Use of Population Viability Analysis to Evaluate CITES Trade‐Management Options for Threatened Marine Fishes

Abstract: Achieving multiple conservation objectives can be challenging, particularly under high uncertainty. Having agreed to limit seahorse (Hippocampus) exports to sustainable levels, signatories to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) were offered the option of a single 10‐cm minimum size limit (MSL) as an interim management measure for all Hippocampus species (≥34). Although diverse stakeholders supported the recommended MSL, its biological and socioeconomic implications were not assessed quantitatively. We combined population viability analysis, model sensitivity analysis, and economic information to evaluate the trade‐off between conservation threat to and long‐term cumulative income from these exploited marine fishes of high conservation concern. We used the European long‐snouted seahorse (Hippocampus guttulatus) as a representative species to compare the performance of MSLs set at alternative biological reference points. Our sensitivity analyses showed that in most of our scenarios, setting the MSL just above size at maturity (9.7 cm in H. guttulatus) would not prevent exploited populations from becoming listed as vulnerable. By contrast, the relative risk of decline and extinction were almost halved—at a cost of only a 5.6% reduction in long‐term catches—by increasing the MSL to the size reached after at least one full reproductive season. On the basis of our analysis, a precautionary increase in the MSL could be compatible with sustaining fishers' livelihoods and international trade. Such management tactics that aid species conservation and have minimal effects on long term catch trends may help bolster the case for CITES trade management of other valuable marine fishes.     

Realities of offering advice to governments on CITES

What happens when those who provide conservation advice are required to take policy and management action based on that advice? Conservation advocates and scientists often try to prompt regulatory change that has significant implications for government without facing the challenge of managing such change. Through a case study, we placed ourselves in the role of the government of Thailand, facing obligations to seahorses (Hippocampus spp.) under the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). These obligations include ensuring that its exports of seahorses do not damage wild populations. We applied a CITES-approved framework (which we developed) to evaluate the risks of such exports to 2 seahorse species. We used the framework to evaluate the pressures that put wild populations of the species at risk; whether current management mitigates the risk or offsets these pressures; and whether the species is responding as hoped to management policy. We based our analysis on information in published and grey literature, local knowledge, citizen science data, results of government research, and expert opinion. To meet CITES obligations, exports of both species would need to be prohibited until more precautionary adaptive management emerged. The risk of any exports of Hippocampus trimaculatus was above a tolerable level because of a lack of appropriate management to mitigate risks. In contrast, the risk of any exports of Hippocampus kuda could become tolerable if monitoring were put in place to assess the species’ response to management. The process we developed for Authorities to determine risk in response to CITES guidelines was challenging to implement even without the need for government to consider social implications of conservation action. Despite the imperfections of our risk evaluation, however, it still served to support adaptive management. Conservationists need to keep implementation in mind when offering advice.     

Discrepancies in Reported Levels of International Wildlife Trade

Abstract:  The international wildlife trade is a principal cause of biodiversity loss, involving hundreds of millions of plants and animals each year, yet wildlife trade records are notoriously unreliable. We assessed the precision of wildlife trade reports for the United States, the world's largest consumer of endangered wildlife, by comparing data from the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) with U.S. Customs data. For both U.S. imports and exports, CITES and Customs reported substantially different trade volumes for all taxa in all years. Discrepancies ranged from a CITES-reported volume 376% greater than that reported by Customs (live coral imports, 2000) to a Customs' report 5202% greater than CITES (conch exports, 2000). These widely divergent data suggest widespread inaccuracies that may distort the perceived risk of targeted wildlife exploitation, leading to misallocation of management resources and less effective conservation strategies. Conservation scientists and practitioners should reexamine assumptions regarding the significance of the international wildlife trade.     

Comparative Analysis of Management Regimes and Medicinal Plant Trade Monitoring Mechanisms for American Ginseng and Goldenseal

Abstract: Two popular and profitable native North American medicinal plants, American ginseng (    Panax quinquefolius ) and goldenseal (   Hydrastis canadensis ), both of which are listed in Appendix 2 of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), are monitored under disparate domestic strategies that are designed to satisfy CITES requirements. The P. quinquefolius program has benefited the species by encouraging U.S. states to enact laws to protect wild populations and regulate collection, and by establishing a transparent system under which harvest, commerce, and export can be monitored, evaluated, and controlled routinely. But certain programmatic constraints, such as insufficient funding and gaps in biological monitoring, undermine its effectiveness as a management strategy for the species. The joint industry and government H. canadensis initiative is intended to give commercial traders more responsibility in monitoring plant trade and the federal government access to information that may otherwise be difficult to obtain without the help of traders. I examined the structure, successes, and deficiencies of the P. quinquefolius program, promising features of the evolving H. canadensis program, Turkey's management of geophytes, and other sources of information from federal agencies that might contribute to more effective management of medicinal plants in the United States. Although the main goal of domestic monitoring programs for P. quinquefolius and H. canadensis is to implement their CITES listings, it is conceivable that similar programs could be established for non–CITES medicinal plants, thereby minimizing or replacing the need for CITES protection.     

Prevalence and perspectives of illegal trade in cacti and succulent plants in the collector community

Although illegal wildlife trade (IWT) represents a serious threat to biodiversity, research into the prevalence of illegal plant collection and trade remains scarce. Because cacti and succulents are heavily threatened by overcollection for often illegal, international ornamental trade, we surveyed 441 members of the cacti and succulent hobbyist collector community with a mixed quantitative and qualitative approach. We sought to understand collector perspectives on the Convention on the International Trade in Endangered Species of Wild Flora and Fauna (CITES) and on the threats IWT poses to cactus and succulent conservation. Most respondents (74% of 401 respondents) stated that illegal collection in cacti and succulents represents a “very serious problem” and that the problem of wild plant collection is increasing (72% of 319 respondents). Most forms of illegal collection and trade were seen as very unacceptable by respondents. Self-reported noncompliance with CITES rules was uncommon (11.2% of 418 respondents); it remains a persistent problem in parts of the cacti and succulent hobbyist community. People engaging in rule breaking, such as transporting plants without required CITES documents, generally did so knowingly. Although 60.6% of 381 respondents regarded CITES as a very important tool for conservation, sentiment toward CITES and its efficacy in helping species conservation was mixed. Collectors in our survey saw themselves as potentially playing important roles in cactus and succulent conservation, but this potential resource remains largely untapped. Our results suggest the need for enhanced consultation with stakeholders in CITES decision-making. For challenging subjects like IWT, developing evidence-based responses demands deep interdisciplinary engagement, including assessing the conservation impact of species listings on CITES appendices.     

International Trade Status and Crisis for Snake Species in China

Abstract:  In recent years, the purchase of snakes for leather, food, and traditional medicine has increased in China, which has greatly reduced certain snake populations. Trade records show that since the 1990s, with respect to some species of snakes, China is changing from a net export country to a net import country. We analyzed data on international trade in snake species, concentrating, in particular, on trade dynamics and species composition. The overall number of snakes exported appears to have decreased in the last 10 years. However, the number of snakes imported during this period has increased steadily. Many species of snakes that are traded in significant numbers are endangered or threatened species. To conserve snakes in China, we recommended that the Chinese government and the international conservation community take the following actions: enhance legislation and list several species in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) appendices; register all snake farms in China; carry out population and market surveys; monitor the dynamics of trade; encourage biological research; encourage change in food habits; and enhance cooperation between Hong Kong and mainland China.     

Global Trade in Exotic Pets 2006–2012

International trade in exotic pets is an important and increasing driver of biodiversity loss and often compromises the standards required for good animal welfare. We systematically reviewed the scientific and gray literature and used the United Nations Environment Programme ‐ World Conservation Monitoring Centre (UNEP‐WCMC) Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) trade database to establish temporal and geographical trade patterns of live exotic birds, mammals, and reptiles and to describe trends in research, taxonomic representation, and level of threat and legal protection of species traded. Birds were the most species‐rich and abundant class reported in trade; reptiles were second most abundant but unusually the most studied in this context; and mammals were least abundant in trade. Mammalian and reptilian species traded as pets were more likely to be threatened than expected by random. There have been a substantial number of Appendix I listed captive‐bred mammals and birds and wild‐caught birds and reptiles reported in trade to CITES. We identified the Middle East's emerging role as a driver of demand for exotic pets of all taxa alongside the well‐established and increasing role of South America and Southeast Asia in the market. Europe, North America, and the Middle East featured most heavily in trade reports to CITES, whereas trade involving South America and Southeast Asia were given most emphasis in the literature. For effective monitoring of and appropriate response to the international exotic pet trade, it is imperative that the reliability and detail of CITES trade reports improve and that scientific research be directed toward those taxa and locations that are most vulnerable. El Mercado Global de Mascotas Exóticas 2006‐2012     

Gaining Traction: Retreading the Wheels of Marine Conservation

Abstract:  A number of international treaties address the conservation of marine resources. The declining state of the world's oceans suggests that these treaties are not succeeding and could use improvement. The Convention on International Trade in Endangered Species (CITES) is increasingly embracing the conservation of marine species. We examine the evolution of marine species protection under CITES and illuminate some of the mechanisms used and challenges faced in implementing CITES protection. We found that clarification is needed on when and where CITES applies and how CITES should work with other treaties and institutions. The Society for Conservation Biology (SCB) can contribute to increased effectiveness of CITES for marine conservation. Foremost, the SCB community could foster dialogue on creating a broad vision of how CITES should apply to marine species and how it can synergistically interact with other important marine-conservation treaties and institutions. More specific contributions could focus on defining listing criteria for marine species, improving the science behind the nondetriment finding, and offering technical guidance on species proposals. A future role for SCB could be to contribute to the enhanced effectiveness of other marine conservation agreements such as the Convention on the Conservation of Migratory Species of Wild Animals, the International Whaling Commission, and the United Nations Convention on the Law of the Sea .     

Body size preferences in the pot-bellied seahorse <Emphasis Type="Italic">Hippocampus abdominalis:</Emphasis> choosy males and indiscriminate females

Male seahorses (genus Hippocampus) provide all post-fertilization parental care, yet despite high levels of paternal investment, these species have long been thought to have conventional sex roles, with female mate choice and male–male competition. Recent studies of the pot-bellied seahorse (Hippocampus abdominalis) have shown that sex-role reversal occurs in high-density female-biased populations, indicating that male mating preferences may lead to sexual selection on females in this species. Egg size, egg number, and offspring size all correlate positively with female body size in Hippocampus, and by choosing large mating partners, male seahorses may increase their reproductive success. While male brood size is also positively correlated with body size, small H. abdominalis males can carry exceptionally large broods, suggesting that the fecundity benefits of female preference for large partners may be limited. We investigated the importance of body size in reproductive decisions of H. abdominalis, presenting focal individuals of both sexes with potential mating partners of different sizes. Mating preferences were quantified in terms of time spent courting each potential partner. Male seahorses were highly active throughout the mate-choice trials and showed a clear behavioral preference for large partners, while females showed significantly lower levels of activity and equivocal mating preferences. The strong male preferences for large females demonstrated here suggest that sexual selection may act strongly on female body size in wild populations of H. abdominalis, consistent with predictions on the importance of female body size for reproductive output in this species. An erratum to this article can be found at     

Using cumulative human-impact models to reveal global threat patterns for seahorses

Understanding threats acting on marine organisms and their conservation status is vital but challenging given a paucity of data. We studied the cumulative human impact (CHI) on and conservation status of seahorses (Hippocampus spp.)—a genus of rare and data-poor marine fishes. With expert knowledge and relevant spatial data sets, we built linear-additive models to assess and map the CHI of 12 anthropogenic stressors on 42 seahorse species. We examined the utility of indices of estimated impact (impact of each stressor and CHI) in predicting conservation status for species with random forest (RF) models. The CHI values for threatened species were significantly higher than those for nonthreatened species (category based on International Union for Conservation of Nature Red List). We derived high-accuracy RF models (87% and 96%) that predicted that 5 of the 17 data-deficient species were threatened. Demersal fishing practices with high bycatch and pollution were the best predictors of threat category. Major threat epicenters were in China, Southeast Asia, and Europe. Our results and maps of CHI may help guide global seahorse conservation and indicate that modeling and mapping human impacts can reveal threat patterns and conservation status for data-poor species. We found that for exploring threat patterns of focal species, species-level CHI models are better than existing ecosystem-level CHI models.     

Association of reproductive traits with captive- versus wild-sourced birds in trade

The wildlife trade is a billion-dollar global business, involving millions of people, thousands of species, and hundreds of millions of individual organisms. Unravelling whether trade targets reproductively distinct species and whether this preference varies between captive- and wild-sourced species is a crucial question. We used a comprehensive list of all bird species traded, trade listings and records kept in compliance with the Convention on International Trade in Endangered Species (CITES), and a suite of avian reproductive parameters to examine whether wildlife trade is associated with particular facets of life history and to examine the association between life-history traits and captive- and wild-sourced traded volumes over time. Across all trade, CITES listing, and CITES trade, large birds were more likely to be traded and listed, but their longevity and age at maturity were not associated with CITES listing or trade. We found species across almost the full range of trait values in both captive and wild trade between 2000 and 2020. Captive trade volumes clearly associated with relatively longer lived and early-maturing species; these associations remained stable and largely unchanged over time. Trait–volume associations in wild-sourced trade were more uncertain. Only body mass had a clear association, and it varied from negative to positive over time. Although reproductive traits were important in captive-sourced trade, species-level variation dominated trade, with even congeneric species varying greatly in volume despite similar traits. The collection and incorporation of trait data into sustainability assessments of captive breeding facilities are crucial to ensure accurate quotas and guard against laundering.     

Experimental Demonstration of an Allee Effect in American Ginseng

Abstract: Harvesting of wild American ginseng (   Panax quinquefolius ) for the herbal trade has lowered natural population sizes. We tested for reproductive limitation due to small population size (a form of the Allee effect) by experimentally planting "natural" populations numbering 4, 16, and 64 using 4-year-old cultivated plants. Plant size traits and reproductive traits ( bud, flower, green fruit, and mature fruit) were recorded through the ensuing summer. Fruit production per flower and per plant increased in proportion to flowering population size (  p = 0.0063 and p = 0.0017, respectively), strongly suggesting that an Allee effect occurs in very small populations. The increase in fruit production was not explained by either plant or inflorescence size differences. Although population size-dependent pollination, through insufficient pollinator visitation rate or pollen transfer rate, seems the most likely cause of the observed effects, our limited observations of pollinators were not sufficient to demonstrate a change in pollination rates as a function of population size. Knowledge of the presence as well as the mechanism underlying this Allee effect may be especially useful for management and determination of minimum viable population size of the species in the wild.     

A Global Indicator for Biological Invasion

Abstract:  "Trends in invasive alien species" is one of only two indicators of threat to biodiversity that form part of the Convention on Biological Diversity's (CBD) framework for monitoring progress toward its "2010 target" (i.e., the commitment to achieve by 2010 a significant reduction in the current rate of biodiversity loss). To date, however, there is no fully developed indicator for invasive alien species (IAS) that combines trends, derived from a standard set of methods, across species groups, ecosystems, and regions. Here we provide a rationale for the form and characteristics of an indicator of trends in IAS that will meet the 2010 framework goal and targets for this indicator. We suggest single and composite indicators that include problem-status and management-status measures that are designed to be flexible, readily disaggregated, and as far as possible draw on existing data. The single indicators at national and global scales are number of IAS and numbers of operational management plans for IAS. Global trends in IAS are measured as the progress of nations toward the targets of stabilizing IAS numbers and the implementation of IAS management plans. The proposed global indicator thus represents a minimum information set that most directly addresses the indicator objective and simultaneously aims to maximize national participation. This global indicator now requires testing to assess its accuracy, sensitivity, and tractability. Although it may not be possible to achieve the desired objective for a global indicator of biological invasion by 2010 as comprehensively as desired, it seems possible to obtain trend estimates for a component of the taxa, ecosystems, and regions involved. Importantly, current indicator development initiatives will also contribute to developing the mechanisms necessary for monitoring global trends in IAS beyond 2010.     

Implementing CITES regulations for timber.

Foresters are currently confronted with a new challenge. For the first time a commonly traded timber species has been listed on the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). At the 12th Conference of the Parties in November 2002, countries voted 68 to 30 to place the premier timber species of Latin America, big-leaf mahogany (Swietenia macrophylla King [Meliaceae]), on CITES Appendix II. Under Appendix II regulations, trade in mahogany requires that exporting countries verify that each shipment was legally obtained and that its harvest was non-detrimental to the survival of the species. Unfortunately, implementation has been weak, in part because countries have yet to develop a common, pragmatic, cost-effective system to make the legal and non-detriment findings. This paper recommends what such a system might include.     

Amplifying Nuclear and Mitochondrial DNA from African Elephant Ivory: a Tool for Monitoring the Ivory Trade

Abstract:   The ability to extract DNA from ivory provides the basis for genetically tracking the origin of poached ivory and thus has important implications for elephant conservation and management. We describe a method to isolate and amplify both genomic and mitochondrial DNA from African elephant ivory that requires very small amounts of ivory taken from any location on the tusk. We pulverized ivory and isolated DNA with a modified QIAamp kit. Ivory as old as 10 to 20 years, stored at ambient conditions, was amenable to DNA isolation with this method. The isolated DNA was robustly amplified at 16 elephant microsatellite loci and two mitochondrial DNA loci. This method has important applications for the forensic analysis of poached African elephant ivory. It enables determination of where stronger antipoaching efforts are needed and provides the basis for monitoring the extent of the trade as well as the consequences of future international trade decisions.     

A Retrospective Evaluation of the Global Decline of Carnivores and Ungulates

Assessing temporal changes in species extinction risk is necessary for measuring conservation success or failure and for directing conservation resources toward species or regions that would benefit most. Yet, there is no long‐term picture of genuine change that allows one to associate species extinction risk trends with drivers of change or conservation actions. Through a review of 40 years of IUCN‐related literature sources on species conservation status (e.g., action plans, red‐data books), we assigned retrospective red‐list categories to the world's carnivores and ungulates (2 groups with relatively long generation times) to examine how their extinction risk has changed since the 1970s. We then aggregated species’ categories to calculate a global trend in their extinction risk over time. A decline in the conservation status of carnivores and ungulates was underway 40 years ago and has since accelerated. One quarter of all species (n = 498) moved one or more categories closer to extinction globally, while almost half of the species moved closer to extinction in Southeast Asia. The conservation status of some species improved (toward less threatened categories), but for each species that improved in status 8 deteriorated. The status of large‐bodied species, particularly those above 100 kg (including many iconic taxa), deteriorated significantly more than small‐bodied species (below 10 kg). The trends we found are likely related to geopolitical events (such as the collapse of Soviet Union), international regulations (such as CITES), shifting cultural values, and natural resource exploitation (e.g., in Southeast Asia). Retrospective assessments of global species extinction risk reduce the risk of a shifting baseline syndrome, which can affect decisions on the desirable conservation status of species. Such assessments can help conservationists identify which conservation policies and strategies are or are not helping safeguard biodiversity and thus can improve future strategies. Una Evaluación Retrospectiva de la Declinación Global de Carnívoros y Ungulados     

Effects of a Proposed Ex Situ Conservation Program on In Situ Conservation of the Babirusa, an Endangered Suid

Abstract: Detailed data are rarely available to show how interventions such as captive breeding programs can create an uncontrolled demand for live specimens of endangered species. We present a case study of the effect of a planned, internationally recognized captive breeding program on trade in the endangered babirusa wild pig from July to December 1998. Although the program had not yet begun, international interest in the captive breeding of babirusas gave hunters and dealers the false impression that there was a potentially lucrative and officially sanctioned national and international demand for any live babirusas they might catch. Swift action by the Indonesian authorities halted this trade, but the study provides a warning about the damage that can be caused to the conservation of a species if management programs are instituted without a full understanding of the practicalities of its conservation, particularly interactions between the species and local people.     

Morphology and kinematics of prey capture in the syngnathid fishes Hippocampus erectus and Syngnathus floridae

The mechanism of prey capture in two syngnathid fishes, the lined seahorse Hippocampus erectus (Perry) and the dusky pipefish Syngnathus floridae (Jordan and Gilbert), is described based on anatomical observations and high-speed video recordings (200 and 400 images s⁻¹) of feeding events by four seahorses and three pipefish. The fish were collected near Turkey Point, Florida, U.S.A., in January 1994 to March 1995. The dominant features of the morphology of these and many other syngnathiform fishes include extreme elongation of the suspensorium and neurocranium with a small mouth located at the anterior tip of the head. In the seahorse, a preparatory phase of prey capture consisted of slow ventral head flexion. This was followed by rapid elevation of the head and snout as the prey was drawn into the mouth by suction. Both H. erectus and S. floridae capture prey rapidly, with peak head excursions and mouth opening occurring within 5 to 7 ms of the onset of the strike. There was no upper jaw protrusion. In both species the time to recovery of the cranium and hyoid apparatus to resting positions was highly variable but took at least 500 ms. Manipulations of freshly dead specimens indicated a biomechanical linkage between head elevation and hyoid depression. However, the predictions of a previously proposed four-bar linkage model that couples hyoid depression to head elevation were not fully supported by kinematic data from one seahorse, suggesting that additional linkages act during the expansive phase of prey capture. These species exhibit the generalized kinematic pattern of prey capture in bony fishes, with head elevation, hyoid depression and mouth opening occurring almost simultaneously. The derived morphology results in a unique feeding behav‐ior, in which prey are captured during a sudden up-swing of the head, which brings the mouth to the prey. Suction is used to draw the prey into the buccal cavity. Received: 4 August 1996 / Accepted: 27 August 1996     

Ecological Determinants of Distribution Decline and Risk of Extinction in Moths

Abstract:  For successful conservation of species it is important to identify traits that predispose species to the risk of extinction. By identifying such traits conservation efforts can be directed toward species that are most at risk of becoming threatened. We used data derived from the literature to determine ecological traits that affect distribution, distribution change, and the risk of extinction in Finnish noctuid moths (Lepidoptera, Noctuidae). The ecological traits we examined included body size, larval specificity, length of the flight period, and overwintering stage. In addition, in monophagous species we examined the effects of resource distribution. Larval specificity, length of the flight period, and the overwintering stage each had an independent effect on the risk of extinction when the effects of other traits were controlled by entering all traits into the same regression model. Not a single trait predicted the risk of extinction when analysis was conducted without controlling for the other traits. This discrepancy among the results suggests that a single trait may not be enough to allow prediction of the risk of extinction. Instead, it seems that for successful, predictive conservation science data on several ecological characteristics are needed.     

Estimating Population Size with Noninvasive Capture-Mark-Recapture Data

Abstract:  Estimating population size of elusive and rare species is challenging. The difficulties in catching such species has triggered the use of samples collected noninvasively, such as feces or hair, from which genetic analysis yields data similar to capture-mark-recapture (CMR) data. There are, however, two differences between classical CMR and noninvasive CMR. First, capture and recapture data are gathered over multiple sampling sessions in classical CMR, whereas in noninvasive CMR they can be obtained from a single sampling session. Second, because of genotyping errors and unlike classical CMR, there is no simple relationship between (genetic) marks and individuals in noninvasive CMR. We evaluated, through simulations, the reliability of population size estimates based on noninvasive CMR. For equal sampling efforts, we compared estimates of population size N obtained from accumulation curves, a maximum likelihood, and a Bayesian estimator. For a closed population and without sampling heterogeneity, estimates obtained from noninvasive CMR were as reliable as estimates from classical CMR. The sampling structure (single or multiple session) did not alter the results, the Bayesian estimator in the case of a single sampling session presented the best compromise between low mean squared error and a 95% confidence interval encompassing the parametric value of N in most simulations. Finally, when suitable field and lab protocols were used, genotyping errors did not substantially bias population size estimates (bias < 3.5% in all simulations). The ability to reliably estimate population size from noninvasive samples taken during a single session offers a new and useful technique for the management and conservation of elusive and rare species.