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The sensory morphology of insect pollinators: From structure to behaviour and ecology
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-0203-8216
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Insect pollinators play an important role in balancing our ecosystems and maintaining plant and food diversity. Due to anthropogenic activities such as global warming, habitat loss and degradation, pesticides, and pathogens, many pollinator populations have been undergoing drastic declines in recent decades. Sudden changes in environmental conditions may lead to selection pressures to alter sensory systems, their structures and functions, and, consequently, behaviour. Despite the multitude of studies on insect pollinators and their population declines, these effects are often overlooked. To address this knowledge gap, I studied the morphology of sensory systems in butterflies and bumblebees – two pollinator groups found in temperate regions – from the aspects of development, behaviour, ecology and adaptation. In Chapter I, I used allometry to study how investment into sensory systems varies within and between different sexes of the butterfly Pieris napi. I measured the size and other parameters of sensory traits including eyes, antennae, proboscis, and wings. I showed that sensory system investment varies between sexes and only antennal length and wing size increase allometrically with body size. These findings suggest that not all sensory organs scale with body size and energetic investment between them can vary among sexes of the same species. In Chapter II, I explored the effect of a sub-optimal temperature on the development and morphology of sensory systems in P. napi, an ectothermic solitary insect. I exposed the pupae of P. napi to 23°C (optimal temperature) and 32°C (sub-optimal temperature) and measured their body and sensory organ size after emergence. I found that the mortality rate was higher at the suboptimal temperature and that the eclosion time decreased. Also, body and proboscis size decreased in both sexes, while antennal length decreased only in males. These results show that global warming can have negative consequences for the survival of butterflies and affect the size of their sensory systems potentially by accelerating the developmental process. In Chapter III, we studied the effect of heatwave-like temperatures on the sensory systems and behaviour of another insect pollinator, Bombus terrestris. Our results revealed that development in suboptimal temperatures had a negative impact on behavioural responses of bumblebee workers. Interestingly, the elevated temperature did not have a significant effect on the size of their antennae, eyes and forewings. These findings indicate that an elevated developmental temperature can impair important behavioural responses to sensory stimuli without causing any visible changes in sensory organ morphology. In Chapter IV, I explored how well the qualitative light micro habitat associated with a distribution range of insects, matches with carefully measured quantitative values. I used three butterfly species (P. napi, Pararge aegeria, Vanessa atalanta) that are associated with different light habitats and have different dispersal ranges. The results showed that only P.napi distribution was affected by light intensity. Eye and brain neuropil investment varied among the three species. P. napi had highest eye size investment while V. atalanta had highest optic neuropils investment. These findings suggest that visual and neural investments could only in part be associated with quantitative and/or qualitative light micro habitat and dispersal in these species.

Abstract [sv]

Insektpollinatörer spelar en viktig roll för att balansera våra ekosystem och upprätthålla mångfalden av växter och livsmedel. På grund av antropogena aktiviteter såsom global uppvärmning, förlust och försämring av livsmiljöer, bekämpningsmedel och patogener har många pollinatorpopulationer genomgått drastiska minskningar under de senaste decennierna. Plötsliga förändringar i livsmiljöer kan påverka utvecklingen av insekters sensorsystem och leda till förändringar i deras morfologi, funktion och därigenom beteende. Trots mängden av studier om insektpollinatörer och deras minskande populationer, så förbises ofta effekten av förändrade livsmiljöer på deras sensorsystem. För att fylla denna kunskapslucka studerade jag morfologin hos sensorsystemen hos fjärilar och humlor - två pollinatorgrupper som återfinns i tempererade områden - med avseende på utveckling, beteende, ekologi och anpassning. I Kapitel I använde jag allometri för att studera hur investeringen i sensorsystem varierar inom och mellan olika kön hos fjärilen Pieris napi. Jag mätte storlek och andra parametrar för sensorsystem, inklusive ögon, antenner, snabel och vingar. Jag visade att investeringen i sensorsystem varierar mellan könen och att endast antennlängd och vingstorlek ökar allometriskt med kroppsstorlek. Dessa resultat antyder att inte alla sensorsystem skalar med kroppsstorlek och den energetiska investeringen mellan dem kan variera mellan könen av samma art. I Kapitel II utforskade jag effekten av en suboptimal temperatur på utvecklingen och morfologin av sensorsystem hos P. napi, en ektotherm solitär insekt. Jag exponerade puppor av P. napi för 23°C (optimal temperatur) och 32°C (suboptimal temperatur) och mätte deras kroppsstorlek och storlek på sensorsystemen efter uppkomst. Jag fann att dödligheten var högre vid den suboptimala temperaturen och att uppkomsttiden minskade. Dessutom minskade kroppsstorleken och snabelns storlek hos båda könen, medan antennlängden endast minskade hos hanar. Dessa resultat visar att global uppvärmning kan ha negativa konsekvenser för fjärilars överlevnad och påverka storleken på deras sensorsystem, eventuellt genom att accelerera utvecklingsprocessen. I Kapitel III studerade vi effekten av värmeböljeliknande temperaturer på sensorsystem och beteende hos en annan insektpollinatör, Bombus terrestris. Våra resultat visade att utveckling vid suboptimala temperaturer hade en negativ inverkan på beteendesvar hos humlearbetare. Intressant nog hade den höjda temperaturen ingen signifikant effekt på storleken av deras antenner, ögon och framvingar. Dessa resultat indikerar att en ökad utvecklingstemperatur kan försämra viktiga beteendesvar på sensorsignaler utan att orsaka synliga förändringar i morfologin hos sensorsystemen. I Kapitel IV utforskade jag hur väl den kvalitativa ljusmikromiljön som är förknippad med en utbredningsområde för insekter överensstämmer med noggrant mätta kvantitativa värden. Jag använde tre fjärilarter (P. napi, Pararge aegeria, Vanessa atalanta) som är förknippade med olika ljusmiljöer och har olika spridningsområden. Resultaten visade att endast fördelningen av P. napi påverkades av ljusintensiteten. Investeringen i ögon och hjärnnervvävnad varierade mellan de tre arterna, men denna variation hade ingen tydlig relation till deras kvalitativa eller kvantitativa ljusmiljö. Därför kunde jag visa att noggrann bedömning av ljusmiljöer är avgörande för att förstå och tolka visuella och neurala anpassningar hos insekter.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2023. , p. 31
Keywords [en]
Insect pollinators, butterfly, bumblebee, sensory system, developmental temperature, light habitat
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
URN: urn:nbn:se:su:diva-222642ISBN: 978-91-8014-542-8 (print)ISBN: 978-91-8014-543-5 (electronic)OAI: oai:DiVA.org:su-222642DiVA, id: diva2:1804860
Public defence
2023-12-08, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2023-11-02 Created: 2023-10-13 Last updated: 2023-11-13Bibliographically approved
List of papers
1. Sensory Organ Investment Varies with Body Size and Sex in the Butterfly Pieris napi
Open this publication in new window or tab >>Sensory Organ Investment Varies with Body Size and Sex in the Butterfly Pieris napi
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2021 (English)In: Insects, ISSN 2075-4450, E-ISSN 2075-4450, Vol. 12, no 12, article id 1064Article in journal (Refereed) Published
Abstract [en]

In solitary insect pollinators such as butterflies, sensory systems must be adapted for multiple tasks, including nectar foraging, mate-finding, and locating host-plants. As a result, the energetic investments between sensory organs can vary at the intraspecific level and even among sexes. To date, little is known about how these investments are distributed between sensory systems and how it varies among individuals of different sex. We performed a comprehensive allometric study on males and females of the butterfly Pieris napi where we measured the sizes and other parameters of sensory traits including eyes, antennae, proboscis, and wings. Our findings show that among all the sensory traits measured, only antenna and wing size have an allometric relationship with body size and that the energetic investment in different sensory systems varies between males and females. Moreover, males had absolutely larger antennae and eyes, indicating that they invest more energy in these organs than females of the same body size. Overall, the findings of this study reveal that the size of sensory traits in P. napi are not necessarily related to body size and raises questions about other factors that drive sensory trait investment in this species and in other insect pollinators in general.

Keywords
Pieris napi, eye, antenna, wing, proboscis, allometry, sensory system, body size
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-201275 (URN)10.3390/insects12121064 (DOI)000737891000001 ()34940152 (PubMedID)
Available from: 2022-01-24 Created: 2022-01-24 Last updated: 2023-10-13Bibliographically approved
2. Exposure to elevated temperature during development affects eclosion and morphology in the temperate Pieris napi butterfly (Lepidoptera: Pieridae)
Open this publication in new window or tab >>Exposure to elevated temperature during development affects eclosion and morphology in the temperate Pieris napi butterfly (Lepidoptera: Pieridae)
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(English)In: Article in journal (Other academic) Accepted
Keywords
Developmental temperature, Sensory organs, Body parts, Mortality, Eclosion, Climate change
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-222633 (URN)
Funder
Swedish Research Council
Available from: 2023-10-13 Created: 2023-10-13 Last updated: 2023-10-30
3. Heatwave-Like Events During Development Are Sufficient to Impair Bumblebee Worker Responses to Sensory Stimuli
Open this publication in new window or tab >>Heatwave-Like Events During Development Are Sufficient to Impair Bumblebee Worker Responses to Sensory Stimuli
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2022 (English)In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 9, article id 776830Article in journal (Refereed) Published
Abstract [en]

Heatwaves are increasingly common globally and are known to have detrimental impacts on animal morphology and behaviour. These impacts can be severe, especially if heatwaves occur during development, even on animals that can regulate the temperature of their developing young. The onset and duration of heatwaves are stochastic and therefore may affect all or only part of development. In the heterothermic bumblebee Bombus terrestris, elevated temperatures over the entirety of development cause morphological changes in adults, despite their capability to regulate brood temperature. However, the effects of heatwaves that occur during a short period of development are unclear. We test the impact of elevated developmental temperature during the latter fraction of development on the behaviour and morphology of adult worker B. terrestris. We show that exposure to elevated temperature over a portion of late development is sufficient to impair the initial behavioural responses of workers to various sensory stimuli. Despite this, exposure to elevated temperatures during a period of development did not have any significant impact on body or organ size. The negative effect of elevated developmental temperatures was independent of the exposure time, which lasted from 11–20 days at the end of the workers’ developmental period. Thus, heat stress in bumblebees can manifest without morphological indicators and impair critical behavioural responses to relevant sensory stimuli, even if only present for a short period of time at the end of development. This has important implications for our understanding of deleterious climactic events and how we measure indicators of stress in pollinators.

Keywords
bumblebee, heatwave, behaviour, sensory system, reflex, Bombus terrestris
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-202748 (URN)10.3389/fevo.2021.776830 (DOI)000756036200001 ()
Available from: 2022-03-11 Created: 2022-03-11 Last updated: 2023-10-13Bibliographically approved
4. How variations in light micro-habitats reflect on visual and neural adaptations in three temperate butterfly species
Open this publication in new window or tab >>How variations in light micro-habitats reflect on visual and neural adaptations in three temperate butterfly species
(English)Manuscript (preprint) (Other academic)
Keywords
light micro-habitat, Vision, Brain, Neuropil, Butterfly, Pararge aegeria, Pieris napi, Vanessa Atalanta
National Category
Zoology
Research subject
Functional Zoomorphology; Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-222639 (URN)
Funder
Swedish Research Council
Available from: 2023-10-13 Created: 2023-10-13 Last updated: 2023-10-13

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