Potential consequences of the coqui frog invasion in Hawaii

The Puerto Rican frog, Eleutherodactylus coqui, has invaded Hawaii and has negatively impacted the state's multimillion dollar floriculture, nursery and tourist industries; however, little is known about the ecological consequences of the invasion. Using data from Puerto Rico and Hawaii, the authors summarize the potential consequences of the invasion and describe future research needs. It could be predicted that the coqui would reduce the abundance of Hawaii's endemic invertebrates. However, data suggest that coquis are mostly consuming non‐native invertebrates, and not invertebrate pests, such as mosquitoes and termites. Endemic invertebrates are likely to represent a portion of the coqui diet, but it remains uncertain which endemic invertebrates are most threatened by coqui predation and whether there will be indirect effects that benefit or harm them. It could be predicted that coquis would compete with endemic birds for invertebrate prey, but there is presently little overlap in the habitats used by coquis and endemic birds. Although, coquis may make bird re‐invasion into lowland ecosystems more difficult; alternatively, coquis could serve as an additional food source for some endemic birds. Finally, it could be predicted that coquis serve as a food source for endemic‐bird predators, such as rats and mongoose, and bolster their abundance. Preliminary data suggest that coquis will not bolster rat or mongoose populations. Managing coqui populations in Hawaii has been a challenge. A population has not yet been eradicated using citric acid, the only federally approved pesticide for coquis. It is unlikely that coquis will ever be eradicated from the islands of Hawaii and Maui, where there are now hundreds of populations. Quick and severe responses to new introductions may be the only effective means of containing the spread of the coqui.     

Dietary overlap between the invasive coquí frog (<Emphasis Type="Italic">Eleutherodactylus coqui</Emphasis>) and the Hawaiian hoary bat (<Emphasis Type="Italic">Lasiurus cinereus semotus</Emphasis>) on the Island of Hawai’i

The invasive coquí frog is a likely insectivorous competitor to the native Hawaiian hoary bat. The frog is a sit-and-wait predator native to Puerto Rico, but it has the capacity for producing dense populations in its invasive range and the potential to reduce arthropod populations, including aerial arthropods in the orders Coleoptera, Lepidoptera and Isoptera, which are primary food sources of the Hawaiian hoary bat. Dietary analysis of the coquí frog showed that aerial insects made up 33.8 % of the diet. The dietary similarity of the bat and frog was relatively low (Pianka index = 0.25), however, coquí frogs consumed a wide range of juvenile flying insects. Population densities of coquí frogs at two low elevation sites were projected to range from 750 to 14,000 individuals/hectare, and could consume an estimated 1500–19,000 aerial insects/hectare/night, or nearly 90.6 % of all available aerial insects/hectare. Although direct competition between coquí frogs and Hawaiian hoary bats was not confirmed, the coquí frogs could reduce available prey for bats in newly invaded upland sites where bats appear to be more selective of prey species among available aerial insects.     

Do the evolutionary interactions between moths and bats promote niche partitioning between bats and birds?

Ecological theory suggests that the coexistence of species is promoted by the partitioning of available resources, as in dietary niche partitioning where predators partition prey. Yet, the mechanisms underlying dietary niche partitioning are not always clear. We used fecal DNA metabarcoding to investigate the diets of seven nocturnal insectivorous bird and bat species. Low diet overlap (2%–22%) supported resource partitioning among all species. Differences in diet corresponded with species identity, prey detection method, and foraging behavior of predators. Insects with ultrasonic hearing capabilities were consumed significantly more often by birds than bats, consistent with an evolved avoidance of echolocating strategies. In turn, bats consumed a greater proportion of noneared insects such as spruce budworms. Overall, our results suggest that evolutionary interactions among bats and moths translate to dietary niche partitioning and coexistence among bats and nocturnal birds.     

Trophic structure of a neotropical frugivore community: is there competition between birds and bats?

Summary Dietary overlap and competition between frugivorous birds and bats in the Neotropics have been presumed to be low, but comparative data have been lacking. We determined the diets of volant frugivores in an early successional patch of Costa Rican wet forest over a one month period. Ordination of the diet matrix by Reciprocal Averaging revealed that birds and bats tend to feed on different sets of fruits and that diets differed more among bat species than among bird species. However, there was overlap between Scarlet-rumped Tanagers and three Carollia bat species on fruits of several Piper species which comprised most of the diet of these bats. Day/night exclosure experiments on P. friedrichsthalli treetlets provided evidence that birds deplete the amount of ripe fruit available to bats. These results indicate that distantly related taxa may overlap in diet and compete for fruit, despite the apparent adaptation of animal-dispersed plant species for dispersal by particular animal taxa.     

Hawaiian hoary bat responses to habitat,season, and non-native insectivore suppression

Habitat loss and non-native species are 2 of the most important factors that influence native species persistence and behaviors globally. The insectivorous Hawaiian hoary bat (Lasiurus semotus) is the only extant terrestrial mammal native to the Hawaiian Islands. Non-native invasive insectivore species, which are potential competitors of bats for prey, may influence hoary bat behavior. The goal of this study was to determine how small-scale suppression of invasive insectivores (rodents, ants, and yellowjacket wasps [Vespula pensylvanica]) influenced bat activity in grasslands and woodlands. We measured bat activity as a function of the number of distinct minutes in a night containing bat echolocations (bat call minutes) at 20 experimental plots (each 2.25 ha) in a dryland ecosystem on Hawaiʻi Island, November 2016–January 2018. We included 3 predictor variables: vegetation type (woodland, grassland), season (bat reproductive cycle periods: lactation, mating, pre-pregnancy, and pregnancy), and insectivore treatment type (ant suppressed, yellowjacket wasp suppressed, rodent suppressed, combined ant+wasp+rodent suppressed, and no treatment). Bat activity was associated with all 3 predictors using a negative binomial generalized linear model. Bat call minutes and feeding buzzes were twice as high in woodlands than in the grasslands (2.4 and 2.3 times as high, respectively). Bat activity was slightly lower (0.47 bat call min/night fewer) in plots receiving the combined ant + wasp + rodent treatment compared to all other treatment plots. Feeding buzzes did not differ significantly among treatments. Mean activity was lowest during lactation (mid-Jun–Aug). Although woodlands appear particularly important for the Hawaiian hoary bat, small-scale bat activity and foraging do not appear to be strongly affected by resource competition with the invasive insectivores in this study.     

Bird and bat predation services in tropical forests and agroforestry landscapes

Understanding distribution patterns and multitrophic interactions is critical for managing bat‐ and bird‐mediated ecosystem services such as the suppression of pest and non‐pest arthropods. Despite the ecological and economic importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem services. Here, we review the distribution patterns of insectivorous birds and bats, their local and landscape drivers, and their effects on trophic cascades in tropical ecosystems. We report that for birds but not bats community composition and relative importance of functional groups changes conspicuously from forests to habitats including both agricultural areas and forests, here termed ‘forest‐agri’ habitats, with reduced representation of insectivores in the latter. In contrast to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of arthropods in the tropics with effect sizes similar to those in temperate and boreal communities. The relative importance of birds versus bats in regulating pest abundances varies with season, geography and management. Birds and bats may even suppress tropical arthropod outbreaks, although positive effects on plant growth are not always reported. As both bats and birds are major agents of pest suppression, a better understanding of the local and landscape factors driving the variability of their impact is needed.     

Two Tickets to Paradise: Multiple Dispersal Events in the Founding of Hoary Bat Populations in Hawai'i

The Hawaiian islands are an extremely isolated oceanic archipelago, and their fauna has long served as models of dispersal in island biogeography. While molecular data have recently been applied to investigate the timing and origin of dispersal events for several animal groups including birds, insects, and snails, these questions have been largely unaddressed in Hawai''i’s only native terrestrial mammal, the Hawaiian hoary bat, Lasiurus cinereus semotus. Here, we use molecular data to test the hypotheses that (1) Hawaiian L. c. semotus originated via dispersal from North American populations of L. c. cinereus rather than from South American L. c. villosissimus, and (2) modern Hawaiian populations were founded from a single dispersal event. Contrary to the latter hypothesis, our mitochondrial data support a biogeographic history of multiple, relatively recent dispersals of hoary bats from North America to the Hawaiian islands. Coalescent demographic analyses of multilocus data suggest that modern populations of Hawaiian hoary bats were founded no more than 10 kya. Our finding of multiple evolutionarily significant units in Hawai''i highlights information that should be useful for re-evaluation of the conservation status of hoary bats in Hawai''i.     

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.     

Strong founder effects and low genetic diversity in introduced populations of Coqui frogs

The success of non-native species may depend on the genetic resources maintained through the invasion process. The Coqui ( Eleutherodactylus coqui ), a frog endemic to Puerto Rico, was introduced to Hawaii in the late 1980s via the horticulture trade, and has become an aggressive invader. To explore whether genetic diversity and population structure changed with the introduction, we assessed individuals from 15 populations across the Hawaiian Islands and 13 populations across Puerto Rico using six to nine polymorphic microsatellite loci and five dorsolateral colour patterns. Allelic richness ( R _T) and gene diversity were significantly higher in Puerto Rico than in Hawaii populations. Hawaii also had fewer colour patterns (two versus three to five per population) than Puerto Rico. We found no isolation by distance in the introduced range, even though it exists in the native range. Results suggest extensive mixing among frog populations across Hawaii, and that their spread has been facilitated by humans. Like previous research, our results suggest that Hawaiian Coquis were founded by individuals from sites around San Juan, but unlike previous research the colour pattern and molecular genetic data (nuclear and mtDNA) support two separate introductions, one on the island of Hawaii and one on Maui. Coquis are successful invaders in Hawaii despite the loss of genetic variation. Future introductions may increase genetic variation and potentially its range.     

Top-down control of herbivory by birds and bats in the canopy of temperate broad-leaved oaks (Quercus robur)

The intensive foraging of insectivorous birds and bats is well known to reduce the density of arboreal herbivorous arthropods but quantification of collateral leaf damage remains limited for temperate forest canopies. We conducted exclusion experiments with nets in the crowns of young and mature oaks, Quercus robur, in south and central Germany to investigate the extent to which aerial vertebrates reduce herbivory through predation. We repeatedly estimated leaf damage throughout the vegetation period. Exclusion of birds and bats led to a distinct increase in arthropod herbivory, emphasizing the prominent role of vertebrate predators in controlling arthropods. Leaf damage (e.g., number of holes) differed strongly between sites and was 59% higher in south Germany, where species richness of vertebrate predators and relative oak density were lower compared with our other study site in central Germany. The effects of bird and bat exclusion on herbivory were 19% greater on young than on mature trees in south Germany. Our results support previous studies that have demonstrated clear effects of insectivorous vertebrates on leaf damage through the control of herbivorous arthropods. Moreover, our comparative approach on quantification of leaf damage highlights the importance of local attributes such as tree age, forest composition and species richness of vertebrate predators for control of arthropod herbivory.     

Coqui frog invasions change invertebrate communities in Hawaii

The Puerto Rican coqui frog (Eleutherodactylus coqui) invaded Hawaii in the late 1980s. Because the coqui reaches high densities and consumes large quantities of invertebrates, it was hypothesized to change invertebrate communities where it invades. Previous research found that coquis can change invertebrate communities, but these studies used highly manipulative, small-scale experiments. The objective of this research was to determine whether coquis create community-level changes in invertebrate communities at the landscape scale. We collected leaf litter, flying, and foliage invertebrates on both sides of 15 coqui invasion fronts across the island of Hawaii. Multivariate analyses show that coquis are associated with changes in leaf-litter communities, primarily reductions in Acari, but are not associated with overall changes in flying or foliage communities. Across sites, coquis reduced the total number of leaf-litter invertebrates by 27%, specifically by reducing Acari by 36%. Across sites, coquis increased flying Diptera by 19%. Changes were greater where coqui densities were higher. We suggest that coquis changed leaf-litter communities primarily through direct predation, but that they increased Diptera through the addition of frog carcasses and excrement. Results support previous studies conducted in more controlled settings, but add to our understanding of the invasion by showing that coqui effects on invertebrate communities are measurable at the landscape scale.     

Asymmetric Contribution of Isotopically Contrasting Food Sources to Vertebrate Consumers in a Subtropical Semi‐arid Ecosystem

Habitat heterogeneity is a primary ecological factor that is particularly pronounced in arid ecosystems. The Tehuacán valley is a subtropical semi‐arid ecosystem in which several species of columnar cacti and agave (i.e., CAM plants) constitute the dominant elements accompanied by patches of trees and shrubs (i.e., C₃ plants). Vegetation in Tehuacán is isotopically heterogenous because CAM plants have less depleted δ¹³C values than C₃ plants. Fruits and flowers of cactus and agaves offer abundant food to vertebrates, but their leaves might be less attractive to insects than the leaves of C₃ plants. Therefore, we use carbon and nitrogen stable isotope analysis to test the hypothesis that C₃ and CAM food would contribute asymmetrically to different guilds of birds and bats. We predict that granivorous and frugivorous birds and nectarivorous and frugivorous bats will consume a CAM diet, whereas insectivorous birds and bats will consume a C₃ diet. Due to omnivory of bird and bat consumers, we predict that the importance of CAM food will decrease as the trophic level of the animal increases. Our results showed that CAM food predominated in plant‐eating birds and in some flower‐visiting bats, whereas C₃ food predominated in insect‐eating bats and birds and frugivorous bats. Habitat heterogeneity in Tehuacán is important for conservation due to the asymmetric role of CAM and C₃ food in the nutrition of different feeding guilds of vertebrates. Our study provides basic information to evaluate the potential impact of habitat loss on functional groups of consumers in a semi‐arid ecosystem.     

Parallel trends in the species diversity of west indian birds and bats

Summary In this paper I compare several biogeographic patterns of West Indian resident land birds and bats, including species-area and trophic diversity-area relationships, the number of islands inhabited per species and levels of endemism, trophic structure as compared with tropical mainland areas, and the degree of faunal simlarity between islands of similar sizes but different locations. In most respects, the bat and bird patterns are strikingly similar. Groups of birds that are conspicuously missing from the Antilles because of the absence of appropriate resources also have missing chiropteran counterparts. Plant-visiting bats and birds are better-represented in terms of relative number of species and, in birds, in biomass, on the Lesser Antilles than on the mainland (e.g. Panama). Small Antillean islands tend to share more species of birds and bats than do larger islands. Stochastic (sensu Simberloff 1978), deterministic, and interactive (e.g. competitive and trophic interactions) factors appear to underly these biogeographic trends. No evidence exists to suggest that Caribbean bats and birds have negatively affected each other's diversity.     

Detection probabilities of two introduced frogs in Hawaii: implications for assessing non-native species distributions

Two nonnative Caribbean frogs, the Puerto Rican coqui and the Cuban greenhouse frog, recently invaded Hawaii. Because of its louder breeding call, management efforts have focused on the coqui, while little has been done to address the more cryptic greenhouse frog, even though it may be as widespread and have similar ecological impacts. The goal of this research was to determine the distribution and detection probability of both species on the island of Hawaii. We conducted a breeding call presence/absence survey at 446 sites every 2 km along major road networks. We re-surveyed 125 sites twice to determine detection and occupancy probabilities. Greenhouse frog detection probabilities (0.24, 0.29, 0.48, for each of the three visits, respectively) were lower than coqui detection probabilities (0.58, 0.73, 0.50, respectively) and increased with visits while those of the coqui did not. Greenhouse frog detection probabilities were lower in the presence of coquis for the first two surveys (0.12, 0.14) than in sites with greenhouse frogs alone (0.41), while greenhouse frogs had no effect on the detection of coquis. Site occupancy estimates for the greenhouse and coqui frog were 0.35 and 0.31, respectively, suggesting the species are similarly widespread. Results suggest multiple visits to sites are required to detect the greenhouse frog. Furthermore, results suggest that accounting for detectability is essential when determining the extent of invasion of cryptic species.     

Isolation of polymorphic microsatellite loci in the Hawaii amakihi (Hemignathus virens) and their use in other honeycreeper species

We report the isolation and characterization of five polymorphic microsatellite loci in the Hawaii amakihi, Hemignathus virens, one of the most common native Hawaiian forest birds. These loci exhibit high levels of allelic diversity and heterozygosity in the three honeycreeper species we screened, and promise to be useful in our investigation of differences between honeycreeper populations at different elevations.     

吸血蝙蝠食性特化及其研究现状

翼手目动物（蝙蝠）的食性多样性丰富,其食物包括昆虫、鱼类、两栖动物、爬行动物、鸟类、哺乳动物、植物果实、花、花粉、花蜜、叶片和血液等。其中,大约70%的蝙蝠主要以昆虫为食,而以血液为食的吸血蝙蝠只有3种,它们是哺乳动物中唯一的仅以血液为食的动物类群。因此,吸血蝙蝠是研究动物食性演化的重要模式动物。本文综述了吸血蝙蝠在形态学、生理学、行为学、感觉系统和肠道微生物等方面的研究,指出了吸血蝙蝠食性特化的适应性特征。随着普通吸血蝠高质量基因组的公布,我们将有机会探究食性相关基因在吸血蝙蝠中的功能改变,阐明动物食性转变的分子机理。本文将为吸血蝙蝠和其它动物食性转变的研究提供有益的参考。     

Concealed by darkness: interactions between predatory bats and nocturnally migrating songbirds illuminated by DNA sequencing

Recently, several species of aerial‐hawking bats have been found to prey on migrating songbirds, but details on this behaviour and its relevance for bird migration are still unclear. We sequenced avian DNA in feather‐containing scats of the bird‐feeding bat Nyctalus lasiopterus from Spain collected during bird migration seasons. We found very high prey diversity, with 31 bird species from eight families of Passeriformes, almost all of which were nocturnally flying sub‐Saharan migrants. Moreover, species using tree hollows or nest boxes in the study area during migration periods were not present in the bats’ diet, indicating that birds are solely captured on the wing during night‐time passage. Additional to a generalist feeding strategy, we found that bats selected medium‐sized bird species, thereby assumingly optimizing their energetic cost‐benefit balance and injury risk. Surprisingly, bats preyed upon birds half their own body mass. This shows that the 5% prey to predator body mass ratio traditionally assumed for aerial hunting bats does not apply to this hunting strategy or even underestimates these animals’ behavioural and mechanical abilities. Considering the bats’ generalist feeding strategy and their large prey size range, we suggest that nocturnal bat predation may have influenced the evolution of bird migration strategies and behaviour.     

Measures of the Constitutive Immune System Are Linked to Diet and Roosting Habits of Neotropical Bats

Ecological and social factors are central in the emergence and transmission of infectious diseases, thus bearing the potential for shaping a species’ immune functions. Although previous studies demonstrated a link between social factors and the cellular immune system for captive mammals, it is yet poorly understood how ecological factors are connected with the different branches of the immune system in wild populations. Here, we tested how variation in aspects of the constitutive cellular and humoral immune system of free ranging bats is associated with two ecological factors that likely influence the putative risk of species to become infected by parasites and pathogens: diet and shelter. We found that white blood cell counts of 24 syntopic Neotropical bat species varied with the species’ diet and body mass. Bats that included at least partially vertebrates in their diet exhibited the highest white blood cell counts, followed by phytophagous and insectivorous species, which is in agreement with the assumption that the immune system varies with the pathogen transmission risk of a trophic level. The soluble part of the constitutive immune response, assessed by an in vitro bacterial killing assay, decreased with increasing roost permanence. Our results suggest that the ecology is an important factor in the evolution of the immune system in bats and probably also other mammals.     

An appetite for pests: Synanthropic insectivorous bats exploit cotton pest irruptions and consume various deleterious arthropods

Conservation biological control (CBC) seeks to minimize the deleterious effects of agricultural pests by enhancing the efficiency of natural enemies. Despite the documented potential of insectivorous bats to consume pests, many synanthropic bat species are still underappreciated as beneficial species. We investigated the diet of Kuhl's pipistrelle (Pipistrellus kuhlii), a common synanthropic insectivorous bat that forages in urban and agricultural areas, to determine whether it may function as a natural enemy in CBC. Faecal samples of P. kuhlii were collected throughout the cotton‐growing season from five roost sites near cotton fields located in a Mediterranean agroecosystem, Israel, and analyzed using DNA metabarcoding. Additionally, data on estimated abundance of major cotton pests were collected. We found that the diet of P. kuhlii significantly varied according to sites and dates and comprised 27 species of agricultural pests that were found in 77.2% of the samples, including pests of key economic concern. The dominant prey was the widespread cotton pest, the pink bollworm, Pectinophora gossypiella, found in 31% of the samples and in all the roosts. Pink bollworm abundance was positively correlated with its occurrence in the bat diet. Furthermore, the bats’ dietary breadth narrowed, while temporal dietary overlap increased, in relation to increasing frequencies of pink bollworms in the diet. This suggests that P. kuhlii exploits pink bollworm irruptions by opportunistic feeding. We suggest that synanthropic bats provide important pest suppression services, may function as CBC agents of cotton pests and potentially contribute to suppress additional deleterious arthropods found in their diet in high frequencies.     

Genetic structure and evolved malaria resistance in Hawaiian honeycreepers

Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low‐elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re‐establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948–49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low‐elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life‐history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.