Ecological and genetic measurements of dispersal in a threatened dragonfly

Leucorrhinia caudalis is a rare dragonfly, threatened throughout its European distribution. The species was formerly widespread in the Swiss lowlands, but only a single population remained in the 1980s. However, a spread has recently been observed, with additional ponds being colonised, sometimes at considerable distance. Despite this evidence of recent long-distance dispersal, it is unknown whether L. caudalis regularly moves among ponds or whether this is a rather rare event. A combination of an ecological mark-resight and a population genetic study was applied to investigate contemporary dispersal and the genetic footprint of the recent population history of L. caudalis in Switzerland. DNA for genetic microsatellite analysis was extracted from exuviae. The mark-resight study and the genetic analysis gave congruent results. They showed that L. caudalis is mostly a sedentary species, with only a few contemporary dispersal events over distances up to 5 km being observed. The genetic analysis was in agreement with the recent population history of the Swiss populations. The oldest and largest population showed large genetic diversity and acted as source population for the recent spread of L. caudalis in Switzerland. Recurrent gene flow among this source population and close populations caused substantial local genetic variation in the latter, as well as low population differentiation. The two recently founded distant populations (?30 km distance) were genetically less diverse and highly differentiated. These distant populations and another recently colonised population also expressed signatures of genetic bottlenecks.     

Dynamics of a declining amphibian metapopulation: Survival, dispersal and the impact of climate

Climate can interact with population dynamics in complex ways. In this study we describe how climatic factors influenced the dynamics of an amphibian metapopulation over 12 years through interactions with survival, recruitment and dispersal. Low annual survival of great crested newts (Triturus cristatus) was related to mild winters and heavy rainfall, which impacted the metapopulation at the regional level. Consequently, survival varied between years but not between subpopulations. Despite this regional effect, the four subpopulations were largely asynchronous in their dynamics. Three out of the four subpopulations suffered reproductive failure in most years, and recruitment to the metapopulation relied on one source. Variation in recruitment and juvenile dispersal was therefore probably driving asynchrony in population dynamics. At least one subpopulation went extinct over the 12 year period. These trends are consistent with simulations of the system, which predicted that two subpopulations had an extinction risk of >50% if adult survival fell below 30% in combination with low juvenile survival. Intermittent recruitment may therefore only result in population persistence if compensated for by relatively high adult survival. Mild winters may consequently reduce the viability of amphibian metapopulations. In the face of climate change, conservation actions may be needed at the local scale to compensate for reduced adult survival. These would need to include management to enhance recruitment, connectivity and dispersal.     

Insular pest control within a metapopulation context

Introduced pests threaten many species and their control is generally beneficial for conservation, particularly on islands where complete eradication is possible. Unfortunately on ‘nearshore’ islands neighbouring source populations exist and unaided reinvasion is likely. Pest control programmes at these sites thus require a metapopulation context to adequately manage movements between source and sink populations. We investigated the ecology of introduced ship rats (Rattus rattus) on a nearshore island, and gene flow with adjacent mainland populations, in order to understand the metapopulation dynamics and relative levels of pest control required within the landscape. We sampled the entire population by trapping (n = 30), achieving eradication, and found a low rat density (3.2 ha⁻¹) indicative of a sink population. Seed and other plant material constituted the major dietary component of rats. Despite its proximity to mainland source populations, the island population was genetically distinct with reduced allelic diversity caused by a recent reinvasion founder effect. Genetic analyses also detected recent migrants between the populations. In contrast, two mainland populations separated by a similar distance displayed complete genetic mixing. The small water gap therefore provides a sufficient barrier to lower the migration rate to the island and delay reinvasion, which nonetheless eventually happens. In order to maintain nearshore islands pest-free, conservation management will require a metapopulation approach simultaneously focusing on both island and source population pest control.     

Sex-specific roost movements and population dynamics of the vulnerable long-fingered bat, Myotis capaccinii

The roosts of many IUCN-listed cave-roosting bat species are under threat from tourist development in SE Europe and other regions of the world. Much-needed conservation strategies require, among other information, an understanding of their roost movements and population dynamics, which can now be obtained relatively quickly using advanced models. We have studied the long-fingered bat, Myotis capaccinii, an obligate cave-dweller, in Dadia National Park, Greece. The species formed colonies of up to a few thousand individuals and was highly mobile, frequently switching summer roosts up to 39 km apart, even during late pregnancy. The bats migrated to distant hibernacula including a cave in Bulgaria 140 km NW of the Park. Adult recapture probabilities varied with season and sex: low female recapture rates in autumn, relative to spring and summer, indicated non-random temporary emigration following nursery colony dispersal. The opposite pattern was seen in males: increasing recapture rates in the autumn suggest that males gather in these roosts to mate with females in transit. Adult survival (0.86-0.94) was similar in females and males, similar in winter and summer, and comparable to recent estimates for other bats based on similar modelling techniques. Sex-based differences in juvenile recapture suggest female philopatry and male-biased dispersal. Our work shows that protection of M. capaccinii roosts must extend beyond the Park’s and indeed the country’s boundaries: its conservation requires large-scale, trans-national integrated conservation plans. Our results will apply to many other warm-temperate species with similar life history cycles.     

A range-wide model of landscape connectivity and conservation for the jaguar, Panthera onca

Large, wide-ranging carnivores face greater threats and more persistent declines than most other mammal species. An important conservation tool for these carnivores has been range-wide priority-setting exercises that have helped identify critical threats and key populations. However, such exercises often fail to identify functional movement corridors or account for genetic connectivity. We present a new model for jaguar (Panthera onca) conservation that uses a geographic information system (GIS) and expert input to create a dispersal cost surface and identify least-cost corridors connecting the 90 known populations across the jaguar’s range. Results indicate 78% of historic jaguar range, an area of approximately 14.9 million km², still holds potential for jaguar movement and dispersal. We identified 182 potential corridors between populations, ranging from 3 to 1607 km in length; 44 of these corridors are characterized as being of immediate concern due to their limited width, and thus their high potential for being severed. Resultant maps, displaying priority populations and corridors, are used to direct field-based research and conservation efforts. Field assessment and refinement of the corridors is ongoing. This is the first attempt to create and implement such a holistic model of range-wide conservation for a large carnivore species.     

Monitoring rare or elusive large mammals using effort-corrected voluntary observers

Populations of rare or elusive large mammals are difficult to monitor, because they usually are secretive, solitary, occur at low densities, and have large home ranges. The global trend of generally decreasing large carnivore populations necessitates new, feasible, reliable, and cost-effective monitoring methods. We evaluate an index method developed for monitoring populations of moose (Alces alces) based on voluntarily and systematically collected observations from hunters, corrected for effort, for use in monitoring populations of large carnivores in Sweden. For our evaluation, we used independent estimates of minimum brown bear (Ursus arctos) densities from DNA-based scat surveys and brown bear distribution from mandatory reports from successful bear hunters. We verified that the index correctly reflected bear distribution. We also found strong linear relationships between the indices and the independent density estimates for bears at the scale of local management units (about 1000-2000 km²) in all three regional study areas (adjusted R² = 0.88-0.60). Our results suggest that systematic, effort-corrected reports of observed animals can be an alternative and accurate monitoring method for the conservation and management of large mammals occurring over large areas when large numbers of willing volunteers are available (effort >30,000 h).     

Female biased mortality caused by anthropogenic nest loss contributes to population decline and adult sex ratio of a meadow bird

Meadow breeding birds such as the whinchat Saxicola rubetra have been declining due to increased farming intensity. In modern grassland management, the first mowing and the bird’s breeding cycle coincide, causing high nest destruction rates and low productivity of grassland bird populations. However, it is virtually unknown whether the mowing process directly affects adult survival by accidentally killing incubating females. We studied adult survival of an Alpine whinchat population during two breeding seasons using either colour-ringing or radio-tracking of 71 adults. Assessing territories, mowing phenology and nest destruction from 1988 to 2007 allowed changes in the factors associated with female mowing mortality to be estimated. Adult survival over 5-day-periods was Φ = 0.986, but during the period of mowing female survival was strongly reduced (Φ = 0.946). As a result, 80.6% of the males, but only 68.4% of the females survived the breeding season. Mowing undoubtedly killed two of 20 radio-tagged females when they were laying or incubating. In the 20-year period, an increasing proportion of nests were destroyed before the chicks hatched and this change was associated with an increased distortion of the adult sex ratio. Modelling the population growth rate showed that including the additional effect of mowing on female mortality resulted in a 1.7 times faster local population decline. These results are consistent with the hypothesis that the extinction of whinchat populations in the lowlands of central Europe was caused not only by habitat degradation and low productivity, but also by increased man-made female mortality.     

Life on the edge - High levels of genetic diversity in a cliff population of Bertya ingramii are attributed to B. rosmarinifolia (Euphorbiaceae)

Wind-facilitated migration of new genotypes into small, geographically disjunct populations should buffer them against local extinction. Bertya ingramii, a monoecious, wind-pollinated shrub, is restricted to three populations in a 4 km² area in eastern Australia. Populations are separated by deeply dissected gorges where it is unlikely that seeds are exchanged but where wind movement may facilitate pollen dispersal. Using 156 highly polymorphic ISSR markers, we found moderate genetic variation within and among populations of B. ingramii and less genetic diversity in a nearby and small population of the widespread Bertya rosmarinifolia. The smallest population of B. ingramii (<30 plants) had the highest genetic variation (65% polymorphic markers, Shannon Information Index = 0.30). AMOVA and a Bayesian analysis showed that molecular variance was equally distributed within and among populations suggesting that gene flow is as limited within as in among populations. Genetic distances between populations were only weakly explained by their relative geographic distances (mantel test, R² = 0.21, P = 0.001) but the distribution of private bands, the departure from Hardy-Weinberg equilibrium, and a UPGMA tree showed that the smallest population of B. ingramii was generally more similar to an upstream population of B. rosmarinifolia. Thirty-eight percent of bands in this small population of B. ingramii were exclusively shared with B. rosmarinifolia. This covert hybridisation may have been an ancient event but may be responsible for contemporary declines in germination and establishment in B. ingramii. The conservation implications are amplified by the endangered status of B. ingramii.     

Reproduction and pre-dispersal survival of Iberian lynx in a subpopulation of the Doñana National Park

Little is known about the reproduction of the Iberian lynx (Lynx pardinus) even though it is the most endangered felid in the world. We studied during 9 years several reproductive parameters of the Iberian lynx in one of the subpopulations situated in Doñana National Park (south-western Spain), by means of radio-tracking, direct observations and photo-trapping. The potential breeding subpopulation was usually composed of 3 adult females, which bred 83% of the total possible 29 female-reproductive year. The minimum total number of cubs born during the study was 64 (7.7 ± 0.69 per year). There was no correlation between the number of cubs born or number of breeding females and population size of European rabbit (Oryctolagus cuniculus, the main prey of the lynx). All known births (n = 16) occurred in March except one in April and another in June. Mean litter size was 3.0 ± 0.16 (n = 16, range = 2-4). Sex-ratio (n = 59 cubs) was 1.03:1.00 (females:males). Nevertheless, the commonest picture was a female with 2 cubs older than 3 months. Altogether, at age of 3 months, 75% of cubs survived. Number of lynx alive at 10 months old and before dispersing was 69% and 57%, respectively. Sex did not affect survival for any age. Normally, it was not possible to know the causes of the death of cubs younger than 3 months. Survival at this age was not related with mother, mother age, or rabbit abundance. All females that bred were older than 3 years. The age of last reproduction was 9 years. For 3 females that were tracked during almost their complete reproductive life, the life time reproductive output was between 11 and 19 cubs. Iberian lynx reproductive parameters did not respond to wide changes in prey abundance during the study. Conservation plans considering the extraction of cubs with a low survival probability should be considered by managers, for instance, in translocation campaigns.     

Autumn swarming behaviour of Natterer’s bats in the UK: Population size, catchment area and dispersal

Many species of temperate bats visit underground sites in autumn, prior to hibernation, and chase each other in and around the entrances in an event known as autumn swarming. It has been suggested that swarming is a mating event that facilitates gene flow between bats from otherwise isolated summer colonies. We describe swarming behaviour at a cluster of four caves in the North of England and provide direct evidence for seasonal migration of Natterer’s bats (Myotis nattereri ) between these caves and many summer nursery roosts in a catchment area of at least 60 km radius. Mark-recapture analysis suggests that an estimated 2000-6000 Natterer’s bats use the three best-studied caves, together with smaller numbers of four other species: M. daubentonii, M. brandtii, M. mystacinus and Plecotus auritus. Recaptures also show that there is a small interchange of bats between these three caves, which are 0.6-1.5 km apart. Capture rates, automatic logging and video recordings at one cave suggest that an average 310-400 bats visit the cave each night. Mating at swarming sites would be particularly important for gene flow if a species showed no other dispersal pattern. We provide evidence for natal philopatry, with little or no dispersal, in both sexes of Natterer’s bats. The protection of swarming sites is discussed in light of our findings.     

Metapopulation dynamics and conservation of the marsh fritillary butterfly: Population viability analysis and management options for a critically endangered species in Western Europe

This study investigates the dynamics and viability of a marsh fritillary butterfly Euphydryas aurinia metapopulation in a Belgian successional landscape. Based on capture-mark-recapture and winter nest census data, we first estimated demography (survival and recruitment rates, population size, density dependence) and dispersal parameters (emigration rate, effect of patch connectivity on dispersal, mortality during dispersal). Then using RAMAS/GIS platform, we parameterised a population viability analysis (PVA) model with these parameters to simulate the future of this metapopulation under different scenarios.The metapopulation does not seem viable even if natural reforestation is controlled by adequate management. In its present state, the patch system is not able to sustain enough individuals: due to the large temporal fluctuations in demographic parameters, a carrying capacity far higher than currently would be necessary to limit extinction risk to 1%, suggesting the existence of an extinction debt for the species in Belgium. The situation of E. aurinia appears much worse compared to two other fritillary species threatened in Belgium, for which similar PVA are available. It is therefore urgent to increase the carrying capacity of the patch system. How and where it is achieved are of secondary importance for the gain in viability: improvement of habitat quality through restoration, or increase of habitat quantity via enlargement of existing patches and/or creation of new habitat in the matrix. A regime of management based on regular re-opening and maintenance of habitat patches may be the only guarantee of long-term persistence for this critically endangered species in Belgium.     

Aerial surveying of the world’s largest leatherback turtle rookery: A more effective methodology for large-scale monitoring

For many marine megavertebrate species it is challenging to derive population estimates and knowledge on habitat use needed to inform conservation planning. For marine turtles, the logistics required to undertake comprehensive ground-based censuses, across wide spatial and temporal scales, are often insurmountable. This frequently leads to an approach where a limited number of index nesting beaches are monitored in great detail by foot. In this study we use nationwide aerial surveying interfaced with ground assessments across three seasons of leatherback turtle nesting in Gabon (Equatorial West Africa), highlighting the importance of a synoptic approach to marine turtle monitoring. These surveys allow the first complete population assessment of this nesting aggregation to be made, identifying it as the world’s largest for the species (36,185-126,480 clutches, approximating to 5865-20,499 breeding females per annum and a total estimate of 15,730 to 41,373 breeding females). Our approach also serendipitously provides insights into the spatial appropriateness of Gabon’s protected areas network, for example (mean ± 1SD) 79 ± 6% (range 67-86%) of leatherback turtle activities recorded during aerial surveys (n = 8) occurred within protected areas (345 km, 58%, of surveyed coastline). We identify and discuss sources of potential error in estimating total nesting effort from aerial surveying techniques and show that interannual variation in nesting is considerable, which has implications for the detection of statistically significant changes in population size. Despite its relative costliness per day, aerial surveying can play an important role in providing estimates of relative population abundance of large vertebrates dispersed over extensive areas. Furthermore, it can provide data on habitat use and deliver real-time information on the spatial efficacy of protected area networks.     

Home range, movement and activity patterns, and bedding sites of Malayan sun bears Helarctos malayanus in the Rainforest of Borneo

Six Malayan sun bears were captured and radio-collared from June 1999 to December 2001 in Ulu Segama Forest Reserve, Sabah, Malaysia Borneo to study home-range characteristics, movement patterns, activity patterns, population density, and bedding sites. A total of 343 locations were recorded. Home range sizes, calculated by the 95% adaptive kernel method, averaged 14.8 ± 6.1 (SD) km². Bears were found in both primary and logged forests. Daily movement distances from these bears averaged 1.45 ± 0.24 (SD) km, and were affected by food availability, especially availability of figs. Male Malayan sun bears were primarily diurnal, but a few individuals were active at night for short periods. The majority of the 26 bedding sites consisted of fallen hollow logs. Other bedding sites included standing trees with cavities, cavities underneath fallen logs or tree roots, and tree branches high above the ground. Malayan sun bears exist in primary and logged forests. Well-designed logging practices, maintenance of large trees with cavities, protection of fig trees, and strict control of poaching should be incorporated into forest management practices in logged forests.     

Changes in attitudes toward wolves in Croatia

Against a background of an evolving wolf policy process we carried out personal structured interviews with residents of three regions within Croatian wolf range in 1999 (n = 1209) and repeated the study, using the same methodology in 2003 (n = 1172). We documented a change in public support for wolf conservation and support for control of wolves. The change was a result of a real change in attitudes and not of a change in the age structure of the sampled population. The changes were documented in the two southern regions, Lika and Dalmatia, with attitudes shifting towards a more neutral viewpoint, as there was a decrease in support for wolf conservation and a decrease in support to control wolves. It seems that different birth cohorts react differently to conservation activities. In 1999, the younger cohort groups may have been influenced more by the legal protection campaign. The older cohorts reacted more sympathetically to livestock concerns and thus held stronger negative attitudes toward wolves. Using human dimensions research as an evaluative tool can help large carnivore managers be more adaptive and thus effective in their management solutions.     

Prevalence and dispersal of a facultative bacterial symbiont associated with an endemic metazoan host

Co-dispersal is of primary importance in symbiotic relations between macro- and micro-organisms. Obligate symbionts generally follow the same dispersal pattern as their host, while it still remains unresolved whether hosts and their facultative symbionts follow the same dispersal patterns. Here we addressed the question of symbiont and host co-dispersal by analyses of the earthworm Lumbricus terrestris, and its facultative bacterial symbiont Verminephrobacter. We analyzed co-dispersal by direct sequence-based typing of the earthworm mitochondrial ND4, and the symbiont adk genes, respectively. A total of 96 earthworms from Norwegian (n = 20), German (n = 20), English (n = 31) and Canadian (n = 25) populations were analyzed. We found that the earthworms were mainly endemic, while the symbiont showed a more complex dispersal pattern. The symbiont showed a significant difference in prevalence between the geographic regions. In addition, we found a low degree of co-evolution between host and symbiont, with some of the symbiont sequence types being globally distributed. Future research, however, is needed to resolve whether the symbiont is truly globally distributed, in contrast to its endemic host.     

Protection from harvesting restores the natural social structure of eastern wolf packs

Legal and illegal killing of animals near park borders can significantly increase the threat of extirpation for populations living within ecological reserves, especially for wide-ranging large carnivores that regularly travel into unprotected areas. While the consequences of human-caused mortality near protected areas generally focus on numerical responses, little attention has been given to impacts on social dynamics. For wolves, pack structure typically constitutes an unrelated breeding pair, their offspring, and close relatives, but intense harvest may increase adoption of unrelated individuals into packs. Concerns that high human-caused mortality outside Algonquin Park, Canada threatened the persistence of eastern wolves, led to implementation of a harvest ban in surrounding townships. We combined ecological and genetic data to show that reducing anthropogenic causes of mortality can restore the natural social structure of kin-based groups despite the absence of a marked change in density. Since implementation of the harvest ban, human-caused mortality has decreased (P = 0.000006) but been largely offset by natural mortality, such that wolf density has remained relatively constant at approximately three wolves/100 km². However, the number of wolf packs with unrelated adopted animals has decreased from 80% to 6% (P = 0.00003). Despite the high kinship within packs, incestuous matings were rare. Our results indicate that even in a relatively large protected area, human harvesting outside park boundaries can affect evolutionarily important social patterns within protected areas. This research demonstrates the need for conservation policy to consider effects of harvesting beyond influences on population size.     

Persistence and conservation of a consumer-resource metapopulation with local overexploitation of resources

The monophagous flightless weevil Hadramphus spinipennis causes the frequent local extinction of its host plant Aciphylla dieffenbachii through overexploitation. Both species are endemic and restricted to the Chatham Islands group (New Zealand). The weevil is classified as endangered and the plant as a threatened species. As this herbivore-plant system is locally unstable long-term persistence only appears possible via a metapopulation structure in which subpopulations are connected by dispersal. This paper investigates this hypothesis using a spatially explicit model of a consumer population whose resource is patchily distributed. The parameters are adapted to the H. spinipennis-A. dieffenbachii system. Our model includes local population dynamics and dispersal of the consumer, the destruction of host plant patches due to foraging and their regeneration. The results show that the key factor for long-term persistence is the short-range dispersal of the consumer with high mortality during dispersal. Only this highly inefficient dispersal prevents the synchronisation of local dynamics while ensuring sufficient colonisation of regenerated patches. We also show that although synchronisation through spatially correlated environmental fluctuations may be critical for long-term persistence, it cannot replace the strong effects of dispersal. Thus, in a consumer-resource metapopulation with deterministic local extinction, the strength and spatial scale of consumer dispersal in relation to the spatial and temporal scales of the resource patch dynamics (patch destruction and regeneration, number, size and distance of patches) play a vital role for long-term persistence. The consequence for conservation management is that such metapopulations could in fact profit rather than suffer from decreasing connectivity of resource patches.     

Parthenogenesis, polyploidy and reproductive seasonality in the Taiwanese mountain earthworm Amynthas catenus (Oligochaeta, Megascolecidae)

Amynthas catenusTsai et al., 2001 is a terrestrial earthworm belonging to the Pheretima complex of the family Megascolecidae. It is endemic to Mt. Hohuan of central Taiwan at elevations of 2985-3004 m. Its reproductive organs showed various stages of degeneration in the present study. The spermathecae varied from being absent (athecal) to three pairs in VI-VIII (sexthecal), and the prostate glands from a large, symmetrical pair to complete absence. For the 44 specimens examined from May 2008 to May 2010, there were 47.7% athecals, 36.4% sexthecals and 15.9% intermediates. Results of a flow cytometric analysis showed that there were three DNA ploidy levels - diploid, triploid and tetraploid (2n, 3n, and 4n) - for the athecals but only diploid for the sexthecals. The intermediates consisted of diploids and triploids. The diploids had 2n = 112 and the triploids 3n = 168. The haploid chromosome number of A. catenus was 56. Spermatogenesis occurred throughout the year with the highest activity in summer for both athecals and sexthecals, but the number of mature ova peaked in summer for the athecals and in spring for the sexthecals. There was no significant difference in mean number of mature ova produced between the athecals and the sexthecals, but the sexthecals had significantly higher spermatogenetic activity than the athecals. For all specimens examined, sperm were present in testes and seminal vesicles but not in spermathecae, an indication of parthenogenesis in the species.     

Status assessment of the Indus River dolphin, Platanista gangetica minor, March-April 2001

A survey was conducted in March and April 2001, to assess the status of the Indus River dolphin, Platanista gangetica minor, throughout its present range. A total of 1535 km of survey effort was conducted, consisting of 1375 km of the Indus River main channel, 136 km of Indus River secondary channels, and 24 km of the Panjnad River, a tributary of the Indus. The effective range of the Indus dolphin has declined by 80% since 1870. The sum of best group size estimates produced an abundance estimate of 965 dolphins. Extrapolation of encounter rates to un-surveyed channels and application of a correction factor to account for missed dolphins indicates that the metapopulation may number approximately 1200 individuals. Dolphins occur in five subpopulations separated by irrigation barrages. A pronounced increase in dolphin abundance and encounter rate was observed in each subsequent downstream subpopulation (except the last). The three largest subpopulations were between Chashma and Taunsa Barrages (84 dolphins; 0.28/km), Taunsa and Guddu Barrages (259 dolphins; 0.74/km) and Guddu and Sukkur Barrages (602 dolphins; 3.60/km). Reasons suggested for the high encounter rate between Guddu and Sukkur Barrages, include high carrying capacity, low levels of anthropogenic threat, effective conservation, and augmentation of the subpopulation by downstream migration of dolphins from upstream.     

Integrated diurnal soil respiration model during growing season of a typical temperate steppe: Effects of temperature, soil water content and biomass production

Soil respiration was measured with the enclosed chamber method in an ungrazed Leymus chinensis steppe during the growing seasons of 2001 and 2002. Soil respiration rate (R_S) was significantly influenced by air temperature (T) at the diurnal scale, and could be described by Van't Hoff's equation (R_S = R₁₀ exp(β(T − 10))). At the seasonal scale, the normalized soil respiration rate at 10 °C (R₁₀) was mainly controlled by soil water content (R² = 0.717, P < 0.001), while the sensitivity of soil respiration to temperature (Q₁₀) was partially affected by absolute growth rate (R² = 0.482, P = 0.004). Thus, soil respiration could be described as R_S = (20.015W − 84.085) (0.103AGR + 1.786)^(T−10)/10 during the growing seasons, integrating soil water content (W) and absolute growth rate (AGR) into the temperature-dependent soil respiration equation. It was validated by the observed soil respiration rates in this study (R² = 0.890, P < 0.001) and observations from near-field experiment (R² = 0.687, P = 0.011). It implied that accurately evaluating annual soil respiration should include the effects of plant biomass production and other abiotic factors besides air temperature.