Reconstructing Bioinvasion Dynamics Through Micropaleontologic Analysis Highlights the Role of Temperature Change as a Driver of Alien Foraminifera Invasion

Julian Evans,Roberta Guastella,Claudia Cosentino,Rita Lecci,Leonardo Langone,Nicoletta Mancin,Miriam Cobianchi,Antonio Caruso,Agnese Marchini

doi:10.3389/fmars.2021.675807

Abstract

Invasive alien species threaten biodiversity and ecosystem structure and functioning, but incomplete assessments of their origins and temporal trends impair our ability to understand the relative importance of different factors driving invasion success. Continuous time-series are needed to assess invasion dynamics, but such data are usually difficult to obtain, especially in the case of small-sized taxa that may remain undetected for several decades. In this study, we show how micropaleontologic analysis of sedimentary cores coupled with radiometric dating can be used to date the first arrival and to reconstruct temporal trends of foraminiferal species, focusing on the alien Amphistegina lobifera and its cryptogenic congener A. lessonii in the Maltese Islands. Our results show that the two species had reached the Central Mediterranean Sea several decades earlier than reported in the literature, with considerable implications for all previous hypotheses of their spreading patterns and rates. By relating the population dynamics of the two foraminifera with trends in sea surface temperature, we document a strong relationship between sea warming and population outbreaks of both species. We conclude that the micropaleontologic approach is a reliable procedure for reconstructing the bioinvasion dynamics of taxa having mineralized remains, and can be added to the toolkit for studying invasions.

Highlights

Global trade and worldwide transport of people and goods have largely altered the natural distribution of species (e.g., Sardain et al, 2019), but large gaps of knowledge remain in assessing spatial and temporal patterns of invasions, especially in the marine environment (Seebens et al, 2017; Ojaveer et al, 2018)
In order to identify suitable sites for collecting the sediment cores, where the sea-floor could reasonably reflect the pattern of sedimentation that occurred in the past decades and the history of colonization of Amphistegina spp. in the area, we complied with the following criteria: (I) occurrence of a well-established population of A. lobifera and subordinately of A. lessonii (Figure 1B); (II) absence of fossil amphisteginids in neighboring outcropping rocks, in order to avoid their reworked occurrence in the studied cores, that may confuse the record of current foraminiferal assemblages of marine sediments
While the absence of the Chernobyl peak of 137Cs is common in sediments collected in the southern part of the Mediterranean Sea due to the dispersion pattern of 137Cs fallout that followed the accident, it is surprising to have no signal of nuclear bomb experiments

Summary

Introduction

Global trade and worldwide transport of people and goods have largely altered the natural distribution of species (e.g., Sardain et al, 2019), but large gaps of knowledge remain in assessing spatial and temporal patterns of invasions, especially in the marine environment (Seebens et al, 2017; Ojaveer et al, 2018). Most of the current knowledge of invasions is from larger organisms, whereas very little is known about spatial and temporal patterns of bioinvasions by microscopic taxa such as foraminifera or other unicellular eukaryotes (Langer et al, 2012; Skarlato et al, 2018; Reavie and Cangelosi, 2020). These small-sized invaders can remain unnoticed for several years after their introduction and gain attention from beach visitors or scientists when population sizes reach a certain threshold and become visible to the naked eye (Guastella et al, 2019)

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