Changes in the trade of bycatch species corresponding to CITES regulations: the case of dried seahorse trade in Thailand

Exploitation for trade is one of the biggest threats to many species, especially for marine fishes. Trade regulations should, therefore, be effective in helping conserve marine fish populations. The Convention of International Trade in Endangered Species of Wild Fauna and Flora (CITES), one of the few multilateral environmental agreements with enforcement capacity, has embraced a number of marine fishes in recent years. However, the impacts of such measures on wildlife trade have rarely been assessed. We conducted a case study of the dried seahorse (Hippocampus spp.) trade in Thailand to understand the trade of these species under CITES regulations. We carried out 203 semi-structured interviews with traders to estimate the economic scale of Thai seahorse trade, and compared perceived changes with official trade datasets. Even though most seahorses were incidentally caught, we estimated that dried seahorses could be worth US$26.5 million per year for Thai fishers. However, the total declared annual export value was only around US$5.5 million, and had decreased to US$1 million in 2013. Considering the economic value of seahorses, the large discrepancy between declared export volumes and catch estimates suggested that trade may be underreported. While official data shows the export volume decreased after the implementation of CITES listing in 2005, our respondents did not report a similar trend. In contrast, the prices of seahorses were reported to be increasing. Our study highlights the economic importance of marine fishes captured as bycatch and the importance of international and domestic management measures for the trade of bycatch species.     

Does a No-Take Marine Protected Area Benefit Seahorses?

Seahorses are iconic charismatic species that are often used to ‘champion’ marine conservation causes around the world. As they are threatened in many countries by over-exploitation and habitat loss, marine protected areas (MPAs) could help with their protection and recovery. MPAs may conserve seahorses through protecting essential habitats and removing fishing pressures. Populations of White''s seahorse, Hippocampus whitei, a species endemic to New South Wales, Australia, were monitored monthly from 2006 to 2009 using diver surveys at two sites within a no-take marine protected areas established in 1983, and at two control sites outside the no-take MPA sites. Predators of H. whitei were also identified and monitored. Hippocampus whitei were more abundant at the control sites. Seahorse predators (3 species of fish and 2 species of octopus) were more abundant within the no-take MPA sites. Seahorse and predator abundances were negatively correlated. Substantial variability in the seahorse population at one of the control sites reinforced the importance of long-term monitoring and use of multiple control sites to assess the outcomes of MPAs for seahorses. MPAs should be used cautiously to conserve seahorse populations as there is the risk of a negative impact through increased predator abundance.     

Fishers' knowledge and seahorse conservation in Brazil

From a conservationist perspective, seahorses are threatened fishes. Concomitantly, from a socioeconomic perspective, they represent a source of income to many fishing communities in developing countries. An integration between these two views requires, among other things, the recognition that seahorse fishers have knowledge and abilities that can assist the implementation of conservation strategies and of management plans for seahorses and their habitats. This paper documents the knowledge held by Brazilian fishers on the biology and ecology of the longsnout seahorse Hippocampus reidi. Its aims were to explore collaborative approaches to seahorse conservation and management in Brazil; to assess fishers' perception of seahorse biology and ecology, in the context evaluating potential management options; to increase fishers' involvement with seahorse conservation in Brazil. Data were obtained through questionnaires and interviews made during field surveys conducted in fishing villages located in the States of Piauí, Ceará, Paraíba, Maranhão, Pernambuco and Pará. We consider the following aspects as positive for the conservation of seahorses and their habitats in Brazil: fishers were willing to dialogue with researchers; although captures and/or trade of brooding seahorses occurred, most interviewees recognized the importance of reproduction to the maintenance of seahorses in the wild (and therefore of their source of income), and expressed concern over population declines; fishers associated the presence of a ventral pouch with reproduction in seahorses (regardless of them knowing which sex bears the pouch), and this may facilitate the construction of collaborative management options designed to eliminate captures of brooding specimens; fishers recognized microhabitats of importance to the maintenance of seahorse wild populations; fishers who kept seahorses in captivity tended to recognize the condtions as poor, and as being a cause of seahorse mortality.     

Life history and population dynamics of an endangered seahorse (Hippocampus capensis) within an artificial habitat

Species-specific life-history information is critical for successful conservation, particularly in establishing an accurate baseline status. Obtaining such information is challenging for most species, but in particular for rare and threatened marine species. To facilitate future conservation of the endangered Knysna seahorse (Hippocampus capensis) this study aimed to determine important life-history information for this species. Visible implant fluorescent elastomer (VIFE) tags were used to mark 78 seahorses within a residential marina estate in the Knysna estuary, South Africa, in February 2018. Using a mark-resight approach, the size and movement patterns of the population and growth rate of seahorses were determined over a 14-month period. The closed population estimate for H. capensis, within Thesen Islands Marina, was estimated to be 134 (118–152 95% C.I. ) in February 2018 compared to only 72 (48–108 95% C.I. ) in February 2019. The species showed rapid initial growth with males and females having similar rates of growth based on the specialised von Bertalanffy growth function model. The importance of Reno mattresses as a habitat for H. capensis was confirmed based on the high abundance and site fidelity of the population, which emphasises the conservation potential of heavily modified environments for threatened seahorse species. The use of VIFE tags was deemed effective in studying this endangered seahorse and allowed the collection of important information for this species which can be used in future Red List assessments and conservation actions.     

Life history and ecology of seahorses: implications for conservation and management

We present the first synthesis of the life history and ecology of seahorses, compare relationships for seahorses with other marine teleosts and identify research needs. Seahorses occurred primarily amidst temperate seagrasses and tropical coral reefs. Population densities were generally low, ranging from 0 to 0·51 individuals m^?2, but reached 10 m^?2 in some patches. Inferred life spans ranged from 1 to 5 years. Seahorses consumed live prey and possibly changed diet as they grew. Growth rates are poorly investigated to date. Reproduction and mating systems are the best‐studied aspects of seahorse ecology. The relationship between size at first maturity and maximum size in seahorses conformed to that for other marine teleosts. All seahorse species were monogamous within a cycle, but some were polygamous across cycles. Direct transfer of clutches to the brood pouch of the male fish made it difficult to measure clutch size in live seahorses. After brooding, males released from c. 5 to 2000 young, depending on species and adult size. Newborn young measured from 2 to 20 mm in length, which was a narrower size range than the 17‐fold difference that occurred in adult size. Newborn body size had no relationship to adult size. Both eggs and young were larger than expected among marine teleosts, even when considering only those with parental care, but brood size at release was lower than expected, perhaps because the young were more developed. The size of adults, eggs and young increased with increasing latitude, although brood size did not. Considerable research is needed to advance seahorse conservation and management, including (a) fisheries‐dependent and fisheries‐independent abundance estimates, (b) age‐ or stage‐based natural and fishing mortalities, (c) growth rates and age at first maturity, and (d) intrinsic rates of increase and age‐ or size‐specific reproductive output. Current data confirm that seahorses are likely to be vulnerable to high levels of exploitation.     

The importance of seahorses and pipefishes in the diet of marine animals

A review of 135 accounts of predation on seahorses and pipefishes identified 82 predator species, with nine species of seahorses and 25 of pipefishes recorded as prey. These cryptic fishes were generally depredated in low numbers. Where syngnathids formed a high proportion of predator diets, predation occurred on (1) a single abundant species during a population boom or large die-off, (2) concentrations of individuals utilising floating marine vegetation, or (3) juveniles when abundant during the breeding season. Predation coinciding with high syngnathid densities suggests their predators are foraging opportunistically rather than targeting syngnathids as prey. Invertebrates, fishes, sea turtles, waterbirds and marine mammals were all syngnathid predators: these included taxa that do not frequent the demersal habitat generally occupied by seahorses and pipefishes. Thus, seahorses and pipefishes may be moving in the open ocean more than suspected, perhaps using floating mats of marine vegetation. If so, this behaviour could act as a hitherto unknown vector for syngnathid movement and dispersal. Information on syngnathid abundance in predator diet (measured as percent number, volume, or mass) was available in 45 reviewed accounts; in 27% (n = 12) of these studies seahorses or pipefishes comprised ≥20% of predator diet (range 0.005–100%). Frequency of occurrence (percent stomachs, seabird bill-loads, or regurgitations in which a prey item occurred) was provided in 39 accounts, with 15% (n = 6) of these recording a frequency of ≥20% (range 0.003–65%).     

The catch and trade of seahorses in Vietnam

Catch monitoring and surveys were used to assess the seahorse trade in Vietnam. Despite low daily catch rates, potentially 6.5 t of dried seahorses (~2.2 million seahorses) were taken annually as bycatch by trawlers operating out of five coastal provinces of Vietnam. Individual seahorse catches were collated by a few local buyers, who supplied wholesalers in three major markets: Ho Chi Minh City, Hai Phong City and Da Nang. Domestic consumption was small and most seahorses were exported, generally through unofficial and unregulated channels across the northern border into Guangxi province of China. Overall, the seahorse trade was of low economic value to Vietnam, but may constitute an important source of income to upper level buyers and exporters. Most fishers and buyers surveyed reported that seahorse catch had declined over time. This paper should help in meeting the new CITES requirements – through implementation of an Appendix II listing in 2004 – that all international trade in seahorses must be monitored and managed for sustainability.     

An assessment of West African seahorses in fisheries catch and trade

This study provides the first assessment of a heavily traded West African seahorse species, Hippocampus algiricus, and the first information on short‐snouted seahorse Hippocampus hippocampus biology in Africa. A total of 219 seahorses were sampled from fisher catch in Senegal and The Gambia, with estimated height at reproductive activity for H. algiricus (161 mm) larger than mean ± s.d . catch height (150 ± 31 mm). Catch composition, height at reproductive activity and potential biases in fishery retention are discussed with regard to the current Convention on International Trade of Endangered Species (CITES) guidelines.     

Fisheries and trade of seahorses in Brazil: historical perspective, current trends, and future directions

Seahorses (Hippocampus spp.) are globally threatened by overexploitation and habitat destruction; they are also regarded as susceptible to heavy exploitation due to some of their life-history traits. From an economic perspective, they are fishes with high monetary value and marketability. Seahorses are now listed in Appendix II of CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora), to ensure that the international trade is not detrimental to the survival of wild populations; the effectiveness evaluation of these international controls needs comparable monitoring data, including evaluation of spatial and temporal trends. This study assesses the seahorse trade in Brazil, aiming to detect trends in catch levels, volumes and prices. Our main findings were: the dried trade was unregulated, without formal records, and primarily domestic, although records of unreported exports existed; it was primarily sustained by incidental captures in trawl nets. The live seahorse trade was mainly destined for exports, and regulated through national quotas. Between 2002 and 2009, mean prices for dried seahorses ranged from US$1.06 ± 0.46 (level 1 traders) to US$1.06 ± 0.46 (level 1 traders) to US2.78 ± 0.68 (end-sellers) each, while mean prices for each live seahorse traded on the domestic market (1997–2009) ranged from US$1.13 ± 0.02 (level 1 traders) to US$1.13 ± 0.02 (level 1 traders) to US10.08 ± 1.71 (retailers). Mean declared export price (2006–2008) was 15.57 ± 10.87. Enhanced implementation of the CITES listing in Brazil will require further research, and additional measures to address both direct and indirect fishing pressure on seahorse populations.     

Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity

In pipefishes and seahorses (family Syngnathidae), the males provide all postzygotic care of offspring by brooding embryos on their ventral surfaces. In some species, this phenomenon of male "pregnancy" results in a reversal of the usual direction of sexual selection, such that females compete more than males for access to mates, and secondary sexual characteristics evolve in females. Thus the syngnathids can provide critical tests of theories related to the evolution of sex differences and sexual selection. Microsatellite-based studies of the genetic mating systems of several species of pipefishes and seahorses have provided insights into important aspects of the natural history and evolution of these fishes. First, males of species with completely enclosed pouches have complete confidence of paternity, as might be predicted from parental investment theory for species in which males invest so heavily in offspring. Second, a wide range of genetic mating systems have been documented in nature, including genetic monogamy in a seahorse, polygynandry in two species of pipefish, and polyandry in a third pipefish species. The genetic mating systems appear to be causally related to the intensity of sexual selection, with secondary sex characters evolving most often in females of the more polyandrous species. Third, genetic studies of captive-breeding pipefish suggest that the sexual selection gradient (or Bateman gradient) may be a substantially better method for characterizing the mating system than previously available techniques. Finally, these genetic studies of syngnathid mating systems have led to some general insights into the occurrence of clustered mutations at microsatellite loci, the utility of linked loci in studies of parentage, and the use of parentage data for direct estimation of adult population size.     

The origin and evolution of seahorses (genus Hippocampus): a phylogenetic study using the cytochrome b gene of mitochondrial DNA

Phylogenetic relationships among 93 specimens of 22 species of seahorses (genus Hippocampus) from the Atlantic and Indo-Pacific Oceans were analysed using cytochrome b gene sequence data. A maximum sequence divergence of 23.2% (Kimura 2-parameter model) suggests a pre-Tethyan origin for the genus. Despite a greater number of seahorse species in the Indo-Pacific than in the Atlantic Ocean, there was no compelling genetic evidence to support an Indo-Pacific origin for the genus Hippocampus. The phylogenetic data suggest that high diversity in the Indo-Pacific results from speciation events dating from the Pleistocene to the Miocene, or earlier. Both vicariance and dispersal events in structuring the current global distribution of seahorses. The results suggested that several species designations need re-evaluating, and further phylogeographic studies are required to determine patterns and processes of seahorse dispersal.     

Seahorses in focus: local ecological knowledge of seahorse-watching operators in a tropical estuary

Background

Seahorses are endangered teleost fishes under increasing human pressures worldwide. In Brazil, marine conservationists and policy-makers are thus often skeptical about the viability of sustainable human-seahorse interactions. This study focuses on local ecological knowledge on seahorses and the implications of their non-lethal touristic use by a coastal community in northeastern Brazil. Community-based seahorse-watching activities have been carried out in Maracaípe village since 1999, but remained uninvestigated until the present study. Our goal is to provide ethnoecological understanding on this non-extractive use to support seahorse conservation and management.

Methods

We interviewed 32 informants through semi-structured questionnaires to assess their socioeconomic profile, their knowledge on seahorse natural history traits, human uses, threats and abundance trends.

Results

Seahorse-watching has high socioeconomic relevance, being the primary income source for all respondents. Interviewees elicited a body of knowledge on seahorse biology largely consistent with up-to-date research literature. Most informants (65.5 %) perceived no change in seahorse abundance. Their empirical knowledge often surpassed scientific reports, i.e. through remarks on trophic ecology; reproductive aspects, such as, behavior and breeding season; spatial and temporal distribution, suggesting seahorse migration related to environmental parameters.

Conclusions

Seahorse-watching operators were aware of seahorse biological and ecological aspects. Despite the gaps remaining on biological data about certain seahorse traits, the respondents provided reliable information on all questions, adding ethnoecological remarks not yet assessed by conventional scientific surveys. We provide novel ethnobiological insight on non-extractive modes of human-seahorse interaction, eliciting environmental policies to integrate seahorse conservation with local ecological knowledge and innovative ideas for seahorse sustainable use. Our study resonates with calls for more active engagement with communities and their local ecologies if marine conservation and development are to be reconciled.

     

Species identification and genetic structure of threatened seahorses in Gran Canaria Island (Spain) using mitochondrial and microsatellite markers

A non-invasive DNA analysis of seahorse populations was carried out after extensive underwater surveys in Gran Canaria Island (Spain). In this geographical area, the presence of two species, Hippocampus hippocampus and H. guttulatus, has been previously reported. Sequencing of 16S ribosomal DNA (16S rDNA) was used for specific identification of live seahorses sampled in situ, as a previous step to evaluate genetic structure based on ten microsatellite markers. Phylogenetic analyses revealed the presence of a single species, H. hippocampus, in the seahorse communities found at Gran Canaria. No evidences of H. guttulatus or interspecific hybrids were found based on 16S rDNA and microsatellite data. The nuclear markers revealed low genetic diversity and lack of population structure across populations of Gran Canaria Island, with evidence of small population sizes. This study provides critical information to support conservation strategies of Gran Canaria seahorses.     

Conservation value of Codium tenue habitat for the endangered Knysna seahorse Hippocampus capensis

We investigated the density and size structure of the endangered Knysna seahorse Hippocampus capensis in the macroalga Codium tenue at three sites in a residential marina estate in the Knysna Estuary, South Africa, over an 18 month period from March 2017 to August 2018. Seahorses were present in C. tenue throughout the year. Average (± SE) densities of 0.33 (± 0.03) and 0.23 (± 0.03) seahorses per kg of C. tenue were found for 2017 and 2018 respectively. Density did not vary across sites but varied significantly across months with a decreasing trend from summer to spring. The average (± SE) adult seahorse height was 75.16 mm (± 0.63 mm) and 69.09 mm (± 0.64 mm) and mass was 2.05 g (± 0.04 g) and 1.65 g (± 0.04 g) for males and females, respectively, and an even sex ratio was observed throughout the sampling period. Height varied across months, with significantly smaller seahorses found in June and August of 2017. Tail length was highly correlated with height and therefore can serve as a potential proxy for determining the height of H. capensis. This study showed that C. tenue is consistently utilised by Knysna seahorse and should therefore be considered an important habitat to protect and facilitate the ongoing conservation of this endangered seahorse species.     

Two new species of seahorses (Syngnathidae, Hippocampus) from the Middle Miocene (Sarmatian) Coprolitic Horizon in Tunjice Hills, Slovenia: The oldest fossil record of seahorses

Two new and the only known extinct seahorse species Hippocampus sarmaticus and Hippocampus slovenicus are described from the Middle Miocene beds (Lower Sarmatian) in Slovenia, representing the oldest known fossil record of seahorses. Hippocampus sarmaticus was most similar to the extant seahorse species Hippocampus trimaculatus, while H. slovenicus can be most easily compared to the extant pygmy seahorses H. bargibanti, H. denise, and H. colemani. These Sarmatian seahorses lived among seagrasses and macroalgae in the temperate shallow costal waters of the western part of the Central Paratethys Sea.     

The tip of the tail: molecular identification of seahorses for sale in apothecary shops and curio stores in California

Millions of seahorses a year are traded internationally, with many eventually sold at retail shops as curios, as aquarium pets, and especially for use in traditional medicine. The entire genus is now protected by CITES, but conservation measures have been limited in part by difficulties with species identification and incomplete understanding of trade patterns. In this study, we use molecular techniques to make species- and population-level identifications of 56 seahorses sampled from both traditional medicine and curio shops in San Francisco and central California. Seahorses from medicinal sources included unexpectedly large numbers of the eastern Pacific Hippocampus ingens, a species poorly protected by current CITES export recommendations. Curio shops were dominated by H. barbouri, a spiny species that has been reportedly confused in trading records as H. histrix. Specific populations of origin could be inferred for several species through comparison with publicly available phylogeographic data. Our results underscore the strengths and weaknesses of current recommended export regulations, and we suggest that molecular forensics can help in verifying trade documentation and developing more effective conservation measures.     

Otolith morphology, microstructure and ageing in the hedgehog seahorse, Hippocampus spinosissimus (Weber, 1913)

The life history characteristics of many species of seahorse, including the hedgehog seahorse Hippocampus spinosissimus, make them sensitive to exploitation. Consequently, proper management tools must be employed; these are often based on reliable ageing. The aim of the present study was to evaluate the possibility of using otoliths for ageing hedgehog seahorses from Vietnam. Asteriscus, lapillus and sagitta all showed moderate to strong correlations between fish standard length (SL), otolith length and number of increments in seahorses between 83 and 188 mm SL. There were no annual or seasonal marks in any of the three otolith pairs observed using dissecting or light microscopy, and only asteriscus revealed microincrements under light microscopy. The number of increments ranged between 71 and 137. A full trajectory of lapillar microincrements was only visible when using scanning electron microscopy, and then only in two of the examined individuals (88 and 115 increments). A validation experiment showed that the number of increments in the asterisci did not correspond to the age of seahorses bred and reared for 717 and 868 days. Furthermore, a second validation study using Alizarine Complexone (ALZ) otolith marking did not reveal any increments peripheral to the ALZ mark 30 days after marking. The conclusion of the study was that otoliths do not at present provide a reliable tool for estimating age in adult hedgehog seahorses, and therefore other tools have to be employed to improve their management.     

Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

Specific authentication of Hippocampus based on SNP markers

Seahorses, which are used as traditional Chinese medicine, have large market demands and premium price. Because of overfishing, many seahorse species are endangered and listed in IUCN Red List. The purpose of this study was to develop a simple, rapid and reliable molecular method for specific authentication of seahorse species. Cytochrome c oxidase subunit I (COI) sequences were analyzed for molecular authentication of seahorses in this study. Many single nucleotide polymorphism (SNP) sites were detected among COI sequences of nine seahorse species. Based on the SNP sites, four pairs of modified specific primers were designed respectively for authentication of Hippocampus kuda, Hippocampus japonicus, Hippocampus trimaculatus and Hippocampus kelloggi using allele-specific PCR. Moreover, a multiplex allele-specific PCR for simultaneous authentication of H. kuda, H. japonicus and H. trimaculatus was also developed. The study showed that allele-specific PCR required no sequencing and electrophoresis, and the only necessity is to add fluorochrome into PCR products. Hence the whole authentication procedure only takes about 1.5 h. This work provides an effective method for rapid and reliable identification of seahorse species.     

Non-lethal dorsal fin sampling for stable isotope analysis in seahorses

Sampling collection for stable isotope analysis has traditionally involved the sacrifice of the animal. Seahorses (Hippocampus spp.) are listed as threatened by the Convention on International Trade in Endangered Species (http://www.cites.org) and consequently lethal sampling is undesirable. We evaluated the adequacy of dorsal fin tissue of adult seahorses Hippocampus guttulatus for stable isotope analysis as an alternative to lethal tissue sampling. Three seahorse tissues (dorsal fin, muscle, and liver) were analyzed for comparisons of δ¹⁵N and δ¹³C values. Similarities found between δ¹⁵N and δ¹³C values in dorsal fin and muscle tissue of H. guttulatus suggest that both tissues are adequate for stable isotope analysis to understand feeding ecology of seahorses. However, considering the threatened status of the species, dorsal fin tissue would be recommended in adult seahorses as a non-lethal sampling. The effect of lipid extraction on carbon and nitrogen stable isotope values was also evaluated in each seahorse tissues. Significant effects of lipids extraction did only occur for δ¹³C values in muscle and liver. It was found that lipid removal was not necessary to perform SIA in dorsal fin tissues. Due to the limited availability of fin tissue obtained from fin-clipping in seahorses, the relationship between the mass/surface of dorsal fin clip and stable isotope values was analyzed. δ¹⁵N and δ¹³C values in fin samples were found to be independent of the size of fin analyzed. According to our study, the use of fin-clipping sampling, with a minimum surface analyzed of 12.74?mm², was found to be an adequate method for SIA in seahorses.