Adaptations for nocturnal vision in insect apposition eyes

Birgit Greiner

Adaptations for nocturnal vision in insect apposition eyes

Birgit Greiner

Biologiska institutionen

Forskningsoutput: Avhandling › Doktorsavhandling (sammanläggning)

1649 Nedladdningar (Pure)

Sammanfattning

Popular Abstract in Swedish
Hur kan nattaktiva insekter se i mörker med fel sorts ögon?

Majoriteten av alla dagaktiva insekter har en sorts facettöga som kallas appositionsöga. Appositionsögon är anpassade till ett liv med god tillgång på ljus ? nattaktiva djur har därför i princip alltid andra sorters ögon (superpositionsögon). Anledningen till att appositionsögon fungerar bäst på dagen är att de har små linser vilket gör dem mycket okänsliga och opålitliga i mörker. I avhandlingens introduktion behandlar jag insekternas synsinne och anledningen till att vissa ändå använder dåligt anpassade ögon för nattseende. Men det är bara i en enda insekt, ett väldigt speciellt nattaktivt bi, som hittills alla aspekter undersökts ? såväl beteende som optiska och neurala anpassningar och teorin bakom det hela.

De flesta bin i världen är dagaktiva och har appositionsögon. Ändå finns det bin i Panama som flyger runt på natten. Teoretiska beräkningar visar att dessa bin inte borde kunna se någonting så fort det börjar skymma, men Panamabina flyger från sitt bo (ett 5 mm stort hål i en liten pinne), genom grenar och lövverk i djungeln, letar reda på nektargömmor långt borta från sitt hem och hittar sedan tillbaka till boet utan att flyga vilse. Dessutom, som visas i första artikeln, kan de även urskilja och använda landmärken för att orientera i mörker. Men hur klarar de det med sina okänsliga appositionsögon?

Den andra och tredje artikeln visar att appositionsögon hos nattaktiva bin och getingar har specifika optiska och anatomiska anpassningar som gör dem 30 gånger ljuskänsligare än deras dagaktiva släktingar. Mest effektivt är otroligt stora ljuskänsliga fotoreceptorer som absorberar ljus från en mycket bredare infallsvinkel än i ett normalt appositionsöga. En känslighetsförbättring på 30 gånger är inte att förakta, men inte tillräcklig om man tänker på att ljusintensitetsskillnaden är 100 millioner gånger mellan dag och natt. Därför undrade jag vilka andra möjliga anpassningar som måste finnas.

Enligt vår teoretiska modell (artikel VI), skulle nattaktiva bin använda sig av fotonsummering (i rum och tid) för att kunna se i svag belysning. Om Panamabina summerar signaler från flera facetter kan de få tillräckligt med ljus för att även kunna se under natten. Som jag visar i artiklarna IV & V, finns det stora, sidoförgrenade celler i den optiska delen av deras hjärna. Alla förgreningarna är mycket större jämfört med motsvarande celler i dagaktiva bin ? en tendens som finns också i andra insektgrupper ? och täcker en stor yta av 10-18 facetter. Vår modell förutsäger detta, vilket förstärker hypotesen att dessa celler förmedlar spatiell fotonsummering.

I min avhandling visar jag att nattaktiva insekter med appositionsögon har utvecklat specifika optiska och neurala anpassningar vilka möjliggör för dem att vara aktiva under natten i en tryggare miljö med förminskad konkurrens.

Originalspråk	engelska
Kvalifikation	Doktor
Tilldelande institution	Biologiska institutionen
Handledare	Warrant, Eric, handledare
Tilldelningsdatum	2005 dec. 16
Förlag	Lund Unversity, Department of Cell and Organism Biology
ISBN (tryckt)	91-85067-22-9
Status	Published - 2005

Bibliografisk information

Defence details

Date: 2005-12-16
Time: 10:00
Place: Högtidssalen, Zoologihuset, Helgonav. 3, Lund

External reviewer(s)

Name: Meinertzhagen, Ian A.
Title: Prof.
Affiliation: Life Sciences Centre, Dalhousie University, Halifax, Canada.

---

<div class="article_info">E.J. Warrant, A. Kelber, A. Gislén, B. Greiner, W.A. Ribi and W.T Wcislo. <span class="article_issue_date">2004</span>. <a href="javascript:downloadFile(545734)" class="article_link">Nocturnal vision and landmark orientation in a tropical halictid bee</a> <span class="journal_series_title">Current Biology</span>, <span class="journal_pages">pp 1309-1318</span>. <span class="journal_distributor">Elsevier</span></div>
<div class="article_info">B. Greiner, W.A. Ribi and E.J. Warrant. <span class="article_issue_date">2004</span>. <span class="article_title">Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research</span>, <span class="journal_pages">pp 377-390</span>. <span class="journal_distributor">Springer</span></div>
<div class="article_info">B. Greiner. <span class="article_issue_date">2005</span>. <span class="article_title">Visual adaptations in the night active wasp Apoica pallens</span> <span class="journal_series_title">The Journal of Comparative Neurology</span>, <span class="journal_distributor">.</span> (accepted)</div>
<div class="article_info">B. Greiner, W.A. Ribi, W.T Wcislo and E.J. Warrant. <span class="article_issue_date">2004</span>. <span class="article_title">Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research</span>, <span class="journal_volume">vol 318</span> <span class="journal_pages">pp 429-437</span>. <span class="journal_distributor">Springer</span></div>
<div class="article_info">B. Greiner, W.A. Ribi and E.J. Warrant. <span class="article_issue_date">2005</span>. <span class="article_title">A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research,</span>, <span class="journal_distributor">Springer</span> (inpress)</div>
<div class="article_info">J.C. Theobald, B. Greiner, W.T Wcislo and E.J. Warrant. <span class="article_issue_date">2005</span>. <span class="article_title">Visual summation in night-flying sweat bees: a theoretical study.</span> <span class="journal_series_title">Vision Research</span>, (submitted)</div>

The information about affiliations in this record was updated in December 2015.
The record was previously connected to the following departments: Zoology (Closed 2011) (011012000)

Ämnesklassifikation (UKÄ)

Zoologi

Tillgång till dokument

2 Artikel i vetenskaplig tidskrift

Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis
Greiner, B., Ribi, W., Wcislo, W. & Warrant, E., 2004, I: Cell and Tissue Research. 318, 2, s. 429-437
Forskningsoutput: Tidskriftsbidrag › Artikel i vetenskaplig tidskrift › Peer review
Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis
Greiner, B., Ribi, W. & Warrant, E., 2004, I: Cell and Tissue Research. 316, 3, s. 377-390
Forskningsoutput: Tidskriftsbidrag › Artikel i vetenskaplig tidskrift › Peer review

Citera det här

@phdthesis{97598f0d109f424e97d58aa872e25362,

title = "Adaptations for nocturnal vision in insect apposition eyes",

abstract = "Due to our own preference for bright light, we tend to forget that many insects are active in very dim light. The reasons for nocturnal activity are most easily seen in tropical areas of the world, where animals face severe competition for food and nocturnal insects are able to forage in a climate of reduced competition and predation. Generally nocturnal insects possess superposition compound eyes. This eye design is truly optimized for dim light as photons can be gathered through large apertures comprised of hundreds of lenses. In apposition eyes, on the other hand, the aperture consists of a single lens resulting in a poor photon catch and unreliable vision in dim light. Apposition eyes are therefore typically found in day-active insects and according to theoretical calculations should render bees blind by mid dusk. Nevertheless, the tropical bee Megalopta genalis and the wasp Apoica pallens have managed the transition to a nocturnal lifestyle while retaining their highly unsuitable apposition eye design. Far from being blind, these bees and wasps forage at extremely low light intensities. Moreover, M. genalis is the first insect shown to use landmark navigation at light intensities less than starlight. How do their apposition eyes permit such complex visual behaviour in so little light? Optical adaptations can significantly enhance sensitivity in apposition eyes. In bees and wasps, the major effect comes from their extremely wide photoreceptors, which are able to trap light reaching the eye from a large visual angle. These optical adaptations lead to a 30-fold increase in sensitivity compared to diurnal bees and wasps. This however is not sufficient for the 8 log units difference in light intensity between day and night. Our hypothesis is that neural adaptations in the form of spatial and temporal summation must be involved. By means of spatial summation the eyes could sum signals from large groups of visual units (ommatidia), in order to improve sensitivity at the cost of coarser spatial resolution. In nocturnal bees, spatial summation could be mediated via their wide laterally-spreading first-order interneurons (L-fibres) present in the first optic ganglion (lamina). These L-fibres have significantly larger dendritic fields than equivalent neurons in diurnal bees and the potential to sum photons from up to 18 visual units. Theoretical modelling further supports this hypothesis, as the optimal dendritic field size predicted by the model agrees well with the anatomical data.",

keywords = "temporal and spatial summation, optical and neural adaptations, theoretical modelling., Djurs anatomi och morfologi, Zoologi, dim light, vision, landmark navigation, nocturnal bees and wasps, Zoology, Animal anatomy, animal morphology",

author = "Birgit Greiner",

note = "Defence details Date: 2005-12-16 Time: 10:00 Place: H{\"o}gtidssalen, Zoologihuset, Helgonav. 3, Lund External reviewer(s) Name: Meinertzhagen, Ian A. Title: Prof. Affiliation: Life Sciences Centre, Dalhousie University, Halifax, Canada. --- <div class={"}article_info{"}>E.J. Warrant, A. Kelber, A. Gisl{\'e}n, B. Greiner, W.A. Ribi and W.T Wcislo. <span class={"}article_issue_date{"}>2004</span>. <a href={"}javascript:downloadFile(545734){"} class={"}article_link{"}>Nocturnal vision and landmark orientation in a tropical halictid bee</a> <span class={"}journal_series_title{"}>Current Biology</span>, <span class={"}journal_pages{"}>pp 1309-1318</span>. <span class={"}journal_distributor{"}>Elsevier</span></div> <div class={"}article_info{"}>B. Greiner, W.A. Ribi and E.J. Warrant. <span class={"}article_issue_date{"}>2004</span>. <span class={"}article_title{"}>Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis.</span> <span class={"}journal_series_title{"}>Cell and Tissue Research</span>, <span class={"}journal_pages{"}>pp 377-390</span>. <span class={"}journal_distributor{"}>Springer</span></div> <div class={"}article_info{"}>B. Greiner. <span class={"}article_issue_date{"}>2005</span>. <span class={"}article_title{"}>Visual adaptations in the night active wasp Apoica pallens</span> <span class={"}journal_series_title{"}>The Journal of Comparative Neurology</span>, <span class={"}journal_distributor{"}>.</span> (accepted)</div> <div class={"}article_info{"}>B. Greiner, W.A. Ribi, W.T Wcislo and E.J. Warrant. <span class={"}article_issue_date{"}>2004</span>. <span class={"}article_title{"}>Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis.</span> <span class={"}journal_series_title{"}>Cell and Tissue Research</span>, <span class={"}journal_volume{"}>vol 318</span> <span class={"}journal_pages{"}>pp 429-437</span>. <span class={"}journal_distributor{"}>Springer</span></div> <div class={"}article_info{"}>B. Greiner, W.A. Ribi and E.J. Warrant. <span class={"}article_issue_date{"}>2005</span>. <span class={"}article_title{"}>A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis.</span> <span class={"}journal_series_title{"}>Cell and Tissue Research,</span>, <span class={"}journal_distributor{"}>Springer</span> (inpress)</div> <div class={"}article_info{"}>J.C. Theobald, B. Greiner, W.T Wcislo and E.J. Warrant. <span class={"}article_issue_date{"}>2005</span>. <span class={"}article_title{"}>Visual summation in night-flying sweat bees: a theoretical study.</span> <span class={"}journal_series_title{"}>Vision Research</span>, (submitted)</div> The information about affiliations in this record was updated in December 2015. The record was previously connected to the following departments: Zoology (Closed 2011) (011012000)",

year = "2005",

language = "English",

isbn = "91-85067-22-9",

publisher = "Lund Unversity, Department of Cell and Organism Biology",

type = "Doctoral Thesis (compilation)",

school = "Department of Biology",

}

TY - THES

T1 - Adaptations for nocturnal vision in insect apposition eyes

AU - Greiner, Birgit

N1 - Defence details Date: 2005-12-16 Time: 10:00 Place: Högtidssalen, Zoologihuset, Helgonav. 3, Lund External reviewer(s) Name: Meinertzhagen, Ian A. Title: Prof. Affiliation: Life Sciences Centre, Dalhousie University, Halifax, Canada. --- <div class="article_info">E.J. Warrant, A. Kelber, A. Gislén, B. Greiner, W.A. Ribi and W.T Wcislo. <span class="article_issue_date">2004</span>. <a href="javascript:downloadFile(545734)" class="article_link">Nocturnal vision and landmark orientation in a tropical halictid bee</a> <span class="journal_series_title">Current Biology</span>, <span class="journal_pages">pp 1309-1318</span>. <span class="journal_distributor">Elsevier</span></div> <div class="article_info">B. Greiner, W.A. Ribi and E.J. Warrant. <span class="article_issue_date">2004</span>. <span class="article_title">Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research</span>, <span class="journal_pages">pp 377-390</span>. <span class="journal_distributor">Springer</span></div> <div class="article_info">B. Greiner. <span class="article_issue_date">2005</span>. <span class="article_title">Visual adaptations in the night active wasp Apoica pallens</span> <span class="journal_series_title">The Journal of Comparative Neurology</span>, <span class="journal_distributor">.</span> (accepted)</div> <div class="article_info">B. Greiner, W.A. Ribi, W.T Wcislo and E.J. Warrant. <span class="article_issue_date">2004</span>. <span class="article_title">Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research</span>, <span class="journal_volume">vol 318</span> <span class="journal_pages">pp 429-437</span>. <span class="journal_distributor">Springer</span></div> <div class="article_info">B. Greiner, W.A. Ribi and E.J. Warrant. <span class="article_issue_date">2005</span>. <span class="article_title">A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis.</span> <span class="journal_series_title">Cell and Tissue Research,</span>, <span class="journal_distributor">Springer</span> (inpress)</div> <div class="article_info">J.C. Theobald, B. Greiner, W.T Wcislo and E.J. Warrant. <span class="article_issue_date">2005</span>. <span class="article_title">Visual summation in night-flying sweat bees: a theoretical study.</span> <span class="journal_series_title">Vision Research</span>, (submitted)</div> The information about affiliations in this record was updated in December 2015. The record was previously connected to the following departments: Zoology (Closed 2011) (011012000)

PY - 2005

Y1 - 2005

N2 - Due to our own preference for bright light, we tend to forget that many insects are active in very dim light. The reasons for nocturnal activity are most easily seen in tropical areas of the world, where animals face severe competition for food and nocturnal insects are able to forage in a climate of reduced competition and predation. Generally nocturnal insects possess superposition compound eyes. This eye design is truly optimized for dim light as photons can be gathered through large apertures comprised of hundreds of lenses. In apposition eyes, on the other hand, the aperture consists of a single lens resulting in a poor photon catch and unreliable vision in dim light. Apposition eyes are therefore typically found in day-active insects and according to theoretical calculations should render bees blind by mid dusk. Nevertheless, the tropical bee Megalopta genalis and the wasp Apoica pallens have managed the transition to a nocturnal lifestyle while retaining their highly unsuitable apposition eye design. Far from being blind, these bees and wasps forage at extremely low light intensities. Moreover, M. genalis is the first insect shown to use landmark navigation at light intensities less than starlight. How do their apposition eyes permit such complex visual behaviour in so little light? Optical adaptations can significantly enhance sensitivity in apposition eyes. In bees and wasps, the major effect comes from their extremely wide photoreceptors, which are able to trap light reaching the eye from a large visual angle. These optical adaptations lead to a 30-fold increase in sensitivity compared to diurnal bees and wasps. This however is not sufficient for the 8 log units difference in light intensity between day and night. Our hypothesis is that neural adaptations in the form of spatial and temporal summation must be involved. By means of spatial summation the eyes could sum signals from large groups of visual units (ommatidia), in order to improve sensitivity at the cost of coarser spatial resolution. In nocturnal bees, spatial summation could be mediated via their wide laterally-spreading first-order interneurons (L-fibres) present in the first optic ganglion (lamina). These L-fibres have significantly larger dendritic fields than equivalent neurons in diurnal bees and the potential to sum photons from up to 18 visual units. Theoretical modelling further supports this hypothesis, as the optimal dendritic field size predicted by the model agrees well with the anatomical data.

AB - Due to our own preference for bright light, we tend to forget that many insects are active in very dim light. The reasons for nocturnal activity are most easily seen in tropical areas of the world, where animals face severe competition for food and nocturnal insects are able to forage in a climate of reduced competition and predation. Generally nocturnal insects possess superposition compound eyes. This eye design is truly optimized for dim light as photons can be gathered through large apertures comprised of hundreds of lenses. In apposition eyes, on the other hand, the aperture consists of a single lens resulting in a poor photon catch and unreliable vision in dim light. Apposition eyes are therefore typically found in day-active insects and according to theoretical calculations should render bees blind by mid dusk. Nevertheless, the tropical bee Megalopta genalis and the wasp Apoica pallens have managed the transition to a nocturnal lifestyle while retaining their highly unsuitable apposition eye design. Far from being blind, these bees and wasps forage at extremely low light intensities. Moreover, M. genalis is the first insect shown to use landmark navigation at light intensities less than starlight. How do their apposition eyes permit such complex visual behaviour in so little light? Optical adaptations can significantly enhance sensitivity in apposition eyes. In bees and wasps, the major effect comes from their extremely wide photoreceptors, which are able to trap light reaching the eye from a large visual angle. These optical adaptations lead to a 30-fold increase in sensitivity compared to diurnal bees and wasps. This however is not sufficient for the 8 log units difference in light intensity between day and night. Our hypothesis is that neural adaptations in the form of spatial and temporal summation must be involved. By means of spatial summation the eyes could sum signals from large groups of visual units (ommatidia), in order to improve sensitivity at the cost of coarser spatial resolution. In nocturnal bees, spatial summation could be mediated via their wide laterally-spreading first-order interneurons (L-fibres) present in the first optic ganglion (lamina). These L-fibres have significantly larger dendritic fields than equivalent neurons in diurnal bees and the potential to sum photons from up to 18 visual units. Theoretical modelling further supports this hypothesis, as the optimal dendritic field size predicted by the model agrees well with the anatomical data.

KW - temporal and spatial summation

KW - optical and neural adaptations

KW - theoretical modelling.

KW - Djurs anatomi och morfologi

KW - Zoologi

KW - dim light

KW - vision

KW - landmark navigation

KW - nocturnal bees and wasps

KW - Zoology

KW - Animal anatomy

KW - animal morphology

M3 - Doctoral Thesis (compilation)

SN - 91-85067-22-9

PB - Lund Unversity, Department of Cell and Organism Biology

ER -

Adaptations for nocturnal vision in insect apposition eyes

Sammanfattning

Bibliografisk information

Ämnesklassifikation (UKÄ)

Tillgång till dokument

Fingeravtryck

Forskningsoutput

Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis

Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis

Citera det här