Is the spread of the alien water boatman Trichocorixa verticalis verticalis (Hemiptera, Corixidae) aided by zoochory and drought resistant eggs?

Abstract

Desiccation resistance is a key trait determining the distribution of aquatic insects, their potential for overland dispersal, and survival during drought periods in temporary waterbodies, as well as the spread of invasive species. Passive dispersal by waterbirds is considered to be a key process favouring the spread of invasive species and is more likely to occur for insects with eggs that are resistant to desiccation or gut passage. We investigated the hypothesis that the eggs of the alien boatman Trichocorixa verticalis verticalis are resistant to desiccation and digestion and thus able to disperse via waterbirds. We conducted experiments to test for egg resistance to desiccation in still air and under moving air conditions, to simulate bird flight. Oviposition on greater flamingo (Phoenicopterus roseus) legs and wetland plants was tested in the laboratory and in the field. Resistance of eggs to simulated gut passage was studied, as was the viability of eggs recovered from Eurasian coot (Fulica atra) droppings in the field. Only a fraction of eggs hatched after 8 hr of exposure to still air at 15°C (4% of exposed eggs), and after 2 hr exposure to air flow conditions at 20°C (8%). Oviposition on flamingo legs was confirmed in the laboratory but not in the field. However, oviposition rates were higher on plant stems than on flamingo legs. Digestion simulations showed very low resistance to chemical treatment and no resistance to scarification, and eggs recovered from coot droppings did not hatch. Our experiments demonstrated that T. v. verticalis cannot be considered to have eggs resistant to desiccation or gut passage. However, the dispersal of eggs on legs of flamingos or other waterbirds may occur as rare events. This epizoochory of eggs could potentially contribute to the expansion and gene flow of T. v. verticalis around the Mediterranean region.

Dispersal of aquatic and terrestrial organisms by waterbirds: A review of current knowledge and future priorities

“…Likewise, live chironomid larvae were found in shorebird faeces from the field (Green & Sánchez, 2006). Insect eggs and aquatic snails also may be dispersed by epizoochory, as when corixids lay eggs on bird legs or snails crawl on birds (Carbonell et al, 2021; van Leeuwen & van der Velde, 2012). Alien aquatic snails are now known to be dispersed via endozoochory in regurgitated pellets as well as faeces (Martín‐Vélez et al, 2022).…”

“…However, they are sufficient to suggest that propagule size and hardness are key traits. The survival rate after gut passage is higher for hard, resistant structures such as Artemia cysts than for softer propagules such as Corixidae eggs (Carbonell et al, 2021; Sánchez et al, 2012). Studies on snails indicate greater survival for smaller operculated species and those with greatest resistance to external stressors such as desiccation (Simonova et al, 2016; van Leeuwen, van der Velde, van Lith, et al, 2012).…”

Seed dispersal by waterbirds: a mechanistic understanding by simulating avian digestion

“…Ingested seeds therefore encounter a combination of stressors: mechanical grinding, acid conditions, high temperatures, digestive enzymes and anoxia (Martinez-Haro et al 2009, McWhorter et al 2009. Previous studies have exposed seeds to either chemical or mechanical simulations of digestion, for example by mechanical scarification or exposure to low pH conditions (Martinez-Haro et al 2009, 2010, Vazacova and Munzbergova 2013, Kleyheeg et al 2018a, Tesson et al 2018, Carbonell et al 2021. These experiments revealed that avian digestion is particularly effective because it combines multiple stressors in a living animal (Kleyheeg et al 2018a).…”

Genomic data support multiple introductions and explosive demographic expansions in a highly invasive aquatic insect

“…Multiple nonmutually exclusive factors could explain admixture and/or gene flow among populations within the invasive range of the species in the Western Mediterranean: (i) Different studies have suggested that the species can survive in the open sea (Gunter & Christmas, 1959; Hutchinson, 1931) and, thus, passive dispersal through marine currents and possibly severe storms might play a role in the spread of the species at regional scales (Sailer, 1948; Sala & Boix, 2005); (ii) Low wing loading and high aspect ratios suggest that T. verticalis is probably a good flyer in comparison with native syntopic corixid species, which could facilitate dispersal among nearby water bodies and explain low levels of genetic differentiation among populations ( F ST < 0.12; Table ); (iii) Recent empirical evidence also suggests that T. verticalis could be passively dispersed by attachment of eggs to legs of waterbirds (i.e., epizoochory), a phenomenon that can greatly increase the dispersal distances that can be travelled by the species. Zoochory may potentially explain the recurrent colonization of inland temporary ponds located far away from their likely source populations in permanently flooded coastal wetlands (Carbonell et al, 2016, 2021); (iv) Human‐transportation (e.g., via ballast water) within the invasive range could still also facilitate gene flow between distant populations and contribute to genetic admixture among introduced lineages in different areas (Medley et al, 2015; Robinet et al, 2009; Valls et al, 2016); (v) Finally, we cannot rule out the possibility that introduced populations have experienced local admixture after independent introduction events involving different proportions of multiple lineages, or even that some source populations from the native range already had admixed gene pools resulted from natural (i.e., contact/hybrid zones; Hewitt, 1988) or anthropogenic processes (van Boheemen et al, 2017; Martin et al, 2014).…”

“…Different intrinsic factors have been suggested to make T. verticalis a successful invader, including high physiological plasticity (euryhalinity, broad thermal tolerance, etc. ), short life cycle, extraordinary fecundity, and capacity to be passively transported as eggs (Carbonell et al, 2016(Carbonell et al, , 2020(Carbonell et al, , 2021Céspedes, Coccia, et al, 2019;Guareschi et al, 2013). However, no study has yet been performed on the demography and population genetics of the species in either the native or invasive ranges.…”