubiquitous event in flowers of the population, it is possible that the attractiveness of flowers alone is not responsible for explaining such behavior. Since these flowers are used as a mating site for beetles, it is likely that the first beetles to arrive would release aggregating pheromones responsible for attracting conspecific individuals, a very common behavior in many Coleoptera, including Nitidulidae (Bartelt 1997; Francke & Dettner 2005).

Differences in flower occupancy patterns by C. paraguayensis and N. aff. pilosocerei suggest that niche partitioning may occur between these species, a common pattern in beetle guilds with diverse habits such as coprophagy, necrophagy or xylophagy (Simandl 1993, Chao et al. 2013, Keller et al. 2019). This would make sense, as competitive exclusion is a common process between species that use the same floral resource, where the largest, most abundant, or most aggressive species usually suppresses the others (Camfield 2006; Carr & Golinski 2020; Ford & Paton 1982; Hung et al. 2019). However, the high frequency with which both beetle species were found together suggests that there is no antagonistic relationship between them (as supported by our focal observation on dissected flowers). This conclusion is supported by at least two aspects: 1) although both species utilize the same resources, which could lead to indirect competition, none of them appears to be voracious consumers to an extent that would compromise the availability of pollen or nectar for the other and 2) the flowers of P. pachycladus are large enough to properly accommodate several individuals of both species. This interpretation is further supported by the fact that although large, individuals of C. paraguayensiscommonly occurred alone or in low abundance in the flowers, and N. aff. pilosocerei is so small that they would hardly occupy much space in flowers, even when occurring in large numbers. In this context, the differences in the spatial distribution of these beetles along the flowers of the population might be mainly related to autecological processes rather than to niche partitioning.

Similar to our findings, previous studies have shown that Cyclocephalini and Carpophilini beetles differ in their responses to floral resource density, with the former increasing frequency in distant plants and the latter in clustered ones (García-Robledo et al. 2005). This pattern may be attributed to the beetles’ limited displacement ability. Insects’ body sizes are typically linked to their flying performance, with larger insects having better flight capabilities (Farisenkov et al. 2022, Tennekes 1997). Therefore, it is likely that the more robust Cyclocephalini beetles have a high flight capacity, whereas smaller Carpophilini beetles may experience difficulty flying in open and windy areas. The studied population occurs in open areas of sedimentary Caatinga, where the wind can reach up to 28 km/h (Meteoblue 2024). Consequently, the distance between cactus plants does not affect the occupation by C. paraguayensis, whose few individuals occur scattered throughout the flowers of the population. These findings are consistent with previous reports of long-distance pollen flow facilitated by Cyclocephalini beetles (García-Robledo 2010).

In contrast, N. aff. pilosocerei is a small species with lower flight capacity and is distributed primarily in plants close to each other. Once these beetles reach a cactus individual, they spread throughout the flowers, concentrating on the lower ones. Concomitantly, the lowest flowers occur on smaller plants with fewer flowers, where such beetles are forced to stay together, while on plants with more flowers, the occupation may be more evenly distributed.

Regarding the consequences of this interaction for the plant perspective, both beetle species appear to establish a commensal relationship with P. pachycladus, consuming resources without necessarily providing a pollination service or causing significant damage. However, when they arrive at the flowers and cross the floral entrance, these beetles probably touch the stigma (unfortunately we could not confirm this in the present study). This possibility is particularly applicable for C. paraguayensis given its larger size, greater flight range, and comparatively shorter hosting time in the flowers of P. pachycladus (features that may optimize pollen flow). In addition, many beetle-pollinated plants produce sticky exudates from stigmas or petals that optimize pollen adhesion to the slick bodies of these insects (Lau et al. 2017, Gottsberger et al. 2012, Gasca-Alvarez 2013). A similar process could occur in nocturnal cacti flowers, where large amounts of nectar could play an analogous adhesive role. Indeed, we observed some beetles in the field covered with pollen. However, for these beetles to act as effective pollinators, the pollen would need to have long viability (see Dafni & Firmage 2000 for a review), as it can take a few days for a beetle to move from one flower to another, thus promoting pollen flow. Nonetheless, even if these beetles could contribute to pollination, we can assume their effectiveness would be far inferior to the high-quality service provided by other pollinators, such as bats and hawkmoths (Rocha et al. 2019, Ortega-Baes et al. 2011).

Beetles, like numerous other anthophiles, explore flowers as resource-rich ephemeral habitats (Raguso 2023). Therefore, the intricate role of beetles, even in non-cantharophilous flowers, merits further exploration. In this study, we demonstrate that different beetle species, despite sharing the same floral resource, respond in completely distinct ways to the spatial distribution of flowers in the environment. The Caatinga stands out globally as one of the regions with an exceptionally high abundance of chiropterophilous plant species, notably featuring columnar cacti such as Pilosocereus (Domingos-Melo et al. 2023), which possess the same morphological characteristics as P. pachycladus (Albuquerque-Lima et al. 2023b). Future studies that investigate the effect of cactus flower distribution on beetle abundance at a geographic and interspecific level could reveal whether beetles are subject to interactions with other species in a similar way to what we report here. We also recommend that future studies conduct selective pollination experiments to conclusively determine whether these beetles can act as pollinators of Cactaceae species. Our findings highlight the necessity of understanding how other flower-beetle interaction systems are affected by the spatial distribution of flowers and individuals, as well as their potential implications for processes ranging from florivory to pollination.

ACKNOWLEDGMENTS

We thank “Curso de Campo: Ecologia e Conservação da Caatinga” for logistical support and Profs. Inara Leal and Marcelo Tabarelli for their assistance in fieldwork. This ressearch was funded by FACEPE (Fundação de Amparo à Ciência e Tecnologia de Pernambuco; DCR-0031-2.03/21; APQ-0226-2.03/21). We also thank CNPq (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil; Finance Code 001) for finantial support.

REFERENCES

AGÜERO JI, GALATI BG & TORRETTA JP. 2018. Structure and ultrastructure of floral nectaries of two Opuntia species (Cactaceae) in relation to their floral visitors. Pl Syst Evol 304: 1057-1067.
AGUILAR-GARCÍA SA, FIGUEROA-CASTRO DM, VALVERDE PL, VITE F, LÓPEZ-ORTEGA G & PÉREZ-HERNÁNDEZ MA. 2022. Reproductive biology of Myrtillocactus geometrizans (Cactaceae) flowers with contrasting orientation. Plant Species Biol 37: 243-256.
ALBUQUERQUE-LIMA S, DOMINGOS-MELO A, MILET-PINHEIRO P, NAVARRO D, FERRAZ MDOA, TAYLOR NP, ZAPPI DC & MACHADO IC. 2023a. The iconic cactus of the Caatinga dry forest, Cereus jamacaru (Cactaceae) has high sphingophily specialization and pollinator dependence. An Acad Bras Cienc 95: e20220460. https://doi.org/10.1590/0001-3765202320220460.
» https://doi.org/10.1590/0001-3765202320220460
ALBUQUERQUE-LIMA S, TAYLOR NP, ZAPPI DC & MACHADO IC. 2023b. Floral Specialization and Bat Pollination in Subtribe Cereinae (Cactaceae): A Morphological Approach. Diversity (Basel) 15: 207.
BARLEY TA, MARTINEZ ALGARIN MG & BAUER JT. 2022. The Effects of Flower Patch Density on Pollinator Visitation. Environ Entomol 51: 482-491.
BARTELT RJ. 1997. Aggregation pheromones of Carpophilus spp.(Coleoptera: Nitidulidae): Review of chemistry and biology. Recent Res Dev Entomol 1: 115-129.
BELLEC L, CORTESERO A-M, GIGUÈRE T, FAURE S & HERVÉ MR. 2022. Food preferences in a generalist pollen feeder: A nutritional strategy mainly driven by plant carbohydrates. Front Ecol Evol 10: 1050321.
BENTON MJ, WILF P & SAUQUET H. 2022. The Angiosperm Terrestrial Revolution and the origins of modern biodiversity. New Phytologist 233: 2017-2035.
BERNHARDT P. 2000. Convergent Evolution and Adaptive Radiation of Beetle-Pollinated Angiosperms. In: DAFNI A et al. (Eds), Pollen and Pollination, Vienna: Springer Vienna, p. 293-320.
BIAN F, LUO Y, LI L, PANG Y & PENG Y. 2021. Inflorescence development, thermogenesis and flower-visiting insect activity in Alocasia odora. Flora 279: 151818.
BLAIR AW & WILLIAMSON PS. 2008. Effectiveness and Importance of Pollinators to the Star Cactus Astrophylum asterias. Southwest Nat 53: 423-430.
BOBROWIEC PED & OLIVEIRA PE. 2012. Removal Effects on Nectar Production in Bat‐pollinated Flowers of the Brazilian Cerrado. Biotropica 44: 1-5.
BORGES RM, SOMANATHAN H & KELBER A. 2016. Patterns and Processes in Nocturnal and Crepuscular Pollination Services. Q Rev Biol 91: 389-418.
BRIEVA-OVIEDO E & NÚÑEZ-AVELLANEDA LA. 2020. Biología reproductiva de la palma amarga (Sabal mauritiiformis: Arecaceae): especie económicamente importante para la Costa Caribe colombiana. Caldasia 42: 278-293.
BRISEÑO-SÁNCHEZ MI, MARTÍNEZ-PERALTA C & MANDUJANO MC. 2020. Population structure and reproductive biology of peyote (Lophophora diffusa, Cactaceae), a threatened species with pollen limitation. J Torrey Bot Soc 147: 243-257.
BROOKS ME, KRISTENSEN K, VAN BENTHEM KJ, MAGNUSSON A, BERG CW, NIELSEN A, SKAUG HJ, MACHLER M & BOLKER BM. 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9: 378-400.
BUSTAMANTE E, CASAS A & BÚRQUEZ A. 2010. Geographic variation in reproductive success of Stenocereus thurberi (Cactaceae): Effects of pollination timing and pollinator guild. Am J Bot 97: 2020-2030.
CAI C ET AL. 2022. Integrated phylogenomics and fossil data illuminate the evolution of beetles. R Soc Open Sci 9: 211771.
CAI C, ESCALONA HE, LI L, YIN Z, HUANG D & ENGEL MS. 2018. Beetle Pollination of Cycads in the Mesozoic. Current Biology 28: 2806-2812.e1.
CAMFIELD AF. 2006. Resource value affects territorial defense by Broad-tailed and Rufous hummingbirds. J Field Ornithol 77: 120-125.
CARDEL YJ & KOPTUR S. 2010. Effects of Florivory on the Pollination of Flowers: An Experimental Field Study with a Perennial Plant. Int J Plant Sci 171: 283-292.
CARR JM & GOLINSKI JE. 2020. Vigilance behaviors of Ruby-throated Hummingbirds (Archilochus colubris) reflect elevated risk of competitive interactions with vespine wasps. Wilson J Ornithol 132: 295-305.
CARREÑO-BARRERA J, MAIA ACD, COLOMBO CA & NÚÑEZ-AVELLANEDA LA. 2021. Co-pollination, constancy, and efficiency over time: small beetles and the reproductive success of Acrocomia aculeata (Arecaceae) in the Colombian Orinoquia. Bot Lett 168: 395-407.
CASAS A, VALIENTE-BANUET A, ROJAS-MARTÍNEZ A & DA´VILA P. 1999. Reproductive biology and the process of domestication of the columnar cactus Stenocereus Stellatus in Central Mexico. Am J Bot 86: 534-542.
CHAO A, SIMON-FREEMAN R & GRETHER G. 2013. Patterns of Niche Partitioning and Alternative Reproductive Strategies in an East African Dung Beetle Assemblage. J Insect Behav 26: 525-539.
CLINE AR, SMITH TR, MILLER K, MOULTON M, WHITINH M & AUDISIO P. 2014. Molecular phylogeny of Nitidulidae: assessment of subfamilial and tribal classification and formalization of the family Cybocephalidae (Coleoptera: Cucujoidea). Syst Entomol 39: 758-772.
CORDERO-SCHMIDT E, BARBIER E, VARGAS-MENA JC, OLIVEIRA PP, SANTOS FAR, MEDELLÍN RA, HERRERA BR & VENTICINQUE EM. 2017. Natural history of the Caatinga endemic Vieira’s flower bat, Xeronycteris vieirai. Acta Chiropt 19: 399-408.
CORDERO-SCHMIDT E, MARUYAMA PK, VARGAS-MENA JC, PEREIRA OLIVEIRA P, DE ASSIS R, SANTOS F, MEDELLÍN RA, RODRIGUEZ-HERRERA B & VENTICINQUE EM. 2021. Bat–flower interaction networks in Caatinga reveal generalized associations and temporal stability. Biotropica 53: 1546-1557.
CROWSON RA. 1988. Meligethinae as Possible Pollinators (Coleoptera: Nitidulidae). Entomologia Generalis 14: 61-62.
DA SILVA AV & ROSSI MN. 2019. When a seed-feeding beetle is a predator and also increases the speed of seed germination: an intriguing interaction with an invasive plant. Evol Ecol 33: 211-232.
DAFNI A & FIRMAGE D. 2000. Pollen viability and longevity: practical, ecological and evolutionary implications. Pollen and pollination, 113-132.
DIERINGER G & S JEE. 1994. Reproductive ecology of Magnolia schiedeana (Magnoliaceae), a threatened cloud forest tree species in Veracruz, Mexico. Bull. Torrey Bot Club, 154-159.
DOMINGOS-MELO A, ALBUQUERQUE-LIMA S, DINIZ UM, LOPES AV & MACHADO IC. 2023. Bat pollination in the Caatinga: A review of studies and peculiarities of the system in the new world’s largest and most diverse seasonally dry tropical forest. Flora 305: 152332.
DOMINGOS-MELO A, DINIZ UM, CHALEGRE SL & MACHADO IC. 2020a. “Sweet Rain” from Bat-Pollinated Flowers: How Does Sugar Concentration Modulate Nectar Retention? Int J Plant Sci 182: 71-77.
DOMINGOS-MELO A, MILET-PINHEIRO P, NAVARRO DMAF, LOPES AV & MACHADO IC. 2020b. It’s raining fragrant nectar in the Caatinga: evidence of nectar olfactory signaling in bat-pollinated flowers. Ecology 101: e02914.
FARISENKOV SE, KOLOMENSKIY D, PETROV PN, ENGELS T, LAPINA NA, LEHMANN F-O, ONISHI R, LIU H & POLILOV AA. 2022. Novel flight style and light wings boost flight performance of tiny beetles. Nature 602: 96-100.
FAVARIS AP, TÚLER AC, SILVA WD, PEC M, RODRIGUES SR, MAIA ACD & BENTO JMS. 2023. Methyl benzoate and nerolidol attract the cyclocephaline beetle Cyclocephala paraguayensis to trumpet flowers. The Science of Nature 110: 3.
FERREIRA BHS, GOMES AC, SOUZA CS, FABRI JR & SIGRIST MR. 2018. Pollination and reproductive system of synchronopatric species of Cactaceae (Cactoideae) subject to interspecific flow of pollen: an example of ecological adaptation in the Brazilian Chaco. Plant Biol 20: 101-112.
FIGUEROA-CASTRO DM, VALVERDE PL, VITE F & CARRILLO-RUIZ H. 2014. Spatial Variation in the Community of Insects Associated With the Flowers of Pachycereus weberi (Caryophyllales: Cactaceae). Environ Entomol 43: 889-895.
FORD HA & PATON DC. 1982. Partitioning of nectar sources in an Australian honeyeater community. Aust J Ecol 7: 149-159.
FRANCKE W & DETTNER K. 2005. Chemical signalling in beetles. Top Curr Chem 240: 85-166.
FREILIJ D, LARREA-ALCAZAR D, LOPEZ RP, VELARDE SIMONINI F, NAOKI K & BESSEGA C. 2023. Environmental gradualism explains variation in pollination systems of columnar cacti: Phylogenetic and trait evolution analyses. Glob Ecol Biogeogr 32: 1015-1029.
GARCÍA-ROBLEDO C. 2010. Restoration of Plant–Pollinator Interactions: Pollination Neighborhood and Asymmetric Pollen Flow Between Restored Habitats in a Beetle-Pollinated Aroid. Restor Ecol 18: 94-102.
GARCÍA-ROBLEDO C, KATTAN G, MURCIA C & QUINTERO-MARÍN P. 2005. Equal and Opposite Effects of Floral Offer and Spatial Distribution on Fruit Production and Predispersal Seed Predation in Xanthosoma daguense (Araceae)1. Biotropica 37: 373-380.
GASCA-ALVAREZ HJ. 2013. New records of Cyclocephala Dejean (Coleoptera: Scarabaeidae: Dynastinae) associated with Caladium bicolor (Aiton) Vent.(Araceae). Coleopt Bull 67: 416-418.
GITTLEMAN JL & KOT M. 1990. Adaptation: Statistics and a Null Model for Estimating Phylogenetic Effects. Syst Biol 39: 227-241.
GONZALEZ VV, GOROSTIAGUE P, ORTEGA-BAES P, GALATI BG & FERRUCCI MS. 2021. Nectary structure is not related to pollination system in Trichocereeae cactus from Northwest Argentina. An Acad Bras Cienc 93: e20201401. https://doi.org/10.1590/0001-3765202120201401.
» https://doi.org/10.1590/0001-3765202120201401
GONZALEZ-TERRAZAS TP, MARTEL C, MILET-PINHEIRO P, AYASSE M, KALKO EK V & TSCHAPKA M. 2016. Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar. R Soc Open Sci 3: 160199.
GOROSTIAGUE P, OLLERTON J & ORTEGA-BAES P. 2023. Latitudinal gradients in biotic interactions: Are cacti pollination systems more specialized in the tropics? Plant Biol 25: 187-197.
GÖTTLINGER T, SCHWERDTFEGER M, TIEDGE K & LOHAUS G. 2019. What do nectarivorous bats like? Nectar composition in Bromeliaceae with special emphasis on bat-pollinated species. Front Plant Sci 10: 205.
GOTTSBERGER G. 1986. Some pollination strategies in neotropical savannas and forests. Pl Syst Evol 152: 29-45.
GOTTSBERGER G. 2016. Generalist and specialist pollination in basal angiosperms (ANITA grade, basal monocots, magnoliids, Chloranthaceae and Ceratophyllaceae): what we know now. Plant Divers Evol 131: 263-362.
GOTTSBERGER G & SILBERBAUER-GOTTSBERGER I. 1991. Olfactory and visual attraction of Erioscelis emarginata (Cyclocephalini, Dynastinae) to the inflorescences of Philodendron selloum (Araceae). Biotropica, 23-28.
GOTTSBERGER G, SILBERBAUER-GOTTSBERGER I & DÖTTERL S. 2013. Pollination and floral scent differentiation in species of the Philodendron bipinnatifidum complex (Araceae). Pl Syst Evol 299: 793-809.
GOTTSBERGER G, SILBERBAUER-GOTTSBERGER I, SEYMOUR RS & DÖTTERL S. 2012. Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus. Flora - Morphology, Distribution, Functional Ecology of Plants 207: 107-118.
GRANT V, GRANT KA & HURD PD. 1979. Pollination of Opuntia lindheimeri and related species. Pl Syst Evol 132: 313-320.
GRIBEL R & GIBBS PE. 2002. High Outbreeding as a Consequence of Selfed Ovule Mortality and Single Vector Bat Pollination in the Amazonian Tree Pseudobombax munguba (Bombacaceae). Int J Plant Sci 163: 1035-1043.
GRINDELAND JM, SLETVOLD N & IMS RA. 2005. Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Funct Ecol, 383-390.
GROVE SJ & STORK NE. 2000. An inordinate fondness for beetles. Invertebr Syst 14: 733-739.
HARAN J, KERGOAT GJ & DE MEDEIROS BAS. 2023. Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. Peer Community Journal 3.
HARTING F. 2020. DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.3.1.
HERRERA CM & OTERO C. 2021. Plant phylogeny as a major predictor of flower visitation by nitidulid beetles, a lineage of ancestral angiosperm pollinators. J Pollinat Ecol 29: 179-188.
HUNG K-LJ, KINGSTON JM, LEE A, HOLWAY DA & KOHN JR. 2019. Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proceedings of the Royal Society B: Biological Sciences 286: 20182901.
HUNT T ET AL 2007. A Comprehensive Phylogeny of Beetles Reveals the Evolutionary Origins of a Superradiation. Science (1979) 318: 1913-1916.
JANEBA Z. 2009. Insect flower visitors and pollinators of cacti from the southwest USA. Bradleya 2009: 59-68.
JOHNSON RA. 1992. Pollination and Reproductive Ecology of Acuña Cactus, Echinomastus erectrocentrus var. Acunensis (Cactaceae). Int J Plant Sci 153: 400-408.
JÜRGENS A, WEBBER AC & GOTTSBERGER G. 2000. Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55: 551-558.
KAISER R & TOLLSTEN L. 1995. An introduction to the scent of cacti. Flavour Fragr J 10: 153-164.
KELLER ML, HOWARD DR & HALL CL. 2019. Spatiotemporal niche partitioning in a specious silphid community (Coleoptera: Silphidae Nicrophorus). The Science of Nature 106: 57.
KIRMSE S & CHABOO CS. 2018. Polyphagy and florivory prevail in a leaf-beetle community (Coleoptera: Chrysomelidae) inhabiting the canopy of a tropical lowland rainforest in southern Venezuela. J Nat Hist 52: 2677-2721.
KIRMSE S & CHABOO CS. 2020. Flowers are essential to maintain high beetle diversity (Coleoptera) in a Neotropical rainforest canopy. J Nat Hist 54: 1661-1696.
KLINKHAMER PGL, DE JONG TJ & LINNEBANK LA. 2001. Small-scale spatial patterns determine ecological relationships: an experimental example using nectar production rates. Ecol Lett 4: 559-567.
LAU JYY, PANG C-C, RAMSDEN L & SAUNDERS RMK. 2017. Stigmatic exudate in the Annonaceae: Pollinator reward, pollen germination medium or extragynoecial compitum? J Integr Plant Biol 59: 881-894.
LAVOR P, VERSIEUX LM & CALVENTE A. 2020. Phylogenetic relationships of Pilosocereus (Cactaceae) and taxonomic implications. PlantNow 1: 52-70.
LEISS KA & KLINKHAMER PGL. 2005. Spatial distribution of nectar production in a natural Echium vulgare population: implications for pollinator behaviour. Basic Appl Ecol 6: 317-324.
LI K-Q, REN Z-X & LI Q. 2021. Diversity of flower visiting beetles at higher elevations on the Yulong Snow Mountain (Yunnan, China). Diversity (Basel) 13: 604.
MACGREGOR CJ & SCOTT-BROWN AS. 2020. Nocturnal pollination: an overlooked ecosystem service vulnerable to environmental change. Emerg Top Life Sci 4: 19-32.
MAIA ACD, DE LIMA CT, NAVARRO DMAF, CHARTIER M, GIULIETTI AM & MACHADO IC. 2014. The floral scents of Nymphaea subg. Hydrocallis (Nymphaeaceae), the New World night-blooming water lilies, and their relation with putative pollinators. Phytochemistry 103: 67-75.
MAIA ACD, DÖTTERL S, GONÇALVES EG, SILBERBAUER-GOTTSBERGER I & GOTTSBERGER G. 2023. Floral scent chemistry of sympatric species of Philodendron (Araceae) sharing a common pollinator in the fragmented coastal Atlantic Forest of southeastern Brazil. Flora 300: 152224.
MAIA ACD, DÖTTERL S, KAISER R, SILBERBAUER-GOTTSBERGER I, TEICHERT H, GIBERNAU M, DO AMARAL DMFN, SCHLINDWEIN C & GOTTSBERGER G. 2012. The Key Role of 4-methyl-5-vinylthiazole in the Attraction of Scarab Beetle Pollinators: a Unique Olfactory Floral Signal Shared by Annonaceae and Araceae. J Chem Ecol 38: 1072-1080.
MAIA ACD, GIBERNAU M, CARVALHO AT, GONÇALVES EG & SCHLINDWEIN C. 2013. The cowl does not make the monk: scarab beetle pollination of the Neotropical aroid Taccarum ulei (Araceae: Spathicarpeae). Biol J Linn Soc Lond 108: 22-34.
MAIA ACD & SCHLINDWEIN C. 2006. Caladium bicolor (Araceae) and Cyclocephala celata (Coleoptera, Dynastinae): A Well-Established Pollination System in the Northern Atlantic Rainforest of Pernambuco, Brazil. Plant Biol 8: 529-534.
MARTÍNEZ-PERALTA C & MANDUJANO MC. 2011. Reproductive ecology of the endangered living rock cactus, Ariocarpus fissuratus (Cactaceae). J Torrey Bot Soc 138: 145-155.
MAWDSLEY JR. 2003. The Importance of Species of Dasytinae (Coleoptera: Melyridae) as Pollinators in Western North America. Coleopt Bull 57: 154-160.
MCFARLAND JD, KEVAN PG & LANE MA. 1989. Pollination biology of Opuntia imbricata (Cactaceae) in southern Colorado. Canad J Bot 67: 24-28.
MCKENNA DD ET AL. 2019. The evolution and genomic basis of beetle diversity. PNAS 116: 24729-24737.
MENEZES MOT & SAMPAIO VG. 2021. The ecological relationship between sap beetles and Pilosocereus Byles & Rowley (Cactaceae) in Northeastern Brazil. Bradleya 2021: 36-44.
METEOBLUE. 2024. http://www.meteoblue.com/en/weather/forecast/modelclimate accessed December 5, 2024.
» http://www.meteoblue.com/en/weather/forecast/modelclimate
MIRANDA-JÁCOME A, FERNÁNDEZ-TLAPA F & MUNGUÍA-ROSAS MA. 2021. Visiting and feeding behavior of sap beetles (Carpophilus lugubris) in the flowers of a chiropterophilic columnar cactus (Pilosocereus leucocephalus). J Arid Environ 189: 104482.
MOORE MR, CAVE RD & BRANHAM MA. 2018. Annotated catalog and bibliography of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae, Cyclocephalini). Zookeys 101.
MOORE MR & JAMESON ML. 2013. Floral associations of cyclocephaline scarab beetles. J Insect Sci 13: 100.
MUCHHALA N & THOMSON JD. 2010. Fur versus feathers: pollen delivery by bats and hummingbirds and consequences for pollen production. Am Nat 175: 717-726.
NUNES CEP, MARUYAMA PK, AZEVEDO-SILVA M & SAZIMA M. 2018. Parasitoids Turn Herbivores into Mutualists in a Nursery System Involving Active Pollination. Current Biology 28: 980-986.e3.
ORTEGA-BAES P, SARAVIA M, SÜHRING S, GODÍNEZ-ALVAREZ H & ZAMAR M. 2011. Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators. Plant Biol 13: 33-40.
PARADIS E & SCHLIEP K. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526-528.
PAULINO-NETO HF. 2014. Polinização por besouros. Biologia da polinização 259.
PERIS D, LABANDEIRA CC, BARRÓN E, DELCLÒS X, RUST J & WANG B. 2020. Generalist Pollen-Feeding Beetles during the Mid-Cretaceous. iScience 23: 100913.
PRANCE GT & ANDERSON AB. 1976. Studies of the floral biology of neotropical Nymphaeaceae. 3. Acta Amazon 6: 163-170.
PROCHEŞ Ş & JOHNSON SD. 2009. Beetle pollination of the fruit-scented cones of the South African cycad Stangeria eriopus. Am J Bot 96: 1722-1730.
PYKE GH. 2016. Plant–pollinator co-evolution: It’s time to reconnect with Optimal Foraging Theory and Evolutionarily Stable Strategies. Perspect Plant Ecol Evol Syst 19: 70-76.
QUEIROZ JA, DINIZ UM, VÁZQUEZ DP, QUIRINO ZM, SANTOS FAR, MELLO MAR & MACHADO IC. 2021. Bats and hawkmoths form mixed modules with flowering plants in a nocturnal interaction network. Biotropica 53: 596-607.
RAGUSO RA. 2023. Hidden worlds within flowers. Current Biology 33: R506-R512.
RAGUSO RA, HENZEL C, BUCHMANN SL & NABHAN GP. 2003. Trumpet Flowers of the Sonoran Desert: Floral Biology of Peniocereus Cacti and Sacred Datura. Int J Plant Sci 164: 877-892.
R CORE TEAM. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
» https://www.R-project.org/
REGO JO, FRANCESCHINELLI EV & ZAPPI DC. 2012. Reproductive biology of a highly endemic species: Cipocereus laniflorus NP Taylor & Zappi (Cactaceae). Acta Bot Brasilica 26: 243-250.
RITO KF, ARROYO-RODRÍGUEZ V, QUEIROZ RT, LEAL IR & TABARELLI M. 2017. Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation NORDEN N (Ed.). J Ecol 105: 828-838.
ROCHA EA, DOMINGOS-MELO A, ZAPPI DC & MACHADO IC. 2019. Reproductive biology of columnar cacti: are bats the only protagonists in the pollination of Pilosocereus, a typical chiropterophilous genus? Folia Geobot 54: 239-256.
SAYERS TDJ, STEINBAUER MJ & MILLER RE. 2019. Visitor or vector? The extent of rove beetle (Coleoptera: Staphylinidae) pollination and floral interactions. Arthropod Plant Interact 13: 685-701.
SCHATZ GE. 1990. Some aspects of pollination biology in Central American forests. Reproductive Ecology Of Tropical Forest Plants 7: 69-84.
SCHLINDWEIN C & MARTINS CF. 2000. Competition between the oligolectic bee Ptilothrix plumata (Anthophoridae) and the flower closing beetle Pristimerus calcaratus (Curculionidae) for floral resources of Pavonia cancellata (Malvaceae). Pl Syst Evol 224: 183-194.
SCHULUMPBERGER BO & BADANO EI. 2005. Diversity of floral visitors in Echinopsis atacamensis ssp. pasacana (Cactaceae). Haseltonia 11: 18-26.
SCHLUMPBERGER BO & RAGUSO RA. 2008. Geographic variation in floral scent of Echinopsis ancistrophora (Cactaceae); evidence for constraints on hawkmoth attraction. Oikos 117: 801-814.
SILVA JLS, CRUZ-NETO O & LOPES AV. 2022. Higher flower number in Jatropha mutabilis (Euphorbiaceae) increases the frequency of floral visitors in the Caatinga dry forest. Arthropod Plant Interact 16: 317-327.
SILVA WR & SAZIMA M. 1995. Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil. Flora 190: 339-343.
SIMANDL J. 1993. The spatial pattern, diversity and niche partitioning in xylophagous beetles (Coleoptera) associated with Frangula alnus Mill. Acta Oecologica 14: 161-171.
SOUSA-LOPES B, SANTOS AT, RIBEIRO-COSTA CS & DEL-CLARO K. 2020. Spatio-temporal variation in seed traits affects the occurrence and body-size pattern of a seed-feeding beetle (Chrysomelidae: Bruchinae) in Brazilian Cerrado. Acta Oecologica 105: 103579.
STEFANO M, PAPINI A, ANDALÒ C & BRIGHIGNA L. 2001. Ultrastructural aspects of the hypanthial epithelium of Selenicereus grandiflorus (L.) Britton & Rose (Cactaceae). Flora 196: 194-203.
STEVEN JC, ROONEY TP, BOYLE OD & WALLER DM. 2003. Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum. J Torrey Bot Soc 23–29.
TAYLOR NP & ALBUQUERQUE-LIMA S. 2020. Annotated checklist of Cactaceae in the Catimbau National Park, Pernambuco, Brazil. Bradleya 2020: 231-246.
TAYLOR NP & ZAPPI DC. 2020. Nomenclatural adjustments in Brazilian Cereeae (Cactaceae). Phytotaxa 470: 256-258.
TENNEKES H. 1997. The Simple Science of Flight: From Insects to Jumbo Jets The MIT Press. Cambridge, MA.
WARDHAUGH CW. 2015. How many species of arthropods visit flowers? Arthropod Plant Interact 9: 547-565.
WILLMER P. 2011. Pollination and floral ecology. In: Pollination and floral ecology, Princeton University Press.
YOSHIMOTO J, POWELL GS & CLINE AR. 2018. Flower-Inhabiting Sap Beetles (Coleoptera: Nitidulidae: Carpophilinae) in Guatemala. Coleopt Bull 72: 762-766.
ZAPPI DC. 1994. Pilosocereus (Cactaceae). The genus in Brazil. Succ Pl Res 3: 1-160.
ZHANG S-Q, CHE L-H, LI Y, LIANG D, PANG H, ŚLIPIŃSKI A & ZHANG P. 2018. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat Commun 9: 205.

Publication Dates

Publication in this collection
16 Dec 2024
Date of issue
2024

History

Received
15 Dec 2023
Accepted
12 Oct 2024

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] AGÜERO JI, GALATI BG & TORRETTA JP. 2018. Structure and ultrastructure of floral nectaries of two Opuntia species (Cactaceae) in relation to their floral visitors. Pl Syst Evol 304: 1057-1067.

[2] AGUILAR-GARCÍA SA, FIGUEROA-CASTRO DM, VALVERDE PL, VITE F, LÓPEZ-ORTEGA G & PÉREZ-HERNÁNDEZ MA. 2022. Reproductive biology of Myrtillocactus geometrizans (Cactaceae) flowers with contrasting orientation. Plant Species Biol 37: 243-256.

[3] ALBUQUERQUE-LIMA S, DOMINGOS-MELO A, MILET-PINHEIRO P, NAVARRO D, FERRAZ MDOA, TAYLOR NP, ZAPPI DC & MACHADO IC. 2023a. The iconic cactus of the Caatinga dry forest, Cereus jamacaru (Cactaceae) has high sphingophily specialization and pollinator dependence. An Acad Bras Cienc 95: e20220460. https://doi.org/10.1590/0001-3765202320220460.
» https://doi.org/10.1590/0001-3765202320220460

[4] ALBUQUERQUE-LIMA S, TAYLOR NP, ZAPPI DC & MACHADO IC. 2023b. Floral Specialization and Bat Pollination in Subtribe Cereinae (Cactaceae): A Morphological Approach. Diversity (Basel) 15: 207.

[5] BARLEY TA, MARTINEZ ALGARIN MG & BAUER JT. 2022. The Effects of Flower Patch Density on Pollinator Visitation. Environ Entomol 51: 482-491.

[6] BARTELT RJ. 1997. Aggregation pheromones of Carpophilus spp.(Coleoptera: Nitidulidae): Review of chemistry and biology. Recent Res Dev Entomol 1: 115-129.

[7] BELLEC L, CORTESERO A-M, GIGUÈRE T, FAURE S & HERVÉ MR. 2022. Food preferences in a generalist pollen feeder: A nutritional strategy mainly driven by plant carbohydrates. Front Ecol Evol 10: 1050321.

[8] BENTON MJ, WILF P & SAUQUET H. 2022. The Angiosperm Terrestrial Revolution and the origins of modern biodiversity. New Phytologist 233: 2017-2035.

[9] BERNHARDT P. 2000. Convergent Evolution and Adaptive Radiation of Beetle-Pollinated Angiosperms. In: DAFNI A et al. (Eds), Pollen and Pollination, Vienna: Springer Vienna, p. 293-320.

[10] BIAN F, LUO Y, LI L, PANG Y & PENG Y. 2021. Inflorescence development, thermogenesis and flower-visiting insect activity in Alocasia odora. Flora 279: 151818.

[11] BLAIR AW & WILLIAMSON PS. 2008. Effectiveness and Importance of Pollinators to the Star Cactus Astrophylum asterias. Southwest Nat 53: 423-430.

[12] BOBROWIEC PED & OLIVEIRA PE. 2012. Removal Effects on Nectar Production in Bat‐pollinated Flowers of the Brazilian Cerrado. Biotropica 44: 1-5.

[13] BORGES RM, SOMANATHAN H & KELBER A. 2016. Patterns and Processes in Nocturnal and Crepuscular Pollination Services. Q Rev Biol 91: 389-418.

[14] BRIEVA-OVIEDO E & NÚÑEZ-AVELLANEDA LA. 2020. Biología reproductiva de la palma amarga (Sabal mauritiiformis: Arecaceae): especie económicamente importante para la Costa Caribe colombiana. Caldasia 42: 278-293.

[15] BRISEÑO-SÁNCHEZ MI, MARTÍNEZ-PERALTA C & MANDUJANO MC. 2020. Population structure and reproductive biology of peyote (Lophophora diffusa, Cactaceae), a threatened species with pollen limitation. J Torrey Bot Soc 147: 243-257.

[16] BROOKS ME, KRISTENSEN K, VAN BENTHEM KJ, MAGNUSSON A, BERG CW, NIELSEN A, SKAUG HJ, MACHLER M & BOLKER BM. 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9: 378-400.

[17] BUSTAMANTE E, CASAS A & BÚRQUEZ A. 2010. Geographic variation in reproductive success of Stenocereus thurberi (Cactaceae): Effects of pollination timing and pollinator guild. Am J Bot 97: 2020-2030.

[18] CAI C ET AL. 2022. Integrated phylogenomics and fossil data illuminate the evolution of beetles. R Soc Open Sci 9: 211771.

[19] CAI C, ESCALONA HE, LI L, YIN Z, HUANG D & ENGEL MS. 2018. Beetle Pollination of Cycads in the Mesozoic. Current Biology 28: 2806-2812.e1.

[20] CAMFIELD AF. 2006. Resource value affects territorial defense by Broad-tailed and Rufous hummingbirds. J Field Ornithol 77: 120-125.

[21] CARDEL YJ & KOPTUR S. 2010. Effects of Florivory on the Pollination of Flowers: An Experimental Field Study with a Perennial Plant. Int J Plant Sci 171: 283-292.

[22] CARR JM & GOLINSKI JE. 2020. Vigilance behaviors of Ruby-throated Hummingbirds (Archilochus colubris) reflect elevated risk of competitive interactions with vespine wasps. Wilson J Ornithol 132: 295-305.

[23] CARREÑO-BARRERA J, MAIA ACD, COLOMBO CA & NÚÑEZ-AVELLANEDA LA. 2021. Co-pollination, constancy, and efficiency over time: small beetles and the reproductive success of Acrocomia aculeata (Arecaceae) in the Colombian Orinoquia. Bot Lett 168: 395-407.

[24] CASAS A, VALIENTE-BANUET A, ROJAS-MARTÍNEZ A & DA´VILA P. 1999. Reproductive biology and the process of domestication of the columnar cactus Stenocereus Stellatus in Central Mexico. Am J Bot 86: 534-542.

[25] CHAO A, SIMON-FREEMAN R & GRETHER G. 2013. Patterns of Niche Partitioning and Alternative Reproductive Strategies in an East African Dung Beetle Assemblage. J Insect Behav 26: 525-539.

[26] CLINE AR, SMITH TR, MILLER K, MOULTON M, WHITINH M & AUDISIO P. 2014. Molecular phylogeny of Nitidulidae: assessment of subfamilial and tribal classification and formalization of the family Cybocephalidae (Coleoptera: Cucujoidea). Syst Entomol 39: 758-772.

[27] CORDERO-SCHMIDT E, BARBIER E, VARGAS-MENA JC, OLIVEIRA PP, SANTOS FAR, MEDELLÍN RA, HERRERA BR & VENTICINQUE EM. 2017. Natural history of the Caatinga endemic Vieira’s flower bat, Xeronycteris vieirai. Acta Chiropt 19: 399-408.

[28] CORDERO-SCHMIDT E, MARUYAMA PK, VARGAS-MENA JC, PEREIRA OLIVEIRA P, DE ASSIS R, SANTOS F, MEDELLÍN RA, RODRIGUEZ-HERRERA B & VENTICINQUE EM. 2021. Bat–flower interaction networks in Caatinga reveal generalized associations and temporal stability. Biotropica 53: 1546-1557.

[29] CROWSON RA. 1988. Meligethinae as Possible Pollinators (Coleoptera: Nitidulidae). Entomologia Generalis 14: 61-62.

[30] DA SILVA AV & ROSSI MN. 2019. When a seed-feeding beetle is a predator and also increases the speed of seed germination: an intriguing interaction with an invasive plant. Evol Ecol 33: 211-232.

[31] DAFNI A & FIRMAGE D. 2000. Pollen viability and longevity: practical, ecological and evolutionary implications. Pollen and pollination, 113-132.

[32] DIERINGER G & S JEE. 1994. Reproductive ecology of Magnolia schiedeana (Magnoliaceae), a threatened cloud forest tree species in Veracruz, Mexico. Bull. Torrey Bot Club, 154-159.

[33] DOMINGOS-MELO A, ALBUQUERQUE-LIMA S, DINIZ UM, LOPES AV & MACHADO IC. 2023. Bat pollination in the Caatinga: A review of studies and peculiarities of the system in the new world’s largest and most diverse seasonally dry tropical forest. Flora 305: 152332.

[34] DOMINGOS-MELO A, DINIZ UM, CHALEGRE SL & MACHADO IC. 2020a. “Sweet Rain” from Bat-Pollinated Flowers: How Does Sugar Concentration Modulate Nectar Retention? Int J Plant Sci 182: 71-77.

[35] DOMINGOS-MELO A, MILET-PINHEIRO P, NAVARRO DMAF, LOPES AV & MACHADO IC. 2020b. It’s raining fragrant nectar in the Caatinga: evidence of nectar olfactory signaling in bat-pollinated flowers. Ecology 101: e02914.

[36] FARISENKOV SE, KOLOMENSKIY D, PETROV PN, ENGELS T, LAPINA NA, LEHMANN F-O, ONISHI R, LIU H & POLILOV AA. 2022. Novel flight style and light wings boost flight performance of tiny beetles. Nature 602: 96-100.

[37] FAVARIS AP, TÚLER AC, SILVA WD, PEC M, RODRIGUES SR, MAIA ACD & BENTO JMS. 2023. Methyl benzoate and nerolidol attract the cyclocephaline beetle Cyclocephala paraguayensis to trumpet flowers. The Science of Nature 110: 3.

[38] FERREIRA BHS, GOMES AC, SOUZA CS, FABRI JR & SIGRIST MR. 2018. Pollination and reproductive system of synchronopatric species of Cactaceae (Cactoideae) subject to interspecific flow of pollen: an example of ecological adaptation in the Brazilian Chaco. Plant Biol 20: 101-112.

[39] FIGUEROA-CASTRO DM, VALVERDE PL, VITE F & CARRILLO-RUIZ H. 2014. Spatial Variation in the Community of Insects Associated With the Flowers of Pachycereus weberi (Caryophyllales: Cactaceae). Environ Entomol 43: 889-895.

[40] FORD HA & PATON DC. 1982. Partitioning of nectar sources in an Australian honeyeater community. Aust J Ecol 7: 149-159.

[41] FRANCKE W & DETTNER K. 2005. Chemical signalling in beetles. Top Curr Chem 240: 85-166.

[42] FREILIJ D, LARREA-ALCAZAR D, LOPEZ RP, VELARDE SIMONINI F, NAOKI K & BESSEGA C. 2023. Environmental gradualism explains variation in pollination systems of columnar cacti: Phylogenetic and trait evolution analyses. Glob Ecol Biogeogr 32: 1015-1029.

[43] GARCÍA-ROBLEDO C. 2010. Restoration of Plant–Pollinator Interactions: Pollination Neighborhood and Asymmetric Pollen Flow Between Restored Habitats in a Beetle-Pollinated Aroid. Restor Ecol 18: 94-102.

[44] GARCÍA-ROBLEDO C, KATTAN G, MURCIA C & QUINTERO-MARÍN P. 2005. Equal and Opposite Effects of Floral Offer and Spatial Distribution on Fruit Production and Predispersal Seed Predation in Xanthosoma daguense (Araceae)1. Biotropica 37: 373-380.

[45] GASCA-ALVAREZ HJ. 2013. New records of Cyclocephala Dejean (Coleoptera: Scarabaeidae: Dynastinae) associated with Caladium bicolor (Aiton) Vent.(Araceae). Coleopt Bull 67: 416-418.

[46] GITTLEMAN JL & KOT M. 1990. Adaptation: Statistics and a Null Model for Estimating Phylogenetic Effects. Syst Biol 39: 227-241.

[47] GONZALEZ VV, GOROSTIAGUE P, ORTEGA-BAES P, GALATI BG & FERRUCCI MS. 2021. Nectary structure is not related to pollination system in Trichocereeae cactus from Northwest Argentina. An Acad Bras Cienc 93: e20201401. https://doi.org/10.1590/0001-3765202120201401.
» https://doi.org/10.1590/0001-3765202120201401

[48] GONZALEZ-TERRAZAS TP, MARTEL C, MILET-PINHEIRO P, AYASSE M, KALKO EK V & TSCHAPKA M. 2016. Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar. R Soc Open Sci 3: 160199.

[49] GOROSTIAGUE P, OLLERTON J & ORTEGA-BAES P. 2023. Latitudinal gradients in biotic interactions: Are cacti pollination systems more specialized in the tropics? Plant Biol 25: 187-197.

[50] GÖTTLINGER T, SCHWERDTFEGER M, TIEDGE K & LOHAUS G. 2019. What do nectarivorous bats like? Nectar composition in Bromeliaceae with special emphasis on bat-pollinated species. Front Plant Sci 10: 205.

[51] GOTTSBERGER G. 1986. Some pollination strategies in neotropical savannas and forests. Pl Syst Evol 152: 29-45.

[52] GOTTSBERGER G. 2016. Generalist and specialist pollination in basal angiosperms (ANITA grade, basal monocots, magnoliids, Chloranthaceae and Ceratophyllaceae): what we know now. Plant Divers Evol 131: 263-362.

[53] GOTTSBERGER G & SILBERBAUER-GOTTSBERGER I. 1991. Olfactory and visual attraction of Erioscelis emarginata (Cyclocephalini, Dynastinae) to the inflorescences of Philodendron selloum (Araceae). Biotropica, 23-28.

[54] GOTTSBERGER G, SILBERBAUER-GOTTSBERGER I & DÖTTERL S. 2013. Pollination and floral scent differentiation in species of the Philodendron bipinnatifidum complex (Araceae). Pl Syst Evol 299: 793-809.

[55] GOTTSBERGER G, SILBERBAUER-GOTTSBERGER I, SEYMOUR RS & DÖTTERL S. 2012. Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus. Flora - Morphology, Distribution, Functional Ecology of Plants 207: 107-118.

[56] GRANT V, GRANT KA & HURD PD. 1979. Pollination of Opuntia lindheimeri and related species. Pl Syst Evol 132: 313-320.

[57] GRIBEL R & GIBBS PE. 2002. High Outbreeding as a Consequence of Selfed Ovule Mortality and Single Vector Bat Pollination in the Amazonian Tree Pseudobombax munguba (Bombacaceae). Int J Plant Sci 163: 1035-1043.

[58] GRINDELAND JM, SLETVOLD N & IMS RA. 2005. Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Funct Ecol, 383-390.

[59] GROVE SJ & STORK NE. 2000. An inordinate fondness for beetles. Invertebr Syst 14: 733-739.

[60] HARAN J, KERGOAT GJ & DE MEDEIROS BAS. 2023. Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. Peer Community Journal 3.

[61] HARTING F. 2020. DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.3.1.

[62] HERRERA CM & OTERO C. 2021. Plant phylogeny as a major predictor of flower visitation by nitidulid beetles, a lineage of ancestral angiosperm pollinators. J Pollinat Ecol 29: 179-188.

[63] HUNG K-LJ, KINGSTON JM, LEE A, HOLWAY DA & KOHN JR. 2019. Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proceedings of the Royal Society B: Biological Sciences 286: 20182901.

[64] HUNT T ET AL 2007. A Comprehensive Phylogeny of Beetles Reveals the Evolutionary Origins of a Superradiation. Science (1979) 318: 1913-1916.

[65] JANEBA Z. 2009. Insect flower visitors and pollinators of cacti from the southwest USA. Bradleya 2009: 59-68.

[66] JOHNSON RA. 1992. Pollination and Reproductive Ecology of Acuña Cactus, Echinomastus erectrocentrus var. Acunensis (Cactaceae). Int J Plant Sci 153: 400-408.

[67] JÜRGENS A, WEBBER AC & GOTTSBERGER G. 2000. Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55: 551-558.

[68] KAISER R & TOLLSTEN L. 1995. An introduction to the scent of cacti. Flavour Fragr J 10: 153-164.

[69] KELLER ML, HOWARD DR & HALL CL. 2019. Spatiotemporal niche partitioning in a specious silphid community (Coleoptera: Silphidae Nicrophorus). The Science of Nature 106: 57.

[70] KIRMSE S & CHABOO CS. 2018. Polyphagy and florivory prevail in a leaf-beetle community (Coleoptera: Chrysomelidae) inhabiting the canopy of a tropical lowland rainforest in southern Venezuela. J Nat Hist 52: 2677-2721.

[71] KIRMSE S & CHABOO CS. 2020. Flowers are essential to maintain high beetle diversity (Coleoptera) in a Neotropical rainforest canopy. J Nat Hist 54: 1661-1696.

[72] KLINKHAMER PGL, DE JONG TJ & LINNEBANK LA. 2001. Small-scale spatial patterns determine ecological relationships: an experimental example using nectar production rates. Ecol Lett 4: 559-567.

[73] LAU JYY, PANG C-C, RAMSDEN L & SAUNDERS RMK. 2017. Stigmatic exudate in the Annonaceae: Pollinator reward, pollen germination medium or extragynoecial compitum? J Integr Plant Biol 59: 881-894.

[74] LAVOR P, VERSIEUX LM & CALVENTE A. 2020. Phylogenetic relationships of Pilosocereus (Cactaceae) and taxonomic implications. PlantNow 1: 52-70.

[75] LEISS KA & KLINKHAMER PGL. 2005. Spatial distribution of nectar production in a natural Echium vulgare population: implications for pollinator behaviour. Basic Appl Ecol 6: 317-324.

[76] LI K-Q, REN Z-X & LI Q. 2021. Diversity of flower visiting beetles at higher elevations on the Yulong Snow Mountain (Yunnan, China). Diversity (Basel) 13: 604.

[77] MACGREGOR CJ & SCOTT-BROWN AS. 2020. Nocturnal pollination: an overlooked ecosystem service vulnerable to environmental change. Emerg Top Life Sci 4: 19-32.

[78] MAIA ACD, DE LIMA CT, NAVARRO DMAF, CHARTIER M, GIULIETTI AM & MACHADO IC. 2014. The floral scents of Nymphaea subg. Hydrocallis (Nymphaeaceae), the New World night-blooming water lilies, and their relation with putative pollinators. Phytochemistry 103: 67-75.

[79] MAIA ACD, DÖTTERL S, GONÇALVES EG, SILBERBAUER-GOTTSBERGER I & GOTTSBERGER G. 2023. Floral scent chemistry of sympatric species of Philodendron (Araceae) sharing a common pollinator in the fragmented coastal Atlantic Forest of southeastern Brazil. Flora 300: 152224.

[80] MAIA ACD, DÖTTERL S, KAISER R, SILBERBAUER-GOTTSBERGER I, TEICHERT H, GIBERNAU M, DO AMARAL DMFN, SCHLINDWEIN C & GOTTSBERGER G. 2012. The Key Role of 4-methyl-5-vinylthiazole in the Attraction of Scarab Beetle Pollinators: a Unique Olfactory Floral Signal Shared by Annonaceae and Araceae. J Chem Ecol 38: 1072-1080.

[81] MAIA ACD, GIBERNAU M, CARVALHO AT, GONÇALVES EG & SCHLINDWEIN C. 2013. The cowl does not make the monk: scarab beetle pollination of the Neotropical aroid Taccarum ulei (Araceae: Spathicarpeae). Biol J Linn Soc Lond 108: 22-34.

[82] MAIA ACD & SCHLINDWEIN C. 2006. Caladium bicolor (Araceae) and Cyclocephala celata (Coleoptera, Dynastinae): A Well-Established Pollination System in the Northern Atlantic Rainforest of Pernambuco, Brazil. Plant Biol 8: 529-534.

[83] MARTÍNEZ-PERALTA C & MANDUJANO MC. 2011. Reproductive ecology of the endangered living rock cactus, Ariocarpus fissuratus (Cactaceae). J Torrey Bot Soc 138: 145-155.

[84] MAWDSLEY JR. 2003. The Importance of Species of Dasytinae (Coleoptera: Melyridae) as Pollinators in Western North America. Coleopt Bull 57: 154-160.

[85] MCFARLAND JD, KEVAN PG & LANE MA. 1989. Pollination biology of Opuntia imbricata (Cactaceae) in southern Colorado. Canad J Bot 67: 24-28.

[86] MCKENNA DD ET AL. 2019. The evolution and genomic basis of beetle diversity. PNAS 116: 24729-24737.

[87] MENEZES MOT & SAMPAIO VG. 2021. The ecological relationship between sap beetles and Pilosocereus Byles & Rowley (Cactaceae) in Northeastern Brazil. Bradleya 2021: 36-44.

[88] METEOBLUE. 2024. http://www.meteoblue.com/en/weather/forecast/modelclimate accessed December 5, 2024.
» http://www.meteoblue.com/en/weather/forecast/modelclimate

[89] MIRANDA-JÁCOME A, FERNÁNDEZ-TLAPA F & MUNGUÍA-ROSAS MA. 2021. Visiting and feeding behavior of sap beetles (Carpophilus lugubris) in the flowers of a chiropterophilic columnar cactus (Pilosocereus leucocephalus). J Arid Environ 189: 104482.

[90] MOORE MR, CAVE RD & BRANHAM MA. 2018. Annotated catalog and bibliography of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae, Cyclocephalini). Zookeys 101.

[91] MOORE MR & JAMESON ML. 2013. Floral associations of cyclocephaline scarab beetles. J Insect Sci 13: 100.

[92] MUCHHALA N & THOMSON JD. 2010. Fur versus feathers: pollen delivery by bats and hummingbirds and consequences for pollen production. Am Nat 175: 717-726.

[93] NUNES CEP, MARUYAMA PK, AZEVEDO-SILVA M & SAZIMA M. 2018. Parasitoids Turn Herbivores into Mutualists in a Nursery System Involving Active Pollination. Current Biology 28: 980-986.e3.

[94] ORTEGA-BAES P, SARAVIA M, SÜHRING S, GODÍNEZ-ALVAREZ H & ZAMAR M. 2011. Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators. Plant Biol 13: 33-40.

[95] PARADIS E & SCHLIEP K. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526-528.

[96] PAULINO-NETO HF. 2014. Polinização por besouros. Biologia da polinização 259.

[97] PERIS D, LABANDEIRA CC, BARRÓN E, DELCLÒS X, RUST J & WANG B. 2020. Generalist Pollen-Feeding Beetles during the Mid-Cretaceous. iScience 23: 100913.

[98] PRANCE GT & ANDERSON AB. 1976. Studies of the floral biology of neotropical Nymphaeaceae. 3. Acta Amazon 6: 163-170.

[99] PROCHEŞ Ş & JOHNSON SD. 2009. Beetle pollination of the fruit-scented cones of the South African cycad Stangeria eriopus. Am J Bot 96: 1722-1730.

[100] PYKE GH. 2016. Plant–pollinator co-evolution: It’s time to reconnect with Optimal Foraging Theory and Evolutionarily Stable Strategies. Perspect Plant Ecol Evol Syst 19: 70-76.

[101] QUEIROZ JA, DINIZ UM, VÁZQUEZ DP, QUIRINO ZM, SANTOS FAR, MELLO MAR & MACHADO IC. 2021. Bats and hawkmoths form mixed modules with flowering plants in a nocturnal interaction network. Biotropica 53: 596-607.

[102] RAGUSO RA. 2023. Hidden worlds within flowers. Current Biology 33: R506-R512.

[103] RAGUSO RA, HENZEL C, BUCHMANN SL & NABHAN GP. 2003. Trumpet Flowers of the Sonoran Desert: Floral Biology of Peniocereus Cacti and Sacred Datura. Int J Plant Sci 164: 877-892.

[104] R CORE TEAM. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
» https://www.R-project.org/

[105] REGO JO, FRANCESCHINELLI EV & ZAPPI DC. 2012. Reproductive biology of a highly endemic species: Cipocereus laniflorus NP Taylor & Zappi (Cactaceae). Acta Bot Brasilica 26: 243-250.

[106] RITO KF, ARROYO-RODRÍGUEZ V, QUEIROZ RT, LEAL IR & TABARELLI M. 2017. Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation NORDEN N (Ed.). J Ecol 105: 828-838.

[107] ROCHA EA, DOMINGOS-MELO A, ZAPPI DC & MACHADO IC. 2019. Reproductive biology of columnar cacti: are bats the only protagonists in the pollination of Pilosocereus, a typical chiropterophilous genus? Folia Geobot 54: 239-256.

[108] SAYERS TDJ, STEINBAUER MJ & MILLER RE. 2019. Visitor or vector? The extent of rove beetle (Coleoptera: Staphylinidae) pollination and floral interactions. Arthropod Plant Interact 13: 685-701.

[109] SCHATZ GE. 1990. Some aspects of pollination biology in Central American forests. Reproductive Ecology Of Tropical Forest Plants 7: 69-84.

[110] SCHLINDWEIN C & MARTINS CF. 2000. Competition between the oligolectic bee Ptilothrix plumata (Anthophoridae) and the flower closing beetle Pristimerus calcaratus (Curculionidae) for floral resources of Pavonia cancellata (Malvaceae). Pl Syst Evol 224: 183-194.

[111] SCHULUMPBERGER BO & BADANO EI. 2005. Diversity of floral visitors in Echinopsis atacamensis ssp. pasacana (Cactaceae). Haseltonia 11: 18-26.

[112] SCHLUMPBERGER BO & RAGUSO RA. 2008. Geographic variation in floral scent of Echinopsis ancistrophora (Cactaceae); evidence for constraints on hawkmoth attraction. Oikos 117: 801-814.

[113] SILVA JLS, CRUZ-NETO O & LOPES AV. 2022. Higher flower number in Jatropha mutabilis (Euphorbiaceae) increases the frequency of floral visitors in the Caatinga dry forest. Arthropod Plant Interact 16: 317-327.

[114] SILVA WR & SAZIMA M. 1995. Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil. Flora 190: 339-343.

[115] SIMANDL J. 1993. The spatial pattern, diversity and niche partitioning in xylophagous beetles (Coleoptera) associated with Frangula alnus Mill. Acta Oecologica 14: 161-171.

[116] SOUSA-LOPES B, SANTOS AT, RIBEIRO-COSTA CS & DEL-CLARO K. 2020. Spatio-temporal variation in seed traits affects the occurrence and body-size pattern of a seed-feeding beetle (Chrysomelidae: Bruchinae) in Brazilian Cerrado. Acta Oecologica 105: 103579.

[117] STEFANO M, PAPINI A, ANDALÒ C & BRIGHIGNA L. 2001. Ultrastructural aspects of the hypanthial epithelium of Selenicereus grandiflorus (L.) Britton & Rose (Cactaceae). Flora 196: 194-203.

[118] STEVEN JC, ROONEY TP, BOYLE OD & WALLER DM. 2003. Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum. J Torrey Bot Soc 23–29.

[119] TAYLOR NP & ALBUQUERQUE-LIMA S. 2020. Annotated checklist of Cactaceae in the Catimbau National Park, Pernambuco, Brazil. Bradleya 2020: 231-246.

[120] TAYLOR NP & ZAPPI DC. 2020. Nomenclatural adjustments in Brazilian Cereeae (Cactaceae). Phytotaxa 470: 256-258.

[121] TENNEKES H. 1997. The Simple Science of Flight: From Insects to Jumbo Jets The MIT Press. Cambridge, MA.

[122] WARDHAUGH CW. 2015. How many species of arthropods visit flowers? Arthropod Plant Interact 9: 547-565.

[123] WILLMER P. 2011. Pollination and floral ecology. In: Pollination and floral ecology, Princeton University Press.

[124] YOSHIMOTO J, POWELL GS & CLINE AR. 2018. Flower-Inhabiting Sap Beetles (Coleoptera: Nitidulidae: Carpophilinae) in Guatemala. Coleopt Bull 72: 762-766.

[125] ZAPPI DC. 1994. Pilosocereus (Cactaceae). The genus in Brazil. Succ Pl Res 3: 1-160.

[126] ZHANG S-Q, CHE L-H, LI Y, LIANG D, PANG H, ŚLIPIŃSKI A & ZHANG P. 2018. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat Commun 9: 205.