Sigrid Heise-Pavlov

Bio: Sigrid Heise-Pavlov is an academic researcher from The School for Field Studies. The author has contributed to research in topics: Dendrolagus lumholtzi & Tree-kangaroo. The author has an hindex of 6, co-authored 16 publications receiving 109 citations.

Debugging diversity - a pan-continental exploration of the potential of terrestrial blood-feeding leeches as a vertebrate monitoring tool.

Abstract: The use of environmental DNA (eDNA) has become an applicable noninvasive tool with which to obtain information about biodiversity. A subdiscipline of eDNA is iDNA (invertebrate-derived DNA), where genetic material ingested by invertebrates is used to characterize the biodiversity of the species that served as hosts. While promising, these techniques are still in their infancy, as they have only been explored on limited numbers of samples from only a single or a few different locations. In this study, we investigate the suitability of iDNA extracted from more than 3,000 haematophagous terrestrial leeches as a tool for detecting a wide range of terrestrial vertebrates across five different geographical regions on three different continents. These regions cover almost the full geographical range of haematophagous terrestrial leeches, thus representing all parts of the world where this method might apply. We identify host taxa through metabarcoding coupled with high-throughput sequencing on Illumina and IonTorrent sequencing platforms to decrease economic costs and workload and thereby make the approach attractive for practitioners in conservation management. We identified hosts in four different taxonomic vertebrate classes: mammals, birds, reptiles and amphibians, belonging to at least 42 different taxonomic families. We find that vertebrate blood ingested by haematophagous terrestrial leeches throughout their distribution is a viable source of DNA with which to examine a wide range of vertebrates. Thus, this study provides encouraging support for the potential of haematophagous terrestrial leeches as a tool for detecting and monitoring terrestrial vertebrate biodiversity.

Studying food preferences in captive cryptic folivores can assist in conservation planning: the case of the Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi)

Abstract: Food preferences of the arboreal Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi), endemic to the tropical rainforests of north-eastern Australia, are largely unknown, but are likely to affect the movements of this mammal within its home range and across a fragmented landscape. Food selection was investigated by applying a consumption ranking system to 35 browse species provided to six captive animals throughout different years. Animals consumed foliage from a wide range of rainforest tree species, but at different intensities, suggesting that Lumholtz’s tree-kangaroo is a selective folivore. All studied animals showed a general preference for the foliage of the northern olive (Chionanthus ramiflorus) and the umbrella tree (Schefflera actinophylla) throughout the year while foliage from acacias (Acacia spp.), milky pine (Alstonia scholaris) and pink ash (Alphitonia petriei) was less frequently consumed. Foliage from figs (Ficus spp.) and the northern tamarind (Diploglottis diphyllostegia) was consumed at higher rates only at certain times of the year, suggesting the existence of seasonal preferences. The knowledge of general and seasonal food preferences of this large arboreal mammal may allow a better prediction of animal movements and therefore can assist in conservation efforts. Recommendations for the integration of these findings in restoration projects are given.

Conservation of a rare arboreal mammal: habitat preferences of the Lumholtz's tree-kangaroo, Dendrolagus lumholtzi

Abstract: Success of conservation efforts of large and cryptic mammals is often limited due to a lack of knowledge of their habitat preferences. This study investigates factors that affect the habitat selection of the rare Lumholtz’s tree-kangaroo, Dendrolagus lumholtzi, using signs of its activity. The presence and absence of scratch marks on tree trunks and faecal pellets within a 100-cm radius around them were surveyed on 23 ha within a 65-ha large fragment of rainforest on the Atherton Tablelands, north-eastern Australia in order to classify trees as ‘actively used’ or ‘inactive’. Structural features of the 315 surveyed tree trunks were also recorded. Using discriminant function analysis, ‘actively used’ trees were found to have no epiphytes on the main trunk, less obstruction by neighbouring trees, shrubs or lianas within a 0.5-m radius of the trunk (particularly in the eastern direction), and a smaller diameter at breast height than ‘inactive’ trees. Smaller tree trunks and less obstruction may facilitate a more rapid movement into the canopy as well as provide potential escape routes from predators. More specific knowledge on factors that affect habitat selection of the Lumholtz’ tree-kangaroo will help in a reclassification of the threatened status of this species and assist in more effective conservation efforts.

Current knowledge of the behavioural ecology of Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi)*

Abstract: Behavioural ecology increasingly contributes to effective species conservation. It provides a better understanding of habitat requirements and landscape use of a species. In this review the current knowledge of the behavioural ecology of the Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi) is summarised. It describes how the species utilises a structurally diverse environment such as rainforest with respect to its climbing abilities and the consumption of partly toxic rainforest foliage. It presents the latest findings on the use of non-rainforest habitats by this species, how it copes with highly fragmented landscapes within its distribution and the evolutionary bases of its antipredatory behaviours. Available information on home ranges of D. lumholtzi in various habitats is compiled and supplemented by our sparse knowledge of conspecific interactions of this species. The review shows how limited our current knowledge on the behavioural ecology of this species is, and how this knowledge should be integrated into conservation efforts for this species, and aims at encouraging more research in this field.

Diet and dietary selectivity of Cane Toads (Rhinella marina) in restoration sites: a case study in Far North Queensland, Australia

Abstract: Summary Cane Toads (Rhinella marina, formerly Bufo marinus) in restoration sites on the Atherton Tableland in NE Australia consumed invertebrates belonging to 11 different taxa with ants being the most abundant prey item. Principal component analyses showed that the composition of invertebrates in Cane Toad diet is largely a reflection of invertebrates found in pitfall and leaf litter samples suggesting that the species is an indiscriminant feeder. However, pitfall samples contained more Collembola and Isopoda than were found in Cane Toad stomachs. The Cane Toad may benefit from restoration management practices by utilizing food resources enhanced by mulching and providing microhabitats (e.g. rock piles, logs) as shelter. While further studies would be needed to test this practitioners working in areas where the Cane Toad is problematic may consider trade-offs between attracting invertebrates and Cane Toads by monitoring provided microhabitat features.

Promises and pitfalls of using high-throughput sequencing for diet analysis

Abstract: The application of high-throughput sequencing-based approaches to DNA extracted from environmental samples such as gut contents and faeces has become a popular tool for studying dietary habits of animals. Due to the high resolution and prey detection capacity they provide, both metabarcoding and shotgun sequencing are increasingly used to address ecological questions grounded in dietary relationships. Despite their great promise in this context, recent research has unveiled how a wealth of biological (related to the study system) and technical (related to the methodology) factors can distort the signal of taxonomic composition and diversity. Here, we review these studies in the light of high-throughput sequencing-based assessment of trophic interactions. We address how the study design can account for distortion factors, and how acknowledging limitations and biases inherent to sequencing-based diet analyses are essential for obtaining reliable results, thus drawing appropriate conclusions. Furthermore, we suggest strategies to minimize the effect of distortion factors, measures to increase reproducibility, replicability and comparability of studies, and options to scale up DNA sequencing-based diet analyses. In doing so, we aim to aid end-users in designing reliable diet studies by informing them about the complexity and limitations of DNA sequencing-based diet analyses, and encourage researchers to create and improve tools that will eventually drive this field to its maturity.

Shifting up a gear with iDNA: From mammal detection events to standardised surveys

Abstract: Invertebrate-derived DNA (iDNA), in combination with high throughput sequencing, has been proposed as a cost-efficient and powerful tool to survey vertebrate species. Previous studies, however, have only provided evidence that vertebrates can be detected using iDNA, but have not taken the next step of placing these detection events within a statistical framework that allows for robust biodiversity assessments. Here, we compare concurrent iDNA and camera-trap surveys. Leeches were repeatedly collected in close vicinity to 64 camera-trap stations in Sabah, Malaysian Borneo. We analyse iDNA-derived mammalian detection events in a modern occupancy model that accounts for imperfect detection and compare the results with those from occupancy models parameterised with camera-trap-derived detection events. We also combine leech-iDNA and camera-trap data in a single occupancy model. We found consistent estimates of occupancy probabilities produced by our camera-trap and leech datasets. This indicates that the metabarcoding of leech-iDNA method provides reasonable estimates of occupancy and may be a suitable method for studying and monitoring mammal species in tropical rainforests. However, we also show that a more extensive collection of leeches would be needed to assess mammal biodiversity with a robustness similar to that of camera traps. As certain taxa were only detected in leeches, we see great potential in complementing camera-trap studies with the iDNA approach, as long as the collection of leeches follows a robust and standardised sampling scheme. Synthesis and applications. Here, we describe an approach to analyse detection records of mammals derived from leech samples using an occupancy framework that accounts for leech-specific factors influencing the detection probability. We further combined camera trap and leech data, which lead to increased confidence in occupancy estimates. Our approach is not restricted to the processing of leech samples, but can be used for the analysis of other invertebrate DNA and environmental DNA data. Our study is the first step to shift the application of invertebrate DNA studies from opportunistic ad-hoc collections to the systematic surveys required for long-term management of wildlife populations.

Detection and Control of Invasive Freshwater Crayfish: From Traditional to Innovative Methods

Abstract: Invasive alien species are widespread in freshwater systems compared to terrestrial ecosystems. Among crustaceans, crayfish in particular have been widely introduced and are considered a major threat to freshwater ecosystem functioning. New emerging techniques for detecting and controlling invasive crayfish and protecting endangered native species are; thus, now highly desirable and several are under evaluation. Important innovations have been developed in recent years for detection of both invasive and native crayfish, mainly through eDNA, which allows for the detection of the target species even at low abundance levels and when not directly observable. Forecasting models have also moved towards the creation of realistic invasion scenarios, allowing effective management plans to be developed in advance of invasions. The importance of monitoring the spread and impacts of crayfish and pathogens in developing national data and research networks is emphasised; here “citizen science” can also play a role. Emerging techniques are still being considered in the field of invasive crayfish control. Although for decades the main traditional techniques to manage invasive crayfish were solely based on trapping, since 2010 biological, biocidal, autocidal controls and sexual attractants, monosex populations, RNA interference, the sterile male release technique and oral delivery have all also been investigated for crayfish control. In this review, ongoing methodologies applied to the detection and management of invasive crayfish are discussed, highlighting their benefits and limitations.

An efficient and robust laboratory workflow and tetrapod database for larger scale environmental DNA studies

Abstract: BACKGROUND: The use of environmental DNA for species detection via metabarcoding is growing rapidly. We present a co-designed lab workflow and bioinformatic pipeline to mitigate the 2 most important risks of environmental DNA use: sample contamination and taxonomic misassignment. These risks arise from the need for polymerase chain reaction (PCR) amplification to detect the trace amounts of DNA combined with the necessity of using short target regions due to DNA degradation. FINDINGS: Our high-throughput workflow minimizes these risks via a 4-step strategy: (i) technical replication with 2 PCR replicates and 2 extraction replicates; (ii) using multi-markers (12S,16S,CytB); (iii) a "twin-tagging," 2-step PCR protocol; and (iv) use of the probabilistic taxonomic assignment method PROTAX, which can account for incomplete reference databases. Because annotation errors in the reference sequences can result in taxonomic misassignment, we supply a protocol for curating sequence datasets. For some taxonomic groups and some markers, curation resulted in >50% of sequences being deleted from public reference databases, owing to (i) limited overlap between our target amplicon and reference sequences, (ii) mislabelling of reference sequences, and (iii) redundancy. Finally, we provide a bioinformatic pipeline to process amplicons and conduct PROTAX assignment and tested it on an invertebrate-derived DNA dataset from 1,532 leeches from Sabah, Malaysia. Twin-tagging allowed us to detect and exclude sequences with non-matching tags. The smallest DNA fragment (16S) amplified most frequently for all samples but was less powerful for discriminating at species rank. Using a stringent and lax acceptance criterion we found 162 (stringent) and 190 (lax) vertebrate detections of 95 (stringent) and 109 (lax) leech samples. CONCLUSIONS: Our metabarcoding workflow should help research groups increase the robustness of their results and therefore facilitate wider use of environmental and invertebrate-derived DNA, which is turning into a valuable source of ecological and conservation information on tetrapods.

Identifying conservation priorities in a defaunated tropical biodiversity hotspot

Abstract: Aim Unsustainable hunting is leading to widespread defaunation across the tropics. To mitigate against this threat with limited conservation resources, stakeholders must make decisions on where to focus anti-poaching activities. Identifying priority areas in a robust way allows decision-makers to target areas of conservation importance, therefore maximizing the impact of conservation interventions. Location Annamite mountains, Vietnam and Laos. Methods We conducted systematic landscape-scale surveys across five study sites (four protected areas, one unprotected area) using camera-trapping and leech-derived environmental DNA. We analyzed detections within a Bayesian multi-species occupancy framework to evaluate species responses to environmental and anthropogenic influences. Species responses were then used to predict occurrence to unsampled regions. We used predicted species richness maps and occurrence of endemic species to identify areas of conservation importance for targeted conservation interventions. Results Analyses showed that habitat-based covariates were uninformative. Our final model therefore incorporated three anthropogenic covariates as well as elevation, which reflects both ecological and anthropogenic factors. Conservation-priority species tended to found in areas that are more remote now or have been less accessible in the past, and at higher elevations. Predicted species richness was low and broadly similar across the sites, but slightly higher in the more remote site. Occupancy of the three endemic species showed a similar trend. Main conclusion Identifying spatial patterns of biodiversity in heavily-defaunated landscapes may require novel methodological and analytical approaches. Our results indicate to build robust prediction maps it is beneficial to sample over large spatial scales, use multiple detection methods to increase detections for rare species, include anthropogenic covariates that capture different aspects of hunting pressure, and analyze data within a Bayesian multi-species framework. Our models further suggest that more remote areas should be prioritized for anti-poaching efforts to prevent the loss of rare and endemic species.