Vertical stratification and defensive traits of caterpillars against parasitoids in a lowland tropical forest in Cameroon.

Insect herbivores and their parasitoids play a crucial role in terrestrial trophic interactions in tropical forests. These interactions occur across the entire vertical gradient of the forest. This study compares how caterpillar communities, and their parasitism rates, vary across vertical strata and between caterpillar defensive strategies in a semi deciduous tropical forest in Nditam, Cameroon. Within a 0.1 ha plot, all trees with a diameter at breast height (DBH) ≥ 5 cm were felled and systematically searched for caterpillars. We divided the entire vertical gradient of the forest into eight, five-metre strata. All caterpillars were assigned to a stratum based on their collection height, reared, identified, and classified into one of three defensive traits: aposematic, cryptic and shelter-building. Caterpillar species richness and diversity showed a midstory peak, whereas density followed the opposite pattern, decreasing in the midstory and then increasing towards the highest strata. This trend was driven by some highly dense shelter-building caterpillars in the upper canopy. Specialisation indices indicated decreasing levels of caterpillar generality with increasing height, a midstory peak in vulnerability, and increasing connectance towards the upper canopy, although the latter was likely driven by decreasing network size. Both aposematic and shelter-building caterpillars had significantly higher parasitism rates than cryptic caterpillars. Our results highlight nuanced changes in caterpillar communities across forest strata and provide evidence that defences strategies are important indicators of parasitism rates in caterpillars and that both aposematic and shelter-building caterpillars could be considered a "safe haven" for parasitoids.

Tropical butterflies use thermal buffering and thermal tolerance as alternative strategies to cope with temperature increase.

Climate change poses a severe threat to many taxa, with increased mean temperatures and frequency of extreme weather events predicted. Insects can respond to high temperatures using behaviour, such as angling their wings away from the sun or seeking cool local microclimates to thermoregulate or through physiological tolerance. In a butterfly community in Panama, we compared the ability of adult butterflies from 54 species to control their body temperature across a range of air temperatures (thermal buffering ability), as well as assessing the critical thermal maxima for a subset of 24 species. Thermal buffering ability and tolerance were influenced by family, wing length, and wing colour, with Pieridae, and butterflies that are large or darker in colour having the strongest thermal buffering ability, but Hesperiidae, small, and darker butterflies tolerating the highest temperatures. We identified an interaction between thermal buffering ability and physiological tolerance, where species with stronger thermal buffering abilities had lower thermal tolerance, and vice versa. This interaction implies that species with more stable body temperatures in the field may be more vulnerable to increases in ambient temperatures, for example heat waves associated with ongoing climate change. Our study demonstrates that tropical species employ diverse thermoregulatory strategies, which is also reflected in their sensitivity to temperature extremes.

El cambio climático representa una grave amenaza para muchos taxones, con un aumento de las temperaturas medias y la frecuencia de eventos climáticos extremos pronosticados. Los insectos pueden responder a las altas temperaturas mediante comportamientos, como inclinar sus alas fuera del alcance del sol o buscar microclimas frescos locales para termorregular, o a través de la tolerancia fisiológica. En una comunidad de mariposas en Panamá, comparamos la capacidad de las mariposas adultas de 54 especies para controlar su temperatura corporal en un rango de temperaturas del aire (capacidad de amortiguación térmica), así como evaluar el máximo térmico crítico para un subconjunto de 24 especies. La capacidad de amortiguación térmica y la tolerancia se influenciaron por la familia, la longitud del ala y el colour del ala; con Pieridae y mariposas grandes o de colour más oscuro teniendo la capacidad de amortiguación térmica más fuerte, pero Hesperiidae, mariposas pequeñas y de colour más oscuro tolerando las temperaturas más altas. Identificamos una relación entre la capacidad de amortiguación térmica y la tolerancia fisiológica, en la que las especies con mayores capacidades de amortiguación térmica tenían una menor tolerancia térmica, y viceversa. Esta interacción implica que las especies con temperaturas corporales más estables en el campo pueden ser más vulnerables a los aumentos en las temperaturas ambientales, por ejemplo, las olas de calor asociadas con el cambio climático actual. Nuestra investigación demuestra que las especies tropicales emplean diversas estrategias de termorregulación, las cuales también se reflejan en su sensibilidad a las temperaturas extremas.

Thermoregulatory ability and mechanism do not differ consistently between neotropical and temperate butterflies.

Climate change is a major threat to species worldwide, yet it remains uncertain whether tropical or temperate species are more vulnerable to changing temperatures. To further our understanding of this, we used a standardised field protocol to (1) study the buffering ability (ability to regulate body temperature relative to surrounding air temperature) of neotropical (Panama) and temperate (the United Kingdom, Czech Republic and Austria) butterflies at the assemblage and family level, (2) determine if any differences in buffering ability were driven by morphological characteristics and (3) used ecologically relevant temperature measurements to investigate how butterflies use microclimates and behaviour to thermoregulate. We hypothesised that temperate butterflies would be better at buffering than neotropical butterflies as temperate species naturally experience a wider range of temperatures than their tropical counterparts. Contrary to our hypothesis, at the assemblage level, neotropical species (especially Nymphalidae) were better at buffering than temperate species, driven primarily by neotropical individuals cooling themselves more at higher air temperatures. Morphology was the main driver of differences in buffering ability between neotropical and temperate species as opposed to the thermal environment butterflies experienced. Temperate butterflies used postural thermoregulation to raise their body temperature more than neotropical butterflies, probably as an adaptation to temperate climates, but the selection of microclimates did not differ between regions. Our findings demonstrate that butterfly species have unique thermoregulatory strategies driven by behaviour and morphology, and that neotropical species are not likely to be more inherently vulnerable to warming than temperate species.

El calentamiento global es una gran amenaza para las especies alrededor del mundo, sin embargo, no se tiene bien definido sí en los insectos, las especies distribuídas en las zonas tropicales son más vulnerables a los cambios de temperature que las especies de zonas templadas o viceversa. Para responder a este interrogante, utilizamos un protocolo de campo estandarizado aplicado a especies de mariposas distribuídas en zonas tropicales (Panamá) versus zonas templadas (Reino Unido, República Checa y Austria), con el cual buscamos: (1) Evaluar la capacidad de amortiguación (capacidad de regular la temperatura corporal en relación con la temperatura del aire circundante) en el a nivel de ensamblaje y familia, (2) Determinar sí las diferencias en la capacidad de amortiguación es facilitada por sus características morfológicas, y (3) Investigar cómo las mariposas usan los microclimas y el comportamiento para termorregularse a tráves de mediciones de temperatura ecológicamente relevantes. Nuestra hipotesis incial soportaba que las mariposas templadas estaban adaptadas para amortiguar los cambios de temperatura en comparación con las mariposas neotropicales, ya que las especies templadas experimentan un rango más amplio de temperaturas que sus contrapartes tropicales. Contrariamente a nuestra hipótesis, a nivel de ensamble, las especies neotropicales (especialmente familia Nymphalidae) fueron mejores en la capaicidad de amortiguacion que las especies templadas, explicado por el hecho de que individuos se enfrían más a altas temperaturas del aire. Así, la morfología fué el principal impulsor de las diferencias en la capacidad de amortiguación entre las especies neotropicales y templadas en comparación con el ambiente térmico experimentado por las mismas. Encontramos que las mariposas templadas utilizaron la termorregulación de postura para elevar su temperatura corporal más que las mariposas neotropicales, probablemente como una adaptación a los climas templados, aunque la selección de microclimas no difirió entre regiones. Nuestros hallazgos demuestran que las especies de mariposas tienen estrategias de termorregulación únicas, impulsadas principalmente por el comportamiento y morfología, además nuestros resultados demuestran que a diferencia de lo que se ha pensado, las especies neotropicales son igual de vulnerables al calentamiento de su hábitat que las especies templadas.

Global insect decline is the result of wilful political failure: A battle plan for entomology.

The Millennium Ecosystem Assessment assessed ecosystem change, human wellbeing and scientific evidence for sustainable use of biological systems. Despite intergovernmental acknowledgement of the problem, global ecological decline has continued, including declines in insect biodiversity, which has received much media attention in recent years. Several roadmaps to averting biological declines have failed due to various economic and political factors, and so biodiversity loss continues, driven by several interacting human pressures. Humans are innately linked with nature but tend to take it for granted. The benefits we gain from the insect world are broad, yet aversion or phobias of invertebrates are common, and stand firmly in the path of their successful conservation. Providing an integrated synthesis for policy teams, conservation NGOs, academic researchers and those interested in public engagement, this article considers: (1) The lack of progress to preserve and protect insects. (2) Examples relating to insect decline and contributions insects make to people worldwide, and consequently what we stand to lose. (3) How to engage the public, governmental organizations and researchers through "insect contributions to people" to better address insect declines. International political will has consistently acknowledged the existence of biodiversity decline, but apart from a few narrow cases of charismatic megafauna, little meaningful change has been achieved. Public values are reflected in political willpower, the progress being made across the world, changing views on insects in the public should initiate a much-needed political sea-change. Taking both existing activity and required future actions, we outline an entomologist's "battle plan" to enormously expand our efforts and become the champions of insect conservation that the natural world needs.

Comparison of traditional and DNA metabarcoding samples for monitoring tropical soil arthropods (Formicidae, Collembola and Isoptera).

The soil fauna of the tropics remains one of the least known components of the biosphere. Long-term monitoring of this fauna is hampered by the lack of taxonomic expertise and funding. These obstacles may potentially be lifted with DNA metabarcoding. To validate this approach, we studied the ants, springtails and termites of 100 paired soil samples from Barro Colorado Island, Panama. The fauna was extracted with Berlese-Tullgren funnels and then either sorted with traditional taxonomy and known, individual DNA barcodes ("traditional samples") or processed with metabarcoding ("metabarcoding samples"). We detected 49 ant, 37 springtail and 34 termite species with 3.46 million reads of the COI gene, at a mean sequence length of 233 bp. Traditional identification yielded 80, 111 and 15 species of ants, springtails and termites, respectively; 98%, 37% and 100% of these species had a Barcode Index Number (BIN) allowing for direct comparison with metabarcoding. Ants were best surveyed through traditional methods, termites were better detected by metabarcoding, and springtails were equally well detected by both techniques. Species richness was underestimated, and faunal composition was different in metabarcoding samples, mostly because 37% of ant species were not detected. The prevalence of species in metabarcoding samples increased with their abundance in traditional samples, and seasonal shifts in species prevalence and faunal composition were similar between traditional and metabarcoding samples. Probable false positive and negative species records were reasonably low (13-18% of common species). We conclude that metabarcoding of samples extracted with Berlese-Tullgren funnels appear suitable for the long-term monitoring of termites and springtails in tropical rainforests. For ants, metabarcoding schemes should be complemented by additional samples of alates from Malaise or light traps.

More winners than losers over 12 years of monitoring tiger moths (Erebidae: Arctiinae) on Barro Colorado Island, Panama.

Understanding the causes and consequences of insect declines has become an important goal in ecology, particularly in the tropics, where most terrestrial diversity exists. Over the past 12 years, the ForestGEO Arthropod Initiative has systematically monitored multiple insect groups on Barro Colorado Island (BCI), Panama, providing baseline data for assessing long-term population trends. Here, we estimate the rates of change in abundance among 96 tiger moth species on BCI. Population trends of most species were stable (n = 20) or increasing (n = 62), with few (n = 14) declining species. Our analysis of morphological and climatic sensitivity traits associated with population trends shows that species-specific responses to climate were most strongly linked with trends. Specifically, tiger moth species that are more abundant in warmer and wetter years are more likely to show population increases. Our study contrasts with recent findings indicating insect decline in tropical and temperate regions. These results highlight the significant role of biotic responses to climate in determining long-term population trends and suggest that future climate changes are likely to impact tropical insect communities.

Spatial covariance of herbivorous and predatory guilds of forest canopy arthropods along a latitudinal gradient.

In arthropod community ecology, species richness studies tend to be prioritised over those investigating patterns of abundance. Consequently, the biotic and abiotic drivers of arboreal arthropod abundance are still relatively poorly known. In this cross-continental study, we employ a theoretical framework in order to examine patterns of covariance among herbivorous and predatory arthropod guilds. Leaf-chewing and leaf-mining herbivores, and predatory ants and spiders, were censused on > 1000 trees in nine 0.1 ha forest plots. After controlling for tree size and season, we found no negative pairwise correlations between guild abundances per plot, suggestive of weak signals of both inter-guild competition and top-down regulation of herbivores by predators. Inter-guild interaction strengths did not vary with mean annual temperature, thus opposing the hypothesis that biotic interactions intensify towards the equator. We find evidence for the bottom-up limitation of arthropod abundances via resources and abiotic factors, rather than for competition and predation.

Plant phylogeny drives arboreal caterpillar assemblages across the Holarctic.

Assemblages of insect herbivores are structured by plant traits such as nutrient content, secondary metabolites, physical traits, and phenology. Many of these traits are phylogenetically conserved, implying a decrease in trait similarity with increasing phylogenetic distance of the host plant taxa. Thus, a metric of phylogenetic distances and relationships can be considered a proxy for phylogenetically conserved plant traits and used to predict variation in herbivorous insect assemblages among co-occurring plant species.Using a Holarctic dataset of exposed-feeding and shelter-building caterpillars, we aimed at showing how phylogenetic relationships among host plants explain compositional changes and characteristics of herbivore assemblages.Our plant-caterpillar network data derived from plot-based samplings at three different continents included >28,000 individual caterpillar-plant interactions. We tested whether increasing phylogenetic distance of the host plants leads to a decrease in caterpillar assemblage overlap. We further investigated to what degree phylogenetic isolation of a host tree species within the local community explains abundance, density, richness, and mean specialization of its associated caterpillar assemblage.The overlap of caterpillar assemblages decreased with increasing phylogenetic distance among the host tree species. Phylogenetic isolation of a host plant within the local plant community was correlated with lower richness and mean specialization of the associated caterpillar assemblages. Phylogenetic isolation had no effect on caterpillar abundance or density. The effects of plant phylogeny were consistent across exposed-feeding and shelter-building caterpillars.Our study reveals that distance metrics obtained from host plant phylogeny are useful predictors to explain compositional turnover among hosts and host-specific variations in richness and mean specialization of associated insect herbivore assemblages in temperate broadleaf forests. As phylogenetic information of plant communities is becoming increasingly available, further large-scale studies are needed to investigate to what degree plant phylogeny structures herbivore assemblages in other biomes and ecosystems.

Vertical stratification of a temperate forest caterpillar community in eastern North America.

Vertical niche partitioning might be one of the main driving forces explaining the high diversity of forest ecosystems. However, the forest's vertical dimension has received limited investigation, especially in temperate forests. Thus, our knowledge about how communities are vertically structured remains limited for temperate forest ecosystems. In this study, we investigated the vertical structuring of an arboreal caterpillar community in a temperate deciduous forest of eastern North America. Within a 0.2-ha forest stand, all deciduous trees ≥ 5 cm diameter at breast height (DBH) were felled and systematically searched for caterpillars. Sampled caterpillars were assigned to a specific stratum (i.e. understory, midstory, or canopy) depending on their vertical position and classified into feeding guild as either exposed feeders or shelter builders (i.e. leaf rollers, leaf tiers, webbers). In total, 3892 caterpillars representing 215 species of butterflies and moths were collected and identified. While stratum had no effect on caterpillar density, feeding guild composition changed significantly with shelter-building caterpillars becoming the dominant guild in the canopy. Species richness and diversity were found to be highest in the understory and midstory and declined strongly in the canopy. Family and species composition changed significantly among the strata; understory and canopy showed the lowest similarity. Food web analyses further revealed an increasing network specialization towards the canopy, caused by an increase in specialization of the caterpillar community. In summary, our study revealed a pronounced stratification of a temperate forest caterpillar community, unveiling a distinctly different assemblage of caterpillars dwelling in the canopy stratum.

Quantitative assessment of plant-arthropod interactions in forest canopies: A plot-based approach.

Research on canopy arthropods has progressed from species inventories to the study of their interactions and networks, enhancing our understanding of how hyper-diverse communities are maintained. Previous studies often focused on sampling individual tree species, individual trees or their parts. We argue that such selective sampling is not ideal when analyzing interaction network structure, and may lead to erroneous conclusions. We developed practical and reproducible sampling guidelines for the plot-based analysis of arthropod interaction networks in forest canopies. Our sampling protocol focused on insect herbivores (leaf-chewing insect larvae, miners and gallers) and non-flying invertebrate predators (spiders and ants). We quantitatively sampled the focal arthropods from felled trees, or from trees accessed by canopy cranes or cherry pickers in 53 0.1 ha forest plots in five biogeographic regions, comprising 6,280 trees in total. All three methods required a similar sampling effort and provided good foliage accessibility. Furthermore, we compared interaction networks derived from plot-based data to interaction networks derived from simulated non-plot-based data focusing either on common tree species or a representative selection of tree families. All types of non-plot-based data showed highly biased network structure towards higher connectance, higher web asymmetry, and higher nestedness temperature when compared with plot-based data. Furthermore, some types of non-plot-based data showed biased diversity of the associated herbivore species and specificity of their interactions. Plot-based sampling thus appears to be the most rigorous approach for reconstructing realistic, quantitative plant-arthropod interaction networks that are comparable across sites and regions. Studies of plant interactions have greatly benefited from a plot-based approach and we argue that studies of arthropod interactions would benefit in the same way. We conclude that plot-based studies on canopy arthropods would yield important insights into the processes of interaction network assembly and dynamics, which could be maximised via a coordinated network of plot-based study sites.

The Saturniidae of Barro Colorado Island, Panama: A model taxon for studying the long-term effects of climate change?

We have little knowledge of the response of invertebrate assemblages to climate change in tropical ecosystems, and few studies have compiled long-term data on invertebrates from tropical rainforests. We provide an updated list of the 72 species of Saturniidae moths collected on Barro Colorado Island (BCI), Panama, during the period 1958-2016. This list will serve as baseline data for assessing long-term changes of saturniids on BCI in the future, as 81% of the species can be identified by their unique DNA Barcode Index Number, including four cryptic species not yet formally described. A local species pool of 60 + species breeding on BCI appears plausible, but more cryptic species may be discovered in the future. We use monitoring data obtained by light trapping to analyze recent population trends on BCI for saturniid species that were relatively common during 2009-2016, a period representing >30 saturniid generations. The abundances of 11 species, of 14 tested, could be fitted to significant time-series models. While the direction of change in abundance was uncertain for most species, two species showed a significant increase over time, and forecast models also suggested continuing increases for most species during 2017-2018, as compared to the 2009 base year. Peaks in saturniid abundance were most conspicuous during El Niño and La Niña years. In addition to a species-specific approach, we propose a reproducible functional classification based on five functional traits to analyze the responses of species sharing similar functional attributes in a fluctuating climate. Our results suggest that the abundances of larger body-size species with good dispersal abilities may increase concomitantly with rising air temperature in the future, because short-lived adults may allocate less time to increasing body temperature for flight, leaving more time available for searching for mating partners or suitable oviposition sites.

Taxonomic and functional composition of arthropod assemblages across contrasting Amazonian forests.

Arthropods represent most of global biodiversity, with the highest diversity found in tropical rain forests. Nevertheless, we have a very incomplete understanding of how tropical arthropod communities are assembled. We conducted a comprehensive mass sampling of arthropod communities within three major habitat types of lowland Amazonian rain forest, including terra firme clay, white-sand and seasonally flooded forests in Peru and French Guiana. We examined how taxonomic and functional composition (at the family level) differed across these habitat types in the two regions. The overall arthropod community composition exhibited strong turnover among habitats and between regions. In particular, seasonally flooded forest habitats of both regions comprised unique assemblages. Overall, 17·7% (26 of 147) of arthropod families showed significant preferences for a particular habitat type. We present a first reproducible arthropod functional classification among the 147 taxa based on similarity among 21 functional traits describing feeding source, major mouthparts and microhabitats inhabited by each taxon. We identified seven distinct functional groups whose relative abundance contrasted strongly across the three habitats, with sap and leaf feeders showing higher abundances in terra firme clay forest. Our novel arthropod functional classification provides an important complement to link these contrasting patterns of composition to differences in forest functioning across geographical and environmental gradients. This study underlines that both environment and biogeographical processes are responsible for driving arthropod taxonomic composition while environmental filtering is the main driver of the variance in functional composition.

Insect herbivores, chemical innovation, and the evolution of habit specialization in Amazonian trees.

Herbivores are often implicated in the generation of the extraordinarily diverse tropical flora. One hypothesis linking enemies to plant diversification posits that the evolution of novel defenses allows plants to escape their enemies and expand their ranges. When range expansion involves entering a new habitat type, this could accelerate defense evolution if habitats contain different assemblages of herbivores and/or divergent resource availabilities that affect plant defense allocation. We evaluated this hypothesis by investigating two sister habitat specialist ecotypes of Protium subserratum (Burseraceae), a common Amazonian tree that occurs in white-sand and terra firme forests. We collected insect herbivores feeding on the plants, assessed whether growth differences between habitats were genetically based using a reciprocal transplant experiment, and sampled multiple populations of both lineages for defense chemistry. Protium subserratum plants were attacked mainly by chrysomelid beetles and cicadellid hemipterans. Assemblages of insect herbivores were dissimilar between populations of ecotypes from different habitats, as well as from the same habitat 100 km distant. Populations from terra firme habitats grew significantly faster than white-sand populations; they were taller, produced more leaf area, and had more chlorophyll. White-sand populations expressed more dry mass of secondary compounds and accumulated more flavone glycosides and oxidized terpenes, whereas terra firme populations produced a coumaroylquinic acid that was absent from white-sand populations. We interpret these results as strong evidence that herbivores and resource availability select for divergent types and amounts of defense investment in white-sand and terra firme lineages of Protium subserratum, which may contribute to habitat-mediated speciation in these trees.

Evolution of Manduca sexta hornworms and relatives: biogeographical analysis reveals an ancestral diversification in Central America.

The hawkmoth genus Manduca is a diverse group of very large, conspicuous moths that has served as an important model across many biological disciplines. Two species in particular, the tobacco hornworm (Manduca sexta) and the tomato hornworm (Manduca quinquemaculatus) have been researched extensively. Studies across biological fields have referred to these two species as being closely related or even sister species, but the extent to which these two model organisms are related remains largely unknown. We conducted a comprehensive multi-gene phylogenetic analysis of Manduca, based on both an ML and Bayesian framework, which resulted in a monophyletic Manduca but only when two other genera, Dolba and Euryglottis are included. We tentatively conclude that the sister group to Manduca sexta comprises the Caribbean M. afflicta and M. johanni, and the sister lineage to this clade includes M. quinquemaculatus and the Hawaiian M. blackburni. Thus, M. sexta and M. quinquemaculatus are closely related, but are not sister species. Biogeographical analyses reveal an ancestral center of diversification in Central America, and Manduca appears to have subsequently colonized North and South America. Our phylogeny provides an important foundation for comparative studies of two model organisms and their relatives.

A comparison of two common flight interception traps to survey tropical arthropods.

Tropical forests are predicted to harbor most of the insect diversity on earth, but few studies have been conducted to characterize insect communities in tropical forests. One major limitation is the lack of consensus on methods for insect collection. Deciding which insect trap to use is an important consideration for ecologists and entomologists, yet to date few study has presented a quantitative comparison of the results generated by standardized methods in tropical insect communities. Here, we investigate the relative performance of two flight interception traps, the windowpane trap, and the more widely used malaise trap, across a broad gradient of lowland forest types in French Guiana. The windowpane trap consistently collected significantly more Coleoptera and Blattaria than the malaise trap, which proved most effective for Diptera, Hymenoptera, and Hemiptera. Orthoptera and Lepidoptera were not well represented using either trap, suggesting the need for additional methods such as bait traps and light traps. Our results of contrasting trap performance among insect orders underscore the need for complementary trapping strategies using multiple methods for community surveys in tropical forests.