Exploring Cryptic Diversity with Indian and Pacific Ocean Big Fin Reef Squids

Samantha with freshly caught Sepioteuthis cf. lessoniana in Pulau Seribu Islands off of Jakarta Bay in Java.

The coral reef ecosystems of the Coral Triangle (Indonesia, Malaysia, the Philippines, Papua New Guinea) and the Southeast Asian Peninsula support the highest marine biodiversity in the world and new species continue to be discovered. These ecosystems are of major biological importance and are also the main source of protein and income in a rapidly developing region. Despite the importance of maintaining the health of these marine resources, there is a scarcity of research about the basic biology and ecology of many harvested organisms. This is primarily due to both the difficulty of conducting thorough surveys and the lack of scientific infrastructure supporting research efforts in the region. However, another significant difficulty is that marine environments are notoriously full of cryptic species (species that are so similar in outward appearance that they are mistaken for a single species until genetic or behavioral studies reveal otherwise), and the Coral Triangle has the highest rate of cryptic species discoveries in the world. It is especially difficult to monitor species effectively when what we think is one species is really three species!

Human communities living in the Coral Reef ecosystem depend heavily on artisanal fisheries. Artisanal fisheries are small-scale fisheries that are principally used for local subsistence, driving the economy and maintaining the food security of coastal communities around the world. Artisanal fishing communities are the first to suffer when the health of specific reef ecosystems suffers, adversely affecting harvests. Reef squids are a major component supporting these fisheries in the Coral Triangle and this area contains the highest number of cryptic species complexes of reef squids in the world. The population of reef squids has been very difficult to monitor due to the small-scale nature of these fisheries. Little catch data is collected by monitoring officials and it is unclear what the status of these squid stocks is, whether they are underexploited, fully exploited or overexploited. To complicate the situation even further, while a tremendous tonnage of squid is harvested yearly (2.18 million tons in 2002), 25 percent of this catch cannot be identified to a species. Furthermore, for harvested reef squids, it is unclear how many species exist, where they exist, and how their populations are interconnected and change over time—all crucial and basic information to effectively manage a fishery. This region has the highest human population growth rates worldwide (2-3% annual increase), which could pose significant threats to food security and sustainability if not accompanied by appropriate development and management.

Current and former students from Universitas Syiah Kuala (left to right – Aidia MJ, Achmad Muhadjier and Zulkarnaini Ijul) measuring specimens in Banda Aceh.

My preliminary research suggests that within one group of heavily harvested reef squids, what is commonly identified as a single species known as the big fin reef squid (Sepioteuthis cf. lessoniana) actually comprises multiple cryptic species that coexist within the Coral Triangle. In most ecosystems, species that play very similar roles and/or have very similar traits will compete with each other to exist within that particular ecosystem. Usually, the best-adapted species will dominate in an area and the less-adapted species will become locally extinct (i.e. will not exist in that area). If one of these species were able to play a slightly different role in the ecosystem, whether by feeding on different prey, mating at different times, or utilizing a different part of the habitat, co-existence (also called “sympatry”) is more likely. My research focuses on discovering what mechanisms – diet, behavior, and habitat – may play a role in maintaining the co-existence of these multiple species. Issues such as overfishing and climate change alter ecosystem factors that determine the survival of populations and could alter the dynamics that allow these species to co-exist. For example, climate change will alter sea surface temperatures, which are a primary factor in determining reproduction times and growth for reef squids. Thus, understanding how different cryptic squid species respond to environmental changes is crucial for creating effective management and conservation plans. Understanding the factors that maintain species boundaries within sympatrically occurring cryptic species will provide more species-level and ecosystem-level detail for informing management plans for this fisheries stock.

Left: Dissecting specimen fished near Waigeo Island in Raja Ampat. The presence of developing eggs indicates a mature female. Photo courtesy of Ross Pooley of Papua Diving on Pulau Kri. Right: Fishing boats coming into the landing in Kota Banda Aceh in the early morning.

During 2012, I visited Vietnam and Indonesia for my second field season. I traveled to Nha Trang, Vietnam, and to northern Sulawesi (Donggala and Manado), Pulau Seribu, Banda Aceh and Raja Ampat in Indonesia. I collected samples from local fish markets and fishermen in these areas to:

1. Identify cryptic lineages occurring in the area by collecting mantle tissue for phylogenetic analysis and delineation of range limits. GPS coordinates of fishing sites were also collected when possible.

2. Identify differences in size class and maturity by measuring the size of individuals at each location as well as looking at the degree of gonad maturity and calculating gonadosomatic indices. This is done to determine if co-existing lineages have different growth and maturity patterns, allowing them to prevent hybridization.

3. Identify differences in diet both between cryptic lineages at all locations and within lineages between locations in order to observe any likely differences in ecological niches for co-existing lineages. Squid are remarkably efficient eaters –generally chewing their prey into unidentifiable pieces. Thus, diet analysis will have to be conducted through DNA barcoding for prey species from big fin reef squid stomachs.

To further expand on the second point above, I also set up a long-term, collaborative study with Dr. Z.A. Muchlisin with the Faculty of Fisheries and Marine Science at Universitas Syiah Kuala in Banda Aceh. To determine if different lineages mature at different times, which limits the chances for hybridization, two undergraduate students are collecting samples of Sepioteuthis each month from the fish landings and markets and measuring growth and maturity over the year. Cryptic lineages are identified using DNA barcoding methods.

Fish market in Nha Trang, Vietnam.

This season’s fieldwork in Vietnam was funded by a National Science Foundation “Partnerships in International Research and Education” (PIRE) grant under Dr. Paul Barber. The fieldwork in Indonesia was funded by a grant from the Explorer’s Club.