Invasion of the Atlantic Ocean and Caribbean Sea by a Large Benthic Foraminifer in the Little Ice Age

Abstract

The larger benthic foraminifera is a group of marine protists harbouring symbiotic algae, that are geographically confined to shallow tropical and subtropical waters, often associated with coral reefs. The resulting controls on availability of habitat and rates of dispersion make these foraminifers, particularly the genus Amphistegina, useful proxies in the study of invasive marine biota, transported through hull fouling and ballast water contamination in modern commercial shipping. However, there is limited information on the importance of these dispersal mechanisms for foraminifers in the Pre-Industrial Era (pre-1850) for the Atlantic and Caribbean region. This paper examines possible constraints and vectors controlling the invasion of warm-water taxa from the Indo-Pacific region to the Atlantic and Caribbean region. Heterostegina depressa, first described from St. Helena, a remote island in the South Atlantic, provides a test case. The paper postulates that invasions through natural range expansion or ocean currents were unlikely along the possible available routes and hypothesises that anthropogenic vectors, particularly sailing ships, were the most likely means of transport. It concludes that the invasion of the Atlantic by H. depressa was accomplished within the Little Ice Age (1350–1850 C.E.), during the period between the start of Portuguese marine trade with east Africa in 1497 and the first description of H. depressa in 1826. This hypothesis is likely applicable to other foraminifers and other biota currently resident in the Atlantic and Caribbean region. The model presented provides well-defined parameters that can be tested using methods such as isotopic dating of foraminiferal assemblages in cores and genetic indices of similarity of geographic populations.

Full text

Academic Editor: Michael Wink
Received: 31 December 2024
Revised: 22 January 2025
Accepted: 23 January 2025
Published: 2 February 2025
Citation: Robinson, E.; Edwards, T.
Invasion of the Atlantic Ocean and
Caribbean Sea by a Large Benthic
Foraminifer in the Little Ice Age.
Diversity 2025,17, 110. https://
doi.org/10.3390/d17020110
Copyright: © 2025 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license
(https://creativecommons.org/
licenses/by/4.0/).
Communication
Invasion of the Atlantic Ocean and Caribbean Sea by a Large
Benthic Foraminifer in the Little Ice Age
Edward Robinson and Thera Edwards *
Department of Geography & Geology, The University of the West Indies, Mona Campus, Kingston 7, Jamaica;
tedforams@gmail.com
*Correspondence: thera.edwards@uwi.edu; Tel.: +1-876-927-2129
Abstract: The larger benthic foraminifera is a group of marine protists harbouring symbiotic
algae, that are geographically confined to shallow tropical and subtropical waters, often
associated with coral reefs. The resulting controls on availability of habitat and rates of
dispersion make these foraminifers, particularly the genus Amphistegina, useful proxies
in the study of invasive marine biota, transported through hull fouling and ballast water
contamination in modern commercial shipping. However, there is limited information on
the importance of these dispersal mechanisms for foraminifers in the Pre-Industrial Era
(pre-1850) for the Atlantic and Caribbean region. This paper examines possible constraints
and vectors controlling the invasion of warm-water taxa from the Indo-Pacific region to
the Atlantic and Caribbean region. Heterostegina depressa, first described from St. Helena,
a remote island in the South Atlantic, provides a test case. The paper postulates that
invasions through natural range expansion or ocean currents were unlikely along the
possible available routes and hypothesises that anthropogenic vectors, particularly sailing
ships, were the most likely means of transport. It concludes that the invasion of the
Atlantic by H. depressa was accomplished within the Little Ice Age (1350–1850 C.E.), during
the period between the start of Portuguese marine trade with east Africa in 1497 and
the first description of H. depressa in 1826. This hypothesis is likely applicable to other
foraminifers and other biota currently resident in the Atlantic and Caribbean region. The
model presented provides well-defined parameters that can be tested using methods such
as isotopic dating of foraminiferal assemblages in cores and genetic indices of similarity of
geographic populations.
Keywords: Heterostegina depressa; Little Ice Age; anthropogenic dispersal; range expansion;
Caribbean Sea; Atlantic Ocean
1. Introduction
The Larger Benthic Foraminifera (LBF), an informal group of protists harbouring algal
symbionts of various kinds are an important global component of the marine biosphere,
occupying a wide variety of ecological niches in the euphotic zone of the warm-temperate
to tropical marine realm (average Sea Surface Temperature (SST) > 18
◦
C) [
1
]. The nature of
these symbiotic relationships can be experimentally related to their habitats through various
controlling factors such as nutrients, temperature and available light [
2
–
13
]. Their global
distribution is well illustrated in the discussion by Prazeres & Renema of the associated
symbionts [14].
The cosmopolitan distribution and well-studied physiology and metabolic activities
of the diatom symbiont-bearing genus Amphistegina has proven it particularly useful in
Diversity 2025,17, 110 https://doi.org/10.3390/d17020110

Diversity 2025,17, 110 2 of 17
the investigation of the rates of invasion and dispersal of biota that have appeared and
spread in the Mediterranean Sea region since the opening of the Suez Canal in 1869,
the so-called Lessepsian migration [
15
–
23
]. Genetic research has indicated that modern
wartime and commercial shipping activities have provided important vectors for the
global dispersion of diverse alien invasive marine and terrestrial species in an increasingly
warming world [24–34].
The prime importance of modern shipping as the agent for many of these introduc-
tions has been well documented and even taken for granted [
35
]. However, published
information on historical (pre-19th Century) participation of human trade and migration in
providing vectors for the dispersal of foraminifers into or out of the Atlantic and Caribbean
Region (ACR) is sparse. Literature that has explored the importance of such participation
among remote ocean islands and other places is based almost exclusively on examples from
the Indo-Pacific Region (IPR) and Mediterranean/north-west Europe [
25
,
36
–
38
]. The paper
presents a hypothesis for a LBF-based invasion of the Atlantic Ocean and the Caribbean to
supplement this previous work
2. Methods
Concisely presented data and distribution maps assembled by Langer and Hottinger
provided a starting point for the comprehensive literature search and review [
7
]. Sources
and data gleaned from that review were used to determine the nature of potential vectors
and barriers that might influence or inhibit the timing, direction and spread of H. depressa
between the IPR and the ACR. Factors such as sea and ocean temperatures, circulation
patterns, ocean transport routes and species presence and absence were key observations
while reviewing each source.
3. Hypothesis
Heterostegina depressa d’Orbigny, (Figure 1), an easily recognisable, extant, cosmopoli-
tan LBF hosting diatom symbionts, belonging to the family Nummulitidae was selected to
test the hypothesis that Holocene, and possibly earlier Quaternary intrusion by LBFs and
probably other biota from the IPR into the ACR by natural processes was unlikely due to the
physical impediments that exist [
7
,
39
]. It was posited that anthropogenic vectors were the
most likely means of transport for this species and probably other foraminifers introduced
to the ACR from the IPR. The choice of species was guided by two main considerations.
Firstly, H. depressa, the genus type, was initially described from a remote island in the ACR
in 1826 near the end of the Little Ice Age (1350–1850 C.E. [
40
–
43
]. Wooden sailing ships
were the mode of marine transport at that time. Secondly, the occurrence of H. depressa in
the ACR is apparently restricted to Upper Holocene sediments. The propositions of our
hypothesis are presented sequentially below.

Diversity 2025,17, 110 3 of 17
Diversity 2025, 17, x PEER REVIEWED 3 of 17
Figure 1. Heterostegina depressa d’Orbigny, Recent, Discovery Bay, Jamaica. (Edward Robinson col-
lection, donated by Thomas. F. Goreau).
3.1. Heterostegina Depressa Invaded the Atlantic Caribbean Region from the Indo-Pacific Region
but Not via the Central American Seaway
Heterostegina depressa was first described from Recent sediments from St. Helena, one
of the remotest islands in the South Atlantic, where Napoleon Bonaparte was exiled fol-
lowing his defeat at the Battle of Waterloo [43–45]. An ACR species, H. antillarum, was
described by [46] from the Caribbean islands of Cuba and Jamaica and, subsequently,
from numerous Recent localities in the Greater Caribbean region and other locations in
the tropical ACR (Figure 2) [7,47–56]. In 1826 d’Orbigny also described H. suborbicularis
and one of its variants from the IPR. These are all now considered to be conspecific with
H. depressa based on genetic studies [39].
The youngest records of fossil species of Heterostegina in the Caribbean and Central
American region are from the early and early mid Miocene, some 20 to 18 million years
ago while the Central American Seaway, separating North America from South America,
was still open [57–59]. For H. depressa, Plio-Pleistocene as well as Recent occurrences have
been documented from the IPR within the Indonesian region of high nummulitid diver-
sity, from remote Pacific islands and from the west coast of the Americas, frequently as H.
suborbicularis [8,60–62]. These occurrences include the Upper Pleistocene Armuelles For-
mation of the Pacific coast of Central America Figure 2 [63]. But there are, as yet, no fossil
records of H. depressa from the Caribbean side of Central America.
Figure 1. Heterostegina depressa d’Orbigny, Recent, Discovery Bay, Jamaica. (Edward Robinson
collection, donated by Thomas. F. Goreau).
3.1. Heterostegina Depressa Invaded the Atlantic Caribbean Region from the Indo-Pacific Region
but Not via the Central American Seaway
Heterostegina depressa was first described from Recent sediments from St. Helena,
one of the remotest islands in the South Atlantic, where Napoleon Bonaparte was exiled
following his defeat at the Battle of Waterloo [
43
–
45
]. An ACR species, H. antillarum, was
described by [
46
] from the Caribbean islands of Cuba and Jamaica and, subsequently,
from numerous Recent localities in the Greater Caribbean region and other locations in
the tropical ACR (Figure 2) [
7
,
47
–
56
]. In 1826 d’Orbigny also described H. suborbicularis
and one of its variants from the IPR. These are all now considered to be conspecific with
H. depressa based on genetic studies [39].
The youngest records of fossil species of Heterostegina in the Caribbean and Central
American region are from the early and early mid Miocene, some 20 to 18 million years
ago while the Central American Seaway, separating North America from South America,
was still open [
57
–
59
]. For H. depressa, Plio-Pleistocene as well as Recent occurrences
have been documented from the IPR within the Indonesian region of high nummulitid
diversity, from remote Pacific islands and from the west coast of the Americas, frequently
as H. suborbicularis [
8
,
60
–
62
]. These occurrences include the Upper Pleistocene Armuelles
Formation of the Pacific coast of Central America Figure 2[
63
]. But there are, as yet, no
fossil records of H. depressa from the Caribbean side of Central America.
The absence of pre-Late Holocene records of H. depressa can also be attributed to
insufficient sampling of appropriate Holocene facies and localities. However, as of now
such records are apparently lacking in ACR sedimentary strata, including Pleistocene
cores from southeast Florida, in which the endemic Caribbean LBF soritid genera are well-
represented [
64
]. This species has not been reported in Pliocene to Pleistocene formations
in Jamaica [
65
], nor was it recorded in the Ruth Todd Library’s card catalogue at the

Diversity 2025,17, 110 4 of 17
Smithsonian Institute, and also not recorded in isotopically dated mid-Holocene (~6 kyr
BP) sedimentary deposits from Caribbean Panama [66].
Diversity 2025, 17, x PEER REVIEWED 4 of 17
Figure 2. Caribbean and Central American localities for Heterostegina depressa. See Appendix A
Table A1.
The absence of pre-Late Holocene records of H. depressa can also be attributed to in-
sufficient sampling of appropriate Holocene facies and localities. However, as of now
such records are apparently lacking in ACR sedimentary strata, including Pleistocene
cores from southeast Florida, in which the endemic Caribbean LBF soritid genera are well-
represented [64]. This species has not been reported in Pliocene to Pleistocene formations
in Jamaica [65], nor was it recorded in the Ruth Todd Library’s card catalogue at the Smith-
sonian Institute, and also not recorded in isotopically dated mid-Holocene (~6 kyr BP)
sedimentary deposits from Caribbean Panama [66].
This leads to the conclusion that H. depressa was introduced to the ACR from the IPR
and not the other way around as suggested by [63] (p. 163), sometime within the Holo-
cene, well after closure of the Central American Seaway 3 million years ago [67].
3.2. The Only Other Available Invasion Route Was Around South Africa
In examining other possible routes into the ACR besides the Central American Sea-
way the Suez Canal opened in 1869. Since then, several genera of foraminifers have en-
tered the Mediterranean Sea from the Gulf of Aqaba (Red Sea), including H. depressa and
other LBF, providing future potential for H. depressa to reach the ACR via the Mediterra-
nean [18,61]. However, the descriptions of H. depressa from the ACR antedate the Suez
Canal opening by 44 years and the Panama Canal opening in 1914 post-dates these de-
scriptions by 88 years.
A seaway extending from the Indian subcontinent through the Mediterranean region
to the Atlantic (the Tethyan Seaway) existed for much of the Cenozoic Era, allowing the
interchange of LBF genera and species between the ACR and the Tethyan/IPR, leading to
LBF centres of diversification in several shifting locations through time [68,69]. This sea-
way became restricted and was eventually closed off in the Miocene, well before the emer-
gence of H. depressa in the IPC and ACR [70,71].
Figure 2. Caribbean and Central American localities for Heterostegina depressa. See Appendix ATable A1.
This leads to the conclusion that H. depressa was introduced to the ACR from the IPR
and not the other way around as suggested by [
63
] (p. 163), sometime within the Holocene,
well after closure of the Central American Seaway 3 million years ago [67].
3.2. The Only Other Available Invasion Route Was Around South Africa
In examining other possible routes into the ACR besides the Central American Seaway
the Suez Canal opened in 1869. Since then, several genera of foraminifers have entered the
Mediterranean Sea from the Gulf of Aqaba (Red Sea), including H. depressa and other LBF,
providing future potential for H. depressa to reach the ACR via the Mediterranean [
18
,
61
].
However, the descriptions of H. depressa from the ACR antedate the Suez Canal opening by
44 years and the Panama Canal opening in 1914 post-dates these descriptions by 88 years.
A seaway extending from the Indian subcontinent through the Mediterranean region
to the Atlantic (the Tethyan Seaway) existed for much of the Cenozoic Era, allowing the
interchange of LBF genera and species between the ACR and the Tethyan/IPR, leading to
LBF centres of diversification in several shifting locations through time [
68
,
69
]. This seaway
became restricted and was eventually closed off in the Miocene, well before the emergence
of H. depressa in the IPC and ACR [70,71].
Two other naturally existing corridors linking the IPR with the ACR have remained
open for millions of years [
7
]. Around the southern tip of South America SST data indicate
temperatures of 6–10
◦
C thus greatly inhibiting the survival prospects of tropical symbiont-
bearing foraminifers invading the ACR from that direction. The nearest IPC source today,
Rapa Nui (Easter Island), is at the northern edge of the temperate zone, well over 4000 km
away from the tip of South America [
7
,
72
]. The other route is around the southern tip
of Africa. As discussed below, although SSTs there are marginally unfavourable for the

Diversity 2025,17, 110 5 of 17
existence of the tropical H. depressa, it remains the most probable marine corridor from the
IPR to the ACR.
3.3. South Africa Presents Barriers for LBF Invasion of the ACR Through Natural Vectors
The two most widely accepted natural processes promoting the expansion or invasion
of a marine species are either via expansion of its range through local interaction with its
environment [
23
] or via dispersal through transport by ocean currents, including rafting
on seaweed or other floating debris [
73
–
76
]. Other less likely natural vectors include
transport in tsunami debris [
77
]; lateral and vertical dispersal of debris and animals by
storm events [
78
,
79
]; transport on or in the feet/feathers/guts of birds; and on, or in,
fish [80,81]
Turning first to possible range expansion from the East African coast, where H. depressa
is widely recorded [
7
,
82
], the journey around the Cape of Good Hope and up the west coast
of South Africa into the ACR presents difficulties. H. depressa was recorded as tolerating the
lowest SST among the Nummulitidae, based on its distribution pattern, at about 18
◦
C [
7
].
Langer and Hottinger’s isotherms indicate that temperatures at the southern extremity
of South Africa were just outside H. depressa’s range of tolerance. While today’s SSTs are
noticeably higher [
20
], south Atlantic SSTs at the time the species was first described, near
the termination of the Little Ice Age, are estimated variously to have been about 0.3–0.9
◦
C,
even up to more than 2
◦
C lower than those of the latter part of the 20th Century [
42
,
83
,
84
].
For any LBF that might reach the Cape of Good Hope from the tropical east African
coast via coastwise migration, the southwest coast of Africa presents a region of un-
favourable temperatures for some 2000 km north, from the Cape of Good Hope to Angola
due to coastal upwelling [
7
]. At an average natural invasion rate in shallow coastal waters
of around 11–13 km per year, using Amphistegina as a proxy [
20
], it would take as much
as 150 years for H. depressa, migrating along a coast with variable temperature conditions
as low as 14
◦
C [
72
], to reach the LBF tolerance zone, assuming that reproduction was
possible. Evidential support for this proposition is available through the study by [
85
]
concerning the changes in the distribution of Amphistegina on the southeast coast of South
Africa, especially their Figure 1showing the absence of Amphistegina on the southwest
coast of Africa. Additionally, the predictive model shown in their Figure 2suggests that,
even in today’s immediate warming future, conditions along that southwestern shore form
an important barrier, restricting intrusion of H. depressa into the ACR by this route (see also
a similar argument for the goatfish Mulloidichthys [
86
]). Therefore, the main alternative
method of dispersal of H. depressa into the South Atlantic must be by surface currents or
other suitable ocean vectors.
An important possibility for the natural transport of H. depressa by ocean currents
westward into the ACR, beyond South Africa, would be a ‘piggy-back’ vector or as propag-
ules caught in one or more of the westerly drifting current eddies (Agulhas Rings) spun off
into the South Atlantic by the warm Agulhas Current of southeast Africa [
87
,
88
]. However,
based on the information indicated by [
88
] (Figure 1), such Rings weaken and dissipate
while the surrounding ocean SST is still below 20
◦
C. Even if the Rings intercepted the
warmer surface waters of the southward flowing Brazil Current, east of South Amer-
ica, any contained propagules would face the prospect of being carried southwards into
the cold waters of the South Atlantic Malvinas (Falkland) Current and Southern Ocean
(formerly Antarctic Ocean) [
89
]. The NASA SVS video illustrates this situation clearly
(https://svs.gsfc.nasa.gov/3912) (accessed on 20 January 2025)).

Diversity 2025,17, 110 6 of 17
3.4. Anthropogenic Vectors Transported H. depressa to the ACR
A review of anthropogenic vectors shows hull fouling and ballast water contamination
in shipping to be the most common vector-related mechanisms for the modern (post
1850 CE) invasion of non-endemic species of foraminifers and other biota into northern
European waters, the northeast coast of North America and the central and northeast
Pacific [
24
,
26
,
28
,
90
]. Gollasch attributed nearly 40% of species invasive to European waters
as resulting from hull fouling and ballast water contamination, and about a further 25%
from processes resulting from deliberate or inadvertent interventions in the aquaculture
and stocking industries [
38
]. Only 6% were judged to result from species range expansion,
while about 25% probably arrived via Lessepsian migration, vector not stated.
At the time H. depressa was described by d’Orbigny, wooden-hulled sailing ships
carrying dry ballast were the common mode of transport. Experimental investigations in
the Pacific Ocean using a replica of a 16thCentury wooden sailing ship, showed that many
kinds of marine organisms were transported through attachment to the hull exterior [
91
].
Fouling of the hull was probably enhanced by the niches produced by boring species such
as Teredo, dry rot, and local scraping of the hulls against rocks while ships were anchored
or beached for maintenance or repairs [
25
,
92
,
93
] and [
94
] (illustration p. 49). The dry
ballast carried in these ships would have varied depending on the purpose of the voyage
and nature of the cargo. Frequent dumping of non-commercial ballast in exchange for
new materials was, and still is, commonplace [
95
]. Ballast ranged from rocks and sand
collected from the local coastline or beaches, commercial supplies of rock for construction,
even spare cannons [
95
]. Ballast collected from Indo-Pacific coastlines, particularly coral
reefal coasts would almost certainly have included LBF and other biota, including coral
fragments, either directly in the associated sediments or attached to other organisms such
as seagrass [
54
,
74
] and algae growing on the ballast. Although this is admittedly still
conjectural, archaeological investigation of medieval shipwrecks, including assessment
of ballast materials, has become an important field of research [
95
,
96
]. Sailing ships have
the enormous advantage over natural ocean currents of being steerable vectors, able to
choose their destinations, including remote ocean islands. Therefore, we regard most of the
natural mechanisms discussed in Section 3above as being relatively unlikely compared
with the transport opportunities offered by the shipping trade [97].
3.5. Heterostegina Depressa Invaded the ACR After the Late 15th Century
Before the late 15th Century, trans-ocean shipping in the central and southern ACR
was non-existent. Only local operations originating from the Mediterranean along the
northwest and west African coasts were active [
98
]. Ocean-going vessels refined by the
Portuguese led to the first European ship venturing around the Cape into the Indian Ocean
by the Portuguese navigator Bartelomeu Diaz in 1488, who sailed as far as Algoa Bay [
99
].
A replica of Diaz’s caravel “Boa Esperanca”, launched in 1990, provides an example of the
trading vessels of the late 15th Century. With a length of 28.8 m and a beam of 6.6 m, it has
a draught of 3.3 m and can accommodate 22 people (https://fundacionnaovictoria.org/
caravel-boa-esperanca) (accessed on 27 December 2024).
Vasco da Gama’s successful follow-up voyage into the Indian Ocean in 1497 brought
the Portuguese into direct contact with the Swahili traders who had been sailing up and
down the east African coast and lands further east for several centuries Figure 3[
94
,
98
,
100
].
Simultaneously it also brought the Portuguese into tropical coastal areas that, today at least,
and almost certainly then, contained H. depressa as an important component of the shallow-
water foraminiferal assemblages [
7
,
19
,
82
,
101
]. After 1497 there was constant passage of
ships between the Atlantic and Indian Oceans for trade and colonisation, frequently with

Diversity 2025,17, 110 7 of 17
conflict [
99
], extending to India, the South China Sea and present-day Indonesia, the “Coral
Triangle”, where H. depressa probably evolved [10,98,102].
Diversity 2025, 17, x PEER REVIEWED 7 of 17
today at least, and almost certainly then, contained H. depressa as an important component
of the shallow-water foraminiferal assemblages [7,19,82,101]. After 1497 there was con-
stant passage of ships between the Atlantic and Indian Oceans for trade and colonisation,
frequently with conflict [99], extending to India, the South China Sea and present-day In
Figure 3. Introduction and spread of shipping activity in the Atlantic and Caribbean at the end of
the 15th Century. Bold black line—the Swahili Coast of east Africa. Red lines—routes opened by
Portuguese traders to the Swahili Coast and Indo-Pacific,[98] (p. 390). Blue area—approximate area
of Spanish trading and expansion to the Caribbean and Central America, based on the routes of
Columbus’ four voyages [103] (p. 80).
The return journey to Portugal from the IPR after rounding South Africa was north
through the central South Atlantic Ocean to maximise the wind patterns [98] (p. 39) (Fig-
ure 3). On one of these voyages the remote subtropical South Atlantic island of St. Helena
(type locality for H. depressa) was discovered by the Portuguese in 1502 only four years
after trade commenced [104]. It quickly became an important stopover for the repair and
revictualing of the Portuguese merchant ships [104,105]. The central Atlantic Portuguese
island colonies of Cape Verde and the Azores also provided important in-transit stops, as
illustrated in [98]and [99] (pp. 214 &234).
Around that same time, trans-Atlantic shipping activity in the tropical ACR between
maritime Europe, particularly Spain, and the Greater Caribbean sprang into life and flour-
ished from the end of the 15th Century, following Columbus’s 1492 voyage to the New
World [103] (pp. 77–88). This development introduced a host of additional vectors to fa-
vourable LBF habitats within the tropical ACR (Figure 3). Trade was driven by European
colonisation, accompanied by immigrant ships, naval rivalry, privateers and piracy [103];
by the growth of the transatlantic slave trade [106]; by the establishment of botanical and
other centres across the growing colonies to collect and secure supplies of plants and other
produce for agricultural and medical use [107,108]. By the mid-17th Century, the Dutch,
French and British, using the same general ocean routes, had caught up and surpassed
Figure 3. Introduction and spread of shipping activity in the Atlantic and Caribbean at the end of
the 15th Century. Bold black line—the Swahili Coast of east Africa. Red lines—routes opened by
Portuguese traders to the Swahili Coast and Indo-Pacific [98] (p. 390). Blue area—approximate area
of Spanish trading and expansion to the Caribbean and Central America, based on the routes of
Columbus’ four voyages [103] (p. 80).
The return journey to Portugal from the IPR after rounding South Africa was north
through the central South Atlantic Ocean to maximise the wind patterns [
98
] (p. 39)
(Figure 3). On one of these voyages the remote subtropical South Atlantic island of St.
Helena (type locality for H. depressa) was discovered by the Portuguese in 1502 only four
years after trade commenced [
104
]. It quickly became an important stopover for the
repair and revictualing of the Portuguese merchant ships [
104
,
105
]. The central Atlantic
Portuguese island colonies of Cape Verde and the Azores also provided important in-transit
stops, as illustrated in [98] and [99] (pp. 214 & 234).
Around that same time, trans-Atlantic shipping activity in the tropical ACR between
maritime Europe, particularly Spain, and the Greater Caribbean sprang into life and
flourished from the end of the 15th Century, following Columbus’s 1492 voyage to the
New World [
103
] (pp. 77–88). This development introduced a host of additional vectors to
favourable LBF habitats within the tropical ACR (Figure 3). Trade was driven by European
colonisation, accompanied by immigrant ships, naval rivalry, privateers and piracy [
103
];
by the growth of the transatlantic slave trade [
106
]; by the establishment of botanical and
other centres across the growing colonies to collect and secure supplies of plants and other
produce for agricultural and medical use [
107
,
108
]. By the mid-17th Century, the Dutch,
French and British, using the same general ocean routes, had caught up and surpassed
Portugal as the primary global traders and colonisers [
99
]. In 1659 St. Helena became a
British colony but the island continued to be an important staging post [104].
The route of Portuguese traders from South Africa and the IPR intersected with some
of the routes of Caribbean-bound European shipping, pioneered by Columbus’ third voyage

Diversity 2025,17, 110 8 of 17
in 1498, within the tropical Cape Verde Islands an important entrepot for the slave trade
and goods [
98
] (p. 138) and [
99
]. This would have provided in-transit and vector exchange
opportunities for H. depressa. This is evidenced by the several localities recorded there for
the species [48] and [109] (p. 746).
This suggests that the window of opportunity for invasion by H. depressa of the ACR
from the IPR existed from sometime after about 6 kyr BP, the youngest dated ACR sediments
in which H. depressa was not encountered [
66
], until sometime before 1826, the date of
the first description of the species [
43
]. As the beginning of the 16th Century coincided
with a revolutionary change for the better in the options for vectors via South Africa and
within the tropical ACR, it leads to the conclusion that the introduction of H. depressa to the
ACR occurred shortly after that date, perhaps even as early as 1502, when St. Helena was
discovered. The probable route of the H. depressa invasion of the Caribbean is illustrated
in Figure 4.
Diversity 2025, 17, x PEER REVIEWED 8 of 17
Portugal as the primary global traders and colonisers [99]. In 1659 St. Helena became a
British colony but the island continued to be an important staging post [104].
The route of Portuguese traders from South Africa and the IPR intersected with some
of the routes of Caribbean-bound European shipping, pioneered by Columbus’ third voy-
age in 1498, within the tropical Cape Verde Islands an important entrepot for the slave
trade and goods [98] (p. 138) and [99]. This would have provided in-transit and vector
exchange opportunities for H. depressa. This is evidenced by the several localities recorded
there for the species [48] and [109] (p. 746).
This suggests that the window of opportunity for invasion by H. depressa of the ACR
from the IPR existed from sometime after about 6 kyr BP, the youngest dated ACR sedi-
ments in which H. depressa was not encountered [66], until sometime before 1826, the date
of the first description of the species [43]. As the beginning of the 16th Century coincided
with a revolutionary change for the better in the options for vectors via South Africa and
within the tropical ACR, it leads to the conclusion that the introduction of H. depressa to
the ACR occurred shortly after that date, perhaps even as early as 1502, when St. Helena
was discovered. The probable route of the H. depressa invasion of the Caribbean is illus
Figure 4. Suggested route of the invasion of the Caribbean by Heterostegina depressa, Blue line -.
Circular Points, locations yielding Recent H. depressa based on [7] with the additions of Bermuda
and some Caribbean localities (Panama, CP). Yellow area—routes of the Atlantic Slave Trade as
described in [103,110]. Dashed lines—approximate limits of the tropical zone with year-long SSTs
above 20 °C, based on data from [111]. Other symbols are the same as Figure 3.
4. Discussion
In suggesting the Portuguese trade route around South Africa as the most likely av-
enue for the introduction of tropical H. depressa to the ACR, the response of the species to
various factors, including light and temperature tolerances [4,12,13,23] as well as vector
velocities requires comment [112–114].
Survival Times. Experiments by [12] showed that the photosymbionts of H. depressa
remained active even after 15 days without light, while experimental studies over a 4-
week period by [13] showed that survival at temperatures as low as 15.6 °C occurred. Alve
Figure 4. Suggested route of the invasion of the Caribbean by Heterostegina depressa, Blue line -.
Circular Points, locations yielding Recent H. depressa based on [
7
] with the additions of Bermuda and
some Caribbean localities (Panama, CP). Yellow area—routes of the Atlantic Slave Trade as described
in [
103
,
110
]. Dashed lines—approximate limits of the tropical zone with year-long SSTs above 20
◦
C,
based on data from [111]. Other symbols are the same as Figure 3.
4. Discussion
In suggesting the Portuguese trade route around South Africa as the most likely
avenue for the introduction of tropical H. depressa to the ACR, the response of the species to
various factors, including light and temperature tolerances [
4
,
12
,
13
,
23
] as well as vector
velocities requires comment [112–114].
Survival Times. Experiments by [
12
] showed that the photosymbionts of H. depressa
remained active even after 15 days without light, while experimental studies over a
4-week
period by [
13
] showed that survival at temperatures as low as 15.6
◦
C occurred. Alve
& Goldstein demonstrated that some shallow water benthic foraminiferal propagules
can survive quiescently for up to two years in many cases before growth starts [
115
],
while [
21
,
116
] have shown that foraminifers that have diatom endosymbionts (Amphistegina)

Diversity 2025,17, 110 9 of 17
may become dormant and mostly survive for as long as 12 months of darkness and, with
slower and less complete recovery, as long as 20 months. Most studies have been concerned
with LBF survival in a warming world, with less attention directed to research specifically
concerned with the survival prospects of tropical LBF subjected to extended decreased water
temperatures, such as might be encountered during transit between two geographically
separated tropical regions [117,118]
Although the light tolerances of members of the Nummulitidae favour a relatively
deep habitat, H. depressa is an exception [
1
,
119
]. This species is found living in a wide range
of water-depth situations, ranging from a cryptic sensu [
114
] in intertidal pools, where it
protects itself from the strongest sunlight by living in crevices and other sheltered habitats,
down to the base of the euphotic zone [
114
,
120
,
121
]. It has also been found attached to
algae and seagrasses [
63
], as well as in sediments associated with seagrass meadows [
56
].
This would favour involuntary transport for the species as fouling on wooden vessels that
were anchored or beached in the intertidal zone in the source region. This paper postulates
that the sheltered living ability of H. depressa might be a factor which has resulted in the
successful intrusion of the species into the ACR, in contrast to the current absence of other
members of the Nummulitidae, which tend to be restricted to greater depth habitats (pers.
comm. Geoffrey Adams, 13 November 1973) [1] (Figure 2).
Rates of Dispersal. The average speed of the Portuguese traders, and similar 16th
and 17th Century ships, was about 3.5 knots, sometimes up to 7 or 8 knots, depending on
wind and current speeds and directions, or about 160 km per day [
91
,
98
]. At that speed
the average 16th Century Nao would reach subtropical St. Helena with average SST of
20–22
◦
C from the vicinity of the Cape of Good Hope, South Africa, in 3 to 4 weeks [
122
].
These transit times are well within the reported survival times of quiescent foraminifers
mentioned above. The intertidal habitat tolerance of H. depressa would also favour dispersal
from the same wooden ships, anchored or beached, or wrecked in storms, or driven ashore,
or from drifted floating remains of ships sunk by unfriendly adversaries, while in transit
through favourable shallow marine habitats in the tropical and subtropical ACR [
103
]. On
average about one in four ships was lost on each Portuguese voyage [99].
5. Conclusions
The particular problems accompanying invasion of the ACR from the IPR through the
natural processes outlined above suggest that anthropogenic vectors appear to be the only
likely means of dispersal for H. depressa. These vectors only became available at the end
of the 15th Century, hence it is concluded that H. depressa was introduced into the South
Atlantic and Caribbean as hull fouling and/or as a contaminant of solid ballast material on
Portuguese or later commercial shipping via South Africa, commencing around the end
of the 15th Century, when the trans-Atlantic shipping trade, in general, rapidly expanded
from non-existence, and ended before 1826 when the first formal description of the species
was recorded, a period of about 330 years.
When one considers the expansion of the LBF Amphistegina into, and through, the
Mediterranean Sea within the last 150 years [
123
], there appears to have been adequate time
for H. depressa to have achieved its present-day distribution in the ACR, especially in terms
of the colonisation of remote islands, such as St Helena and Bermuda [
47
], and into the
favourable environmental conditions of the Caribbean, initially through commercial trade
between the Indo-Pacific and the ACR and subsequent dispersal within the tropical ACR.
This paper did not examine or review the paleobiogeography of the LBF Borelis
pulchra [
46
], initially described from Cuba in the ACR. However, it is possible to apply a
similar reasoning to the timing and method of its introduction into the ACR as it does not
appear to be present there in sediments aged between its doubtful reported occurrence in

Diversity 2025,17, 110 10 of 17
the late Miocene around St Martin [
124
,
125
] and the Late Holocene [
64
] and as indicated
in [126] (p. 1417).
Culver and Buzas remarked that 53 of 878 species of modern benthic foraminifera on
the North and Central American Atlantic coasts have no fossil record but are geographically
widespread, suggesting recent evolution and rapid dispersal [
127
] (p. 102). Based on this
remark this paper offers that the distribution pattern could also be related to an invasion
event such as the one described.
The hypothesis and its propositions presented in this paper provide a first explo-
ration of some of the factors that might inhibit the introduction of LBF from the IPR to
the ACR regions (and perhaps vice versa) by natural processes. This model has an ad-
vantage over most other early historical biotic dispersion accounts in supplying specific
temporal parameters that can be tested using such methods as radiocarbon dating of
foraminiferal assemblages and other organisms from cores [
118
], comparative studies of
genetic diversity [
86
] sedimentary ancient DNA analyses in the sediment cores from the
key regions [128].
Author Contributions: Conceptualization, E.R.; methodology, E.R., T.E.; software, E.R., T.E.; formal
analysis, E.R., T.E.; investigation, E.R., T.E.; data curation, T.E.; writing—original draft preparation,
E.R., T.E.; writing—review and editing, E.R., T.E.; visualisation, E.R., T.E. All authors have read and
agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Data Availability Statement: No new data were created or analyzed in this study. Data sharing is not
applicable to this article. The original map contributions of Figures 3and 4presented in this study are
included in the article/Appendix A. Further inquiries can be directed to the corresponding author.
Acknowledgments: Laurel Collins, Florida International University, for providing helpful comments
and suggestions on early versions of this manuscript. Brian Huber, Smithsonian Institute, for access-
ing and searching the Ruth Todd card index catalogue of foraminiferal species at the Smithsonian
Institute. Stephen Stukins, Natural History Museum, UK, for verifying the neotypes of Heterostegina
depressa. NASA/Goddard Space Flight Center Scientific Visualization Studio and personnel for access
to the NASA SVS video.
Conflicts of Interest: The authors declare no conflicts of interest.
Abbreviations
The following abbreviations are used in this manuscript:
ACR Atlantic and Caribbean region
BP Before Present
CE Common Era
DOAJ Directory of open access journals
IPR Indo-Pacific region
LBF Larger Benthic Foraminifera
MDPI Multidisciplinary Digital Publishing Institute
NASA National Aeronautics and Space Administration.
SST Sea Surface Temperature
SVS Scientific Visualization Studio

Diversity 2025,17, 110 11 of 17
Appendix A
Table A1. Locations of Heterostegina antillarum (depressa) shown in Figure 2[51–53].
Record
No Publication Year Genus Species Locality Lat Long Country
12802 Brooks 1973 1973
Heterostegina
antillarum S Puert
Rico 17.56 −66.31 Puerto
Rico
12803
Bermudez 1935
1935
Heterostegina
antillarum Northern
Cuba 23.08 −81.33 Cuba
12804
d’Orbigny 1839
1839
Heterostegina
antillarum Cuba 23 −80 Cuba
12805 Seiglie 1970 A 1970
Heterostegina
antillarum SE Puerto
Rico 18.03 −65.49 Puerto
Rico
12806 Seiglie 1971 A 1971
Heterostegina
antillarum
SW Puerto
Rico 18.02 −67.16 Puerto
Rico
12807 Sen Gupta
Schafer 1973
1973
Heterostegina
antillarum NW St.
Lucia 14.02 −61 St Lucia
12808
d’Orbigny 1839
1839
Heterostegina
antillarum Jamaica 17.57 −76.58 Jamaica
12809 Hofker, Sr.
1956
1956
Heterostegina
antillarum St. Croix 17.3 −64 St. Croix
12810 Drooger
Kaasshjeter
1958
1958
Heterostegina
antillarum Trinidad
Shelf 11 −61 Trinidad
12811 Hofker, Sr.
1964
1964
Heterostegina
antillarum Grenada 12.05 −61.45 Aruba
12812 Hofker, Sr.
1964
1964
Heterostegina
antillarum Aruba 12.3 −70 Aruba
12813 Radford 1976B 1976
Heterostegina
antillarum Tobago
Island 11.12 −60.48 Tobago
12814 Hofker, Sr.
1976
1976
Heterostegina
antillarum La
Desirade 16.2 −61 La
Desirade
12815 Hofker, Sr.
1976
1976
Heterostegina
antillarum St. Martin 18.05 −63.02 St Martin
12816 Hofker, Sr 1976 1976
Heterostegina
antillarum Curacao 12.05 −68.57 Curacao
12817 Hofker, Sr.
1976
1976
Heterostegina
antillarum Grand
Cayman 19.25 −81.15 Grand
Cayman
12818 Hofker, Sr.
1976
1976
Heterostegina
antillarum Havana,
Cuba 23.1 −82.3 Cuba
12819 Hofker, Sr.
1964
1964
Heterostegina
antillarum St. Martin 18.01 −63.03 St Martin
12820 Hofker, Sr.
1964
1964
Heterostegina
antillarum St.
Eustacius 17.3 −63.01 St
Eustatius
12821 Hofker, Sr.
1976
1976
Heterostegina
antillarum Virgin
Islands 18.25 −64.55 Aruba
12822 Hofker, Sr.
1976
1976
Heterostegina
antillarum W Puerto
Rico 18.13 −67.13 Puerto
Rico
12823 Hofker, Sr.
1976
1976
Heterostegina
antillarum
Martinique
14.3 −61.05
Martinique
12824 Hofker, Sr.
1976
1976
Heterostegina
antillarum Grenada 12.04 −61.44 Grenada

Diversity 2025,17, 110 12 of 17
Table A1. Cont.
Record
No Publication Year Genus Species Locality Lat Long Country
12825 Iling 1952 1952
Heterostegina
antillarum Bahama
Banks 22.08 −75.54 Bahamas
12826 Bermudez
1937
1937
Heterostegina
antillarum
Morant
Cays,
Jamaica
17.25 −76 Jamaica
12827
Brasier 1975 B
1975
Heterostegina
antillarum Barbuda 17.38 −61.53 Barbuda
12828 Brasier 1975
A
1975
Heterostegina
antillarum Barbuda 17.4 −61.52 Barbuda
12829 Cushman
1921
1921
Heterostegina
antillarum
Montego
Bay,
Jamaica
18.28 −77.56 Jamaica
12830 Seiglie 1967 1967
Heterostegina
antillea
Araya-
Los
Testigos
Shelf
11 −63.3 Araya Los
Testigos
19087 Norton 1930 1930
Heterostegina
antillarum Tortugas,
Fla. 24.4 −82.52 Tortugas
Florida
19088 Cushman
1930
1930
Heterostegina
antillarum Tortugas,
Fla 24.58 −82.55 Tortugas
Florida
19089 Cushman
1922A
1922
Heterostegina
antillarum Tortugas 24.38 −82.54 Tortugas
14797 Howard 1965 1965
Heterostegina
depressa S. Florida
Keys 24.4 −81.22 Florida
Keys
14798 Bock 1971 1971
Heterostegina
depressa Florida
Bay 25 −80.5 Florida
Bay
MO64322 Geol.Soc.Mem.
(n.1): 57,
pl.21,f.3.
1958
Heterostegina
depressa Gulf of
Mexico 24.38 −82.67 Gulf of
Mexico
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