European phenological response to climate change matches the warming pattern

Global climate change impacts can already be tracked in many physical and biological systems; in particular, terrestrial ecosystems provide a consistent picture of observed changes. One of the preferred indicators is phenology, the science of natural recurring events, as their recorded dates provide a high-temporal resolution of ongoing changes. Thus, numerous analyses have demonstrated an earlier onset of spring events for mid and higher latitudes and a lengthening of the growing season. However, published single-site or single-species studies are particularly open to suspicion of being biased towards predominantly reporting climate change-induced impacts. No comprehensive study or meta-analysis has so far examined the possible lack of evidence for changes or shifts at sites where no temperature change is observed. We used an enormous systematic phenological network data set of more than 125 000 observational series of 542 plant and 19 animal species in 21 European countries (1971–2000). Our results showed that 78% of all leafing, flowering and fruiting records advanced (30% significantly) and only 3% were significantly delayed, whereas the signal of leaf colouring/fall is ambiguous. We conclude that previously published results of phenological changes were not biased by reporting or publication predisposition: the average advance of spring/summer was 2.5 days decade⁻¹ in Europe. Our analysis of 254 mean national time series undoubtedly demonstrates that species' phenology is responsive to temperature of the preceding months (mean advance of spring/summer by 2.5 days°C⁻¹, delay of leaf colouring and fall by 1.0 day°C⁻¹). The pattern of observed change in spring efficiently matches measured national warming across 19 European countries (correlation coefficient r =−0.69, P <0.001).     

Phenological changes in intertidal con‐specific gastropods in response to climate warming

There is substantial evidence from terrestrial and freshwater systems of species responding to climate change through changes in their phenology. In the marine environment, however, there is less evidence. Using historic (1946–1949) and contemporary (2003–2007) data, collected from rocky shores of south‐west Britain, we investigated the affect of recent climate warming on the reproductive phenology of two con‐specific intertidal limpet grazers, with cool/boreal and warm/lusitanian centres of distribution. Reproductive development in the southern limpet, Patella depressa, has advanced, on average, 10.2 days per decade since the 1940s, with a longer reproductive season and more of the population reproductively active. The peak in the proportion of the population in advanced stages of gonad development was positively correlated with sea surface temperature (SST) in late spring/early summer, which has increased between the 1940s and 2000s. The advance in peak reproductive development of this species is double the average observed for terrestrial and freshwater systems and indicates, along with other studies, that marine species may be responding faster to climate warming. In contrast, the northern limpet, Patella vulgata, has experienced a delay in the timing of its reproductive development (on average 3.3 days per decade), as well as an increase in reproductive failure years and a reduction in the proportion of the population reaching advanced gonad stages. These results are the first to demonstrate a delay in the reproductive development of a cool‐temperate, winter spawner, towards cooler more favourable environmental conditions in response to climate warming. Such a delay in spawning will potentially lead to trophic miss‐matches, resulting in a rapid nonlinear decline of this species.     

Bayesian analysis of climate change impacts in phenology

The identification of changes in observational data relating to the climate change hypothesis remains a topic of paramount importance. In particular, scientifically sound and rigorous methods for detecting changes are urgently needed. In this paper, we develop a Bayesian approach to nonparametric function estimation. The method is applied to blossom time series of Prunus avium L., Galanthus nivalis L. and Tilia platyphyllos SCOP. The functional behavior of these series is represented by three different models: the constant model, the linear model and the one change point model. The one change point model turns out to be the preferred one in all three data sets with considerable discrimination of the other alternatives. In addition to the functional behavior, rates of change in terms of days per year were also calculated. We obtain also uncertainty margins for both function estimates and rates of change. Our results provide a quantitative representation of what was previously inferred from the same data by less involved methods.     

Methane and nitrous oxide emissions under no‐till farming in China: a meta‐analysis

No‐till (NT) practices are among promising options toward adaptation and mitigation of climate change. However, the mitigation effectiveness of NT depends not only on its carbon sequestration potential but also on soil‐derived CH₄ and N₂O emissions. A meta‐analysis was conducted, using a dataset involving 136 comparisons from 39 studies in China, to identify site‐specific factors which influence CH₄ emission, CH₄ uptake, and N₂O emission under NT. Comparative treatments involved NT without residue retention (NT0), NT with residue retention (NTR), compared to plow tillage (PT) with residue removed (PT0). Overall, NT0 significantly decreased CH₄ emission by ~30% (P < 0.05) compared to PT0 with an average emission 218.8 kg ha⁻¹ for rice paddies. However, the increase in N₂O emission could partly offset the benefits of the decrease in CH₄ emission under NT compared to PT0. NTR significantly enhanced N₂O emission by 82.1%, 25.5%, and 20.8% (P < 0.05) compared to PT0 for rice paddies, acid soils, and the first 5 years of the experiments, respectively. The results from categorical meta‐analysis indicated that the higher N₂O emission could be mitigated by adopting NT within alkaline soils, for long‐term duration, and with less N fertilization input when compared to PT0. In addition, the natural log (lnR) of response ratio of CH₄ and N₂O emissions under NT correlated positively (enhancing emission) with climate factors (temperature and precipitation) and negatively (reducing emission) with experimental duration, suggesting that avoiding excess soil wetness and using NT for a long term could enhance the benefits of NT. Therefore, a thorough understanding of the conditions favoring greenhouse gas(es) reductions is essential to achieving climate change mitigation and advancing food security in China.     

Interactions between climate and habitat loss effects on biodiversity: a systematic review and meta‐analysis

Climate change and habitat loss are both key threatening processes driving the global loss in biodiversity. Yet little is known about their synergistic effects on biological populations due to the complexity underlying both processes. If the combined effects of habitat loss and climate change are greater than the effects of each threat individually, current conservation management strategies may be inefficient and at worst ineffective. Therefore, there is a pressing need to identify whether interacting effects between climate change and habitat loss exist and, if so, quantify the magnitude of their impact. In this article, we present a meta‐analysis of studies that quantify the effect of habitat loss on biological populations and examine whether the magnitude of these effects depends on current climatic conditions and historical rates of climate change. We examined 1319 papers on habitat loss and fragmentation, identified from the past 20 years, representing a range of taxa, landscapes, land‐uses, geographic locations and climatic conditions. We find that current climate and climate change are important factors determining the negative effects of habitat loss on species density and/or diversity. The most important determinant of habitat loss and fragmentation effects, averaged across species and geographic regions, was current maximum temperature, with mean precipitation change over the last 100 years of secondary importance. Habitat loss and fragmentation effects were greatest in areas with high maximum temperatures. Conversely, they were lowest in areas where average rainfall has increased over time. To our knowledge, this is the first study to conduct a global terrestrial analysis of existing data to quantify and test for interacting effects between current climate, climatic change and habitat loss on biological populations. Understanding the synergistic effects between climate change and other threatening processes has critical implications for our ability to support and incorporate climate change adaptation measures into policy development and management response.     

Soil carbon stock change following afforestation in Northern Europe: a meta‐analysis

Northern Europe supports large soil organic carbon (SOC) pools and has been subjected to high frequency of land‐use changes during the past decades. However, this region has not been well represented in previous large‐scale syntheses of land‐use change effects on SOC, especially regarding effects of afforestation. Therefore, we conducted a meta‐analysis of SOC stock change following afforestation in Northern Europe. Response ratios were calculated for forest floors and mineral soils (0–10 cm and 0–20/30 cm layers) based on paired control (former land use) and afforested plots. We analyzed the influence of forest age, former land‐use, forest type, and soil textural class. Three major improvements were incorporated in the meta‐analysis: analysis of major interaction groups, evaluation of the influence of nonindependence between samples according to study design, and mass correction. Former land use was a major factor contributing to changes in SOC after afforestation. In former croplands, SOC change differed between soil layers and was significantly positive (20%) in the 0–10 cm layer. Afforestation of former grasslands had a small negative (nonsignificant) effect indicating limited SOC change following this land‐use change within the region. Forest floors enhanced the positive effects of afforestation on SOC, especially with conifers. Meta‐estimates calculated for the periods <30 years and >30 years since afforestation revealed a shift from initial loss to later gain of SOC. The interaction group analysis indicated that meta‐estimates in former land‐use, forest type, and soil textural class alone were either offset or enhanced when confounding effects among variable classes were considered. Furthermore, effect sizes were slightly overestimated if sample dependence was not accounted for and if no mass correction was performed. We conclude that significant SOC sequestration in Northern Europe occurs after afforestation of croplands and not grasslands, and changes are small within a 30‐year perspective.     

Changes in satellite‐derived spring vegetation green‐up date and its linkage to climate in China from 1982 to 2010: a multimethod analysis

The change in spring phenology is recognized to exert a major influence on carbon balance dynamics in temperate ecosystems. Over the past several decades, several studies focused on shifts in spring phenology; however, large uncertainties still exist, and one understudied source could be the method implemented in retrieving satellite‐derived spring phenology. To account for this potential uncertainty, we conducted a multimethod investigation to quantify changes in vegetation green‐up date from 1982 to 2010 over temperate China, and to characterize climatic controls on spring phenology. Over temperate China, the five methods estimated that the vegetation green‐up onset date advanced, on average, at a rate of 1.3 ± 0.6 days per decade (ranging from 0.4 to 1.9 days per decade) over the last 29 years. Moreover, the sign of the trends in vegetation green‐up date derived from the five methods were broadly consistent spatially and for different vegetation types, but with large differences in the magnitude of the trend. The large intermethod variance was notably observed in arid and semiarid vegetation types. Our results also showed that change in vegetation green‐up date is more closely correlated with temperature than with precipitation. However, the temperature sensitivity of spring vegetation green‐up date became higher as precipitation increased, implying that precipitation is an important regulator of the response of vegetation spring phenology to change in temperature. This intricate linkage between spring phenology and precipitation must be taken into account in current phenological models which are mostly driven by temperature.     

东北地区植被物候对气候变化的响应

使用1982—2003年GIMMS-NDVI数据和气候数据,借助GIS空间分析和统计分析方法,分析了东北地区不同植被物候期与气候变化的关系。结果表明:22年东北地区年均温度以升高趋势为主,年降水量以减少趋势为主;针叶林、针阔叶混交林、阔叶林、草甸和沼泽植被生长季开始日期提前受春季温度升高影响显著(P<0.05)。春季降水对植被生长季开始日期变化影响较小,仅对针叶林生长季开始日期的推迟有显著的影响(P<0.05)。植被生长季结束日期受温度变化影响较小,仅草原植被生长季结束日期提前受秋季温度降低影响显著(P<0.05)。降水对东北地区植被生长季结束日期的变化影响高于温度。随着秋季降水量的减少,针阔叶混交林、草原和农田植被生长季结束日提前(P<0.05)。草丛生长季结束日期提前受夏季降水减少的影响显著(P<0.05);农田生长季结束日期提前亦受夏季和9月降水量减少的显著影响(P<0.05)。阔叶林和沼泽植被生长季延长受春季温度升高影响显著(P<0.05);灌丛植被生长季缩短受春季降水量减少影响显著(P<0.05);草丛和农田植被生长季延长受夏季降水量增加影响显著(P<0.05)。     

Effects of climate warming on carbon fluxes in grasslands— A global meta‐analysis

Climate warming will affect terrestrial ecosystems in many ways, and warming‐induced changes in terrestrial carbon (C) cycling could accelerate or slow future warming. So far, warming experiments have shown a wide range of C flux responses, across and within biome types. However, past meta‐analyses of C flux responses have lacked sufficient sample size to discern relative responses for a given biome type. For instance grasslands contribute greatly to global terrestrial C fluxes, and to date grassland warming experiments provide the opportunity to evaluate concurrent responses of both plant and soil C fluxes. Here, we compiled data from 70 sites (in total 622 observations) to evaluate the response of C fluxes to experimental warming across three grassland types (cold, temperate, and semi‐arid), warming methods, and short (≤3 years) and longer‐term (>3 years) experiment lengths. Overall, our meta‐analysis revealed that experimental warming stimulated C fluxes in grassland ecosystems with regard to both plant production (e.g., net primary productivity (NPP) 15.4%; aboveground NPP (ANPP) by 7.6%, belowground NPP (BNPP) by 11.6%) and soil respiration (Rs) (9.5%). However, the magnitude of C flux stimulation varied significantly across cold, temperate and semi‐arid grasslands, in that responses for most C fluxes were larger in cold than temperate or semi‐arid ecosystems. In semi‐arid and temperate grasslands, ecosystem respiration (Reco) was more sensitive to warming than gross primary productivity (GPP), while the opposite was observed for cold grasslands, where warming produced a net increase in whole‐ecosystem C storage. However, the stimulatory effect of warming on ANPP and Rs observed in short‐term studies (≤3 years) in both cold and temperate grasslands disappeared in longer‐term experiments (>3 years). These results highlight the importance of conducting long‐term warming experiments, and in examining responses across a wide range of climate.     

Monitoring biogeographical response to climate change: The potential role of aeropalynology

To test models predicting biological reponse to future climate change, it is essential to find climatically-sensitive, easily monitored biological indicators that respond to climate change. Routine monitoring of airborne pollen, now undertaken on a near-global basis, could be adapted for this purpose. Analysis of spatial and seasonal variations in pollen levels in New Zealand suggests that the timing of onset and peak abundance of certain pollen taxa should be explored as possible bio-indicators of climate change. The onset of the airborne grass pollen season during the summer of 1988/89 varied consistently with latitude, and hence temperature, with the season in Southland commencing 8--9 days after Northland. However, these patterns were only apparent after sampling sites were separated into two groups reflecting predominantly urban or rural pollen sources. A less consistent north to south trend was apparent in the frequency of high (30 grains/m³) grass pollen levels, with high levels frequent in North Island localities in November, December and January and in southern localities during December and January. The successive onset of pollen seasons for the principal tree species during the spring-to-early summer warming interval may also be a useful bio-indicator of climate change. As well as assisting forecasts of the onset of the pollinosis season, these biogeographical patterns, reflecting climatic variation with latitude, suggest that routine aeropalynological monitoring might provide early signals of vegetation response to climate change. These conclusions are supported by recent investigations of long-term aeropalynological datasets in Europe that indicate earlier onset of pollen seasons in response to recent global warming.     

Phylogenetic conservatism and trait correlates of spring phenological responses to climate change in northeast China

Climate change has resulted in major changes in plant phenology across the globe that includes leaf‐out date and flowering time. The ability of species to respond to climate change, in part, depends on their response to climate as a phenological cue in general. Species that are not phenologically responsive may suffer in the face of continued climate change. Comparative studies of phenology have found phylogeny to be a reliable predictor of mean leaf‐out date and flowering time at both the local and global scales. This is less true for flowering time response (i.e., the correlation between phenological timing and climate factors), while no study to date has explored whether the response of leaf‐out date to climate factors exhibits phylogenetic signal. We used a 52‐year observational phenological dataset for 52 woody species from the Forest Botanical Garden of Heilongjiang Province, China, to test phylogenetic signal in leaf‐out date and flowering time, as well as, the response of these two phenological traits to both temperature and winter precipitation. Leaf‐out date and flowering time were significantly responsive to temperature for most species, advancing, on average, 3.11 and 2.87 day/°C, respectively. Both leaf‐out and flowering, and their responses to temperature exhibited significant phylogenetic signals. The response of leaf‐out date to precipitation exhibited no phylogenetic signal, while flowering time response to precipitation did. Native species tended to have a weaker flowering response to temperature than non‐native species. Earlier leaf‐out species tended to have a greater response to winter precipitation. This study is the first to assess phylogenetic signal of leaf‐out response to climate change, which suggests, that climate change has the potential to shape the plant communities, not only through flowering sensitivity, but also through leaf‐out sensitivity.     

Phenological plasticity will not help all species adapt to climate change

Concerns are rising about the capacity of species to adapt quickly enough to climate change. In long‐lived organisms such as trees, genetic adaptation is slow, and how much phenotypic plasticity can help them cope with climate change remains largely unknown. Here, we assess whether, where and when phenological plasticity is and will be adaptive in three major European tree species. We use a process‐based species distribution model, parameterized with extensive ecological data, and manipulate plasticity to suppress phenological variations due to interannual, geographical and trend climate variability, under current and projected climatic conditions. We show that phenological plasticity is not always adaptive and mostly affects fitness at the margins of the species' distribution and climatic niche. Under current climatic conditions, phenological plasticity constrains the northern range limit of oak and beech and the southern range limit of pine. Under future climatic conditions, phenological plasticity becomes strongly adaptive towards the trailing edges of beech and oak, but severely constrains the range and niche of pine. Our results call for caution when interpreting geographical variation in trait means as adaptive, and strongly point towards species distribution models explicitly taking phenotypic plasticity into account when forecasting species distribution under climate change scenarios.     

Sensitivity of coral calcification to ocean acidification: a meta‐analysis

To date, meta‐analyses of effects of acidification have focused on the overall strength of evidence for statistically significant responses; however, to anticipate likely consequences of ocean acidification, quantitative estimates of the magnitude of likely responses are also needed. Herein, we use random effects meta‐analysis to produce a systematically integrated measure of the distribution of magnitudes of the response of coral calcification to decreasing Ω_Arag. We also tested whether methodological and biological factors that have been hypothesized to drive variation in response magnitude explain a significant proportion of the among‐study variation. We found that the overall mean response of coral calcification is ~15% per unit decrease in Ω_Arag over the range 2 < Ω_Arag < 4. Among‐study variation is large (standard deviation of 8% per unit decrease in Ω_Arag). Neither differences in carbonate chemistry manipulation method, study duration, irradiance level, nor study species growth rate explained a significant proportion of the among‐study variation. However, studies employing buoyant weighting found significantly smaller decreases in calcification per unit Ω_Arag (~10%), compared with studies using the alkalinity anomaly technique (~25%). These differences may be due to the greater tendency for the former to integrate over light and dark calcification. If the existing body of experimental work is indeed representative of likely responses of corals in nature, our results imply that, under business as usual conditions, declines in coral calcification by end‐of‐century will be ~22%, on average, or ~15% if only studies integrating light and dark calcification are considered. These values are near the low end of published projections, but support the emerging view that variability due to local environmental conditions and species composition is likely to be substantial.     

羊草物候特征对气候因子的响应

研究了内蒙古高原典型草原优势植物羊草的物候特征及其对气候因子的响应,结果表明,3～4月的平均温度与羊草的展叶显著相关,温度每升高1℃,羊草展叶提前4．35d;日照时数与羊草枯黄期显著相关,随着日照时数增加,羊草展叶期推后,枯黄期提前;4～10月平均风速与羊草生长季长相关,平均风速越大,生长期越长。     

Responses of soil carbon sequestration to climate‐smart agriculture practices: A meta‐analysis

Climate‐smart agriculture (CSA) management practices (e.g., conservation tillage, cover crops, and biochar applications) have been widely adopted to enhance soil organic carbon (SOC) sequestration and to reduce greenhouse gas emissions while ensuring crop productivity. However, current measurements regarding the influences of CSA management practices on SOC sequestration diverge widely, making it difficult to derive conclusions about individual and combined CSA management effects and bringing large uncertainties in quantifying the potential of the agricultural sector to mitigate climate change. We conducted a meta‐analysis of 3,049 paired measurements from 417 peer‐reviewed articles to examine the effects of three common CSA management practices on SOC sequestration as well as the environmental controlling factors. We found that, on average, biochar applications represented the most effective approach for increasing SOC content (39%), followed by cover crops (6%) and conservation tillage (5%). Further analysis suggested that the effects of CSA management practices were more pronounced in areas with relatively warmer climates or lower nitrogen fertilizer inputs. Our meta‐analysis demonstrated that, through adopting CSA practices, cropland could be an improved carbon sink. We also highlight the importance of considering local environmental factors (e.g., climate and soil conditions and their combination with other management practices) in identifying appropriate CSA practices for mitigating greenhouse gas emissions while ensuring crop productivity.     

Contemporary climate change in the Sonoran Desert favors cold‐adapted species

Impacts of long‐term climate shifts on the dynamics of intact communities within species ranges are not well understood. Here, we show that warming and drying of the Southwestern United States over the last 25 years has corresponded to a shift in the species composition of Sonoran Desert winter annuals, paradoxically favoring species that germinate and grow best in cold temperatures. Winter rains have been arriving later in the season, during December rather than October, leading to the unexpected result that plants are germinating under colder temperatures, shifting community composition to favor slow growing, water‐use efficient, cold‐adapted species. Our results demonstrate how detailed ecophysiological knowledge of individual species, combined with long‐term demographic data, can reveal complex and sometimes unexpected shifts in community composition in response to climate change. Further, these results highlight the potentially overwhelming impact of changes in phenology on the response of biota to a changing climate.     

Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology

The timing of the end of the vegetation growing season (EOS) plays a key role in terrestrial ecosystem carbon and nutrient cycles. Autumn phenology is, however, still poorly understood, and previous studies generally focused on few species or were very limited in scale. In this study, we applied four methods to extract EOS dates from NDVI records between 1982 and 2011 for the Northern Hemisphere, and determined the temporal correlations between EOS and environmental factors (i.e., temperature, precipitation and insolation), as well as the correlation between spring and autumn phenology, using partial correlation analyses. Overall, we observed a trend toward later EOS in ~70% of the pixels in Northern Hemisphere, with a mean rate of 0.18 ± 0.38 days yr^?1. Warming preseason temperature was positively associated with the rate of EOS in most of our study area, except for arid/semi‐arid regions, where the precipitation sum played a dominant positive role. Interestingly, increased preseason insolation sum might also lead to a later date of EOS. In addition to the climatic effects on EOS, we found an influence of spring vegetation green‐up dates on EOS, albeit biome dependent. Our study, therefore, suggests that both environmental factors and spring phenology should be included in the modeling of EOS to improve the predictions of autumn phenology as well as our understanding of the global carbon and nutrient balances.     

Detecting nonlinear response of spring phenology to climate change by Bayesian analysis

The impact of climate change on the advancement of plant phenological events has been heavily studied in the last decade. Although the majority of spring plant phenological events have been trending earlier, this is not universally true. Recent work has suggested that species that are not advancing in their spring phenological behavior are responding more to lack of winter chill than increased spring heat. One way to test this hypothesis is by evaluating the behavior of a species known to have a moderate to high chilling requirement and examining how it is responding to increased warming. This study used a 60‐year data set for timing of leaf‐out and male flowering of walnut (Juglans regia) cultivar ‘Payne’ to examine this issue. The spring phenological behavior of ‘Payne’ walnut differed depending on bud type. The vegetative buds, which have a higher chilling requirement, trended toward earlier leaf‐out until about 1994, when they shifted to later leaf‐out. The date of male bud pollen shedding advanced over the course of the whole record. Our findings suggest that many species which have exhibited earlier bud break are responding to warmer spring temperatures, but may shift into responding more to winter temperatures (lack of adequate chilling) as warming continues.     

Keeping up with a warming world; assessing the rate of adaptation to climate change

The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity.The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions.Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.     

A population‐averaged approach to diagnostic test meta‐analysis

The meta‐analysis of diagnostic accuracy studies is often of interest in screening programs for many diseases. The typical summary statistics for studies chosen for a diagnostic accuracy meta‐analysis are often two dimensional: sensitivities and specificities. The common statistical analysis approach for the meta‐analysis of diagnostic studies is based on the bivariate generalized linear‐mixed model (BGLMM), which has study‐specific interpretations. In this article, we present a population‐averaged (PA) model using generalized estimating equations (GEE) for making inference on mean specificity and sensitivity of a diagnostic test in the population represented by the meta‐analytic studies. We also derive the marginalized counterparts of the regression parameters from the BGLMM. We illustrate the proposed PA approach through two dataset examples and compare performance of estimators of the marginal regression parameters from the PA model with those of the marginalized regression parameters from the BGLMM through Monte Carlo simulation studies. Overall, both marginalized BGLMM and GEE with sandwich standard errors maintained nominal 95% confidence interval coverage levels for mean specificity and mean sensitivity in meta‐analysis of 25 of more studies even under misspecification of the covariance structure of the bivariate positive test counts for diseased and nondiseased subjects.