Karen L. Hollis’s research while affiliated with Mount Holyoke College and other places

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Publications (47)


The Wild Man in the Laboratory: Introduction to the Special Issue in honor of Michael Domjan
  • Article
  • Full-text available

June 2022

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49 Reads

Learning & Behavior

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Karen L. Hollis

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Download


Introduction: Perspectives on the Evolution of Learning and Memory Mechanisms

May 2022

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61 Reads

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1 Citation

Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.


Learning in Insects: Perspectives and Possibilities

May 2022

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19 Reads

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1 Citation

Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.


Depiction of the procedure used for conditioning in Lymnaea stagnalis. Snails in the PAV (or learning) group were exposed to a solution of amyl acetate (that is, banana essence) followed by the presentation of a conspecific. For the CON (control) group these two events never occurred together as indicated by the red X
Percentage of PAV (Pavlovian conditioned) and CON (control) subjects that mated first in the male role in the Role Conflict experiment. Statistically significant differences are indicated by asterisks
Mean latency of PAV (Pavlovian conditioned) and CON (control) subjects to mount the other snail’s shell in the No Role Conflict. Vertical bars represent SEMs
A Mean latency of PAV (Pavlovian conditioned) and CON (control) subjects to show partial eversion and B to show full eversion in the No Role Conflict experiment. Vertical bars represent SEMs. Statistically significant differences are indicated by asterisks
A Mean latency of PAV (Pavlovian conditioned) and CON (control) subjects to start probing and B to intromit in the No Role Conflict experiment. Vertical bars represent SEMs. Statistically significant differences are indicated by asterisks
Learning to anticipate mate presence shapes individual sex roles in the hermaphroditic pond snail, Lymnaea stagnalis

May 2022

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57 Reads

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4 Citations

Animal Cognition

Despite being simultaneously male and female, hermaphrodites may still need to assume the male or female sexual role in a mating encounter, with the option to swap roles afterwards. For the great pond snail, Lymnaea stagnalis, deciding which sexual role to perform has important consequences, since sperm transfer and male reproductive success can be decreased. We hypothesised that detecting cues that indicate a possible mating encounter could help them to adapt their mating behaviour. Therefore, we experimentally assessed whether signalling the presence of a conspecific with an odour can affect the sexual role of Lymnaea stagnalis. The results showed that learning resulted in either an increased ability to mate as a male or in faster mating compared to the control group. These findings reveal that learning shapes the mating dynamics of Lymnaea stagnalis, thus showing that cognitive processes not only affect mating in separate-sexed species but also in hermaphrodites.


Part I - Evolution of Learning Processes

May 2022

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98 Reads

Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.


Part II - Evolution of Memory Processes

May 2022

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58 Reads

Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.


Cause, development, function, and evolution: Toward a behavioral ecology of rescue behavior in ants

February 2022

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78 Reads

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8 Citations

Learning & Behavior

In a species of Mediterranean desert-dwelling ant, Cataglyphis piliscapa (formerly, C. cursor), some individuals, mostly foragers, engage in highly orchestrated behavior to free a trapped nestmate. Their behavior, which we have labeled rescue, is a heritable trait in this species, and it appears fully formed within a few days of an ant’s emergence as an adult. Not only is the rescue behavior by these ant specialists precisely targeted, but also it involves a complex, dynamic sequence of behavioral patterns. That is, each rescue operation is responsive both to the specific circumstances of the nestmate’s entrapment and to the way in which that particular rescue operation unfolds, relying on the rescuer’s short-term memory of its previous actions to increase efficiency and to decrease energy expenditure. Rescue appears in several other ant species as well, and, although the specific behavioral patterns and contexts vary across species, the outcome—namely, releasing a distressed nestmate—remains the same. Here, we describe research designed to address questions about the function, evolution, cause, and development of rescue behavior in C. piliscapa—a behavior ecological approach—drawing on research in other species, and by other researchers, both to highlight comparative similarities and differences and, importantly, to draw attention to still unanswered questions. In addition, by shedding light on the rescue behavior of ants, we also hope to engender increased attention to, and research on, this extraordinary form of helping behavior in multiple other taxa.


Fig. 3 Total duration in seconds of sand excavation performed by a potential helper (either a confirmed rescuer or a confirmed nonrescuer) to a victim (either a confirmed rescuer or a confirmed nonrescuer) in Experiment 1. Error bars represent the standard error of the mean. *** = P < .01
Fig. 4 Total duration in seconds of limb pulling performed by a potential helper (either a confirmed rescuer or a confirmed nonrescuer) to a victim (either a confirmed rescuer or a confirmed nonrescuer) in Experiment 1. Error bars represent the standard error of the mean. *** = P < .0001
Fig. 5 Total duration in seconds of snare biting performed by a potential helper (either a confirmed rescuer or a confirmed nonrescuer) to a victim (either a confirmed rescuer or a confirmed nonrescuer) in Experiment 1. Error bars represent the standard error of the mean. * = P = .03
Fig. 6 Total duration in seconds of rescue behavior delivered to victims belonging to one of four different age groups-namely less than 2 days of age, 5 days of age, 10 days of age, and 20 days of age. Error bars represent the standard error of the mean
Fig. 10 Total duration in seconds of responsivity behavior delivered by potential helpers belonging to one of four different age groupsnamely, less than 2 days of age, 5 days of age, 10 days of age, and 20 days of age. Error bars represent the standard error of the mean. ***P' < .001
Rescue specialists in Cataglyphis piliscapa ants: The nature and development of ant first responders

December 2021

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82 Reads

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7 Citations

Learning & Behavior

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Karen L. Hollis

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[...]

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Previous research in our laboratories has demonstrated that, within each colony of Cataglyphis piliscapa (formerly C. cursor) ants, only some individuals are capable of performing a complex sequence of behavioral patterns to free trapped nestmates—a sequence that not only is memory-dependent but also is responsive to the particular circumstances of that entrapment and how the rescue operation unfolds. Additionally, this rescue behavior is inherited patrilineally from but a few of the many males that fertilize the eggs of the colony’s single queen. Here, we describe three experiments to explore rescue behavior further—namely, whether rescuers are in any way selective about which nestmates they help, how the age of rescuers and the victims that they help affect the quantity and quality of the rescue operation, and when this complex behavior first emerges in an ant’s development. Taken together with the previous heritability analysis, these behavioral experiments provide clear evidence that the ability to rescue nestmates in distress should be recognized as a specialization, which together with other specialized tasks in C. piliscapa, contributes to a division of labor that increases the efficiency of the colony as a whole and, thus increases its reproductive success.


Analysis of ants’ rescue behavior reveals heritable specialization for first responders

February 2020

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60 Reads

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14 Citations

Journal of Experimental Biology

In colonies of Cataglyphis cursor ants, a single queen mates with multiple males, creating the foundation for heritable behavioral specializations. A novel and unique candidate for such specializations is rescue behavior, a precisely delivered form of altruism in which workers attempt to release trapped nestmates and which relies on short-term memory of previous actions to increase its efficiency. Consistent with task specialization, not all individuals participate; instead, some individuals move away from the victim, which gives rescuers unrestricted access. Using a bioassay to identify rescuers and non-rescuers, coupled with paternity assignment via polymorphic microsatellite markers, we not only show that rescue behavior is heritable, with 34% of the variation explained by paternity, but also establish that rescue, heretofore overlooked in analyses of division of labor, is a true specialization, an ant version of first responders. Moreover, this specialization emerges as early as 5 days of age, and the frequency of rescuers remains constant across ants' age ranges. The extremely broad range of these ants' heritable polyethism provides further support for the critical role of polyandry in increasing the efficiency of colony structure and, in turn, reproductive success.


Citations (38)


... This is a well-known non-invasive method for marking individuals and has been used without problem in A. carolinensis and other lizard species (e.g. Rodda et al., 1988;Robson and Miles, 2000;Lopez and Martin, 2001;Hollis et al., 2004;Henningsen and Irschick, 2012). When individuals lost their colour markings (for example by moulting) they were caught and the markings were reapplied. ...

Reference:

The (dis)advantages of dominance in a multiple male group of Anolis carolinensis lizards
Maintaining a Competitive Edge: Dominance Hierarchies, Food Competition and Strategies To Secure Food in Green Anoles (Anolis carolinensis) and Firemouth Cichlids (Thorichthys meeki)
  • Citing Article
  • December 2004

International Journal of Comparative Psychology

... Only one published study has claimed to demonstrate associative learning in Physarum (Shirakawa et al. 2011). As discussed in the subsequent literature (Dussutour 2021;Krause et al. 2022;Loy et al. 2021), and conceded by the authors themselves, the observed results have more parsimonious explanations. Pairing the food reward stimulus with the conditioned negative stimulus of low temperature, trained plasmodia were observed to move towards both stimuli, while untrained control plasmodia avoided the low-temperature option. ...

Introduction: Perspectives on the Evolution of Learning and Memory Mechanisms
  • Citing Chapter
  • May 2022

... Thus, in reality, the present state of each rescuer influences, and is influenced by, a complex, truly dynamically unfolding operation in which the actions of all rescuers contribute. In short, rescue in ants exhibits, yet again, that ants are not hardwired reflex automatons; instead, their execution of highly organized and precisely directed rescue behavior is one more example of their especially high cognitive capacities in general (Cheng, 2010;Kriete & Hollis, 2022;Perry et al., 2013). ...

Learning in Insects: Perspectives and Possibilities
  • Citing Chapter
  • May 2022

... The pond snail Lymnaea stagnalis is an important model system for studying the causal neuronal mechanisms of associative learning and the subsequent formation of long-term memory. Lymnaea can be both classically and operantly conditioned for a number of different behaviors, and researchers have primarily focused on feeding, withdrawal, and aerial respiratory behaviors [1][2][3][4][5]. Lymnaea possesses relatively simple nervous systems, and the neuronal circuits mediating many of the behaviors that exhibit learning and memory have been well elucidated. ...

Learning to anticipate mate presence shapes individual sex roles in the hermaphroditic pond snail, Lymnaea stagnalis

Animal Cognition

... Ant species with predacious habits and longer mandibles tend to have narrower and more elongated mandalus (Richter et al., 2021). It was found that there is possible involvement of mandibular glands in rescue behavior of certain ant species (Hollis and Nowbahari, 2022). Mandibular glands produce ectosymbiotic secretion with antibiotic properties that diffuse into plants when ants feed or groom the plant. ...

Cause, development, function, and evolution: Toward a behavioral ecology of rescue behavior in ants
  • Citing Article
  • February 2022

Learning & Behavior

... About twenty years ago Czechowski et al. (2002) employed the term "rescue behaviour" in the title and the text of the paper describing rescue behaviour displayed by workers of three ant species (Formica sanguinea, Formica fusca and Formica cinerea) in response to ant victims captured by predatory antlion larvae (Myrmeleon formicarius) [27]. This study provided inspiration for extensive further research carried out both in the field and in the laboratory with the use of two main bioassays: antlion larva capture bioassay, during which ant rescue behaviour was elicited in response to an ant captured by an antlion larva [88][89][90][91][92], and artificial snare bioassay, during which ant rescue behaviour was elicited in response to a victim ant entrapped in an artificial snare [28,88,90,91,[93][94][95][96][97][98][99][100][101][102][103][104][105][106]. ...

Rescue specialists in Cataglyphis piliscapa ants: The nature and development of ant first responders

Learning & Behavior

... Notably, research has focused on fruit flies and bees, but associative learning has been demonstrated in a variety of insect orders. Animals like cockroaches, mantids, beetles, moths, butterflies, and ants have been studied (Hollis & Guillette, 2015). It is considered that all insects rely on learning in many aspects of their life like foraging, predation, and navigation. ...

What Associative Learning in Insects Tells Us about the Evolution of Learned and Fixed Behavior

International Journal of Comparative Psychology

... About twenty years ago Czechowski et al. (2002) employed the term "rescue behaviour" in the title and the text of the paper describing rescue behaviour displayed by workers of three ant species (Formica sanguinea, Formica fusca and Formica cinerea) in response to ant victims captured by predatory antlion larvae (Myrmeleon formicarius) [27]. This study provided inspiration for extensive further research carried out both in the field and in the laboratory with the use of two main bioassays: antlion larva capture bioassay, during which ant rescue behaviour was elicited in response to an ant captured by an antlion larva [88][89][90][91][92], and artificial snare bioassay, during which ant rescue behaviour was elicited in response to a victim ant entrapped in an artificial snare [28,88,90,91,[93][94][95][96][97][98][99][100][101][102][103][104][105][106]. ...

Analysis of ants’ rescue behavior reveals heritable specialization for first responders
  • Citing Article
  • February 2020

Journal of Experimental Biology

... Cognitive abilities of ants are no less spectacular [110][111][112] and include, among others, cooperative transport of objects too large to be moved by a single individual [120][121][122], individual recognition of specific nestmates on the basis of chemical cues present on their body surface [123], tool use [124][125][126], ability to count steps to evaluate distances [127], rapid learning to avoid antlion traps following a single successful escape from a pit [128], and teaching of naive individuals by the more experienced ones [129,130]. ...

Natural Aversive Learning in Tetramorium Ants Reveals Ability to Form a Generalizable Memory of Predators' Pit Traps
  • Citing Article
  • March 2017

Behavioural Processes

... About twenty years ago Czechowski et al. (2002) employed the term "rescue behaviour" in the title and the text of the paper describing rescue behaviour displayed by workers of three ant species (Formica sanguinea, Formica fusca and Formica cinerea) in response to ant victims captured by predatory antlion larvae (Myrmeleon formicarius) [27]. This study provided inspiration for extensive further research carried out both in the field and in the laboratory with the use of two main bioassays: antlion larva capture bioassay, during which ant rescue behaviour was elicited in response to an ant captured by an antlion larva [88][89][90][91][92], and artificial snare bioassay, during which ant rescue behaviour was elicited in response to a victim ant entrapped in an artificial snare [28,88,90,91,[93][94][95][96][97][98][99][100][101][102][103][104][105][106]. ...

Organization of rescue behaviour sequences in ants, Cataglyphis cursor, reflects goal-directedness, plasticity and memory
  • Citing Article
  • February 2017

Behavioural Processes