Tropical Mammals Research Articles

A meta‐analysis of the effects of anthropogenic disturbances on tropical mammal functional diversity

Abstract Understanding the processes that shape biological communities under a variety of perturbations is a central challenge in ecology and conservation. Mammals contribute to critical functional processes of an ecosystem, such as seed dispersal to maintain forest carbon stocks. The analysis of functional diversity, which measures the range and value of the ecological traits of organisms, provides critical information to understanding the link between biodiversity and ecosystem functioning. A growing number of studies have investigated the effects of anthropogenic disturbances on mammalian functional diversity; however, their results are very heterogeneous. Here, we conduct a comprehensive meta‐analysis of the effects of such anthropogenic disturbances on mammalian functional diversity in the tropics. We highlight major trends and analyse the influence of the type of anthropogenic disturbance, subgroups, and the functional diversity index used/applied. Our results indicate a negative effect of anthropogenic disturbances on mammalian functional diversity, particularly on functional richness (FRic) and functional dispersion (FDis). Habitat isolation was the stressor with the strongest effect, while agriculture and urbanisation showed a positive link with functional diversity. These results indicate that anthropogenic disturbances not only affect taxonomic diversity, but also reduce the functional diversity of mammals, which is likely to affect ecosystem functioning and possibly ecosystem service provision.

Testing and optimizing metabarcoding of iDNA from dung beetles to sample mammals in the hyperdiverse Neotropics.

Over the past few years, insects have been used as samplers of vertebrate diversity by assessing the ingested-derived DNA (iDNA), and dung beetles have been shown to be a good mammal sampler given their broad feeding preference, wide distribution and easy sampling. Here, we tested and optimized the use of iDNA from dung beetles to assess the mammal community by evaluating if some biological and methodological aspects affect the use of dung beetles as mammal species samplers. We collected 403 dung beetles from 60 pitfall traps. iDNA from each dung beetle was sequenced by metabarcoding using two mini-barcodes (12SrRNA and 16SrRNA). We assessed whether dung beetles with different traits related to feeding, nesting and body size differed in the number of mammal species found in their iDNA. We also tested differences among four killing solutions in preserving the iDNA and compared the effectiveness of each mini barcode to recover mammals. We identified a total of 50 mammal OTUs (operational taxonomic unit), including terrestrial and arboreal species from 10 different orders. We found that at least one mammal-matching sequence was obtained from 70% of the dung beetle specimens. The number of mammal OTUs obtained did not vary with dung beetle traits as well as between the killing solutions. The 16SrRNA mini-barcode recovered a higher number of mammal OTUs than 12SrRNA, although both sets were partly non-overlapping. Thus, the complete mammal diversity may not be achieved by using only one of them. This study refines the methodology for routine assessment of tropical mammal communities via dung beetle 'samplers' and its universal applicability independently of the species traits of local beetle communities.

Evolutionary history and environmental variability structure contemporary tropical vertebrate communities

AbstractAimTropical regions harbour over half of the world's mammals and birds, but how their communities have assembled over evolutionary timescales remains unclear. To compare eco‐evolutionary assembly processes between tropical mammals and birds, we tested how hypotheses concerning niche conservatism, environmental stability, environmental heterogeneity and time‐for‐speciation relate to tropical vertebrate community phylogenetic and functional structure.LocationTropical rainforests worldwide.Time periodPresent.Major taxa studiedGround‐dwelling and ground‐visiting mammals and birds.MethodsWe used in situ observations of species identified from systematic camera trap sampling as realized communities from 15 protected tropical rainforests in four tropical regions worldwide. We quantified standardized phylogenetic and functional structure for each community and estimated the multi‐trait phylogenetic signal (PS) in ecological strategies for the four regional species pools of mammals and birds. Using linear regression models, we test three non‐mutually exclusive hypotheses by comparing the relative importance of colonization time, palaeo‐environmental changes in temperature and land cover since 3.3 Mya, contemporary seasonality in temperature and productivity and environmental heterogeneity for predicting community phylogenetic and functional structure.ResultsPhylogenetic and functional structure showed non‐significant yet varying tendencies towards clustering or dispersion in all communities. Mammals had stronger multi‐trait PS in ecological strategies than birds (mean PS: mammal = 0.62, bird = 0.43). Distinct dominant processes were identified for mammal and bird communities. For mammals, colonization time and elevation range significantly predicted phylogenetic clustering and functional dispersion tendencies respectively. For birds, elevation range and contemporary temperature seasonality significantly predicted phylogenetic and functional clustering tendencies, respectively, while habitat diversity significantly predicted functional dispersion tendencies.Main conclusionsOur results reveal different eco‐evolutionary assembly processes structuring contemporary tropical mammal and bird communities over evolutionary timescales that have shaped tropical diversity. Our study identified marked differences among taxonomic groups in the relative importance of historical colonization and sensitivity to environmental change.

REPRODUCTIVE CYCLE STAGE ASSESSMENT IN THE TWO-TOED SLOTH (CHOLOEPUS HOFFMANNI), PRELIMINARY RESULTS.

The number of two-toed sloths (Choloepus hoffmanni) has significantly decreased in the last years. Deepening the knowledge of this tropical mammal's reproductive physiology is essential to improve captive breeding within conservation programs for this species. However, several aspects of its reproductive biology remain unexplored and have not been described sufficiently. The aim of this work was to describe the estrous cycle and reproductive physiology of two adult female C. hoffmanni by vaginal cytology, appearance of the external genitalia, and behavior. Vaginal cytology assay showed that the average duration of the estrous cycle was 15.1 ± 4.53 d. Positive correlations (P < 0.05) were found between the peak presence of superficial cells (estrous phase) and four parameters: aggressive behavior, pursuing behavior, vulvar swelling, and vaginal discharge. This pilot study, conducted on just two animals, forms a basis for a study design that may be employed for a more comprehensive assessment of the two-toed sloth reproductive physiology and behavior.

Comparative Study on Blowfly-Derived DNA and Camera Trapping in Assessing Mammalian Diversity in Subtropical Forests

Mammalian DNA derived from invertebrates (iDNA), including blowfly iDNA, is an alternative tool to conventional camera trapping in assessing mammalian diversity. The method has been used in tropical mammal surveillance but no attempt has been made to compare the efficacy of blowfly iDNA and camera trapping for monitoring mammal diversity in subtropical forests. We compared the blowfly iDNA monitoring with camera trapping to assess mammal diversity in the subtropical Jiulongfeng Nature Reserve (JLF), China, over a one-month period. The camera traps captured 2508 animal photos of 11 species belonging to four orders, eight genera, and eight families, whereas the blowfly iDNA method successfully detected ten species from six orders, eight genera, and eight families in JLF. Both methods were complementing each other instead of competing due to the low overlaps of mammal species detected. Of the total number of mammal species listed in JLF’s threatened list, 40% and 10% were detected through camera traps and blowfly iDNA methods, respectively. The estimated species richness curves indicated that combining camera traps and blowfly traps would increase the detection of mammal species. The strategy would significantly contribute to mammalian diversity surveillance and conservation programs in the tropical and subtropical forests.

A predominantly diurnal tropical mammal increases nocturnality in response to high temperatures

AbstractThe extent to which animals may compensate for rising temperatures through behavioral thermoregulation is an important unknown in predicting responses to climate change. Flexibility in temporal activity in particular may be an important factor in determining species' vulnerability. In this study, we examine whether the white‐lipped peccary, a predominantly diurnal Neotropical mammal, shifts its temporal activity and microclimate selection in response to daily temperature variation in the Pantanal biome of Brazil. From November 2021 to October 2022, we deployed camera traps and microclimate data loggers to record white‐lipped peccary activity and air temperature on a fine spatiotemporal scale. We found that the percentage of peccary activity that is nocturnal increased with maximum daily temperature at a rate of 3.7% per 1°C past a threshold of 31.2°C, and increased with maximum daily wet‐bulb temperature at a rate of 4.7% per 1°C past a threshold of 24.9°C. The afternoon period (i.e., solar noon to sunset) went from having the highest frequency of peccary activity at the lower end of our observed temperature range to having the lowest frequency of activity at the higher end. We did not find evidence of microclimate selection. Our findings indicate that white‐lipped peccaries in the Pantanal demonstrate substantial behavioral flexibility in their response to high temperatures, which may help to buffer them against the impact of rising temperatures caused by climate change.Abstract in Portuguese is available with online material.

Thermoregulation in the wild boar (Sus scrofa)

The wild boar (Sus scrofa) originates from warm islands but now inhabits large areas of the world, with Antarctica as the only continent not inhabited by this species. One might be tempted to think that its wide distribution results from increasing environmental temperatures. However, any effect of temperature is only indirect: Abundant availability of critical food resources can fully compensate the negative effects of cold winters on population growth. Here, we asked if temperature as a habitat factor is unimportant compared with other habitat indices, simply because wild boars are excellent thermoregulators. We found that the thermoneutral zone in summer was approximately 6–24 °C. In winter, the thermoneutral zone was lowered to 0–7 °C. The estimated increase in the heart rate and energy expenditure in the cold was less than 30% per 10 °C temperature decline. This relatively small increase of energy expenditure during cold exposure places the wild boar in the realm of arctic animals, such as the polar bear, whereas tropical mammals raise their energy expenditure several fold. The response of wild boars to high Ta was weak across all seasons. In the heat, wild boars avoid close contact to conspecifics and particularly use wallowing in mud or other wet substrates to cool and prevent hyperthermia. Wild boars also rely on daily cycles, especially of rhythms in subcutaneous temperature that enables them to cheaply build large core–shell gradients, which serve to lower heat loss. We argue it is predominantly this ability which allowed wild boars to inhabit most climatically diverse areas in the world.

Stratified activity: Vertical partitioning of the diel cycle by rainforest mammals in Borneo

AbstractAnimal activity is driven by the environmental conditions and physical structure of a habitat, and the need to interact with, or avoid, other animals. Knowledge of the proportion of the 24‐hour cycle spent active (activity level), and the time/s of day in which activity is concentrated (activity pattern), informs our understanding of species' ecology and community dynamics. In multidimensional habitats such as tropical rainforests, arboreal (canopy‐dwelling) taxa comprise up to three‐quarters of vertebrate assemblages; yet, wildlife surveys are typically limited to ground level. Terrestrial‐only sampling can result in activity metrics that do not take account of species' full use of horizontal and vertical habitat space. We paired ground‐ and canopy‐level camera traps to characterize mammal activity across vertical strata in Borneo. Additionally, we sampled unlogged and recovering‐logged rainforest to evaluate whether this activity was impacted by logging. Activity across vertical strata varied substantially among 37 species. Arboreal mammals were predominantly nocturnal or diurnal but never cathemeral, terrestrial mammals were mostly nocturnal or cathemeral, and semi‐arboreal mammals appeared to fill the temporal niches under‐utilized by other groups. Differences in activity between unlogged and recovering‐logged forest were minimal, with 92% of species found in both forest types retaining the same activity pattern. Our study demonstrates that the inclusion of canopy‐based sampling provides much greater insights into overall rainforest mammal activity than terrestrial sampling alone. Our results suggest that the varying opportunities and constraints of each stratum act in concert to influence the diel patterns of tropical mammals.Abstract in Malay is available with online material.

Living on the edge: forest edge effects on microclimate and terrestrial mammal activity in disturbed lowland forest in Sumatra, Indonesia

AbstractSpecies–environment relationships are often studied at large spatial scales, but effective conservation requires an understanding of local-scale environmental drivers and pressures. Widespread degradation and fragmentation of forests have increased the proportion of tropical mammal habitat that is affected by edge effects. Edge effects include greater exposure to anthropogenic disturbance and abiotic changes that synergistically influence how well populations can cope with climate change. We investigated relationships between distance to the forest edge, forest structure, microclimate and terrestrial mammal detections in a selectively logged forest at the boundary of Gunung Leuser National Park in Sumatra, Indonesia. We collected mammal detection data from motion-activated camera traps, microclimate data from automated climate data loggers and forest structure data from vegetation plots. Daily mean and maximum temperatures significantly decreased with distance from the forest edge, whereas tree height and minimum temperature increased. Mammal diversity was lower at the forest edge compared to the interior. Mammals were detected less frequently at the forest edge, although this relationship varied between mammal orders. Mammal detections were best explained by temperature, tree height and tree diameter at breast height. These results demonstrate that abiotic changes in forests brought on by edge effects have negative impacts on mammals, but these effects vary between mammal taxa because of differing sensitivities to human disturbance. Our findings highlight the importance of considering local-scale environmental drivers in determining species–environment relationships to identify key habitat features such as microclimate refuges that should be prioritized in ecosystem management.

Pyrodiversity begets taxonomic and functional richness of tropical mammals

Pyrodiversity begets taxonomic and functional richness of tropical mammals

Olingos do eat insects: Records of nocturnal mammals preying on arthropods in arboreal live-capture traps

The natural history of arboreal tropical mammals is poorly known, especially nocturnal species, because they are difficult to find. Most observations in the wild come from congregations at fruiting trees, but the extent to which they eat items other than fruit is not known. Here we report the first recorded insectivore behavior of eastern lowland olingos (Bassaricyon alleni) in the wild, confirming that insects are part of their diet. We also report Orthoptera and Lepidoptera as part of the diet of brown-eared wooly opossums (Caluromys lanatus) and mouse opossums (Marmosa sp.). We used camera traps to record the behavior of animals attracted to different baits as part of a program of pre-baiting arboreal live-capture traps in Amazonian Peru. We recorded 4 predatory events of olingos, 11 of wooly opossums, and 3 of mouse opossums catching and eating Orthoptera, Lepidoptera, and possibly other arthropods. These observations confirm that olingos eat insects, as well as fruits, and add information to the known omnivore diet of arboreal opossums and possible niche differences with sympatric species like the kinkajou (Potos flavus). We suggest more detailed diet studies through collection of feces or isotopic analysis should be used to determine the relative importance of these food items, and thus the ecological roles they play in neotropical forests.

Destabilizing effect of climate change on the persistence of a short-lived primate

Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.

Consistent diel activity patterns of forest mammals among tropical regions

An animal’s daily use of time (their “diel activity”) reflects their adaptations, requirements, and interactions, yet we know little about the underlying processes governing diel activity within and among communities. Here we examine whether community-level activity patterns differ among biogeographic regions, and explore the roles of top-down versus bottom-up processes and thermoregulatory constraints. Using data from systematic camera-trap networks in 16 protected forests across the tropics, we examine the relationships of mammals’ diel activity to body mass and trophic guild. Also, we assess the activity relationships within and among guilds. Apart from Neotropical insectivores, guilds exhibited consistent cross-regional activity in relation to body mass. Results indicate that thermoregulation constrains herbivore and insectivore activity (e.g., larger Afrotropical herbivores are ~7 times more likely to be nocturnal than smaller herbivores), while bottom-up processes constrain the activity of carnivores in relation to herbivores, and top-down processes constrain the activity of small omnivores and insectivores in relation to large carnivores’ activity. Overall, diel activity of tropical mammal communities appears shaped by similar processes and constraints among regions reflecting body mass and trophic guilds.

The role of non‐natural foods in the nutritional strategies of monkeys in a human‐modified mosaic landscape

AbstractMany tropical animals inhabit mosaic landscapes including human‐modified habitat. In such landscapes, animals commonly adjust feeding behavior, and may incorporate non‐natural foods. These behavioral shifts can influence consumers' nutritional states, with implications for population persistence. However, few studies have addressed the nutritional role of non‐natural food. We examined nutritional ecology of wild blue monkeys to understand how dietary habits related to non‐natural foods might support population persistence in a mosaic landscape. We documented prevalence and nutritional composition of non‐natural foods in monkey diets to assess how habitat use influenced their consumption, and their contribution to nutritional strategies. While most energy and macronutrients came from natural foods, subjects focused non‐natural feeding activity on five exotic plants, and averaged about a third of daily calories from non‐natural foods. Most non‐natural food calories came from non‐structural carbohydrates and least from protein. Consumption of non‐natural foods related to time in human‐modified habitats, which two groups used non‐randomly. Non‐natural and natural foods were similar in nutrients, and the amount of non‐natural food consumed drove variation in nutritional strategy. When more daily calories came from non‐natural foods, females consumed a higher ratio of non‐protein energy to protein (NPE:P). Females also prioritized protein while allowing NPE:P to vary, increasing NPE while capitalizing on non‐natural foods. Overall, these tropical mammals achieved a similar nutrient balance regardless of their intake of non‐natural foods. Forest and forest‐adjacent areas with non‐natural vegetation may provide adequate nutrient access for consumers, and thus contribute to wildlife conservation in mosaic tropical landscapes.

Do Wildlife Crossings Mitigate the Roadkill Mortality of Tropical Mammals? A Case Study from Costa Rica

Although Central America is one of the most biologically diverse regions in the world, booming road construction is driving roadkill mortality that threatens to alter the demography, genetic diversity, and viability of wild mammalian populations. Costa Rica has the highest road density in Central America, but the effectiveness of wildlife crossings in mitigating roadkill mortality has not been assessed with controlled experimental studies. Hacienda Baru National Wildlife Refuge is located along a critical biological corridor bisected by one of the busiest highways in the country. The first wildlife underpasses in Costa Rica were built here in 2010 as part of the expansion of Route 34 and subsequently documented by camera-trap and roadkill surveys. Using a control-impact design, we demonstrate a considerable reduction in wildlife mortality in the presence of the crossing structures compared with controls, with the underpasses and overpasses eventually used by 21 mammalian species. Some species made use of the structures right away, while others took over a year to learn to use them. This is the first controlled study in Central America to document the effectiveness of wildlife crossings and provides evidence that well-designed mitigation structures can contribute to wildlife-friendly roadways.

Disappearance of an ecosystem engineer, the white-lipped peccary (Tayassu pecari), leads to density compensation and ecological release

Given the rate of biodiversity loss, there is an urgent need to understand community-level responses to extirpation events, with two prevailing hypotheses. On one hand, the loss of an apex predator leads to an increase in primary prey species, triggering a trophic cascade of other changes within the community, while density compensation and ecological release can occur because of reduced competition for resources and absence of direct aggression. White-lipped peccary (Tayassu pecari—WLP), a species that typically co-occurs with collared peccary (Pecari tajacu), undergo major population crashes—often taking 20 to 30-years for populations to recover. Using a temporally replicated camera trapping dataset, in both a pre- and post- WLP crash, we explore how WLP disappearance alters the structure of a Neotropical vertebrate community with findings indicative of density compensation. White-lipped peccary were the most frequently detected terrestrial mammal in the 2006–2007 pre-population crash period but were undetected during the 2019 post-crash survey. Panthera onca (jaguar) camera trap encounter rates declined by 63% following the WLP crash, while collared peccary, puma (Puma concolor), red-brocket deer (Mazama americana) and short-eared dog (Atelocynus microtis) all displayed greater encounter rates (490%, 150%, 280%, and 500% respectively), and increased in rank-abundance. Absence of WLP was correlated with ecological release changes in habitat-use for six species, with the greatest increase in use in the preferred floodplain habitat of the WLP. Surprisingly, community-weighted mean trait distributions (body size, feeding guild and nocturnality) did not change, suggesting functional redundancy in diverse tropical mammal assemblages.

Direct comparisons of logging and agroforestry influence on tropical mammals in Sarawak, Borneo

AbstractTropical regions are undergoing rapid land use change, with major implications for global biodiversity. Selective logging and agroforestry are particularly widespread across tropical forests, often occurring in close proximity. But while a number of studies have addressed their impacts separately, few have directly compared how they influence forest vertebrates. Here, we assessed the occurrence of medium‐ to large‐bodied mammals in logged forest, unlogged forest, and agroforestry areas in three study areas in interior Sarawak, Malaysian Borneo. We detected 34 species across 99 camera trap locations and used multi‐species occupancy models to estimate species‐specific occurrence while accounting for imperfect detectability, spatial autocorrelation, natural habitat heterogeneity, and metrics of site accessibility (distance to human infrastructure) as proxies for potential hunting pressure. We found that species occurrences were unaffected by the distance to the nearest road or village and only responded to elevation and the distance to the nearest river in a single species each. Detection rates tended to vary with micro‐habitat characteristics such as the size of tree stumps and the prevalence of trees and rattan palms, which are often not considered in camera‐based occupancy studies. Occurrence rates of five species varied across habitat types but were not detectably lower in agroforestry sites than in unlogged forest for any species. Our results indicate that without unsustainable hunting, agroforestry and logged forest provide usable habitat for some, though not all, rainforest mammals. We also suggest that camera trap studies may benefit from the incorporation of fine‐scale habitat information into detectability estimation.Abstract in Malaysian is available with online material.

A global indicator of utilized wildlife populations: Regional trends and the impact of management

A global indicator of utilized wildlife populations: Regional trends and the impact of management

Forest structure and seasonally inundated grassland shape tropical mammal communities under moderate disturbance

AbstractTropical biodiversity is threatened globally by anthropogenic disturbances, particularly forest degradation and overhunting. Where large mammals have been extirpated, smaller bodied “mesomammals” may play an important ecological role (e.g., as seed dispersers). However, these species are disproportionally affected by overhunting for wildlife trade markets and are routinely understudied as they tend to be rare, cryptic, and nocturnal. Few studies have examined spatiotemporal responses to anthropogenic disturbance by mesomammals at the community level, which may identify imbalances within an ecosystem that could threaten species persistence. We deployed camera traps throughout Cat Tien National Park (i.e., Nam Cat Tien area), southern Vietnam, to (1) identify long‐term changes in terrestrial mesomammal richness and (2) evaluate the effects of forest structure and anthropogenic disturbance on an 18‐species mesomammal community within a historically disturbed tropical forest using hierarchical Bayesian community occupancy models. We found that site occupancy was driven by the interaction between distance to seasonally inundated grassland and absolute forest cover (basal area per hectare). This may be due to the combination of intact forest benefits (refuge from predators and hunters, denning sites) and early successional grassland resources (forage quality), as well as high levels of tolerance for disturbed forest among the largely generalist mesomammal community of Nam Cat Tien. We found no negative effects of current anthropogenic factors at the community level. However, we did find that four disturbance‐tolerant small carnivores have been extirpated since the 1990s and continued human presence in the park suggests that hunting and snaring remain an acute threat to native mesomammals. Without continued efforts to address the unsustainable harvest of wildlife, Southeast Asian's remaining mesomammals are at risk of extirpation despite resilience to moderate levels of disturbance.

Environmental and socioeconomic correlates of extinction risk in endemic species

AbstractAimOur current understanding of the causes of global extinction risk is mostly informed by the expert knowledge‐based “threats classification scheme” of the IUCN Red List of Threatened Species. Studies based on this dataset came to different conclusions about the relative importance of threats to species, depending on which taxonomic groups and levels of extinction risk were considered, and which version of the database was used. A key reason may lie in data limitations as causes of threat are well known for charismatic and well‐studied species, but not for the majority of species assessed. Here, we aim to fill current knowledge gaps about the importance of drivers of global extinction risks by focusing on endemic species.LocationGlobal.MethodsWe examined country‐level variation in the proportion of globally threatened and extinct endemic species (Index of Threat, IoT) with a range of spatially explicit information about anthropogenic pressures, mitigation measures and data limitations.ResultsIoT coincided with several anthropogenic pressures, with substantial differences among kingdoms, life‐forms, levels of extinction risk and geographic locations. IoT of plants, particularly tropical woody plants of moderate extinction risk, was higher in countries with higher GDP and more invasive species. Furthermore, IoT of animals, particularly tropical mammals and invertebrates of moderate extinction risk, was higher in countries with higher GDP and smaller roadless areas.Main conclusionsThe extinction crisis for endemic species is associated with a complex network of potential drivers that need to be considered in concert in conservation policy and practice. Although our results require careful interpretation and remain sensitive to data limitations, we encourage similar studies at smaller scales to identify potential drivers of extinction risk at a higher resolution, particularly in regions where species assessments have been conducted consistently or on organisms with a uniform response time to pressures.