Logical problems and misunderstandings in “problems with dimensionless measurement models of synchrony in biological systems”

A model for the standardized measurement of synchrony in behavioral or biological states was proposed for use in comparative analyses of synchrony's adaptive significance. A recent critique attempts to discredit dimensionless (unitless) or standardized measures of synchrony in general and the proposed model in particular. Although the critique helps define and sharpen thinking about the measurement of synchrony and makes some well‐taken points, it also arrives at questionable conclusions based upon dubious assumptions. The critique proceeds from a fictional example in which all biological states being considered always have exactly the same durations for all individuals and always start or end for all individuals at exactly the same instants in time. These unreal, biologically meaningless premises, together with other questionable assumptions, are the basis of inappropriate analyses of standardized measures. The critique's arguments reveal a failure to understand the basic underlying principle of the standardized method and are dependent upon faulty logic. A statistical discussion contains both worthy points and arguable comments based not on data or actual probabilities of real events but on irrelevant chance outcomes derived from the biologically meaningless assumptions. The critique's conclusions are not credible, and its basic question probably is not scientifically answerable. Am. J. Primatol. 47:29–42, 1999. © 1999 Wiley‐Liss, Inc.     

A New Type of Synchronized Flashing in a North American Firefly

Continuous synchronic flashing occurs in stationary and flying male congregations of members of some firefly species in Southeast Asia. In the present paper, low-light videography and photometry was used to demonstrate that synchrony occurs in the North American genus Photuris. We found that the Georgia coastal plain firefly Ph. frontalis flashed synchronically. From a distance, the synchronic flashes of a population of flying Ph. frontalis appeared to occur in a continuous synchrony. However, when pairs of males were viewed, it was difficult to verify that their flashing was continuously synchronic. In the laboratory, caged fireflies flashed synchronically, stopped, and then flashed synchronically again. To study this flash behavior, recordings of individual and group flashing were analyzed statistically to validate the conclusions about rhythm and synchrony. Although the mass synchrony appeared continuous, the individual flying males switch on and off, coming in again on the beat. The synchrony in Ph. frontalis is common and pervasive rather than rare and sporadic, as shown by other North American fireflies. The precision of the frontalis synchrony approaches that of Southeast Asian fireflies. The intermittent synchrony of this firefly reinforces the evidence that there is a diversity of synchronies in fireflies.     

The occurrence of synchrony in the North American fireflyPhotinus carolinus (Coleoptera: Lampyridae)

Synchronous flashing has been described for some Southeast Asian fireflies but has rarely been reported in North American fireflies. Our field observations indicated thatPhotinus carolinus flash synchronously. The flash pattern of individualP. carolinus was characterized by a burst of five to eight flashes over a period of approximately 4 s. These flash bursts were repeated about every 12 s. Groups of fireflies comprised individuals exhibiting this species-specific flash pattern. Remarkably, members of the group flashed synchronously: Flash bursts started and stopped at the same time and the flashes among individuals occurred at the same time as well. We used low-light level videography to examine this behavior in caged groups of (3 or 10) fireflies for synchronic flashing. The occurrence of concurrent rhythmic group flashing satisfies the criteria for synchrony as defined by Buck (1988). The intermittent nature of the bursts of flashes shown byP. carolinus makes this a discontinuous synchrony. The mechanisms underlying discontinuous synchrony are not known.     

Population synchrony within and among Lepidoptera species in relation to weather, phylogeny, and larval phenology

Abstract.  1. The population dynamics of native herbivore species in central Appalachian deciduous forests were studied by analysing patterns of synchrony among intra- and interspecific populations and weather.
2. Spatial synchrony of 10 Lepidoptera species and three weather variables (minimum temperature, maximum temperature, precipitation) from 12 sites was measured using cross-correlation functions relating levels of synchrony to the distance separating each set of populations. Based on both the pattern of synchrony and the region-wide cross-correlation coefficients, Lepidoptera species appear to be synchronised, at least in part, by local weather conditions.
3. Interspecific cross-correlations were calculated for all sympatric species pairs and trends in interspecific synchrony were related to phylogenetic relatedness, life-history timing, and weather. Interspecific synchrony was highest among species whose larvae were present during the same time of the season, but there was no relationship between interspecific synchrony and phylogenetic affinity.
4. Spatial synchrony of weather variables was significantly related to both species of some interspecific pairs, indicating weather as a potential mechanism involved in synchronising populations of different species.     

Problems with dimensionless measurement models of synchrony in biological systems

Synchrony is surprisingly complex even in the simplest cases. One strategy for simplifying complex phenomena is to define a dimensionless measurement model with the aim of (1) finding order, (2) comparing complex phenomena, and (3) making decisions about statistical significance. However, a model is only as good as its assumptions. In this paper, several types of dimensionless measurement models of synchrony among biological states are evaluated using the preceding criteria. These dimensionless measurement models are found to be inadequate even in the simplest cases of N individuals cycling through k non-overlapping states. Moreover, independent of their adequacy as measures of synchrony, there is the additional problem of the applicability of biological-state measurement models to rhythmic biological processes. Biological states are often just quantized observations of the phases of rhythmic biological processes. With the help of a concrete example, it is shown that quantizing the phases of a process into discrete states can lead to serious errors. These conclusions do not imply that the study of synchrony in biological systems is intractable. There are statistical approaches for detecting synchrony in groups and researchers are making progress towards understanding the general mechanisms of rhythmic phenomena in biological systems. Am. J. Primatol. 41:65–85, 1997. © 1997 Wiley-Liss, Inc.     

Marching into battle: synchronized walking diminishes the conceptualized formidability of an antagonist in men

Paralleling behaviours in other species, synchronized movement is central to institutionalized collective human activities thought to enhance cooperation, and experiments demonstrate that synchrony has this effect. The influence of synchrony on cooperation may derive from an evolutionary history wherein such actions served to signal coalitional strength to both participants and observers—including adversaries. If so, then synchronous movement should diminish individuals'' estimations of a foe''s formidability. Envisioned physical size and strength constitute the dimensions of a representation that summarizes relative fighting capacity. Experiencing synchrony should therefore lead individuals to conceptualize an antagonist as smaller and weaker. We found that men who walked synchronously with a male confederate indeed envisioned a purported criminal as less physically formidable than did men who engaged in this task without synchronizing.     

Adult male Cuvier's beaked whales (Ziphius cavirostris) engage in prolonged bouts of synchronous diving

Studies of the social behavior of Cuvier's beaked whales (Ziphius cavirostris) are challenging because of their deep-water habitat usually far from shore and the limited time they spend at the surface. The sociality of these deepest diving mammals is of interest, however, especially for our understanding of how social systems evolve in extreme habitats. High levels of scarring suggest that males compete agonistically for access to females and so we predicted that associations among adult males would be unstable due to competitive exclusion. We tested this prediction by evaluating the diving behavior of animals within social groups off Cape Hatteras, North Carolina, considering diving synchrony a proxy for group membership. Using data from satellite-linked depth-recording tags, we found that adult male–male pairs showed extended periods of synchrony in diving behavior, while all pairs that included an adult male with an individual of another age and/or sex dove synchronously for less than a day. We assessed three hypotheses to explain these surprising results: sexual segregation; extended bouts of male–male competition; and the presence of male alliances. Finally, we considered testable predictions to distinguish among these explanations.     

The sugarcane borer Diatraea saccharalis (Fabr.) (Lep., Crambidae) and its parasitoids: a synchrony approach to spatial and temporal dynamics

Abstract:  A data set on Diatraea saccharalis and its parasitoids, Cotesia flavipes and tachinid flies, was analysed at five spatial scales – sugarcane mill, region, intermediary, farm and zone – to determine the role of spatial scale in synchrony patterns, and on temporal population variability. To analyse synchrony patterns, only the three highest spatial scales were considered, but for temporal population variability, all spatial scales were adopted. The synchrony–distance relationship revealed complex spatial structures depending on both species and spatial scale. Temporal population variability [SD log( x  + 1)] levels were highest at the smallest spatial scales although, in the majority of the cases, temporal variability was inversely dependent on sample size. All the species studied, with a few exceptions, presented spatial synchrony independent of spatial scale. The tachinid flies exhibited stronger synchrony dynamics than D. saccharalis and C. flavipes in all spatial scales with the latter displaying the weakest synchrony levels, except when mill spatial scales were compared. In some cases spatial synchrony may at first decay and then increase with distance, but the presence of such patterns can change depending on the spatial scale adopted.     

Women do not synchronize their menstrual cycles

It is widely believed that women who live together or who are close friends synchronize their menstrual cycles. We reexamined this phenomenon in two ways. First, we collected data on menstrual cycles from 186 Chinese women living in dorms for over a year. We found that women living in groups did not synchronize their cycles. Second, we reviewed the first study reporting menstrual synchrony. We found that group synchrony in that study was at the level of chance. We then show that cycle variability produces convergences and subsequent divergences of cycle onsets and may explain perceptions of synchrony. This study was supported by the Sichuan Youth Foundation of Science and Technology (Chuan Ke Ji [2001] 2) and NIH Grant No. 5R01MH065555-02. We thank Shuhuan Yang, Xia Xu, Jun Qu, Jing Zhu, Meijia Yu, & Chang Zhou for all their work in collecting the data. Without them, this study could never have been done. Zheng-Wei Yang is director and professor of the Morphometric Research Laboratory, North Sichuan Medical College, China. His main research interests are in spermatogenesis, morphometry, and stereology. Jeff Schank is associate professor of psychology at the University of California, Davis. His main research interests are in computational and biorobotic modeling of group behavior and the development of sensorimotor behavior in animals.     

Egg-hatching synchrony and larval cannibalism in the dock leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae)

Females of leaf beetles and many other herbivorous insects lay eggs in coherent batches. Hatchlings emerge more or less simultaneously and often prey on their late-hatching clutchmates. It is not certain, however, whether this synchrony of hatching is a mere by-product of cannibalism or whether an additional synchronizing factor exists. The following simple experiment was aimed at determining the causal relationship between cannibalism and simultaneous larval emergence. Egg clutches of the dock leaf beetle Gastrophysa viridula were split into two halves. These halves were either kept as coherent groups in two separate dishes or, alternatively, only one half remained whole, whereas the other one was divided into single eggs, each of which was incubated in a separate dish. Halving of a clutch into coherent groups only slightly disrupted the synchrony of emergence. The consequence of individual isolation was more dramatic. Half-clutches consisting of disconnected solitary eggs required almost twice as much time for complete emergence of all larvae, which was significantly more than cannibalism as a sole synchronizing factor might explain. Moreover, survival rates were the same in coherent half-clutches (in the presence of cannibalism) and among isolated individuals. This group effect and the small contribution of cannibalism suggest the existence of an additional synchronizing factor. Possible mechanisms underpinning this phenomenon are discussed.     

有色环境噪音对空间异质种群动态同步性的影响

随着种群动态和空间结构研究兴趣的增加,激发了大量的有关空间同步性的理论和实验的研究工作。空间种群的同步波动现象在自然界广泛存在,它的影响和原因引起了很多生态学家的兴趣。Moran定理是一个非常重要的解释。但以往的研究大多假设环境变化为空间相关的白噪音。越来越多的研究表明很多环境变化的时间序列具有正的时间自相关性,也就是说用红噪音来描述更加合理。因此,推广经典的Moran效应来处理空间相关红噪音的情形很有必要。利用线性的二阶自回归过程的种群模型,推导了两种群空间同步性与种群动态异质性和环境变化的时间相关性(即环境噪音的颜色)之间的关系。深入分析了种群异质性和噪音颜色对空间同步性的影响。结果表明种群动态异质性不利于空间同步性,但详细的关系比较复杂。而红色噪音的同步能力体现在两方面:一方面,本身的相关性对同步性有贡献;另一方面,环境变化时间相关性可以通过改变种群密度依赖来影响同步性,但对同步性的影响并无一致性的结论,依赖于种群的平均动态等因素。这些结果对理解同步性的机理、利用同步机理来制定物种保护策略和害虫防治都有重要的意义。     

森林害虫发生的空间模式研究进展

森林昆虫种群表现出多样的时空模式,空间同步性是其中最常见的。回顾了森林昆虫空间同步性的特点、形成机制及研究方法方面的进展。森林害虫发生的同步性是广泛存在的,但不同昆虫种类的同步性大小不同。空间同步性常随距离的增大而下降,还与时间尺度有关。Moran效应和扩散是解释空间同步性的两种主要机制,通常Moran效应的影响要比扩散大。从虫害发生数据的获取、同步性的度量及成因3个方面介绍了空间同步性的研究方法方面的进展。利用树轮生态学原理重建森林虫害发生历史的方法可在事后获取可靠的数据,很值得国内研究者借鉴和应用。在空间自相关度量上,空间统计学方法和地统计学方法都是非常有力的手段,但由于不能处理多时间点数据而限制了其在同步性研究中的应用。在同步性成因研究中,利用变异分解将基于距离的Moran特征向量图(dbMEM)作为空间变量研究害虫发生的驱动力是比较新颖的研究方法。     

Density-dependent dispersal complicates spatial synchrony in tri-trophic food chains

Spatial synchrony can increase extinction risk and undermines metapopulation persistence. Both dispersal and biotic interactions can strongly affect spatial synchrony. Here, we explore the spatial synchrony of a tri-trophic food chain in two patches connected by density-dependent dispersal, namely the strategies of prey evasion (PE) and predator pursuit (PP). The dynamics of the food chain are depicted by both the Hastings–Powell model and the chemostat model, with synchrony measured by the Pearson correlation coefficient. We use the density-independent dispersal in the system as a baseline for comparison. Results show that the density-independent dispersal of a species in the system can promote its dynamic synchrony. Dispersal of intermediate species in the tri-trophic food chain is the strongest synchronizer. In contrast, the density-dependent PP and PE of intermediate species can desynchronize the system. Highly synchronized dynamics emerged when the basal species has a strong PE strategy or when the top species has a moderate PP strategy. Our results reveal the complex relationship between density-dependent dispersal and spatial synchrony in tri-trophic systems.     

Are bark beetle outbreaks less synchronous than forest Lepidoptera outbreaks?

Comparisons of intraspecific spatial synchrony across multiple epidemic insect species can be useful for generating hypotheses about major determinants of population patterns at larger scales. The present study compares patterns of spatial synchrony in outbreaks of six epidemic bark beetle species in North America and Europe. Spatial synchrony among populations of the Eurasian spruce bark beetle Ips typographus was significantly higher than for the other bark beetle species. The spatial synchrony observed in epidemic bark beetles was also compared with previously published patterns of synchrony in outbreaks of defoliating forest Lepidoptera, revealing a marked difference between these two major insect groups. The bark beetles exhibited a generally lower degree of spatial synchrony than the Lepidoptera, possibly because bark beetles are synchronized by different weather variables that are acting on a smaller scale than those affecting the Lepidoptera, or because inherent differences in their dynamics leads to more cyclic oscillations and more synchronous spatial dynamics in the Lepidoptera.     

Identifying multispecies synchrony in response to environmental covariates

The importance of multispecies models for understanding complex ecological processes and interactions is beginning to be realized. Recent developments, such as those by Lahoz‐Monfort et al. (2011), have enabled synchrony in demographic parameters across multiple species to be explored. Species in a similar environment would be expected to be subject to similar exogenous factors, although their response to each of these factors may be quite different. The ability to group species together according to how they respond to a particular measured covariate may be of particular interest to ecologists. We fit a multispecies model to two sets of similar species of garden bird monitored under the British Trust for Ornithology's Garden Bird Feeding Survey. Posterior model probabilities were estimated using the reversible jump algorithm to compare posterior support for competing models with different species sharing different subsets of regression coefficients. There was frequently good agreement between species with small asynchronous random‐effect components and those with posterior support for models with shared regression coefficients; however, this was not always the case. When groups of species were less correlated, greater uncertainty was found in whether regression coefficients should be shared or not. The methods outlined in this study can test additional hypotheses about the similarities or synchrony across multiple species that share the same environment. Through the use of posterior model probabilities, estimated using the reversible jump algorithm, we can detect multispecies responses in relation to measured covariates across any combination of species and covariates under consideration. The method can account for synchrony across species in relation to measured covariates, as well as unexplained variation accounted for using random effects. For more flexible, multiparameter distributions, the support for species‐specific parameters can also be measured.     

Breathing synchrony in franciscana (Pontoporia blainvillei) and Guiana dolphins (Sotalia guianensis) in Southern Brazil

Synchronous breathing may be a useful proxy for studying other, and perhaps more complex, aspects of cetacean behavior. Here we describe a study conducted in Babitonga Bay, southern Brazil, where we investigated the synchrony of breathing in two small populations of franciscana (Pontoporia blainvillei) and Guiana dolphins (Sotalia guianensis). The bay is affected by different sources of anthropogenic disturbances, such as boat activity and point‐source pollution. We assumed breathing synchrony to be the inverse of the time between breathing surfacing displays of dolphins within a swimming pair, which we refer to as lag. The relationship between lag and anthropogenic and animal‐related variables was evaluated with generalized additive models. For franciscana dolphins, breathing synchrony was only positively related to the proximity between animals. Breathing synchrony in Guiana dolphins was positively related to both the proximity between animals and to group size, and varied significantly depending on the research boat used. Proximal characteristics (i.e., of individuals or of the group) of these dolphin species seem to be more related to the synchronization in breathing than are the environmental variables assessed here. Results presented expand the current knowledge of these two dolphin species and provide general insights into the breathing synchrony for cetaceans.     

Spatio-temporal dynamics of the grey-sided vole in Hokkaido: identifying coupling using state-based Markov-chain modelling

Explaining synchronization of cyclical or fluctuating populations over geographical regions presents ecologists with novel analytical challenges. We have developed a method to measure synchrony within spatial-temporal datasets of population densities applicable to both periodic and irregularly fluctuating populations. The dynamics of each constituent population is represented by a discrete Markov model. The state of a population trajectory at each time-point is classified as one of 'increase', 'decrease', 'peak' or 'trough'. The set of populations at any time-point is characterized by the frequency distribution of these different states, and the time-evolution of this frequency distribution used to test the hypothesis that the dynamics of each population proceeds independently of the others. The analysis identifies years in which population coupling results in synchronous states and onto which states the system converges, and identifies those years in which synchrony remains high but is accounted for by coupling observed in previous years. It also enables identification of which pairs of sites show the highest levels of coupling. Applying these methods to populations of the grey-sided vole on Hokkaido reveals them to be fluctuating in greater synchrony than would be expected from independent dynamics, and that this level of synchrony is maintained through intermittent coupling acting in ca. 1 year in four or five. High synchrony occurs between sites with similar vegetation and of similar altitude indicating that coupling may be mediated through shared environmental stimuli. When coupling is indicated, convergence is equally likely to occur on a peak state as a trough, indicating that synchronization may be brought about by the response of populations to a combination of different stimuli rather than by the action of any single process.     

Synchronous provisioning increases brood survival in cooperatively breeding pied babblers

1.  Behavioural synchrony typically involves trade-offs. In the context of foraging, for example, synchrony may be suboptimal when individuals have different energy requirements but yield net benefits in terms of increased foraging success or decreased predation risk.
2.  Behavioural synchrony may also be advantageous when individuals collaborate to achieve a common goal, such as raising young. For example, in several bird species, provisioners synchronize nest-feeding visits. However, despite the apparent prevalence of provisioning synchrony, it is not known whether it is adaptive or what its function might be.
3.  Here, we propose a novel explanation for provisioning synchrony: it increases brood survival by decreasing the number of temporally separate nest visits and accordingly the chance that the nest will be detected by predators. Using cooperatively breeding pied babblers, we showed experimentally that provisioners synchronized nest visits by waiting for another provisioner before returning to the nest. Brood survival increased with provisioning synchrony. Provisioners were more likely to synchronize feeding visits for older nestlings as they were louder and possibly more conspicuous to predators. Finally, provisioners in large groups were more likely to wait for other provisioners and synchronized a higher proportion of all visits than those in smaller groups. Thus, provisioning synchrony may be one mechanism by which large groups increase brood survival in this species.
4.  This study highlights a novel strategy that birds use to increase the survival of young and demonstrates the advantages of coordinated behaviour in social species.     

Synchrony of spatial populations: heterogeneous population dynamics and reddened environmental noise

Many species exhibit widespread spatial synchrony in population fluctuations. This pattern is of great ecological interest and can be a source of concern when a species is rare or endangered. Moran’s theorem suggests that if two (or more) populations sharing a common linear density-dependence in the renewal process are disturbed with correlated noise, they will become synchronized with correlation matching the noise correlation. In this report, correlation of nonidentical populations that are described by linear and stationary autoregressive processes is analyzed. We show that the expected spatial synchrony between two populations can be decomposed into two multiplicative components. One is the demographic component related to the values of the autoregressive coefficients and the noise color. The other is the spatial correlation of the environmental colored noise. The main results are consistent with the predictions of previous experiments and simulations, and the importance of this report is to provide theoretical support.     

Outbreaking forest insect drives phase synchrony among sympatric folivores: Exploring potential mechanisms

We explore a common feature of insect population dynamics, interspecific synchrony, which refers to synchrony in population dynamics among sympatric populations of different species. Such synchrony can arise via several possible mechanisms, including shared environmental effects and shared trophic interactions, but distinguishing the relative importance among different mechanisms can be challenging. We analyze interannual time series of population densities of the larch budmoth, Zeiraphera griseana (Lepidoptera: Tortricidae), along with six sympatric larch-feeding folivores from a site in the European Alps 1952–1979. These species include five lepidopterans, Exapate duratella, Ptycholomoides aeriferana, Spilonota laricana, Epirrita autumnata and Teleiodes saltuum, and one hymenopteran sawfly Pristiphora laricis. We document that the highly regular oscillatory behavior (period 9–10 years) of Z. griseana populations is similarly evident in the dynamics of most of the sympatric folivores. We also find that all of the sympatric species are phase synchronized with Z. griseana populations with half of the sympatric species exhibiting nonlagged phase synchrony and three of the species exhibiting 2–5 year lags behind Z. griseana populations. We adapt a previously developed tritrophic model of Z. griseana dynamics to explore possible mechanisms responsible for observed phase synchronization. Results suggest that either shared stochastic influences (e.g., weather) or shared parasitoid impacts are likely causes of nonlagged phase synchronization. The model further indicates that observed patterns of lagged phase synchronization are most likely caused by either shared delayed induced host plant defenses or direct density-dependent effects shared with Z. griseana.