Feng-Chun Lin’s research while affiliated with University of Otago and other places

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Publications (5)


The experiment arena was an acrylic tank (60 × 42 × 30 cm) filled with water to 15 cm depth. Wooden cubes (1.5 × 1.5 × 1 cm) colored with red acrylic paints (Mona, SG-203) was used as the quantitative stimuli, attached on two white Velcro boards (11 × 11 cm) with different number pairs. Each turtle was trained to swim toward the stimuli and was rewarded with a food pellet when it made a correct choice (the larger quantity) and reached the designated area (the square marked with blue stripes). The test questions included some highly challenging pairs, such as 8 vs 9 and 9 vs 10. We used a GoPro (SPTM1) and a JVC camcorder (GZ-E10BU) to record the behavioral responses to this system after a two-year retention interval
Memory recalls of the five turtles after the two-year retention interval. If a turtle achieved the criterion of that standard in a trial, the dot of that trial would be marked as filled; otherwise, it would be marked as open. MS16, MS33, and MS31 achieved their first correct choice on the 1st, 5th, and 9th trials, respectively, indicated by the red arrows. In contrast, MS11 and MS14 did not maintain behavioral stability. Although MS11 achieved the first correct choice on the 4th trial (indicated by the red question mark), it gave up making further choices after the 8th trial possibly due to a high failure rate. MS14 had the worst performance at this stage because it did not recognize the red cubes as rewards. The turtle IDs are ordered based on how quickly they were able to recall past memories
Recall curves for five stripe-necked turtles during the ten-day memory tests, ranked by their daily performance represented by success rates (%) above the columns. Each turtle underwent 22 trials daily for ten consecutive days. Light and dark bars represent the correct rates for Section 1 (1st – 11th trials) and Section 2 (12th – 22nd trials), respectively. The red lines of 0.5 success rate represent the level of random choice, while the 0.73 threshold represent their performance significantly better than random on a binomial distribution. The turtles are ordered based on the number of days it took for them to achieve statistically significant accuracy in their choices
A) A comparison of quantity discrimination abilities among the last day of the Initial Stage two years prior (July 11th, 2019), the first day of the Recall Stage (Day 1; July 21st, 2021), and the last day of the experiment (Day 10; July 30th, 2021). The dots represent individual values, the thick black lines indicate the medians, the boxes encompass the interquartile ranges, and the thin lines show the changes for each individual over time. Success rate of the turtles declined after a two-year retention interval and recovered after practice and training. B Mean probability of success predicted by the best-fit model in Table 1, with standard errors represented by the shaded areas, showing improvement over the days. However, there was no significant difference between the first section and the second section of each day. C Using 1000 bootstrap resampling iterations, the overall performance of the five turtles revealed individual differences: MS33 and MS31 performed better than MS14 and MS16, and both outperformed MS11. The points and whiskers represent the means and 95% confidence intervals, respectively
Comparison of numerosity concept in a freshwater turtle after a two-year retention interval
  • Article
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December 2024

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55 Reads

Behavioral Ecology and Sociobiology

Feng-Chun Lin

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Stephanie S. Godfrey

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Cognition and memory ability is pivotal for animal survival and is believed to be particularly adaptive for long-lived species. Numerosity discrimination, crucial for resource management and social interactions, provides a quantitative framework that allows us to compare the performance and the recovery of previously established concepts after a long-term retention interval. In this research, we investigated the capacity of freshwater turtles to remember the experimental process and gradually recall the abstract concept of “greater than”. Five striped-necked turtles (Mauremys sinensis), trained in 2019 to discriminate between quantities represented by red cubes, were retested after a two-year retention interval with no exposure to stimuli or human interaction. Three turtles remembered the training process to acquire food rewards from the stimuli within the first day of testing. However, regaining the concept of “greater than” required more time: one turtle reached 68% accuracy (P = 0.0669) on Day 1, another achieved 77% (P = 0.0085) on Day 2, and a third reached 82% (P = 0.0022) on Day 3. The latter two individuals retained this high accuracy until the end of the experiment. As the study continued, memory recall for each subject improved with greater efficiency than two years prior. Our study confirms that freshwater turtles retain long-term memory of abstract concepts learned two years earlier and reveals significant individual heterogeneity in their recall and decision-making processes. These findings underscore the need for more comprehensive research into the factors shaping animal cognition and behavior, particularly in understanding the ecological and evolutionary pressures that influence memory retention, individual variability, and decision-making strategies. Significance statement This study provides compelling evidence that freshwater turtles possess the ability to retain and recall abstract cognitive concepts over extended periods without reinforcement, highlighting their advanced cognitive capacities. By demonstrating that striped-necked turtles (Mauremys sinensis) can remember training and discriminate based on the concept of "greater than" after a two-year hiatus, our research not only challenges existing assumptions about reptilian memory capabilities but also enriches our understanding of cognitive evolution in long-lived species. The found individual differences in memory recall and decision-making underscore the complexity of animal cognition and highlight the significance of individual variability in behavioral studies. These insights contribute to a deeper understanding of the mechanisms that support long-term memory in animals.

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Hidden social complexity behind vocal and acoustic communication in non-avian reptiles

May 2024

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163 Reads

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2 Citations

Social interactions are inevitable in the lives of most animals, since most essential behaviours require interaction with conspecifics, such as mating and competing for resources. Non-avian reptiles are typically viewed as solitary animals that predominantly use their vision and olfaction to communicate with conspecifics. Nevertheless, in recent years, evidence is mounting that some reptiles can produce sounds and have the potential for acoustic communication. Reptiles that can produce sound have an additional communicative channel (in addition to visual/olfactory channels), which could suggest they have a higher communicative complexity, the evolution of which is assumed to be driven by the need of social interactions. Thus, acoustic reptiles may provide an opportunity to unveil the true social complexity of reptiles that are usually thought of as solitary. This review aims to reveal the hidden social interactions behind the use of sounds in non-avian reptiles. Our review suggests that the potential of vocal and acoustic communication and the complexity of social interactions may be underestimated in non-avian reptiles, and that acoustic reptiles may provide a great opportunity to uncover the coevolution between sociality and communication in non-avian reptiles. This article is part of the theme issue ‘The power of sound: unravelling how acoustic communication shapes group dynamics’.


The experimental arena and quantitative stimuli. a The experiment arena was an acrylic tank (60 × 42 × 30 cm) filled with water to 15 cm depth. We mounted a GoPro (SPTM1) to the back wall of the tank and set a JVC camcorder (GZ-E10BU) on a tripod next to the tank. b We used wooden cubes (1.5 × 1.5 × 1 cm) colored with red acrylic paints (Mona, SG-203) on a white Velcro board (11 × 11 cm) as the quantitative stimuli. c Each turtle was trained to swim toward the stimuli and was rewarded with a food pellet when it reached the designated area (the square marked with blue stripes) for the correct (larger) quantity
Comparison of ratio effects between red-eared slider (Trachemys scripta elegans, orange) and stripe-necked turtle (Mauremys sinensis, blue) in the fixed numerosity tests (Experiment 1). Each numerosity pair was tested 100 times on each individual, starting from the lowest ratio (1 vs 3, ratio = 0.33) to the highest ratio (6 vs 7, ratio = 0.86)
Comparison of ratio effects between red-eared slider (Trachemys scripta elegans, orange) and stripe-necked turtle (Mauremys sinensis, blue) in the mixed numerosity tests (Experiment 2). a The success rates between the two turtle species did not exhibit notable differences when all three phases were combined (Table S3). The performance of both species adhered to Weber’s law, where an increased ratio led to decreased performance (P < 0.001). b When analyzing the data separately by phase, the stripe-necked turtles showed a more pronounced decrease in performance during high-ratio trials compared to the sliders during the first phase (P = 0.0476)
Trained quantity discrimination in the invasive red-eared slider and a comparison with the native stripe-necked turtle

March 2024

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173 Reads

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1 Citation

Animal Cognition

Feng-Chun Lin

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Ming-Ying Hsieh

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[...]

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Little is known about the behavioral and cognitive traits that best predict invasion success. Evidence is mounting that cognitive performance correlates with survival and fecundity, two pivotal factors for the successful establishment of invasive populations. We assessed the quantity discrimination ability of the globally invasive red-eared slider (Trachemys scripta elegans). We further compared it to that of the native stripe-necked turtle (Mauremys sinensis), which has been previously evaluated for its superior quantity discrimination ability. Specifically, our experimental designs aimed to quantify the learning ability as numerosity pairs increased in difficulty (termed fixed numerosity tests), and the immediate response when turtles were presented with varied challenges concurrently in the same tests (termed mixed numerosity tests). Our findings reaffirm the remarkable ability of freshwater turtles to discern numerical differences as close as 9 vs 10 (ratio = 0.9), which was comparable to the stripe-necked turtle’s performance. However, the red-eared slider exhibited a moderate decrease in performance in high ratio tests, indicating a potentially enhanced cognitive capacity to adapt to novel challenges. Our experimental design is repeatable and is adaptable to a range of freshwater turtles. These findings emphasize the potential importance of cognitive research to the underlying mechanisms of successful species invasions.


The experiment arena and quantitative stimuli. A The experiment arena was an acrylic tank (60 × 42 × 30 cm) filled with water to 15 cm depth. We mounted a GoPro (CHDHB-601) to the back wall of the tank and a JVC camcorder (GZ-E10BU) on a tripod next to the tank. B We used wooden cubes (1.5 × 1.5 × 1 cm) colored with red acrylic paints (Mona, SG-203) on a white Velcro board (11 × 11 cm) as the quantitative stimuli. C Each turtle was trained to swim toward the stimuli and was rewarded with a food pellet when it reached the designated area (the square marked with blue stripes) for the correct (larger) quantity
The daily success rate of the turtles in the fixed numerosity tests (Experiment 1). Each numerosity pair was tested 20 times per day on each of the five turtles for five days. The entire experiment lasted 25 days, starting from the lowest ratio (1 versus 3, ratio = 0.33, day 1–5) to the highest ratio (6 versus 7, ratio = 0.85, day 21–25) including two transfer tests and one conflict test. The solid lines with shaded areas are predicted mean probabilities of success ± 1 standard error, estimated from the best-fit model (Table 2 & Additional file 1: Table S2). The horizontal dashed line denotes random choice of the smaller and larger quantity
The 5-day averaged success rate of the turtles in the mixed numerosity tests (Experiment 2). Each numerosity pair was tested twice a day in a random order on each of the five turtles for five days. A Phase I comprised numerosity pairs of small numbers (1–5) with a ratio ranging 0.2–0.8; B Phase II comprised numerosity pairs of at least one large number (6–10) with a ratio ranging 0.2–0.8; C Phase III comprised numerosity pairs of at least one large number (6–10) with a ratio ranging 0.2–0.9. The solid lines with shaded areas are predicted mean probabilities of success ± 1 standard error, estimated from the best-fit model (Table 2 & Additional file 1: Table S3). The dots are the observed success rates with 10% jittering using jitter function in R v3.6.1, and the horizontal dashed line denotes random choice of the smaller and larger quantity
Superior continuous quantity discrimination in a freshwater turtle

September 2021

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248 Reads

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19 Citations

Frontiers in Zoology

Background Quantity discrimination, the ability to discriminate a magnitude of difference or discrete numerical information, plays a key role in animal behavior. While quantitative ability has been well documented in fishes, birds, mammals, and even in previously unstudied invertebrates and amphibians, it is still poorly understood in reptiles and has never been tested in an aquatic turtle despite the fact that evidence is accumulating that reptiles possess cognitive skills and learning ability. To help address this deficiency in reptiles, we investigated the quantitative ability of an Asian freshwater turtle, Mauremys sinensis , using red cubes on a white background in a trained quantity discrimination task. While spontaneous quantity discrimination methods are thought to be more ecologically relevant, training animals on a quantity discrimination task allows more comparability across taxa. Results We assessed the turtles’ quantitative performance in a series of tests with increasing quantity ratios and numerosities. Surprisingly, the turtles were able to discriminate quantities of up to 9 versus 10 (ratio = 0.9), which shows a good quantitative ability that is comparable to some endotherms. Our results showed that the turtles’ quantitative performance followed Weber’s law, in which success rate decreased with increasing quantity ratio across a wide range of numerosities. Furthermore, the gradual improvement of their success rate across different experiments and phases suggested that the turtles possess learning ability. Conclusions Reptile quantitative ability has long been ignored and therefore is likely under-estimated. More comparative research on numerical cognition across a diversity of species will greatly contribute to a clearer understanding of quantitative ability in animals and whether it has evolved convergently in diverse taxa.

Citations (3)


... Thus far, we have established that reptiles can produce and use a range of vocal and non-vocal acoustic signals. Following Lin et al. [110], we suggest that these signals may be used as mediators of complex social behaviours. Exploring how these signals may vary across populations could inform us about cultural behaviours in this group. ...

Reference:

Cold-blooded culture? Assessing cultural behaviour in reptiles and its potential conservation implications
Hidden social complexity behind vocal and acoustic communication in non-avian reptiles

... During the training phase, it typically took several weeks for the turtles to associate food with the tweezers, and a similar amount of time to transfer the food reward from the tweezers to the red cubes. Although the learning speed varied for each individual, the overall training time was approximately 60 days (Lin et al. 2024). Therefore, response to the red cubes on either Day 1 (MS16, MS33, and MS31) or Day 2 (MS11 and MS14) was likely due to memory rather than relearning. ...

Trained quantity discrimination in the invasive red-eared slider and a comparison with the native stripe-necked turtle

Animal Cognition

... As ratios get smaller, the quantities become more dissimilar, and differences become easier to detect. A large range of species have shown ratio dependence in quantification tasks (Beran, 2001;Potrich et al., 2015;Ditz & Nieder, 2016;Lucon-Xiccato et al., 2018;d'Ettorre et al., 2021;Lin et al., 2021). Researchers typically interpreted ratio effects on quantitative judgments as evidence supporting Weber's Law. ...

Superior continuous quantity discrimination in a freshwater turtle

Frontiers in Zoology