Illegal specimen in taxonomy – what should journals do?

In 2018, a new species of centipede graced the pages of the prominent taxonomy journal Zootaxa. More than 14 centimeters long, with striking teal-colored legs, it lives in the montane and mossy forests of the Philippines. Now, however, the centipede is in a harsh spotlight. The Philippine government says the Spanish neurologist and amateur biologist who described the species acquired his specimens illegally.

Neither the journal’s editors nor its peer reviewers caught the lapse—and the journal has no policy requiring documentation that specimens have been collected with proper permits. Some editors tell Science that should change. Others worry about hampering research when undescribed species are vanishing fast. And all agree that journals would struggle to enforce any such rules, given the wide variation in countries’ legal requirements. “There is simply no way for a journal to police this,” says Maarten Christenhusz, an independent botanist and editor-in-chief of the Zoological Journal of the Linnean Society.

Carles Doménech of the University of Alicante in Spain had contacted Filipino collectors after seeing images of the centipede online. One, Michael Andrew Cipat, caught wild centipedes and sold them—dead and alive—to Doménech in 2016 and 2017. Cipat tells Science he had collecting permits and that a friend with export permits shipped the specimens. But the Philippine Department of Environment and Natural Resources (DENR) says it is illegal to sell specimens to a foreign researcher who has not signed an agreement with DENR that delineates the obligations of all parties involved. “We recognize the significance of Mr. Domenech’s study,” a representative of the department wrote to Science. “However, the Philippine government does not tolerate such illegal acts.” The collectors could be imprisoned or fined under a Philippine wildlife protection law.

Doménech says he didn’t know he needed permits to export the centipedes, calling himself a “newbie” who worked largely alone. After he submitted his paper describing the new species, which he named Scolopendra paradoxa, neither Zootaxa nor any of the five reviewers of his manuscript asked about permits, he says. “Now I know it [was] a mistake,” he wrote in an email. “Now I capture my specimens and don’t let anybody do it for me without the corresponding legal permits.”

Zhi-Qiang Zhang, editor-in-chief of Zootaxa, who studies mites at Landcare Research in New Zealand, says that even though the journal does not impose permit requirements, individual editors may reject manuscripts that lack permits. He says the journal’s editors had previously discussed whether it should instruct authors to follow permit requirements and could not agree. “Most editors had negative views about ‘permits’ or ‘legal requirements’ for specimens,” Zhang says, citing opinions that such regulations curb biodiversity research and conservation.

Martínez contacted Cipat and three other Filipino collectors named in the paper. Cipat showed him a package slip that labelled the centipede shipments as “collectible toys”. Martínez also saw a payment receipt made by Doménech to Cipat, allegedly for the centipedes, though it was labelled “family expenses”. Martínez concluded that Doménech had acquired his specimens illegally and had not been honest about his methods. Martínez notified Science of his findings.

“As reviewers, we have the right to know if the specimens were illegally obtained,” he says. “We have the right to refuse to review the paper.”

Martinez admits that he and the other reviewers failed to spot some worrying irregularities. For example, the paper did not name specific collectors and dates for each specimen, and given locations were vague.

But he says reviewers can’t be expected to routinely probe the legality of specimens. “We reviewers are not supposed to be the police.”

Illegal specimens in research have been exposed occasionally, but journal editors disagree about the magnitude of the problem. One editor described it as “insignificant”; another said it is “impossible to know.” They also disagree on what to do about it. Louis Deharveng, deputy editor-in-chief of ZooKeys and an emeritus arthropod researcher at the National Museum of Natural History in Paris, says an editorial policy on permits “is essential.” Such written policy could lead reviewers to examine possible misconduct in manuscripts and request clarification, he says.

However, Deharveng concedes that permits can be difficult or impossible to obtain. He recommends international researchers work with local ones. Such collaborations would both promote local research and respect the law.

Other editors also emphasize the importance of working with local researchers. “Species do not respect political borders,” Christenhusz says. “Collaboration across borders is what is needed for science.”

But among five respected taxonomy journals, two—the Zoological Journal of the Linnean Society and Zootaxa—do not instruct authors to abide by specimen-collecting laws. (Science will soon add such compliance with legal requirements to its editorial policy.)

Shaun Winterton, editor-in-chief of Systematic Entomology and an entomologist at the California Department of Food and Agriculture, says his journal tells authors to follow the law, but adds, “If we as editors suspected that material was illegally collected, it could be difficult for us to confirm.” (He notes that he is speaking on behalf of the journal, not his employer.)

Winterton and Christenhusz say that legal assessment should be done by the institutions that accept specimens, though they acknowledge that it wouldn’t be an easy task for the institutions either. The complex and varying legal conditions that countries impose on research are one obstacle.

A further complication is the international Nagoya Protocol, which aims to ensure “fair and equitable sharing of benefits arising from the utilization of genetic resources.” The agreement may govern the import of some specimens, but whether it applies to taxonomy specimens is unclear.

The Ministry of Ecological Transition and the Demographic Challenge in Spain, which administers Nagoya Protocol matters in the country, tells Science that taxonomic studies are not considered as utilization of genetic resources if they do not examine genetic or biochemical functions.

Such studies, including Domenech’s, are not subjected to Regulation (EU) Nº 511/2014, the legislation that enforces compliance with the Nagoya Protocol within the European Union.

But Spain’s take on the Nagoya Protocol might not apply in other EU countries. The Nagoya Protocol allows each signatory country to define what constitutes use of genetic resources. This added complexity complicates matters for scientists who do cross-border research.

“I don’t think people have a consensus on the limits” of what taxonomy can do while still adhering to the Nagoya Protocol, says Caroline Fukushima, an arachnologist at the Finnish Museum of Natural History.

Gonzalo Giribet, editor-in-chief of Invertebrate Systematics and a zoologist at Harvard University, adds that reviewers can’t take on the responsibility to police specimen legality either. “They are doing this altruistically,” he says, making him leery of adding legal concerns to their reviewing burden. “Journals should have clear statements about the origins of the biological materials and ethics, and the ultimate responsibility [for legality] should lie with the authors.”

Clear information about legal requirements would help reviewers, editors, and researchers, says Caroline Fukushima, an arachnologist at the Finnish Museum of Natural History. In June 2020, in Conservation Biology, she and colleagues recommended creating a platform for countries’ legal requirements for wildlife research. She does not know of any effort to build such a facility.

When asked about permit requirements for insect collection, Matt Hudson, Director of Publications, Communications, and Marketing of the Entomological Society of America, recommends this guide by entomologist Chris Ginter.

A more comprehensive database, though still far from complete, is the Access and Benefit-Sharing Clearing House, an online data facility under the Nagoya Protocol. To date, 68 of the 128 parties to the Nagoya Protocol have not deposited their legal documents there, including the Philippines.

“We are facing habitat destruction, so we must make life easier and faster for scientists,” says Fukushima.