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The visual ecology of bees - Tales of diverse eyes and behaviours

Tichit, Pierre LU (2021)
Abstract
The buzzing flight of bees is a popular summer hit. Yet, outside of a few familiar species of honeybees and bumblebees, these fantastic little creatures are still mostly unknown. With about twenty-five thousand species, bees are a very diverse group. They can be found in drastically different habitats. For example, some kinds of bumblebees endure the freezing temperatures and windswept tundra of Greenland, while others only thrive in the heat and humidity of the Amazonian forest. Some bees live in huge colonies with tens of thousands of members, while others live solitary lives. Some are narrower than a sesame seed, while others can reach the size of a human thumb. Despite these differences, bees all have in common the urge to visit... (More)
The buzzing flight of bees is a popular summer hit. Yet, outside of a few familiar species of honeybees and bumblebees, these fantastic little creatures are still mostly unknown. With about twenty-five thousand species, bees are a very diverse group. They can be found in drastically different habitats. For example, some kinds of bumblebees endure the freezing temperatures and windswept tundra of Greenland, while others only thrive in the heat and humidity of the Amazonian forest. Some bees live in huge colonies with tens of thousands of members, while others live solitary lives. Some are narrower than a sesame seed, while others can reach the size of a human thumb. Despite these differences, bees all have in common the urge to visit flowers where they find their food. This habit makes them very important for the pollination of plants across the world. To go about their laborious life, bees make extensive use of their vision. They possess two types of eyes – ocelli and compound eyes – that they use to control their flight, find their way through the world, discover flowers and spot possible mates. To understand how bees interact with the environment, we thus need to explore the diversity of their eyes and of how they use them.
The first chapter of my thesis is about landing, which is a fundamental behaviour in flying insects. However, in bees it is poorly known whether different species land in different ways. During an expedition to Brazil, I came across a species of bee with the most peculiar landing style. Rather than slowing down to land, as most animals do, these bees accelerate just before touchdown on the entrance to their hive. Why do these bees speed up when they land? Using a computer simulation, I found that this weird strategy may help the bees to avoid mid-air collisions with nestmates and reduce bee ‘traffic jams’ in front of the hive. In turn, this would make food collection more efficient for the colony and it would be easier for hive members to defend against intruders. With this chapter, I showed that the lifestyle of bees – where they live, how many there are and if they are exposed to intruders – can strongly influence their behaviour.
In chapter two, I then asked if and how the bees from chapter one use vision to control their peculiar landing. I found that they did indeed rely on vision to control their landing and that they did so in a simple manner. Essentially, when the image of the entrance of the hive reaches a given size on their eyes, these bees start to speed up. When the image of the entrance reaches a second set size on the eyes of landing bees, they extend their landing gear – which is, for bees, their legs – in preparation for touchdown. This chapter reveals that bees can use simple rules to achieve complex behaviours such as landing safely.
To explore the diversity of eyes in a large number of bees, we use X-ray images taken from a sample as it rotates (an approach known as computed tomography or CT, commonly used in a medical setting) to produce 3D images of the eyes. However, powerful tools are needed to analyse the large amounts of data that this approach generates. As I want to better understand how bee eyes work, I needed an efficient method for analysing 3D eye images created by CT, so I developed an automatic tool for distinguishing essential optical structures in the eyes of insects and other arthropods. In chapter three, I describe this method, provide a guide to use it, and give examples of its application to a few insect eyes.
In the last chapter, I used CT to look into the diversity of the eyes across a range of bumblebees from different habitats around the world. Even though different species are genetically close to each other, I found that their eyes were far from ‘all the same’. For example, bumblebees that live in forests have eyes that may enable them to see less sharp but better in dim light than bumblebees living in open landscapes. I also found that cuckoo bumblebees – bees that lay their eggs in another bumblebee hive like cuckoo birds do – had peculiar eyes in comparison to other bumblebees. This indicates that the eyes of each species of bumblebees may be specialised for a specific combination of lifestyle and habitat. These results are important for the conservation of bumblebees because they suggest that the eyes of some species may make them more sensitive than others to changes in the environment. For example, farming practices that create large open fields may particularly disadvantage bumblebees with eyes adapted to forests.
These four chapters only scratch the surface of the tight links between the eyes of bees, the ways they behave, and the worlds they live in. I hope that efforts to look into their diverse eyes will continue and will help to protect these crucial but endangered animals.
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Abstract (Swedish)
Binas surrande är en viktig komponent för känslan av sommar. Men, förutom många hyllmeter av litteratur om några vanliga arter av honungsbi och humlor, vet vi än idag förvånansvärt lite om många av de tjugofem tusen arter vi kallar bin. Vissa humlor överlever Grönlands minusgrader och hårda vindbyar, medan de i Amazonas snarare älskar skogens höga temperatur och fuktighet. Vissa arter bor i stora bon tillsammans med flera tusen individer, andra lever ensamma. Några är mindre än ett sesamfrö, någon lika långa som en tumme.
Trots dessa olikheter, delar de en stark och gemensam lust av att besöka blommor för att hitta föda. Därför är de så viktiga för att pollinera växter runt jordklotet. För att leva sina korta liv använder bina framför... (More)
Binas surrande är en viktig komponent för känslan av sommar. Men, förutom många hyllmeter av litteratur om några vanliga arter av honungsbi och humlor, vet vi än idag förvånansvärt lite om många av de tjugofem tusen arter vi kallar bin. Vissa humlor överlever Grönlands minusgrader och hårda vindbyar, medan de i Amazonas snarare älskar skogens höga temperatur och fuktighet. Vissa arter bor i stora bon tillsammans med flera tusen individer, andra lever ensamma. Några är mindre än ett sesamfrö, någon lika långa som en tumme.
Trots dessa olikheter, delar de en stark och gemensam lust av att besöka blommor för att hitta föda. Därför är de så viktiga för att pollinera växter runt jordklotet. För att leva sina korta liv använder bina framför allt sina ögon. De har två slags ögon, punkt- och facettögon, som de använder för att säkert flyga, navigera, hitta blommor och upptäcka andra individer för att para sig med.
Avhandlingens första kapitlen handlar om landning. Att kunna landa är en grundläggande förmåga för flygande insekter, men det är i stora drag okänt hur olika arter av bi bemästrar detta. Under en fältresa till Brasilien stötte jag på ett bi med en mycket underlig landnings-stil. I stället för att sakta ner för att landa – som de flesta andra djur inte oväntat gör – accelererade dessa bin strax innan de landade på boets ingång. Varför gasade de på detta sätt? Med hjälp av en datorsimulering kunde jag visa att denna märkliga strategi troligen hjälper bina att inte kroka mot varandra i luften och minskar risken för ”bitrafikstörning” framför boet. Detta kan i sin tur förbättra kolonins kapacitet att samla föda och försvara boet mot inkräktare. I kapitel ett diskuterar jag hur bins livsstil (dvs var de bor, hur många de är och hur känsliga de är för inkräktare) kan påverka deras beteende.
I kapitel två tittar jag djupare på hur dessa ”snabblandande” bin använder sina ögon för att styra denna ovanliga landningsstrategi. I dessa studier upptäckte jag att bina börjar accelerera när bilden på boets ingång når en specifik storlek i deras ögon. Så snart bilden på boets ingång når en annan given storlek fäller de snabbt ut sitt landningsställ, dvs sina ben, för att slutligen landa. Resultaten visar tydligt hur bin kan följa mycket enkla regler för att styra komplicerade och viktiga beteende.
Jag och många andra forskare använder idag röntgen som strålas på ett roterande prov för att producera en 3D-bild av det samma (detta är en teknik som kallas röntgentomografi och har länge använts för diagnostik inom vården). Problemet är att det krävs effektiva algoritmer för att kunna analysera den enorma mängd data som denna teknik genererar. Inom ramarna för att förstå hur ögonen hos bin är uppbyggda, utvecklade jag en snabb metod för att möjliggöra en 3D- analys av röntgentomografiska bilder av denna typ av små, biologiska prov. I avhandlingens tredje kapitel beskriver jag det verktyg jag utvecklat för att automatiskt identifiera viktiga optiska komponenter hos ett insektsöga.
I avhandlingens sista kapitlen presenterar jag hur röntgentomografi kan användas för att utforska mångfalden i ögonegenskap hos humlor som bor i olika miljöer. Även om många av dessa arter var mycket nära släkt, kunde jag utifrån dessa 3D-studier visa att deras ögon skilde sig åt i flera aspekter. Till exempel humlor som lever i skogar har ögon som troligen gör att de ser suddigare – men bättre i mörker – än humlor från öppna landskap. Jag hittade också att snylthumlor (de liknar gökar i och med att de lägger ägg i andra humlornas bo) har distinkta ögon jämfört med andra humlor. Sammantaget pekar min studie mot att ögonen hos var humlaart är nära anpassad till en given kombination av livsstil och miljö. Detta tyder in sin tur på att vissa arter, utifrån hur deras ögon är uppbyggda, är känsligare inför snabba omvärlds-förändringar än andra. Till exempel kan landbruksvanor som skapar ett öppet landskap bli särskilt skadliga för humlor med skogsanpassade ögon.
Denna avhandling är ett litet, men viktigt, steg mot ett djupare förståelse för de nära kopplingarna som finns mellan bins syn, beteende och dess omvärld. Jag hoppas att min avhandling kommer att inspirera andra att forska vidare inom detta ämne, och att de resultat som kommer fram kan hjälpa oss att bevara denna hotade grupp av insekter.
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Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Dr How, Martin, School of Biological Sciences, Bristol, UK
organization
alternative title
Binas visuella ecologi - Sagor om diversa ögon och beteende
publishing date
type
Thesis
publication status
published
subject
keywords
Animal behaviour, Arthropods, Bumblebees, Compound Eyes, Crystalline cones, Flight control, Image analysis, Landing, Sensory ecology, Stingless bees, Vision, X-ray microtomography
pages
231 pages
publisher
MediaTryck Lund
defense location
Blå Hallen, Ekologihuset, Sölvegatan 37, Lund Join via zoom: https://lu-se.zoom.us/j/68592226652?pwd=VzBzRGhCQkRIQW9BWGhxUDdmWUhMZz09
defense date
2021-04-23 09:00:00
ISBN
978-91-7895-785-9
978-91-7895-786-6
language
English
LU publication?
yes
id
ab85ee5d-ef1d-4068-9b51-ce01cd8f449d
date added to LUP
2021-03-22 09:34:52
date last changed
2021-03-31 12:11:00
@phdthesis{ab85ee5d-ef1d-4068-9b51-ce01cd8f449d,
  abstract     = {The buzzing flight of bees is a popular summer hit. Yet, outside of a few familiar species of honeybees and bumblebees, these fantastic little creatures are still mostly unknown. With about twenty-five thousand species, bees are a very diverse group. They can be found in drastically different habitats. For example, some kinds of bumblebees endure the freezing temperatures and windswept tundra of Greenland, while others only thrive in the heat and humidity of the Amazonian forest. Some bees live in huge colonies with tens of thousands of members, while others live solitary lives. Some are narrower than a sesame seed, while others can reach the size of a human thumb. Despite these differences, bees all have in common the urge to visit flowers where they find their food. This habit makes them very important for the pollination of plants across the world. To go about their laborious life, bees make extensive use of their vision. They possess two types of eyes – ocelli and compound eyes – that they use to control their flight, find their way through the world, discover flowers and spot possible mates. To understand how bees interact with the environment, we thus need to explore the diversity of their eyes and of how they use them.<br/>The first chapter of my thesis is about landing, which is a fundamental behaviour in flying insects. However, in bees it is poorly known whether different species land in different ways. During an expedition to Brazil, I came across a species of bee with the most peculiar landing style. Rather than slowing down to land, as most animals do, these bees accelerate just before touchdown on the entrance to their hive. Why do these bees speed up when they land? Using a computer simulation, I found that this weird strategy may help the bees to avoid mid-air collisions with nestmates and reduce bee ‘traffic jams’ in front of the hive. In turn, this would make food collection more efficient for the colony and it would be easier for hive members to defend against intruders. With this chapter, I showed that the lifestyle of bees – where they live, how many there are and if they are exposed to intruders – can strongly influence their behaviour.<br/>In chapter two, I then asked if and how the bees from chapter one use vision to control their peculiar landing. I found that they did indeed rely on vision to control their landing and that they did so in a simple manner. Essentially, when the image of the entrance of the hive reaches a given size on their eyes, these bees start to speed up. When the image of the entrance reaches a second set size on the eyes of landing bees, they extend their landing gear – which is, for bees, their legs – in preparation for touchdown. This chapter reveals that bees can use simple rules to achieve complex behaviours such as landing safely.<br/>To explore the diversity of eyes in a large number of bees, we use X-ray images taken from a sample as it rotates (an approach known as computed tomography or CT, commonly used in a medical setting) to produce 3D images of the eyes. However, powerful tools are needed to analyse the large amounts of data that this approach generates. As I want to better understand how bee eyes work, I needed an efficient method for analysing 3D eye images created by CT, so I developed an automatic tool for distinguishing essential optical structures in the eyes of insects and other arthropods. In chapter three, I describe this method, provide a guide to use it, and give examples of its application to a few insect eyes.<br/>In the last chapter, I used CT to look into the diversity of the eyes across a range of bumblebees from different habitats around the world. Even though different species are genetically close to each other, I found that their eyes were far from ‘all the same’. For example, bumblebees that live in forests have eyes that may enable them to see less sharp but better in dim light than bumblebees living in open landscapes. I also found that cuckoo bumblebees – bees that lay their eggs in another bumblebee hive like cuckoo birds do – had peculiar eyes in comparison to other bumblebees. This indicates that the eyes of each species of bumblebees may be specialised for a specific combination of lifestyle and habitat. These results are important for the conservation of bumblebees because they suggest that the eyes of some species may make them more sensitive than others to changes in the environment. For example, farming practices that create large open fields may particularly disadvantage bumblebees with eyes adapted to forests.<br/>These four chapters only scratch the surface of the tight links between the eyes of bees, the ways they behave, and the worlds they live in. I hope that efforts to look into their diverse eyes will continue and will help to protect these crucial but endangered animals.<br/>},
  author       = {Tichit, Pierre},
  isbn         = {978-91-7895-785-9},
  language     = {eng},
  month        = {03},
  publisher    = {MediaTryck Lund},
  school       = {Lund University},
  title        = {The visual ecology of bees - Tales of diverse eyes and behaviours},
  url          = {https://lup.lub.lu.se/search/ws/files/96141025/e_spik_ex_Tichit.pdf},
  year         = {2021},
}