Insect functional morphology

Insect mouthparts represent modified arthropod appendages. This diversity of feeding devices provides numerous examples for the investigation of constraints and options in organ evolution. Our integrative approaches search for explanations of form-function relationships in the evolution of insect mouthparts in context with feeding techniques of flower-visiting insects.

 Research topics

Flower visiting beetles as potential pollinators

Interdisciplinary research network of the faculty - 2016

The cooperation among zoologists and botanists at the Faculty of Life Sciences investigates flower visiting beetles. Although anthophilous Coleoptera and cantharophilous flowers are regarded to play an insignificant role in European and North American pollination systems, increasing evidence demonstrates that beetles have to be considered one of the “big four” of insect orders that crucially contribute to plant pollination at the global level. In general, beetles are uncouth pollinators and their activity on flowers has been called “soil and mess” pollination as they often destroy floral organs with their mouthparts. A particularly interesting case is pollination by monkey beetles (Scarabaeidae: Hopliini), which represent a species- rich and important group of pollinating insects in the Cape Floristic Region of South Africa where many endemic species are associated with a wide range of plant species. Monkey beetles visit flowers to feed on pollen, nectar, and/or floral tissue. In addition, they use specific flowers as aggregation places where males fight for females.

(1) Our study will focus on flowers that are visited by “embedded feeding” beetles that are destructive to flowers by feeding on floral tissue. We will use high resolution microCT to quantify the destruction caused by the beetles to the different floral organs.

(2) We plan to evaluate the role of flowers as mating places in the life history of monkey beetles.

(3) The importance of fighting male beetles for pollination should be investigated. We hypothesize that certain flowers may counterbalance destructive feeding by offering fighting arenas for pollinating beetles.

> Krenn HW, Fournel J, Bauder JA-S, Hugel S (2016) Mouthparts and nectar feeding of the flower visiting cricket Glomeremus orchidophilus (Gryllacrididae). Arthropod Structure & Development 45: 221-229.

> Karolyi F, Hansal T, Krenn, HW, Colville JF (2016) Comparative morphology of the mouthparts of the megadiverse South African monkey beetles (Scarabaeidae: Hopliini): feeding adaptations and guild structure. PeerJ 4:e1597; DOI 10.7717/peerj.159

Evolutionary morphology of mouthparts of flower visiting insects

Insect mouthparts represent modified arthropod extremities which have evolved in response to different demands of food uptake. Convergent evolutionary trends lead from ancestral biting mouthparts to derived proboscides in many groups of flower visiting insects as a result of the necessity to localize and to take up nectar from deep floral tubes or to feed on pollen.

The diversity of feeding devices in flower-visiting insects provides numerous examples for the investigation of constraints and options of organ evolution. Starting with Lepidoptera and a comparison of the sucking mouthparts or pollen-feeding organs of Neuroptera, Coleoptera, Diptera and Hymenoptera, an integrative approach can provide explanations for form and function relationships in the evolution of insect mouthparts.

For example, adult lepidopteran mouthparts show a wide range of forms, including the ancestral biting mouthparts in primarily pollen-feeding moths, the elongated proboscis of nectar-feeding species, the specialized proboscis of lachryphagous, fruit and skin-piercing species, and the derived proboscis of fruit-feeding or secondary pollen-feeding butterflies. Therefore, Lepidoptera represent a useful model to investigate the morphological, physiological and behavioral adaptations to different feeding habits.

The proboscis of butterflies is primarily adapted for localizing and sucking nectar out of floral tubes. It consists of two elongated mouthpart structures that are tightly linked together, at the tip are slit openings for the uptake of fluids. Precise and rapid action of the proboscis is crucial for efficient foraging in flower-visiting butterflies. Apart from the dimensions of the feeding apparatus, the importance of the sensory organs in localizing concealed floral rewards is paramount.

In the Nymphalidae (s. l.) many other kinds of feeding habits exist. For example, the pollen-feeding Heliconius butterflies use their proboscis to collect and process pollen, in addition to feed on nectar. Current research is focused on proboscis morphology, its movements and the mechanisms of gaining nutrients from pollen.

Fruit-feeding nymphalids of several subfamilies hardly ever visit flowers to obtain nutrition. Instead they feed on rotting fruits, tree sap or decaying organic matter. For these specialized feeding preferences, the butterflies have acquired adaptations in morphology and feeding behavior.

> Krenn HW (1998) Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera) - functional morphology and significance in flower-probing. Zoomorphology. 118: 23-30 PDF

> Krenn HW, Zulka KP, Gatschnegg T (2001) Proboscis morphology and food preferences in Nymphalidae (Lepidoptera, Papilionoidea). Journal of Zoology, London 253, 17-26 PDF

> Molleman F, Krenn HW, Van Alphen ME, Brakefield PM, DeVries PJ, Zwaan BJ (2005) Food intake of fruit-feeding butterflies: evidence for adaptive variation in proboscis morphology. Biological Journal of the Linnean Society 86, 333-34

A comparison of mouthpart morphology in various flower-visiting insects revealed several characteristic form-function relationships of the nectar-feeding and pollen-feeding insects. For example, in nectar-feeding insects, two modes are distinguished: fluid uptake by adhesion and by suction. For nectar sucking, the elongation of the mouthparts and the formation of a functionally sealed food tube with a special uptake region at the apex are essential.
Pollen-feeding mouthparts are characterized by specialized uptake structures which are, at least in some species, moistened to enhance adhesion of pollen.

> Krenn HW, Plant J, Szucsich NU (2005) Mouthparts of flower-visiting insects. Arthopod Strucutre & Development 34: 1-40. PDF

> Krenn HW, Gereben-Krenn B-A, Steinwender BM, Popov A (2008) Flower visiting Neuroptera: Mouthparts and feeding behaviour of Nemoptera sinuta (Nemopteridae). Eur. J. Entomol. 105: 267-277. PDF

> Karolyi F, Gorb SN & Krenn HW (2009) Pollen grains adhere to the moist mouthparts in the flower visiting beetle Cetonia aurata (Scarabaeidae, Coleoptera). Arthopod-Plant Interactions 3: 1-8 PDF

> Wilhemi A, Krenn HW (2012) Elongated mouthparts of nectar-feeding Meloidae (Coleoptera). Zoomorphology 131: 325-337 DOI: 10.1007/s00435-012-0162-3

Structural novelties in organ evolution: morphological innovations in the mouthparts of Lepidoptera

FWF research project P 13944-Bio

The evolution of novel organs is central theme in morphology and evolutionary biology. Such morphological innovations often emerge as interactions between adaptations to new environmental conditions and functional constraints resulting from new form-function relationships. Starting with the ancestral musculature in basal Lepidoptera, the origin, the evolution and functional role of the novel complex musculature of derived groups could be revealed. A comparative investigation of the sensory equipment in electron microscopy allows conclusions to be drawn on the evolutionary origin of the bizarre proboscis tip sensilla. The modified sensilla probably evolved as adaptations to new food sources in specialized butterflies.

> Krenn HW, Kristensen NP (2000) Early evolution of the proboscis of Lepidoptera: external morphology of the galea in basal glossatan moths, with remarks on the origin of the pilifers. Zoologischer Anzeiger 239: 179-196 PDF
> Krenn HW, Kristensen NP (2004) Evolution of proboscis musculature in Lepidoptera. European Journal of Entomology 101: 565-575 PDF

> Barcaba T, Krenn HW (2015) The mouthparts of adult Indian meal moths, Plodia interpunctella (HÜBNER 1813) (Lepidoptera: Pyralidae). Entomologia Austriaca 22: 91-105.

The evolutionary origin of a complex new mouthpart organ could be reconstructed in Yucca moths. This tentacular organ is endowed with separate musculature and sensilla, and it does not have a homolog organ in related taxa. The organ evolved in the female Yucca moths in context with the coevolutionary interaction of pollination of the larval food plant. The comparative investigation of the morphology of these organs led to the establishment of a hypothesis for the development of new complex organs that is based on the shift of existing genetic templates to other organs.

> Pellmyr O, Krenn HW (2002) Origin of a complex key innovation in an obligate insect-plant mutualism. Proceedings of the National Academy of Science 99/8: 5498-5502. PDF

The mouthparts of Lepidoptera provide an ideal opportunity to investigate the development and evolution of novel muscle systems in phylogenetic context. The butterfly proboscis has been excellently studied in ecomorphological and behavioral aspects of derived feeding preferences. Furthermore, the butterfly proboscis provides the best-investigated model for a hydraulic mechanism in a non-articulate arthropod appendage.

> Krenn HW (2010) Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annual Review of Entomology 55: 307-327

Pollen feeding in butterflies: evolution of a new mechanism of nutrient extraction

FWF research project P 18245-B03

The evolution of a novel feeding behavior in Heliconius butterflies includes complex adaptations of form and function in organs in association with the available food plants. In an integrative approach we combine morphological methods (LM and EM-techniques), chemical analysis and experimental work in the laboratory of the University of Vienna and field studies in La Gamba Biological Station (Costa Rica). Understanding the mechanism of pollen-feeding allows conclusions to be made on the evolution of this key innovation which is pivotal for the sophisticated behavior exhibited by this genus of Neotropical butterflies.

> Eberhard, SH, Hikl A-L, Boggs CL, Krenn HW (2009) Saliva or regurgitated nectar? What Heliconius butterflies (Lepidoptera: Nymphalidae) use for pollen feeding. Entomol Soc America 102/6: 1105-1108 PDF

> Krenn HW, MJB Eberhard, SH Eberhard, A-L Hikl, W Huber & LE Gilbert (2009) Mechanical damage to pollen aids nutrient acquisition in Heliconius butterflies (Nymphalidae) Arthopod-Plant Interactions 3/4: 203-208 PDF

> Eberhard SH, Nemeschkal HL & Krenn HW (2009) Biometrical evidence for adaptation of the salivary glands to pollen-feeding Heliconius butterflies (Lepidoptera: Nymphalidae). Biological Journal of the Linnnean Society 97: 604-612 PDF

> Hikl A-L, Krenn HW (2011) Pollen processing behaviour of Heliconius butterflies: A derived grooming behaviour. Journal of Insect Science 11, Article 95, available online:

Extremely long mouthparts in flower-visiting insects: form, function and evolution

FWF research project P 22248 B17 

Extremely long mouthparts that serve for the uptake of nectar in flower-visiting insects provide ample opportunity to examine constraints on organ evolution. The majority of the flower-visiting insects are regarded as short-tongued since their mouthparts are shorter than the head, while extremely long proboscides which exceed body length are rare. Advantages of long proboscides have been previously formulated and examined in the context of nectar-feeding from long spurred flowers. The project represents the first attempt to evaluate the costs of long mouthparts. The research will compare flower-visiting insects which have an average-sized tubular proboscis with related species having extremely long mouthparts.

> Bauder J, Lieskonig N, Krenn HW (2011) The extremely long-tongued Neotropical butterfly Eurybia lycisca (Riodinidae): Proboscis morphology and flower handling. Arthropod Structure & Development 40: 122-127.

>Karolyi F, Morawetz L, Colville JF, Handschuh F, Metscher BD, Krenn HW (2013)Time management and nectar flow: flower handling and suction feeding in long-proboscid flies (Nemestrinidae: Prosoeca). Naturwissenschaften 100: 1083-1093, DOI 10.1007/s00114-013-1114-6.

> Karolyi F, Colville JF., Handschuh S, Metscher BD, Krenn HW. (2014) One proboscis, two tasks: Adaptations to blood-feeding and nectar-extracting in long-proboscid horse flies (Tabanidae, Philoliche). Arthropod Structure & Development 43: 403-413

> Bauder, J. A.-S. Warren A. D. and Krenn H. W. (2014) Evolution of extreme proboscis lengths in Neotropical Hesperiidae (Lepidoptera) The Journal of Research on the Lepidoptera 47: 65-71.

> Bauder J, Morawetz L, Warren A, Krenn HW (2015) Functional constraints on the evolution of long butterfly proboscides: Lessons from Neotropical skippers (Lepidoptera: Hesperiidae) Journal of Evolutionary Biology 28: 678-687.

> Bauder J, Warren A, Krenn HW (2015) The ecological role of extremely long-proboscid Neotropical butterflies (Lepidoptera: Hesperiidae) in plant-pollinator networks. Arthropod Plant Interactions 9, 415-424.