Population attenuation in zooplankton communities during transoceanic transfer in ballast water

Abstract

Successful biological invasion requires introduction of a viable population of a nonindigenous species (NIS). Rarely have ecologists assessed changes in populations while entrained in invasion pathways. Here, we investigate how zooplankton communities resident in ballast water change during transoceanic voyages. We used next‐generation sequencing technology to sequence a nuclear small subunit ribosomal DNA fragment of zooplankton from ballast water during initial, middle, and final segments as a vessel transited between Canada and Brazil. Operational taxonomic unit (OTU) diversity decreased as voyage duration increased, indicating loss of community‐based genetic diversity and development of bottlenecks for zooplankton taxa prior to discharge of ballast water. On average, we observed 47, 26, and 24 OTUs in initial, middle, and final samples, respectively. Moreover, a comparison of genetic diversity within taxa indicated likely attenuation of OTUs in final relative to initial samples. Abundance of the most common taxa (copepods) declined in all final relative to initial samples. Some taxa (e.g., Copepoda) were represented by a high number of OTUs throughout the voyage, and thus had a high level of intraspecific genetic variation. It is not clear whether genotypes that were most successful in surviving transit in ballast water will be the most successful upon introduction to novel environments. This study highlights that population bottlenecks may be common prior to introduction of NIS to new ecosystems.

Simulations indicate that scores of lionfish (Pterois volitans) colonized the Atlantic Ocean

“…Indeed, lionfish introduced through the aquarium trade are hardy adults that are likely to survive ( Wabnitz, 2003 ). In contrast, fragile larvae have a high probability of mortality upon entering bilge tanks ( Gollasch et al, 2000 ), during transport ( Gollasch et al, 2000 ; Ghabooli et al, 2016 ) and after release ( Padilla & Williams, 2004 ). Lionfish egg masses float for ∼36–72 h prior to hatching ( Fishelson, 1975 ; Morris, 2009 ) and are unlikely to enter bilge tanks while floating.…”

“…Whilst larvae of marine fishes tend to be too large to pass through ballast tank screens ( Carlton & Geller, 1993 ), supposing lionfish larvae did successfully enter the bilge, they would then have to survive travel for approximately 26 days between the Indo-Pacific region and Miami, given an average speed of 24 knots ( Notteboom & Cariou, 2009 ) and two days to traverse the Panama Canal. Larvae begin feeding four days post hatch, can survive six days of starvation ( Thresher, 1984 ), and thus, must feed in the bilge for at least 16 days on depleted plankton populations to survive the voyage (see Gollasch et al, 2000 ; Ghabooli et al, 2016 ). A population of lionfish in the bilge would experience an extreme bottleneck and reduced genetic diversity ( Ghabooli et al, 2016 ).…”

“…Larvae begin feeding four days post hatch, can survive six days of starvation ( Thresher, 1984 ), and thus, must feed in the bilge for at least 16 days on depleted plankton populations to survive the voyage (see Gollasch et al, 2000 ; Ghabooli et al, 2016 ). A population of lionfish in the bilge would experience an extreme bottleneck and reduced genetic diversity ( Ghabooli et al, 2016 ). If the population does not perish during transport, the larvae must accrue enough resources to metamorphose 20–35 days after fertilization ( Ahrenholz & Morris, 2010 ) and survive for another 11 months before reaching reproductive maturity in the Atlantic ( Thresher, 1984 ).…”

Can chlorination of ballast water reduce biological invasions?

“…The length between the initial and final sample collections lasted eight, nine, 19 and 15 days for the first, second, third and fourth voyage, respectively. Details of zooplankton sample collection were described previously by Paolucci et al () and Ghabooli et al (). Briefly, at each sampling, 333 L water was pumped from the top, middle and bottom of each tank contributing to a total sample volume of 1 m 3 , which was filtered through a 35‐µm plankton net that captured plankton organisms while filtering away environmental DNA (eDNA; most abundant below 0.2 µm; Turner et al, ).…”

Zooplankton invasions in the early 21st century: a global survey of recent studies and recommendations for future research

“…This may represent the beginning of an upward trend, or simply an outlying value. Nearly all reviewed genetic studies employed a small set of genetic markers such as cytochrome oxidase 1 (COI) or internal transcribed spacer 1 (ITS1), with only a few publications employing next-generation sequencing methods (Ghabooli et al, 2016;Dexter et al, 2018;Scott et al, 2018). Given the power of these tools to reconstruct the demographic history of populations (Estoup & Guillemaud, 2010), the maturation of eDNA technologies and protocols (Taberlet et al, 2012), and the constantly decreasing cost of implementation (Peterson et al, 2012), genetic and genomic tools represent a particularly promising area for growth within the field of invasion biology.…”