Species Translocations Research Articles

Preserving the demographic and genetic integrity of a single source population during multiple translocations

Globally, conservation translocations are common often using island, or ‘virtual island’ populations as a source site. We investigated demographic and genetic consequences of using a single source island population for multiple translocations. Our harvest selection protocol preserves the source population whilst providing individuals that are representative of the source population. Our study species, Tasmanian devils, are endangered due to an infectious cancer with an 80 % reduction in population size across their range. In 2012, an island population was established to protect the species. The island population was harvested three times with devils translocated to wild location across Tasmania (2016, N=16; 2017, N=33; 2018, N=30). Efforts to harvest individuals demographically representative of the source population was achievable in 2017 and 2018, with a large male bias occurring in 2016 due to logistic constraints. Using internal relatedness (IR; proxy for heterozygosity), we showed that harvesting animals in equal-sized groups of high, medium and low IR, succeeded in maintaining genetic profiles of the source population over repeated harvests. There was little within-year variation in observed heterozygosity pre- and post-harvest compared to the harvest group, and only a small reduction (0.001) in heterozygosity across years. We used simulations to show that using a random selection would likely have eroded diversity relative to our structured approach (86.6% of iterations showed greater loss). Our method maintained a viable source population over multiple harvests, providing conservation managers with a tool for conserving single source populations used in threatened species translocations.

(A)wake for ‘the Passions of this Earth’: Extinction and the Absurd ‘Ethics’ of Novel Ecosystems

Drawing on the work of Albert Camus this paper offers a critique of certain discourses around ‘novel ecosystems’. These new species ‘assemblages’ are frequently defended, or even celebrated, as exemplifying resilience and adaptability to the environmental repercussions of a global situation inaccurately glossed as ‘The Anthropocene’. Here the increasing prevalence of economically generated changes, including the accelerating translocations of species, are set against earlier conservation values emphasizing protection of ‘natural’ and ‘native’ ecologies. The proliferation of novel ecosystems, together with an instrumental emphasis on their functional, ‘pragmatic’, and economic benefits, appears to make environmentalists’ ethical concerns about the loss of endangered others seem ‘absurd’ and frames conservation as a Sisyphean task. Yet Camus early work provides arguments for ethical / political resistance in just such absurd and extreme circumstances.

Ex situ collections and their potential for the restoration of extinct plants.

The alarming current and predicted species extinction rates have galvanized conservationists in their efforts to avoid future biodiversity losses, but for species extinct in the wild, few options exist. We posed the questions, can these species be restored, and, if so, what role can ex situ plant collections (i.e., botanic gardens, germplasm banks, herbaria) play in the recovery of plant genetic diversity? We reviewed the relevant literature to assess the feasibility of recovering lost plant genetic diversity with using ex situ material and the probability of survival of subsequent translocations. Thirteen attempts to recover species extinct in the wild were found, most of which used material preserved in botanic gardens (12) and seed banks (2). One case of a locally extirpated population was recovered from herbarium material. Eight (60%) of these cases were successful or partially successful translocations of the focal species or population; the other 5 failed or it was too early to determine the outcome. Limiting factors of the use of ex situ source material for the restoration of plant genetic diversity in the wild include the scarcity of source material, low viability and reduced longevity of the material, low genetic variation, lack of evolution (especially for material stored in germplasm banks and herbaria), and socioeconomic factors. However, modern collecting practices present opportunities for plant conservation, such as improved collecting protocols and improved cultivation and storage conditions. Our findings suggest that all types of ex situ collections may contribute effectively to plant species conservation if their use is informed by a thorough understanding of the aforementioned problems. We conclude that the recovery of plant species currently classified as extinct in the wild is not 100% successful, and the possibility of successful reintroduction should not be used to justify insufficient in situ conservation.

Development of a hybrid CFD-PBPK model to predict the transport of xenon gas around a human respiratory system to systemic regions

Administering incorrect doses of conventional anesthetic agents through the pulmonary route can cause potential health risks such as blood coagulation, platelet dysfunction, and deteriorating organ function. As an alternative, xenon can minimize the impact on the cardiovascular system and provide the neuroprotective effect, hemodynamic stability, and fast recovery. However, the inhalation pattern still needs to be carefully monitored and controlled to avoid health risks caused by over administering xenon to patients during unconsciousness. Thus, high-resolution lung absorption and whole-body translocation data are critically needed to fully understand how to administer the gas and coordinate with the patient to accurately control the dose. Clinical studies are not able to provide accurate dosimetry data due to their limited operational flexibility and imaging resolution. Therefore, a computational fluid dynamics (CFD) model was employed in this study to simulate the transport and absorption of the inhaled xenon which is connected with a physiologically based pharmacokinetic (PBPK) model to predict the translocation into the systemic regions. To study the effects of different breathing patterns on xenon transport dynamics in the human body, a realistic breathing waveform and two steady-state flow rates with inhalation durations of 2 and 1.5 seconds were selected. For the realistic breathing cycle, the inhalation-exhalation periods are defined for a human at rest and the other two cases have a fixed volumetric flow rate of 15 L/min. As the two latter cases only simulate the inspiratory phase, a 1-second holding time was applied to represent the missing periods of the full breathing time. Simulations were performed in a subject-specific human upper airway configuration from mouth to G6. Numerical results show that with the accurate lung uptake predictions obtained from the CFD model, the hybrid CFD-PBPK model with TRANSIT compartments generates more precise and breath-specific trends compared to simple PBPK models. Numerical results demonstrate that breathing pattern can significantly influence the xenon uptake in the human body, which can be utilized as a critical factor to be coordinated by clinicians to achieve the optimized xenon dose. Furthermore, parametric analyses were performed for the influence of breathing patterns on local airflow distributions, gas species translocations, and lung elimination mechanisms followed by species diffusion into the systemic regions.

Post‐release dispersal and spawning movements of a translocated lake sturgeon (Acipenser fulvescens, Rafinesque 1817) population in the Mattagami River, Ontario

Species translocations are increasingly being used as a management tool to mitigate population losses due to such factors as habitat degradation and fragmentation, but post-introduction follow-up is relatively sparse. Post-translocation telemetry can assess success by identifying activity, emigrations, survival, habitat usage, and reproductive events, aiding in the continued management of translocated populations and informing future efforts. This study assessed movement of translocated adult lake sturgeon (Acipenser fulvescens) immediately post-release and a decade later, and tested for associations between environmental variables and spawning movements. Prior to their translocation in 2002, 13 of 51 adult lake sturgeon were surgically implanted with radio telemetry tags and tracked for 1 year. In 2011 and 2013, eight additional adults were captured within the reintroduction site and implanted with radio-tags. Six of the 13 sturgeon tagged in 2002 dispersed downstream over a dam during the early post-release period. In spring 2014, tagged adults were tracked to the spillway at the release area's inflow, and spawning was confirmed by larval captures. Movement data for tagged adults differed between the two tracking periods, showing marked differences in behaviour over time. Water velocity was correlated with upstream and downstream spawning movements, with water temperature also correlated with downstream movement. Research regarding post-translocation movement and dispersal provides insight on behavioural responses following translocation, and may improve outcomes by informing future efforts.

Understanding predator densities for successful co‐existence of alien predators and threatened prey

AbstractThe high failure rate of threatened species translocations has prompted many managers to fence areas to protect wildlife from introduced predators. However, conservation fencing is expensive, restrictive and exacerbates prey naïveté reducing the chance of future co‐existence between native prey and introduced predators. Here, we ask whether two globally threatened mammal species protected in fenced reserves, with a history of predation‐driven decline and reintroduction failure, could co‐exist with introduced predators. We defined co‐existence as population persistence for at least 3 years and successful recruitment. We manipulated the density of feral cats within a large fenced paddock and measured the impact on abundance and reproduction of 353 reintroduced burrowing bettongs and 47 greater bilbies over 3 years. We increased cat densities from 0.038 to 0.46 per square km and both threatened species survived, reproduced and increased their population size. However, a previous reintroduction trial of 66 bettongs into the same paddock found one red fox (Vulpes vulpes), at a density of 0.027 per square km, drove the bettong population extinct within 12 months. Our results show that different predator species vary in their impact and that despite a history of reintroduction failure, threatened mammal species can co‐exist with low densities of feral cats. There may be a threshold density below which it is possible to maintain unfenced populations of reintroduced marsupials. Understanding the numerical relationships between population densities of introduced predators and threatened species is urgently needed if these species are to be re‐established at landscape scales. Such knowledge will enable a priori assessment of the risk of reintroduction failure thereby increasing the likelihood of reintroduction success and reducing the financial and ethical cost of failed translocations.

Mobility and trade in Mediterranean antiquity: Evidence for an ‘Italian connection’ in Mycenaean Greece revealed by ancient DNA of livestock

The Late Bronze Age (ca. 1700/1600–1050 BCE) in the Aegean started with strong connections between societies in the region and beyond, and was accompanied by the collapse of palatial polities around 1200 BCE. The collapse led to unrest and migration in the East Mediterranean. In the present study, we focus on settlement contexts dating to the transition between the Mycenaean palatial and post-palatial periods (ca. 1250–1050 BCE) in Greece, which saw the destruction of the Mycenaean palaces (ca. 1200 BCE). We aim to shed light on trade connections and mobility in the region during this substantial period through ancient DNA of livestock.We sequenced pig and cattle mitochondrial DNA (mtDNA) from Tiryns, Greece - a key Bronze Age site in the Aegean region. We discovered an Italian pig haplotype in palatial Tiryns. This is the first time that this particular haplotype is found outside Italy. By contrast, a genetic haplotype of Near Eastern descent (Y1) that was present in the Mycenaean palatial period cannot be ascertained in the post-palatial period. Whether comparable changes in the composition of livestock are also to be found in cattle, we are not able to say, because only the palatial period samples yielded ancient DNA.The results of this study corroborate the published data on mtDNA of pigs from the Mediterranean Basin from the Bronze and Iron Ages. They suggest that in the Mediterranean, pigs were translocated through various patterns of mobility; by Italian migrants to Mycenaean Greece as well as by other mobile groups (“Sea Peoples”) to the Levant.Ancient DNA is a powerful tool to reveal ancient translocations of species, and pigs serve a good proxy for tracing patterns of human mobility and interconnections.

Agency Coordination of Private Action

This Article explores the previously overlooked role of relational contracting in forming and maintaining public-private partnerships. Relational contracting generally describes firms using formal but legally non-binding agreements to collaborate on shared objectives. Why do parties invest in forming elaborate contracts that they do not—and cannot—enforce in court? Contract theory suggests that the very act of contracting is relationship-building; it generates commitment, trust, cooperation, a win-win philosophy, and strengthened communication. Writing down goals and intentions allows parties to clarify expectations while maintaining flexibility for unforeseen conditions. This Article demonstrates that agencies also use relational contracting— creating unenforceable written agreements to build relationships with external actors. To shed light on agencies’ use of relational contracting, this Article provides a novel review of the recovery planning process required by the Endangered Species Act. A surprising finding emerges: private groups are providing crucial resources and logistical support to prevent the extinction of endangered species. Tribes, states, nongovernmental organizations, and sportsmen’s groups are providing necessary resources to further agency action. By orchestrating private action through recovery planning documents, the agency can garner the resources necessary to undertake species translocations, which it could not unilaterally facilitate. Although the plans are not judicially enforceable, they nevertheless play a coordinating and commitment-generating role in facilitating private actors to engage in recovery efforts. This example highlights the broader trend of relational contracting building and formalizing relationships between agency and non-agency actors. Environmental impact statements, forest management plans, and recovery plans for endangered species are all examples of such “relational contracts” governing inter-agency and private-public collaborations. Viewed in this light, seemingly prosaic planning documents are, in fact, a crucial component in facilitating many agency collaborations. Descriptively, this account adds institutional detail to literatures on new governance and public-private partnerships. Normatively, it raises questions about whether the benefits of contracting offsets the potential distributional inequities and mechanisms to shroud government actions created by the practice.

Re-opening the case of Frankenflora: Evidence of hybridisation between local and introduced Protea species at Van Stadens Wildflower Reserve

The lack of examples of hybridisation within South African Cape Fynbos lineages gives the impression that interspecific hybridisation events may be rare in this system. If this is the case, then long-distance translocations of plant species across the Cape are unlikely to have any impact on the genetic component of biodiversity. Here we demonstrate that local populations of Protea eximia have hybridised with the non-local and introduced Protea susannae at Van Stadens Wildflower Reserve using morphological and genetic data; DNA sequence data were obtained from the internal transcribed spacer from the nuclear ribosomal cistron and a noncoding region of the chloroplast. Of the 24 plants from the reserve that were analysed, 11 were identified as hybrids, and comparing nuclear and chloroplast signals indicated bidirectional gene-flow between these species. This is the first study demonstrating the potential threat of long-distance dispersal in a Cape lineage to the genetic integrity of local populations.

Independent contributions of threat and popularity to conservation translocations

Species translocations are popular tools in conservation, but may be increasingly motivated by species’ popularity, rather than their threat status. We analyzed relative contributions of threat status (a surrogate for extinction risk) and popularity (an estimate of the degree of public knowledge, awareness or notoriety) to the likelihood of developing translocation projects for a representative whole regional fauna (174 conservation translocations during the last two decades for 82 out of the 527 species of Spanish terrestrial vertebrates). Three measures of threat status were obtained from technical (IUCN) and legal sources. Popularity estimates were obtained from body size data and two different Internet search protocols. All combinations of the three factors used to estimate threat status were correlated, as were the three indicators of species popularity (internet popularity indexes and body mass). Selected estimates unbiasedly captured differences in both threat and popularity among species. Threat and popularity were only weakly correlated, as expected when considering faunas as a whole rather than the better-studied subsets. Threat status and popularity had significant and equivalent contributions to explain the development of conservation translocations. Popularity, or lack thereof, partly explained the development of projects for non-threatened but popular species, as well as the lack of projects for several highly endangered species unknown by the public. Observed mismatches between technical and social criteria can be prevented by (a) strict separation of conservation translocations from translocations directed to cover other social demands or (b) development of explicit, quantitative decision-making criteria aimed at rigorous ex-ante evaluations of translocations.

Establishment success and persistence of threatened plant translocations in south west Western Australia: an experimental approach

Establishment of viable threatened plant populations through translocations presents significant practical and logistical challenges. To address these challenges there is a need for experimental studies that inform refinement of translocation methodologies to optimise seedling survival during the establishment phase. In the present study we investigated the effect of three post planting techniques on the survival and growth of six translocated threatened plant species in south-west Western Australia over a 10-year period. Planted seedlings received summer watering for the first year, mulch or protection from vertebrate herbivores. Survival of seedlings was significantly enhanced in both watering and fencing treatments, but was not positively influenced by the mulch treatment. Plant growth was also significantly improved by the fencing treatment. Results showed that both fencing and supplementary summer watering were two very effective approaches for enhancing seedling establishment and plant persistence. We emphasise the value of integrating an experimental approach involving long-term monitoring into threatened plant species translocations and recovery programs for improving plant translocation success.

Native and invasive taxa on the Pacific coast of South America: Impacts on aquaculture, traceability and biodiversity of blue mussels (Mytilus spp.)

AbstractGaining new knowledge of the native distributions of species (phylogeography) is more and more difficult in a world affected by anthropogenic disturbance, in particular by species translocations. Increasingly, molecular markers are required to support decisions about the taxonomy of native vs. introduced species, and the existence of their hybrids, to answer phylogeographic questions. In many fields, including aquaculture, traceability and food security, taxonomic and phylogeographic knowledge is key to the successful management and conservation of biodiversity. The Pacific coast of Chile is one of the last regions without a clear and agreed understanding of the taxonomy and systematics of smooth‐shelled blue mussels of the genus Mytilus. A panel of 49 bi‐allelic single nucleotide polymorphisms (SNPs) was genotyped in 338 Mytilus individuals collected from nine Chilean and five reference populations. All analyses confirmed the hypothesis that the native Chilean blue mussel is genetically distinct from the reference species M. edulis, M. galloprovincialis and M. trossulus. These results support the hypothesis of a unique evolutionary history of the native Chilean blue mussel on the Pacific coast of South America. It is therefore concluded that the native blue mussel from Chile should be recognized as M. chilensis Hupé 1854. We confirmed a recent Mediterranean origin of introduced M. galloprovincialis on the coast of Chile. This knowledge advances the understanding of global phylogeography of blue mussels and their bioinvasions and harmonizes taxonomy in the context of aquaculture production, seafood traceability, labelling and trade.

New occurrence of a non-native ornamental cichlid in the Paranapanema River, southern Brazil

Fish introductions are common practices due to intentionally or unintentionally translocations of species between watersheds. Herein we report the spread of the non-native cichlid Laetacara araguaiae Ottoni & Costa 2009 in the Paranapanema River basin, southern Brazil. Native from the Araguaia River (Central Brazil), this species was probably introduced by releases made by aquarists. Its new area of occurrence is characterized as natural nursery and important for the life cycle of native fish. Due to its biological characteristics, the species has the ability to cause a negative impact on the aquatic biota through possible interactions, such as predation of eggs, larvae and juveniles of native fish, and spread of parasites.Keywords: biological invasion, Cichlinae, fish, exotic species, Upper Paraná River basin.

Genome scale assessment of a species translocation program

Despite increased use of species translocations, controversy remains regarding the efficacy and efficiency of the strategy in obtaining conservation goals. Much of this controversy results from vague program objectives, unclear definitions of success, and lack of follow-up monitoring. We used the translocation program initiated by Zoo Knoxville for the federally threatened Bog Turtle (Glyptemys muhlenbergii) as a case study to demonstrate how genomic assessments not only assess the success of program objectives, but also allow managers to quickly obtain baseline data from which program objectives and explicit definitions of ‘success’ can be determined. Here we used 7030 SNP markers derived from RADseq data to confirm the premise that different source populations are genetically differentiated. Then we tested whether the release population has enhanced genetic diversity, as expected from a deliberate admixture. Although the release population had greater diversity than any source population, variation was lower than expected from modeling admixture with equal source contribution. Our results support the premise that genetic diversity can be maximized by including representatives from as many natural populations as possible. But failure to achieve the expected level of diversity could result from nonrandom success of founders from different sources or unrecorded bias in the implementation of the release program. Many existing and future translocation programs would benefit from genetic assessment similar to that conducted here with Bog Turtles.

Seed ecology informs restoration approaches for threatened species in water-limited environments: a case study on the short-range Banded Ironstone endemic Ricinocarpos brevis (Euphorbiaceae)

Translocation of threatened species is challenging in semiarid environments, especially when seeds are the principal means of in situ establishment. Worldwide, the overall success of translocations using seeds is highly variable and generally unpredictable. Most seed-based translocations are embarked upon with limited understanding of the species’ seed biology or the nuances of the local abiotic environment in which to guide restoration approaches. For instance, within Australia just 14% of threatened species translocations use directly sown seeds and consequently, to improve the chances of restoration success, both the seed biology and the influence of the abiotic environment need to be adequately understood. We investigated these aspects in Ricinocarpos brevis R.J.F.Hend. & Mollemans – a short-range Banded Ironstone endemic – by focusing on a series of laboratory and field experiments to understand the key drivers of dormancy alleviation and germination promotion, as well as in-situ conditions of natural and recipient translocation sites. Fresh seeds were found to have high viability, fully developed linear embryos and possess physiological dormancy, with enhanced germination when exposed to smoke water, karrikinolide (KAR1) and gibberellic acid (GA3). Under laboratory conditions, seeds germinated over a range of temperatures (15−30°C), but germination was suppressed by light and highly sensitive to water stress. Seeds had reduced germination when sown on the soil surface, but could emerge from up to 13 cm in depth. Under field conditions, in-situ emergence was <2%. Using in-situ emergence results, soil loggers and rainfall data, we developed a model of the recruitment bottlenecks faced by this species under in-situ conditions, an approach that provides useful insights to assist future translocations. Understanding seed biology and seed ecology enables better insights into the principal bottlenecks restricting in-situ emergence and consequently restoration success, leading to the development of more effective approaches for conserving other threatened flora in future.

Biodiversity monitoring by community‐based restoration groups in New Zealand

SummaryIn recent decades, community groups have transformed habitat restoration, pest control and species translocations in New Zealand. Large areas of wild New Zealand benefit hugely from ongoing management by community‐based restoration groups. Areas near cities and towns have especially good access to pools of keen volunteers. Community groups are involved in monitoring progress with their work, as well as monitoring biodiversity changes in general at their project sites. New tools powered by modern technologies are creating the opportunity for New Zealand's community volunteers to play a transformative role in biodiversity monitoring for either purpose. These tools are reducing the resources and expertise required for species detection and identification. Smartphones with cameras, GPS, audio recorders and data apps make it easier than ever to record species observations. Crowd‐sourced identification of species in photographs and sounds loaded onto NatureWatch NZ allow volunteers to make observations of a much wider range of taxa than just common birds and trees. Realising this potential requires community groups, scientists and their institutions to collaborate in building and maintaining simple, accessible monitoring systems that (i) require and promote standard monitoring methods, (ii) provide efficient data entry in standard formats, (iii) generate automated results of use to community groups and (iv) facilitate public sharing of data to contribute to regional, national and global biodiversity monitoring. Some New Zealand monitoring systems developed recently to assist community‐based restoration groups with monitoring mammalian predator control are good examples of this approach. Making this happen at a large scale across many community groups and taxa requires increased and coordinated long‐term institutional support for monitoring systems and training.

Human and Non-Human Migration: Understanding Species Introduction and Translocation through Migration Ethics

Despite the propensity of species introductions to disrupt ecosystems through community disassembly, the use of species translocations is becoming more widely accepted. In this paper, we examine ethical investigations into human migration in an attempt to evaluate how translocation may be justified. Previous attempts to make the analogy between human and species migration have been prone to black and white thinking. We argue that the disagreement between nativist and cosmopolitan approaches to introduced species can be defused by extending the analogy through the migration ethics literature. Additionally, by extending the discussion to the special status of refugees, we are able to develop a theoretical framework for species migrations that acknowledges the risk of species introduction while recognising that special obligations towards endangered species may necessitate the use of translocations.

The alien's identity: consequences of taxonomic status for the international bumblebee trade regulations

The species international trade leads to multiple non-native invasions. Besides species invasions, commercial exchanges may also contribute to translocation between closely related taxa or allopatric populations. Consequently, preserving endemic taxa and specificity of local populations require to regulate commercial translocations of species or populations. To be efficient such regulation needs a resolved taxonomy and a thorough analysis of the population structure of native taxa/populations. To provide guidelines for an efficient regulation of the trade of Bombus terrestris within its natural range, we analyzed its taxonomy and its population structure using an integrative taxonomic approach. Our results show that B. terrestris translocations involve two species, three subspecies, and several populations with weak differentiation. These different levels of differentiation imply specific and appropriate regulations of translocations with different levels of prioritization. We ultimately assess the relevance of current policies and propose potentially efficient regulations for policy-makers. Such integrative taxonomic approach should be used in other traded polytypic species.

The Role of Animal Translocations in Conserving British Wildlife: An Overview of Recent Work and Prospects for the Future.

We provide an overview of terrestrial animal translocations carried out for conservation purposes in Britain, summarising what has been achieved in recent decades and discussing the issues raised by this approach to conservation. In the last 40years, at least nine species have been reintroduced following extinction in Britain (or at least one country within Britain), including five birds, one mammal, one amphibian and two invertebrates. Many more species have been translocated within Britain to establish additional populations in order to improve conservation status. We discuss the guidelines and protocols used to assess translocation projects in Britain, notably the IUCN guidelines, most recently revised in 2013. We also discuss the likely use of species translocations in future and suggest that, in our increasingly fragmented landscapes, they will have an important role to play in conservation restoration, especially for animals with limited mobility. Moving species around is a complex undertaking and our understanding of the inherent risks involved, including the risks from disease, has improved significantly in recent years. Conservation translocations should be considered in the context of species recovery targets and high standards should be maintained so that disease risks and other potentially negative impacts are minimised.

Using DNA profiling to investigate human-mediated translocations of an invasive species

The reconstruction of invasion history is the goal or foundation of many investigations of biological invasions. This study applies DNA profiling to investigate the sources and vectors of new propagules, to detect illegal human-mediated translocations and to improve the management of invasions by identifying invasion pathways that can be targeted for more stringent control. We use the European invasion of the American Eastern grey squirrel as a focal example. Many human-mediated translocations of this species have occurred in Europe since the 19th century. We built a genotype database of 1421 individuals from 59 locations across Europe and one in the USA, with each individual genotyped at 12 highly polymorphic microsatellites. DNA from newly detected populations and individuals of unknown sources were compared with this database. Our results indicated illegal human-mediated translocations in Aberdeen, the Isle of Skye and Northumberland in the UK, and revealed precise details of illegal squirrel trade in Italy. We recommend that multi-locus genotype databases be set up for all major invasive species considered attractive or ornamental, as these are often subject to illegal translocations through human actions such as the pet trade.