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Article ; Online: Noisy communities and signal detection: why do foragers visit rewardless flowers?

Lichtenberg, Elinor M / Heiling, Jacob M / Bronstein, Judith L / Barker, Jessica L

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

2020 Volume 375, Issue 1802, Page(s) 20190486

Abstract: Floral communities present complex and shifting resource landscapes for flower-foraging animals. Strong similarities among the floral displays of different plant species, paired with high variability in reward distributions across time and space, can ... ...

Abstract	Floral communities present complex and shifting resource landscapes for flower-foraging animals. Strong similarities among the floral displays of different plant species, paired with high variability in reward distributions across time and space, can weaken correlations between floral signals and reward status. As a result, it should be difficult for foragers to discriminate between rewarding and rewardless flowers. Building on signal detection theory in behavioural ecology, we use hypothetical probability density functions to examine graphically how plant signals pose challenges to forager decision-making. We argue that foraging costs associated with incorrect acceptance of rewardless flowers and incorrect rejection of rewarding ones interact with community-level reward availability to determine the extent to which rewardless and rewarding species should overlap in flowering time. We discuss the evolutionary consequences of these phenomena from both the forager and the plant perspectives. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.
MeSH term(s)	Animals ; Cues ; Flowers/physiology ; Pollination ; Reward
Language	English
Publishing date	2020-05-18
Publishing country	England
Document type	Journal Article
ZDB-ID	208382-6
ISSN	1471-2970 ; 0080-4622 ; 0264-3839 ; 0962-8436
ISSN (online)	1471-2970
ISSN	0080-4622 ; 0264-3839 ; 0962-8436
DOI	10.1098/rstb.2019.0486
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Article: Costs and benefits of alternative food handling tactics help explain facultative exploitation of pollination mutualisms.

Lichtenberg, Elinor M / Irwin, Rebecca E / Bronstein, Judith L

Ecology

2018 Volume 99, Issue 8, Page(s) 1815–1824

Abstract: Many mutualisms are taken advantage of by organisms that take rewards from their partners but provide no benefit in return. In the absence of traits that limit exploitation, facultative exploiters (partners that can either exploit or cooperate) are ... ...

Abstract	Many mutualisms are taken advantage of by organisms that take rewards from their partners but provide no benefit in return. In the absence of traits that limit exploitation, facultative exploiters (partners that can either exploit or cooperate) are widely predicted by mutualism theory to choose an exploitative strategy, potentially threatening mutualism stability. However, it is unknown whether facultative exploiters choose to exploit, and, if so, make this choice because it is the most beneficial strategy for them. We explored these questions in a subalpine plant-insect community in which individuals of several bumble bee species visit flowers both "legitimately" (entering via the flower opening, picking up and depositing pollen, and hence behaving mutualistically) and via nectar robbing (creating holes through corollas or using an existing hole, bypassing stigmas and anthers). We applied foraging theory to (1) quantify handling costs, benefits and foraging efficiencies incurred by three bumble bee species as they visited flowers legitimately or robbed nectar in cage experiments, and (2) determine whether these efficiencies matched the food handling tactics these bee species employed in the field. Relative efficiencies of legitimate and robbing tactics depended on the combination of bee and plant species. In some cases (Bombus mixtus visiting Corydalis caseana or Mertensia ciliata), the robbing tactic permitted more efficient nectar removal. As both mutualism and foraging theory would predict, in the field, B. mixtus visiting C. caseana were observed more frequently robbing than foraging legitimately. However, for Bombus flavifrons visiting M. ciliata, the expectation from mutualism theory did not hold: legitimate visitation was the more efficient tactic. Legitimate visitation to M. ciliata was in fact more frequently observed in free-flying B. flavifrons. Free-flying B. mixtus also frequently visited M. ciliata flowers legitimately. This may reflect lower nectar volumes in robbed than unrobbed flowers in the field. These results suggest that a foraging ecology perspective is informative to the choice of tactics facultative exploiters make. In contrast, the simple expectation that exploiters should always have an advantage, and hence could threaten mutualism persistence unless they are deterred or punished, may not be broadly applicable.
MeSH term(s)	Animals ; Bees ; Cost-Benefit Analysis ; Flowers ; Food Handling ; Plant Nectar ; Pollination ; Symbiosis
Chemical Substances	Plant Nectar
Language	English
Publishing date	2018-06-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1797-8
ISSN	0012-9658
ISSN	0012-9658
DOI	10.1002/ecy.2395
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Article: Competition for nectar resources does not affect bee foraging tactic constancy

Lichtenberg, Elinor M / Richman, Sarah K / Irwin, Rebecca E / Bronstein, Judith L

Ecological entomology. 2020 Aug., v. 45, no. 4

2020

Abstract: 1. Competition alters animal foraging, including promoting the use of alternative resources. It may also impact how animals feed when they are able to handle the same food with more than one tactic. Competition likely impacts both consumers and their ... ...

Abstract	1. Competition alters animal foraging, including promoting the use of alternative resources. It may also impact how animals feed when they are able to handle the same food with more than one tactic. Competition likely impacts both consumers and their resources through its effects on food handling, but this topic has received little attention. 2. Bees often use two tactics for extracting nectar from flowers: they can visit at the flower opening, or rob nectar from holes at the base of flowers. Exploitative competition for nectar is thought to promote nectar robbing. If so, higher competition among floral visitors should reduce constancy to a single foraging tactic as foragers will seek food using all possible tactics. To test this prediction, field observations and two experiments involving bumble bees visiting three montane Colorado plant species (Mertensia ciliata, Linaria vulgaris, Corydalis caseana) were used under various levels of inter‐ and intra‐specific competition for nectar. 3. In general, individual bumble bees remained constant to a single foraging tactic, independent of competition levels. However, bees that visited M. ciliata in field observations decreased their constancy and increased nectar robbing rates as visitation rates by co‐visitors increased. 4. While tactic constancy was high overall regardless of competition intensity, this study highlights some intriguing instances in which competition and tactic constancy may be linked. Further studies investigating the cognitive underpinnings of tactic constancy should provide insight on the ways in which animals use alternative foraging tactics to exploit resources.
Keywords	Corydalis ; Linaria vulgaris ; Mertensia ciliata ; animals ; bees ; cognition ; entomology ; flowers ; intraspecific competition ; nectar ; prediction ; Colorado
Language	English
Dates of publication	2020-08
Size	p. 904-909.
Publishing place	Blackwell Publishing Ltd
Document type	Article
Note	NAL-AP-2-clean ; JOURNAL ARTICLE
ZDB-ID	196048-9
ISSN	0307-6946
ISSN	0307-6946
DOI	10.1111/een.12866
Database	NAL-Catalogue (AGRICOLA)

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Article: Bumble bees are constant to nectar-robbing behaviour despite low switching costs

Lichtenberg, Elinor M / Irwin, Rebecca E / Bronstein, Judith L

The Association for the Study of Animal Behaviour Animal behaviour. 2020 Dec., v. 170

2020

Abstract: Individuals sometimes exhibit striking constancy to a single behaviour even when they are capable of short-term behavioural flexibility. Constancy enables animals to avoid costs such as memory constraints, but can also inflict significant opportunity ... ...

Abstract	Individuals sometimes exhibit striking constancy to a single behaviour even when they are capable of short-term behavioural flexibility. Constancy enables animals to avoid costs such as memory constraints, but can also inflict significant opportunity costs through behaviour–environment mismatch. It is unclear when individuals should exhibit behavioural constancy and which types of costs most strongly influence such behaviour. We use a case in which individuals within a population exhibit more than one handling tactic for a single food type to investigate whether costs associated with switching among tactics constrain expression of intra-individual variation. Using wild bumble bees (Bombus spp.) that feed on nectar through flower openings (legitimate visits) or through holes at the base of flowers (robbing), we asked three questions. (1) Do individual bees exhibit tactic constancy within and across foraging bouts? (2) Are individuals willing to switch their food-handling tactics? (3) Is constancy in food-handling tactics maintained by costs associated with switching tactics? We measured energetic costs in addition to handling times. We found that bees freely foraging in meadows were highly constant to a single food-handling tactic both within and across bouts. However, experiments with individual captive bees showed that these bees were willing to switch tactics and experienced minimal costs in doing so. Thus, switching costs do not drive the observed constancy in food-handling tactics of bumble bees within and across foraging bouts.
Keywords	Bombus ; flowers ; food handling ; memory ; nectar ; nectar robbing
Language	English
Dates of publication	2020-12
Size	p. 177-188.
Publishing place	Elsevier Ltd
Document type	Article
Note	NAL-light
ZDB-ID	281-1
ISSN	0003-3472
ISSN	0003-3472
DOI	10.1016/j.anbehav.2020.09.008
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Article ; Online: Foraging traits modulate stingless bee community disassembly under forest loss.

Lichtenberg, Elinor M / Mendenhall, Chase D / Brosi, Berry

The Journal of animal ecology

2017 Volume 86, Issue 6, Page(s) 1404–1416

Abstract: Anthropogenic land use change is an important driver of impacts to biological communities and the ecosystem services they provide. Pollination is one ecosystem service that may be threatened by community disassembly. Relatively little is known about ... ...

Abstract	Anthropogenic land use change is an important driver of impacts to biological communities and the ecosystem services they provide. Pollination is one ecosystem service that may be threatened by community disassembly. Relatively little is known about changes in bee community composition in the tropics, where pollination limitation is most severe and land use change is rapid. Understanding how anthropogenic changes alter community composition and functioning has been hampered by high variability in responses of individual species. Trait-based approaches, however, are emerging as a potential method for understanding responses of ecologically similar species to global change. We studied how communities of tropical, eusocial stingless bees (Apidae: Meliponini) disassemble when forest is lost. These bees are vital tropical pollinators that exhibit high trait diversity, but are under considerable threat from human activities. We compared functional traits of stingless bee species found in pastures surrounded by differing amounts of forest in an extensively deforested landscape in southern Costa Rica. Our results suggest that foraging traits modulate competitive interactions that underlie community disassembly patterns. In contrast to both theoretical predictions and temperate bee communities, we found that stingless bee species with the widest diet breadths were less likely to persist in sites with less forest. These wide-diet-breadth species also tend to be solitary foragers, and are competitively subordinate to group-foraging stingless bee species. Thus, displacement by dominant, group-foraging species may make subordinate species more dependent on the larger or more diversified resource pool that natural habitats offer. We also found that traits that may reduce reliance on trees-nesting in the ground or inside nests of other species-correlated with persistence in highly deforested landscapes. The functional trait perspective we employed enabled capturing community processes in analyses and suggests that land use change may disassemble bee communities via different mechanisms in temperate and tropical areas. Our results further suggest that community processes, such as competition, can be important regulators of community disassembly under land use change. A better understanding of community disassembly processes is critical for conserving and restoring pollinator communities and the ecosystem services and functions they provide.
MeSH term(s)	Animals ; Bees/physiology ; Biota ; Conservation of Natural Resources ; Costa Rica ; Feeding Behavior ; Forestry ; Forests ; Pollination
Language	English
Publishing date	2017-09-28
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.12747
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Article: Foraging traits modulate stingless bee community disassembly under forest loss

Lichtenberg, Elinor M / Chase D. Mendenhall / Berry Brosi

journal of animal ecology. 2017 Oct., v. 86, no. 6

2017

Abstract	Anthropogenic land use change is an important driver of impacts to biological communities and the ecosystem services they provide. Pollination is one ecosystem service that may be threatened by community disassembly. Relatively little is known about changes in bee community composition in the tropics, where pollination limitation is most severe and land use change is rapid. Understanding how anthropogenic changes alter community composition and functioning has been hampered by high variability in responses of individual species. Traitâbased approaches, however, are emerging as a potential method for understanding responses of ecologically similar species to global change. We studied how communities of tropical, eusocial stingless bees (Apidae: Meliponini) disassemble when forest is lost. These bees are vital tropical pollinators that exhibit high trait diversity, but are under considerable threat from human activities. We compared functional traits of stingless bee species found in pastures surrounded by differing amounts of forest in an extensively deforested landscape in southern Costa Rica. Our results suggest that foraging traits modulate competitive interactions that underlie community disassembly patterns. In contrast to both theoretical predictions and temperate bee communities, we found that stingless bee species with the widest diet breadths were less likely to persist in sites with less forest. These wideâdietâbreadth species also tend to be solitary foragers, and are competitively subordinate to groupâforaging stingless bee species. Thus, displacement by dominant, groupâforaging species may make subordinate species more dependent on the larger or more diversified resource pool that natural habitats offer. We also found that traits that may reduce reliance on treesânesting in the ground or inside nests of other speciesâcorrelated with persistence in highly deforested landscapes. The functional trait perspective we employed enabled capturing community processes in analyses and suggests that land use change may disassemble bee communities via different mechanisms in temperate and tropical areas. Our results further suggest that community processes, such as competition, can be important regulators of community disassembly under land use change. A better understanding of community disassembly processes is critical for conserving and restoring pollinator communities and the ecosystem services and functions they provide.
Keywords	Apidae ; anthropogenic activities ; community structure ; deforestation ; diet ; ecosystem services ; foraging ; forests ; global change ; habitats ; humans ; land use change ; landscapes ; nests ; pastures ; pollination ; pollinators ; prediction ; stingless bees ; tropics ; Costa Rica
Language	English
Dates of publication	2017-10
Size	p. 1404-1416.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.12747
Database	NAL-Catalogue (AGRICOLA)

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Article: Costs and benefits of alternative food handling tactics help explain facultative exploitation of pollination mutualisms

Lichtenberg, Elinor M / Judith L. Bronstein / Rebecca E. Irwin

Ecology. 2018 Aug., v. 99, no. 8

2018

Abstract	Many mutualisms are taken advantage of by organisms that take rewards from their partners but provide no benefit in return. In the absence of traits that limit exploitation, facultative exploiters (partners that can either exploit or cooperate) are widely predicted by mutualism theory to choose an exploitative strategy, potentially threatening mutualism stability. However, it is unknown whether facultative exploiters choose to exploit, and, if so, make this choice because it is the most beneficial strategy for them. We explored these questions in a subalpine plant‐insect community in which individuals of several bumble bee species visit flowers both “legitimately” (entering via the flower opening, picking up and depositing pollen, and hence behaving mutualistically) and via nectar robbing (creating holes through corollas or using an existing hole, bypassing stigmas and anthers). We applied foraging theory to (1) quantify handling costs, benefits and foraging efficiencies incurred by three bumble bee species as they visited flowers legitimately or robbed nectar in cage experiments, and (2) determine whether these efficiencies matched the food handling tactics these bee species employed in the field. Relative efficiencies of legitimate and robbing tactics depended on the combination of bee and plant species. In some cases (Bombus mixtus visiting Corydalis caseana or Mertensia ciliata), the robbing tactic permitted more efficient nectar removal. As both mutualism and foraging theory would predict, in the field, B. mixtus visiting C. caseana were observed more frequently robbing than foraging legitimately. However, for Bombus flavifrons visiting M. ciliata, the expectation from mutualism theory did not hold: legitimate visitation was the more efficient tactic. Legitimate visitation to M. ciliata was in fact more frequently observed in free‐flying B. flavifrons. Free‐flying B. mixtus also frequently visited M. ciliata flowers legitimately. This may reflect lower nectar volumes in robbed than unrobbed flowers in the field. These results suggest that a foraging ecology perspective is informative to the choice of tactics facultative exploiters make. In contrast, the simple expectation that exploiters should always have an advantage, and hence could threaten mutualism persistence unless they are deterred or punished, may not be broadly applicable.
Keywords	anthers ; bees ; Bombus ; cages ; Corydalis ; flowering ; foraging ; Mertensia ciliata ; mutualism ; nectar ; nectar robbing ; pollen ; pollination
Language	English
Dates of publication	2018-08
Size	p. 1815-1824.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	1797-8
ISSN	0012-9658
ISSN	0012-9658
DOI	10.1002/ecy.2395
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The behavioral ecology of nectar robbing: why be tactic constant?

Bronstein, Judith L / Barker, Jessica L / Lichtenberg, Elinor M / Richardson, Leif L / Irwin, Rebecca E

Current opinion in insect science

2017 Volume 21, Page(s) 14–18

Abstract: How do animals forage for variable food resources? For animals foraging at flowers, floral constancy has provided a framework for understanding why organisms visit some flowers while bypassing others. We extend this framework to the flower-handling ... ...

Abstract	How do animals forage for variable food resources? For animals foraging at flowers, floral constancy has provided a framework for understanding why organisms visit some flowers while bypassing others. We extend this framework to the flower-handling tactics that visitors employ. Nectar robbers remove nectar through holes bitten in flowers, often without pollinating. Many foragers can switch between robbing and visiting flowers legitimately to gain access to nectar. We document that even though individuals can switch foraging tactics, they often do not. We explore whether individuals exhibit constancy to either robbing or visiting legitimately, which we term tactic constancy. We then extend hypotheses of floral constancy to understand when and why visitors exhibit tactic constancy and raise questions for future research.
MeSH term(s)	Animals ; Appetitive Behavior ; Behavior, Animal/physiology ; Flowers ; Insecta/physiology ; Magnoliopsida ; Plant Nectar ; Pollination
Chemical Substances	Plant Nectar
Language	English
Publishing date	2017-05-19
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2772833-X
ISSN	2214-5753 ; 2214-5745
ISSN (online)	2214-5753
ISSN	2214-5745
DOI	10.1016/j.cois.2017.05.013
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Article ; Online: Eavesdropping selects for conspicuous signals.

Lichtenberg, Elinor M / Zivin, Joshua Graff / Hrncir, Michael / Nieh, James C

Current biology : CB

2014 Volume 24, Issue 13, Page(s) R598–9

MeSH term(s)	Animal Communication ; Animals ; Appetitive Behavior/physiology ; Bees/physiology ; Biological Evolution ; Decision Making/physiology ; Models, Biological ; Species Specificity
Language	English
Publishing date	2014-07-07
Publishing country	England
Document type	Letter ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2014.05.062
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Article: High bee functional diversity buffers crop pollination services against Amazon deforestation

Campbell, Alistair John / Lichtenberg, Elinor M. / Carvalheiro, Luísa Gigante / Menezes, Cristiano / Borges, Rafael Cabral / Coelho, Beatriz Woiski Texeira / Freitas, Madson Antonio Benjamin / Giannini, Tereza Cristina / Leão, Kamila Leão / de Oliveira, Favízia Freitas / Silva, Thiago Sanna Freire / Maués, Márcia Motta

Agriculture, ecosystems & environment. 2022 Mar. 01, v. 326

2022

Abstract: Predicting outcomes of land use change on biodiversity and ecosystem services remains a key priority for ecologists, but may be particularly challenging in diverse tropical ecosystems. Trait-based approaches are a key tool to meet this challenge. Such ... ...

Abstract	Predicting outcomes of land use change on biodiversity and ecosystem services remains a key priority for ecologists, but may be particularly challenging in diverse tropical ecosystems. Trait-based approaches are a key tool to meet this challenge. Such approaches seek functional mechanisms underpinning species’ responses to environmental disturbance and contributions to ecosystem services. Here, we use a functional trait approach to study effects of land use change on stingless bee communities and on pollination services to açaí palm (Euterpe oleracea, Arecaceae) in the eastern Brazilian Amazon. We compared traits of stingless bees visiting açaí inflorescences across a land use intensity gradient (low to high forest cover) to determine: (1) the role of traits in bee species’ responses to deforestation; (2) how deforestation affects functional composition of bee communities; and (3) whether bee traits better explain variation in açaí fruit production than species diversity metrics. We found that bee species’ responses to deforestation were non-random and predicted by body size, with small-sized bees more susceptible to forest loss, and changes in functional diversity of bee communities were important for pollination services. However, not all changes in functional diversity were associated with forest loss. Together, these results suggest that: (1) large tracts of minimally disturbed tropical rainforest are vital for the conservation of diverse stingless bee communities; (2) efficient pollination is contingent on bee species not only having divergent trait values (functional dispersion), but also traits’ relative abundance in communities (functional evenness); and (3) high functional diversity in stingless bee communities buffers açaí pollination services to loss of sensitive species. Thus, conservation strategies must focus on protecting wider biodiversity, not just ecosystem services, to guarantee conservation of native eusocial bee taxa. Doing so will safeguard crop pollination services, the pollination of native plant communities, and the long-term resilience of Amazon forest ecosystems.
Keywords	Euterpe oleracea ; agriculture ; body size ; deforestation ; environment ; fruits ; functional diversity ; indigenous species ; land use change ; pollination ; species diversity ; stingless bees ; tropical rain forests ; Amazonia
Language	English
Dates of publication	2022-0301
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	602345-9
ISSN	1873-2305 ; 0167-8809
ISSN (online)	1873-2305
ISSN	0167-8809
DOI	10.1016/j.agee.2021.107777
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