Tests of planning and the Bischof-Köhler hypothesis in rhesus monkeys (Macaca mulatta)

The Bischof-Köhler hypothesis posits that nonhuman animals cannot plan for future motivational states that differ from a current state. [Naqshbandi, M., Roberts, W.A., 2006. Anticipation of future events in squirrel monkeys Samiri scireus and rats Rattus norvegicus: tests of the Bischof-Köhler hypothesis. J. Comp. Psychol. 120, 345–357] found that two squirrel monkeys that were not thirsty at the time of choice reversed their preference for a larger amount of food when choice of a smaller amount alleviated future thirst. This apparent anticipation of future thirst contradicts the Bischof-Köhler hypothesis. We used the methods described by Naqshbandi and Roberts with rhesus monkey subjects and found that the monkeys did not alter their behavior in anticipation of future thirst. To assess which factors enhance and inhibit the ability to express planning, we then systematically modified the experimental design in four subsequent experiments and found that monkeys that were not thirsty acted to alleviate future thirst only when the delay between their behavior and the contingent outcome was brief. Taken together these results suggest that the inability of rhesus monkeys to display planning resulted from their inability to learn behavior-outcome associations across long-delay intervals as would be expected from traditional accounts of operant learning, rather than from failure to anticipate future motivational states as posited by the Bischof-Köhler hypothesis.     

Can animals recall the past and plan for the future?

According to the 'mental time travel hypothesis' animals, unlike humans, cannot mentally travel backwards in time to recollect specific past events (episodic memory) or forwards to anticipate future needs (future planning). Until recently, there was little evidence in animals for either ability. Experiments on memory in food-caching birds, however, question this assumption by showing that western scrub-jays form integrated, flexible, trial-unique memories of what they hid, where and when. Moreover, these birds can adjust their caching behaviour in anticipation of future needs. We suggest that some animals have elements of both episodic-like memory and future planning.     

Ravens judge competitors through experience with play caching

Complex social behavior builds on the mutual judgment of individuals as cooperation partners and competitors [1]. Play can be used for assessing the others' dispositions in humans and nonhuman mammals [2], whereas little is known about birds. Recently, food-caching corvids have been found to rival primates in their ability to judge the behaviors and intentions of others in competition for hidden food [3]. Here, we show that ravens Corvus corax quickly learn to assess the competitive strategies of unfamiliar individuals through interactions with them over caches with inedible items and subsequently apply this knowledge when caching food. We confronted birds with two human experimenters who acted differently when birds cached plastic items: the pilferer stole the cached objects, whereas the onlooker did not. Birds responded to the actions of both experimenters with changing the location of their next object caches, either away from or toward the humans, as if they were testing their pilfering dispositions. In contrast, ravens instantly modified their caching behavior with food, preventing only the competitive human from finding the caches. Playful object caching in a social setting could thus aid ravens in evaluating others' pilfering skills.     

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli)

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.     

Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply

In the temperate zone, permanent-resident birds and mammalsthat do not hibernate must survive harsh winter conditions oflow ambient temperature, long nights, and reduced food levels.To understand the energy management strategy of food-hoardingbirds, it has been hypothesized that such birds respond to increasedstarvation risk by increasing the number of their hoards ratherthan by increasing their fat reserves and that they cache earlyin the day and retrieve their caches later to achieve fat reservesnecessary to survive the night We tested these hypotheses byobserving the responses in captivity of a caching bird, thetufted titmouse (Parus bicolor), to the combined influencesof reduced predictability of food and naturally occurring ambienttemperature and photoperiod. When the food supply was unpredictable,birds significantly increased both internal fat reserves atdusk and external food caches. Initially leaner birds tendedto increase their fat reserves to a greater extent and initiallyfatter birds tended to cache more food and to fly significantlyless. Half the birds also increased their dawn and mean dailybody mass. All birds tended to forage, gain body mass, and cachefood at significantly lower rates in the morning and at significantlyhigher rates in the evening. Cache retrieval showed the oppositetrend, with birds retrieving most of their caches in the morning.Our results do not support the hypothesis that caching birdsincrease caching rate but not body mass under an unpredictablefood regime. Instead fat reserves and food caches are both importantcomplementary sources of energy in food-hoarding birds. Energymanagement by wintering birds occurs in response to a numberof biotic and abiotic factors acting simultaneously; thus futuremodels must incorporate independent variables in addition tothe state of the food supply and time of day     

Nitric oxide-induced formation of the S-2 state in the oxygen-evolving complex of photosystem II from Synechococcus elongatus

In spinach photosystem II (PSII) membranes, the tetranuclear manganese cluster of the oxygen-evolving complex (OEC) can be reduced by incubation with nitric oxide at -30 degrees C to a state which is characterized by an Mn(2)(II, III) EPR multiline signal [Sarrou, J., Ioannidis, N., Deligiannakis, Y., and Petrouleas, V. (1998) Biochemistry 37, 3581-3587]. This state was recently assigned to the S(-)(2) state of the OEC [Schansker, G., Goussias, C., Petrouleas, V., and Rutherford, A. W. (2002) Biochemistry 41, 3057-3064]. On the basis of EPR spectroscopy and flash-induced oxygen evolution patterns, we show that a similar reduction process takes place in PSII samples of the thermophilic cyanobacterium Synechococcus elongatus at both -30 and 0 degrees C. An EPR multiline signal, very similar but not identical to that of the S(-)(2) state in spinach, was obtained with monomeric and dimeric PSII core complexes from S. elongatus only after incubation at -30 degrees C. The assignment of this EPR multiline signal to the S(-)(2) state is corroborated by measurements of flash-induced oxygen evolution patterns and detailed fits using extended Kok models. The small reproducible shifts of several low-field peak positions of the S(-)(2) EPR multiline signal in S. elongatus compared to spinach suggest that slight differences in the coordination geometry and/or the ligands of the manganese cluster exist between thermophilic cyanobacteria and higher plants.     

Predators' toxin burdens influence their strategic decisions to eat toxic prey

Toxic prey advertise their unprofitability to predators via conspicuous aposematic coloration [1]. It is widely accepted that avoidance learning by naive predators is fundamental in generating selection for aposematism [2, 3] and mimicry [4, 5] (where species share the same aposematic coloration), and consequently this cognitive process underpins current evolutionary theory [5, 6]. However, this is an oversimplistic view of predator cognition and decision making. We show that predators that have learned to avoid chemically defended prey continue to attack defended individuals at levels determined by their current toxin burden. European starlings learned to discriminate between sequentially presented defended and undefended mealworms with different color signals. Once birds had learned to avoid the defended prey at a stable asymptotic level, we experimentally increased their toxin burdens, which reduced the number of defended prey that they ingested in the subsequent trial. This was due to the birds making strategic decisions to ingest defended prey on the basis of their visual signals. Birds are clearly able to learn about the nutritional benefits and defensive costs of eating defended prey, and they regulate their intake according to their current physiological state. This raises new perspectives on the evolution of aposematism, mimicry, and defense chemistry.     

Sexual differences in food re-caching by New Zealand robins Petroica australis

We presented monogamous pairs of New Zealand robins Petroica australis with a superabundant supply of artificial prey and then observed birds re-cache previously hoarded prey. Males and females frequently relocated and redistributed previously hoarded prey. Both sexes also re-cached prey that was originally hoarded by their mate. However, re-caching rates of retrieved and pilfered prey differed between sexes. Female-made caches were re-cached at the same rate by both females and pilfering males, while male-made caches were re-cached more frequently by pilfering females. The re-caching of previously hoarded prey is consistent with the hypothesis that re-caching reduces theft. However, re-caching pilfered prey suggests that it might also play a role in cache theft strategies. Higher rates of re-caching by pilfering females cannot be explained by current hypotheses used to account avian re-caching behaviours. We suggest two new hypotheses, sexual dimorphism in spatial memory and indirect mate provisioning, which may help to explain the evolution of re-caching in New Zealand robins.     

Decay products of the S(3) state of the oxygen-evolving complex of photosystem II at cryogenic temperatures. Pathways to the formation of the S = 7/2 S(2) state configuration

The water-oxidizing complex of photosystem II cycles through five oxidation states, denoted S(i)() (i = 0-4), during water oxidation to molecular oxygen, which appears at the (transient) S(4) state. The recent detection of bimodal EPR signals from the S(3) state [Matsukawa, T., Mino, H., Yoneda, D., Kawamori, A. (1999) Biochemistry 38, 4072-4077] has drawn significant attention to this critical state. An interesting property of the S(3) state is the sensitivity to near-IR (NIR) light excitation. Excitation of the S(3) state by near-IR light at cryogenic temperatures induces among other signals a derivative-shaped EPR signal at g= 5 [Ioannidis, N., and Petrouleas, V. (2000) Biochemistry 39, 5246-5254]. The signal bears unexpected similarities to a signal observed earlier in samples that had undergone multiple turnovers and subsequently had been stored at 77 K for a week or longer [Nugent, J. H. A., Turconi, S., and Evans, M. C. W. (1997) Biochemistry 36, 7086-7096]. Recently, both signals were assigned to an S = 7/2 configuration of the Mn cluster [Sanakis, Y., Ioannidis, N., Sioros, G., and Petrouleas, V. (2001) J. Am. Chem. Soc. 123, 10766-10767]. In the present study, we employ bimodal EPR spectroscopy to investigate the pathways of formation of this unusual state. The following observations are made: (i) The g = 5 signal evolves in apparent correlation with the diminution of the S(3) state signals during the slow (tens of hours to several days range) charge recombination of S(3) with Q(A)(-) at 77 K. The tyrosyl radical D* competes with S(3) for recombination with Q(A)(-), the functional redox couple at cryogenic temperatures inferred to be D*/D(-). Transfer to -50 degrees C and above results in the relaxation of the g = 5 to the multiline and g = 4.1 signals of the normal S(2) state. (ii) The transition of S(3) to the state responsible for the g = 5 signal can be reversed by visible light illumination directly at -30 degrees C or by illumination at 4.2 K followed by brief (2 min) transfer to -50 degrees C in the dark. The latter step is required in order to overcome an apparent thermal activation barrier (charge recombination appears to be faster than forward electron transfer at 4.2 K). (iii) The "g = 5" state can be reached in a few tens of minutes at 4.2 K by near-IR light excitation of the S(3) state. This effect is attributed to the transfer of the positive hole from the Mn cluster to a radical (probably tyr Z), which recombines much faster than the Mn cluster with Q(A)(-). (iv) The above properties strongly support the assignment of the configuration responsible for the g = 5 signal to a modified S(2) state, denoted S(2)'. Evidence supporting the assignment of the S(2)' to a proton-deficient S(2) configuration is provided by the observation that the spectrum of S(2) at pH 8.1 (obtained by illumination of the S(1) state at -30 degrees C) contains a g = 5 contribution.     

Memory for food caches: not just for retrieval

Many animals use hoarding as a long-term strategy to ensurea food supply at times of shortage. Hoarders employ strategiesthat enhance their ability to relocate caches such as rememberingwhere caches are located. Long-term scatterhoarders, whose cacheshave potentially high pilferage rates, should also hoard ina way to reduce potential cache pilferers' ability to find caches.Previous studies have demonstrated that this could be achievedby hyperdispersing caches to reduce the foraging efficiencyof pilferers. This study investigates whether coal tits (Parusater) indeed place their caches away from existing ones. Inour experiment, birds hoarded food in 3 conditions: when cachesfrom a previous storage session were still present, when cachesfrom a previous storage session were not present anymore becausethe bird had retrieved them, and when caches from a previousstorage session had been removed by the experimenter. We showthat coal tits hoard away from existing caches and that theydo not use cues from extant caches to do this. This evidenceis consistent with the use of memory for the locations of previouscaches when deciding where to place new caches. This findinghas important implications for our understanding of the selectivepressures that have shaped spatial memory in food-hoarding birds.     

A dynamic model of short-term energy management in small food-caching and non-caching birds

The survival of small birds in winter is critically dependenton the birds' ability to accumulate and maintain safe levelsof energy reserves. In some species, food caching facilitatesenergy regulation by providing an energy source complementaryto body fat. We present a dynamic optimization model of short-term,diurnal energy management for both food-caching and non-caching birds in which only short-day, winter conditions are considered.We assumed that birds can either rest, forage and eat, forageand cache, or retrieve existing caches (the two latter optionsare available only to caching birds). The model predicted thatwhen there is variability in foraging success (here modeledstrictly as within-day variability), both caching and non-caching birds should increase their fat reserves almost linearly inthe morning slowing down toward late afternoon, a result consistentwith field data but different than the result of a previousdynamic program. Non-cachers were predicted to carry higherfat levels than cachers especially when the variability inforaging success is high. Probability of death for non-caching birds was predicted to be higher than that for cachers, especiallyat higher levels of variability in foraging success. Amongcaching birds, an increase in number of caches and fat reserveswas also predicted if: (1) mean foraging success was decreased,(2) variability in foraging success was increased, and (3)energy expenditure at night was increased over our baselineconditions. Under the conditions simulated in our model, birdswere predicted to cache only if cache half-life (i.e., timeinterval over which 50% of the caches are forgotten or lostto pilferage) exceeded 2.5 days, indicating that low pilferagerate and long memory favor more caching. Finally, we showedthat such daily patterns of energy management do not necessarilyrequire relaxing assumptions about mass-dependent predationrisk.     

Dosage compensation in birds

The Z and W sex chromosomes of birds have evolved independently from the mammalian X and Y chromosomes [1]. Unlike mammals, female birds are heterogametic (ZW), while males are homogametic (ZZ). Therefore male birds, like female mammals, carry a double dose of sex-linked genes relative to the other sex. Other animals with nonhomologous sex chromosomes possess "dosage compensation" systems to equalize the expression of sex-linked genes. Dosage compensation occurs in animals as diverse as mammals, insects, and nematodes, although the mechanisms involved differ profoundly [2]. In birds, however, it is widely accepted that dosage compensation does not occur [3-5], and the differential expression of Z-linked genes has been suggested to underlie the avian sex-determination mechanism [6]. Here we show equivalent expression of at least six of nine Z chromosome genes in male and female chick embryos by using real-time quantitative PCR [7]. Only the Z-linked ScII gene, whose ortholog in Caenorhabditis elegans plays a crucial role in dosage compensation [8], escapes compensation by this assay. Our results imply that the majority of Z-linked genes in the chicken are dosage compensated.     

贮食动物的盗食与反盗食行为策略

食物贮藏是许多动物应对食物短缺、保障其生存和繁衍的一种适应性行为。保护好贮藏食物以供食物短缺期利用,是食物贮藏成功的标志和进化动力。同种或异种动物盗食是贮藏食物损失的重要原因。嗅觉、视觉与空间记忆、随机搜寻等是动物搜寻和盗取食物的重要手段;避免盗食、阻止盗食和容忍盗食是动物反盗食的重要策略。动物通常采用多种行为策略进行盗食和反盗食,分配食物资源,形成相对稳定的种内、种间关系。盗食与反盗食互作及其对贮食行为进化的意义已成为行为生态学的研究热点和前沿之一,针对鸟类和哺乳类动物的研究尤为丰富。本文总结了贮食动物常见的盗食和反盗食行为策略及其相互作用的研究进展,主要内容涉及贮食动物利用嗅觉、视觉与空间记忆、随机搜寻等盗取其他个体食物的盗食策略,以及通过隐藏、转移、保卫、容忍等方式减少被盗食,保护贮藏食物的行为策略。针对现有研究状况,从种间盗食与反盗食及其与物种共存的关系,种间非对称盗食关系及其适应意义,盗食与反盗食最适行为策略及其与贮食动物适合度的关系等方面对今后研究提出了建议。     

A long-distance avian migrant compensates for longitudinal displacement during spring migration

In order to perform true bicoordinate navigation, migratory birds need to be able to determine geographic latitude and longitude. The determination of latitude is relatively easy from either stellar or magnetic cues [1-3], but the determination of longitude seems challenging [4, 5]. It has therefore been suggested that migrating birds are unable to perform bicoordinate navigation and that they probably only determine latitude during their return migration [5]. However, proper testing of this hypothesis requires displacement experiments with night-migratory songbirds in spring that have not been performed. We therefore displaced migrating Eurasian reed warblers (Acrocephalus scirpaceus) during spring migration about 1000 km toward the east and found that they were correcting for displacements by shifting their orientation from the northeast at the capture site to the northwest after the displacement. This new direction would lead them to their expected breeding areas. Our results suggest that Eurasian reed warblers are able to determine longitude and perform bicoordinate navigation. This finding is surprising and presents a new intellectual challenge to bird migration researchers, namely, which cues enable birds to determine their east-west position.     

Diplochory in western chokecherry: you can��t judge a fruit by its mesocarp

Western chokecherry (Prunus virginiana var. demissa, Rosaceae) is dispersed by frugivorous birds and carnivores, but it has large seeds that are potentially attractive to rodents that could act as seed predators and dispersers. Here, we quantify the benefits of primary dispersal by birds and secondary dispersal by scatter-hoarding rodents. In the fall, avian frugivores (mostly American robins, Turdus migratorius, and cedar waxwings, Bombycilla cedrorum) consumed 87% of the fruit crop and dispersed 67% of the fruit crop away from parent plants. Rodents removed 89% of seeds that simulated bird-dispersed seed rain from transects in riparian zones and 58% from transects in upland habitats. Rodents scatter-hoarded 91.6% of the seeds they removed, burying most in small caches (two to eight seeds) 8?C25?mm deep. About 39% of the seeds in spring caches produced seedlings. Inside rodent-proof exclosures, 52.1% of seeds buried to simulate rodent caches produced seedlings, 29.7% of which were still alive after 1?year. In contrast, only 3.8% of seeds placed on the soil surface, simulating dispersal by avian frugivores, produced seedlings. Seed dispersal by frugivorous birds likely contributes to colonization of unoccupied habitat through long-range dispersal and to escape from distance-dependent seed mortality near the parent plant. Despite seed losses, rodents offer short-range seed dispersal and bury seeds in more favorable sites for germination, improving seedling emergence and establishment. The combined mechanisms of seed dispersal significantly enhanced chokecherry seedling recruitment by providing more dispersal-related benefits than either frugivorous bird or scatter-hoarding rodents could provide alone.     

Clark's Nutcrackers Nucifraga columbiana Remember the Size of Their Cached Seeds

Clark's nutcrackers ( Nucifraga columbiana ) hide thousands of seeds in subterranean caches that they later recover using spatial information about cache location. In two experiments, we tested whether nutcrackers also remember another type of information regarding their caches – the size of the seeds in each cache. We videotaped birds during cache recovery and then measured their bill gape during probing behaviour as captured on the videotape. In experiment one, six birds each experienced two treatments: one that allowed them to cache and then recover large seeds, and the other, an identical treatment using small seeds. During this experiment, all six birds used a wider gape when attempting to recover seeds during the large-seed treatment than during the small-seed treatment, and gape width was significantly correlated with seed size. During experiment two, we presented birds with both large and small seeds within the same caching session. We also increased the retention interval between caching and recovery. These modifications increased the difficulty of the task. Six of the seven birds used a wider gape during seed recovery when digging for caches that contained large seeds than they did when searching for small seeds. The ability to remember the size of seeds placed within caches may serve to increase the likelihood of speedy and successful recovery. It also allows the birds another level of organization of their food supply. These are the first experiments to suggest that Clark's nutcrackers remember more about their caches than location alone.     

Observational visuospatial encoding of the cache locations of others by western scrub-jays (<Emphasis Type="Italic">Aphelocoma californica</Emphasis>)

Western scrub-jays (Aphelocoma californica) hide food and rely on spatial memory to recover their caches at a later date. They also rely on observational spatial memory to steal caches made by other individuals. Successful pilfering may require an understanding of allocentric space because the observer will often be in a different position from the demonstrator when the caching event occurs. We compared cache recovery accuracy of pairs of observers that watched a demonstrator cache food. The pattern of recovery searches showed that observers were more accurate when they had observed the caching event from the same viewing direction as the demonstrator than when they had watched from the opposite direction. Search accuracy was not affected by whether or not the tray-specific local cues provided left–right landmark information (i.e. heterogeneous vs. homogeneous local cues), or whether or not the caching tray location was rotated. Taken together, these results suggest that observers have excellent spatial memory and that they have little difficulty with mental rotation.     

Alterations of the oxygen-evolving apparatus in a (448)Arg --> (448)S mutant in the CP47 protein of photosystem II under normal and low chloride conditions

We have shown previously that a mutant which contained the alteration (448)R --> (448)S (R448S) in the CP47 protein of photosystem II exhibited a defect in its ability to grow and assemble functional photosystem II reaction centers under chloride-limiting conditions [Wu, J., Masri, N., Lee, W., Frankel, L. K., and Bricker, T. M. (1999) Plant Mol. Biol. 39, 381-386]. In this paper we have examined the function of the oxygen-evolving complex under chloride-sufficient (480 microM) and chloride-limiting (< 20 microM) conditions. When placed under chloride-limiting conditions, both the control strain K3 and R448S cells exhibit a loss of steady-state oxygen evolution, with t(1/2) of 16 and 17 min, respectively. Upon the addition of chloride, both recover their oxygen-evolving capacity relatively rapidly. However, R448S exhibits a much slower reactivation of oxygen evolution than does K3 (t(1/2) of 308 and 50 s, respectively). This may indicate a defect at the low-affinity, rapidly exchanging chloride-binding site [Lindberg, K., and Andréasson, L.-E. (1996) Biochemistry 35, 14259-14267]. Additionally, alterations in the distribution of S states and S-state lifetimes were observed. Under chloride-sufficient conditions, the R448S mutant exhibits a significant increase in the proportion of reaction centers in the S(3) state and a greatly increased lifetime of the S(3) state. Under chloride-limiting conditions, the proportion of reaction centers in both the S(2) and S(3) states increases significantly, and there is a marked increase in the lifetime of the S(2) state. These alterations are not observed in the control strain K3. Our observations support the hypothesis that (448)R of CP47 may participate in the formation of the binding domain for chloride in photosystem II and/or in the functional interaction with the 33 kDa protein with the photosystem.     

Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist

Food-caching corvids hide food, but such caches are susceptible to pilfering by other individuals. Consequently, the birds use several counter strategies to protect their caches from theft, e.g. hiding most of them out of sight. When observed by potential pilferers at the time of caching, experienced jays that have been thieves themselves, take further protective action. Once the potential pilferers have left, they move caches those birds have seen, re-hiding them in new places. Naive birds that had no thieving experience do not do so. By focusing on the counter strategies of the cacher when previously observed by a potential pilferer, these results raise the intriguing possibility that re-caching is based on a form of mental attribution, namely the simulation of another bird's viewpoint. Furthermore, the jays also keep track of the observer which was watching when they cached and take protective action accordingly, thus suggesting that they may also be aware of others' knowledge states.